The DOI matches its Crossref record; 60 of the 60 references it cites were found in a registry or an index; 16 of the 35 sources its claims cite were checked for support.
The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti–Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC
Open accessAbstract
INTRODUCTION Gut microbiome affecting the responses to immune checkpoint inhibitors against advanced NSCLC has been investigated in the Western population. However, considering pre-existing genetic and gut microbiota variation, the relevance remains unknown in the East-Asian NSCLC population. This study is designed to explore the relationship between gut microbiome and clinical outcomes in Chinese patients with NSCLC who have received treatment using an anti-programmed death 1 (PD-1) blockade. METHODS Thirty-seven patients with advanced NSCLC receiving treatment with nivolumab were enrolled in CheckMate 078 (NCT02613507) and CheckMate 870 (NCT03195491). Fecal samples were collected at the starting point, when patients received nivolumab, at clinical evaluation, and when disease progression was noted. 16S ribosome RNA gene sequencing was applied to assess gut microbiota profiles. Peripheral immune signatures were determined by multicolor flow cytometry in parallel. RESULTS When subgrouping patients into responder (R) and nonresponder according to the clinical response assessed using Response Evaluation Criteria in Solid Tumor version 1.1, R patients harbored higher diversity of gut microbiome at the starting point with stable composition during the treatment. Patients with high microbiome diversity had significantly prolonged progression-free survival when compared to those with low diversity. Compositional difference was observed between the two groups as well with the enrich…
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In the paper
“It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Supportedcites [36] Noriho, 2013, Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment, Science source
The paper states that gut microbiota affects immunity locally and systemically (opening text, labeled Abstract in our copy). It also reports that disrupting the microbiota impairs antitumor treatment responses in mice by altering immune-cell activity in the tumor microenvironment (Abstract). Together, these passages support the broad background claim. (LLM, conf=0.90)
- Not checked — no full text of the sourcecites [37] Hooper, 2012, Interactions between the microbiota and the immune system, Science source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Supported
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The percentages of total NK cells and PD-1 þ GZMB þ NK cells were also positively correlated with the Shannon index.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Association Between Gut Microbiota Profile and Peripheral Immune Signatures
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In addition, CD45RO þ CD8 þ Tm cells expressing specific markers such as Ki-67, TIM-3, and ICOS were statistically related to the Shannon index as well.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Association Between Gut Microbiota Profile and Peripheral Immune Signatures
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In T cells, functional subsets such as GZMB þ CD45RO þ CD27 þ CD8 þ T cells (GZMB þ CD8 þ Tcm); GZMB þ CD45RO þ CD27 -CD8 þ T cells (GZMB þ CD8 þ Tem) were positively correlated with the Shannon index.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Association Between Gut Microbiota Profile and Peripheral Immune Signatures
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“When we compared the relevant immune signature levels between high-diversity and low-diversity groups, it was shown that the percentages of GZMB þ CD8 þ Tm, Ki67 þ CD8 þ Tm, and CD8 þ Tcm in the periphery were significantly elevated in high-diversity group.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Association Between Gut Microbiota Profile and Peripheral Immune Signatures
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“At the genus level, we identified seven gut bacteria with differential abundance between R and NR at baseline (p < 0.05 for all genera) (Fig. 3A).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Compositional Difference in Gut Microbiome in Response to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“When we compared the relevant immune signature levels between high-diversity and low-diversity groups, it was shown that the percentages of GZMB þ CD8 þ Tm, Ki67 þ CD8 þ Tm, and CD8 þ Tcm in the periphery were significantly elevated in high-diversity group.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Association Between Gut Microbiota Profile and Peripheral Immune Signatures
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The Shannon diversity index remained stable based on Kruskal-Wallis test (p > 0.999) from baseline to different assessment timepoints (T1 to T8) as well as at progression timepoints (Fig. 4A, left).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Gut Microbiota Composition is Stable During Nivolumab Treatment Whether gut microbiota profile is influenced during ICI treatment is very interesting due to the different outcomes of individual patients.In our study using timeserial fecal sampling during the treatment, dynamic analysis of gut microbiota was feasible.The Shannon diversity index remained stable based on Kruskal-Wallis test (p > 0.999) from baseline to different assessment timepoints (T1 to T8) as well as at progression timepoints (Fig. 4A, left).Paired samples at baseline and at the T1 (Fig. 4A, middle) or baseline and progression timepoint (Fig. 4A, right) displayed no differences in Shannon index based on Wilcoxon matched-pairs signed rank test (p > 0.05).We then compared gut microbiota composition at the genera level using 10 paired fecal samples at baseline and timepoint with disease progression.As shown in Figure 4B, the compositions of fecal microbiota were apparently similar.We further conducted PCoA analysis of gut microbiome in longitudinal samples of 10 patients (7 from R and 3 from NR).While gut microbiota from one patient at different sampling timepoints (represented by one shape) were clustered very well, R and NR individuals were separated clearly as well (pink and purple circles) (Fig. 4C).Analyzing precisely, the relative abundance of main bacterial phylum remained stable over time (Fig. 4D).Seven genera which were differentially abundant in R and NR at baseline showed mild turbulence during the therapy.But no statistical difference was noticed (Fig. 4E).Altogether, these data indicate that nivolumab treatment does not modify gut microbiome community in patients with advanced NSCLC.
