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Cited by 586Gut microbiota and healthProbiotics and Fermented FoodsCancer Research and Treatments

Gut Microbiota and Cancer: From Pathogenesis to Therapy

Open access
Vivarelli, Silvia, Salemi, Rossella, Candido, Saverio, Falzone, Luca, Santagati, Maria, Stefani, Stefania, Torino, Francesco, Banna, Giuseppe Luigi +2 more·2019·Cancers
DOI 10.3390/cancers11010038PMC PMC6356461
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Abstract

Cancer is a multifactorial pathology and it represents the second leading cause of death worldwide. In the recent years, numerous studies highlighted the dual role of the gut microbiota in preserving host’s health. Gut resident bacteria are able to produce a number of metabolites and bioproducts necessary to protect host’s and gut’s homeostasis. Conversely, several microbiota subpopulations may expand during pathological dysbiosis and therefore produce high levels of toxins capable, in turn, to trigger both inflammation and tumorigenesis. Importantly, gut microbiota can interact with the host either modulating directly the gut epithelium or the immune system. Numerous gut populating bacteria, called probiotics, have been identified as protective against the genesis of tumors. Given their capability of preserving gut homeostasis, probiotics are currently tested to help to fight dysbiosis in cancer patients subjected to chemotherapy and radiotherapy. Most recently, three independent studies show that specific gut resident species may potentiate the positive outcome of anti-cancer immunotherapy. The highly significant studies, uncovering the tight association between gut microbiota and tumorigenesis, as well as gut microbiota and anti-cancer therapy, are here described. The role of the Lactobacillus rhamnosus GG (LGG), as the most studied probiotic model in cancer, is also reported. Overall, according to the findings here summarized, novel strategies integrating probiotics, such as LGG, with conventional anti-cancer therapies are strongly encouraged.

AI snapshot

Written from the paper’s full text.

TL;DR

This narrative review summarizes the dual role of gut microbiota in cancer, from tumor-suppressive and tumor-promoting mechanisms to modulation of anti-cancer therapy. It highlights probiotics, especially *Lactobacillus rhamnosus* GG (LGG), and the emerging evidence linking specific gut species to immunotherapy response.

Key findings

  • Gut microbiota can be tumor-suppressive or oncogenic: microbial-derived short-chain fatty acids such as butyrate and propionate inhibit histone deacetylases, while dysbiosis-associated pathogens can release toxins causing DNA breaks; microbial pathogens are stated to drive 20% of tumorigenesis.
  • LGG is described as the most studied probiotic model in cancer, with anti-inflammatory effects, attenuation of 5-FU- and radiation-mediated gut epithelial injury in animal models, anti-proliferative/anti-metastatic effects in colorectal, ovary, breast, cervical, hepatic and oral squamous in vitro tumor models, prevention of polyps in a colorectal APC/min mouse model, and reduction of colitis-associated cancer in mice.
  • Inflammasomes are double-edged in tumorigenesis: in colorectal cancer they are protective via IL-18, whereas in lung, skin, breast and pancreatic cancer IL-1β is pro-inflammatory and tumor-promoting; NLRP6 regulates susceptibility to intestinal inflammation through microbiome-modulatory activity.
  • Three independent 2018 studies linked gut microbiome composition to immune checkpoint inhibitor response; anti-PD1 responders were enriched in taxa such as *Akkermansia*, *Alistipes*, *Clostridiales*, *Ruminococcaceae*, *Faecalibacteriae*, *Bifidobacterium longum*, *Enterococcus faecium* and *Collinsella aerofaciens*, and antibiotics were associated with lower survival in melanoma patients treated with anti-PD1/anti-PD-L1.

Methods

  • Narrative review; no systematic search strategy, inclusion criteria, or meta-analysis is stated.
  • Synthesizes preclinical studies (in vitro and mouse models), clinical trials, and translational studies, including three 2018 studies on microbiome and immunotherapy; no primary data are generated.
  • Main analysis is qualitative synthesis of mechanisms and therapeutic implications, with referenced tables of LGG and clinical studies.