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As shown in Figure 2D, baseline samples were clustered by response status of R and NR, respectively.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Baseline Gut Microbiota Diversity is Associated With Favorable Responses to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Prevotella copri, Bifidobacterium longum, Lachnobacterium, Lachnospiraceae, and Shigella were enriched in R (Fig. 3A).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Compositional Difference in Gut Microbiome in Response to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
- Probably not a substantial claim. 28
- It may state two separate claims as one. 14
- The quote only partly states this claim. 1
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Partly supportedcites [20] Bultman, 2014, Emerging roles of the microbiome in cancer, Carcinogenesis sourceExperimental — accuracy not yet measured
The metagenomic-studies section (page unavailable) describes dysbiosis and reports microbiome differences in Crohn’s disease; its discussion of colorectal tumors also supports an association with cancer. The obesity evidence in the cited passages concerns mice, so it does not establish the claimed association between gut dysbiosis and obesity in humans. (LLM, conf=0.83)
- Not checked — no full text of the sourcecites [21] Wallace, 2011, Human gut microbiota and its relationship to health and disease, Nutrition Rev source
- Not checked — no full text of the sourcecites [33] Herbert, 2011, Gut microbiome, obesity, and metabolic dysfunction, J Clin Invest source
- Partly supportedcites [34] Ni, 2017, Gut microbiota and IBD: causation or correlation?, Nat Rev Gastroenterol Hepatol sourceExperimental — accuracy not yet measured
The ‘Microbiota composition and IBD’ section documents differences in gut microbial diversity and composition between people with IBD and healthy individuals, supporting the claimed association with IBD. Our copy does not establish the corresponding associations with obesity or cancer; the cancer-related reference alone does not substantiate that broader claim. The paper also cautions that association does not prove causation, although the citing sentence claims association rather than causation. (LLM, conf=0.88)
Strength:boosted· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Partly supported
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27]”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Not checked — no full text of the sourcecites [25] Falony, 2016, Population-level analysis of gut microbiome variation, Science source
- Partly supportedcites [26] Gupta, 2017, Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity, Front Microbiol sourceExperimental — accuracy not yet measured
The Summary and Gastrointestinal microbiome sections link geographic differences, diet and lifestyle to variation in gut microbiomes. They also discuss genetics, but say its role in shaping the gut microbiome is unclear; the gastrointestinal section mentions early-life exposures such as delivery mode, breastfeeding and antibiotics without establishing them as main contributors to ethnic or racial divergences. The claim is therefore stronger than this review supports. (LLM, conf=0.86)
- Not matchedcites [27] Ran, 2015, Host genetic variation impacts microbiome composition across human body sites, Genome Biol
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
Every source the paper cites for this claim was checked and supports it.
In the paper
“It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Supportedcites [32] Derosa, 2018, Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non–small cell lung cancer, Ann Oncol source
The Results passage on antibiotic use within 60 days before treatment reports no difference in objective response or PFS among NSCLC patients, but significantly shorter OS. The claim accurately reflects that 60-day analysis; the paper separately reports shorter PFS for antibiotic use within 30 days. (LLM, conf=0.94)
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
- Supported
The sources with a verdict support this claim; the rest weren’t checked yet, have no full text we could read, or their verdicts aren’t rated yet.
In the paper
“Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Not checked — no full text of the sourcecites [15] Routy, 2017, Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors, Science source
- Supportedcites [32] Derosa, 2018, Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non–small cell lung cancer, Ann Oncol source
The Discussion reports that antibiotic use before ICI was associated with worse outcomes in patients with advanced renal cell or non-small-cell lung cancer. Tables 3A and 3B also report associations between smoking status and progression-free survival, and between the number of prior treatment regimens and overall survival, respectively, in the non-small-cell lung cancer cohort. These findings support the claim as a broad statement about reported clinical factors, though they do not establish causation. (LLM, conf=0.88)
- Not checked — no full text of the sourcecites [39] Garon, 2015, Pembrolizumab for the treatment of non–small-cell lung cancer, N Engl J Med source
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Partly supportedcites [35] Gopalakrishnan, 2018, Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients, Science sourceExperimental — accuracy not yet measured
The paper’s results report higher gut-microbiome alpha diversity in responders than non-responders and significantly longer progression-free survival in patients with high diversity. These findings support the clinical-outcome association, but the passages in our copy do not identify the cohort as a “Western population”; a search for that term found no such designation. (LLM, conf=0.83)
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
- Partly supported
The sources with a verdict support this claim; the rest weren’t checked yet, have no full text we could read, or their verdicts aren’t rated yet.
In the paper
“Both innate and adaptive immune responses can be reshaped by gut microbiome.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Supportedcites [36] Noriho, 2013, Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment, Science source
The paper reports that antibiotic disruption of the microbiota down-regulated tumor genes related to adaptive immune responses. It also reports that commensal microbiota primes innate myeloid cells for inflammatory cytokine production. Together, these findings support the broad claim that gut microbiota can reshape both types of immune response, although the adaptive evidence cited here is gene-expression based. (LLM, conf=0.85)
- Not checked — no full text of the sourcecites [37] Hooper, 2012, Interactions between the microbiota and the immune system, Science source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Supported
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Not checked — no full text of the sourcecites [7] Sacher, 2016, Biomarkers for the clinical use of PD-1/PD-L1 inhibitors in non–small-cell lung cancer: a review, JAMA Oncol source
- Partly supportedcites [8] Topalian, 2012, Safety, activity, and immune correlates of anti–PD-1 antibody in cancer, N Engl J Med sourceExperimental — accuracy not yet measured
The Results section (PD-L1 Expression in Tumors; page unavailable) reports objective responses in 9 of 25 patients with PD-L1–positive tumors and none of 17 with PD-L1–negative tumors. That supports an association with response to anti–PD-1 treatment, but the analysis pooled cancer types, included only 10 patients with NSCLC, and compared positive with negative specimens; it did not establish a linear relationship between expression level and benefit specifically in NSCLC. (LLM, conf=0.87)
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Partly supportedcites [14] Gopalakrishnan, 2017, Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients, Science sourceExperimental — accuracy not yet measured
The paper’s results support an association between gut bacteria and response to anti-PD-1 therapy in melanoma patients. However, the reported favorable taxa are Clostridiales, Ruminococcaceae and Faecalibacterium; the cited paper does not report a favorable association for Akkermansia muciniphila, Alistipes or Porphyromonas. It instead reports Bacteroidales enrichment in nonresponders (results, page unavailable). (LLM, conf=0.84)
- Not checked — no full text of the sourcecites [15] Routy, 2017, Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors, Science source
- Partly supportedcites [36] Noriho, 2013, Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment, Science sourceExperimental — accuracy not yet measured
The passage on microbiota correlations (section labeled Abstract; page unavailable) identifies gram-negative Alistipes as positively correlated with TNF expression and reports that A. shahii restored a tumor-associated TNF response in mice given CpG-ODN. It does not establish better clinical response to immunotherapy, and the passages do not report such an association for Akkermansia muciniphila or Porphyromonas. (LLM, conf=0.88)
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Partly supported
Every source the paper cites for this claim was checked and supports it.
In the paper
“Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Supportedcites [9] Robert, 2015, Nivolumab in previously untreated melanoma without BRAF mutation, N Engl J Med source
The Subgroup Analyses report a 33.1% objective response rate to nivolumab among patients with negative or indeterminate PD-L1 status. The same section defines PD-L1 positivity as staining in at least 5% of tumor cells, so the negative subgroup supports the claim that responses occurred despite low PD-L1 expression. The finding is from patients with previously untreated melanoma without a BRAF mutation. (LLM, conf=0.93)
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
- Supported
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Not checked — no full text of the sourcecites [7] Sacher, 2016, Biomarkers for the clinical use of PD-1/PD-L1 inhibitors in non–small-cell lung cancer: a review, JAMA Oncol source
- Partly supportedcites [8] Topalian, 2012, Safety, activity, and immune correlates of anti–PD-1 antibody in cancer, N Engl J Med sourceExperimental — accuracy not yet measured
The Discussion describes tumor PD-L1 expression as a candidate marker for response to anti–PD-1 therapy, and the Results report responses in 9 of 25 patients with PD-L1–positive tumors versus none of 17 with PD-L1–negative tumors. But the paper calls this analysis preliminary and says further studies are needed; it does not establish PD-L1 as the most available biomarker or address predictive efficacy across ICIs generally. Page numbers are not provided in our copy. (LLM, conf=0.88)
Strength:boosted· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
The sources with a verdict support this claim; the rest weren’t checked yet, have no full text we could read, or their verdicts aren’t rated yet.
In the paper
“ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Supportedcites [52] Das, 2017, Tim-3 and its role in regulating anti-tumor immunity, Immunolog Rev source
For this sentence with two citations, the source supports the TIM-3 component. Section 2 links TIM-3 expression on CD8+ tumor-infiltrating T cells to exhaustion and tumor immunity; section 6.3 also discusses TIM-3+ FoxP3+ regulatory T cells in tumors. (LLM, conf=0.92)
- Not checked — no full text of the sourcecites [53] Tihui, 2011, The ICOS/ICOSL pathway is required for optimal antitumor responses mediated by anti–CTLA-4 therapy, Cancer Res source
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Supported
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Partly supportedcites [47] Scher, 2013, Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis, Elife sourceExperimental — accuracy not yet measured
The Results (‘Association of Prevotella with new-onset rheumatoid arthritis’; page unavailable) report that P. copri was significantly more prevalent in untreated, new-onset RA patients than in the comparison groups. The paper reports an association with disease presence, not a strong correlation between P. copri and RA severity; its Discussion notes only slightly lower DAS28 disease-activity scores in the chronic RA group. (LLM, conf=0.87)
Strength:boosted· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Partly supported
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Partly supportedcites [51] Kamphorst, 2017, Proliferation of PD-1+ CD8 T cells in peripheral blood after PD-1–targeted therapy in lung cancer patients, Proc Natl Acad Sci U S A sourceExperimental — accuracy not yet measured
The Results report that PD-1–targeted therapy induced proliferation of PD-1+ CD8 T cells in patients with lung cancer. They also report an association between early proliferative responses and positive clinical outcomes, but do not establish that the proliferation itself benefits treatment; the authors call that outcome finding preliminary (Results; page not provided). (LLM, conf=0.86)
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Partly supported
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, difference in Inverse Simpson index was not significant between two groups at T1, although the tendency remained (Fig. 2A).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Baseline Gut Microbiota Diversity is Associated With Favorable Responses to Nivolumab
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Paired samples at baseline and at the T1 (Fig. 4A, middle) or baseline and progression timepoint (Fig. 4A, right) displayed no differences in Shannon index based on Wilcoxon matched-pairs signed rank test (p > 0.05).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Gut Microbiota Composition is Stable During Nivolumab Treatment Whether gut microbiota profile is influenced during ICI treatment is very interesting due to the different outcomes of individual patients.In our study using timeserial fecal sampling during the treatment, dynamic analysis of gut microbiota was feasible.The Shannon diversity index remained stable based on Kruskal-Wallis test (p > 0.999) from baseline to different assessment timepoints (T1 to T8) as well as at progression timepoints (Fig. 4A, left).Paired samples at baseline and at the T1 (Fig. 4A, middle) or baseline and progression timepoint (Fig. 4A, right) displayed no differences in Shannon index based on Wilcoxon matched-pairs signed rank test (p > 0.05).We then compared gut microbiota composition at the genera level using 10 paired fecal samples at baseline and timepoint with disease progression.As shown in Figure 4B, the compositions of fecal microbiota were apparently similar.We further conducted PCoA analysis of gut microbiome in longitudinal samples of 10 patients (7 from R and 3 from NR).While gut microbiota from one patient at different sampling timepoints (represented by one shape) were clustered very well, R and NR individuals were separated clearly as well (pink and purple circles) (Fig. 4C).Analyzing precisely, the relative abundance of main bacterial phylum remained stable over time (Fig. 4D).Seven genera which were differentially abundant in R and NR at baseline showed mild turbulence during the therapy.But no statistical difference was noticed (Fig. 4E).Altogether, these data indicate that nivolumab treatment does not modify gut microbiome community in patients with advanced NSCLC.
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Prevotella copri, Bifidobacterium longum, Lachnobacterium, Lachnospiraceae, and Shigella were enriched in R (Fig. 3A).”