Limitations

  • The paper states that microbiome research is at its beginning, associative and functional studies need corroboration by larger clinical studies, no strong bacterial oncogenic driver has been identified, and it is difficult to determine whether microbiota changes affect cancer genesis or vice versa.
  • The paper notes that lifestyle, diet, immune status and anti-cancer treatment itself influence the microbiome, and that larger controlled trials are needed to confirm probiotic efficacy and safety; FMT lacks control because whole microbiota is transferred, and donor health must be carefully controlled.
  • Evident from the text: as a narrative review, it does not describe a systematic literature search, study selection, or risk-of-bias assessment.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3390/cancers11010038

Cites

202 of 202 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 207 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    The gut microbiome can be either tumor-suppressive or oncogenic.

    “In fact, the gut microbiome can either be tumor-suppressive or oncogenic [22,23].”
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    Leptin and ghrelin can be sensed by gut bacteria and finely tune the gut microbiota composition in rodents.

    “A number of these hormones can be sensed by the gut bacteria, as in the case of leptin and ghrelin, which, in turn, finely tune the gut microbiota composition in rodents [29,30].”
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  • Premisecitation

    The gastro-intestinal microbiome has a dual role in cancer prevention, tumorigenesis and anti-cancer therapy.

    “Metabolomics and metagenomics studies highlighted the dual role of the gastro-intestinal microbiome in cancer prevention, tumorigenesis and anti-cancer therapy [21].”
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    Host hormones and neuro-hormones are able to modify the gut microbiome composition, as during stress response.

    “In particular, it is known that host’s hormones and neuro-hormones are able to modify the gut microbiome composition, as during stress response [27].”
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    The gut microbiota deeply influences host homeostasis.

    “Among the human symbiotic microbial populations, the gut microbiota is the most extensively studied and it deeply influences host’s homeostasis [7].”
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    Premisecitation

    Any imbalance in the gut microbial equilibrium may lead to dysbiosis, which is linked with several human pathologies including cancer.

    “Any imbalance in this delicate equilibrium may lead to an impaired microbiota, condition called dysbiosis, linked with several human pathologies, including cancer [13].”
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    Premisecitation

    The gut microbiota performs vital functions including production of vitamins, metabolization of dietary compounds, and protection against expansion and systemic infiltration of gut pathogens.

    “The gut microbiota performs a number of vital functions, including production of vitamins, metabolization of dietary compounds, protection against the expansion and systemic infiltration of gut pathogens [10,11,12].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
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    Premisecitation

    Among approximately 1000 different bacterial species within the gut microbiota, Firmicutes and Bacteroidetes are highly represented.

    “Among a 1000 of different bacterial species within the gut microbiota, the highly represented ones are the Firmicutes and Bacteroidetes phyla [9].”
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    Premisecitation

    Exposure to infectious agents, UV radiation, toxic substances, individual diet and lifestyle strongly influences cancer rise, although the risk mainly depends on dose, duration, combination of such injuries, and individual genetic background.

    “For example, the exposure to infectious agents, UV radiation and toxic substances, individual diet and lifestyle, strongly influences cancer rise, although the risk mainly depends on the dose, the duration and the combination of such injuries, coupled with the individual genetic background [5].”
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    The gastro-intestinal entero-endocrine cells secrete over 30 different peptide hormones involved in gastro-intestinal motility, digestive functions and neuromodulation.

    “Importantly, the gastro-intestinal entero-endocrine cells secrete over 30 different peptide hormones, involved in several functions, such as gastro-intestinal motility, digestive functions and neuromodulation [28].”
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    Premisecitation

    Cancer formation results from the stochastic intracellular accumulation of spontaneous mutations during DNA replication combined with environmental exposure and lifestyle habits, both of which influence cancer risk.