- Also stated in: § Compositional Difference in Gut Microbiome in Response to Nivolumab · plain
“Two bacteria, Bifidobacterium longum and Prevotella copri, were enriched in the R group both at baseline (p ¼ 0.0303 and p ¼ 0.0093, respectively) and T1 time point (p ¼ 0.0397 and p ¼ 0.0426, respectively) (Fig. 3C).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Compositional Difference in Gut Microbiome in Response to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
- Also stated in: § Compositional Difference in Gut Microbiome in Response to Nivolumab · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Prevotella copri, Bifidobacterium longum, Lachnobacterium, Lachnospiraceae, and Shigella were enriched in R (Fig. 3A).”
- Also stated in: § Compositional Difference in Gut Microbiome in Response to Nivolumab · plain
“Two bacteria, Bifidobacterium longum and Prevotella copri, were enriched in the R group both at baseline (p ¼ 0.0303 and p ¼ 0.0093, respectively) and T1 time point (p ¼ 0.0397 and p ¼ 0.0426, respectively) (Fig. 3C).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Compositional Difference in Gut Microbiome in Response to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
- Also stated in: § Compositional Difference in Gut Microbiome in Response to Nivolumab · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“While gut microbiota from one patient at different sampling timepoints (represented by one shape) were clustered very well, R and NR individuals were separated clearly as well (pink and purple circles) (Fig. 4C).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Gut Microbiota Composition is Stable During Nivolumab Treatment Whether gut microbiota profile is influenced during ICI treatment is very interesting due to the different outcomes of individual patients.In our study using timeserial fecal sampling during the treatment, dynamic analysis of gut microbiota was feasible.The Shannon diversity index remained stable based on Kruskal-Wallis test (p > 0.999) from baseline to different assessment timepoints (T1 to T8) as well as at progression timepoints (Fig. 4A, left).Paired samples at baseline and at the T1 (Fig. 4A, middle) or baseline and progression timepoint (Fig. 4A, right) displayed no differences in Shannon index based on Wilcoxon matched-pairs signed rank test (p > 0.05).We then compared gut microbiota composition at the genera level using 10 paired fecal samples at baseline and timepoint with disease progression.As shown in Figure 4B, the compositions of fecal microbiota were apparently similar.We further conducted PCoA analysis of gut microbiome in longitudinal samples of 10 patients (7 from R and 3 from NR).While gut microbiota from one patient at different sampling timepoints (represented by one shape) were clustered very well, R and NR individuals were separated clearly as well (pink and purple circles) (Fig. 4C).Analyzing precisely, the relative abundance of main bacterial phylum remained stable over time (Fig. 4D).Seven genera which were differentially abundant in R and NR at baseline showed mild turbulence during the therapy.But no statistical difference was noticed (Fig. 4E).Altogether, these data indicate that nivolumab treatment does not modify gut microbiome community in patients with advanced NSCLC.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The increase of Shannon index at the T1 timepoint in R was consistent with that at baseline (p ¼ 0.0301).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Baseline Gut Microbiota Diversity is Associated With Favorable Responses to Nivolumab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesThe quote only partly states this claim.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Components 1 and 2 accounted for 10.82% and 7.69% of variance, respectively, in PCoA.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Baseline Gut Microbiota Diversity is Associated With Favorable Responses to Nivolumab
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patient Characteristics Forty-two Chinese patients with advanced NSCLC were consented and enrolled.All patients were followedup until disease progression or death.Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).Clinical information revealed that the majority of patients enrolled in the study were male (78.3%).All of the patients had received at least one or two-rounds of chemotherapy before enrollment.No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).Recent studies reported negative association between ATB prescription and clinical outcome of PD-1 inhibitors.15,32 When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.However, the R/NR ratio with or without ATB usage was similar (Table 1).Therefore, smoking is the only clinical factor associated with the responses to nivolumab in our study.
Strength:plain· not yet calibratedn = 37Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patient Characteristics Forty-two Chinese patients with advanced NSCLC were consented and enrolled.All patients were followedup until disease progression or death.Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).Clinical information revealed that the majority of patients enrolled in the study were male (78.3%).All of the patients had received at least one or two-rounds of chemotherapy before enrollment.No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).Recent studies reported negative association between ATB prescription and clinical outcome of PD-1 inhibitors.15,32 When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.However, the R/NR ratio with or without ATB usage was similar (Table 1).Therefore, smoking is the only clinical factor associated with the responses to nivolumab in our study.
Strength:plain· not yet calibratedn = 37Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patient Characteristics Forty-two Chinese patients with advanced NSCLC were consented and enrolled.All patients were followedup until disease progression or death.Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).Clinical information revealed that the majority of patients enrolled in the study were male (78.3%).All of the patients had received at least one or two-rounds of chemotherapy before enrollment.No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).Recent studies reported negative association between ATB prescription and clinical outcome of PD-1 inhibitors.15,32 When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.However, the R/NR ratio with or without ATB usage was similar (Table 1).Therefore, smoking is the only clinical factor associated with the responses to nivolumab in our study.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patient Characteristics Forty-two Chinese patients with advanced NSCLC were consented and enrolled.All patients were followedup until disease progression or death.Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).Clinical information revealed that the majority of patients enrolled in the study were male (78.3%).All of the patients had received at least one or two-rounds of chemotherapy before enrollment.No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).Recent studies reported negative association between ATB prescription and clinical outcome of PD-1 inhibitors.15,32 When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.However, the R/NR ratio with or without ATB usage was similar (Table 1).Therefore, smoking is the only clinical factor associated with the responses to nivolumab in our study.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
Tests✓ Asserted: passes✗ Checkable: fails✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may be too vague to check against evidence.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patient Characteristics Forty-two Chinese patients with advanced NSCLC were consented and enrolled.All patients were followedup until disease progression or death.Among them, 1 patient died after a single infusion of nivolumab.Two patients were lost during the follow-up study.Two patients discontinued therapy because of grade 3-4 adverse events.The remaining 37 patients were grouped according to clinical assessment.Twenty-three patients being evaluated as either partial response (n ¼ 5) or stable disease (n ¼ 18) were classified as R whereas the others (n ¼ 14) with disease progression after the first clinical assessment were classified as NR.Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).Clinical information revealed that the majority of patients enrolled in the study were male (78.3%).All of the patients had received at least one or two-rounds of chemotherapy before enrollment.No difference was observed in sex, disease history, disease stage, and the treatment between R and NR patients except smoking history (p ¼ 0.008).Recent studies reported negative association between ATB prescription and clinical outcome of PD-1 inhibitors.15,32 When we examined ATB usage in our cohort, 11 of 37 patients (29.7%) were prescribed ATB within 2 month.However, the R/NR ratio with or without ATB usage was similar (Table 1).Therefore, smoking is the only clinical factor associated with the responses to nivolumab in our study.