    “Cancer formation is the result of the stochastic intracellular accumulation of spontaneous mutations during DNA replication, combined with the environment exposure and lifestyle habits, both able to significantly influence cancer risk [3,4].”
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    Premisecitation

    Cancer development may alter the microbiome and, in turn, microbiome changes may affect cancer progression.

    “As a consequence, cancer development may alter the microbiome and, in turn, microbiome changes may affect cancer progression [24].”
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    • cites [24] Zitvogel, 2017, Anticancer effects of the microbiome and its products, Nat. Rev. Microbiol. source

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    The gut microbiome encodes 100-fold more genes than the human genome.

    “The gut microbiome, defined as the whole genome of the host’s gut microbiota, encodes 100-fold more genes than the human genome [14].”
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    • cites [14] Grice, 2012, The human microbiome: Our second genome, Annu. Rev. Genom. Hum. Genet. source

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    Premisecitation

    The gut microbiota may produce or transform molecules affecting host metabolism, gut barrier integrity, xenobiotics and drug metabolism, protection against gastro-intestinal pathogens, and host immune system modulation.

    “In fact, it has been widely studied that the gut microbiota may produce or transform molecules affecting several aspects of human health, including: host’s metabolism modulation, gut barrier integrity maintenance, xenobiotics and drug metabolism, protection against gastro-intestinal pathogens and host’s immune system modulation [31,32,33,34].”
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    Premisecitation

    Certain commensal bacteria produce essential micronutrients such as vitamin K and various components of vitamin B.

    “With regards to the host’s metabolism, it is known that certain commensal bacteria produce essential micronutrients, such as vitamin K and various components of vitamin B.”
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    The gut is bidirectionally connected with the nervous system through the gut-brain axis, which includes the central nervous system, autonomic nervous system, enteric nervous system, hypothalamic pituitary adrenal axis and entero-endocrine system.

    “The gut is bidirectionally connected with the nervous system through the so-called “gut-brain axis” (GBA), which includes the central nervous system (CNS), the autonomic nervous system (ANS), the enteric nervous system (ENS), the hypothalamic pituitary adrenal (HPA) axis and the entero-endocrine system (EES).”
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    Premisecitation

    Members of the Bacterioides family can synthetize the anti-diabetic compound linoleic acid, catabolize secondary bile acids, and break down phenolic compounds.

    “Also, members of the Bacterioides family are able to synthetize the anti-diabetic compound linoleic acid, to catabolize secondary bile acids and to break down phenolic compounds.”
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    • cites [35] Mohajeri, 2018, The role of the microbiome for human health: From basic science to clinical applications, Eur. J. Nutr. source

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    Premisecitation

    Bacterial lipopolysaccharide activates toll-like receptor 4, thus activating immune T cell-mediated response against cancer cells.

    “For example, the widely studied bacterial lipopolysaccharide (LPS), a major component of the outer membrane in gram-negative bacteria, activates the host’s cell surface receptor toll-like receptor 4 (TLR4), belonging to the family of pattern recognition receptors (PRRs), thus activating immune T cell-mediated response against cancer cells [40].”
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    Premisecitation

    Microbial pathogens drive 20% of tumorigenesis and a larger number of malignancies are associated with microbial commensal imbalance or dysbiosis.

    “Microbial pathogens are known to drive the 20% of tumorigenesis and a larger number of malignancies are associated with microbial commensal imbalance, or dysbiosis [53].”
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    • cites [53] Bhatt, 2017, The role of the microbiome in cancer development and therapy, CA Cancer J. Clin. source

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    Enterococcus faecalis produces extracellular superoxide and derivative oxygen species capable of diffusing into host cells, and the increase in oxidative milieu enhances the possibility of host cellular DNA mutations.

    “Enterococcus faecalis produces extracellular superoxide and derivative oxygen species is capable to diffuse into host’s cells. In turn, the increase in the oxidative milieu enhances the possibility of host’s cellular DNA mutations [79].”
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    Premisecitation

    Lactobacilli may stimulate host immune cells such as NK cells, dendritic cells, or TH1 response, leading to elimination of cancerous or precancerous cells, although the exact bacterial bioproduct mediating this effect still needs identification.