Strength:plain· not yet calibratedn = 42Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“All the procedures were conducted in accordance with the Declaration of Helsinki.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patients
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Not checked — no full text of the sourcecites [54] Tanoue, 2019, A defined commensal consortium elicits CD8 T cells and anti-cancer immunity, Nature source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
Tests✓ Asserted: passes✗ Checkable: fails✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may be too vague to check against evidence.
In the paper
“Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Not checked — no full text of the sourcecites [44] Gettinger, 2016, Nivolumab monotherapy for first-line treatment of advanced non–small-cell lung cancer, J Clin Oncol source
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Not checked — no full text of the sourcecites [48] Haratani, 2018, Association of immune-related adverse events with nivolumab efficacy in non–small-cell lung cancer, JAMA Oncol source
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Not checked — no full text of the sourcecites [6] Spain, 2016, Management of toxicities of immune checkpoint inhibitors, Cancer Treat Rev source
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The study was approved by the Ethics Committee of Shanghai Chest Hospital.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patients
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Introduction Advanced NSCLC is an incurable disease with a poor prognosis and is the leading cause of cancer-related death. 1 With impressive advancement in immune checkpoint inhibitor (ICI) therapies targeting programmed death 1 (PD-1) and programmed death ligand 1 (PD-L1) axis against multiple malignancies, these agents exhibit clinical efficacy against patients with advanced NSCLC both in second-line and first-line treatment when compared to conventional chemotherapy.At present, five therapeutic monoclonal antibodies targeting PD-1 or PD-L1 have been approved by the U.S. Food and Drug Administration (FDA) for the treatment of 11 cancer indications including NSCLC. 2 Nivolumab (Opdivo) is a fully human immunoglobulin G4 monoclonal antibody against PD-1.It blocks the binding of PD-1 to its ligand PD-L1 and restores the function of "exhausted" T cells in tumor sites.The unleashed lymphocytes exert killing ability, resulting in tumor shrinkage.3 It was firstly approved by the FDA in 2015 for the treatment of patients with advanced NSCLC after the failure of platinum-based chemotherapy, and by the National Medical Products Administration in 2018 after the phase III clinical trial CheckMate-078 for previously treated patients with NSCLC. 4 According to results from CheckMate-078, nivolumab yields superior overall survival (OS) compared with the docetaxel arm (median OS: 12 mo versus 9.6 mo). 5 However, only 20% of patients with advanced NSCLC benefit from the treatment, whereas up to 50% experience treatmentrelated adverse events in which grade 3-4 toxicities occur in 10% patients receiving nivolumab.6 Considering high cost of the agents, limited benefit population, and potential severe side effects, biomarkers for selecting patients with likely clinical efficacy from ICI treatment in advanced NSCLC would be of paramount importance. So far, PD-L1 expression on tumor cells is regarded as the most available biomarker to predict the efficacy of ICIs in NSCLC and other malignancies.A linear relationship has been reported between the proportion of ICI benefit and PD-L1 expression in NSCLC tumor sections.7,8 Nevertheless, the responses to ICI treatment have still been observed in those with low or undetectable levels of PD-L1 expression.9 To date, other biomarkers such as high tumor mutation burden, nonsynonymous mutations and neoantigens, CD8 þ T cell counts in tumor regions, defects of mismatch repair genes or high microsatellite instability, microbiota, and metabolic profiles are also supposed to be predictive for favorable responses to ICI treatment, among which gut microbiome property is of great value.[10][11][12][13][14][15][16][17] Human gut harbors more than 10 13 microbes, which outnumbers host cells 10-fold.More and more evidence supports the critical roles of gut microbiota in influencing human health in part through shaping systematic immune responses.18 Certain metabolites such as shortchain fatty acids and bile acid are considered to be key mediators.19 Dysbiosis of intestinal flora has been shown to be associated with multiple diseases.[20][21][22] Recent studies have also revealed that gut microbiota could mediate diverse responses to immunotherapy and might serve as a potential predictive biomarker.Gut commensals such as Bacteroides thetaiotaomicron or B. fragilis are predicable for anti-cytotoxic T-lymphocyte associated protein 4 (CTLA-4) treatment in a mouse melanoma model.23 In patients with melanoma receiving anti-PD-1 therapy, significant difference in the diversity and composition of gut microbiome was observed between the responders and nonresponders to the therapy.14 Germ-free mice receiving fecal transplantation from the responders tended to be more sensitive to anti-PD-1 treatment in contrast to those receiving feces from the nonresponders.14,15 In one cohort study enrolling 60 patients with advanced NSCLC and 40 with renal cell carcinoma undergoing PD-1 blockade therapy, Akkermansia muciniphila was reported to be overrepresented in the responders.15 Nevertheless, the previous studies were performed predominantly in the patients from Western countries.Gut microbiome structures have been elucidated remarkably variable among different races and ethnicities.24 Extrinsic factors, such as geographical location or diet and life styles, and intrinsic factors such as genetics or early-life exposures are main contributors to such divergences.[25][26][27] Therefore, it is still significant to reveal the characteristics of gut microbiota in regional patients with advanced NSCLC and the potential roles of gut microbiota in the prediction for the responses to ICI treatment.
What the sources say
- Not checked — no full text of the sourcecites [5] Wu, 2019, Nivolumab versus docetaxel in a predominantly Chinese patient population with previously treated advanced non-small cell lung cancer: CheckMate 078 randomized phase III clinical trial, J. Thorac Oncol source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“All patients were informed of the study and consented to the enrollment.”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Patients
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46”
§ The Diversity of Gut Microbiome is Associated With Favorable Responses to Anti-Programmed Death 1 Immunotherapy in Chinese Patients With NSCLC > Discussion In the present study, we have investigated gut microbiota profiles in Chinese patients with advanced NSCLC receiving nivolumab treatment.Our results indicate that patients with better clinical responses exhibit higher diversity as well as a distinct gut microbiome composition.In addition, the association between gut microbiome diversity and systematic immune signatures highlights memory CD8 þ T cells and NK cells as potential mediators of antitumor immunity upon ICI treatment.The diversity of gut microbiome is defined as the number and abundance distribution of distinct types of micro-organisms colonizing within the gut.Abnormal diversity (dysbiosis) in the gut has been proven to be associated with human diseases, such as obesity, inflammatory bowel disease, cancer, etc. 20,21,33,34 Recently, Gopalakrishnan et al. 35 reported that patients with a high diversity of gut microbiome favored the clinical outcomes of anti-PD-1 immunotherapy in melanoma patients in the Western population.In our study, both alpha diversity and beta diversity at baseline are dramatically different between R and NR as well.A higher alpha diversity index represented by both the Shannon index and inverse Simpson indexes in R group suggests more species harboring in the gut, which is largely consistent with a differential composition of gut microbiome between R and NR.The higher the diversity of gut microbiota is, the longer PFS the patients undergo.Visualized beta diversity through PCoA analysis of 16S sequencing also displays apparently two clusters based on clinical responses to nivolumab treatment.Our results thus show that regardless of genetic background and geographic location with different lifestyles and diet styles, the diversity of gut microbiota might be a common benefit factor to ICI treatment.In our opinion, this is rational.It is widely accepted that gut microbiota modulates immune responses in a global way including antitumor immunity.36,37 Both innate and adaptive immune responses can be reshaped by gut microbiome.Although how the diversity of gut microbiota reshapes systemic immune responses is still not clearly addressed, microbiota-derived short chain fat acids and other metabolites should be good candidates to exert strong immune regulation.19,38 Further study will focus on the relevant metabolites analysis. Several clinical factors are reported to be involved in affecting the efficacy of ICI therapy, including smoking, previous treatment, and ATB usage.15,32,39 Among them, ATB is supposed to be the most relevant to gut microbiota.It has been reported previously that recent ATB usage in NSCLC patients was associated with shorter OS, although there was no difference in terms of objective response or PFS.32 In another study, ATB treatment is identified as the key factor significantly associated with both PFS and OS. 15 In our study, we retrospectively investigated ATB usage among 37 patients.The composition of gut microbiota at baseline between participants with or without ATB before first nivolumab infusion was similar (Supplementary Fig. 2), which excludes the possible effects of ATB on gut microbiota in our study.Median PFS was similar between ATB-treated and -naïve patients (median PFS: 126 days versus 117.9 days, p > 0.05) (Supplementary Fig. 3).One possibility lies in the number limitation in our study.Another possibility is that gut microbiome possess the ability of resilience.40 The majority of gut microbiota can be normalized after 1 week once ATB usage stops.41 We also observed that gut microbiota remained stable in longitudinal samples within one individual in our study.Such a trait might ensure patient long-term benefit from ICI treatment. Among all the clinical manifestations, smoking is the only factor that affects the responses to nivolumab treatment in our study.The roles of smoking on carcinogenesis refer to both cancer cell itself and immune responses of the host.It has been hypothesized that higher mutational burden could be induced by smoking, which has shown an increased response to ICI. 42,43 Median PFS was longer in current and former smokers compared with nonsmokers in nivolumab monotherapy for first-line treatment of advanced NSCLC as well.44 Smoking is reported to affect both innate and adaptive immunity, including memory T cells in the periphery.45 In our study, memory T cell profiles at baseline are similar between smoking and nonsmoking patients (Supplementary Fig. 4).This result confers that memory T cells are more likely affected by gut microbiota rather than other factors such as smoking.It has also been reported that chemotherapy could influence the gut microbiota of cancer patients largely due to the disruption of the intestinal barrier and subsequent bacteria translocation.In our study all the participants have received nivolumab therapy after failure of traditional chemotherapy.There was no difference in the interval from the date of last chemotherapy to that of first nivolumab infusion between R and NR groups (Supplementary Fig. 5, left).Correlation analysis showed that the diversity of gut microbiota was irrelevant to the time-off of chemotherapy in our cohort study as well (Supplementary Fig. 5, right). In addition to diversity, gut microbiome composition is also related to favorable responses to ICI treatment.In a pre-clinical study, gut commensal Bifidobacterium was shown to facilitate anti-PD-L1 efficacy.46 Clinical investigations reported that Faecalibacterium and some species belonging to Bacteroides genus (such as B. fragilis or B. thetaiotaomicron) are positively associated with the efficacy of PD-1 and CTLA-4 blockade, respectively.14,23 In our study, seven genera were identified different between R and NR.Ruminococcus_unclassified was enriched in NR whereas Bifidobacterium longum, Prevotella copri, and Alistipes putredinis were enriched in R. It has been shown in another study that Bifidobacterium longum could increase the production of pro-inflammatory cytokine tumor necrosis factor-alpha and significantly improve tumor control upon anti-PD-L1 therapy in a B16.SIY tumor mouse model.46 More interestingly, most bacteria enriched in R in our study belong to pro-inflammatory gram-negative bacteria.There are several previous studies reporting the association of gram-negative bacteria, such as Akkermansia muciniphila, Alistipes, and Porphyromonas with better clinical response to immunotherapy.14,15,36 It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide. In another study, mice colonized with Prevotella copri displayed increased inflammation in dextran sulfate sodium-induced colitis.Prevotella copri was strongly correlated with the disease severity in rheumatoid arthritis, which is a systemic autoimmune disease with the proliferation of pro-inflammatory T cells.47 In the antitumor setting, the exacerbation of immune responses might assist the ability of immune surveillance in the patients.This is also consistent with the report that patients who develop immune-related adverse events are more sensitive to ICI treatment.48 Although the direct evidence on the linkage between the inflammation and ICI benefit in the population still needs to be investigated, it is not out of expectation that systemic antitumor immune responses are diverse in patients with different gut microbiome composition.Gut microbiota thus becomes an intrinsic biosensor to sensitize anti-PD-1 treatment, which in turn leads to different clinical outcomes.This can be partially supported by the results from immune signature exploration in our study.Previous studies already highlighted the roles of PD-1 in reshaping immune responses in the mice.49 ICI therapy, to some extent, facilitates the investigation on PD-1 in the regulation of human immunity.By using multi-color flow cytometry, immune signatures including immune cell subsets and their function-related signatures have been detected.Furthermore, correlation analyses were performed between individual immune signatures and microbiota diversity.Among multiple signatures, the frequency and function of memory CD8 þ T cells are mostly dedicated.Memory CD8 þ T cells are a bunch of long-lived cells which are capable of rapid antigenspecific responses and play critical roles in immune recall responses. 50In addition to the percentage of CD8 þ Tm subsets such as effector memory T (Tem) cells and central memory T (Tcm) cells, the functional subset with Granzyme B production is also positively correlated with the diversity index, which can partially explain why patients with high microbiota diversity respond better to ICI therapy.The increase in Ki67 þ CD8 þ Tm in the patients with high microbiota diversity implies that gut microbiota also modulate the proliferation of certain immune cell populations.Recent studies already reported the effects of PD-1 blockade on the proliferation of CD8 þ T cells, which is beneficial for ICI treatment.51 ICOS and TIM3 expressions on specific T cells subsets are also related to antitumor immunity.52,53 Whereas CD8 þ T cells infiltrating in tumor microenvironment are thought to be the executors of tumor killing, circulating CD8 þ T cell subsets reported here are probably inclined to reflect the roles of gut microbiota on systematic immune responses.How peripheral memory CD8 þ T cell signatures affect the efficacy of ICI treatment will be investigated in the future.Once verified, they might become antitumor immune mediators against NSCLC. Our study shows that the diversity of gut microbiota is associated with favorable response to nivolumab therapy against NSCLC in Chinese cohorts.Considering the correlation between microbiota diversity and peripheral memory T cells and NK cells being reshaped upon ICI treatment, we propose that patients with more diverse gut microbiota at baseline benefit from ICI immunotherapy to a greater extent.This might be mediated by reprogramming systemic antitumor immune responses.The significance of our study lies in that the modulation of gut microbiota before the treatment might provide an alternative way to enhance the efficacy of ICI immunotherapy once validated in large cohort studies.A latest publication has introduced 11 bacterial strains from healthy donors' feces to induce interferon-g producing CD8 þ T cells in the intestine, which mediates effective antitumor immunity in a mouse model.54 Once clearly addressed, customized microbiome will exhibit great prospect as biotherapeutics in assistance with ICI treatment against advanced NSCLC.Project (17431906103), Shanghai Economic and Information Commission for oncology data platforms (201602010) and Shanghai Scientific Research Projects (14140902800).The authors thank Prof. Guo-ping Zhao for scientific suggestions on the project.Drs.Hong Li and Guoqing Zhang from Bigdata Center of Shanghai Insistute of Biological Science CAS helped to construct an integrative database with both clinical and multi-omics source data. Figure: 1 Figure 1 . Figure 1.Study scheme.
What the sources say
- Not checked — no full text of the sourcecites [46] Ayelet, 2015, Commensal bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy, Science source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
The paper relies on this without support.
The baseline fecal samples available from 25 of the 37 enrolled patients are representative of the full enrolled cohort.
“Fecal samples at baseline were obtained from 25 patients, among whom 13 patients were R and 12 patients were NR (Fig. 1).”
The paper relies on this without support.
Pro-inflammatory gram-negative bacteria in the gut of older patients increase systemic chronic inflammation largely via lipopolysaccharide release.
“It is already evident that the increase of pro-inflammatory gramnegative bacteria in the gut of older patients is associated with systematic and chronic inflammation.It is largely mediated by more release of lipopolysaccharide.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“Numerous studies have shown that increased gut microbiome diversity is closely associated with improved responses to ICIs25,123,137,138.”
From Microbiome meets immunotherapy: unlocking the hidden predictors of immune checkpoint inhibitors (2025) · cites this paper as [25]
In the citing paper
“the diversity of gut microbiota in patients with lung cancer was positively correlated with the efficacy of immunotherapy (25,26).”
From The Role of Gut Microbiota in Lung Cancer: From Carcinogenesis to Immunotherapy (2021) · cites this paper as [25]
In the citing paper
“This observation was confirmed in prospective trials and large meta-analyses, suggesting that gut microbiota may be instrumental for the immunostimulatory mode of action of ICI 23,24 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [23]
In the citing paper
“Confirming the clinical significance of bacterial diversity and commensals associated with responses, our results validate the growing body of evidence linking ATB use and poor clinical outcome 23,45 .”
From Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer (2022) · cites this paper as [23]
In the citing paper
“In previous baseline studies, P. copri has been associated with ICB response26,27.”
From Longitudinal gut microbiome changes in immune checkpoint blockade-treated advanced melanoma (2024) · cites this paper as [27]
In the citing paper
“Additionally, germline genetic variations389–392 and microbiome differences between individuals359,393–395 are likely to influence therapeutic responses and immune-related adverse effects.”
From TGFβ biology in cancer progression and immunotherapy (2021) · cites this paper as [395]
In the citing paper
“Jin et al enrolled 37 Chinese advanced NSCLC patients receiving nivolumab and patients using second-generation sequencing, found an enrichment of Alistipes putredinis, Bifidobacterium longum and Prevotella copri in responding patients, whereas Ruminococcus_unclassified was enriched in non-responding patients.51”
In the citing paper
“Conversely, antibiotics treatment altered the intestinal microbiota at a family level, followed by reduced cytotoxic NK cells and increased growth of intracranial glioma, suggesting that an abundant microbiome facilitated the accumulation of NK cells and enhanced tumor surveillance [29].”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [29]
In the citing paper
“A. muciniphila is positively associated with anti-PD-1 antibodies response in NSCLC patients,2,38 and its baseline level in stool has been shown to predict this enhanced response.10”
From Faecalibacterium prausnitzii strain EXL01 boosts efficacy of immune checkpoint inhibitors (2024) · cites this paper as [38]
In the citing paper
“According to their results, responding patients harbored higher diversity and stable composition of innate gut microbiome during treatment and also had significantly prolonged PFS.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [58]
In the citing paper
“In detail, Alistipes putredinis, Bifidobacterium longum, and Prevotella copri were enriched in responders, whereas Ruminococcus_unclassified was found mainly in non-responding patients.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [58]
In the citing paper
“As expected, a greater frequency of memory CD8+ T cell and natural killer cell subgroups was also observed in the periphery blood of responding patients.”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [58]
In the citing paper
“In Chinese patients with advanced non-small-cell lung carcinoma, the higher was the diversity of the gut microbiota, the better was the response observed to anti-PD-1 immunotherapy (58).”
From Gut Microbiome as a Potential Factor for Modulating Resistance to Cancer Immunotherapy (2020) · cites this paper as [58]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Responder EGFR-negative percentage is incorrect
MinorTwenty-two of 23 responders were EGFR-mutation negative, or about 95.7%, not 99.6%.
Reported 99.6 · recomputed 95.652174
“| No | 33 | 22(99.6) | 11(78.6) | |”
Responder male percentage is incorrect
MinorThere were 20 male responders among 23 responders, or about 87.0%, not 70.0%.
Reported 70 · recomputed 86.956522
“| Male | 29 | 20(70.0) | 9(69.2) | 0.215 |”
Nonresponder female percentage is incorrect
MinorFive of 14 nonresponders were female, or about 35.7%, not 30.7%.
Reported 30.7 · recomputed 35.714286
“| Female | 8 | 3(30.0) | 5(30.7) | |”
Enrollment count differs between abstract and results
MinorThe abstract says 37 patients were enrolled, whereas the results say 42 were enrolled and that 37 remained after exclusions.
“Methods: Thirty-seven patients with advanced NSCLC receiving treatment with nivolumab were enrolled in CheckMate 078 (NCT02613507) and CheckMate 870 (NCT03195491).”
“Forty-two Chinese patients with advanced NSCLC were consented and enrolled.”
Nonresponder male percentage is incorrect
MinorNine of 14 nonresponders were male, or about 64.3%, not 69.2%.
Reported 69.2 · recomputed 64.285714
“| Male | 29 | 20(70.0) | 9(69.2) | 0.215 |”
Responder squamous-histology percentage is incorrect
MinorNine of 23 responders had squamous histology, or about 39.1%, not 29.1%.
Reported 29.1 · recomputed 39.130435
“| Squamous | 15 | 9(29.1) | 6(42.9) | >0.999 |”
Nonresponder stage III percentage uses the wrong scale
MinorOne of 14 nonresponders had stage III disease, or about 7.1%. The reported 0.07 resembles a fraction rather than a percentage, unlike the adjacent percentages.
Reported 0.07 · recomputed 7.142857
“| III | 6 | 5(21.7) | 1(0.07) | 0.376 |”
Responder female percentage is incorrect
MinorThree of 23 responders were female, or about 13.0%, not 30.0%.
Reported 30 · recomputed 13.043478
“| Female | 8 | 3(30.0) | 5(30.7) | |”
Citations
Cites
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21492 · Cited by 84,109
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887
Safety, activity, and immune correlates of anti–PD-1 antibody in cancer
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Metadata
- Authors
- Jin, Y., Dong, H., Xia, L., Yang, Y., Zhu, Y., Shen, Y., Zheng, H., Yao, C., Wang, Y., & Lu, S.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Chinese National Human Genome Center at Shanghai (CN)
- Venue
- Journal of Thoracic Oncology
- Publisher
- Elsevier BV
- Published
- 2019-08
- Volume
- 14
- Issue
- 8
- Pages
- 1378-1389
- ISSN
- 1556-0864 (ISSN-L)
- OpenAlex
- W2942123458
- Cited by
- 573
- References
- 56
- Citations by year
- 2026: 71 · 2025: 100 · 2024: 97 · 2023: 91 · 2022: 71 · 2021: 90 · 2020: 43 · 2019: 10
- FWCI
- 22.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Thoracic Oncology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- gut microbiota, microbiome diversity, non-small cell lung cancer, anti-PD-1 therapy, nivolumab, immune checkpoint inhibitors, treatment response prediction, progression-free survival, memory CD8+ T cells, natural killer cells, Alistipes putredinis, Bifidobacterium longum, Prevotella copri, Ruminococcus, Chinese patients
- MeSH terms
- Gastrointestinal Microbiome, Antineoplastic Agents, Immunological, Nivolumab, Carcinoma, Non-Small-Cell Lung, Clinical Trials as Topic, Feces, Female, Humans, Lung Neoplasms, Male, Middle Aged, Disease Progression, Asian People, Programmed Cell Death 1 Receptor
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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