    “It has been also reported in several studies that Lactobacilli may stimulate host’s immune cells such as NK cells or dendritic cells (DC) or TH1 response, which, in turn, leads to the elimination of cancerous or precancerous cells, although the exact bacterial bioproduct mediating such stimulatory effect still needs to be identified [45,46,47,48].”
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    Premisecitation

    Fusobacterium nucleatum inhibits host Natural Killer cells to recruit myeloid suppressor cells, indirectly helping cancer genesis.

    “For example, Fusobacterium nucleatum inhibits for its own advantage host’s Natural Killer (NK) cells, in order to recruit at the site of the infection myeloid suppressor cells, therefore indirectly helping cancer genesis.”
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    Premisecitation

    Anti-cancer treatment might shape the patient's microbiome and host-specific microbiome can deeply affect patient's response to therapy.

    “Moreover, the very same anti-cancer treatment might shape the patient’s microbiome and, at the same time, host’s specific microbiome can deeply affect patient’s response to therapy [19].”
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    • cites [19] Gopalakrishnan, 2018, The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy, Cancer Cell source

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    Premisecitation

    CagA from Helicobacter pylori can bind host protein tyrosine phosphatase SHP-2; CagA-SHP-2 complex formation deregulates SHP-2 phosphatase activity, promoting Ras/MAPK signaling activation.

    “In particular, CagA from Helicobacter pylori can bind many host’s proteins intracellularly, including the protein tyrosine phosphatase SHP-2. CagA-SHP-2 complex formation deregulates the phosphatase activity of SHP-2, which, in turn, promotes Ras/MAPK signaling activation [73].”
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    • cites [73] Matozaki, 2009, Protein tyrosine phosphatase SHP-2: A proto-oncogene product that promotes Ras activation, Cancer Sci. source

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    Premisecitation

    Augmented intake of estrogen hormones is linked with increased risk of developing breast cancer, and the gut microbiota composition of women with breast cancer differs from that of healthy controls.

    “Accordingly, this augmented intake of estrogen hormones is linked with an increased risk of developing breast cancer, supporting the finding that the gut microbiota composition of women with breast cancer differs from that from healthy controls, and suggesting that several gut bacteria, which could be over-expressed during dysbiosis, may be linked with breast cancer development [83].”
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    Premisecitation

    In animal models, LGG administered with food attenuates 5-FU-mediated and radiation-mediated gut epithelial injury, helping preservation of gut microbiota balance and intestinal epithelial barrier functionality.

    “In animal models, LGG administered with food attenuates 5-FU-mediated as well as radiation-mediated gut epithelial injury, therefore helping the preservation of the gut microbiota balance and the intestinal epithelial barrier functionality [91,92,93].”
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    Premisecitation

    LGG prevents polyp formation in a colorectal APC/min mouse cancer model and reduces colitis-associated cancer in mice.

    “In addition, LGG prevents polyps’ formation in a colorectal APC/min mouse cancer model, and reduces colitis-associated cancer in mice [108,109].”
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    • cites [108] Ni, 2017, A metagenomic study of the preventive effect of Lactobacillus rhamnosus GG on intestinal polyp formation in APC, J. Appl. Microbiol. source

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    • cites [109] Mendes, 2018, Microbiota modification by probiotic supplementation reduces colitis associated colon cancer in mice, World J. Gastroenterol. source

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    Premisecitation

    Host dendritic cells exposed to LGG induce TH1 immune cell polarization and antitumor immune-response potentiation.

    “Additionally, host’s DC exposed to LGG induce TH1 immune cells polarization and, in turn, antitumor immune-response potentiation [111].”
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    • cites [111] Cai, 2016, Lactobacillus rhamnosus GG Activation of Dendritic Cells and Neutrophils Depends on the Dose and Time of Exposure, J. Immunol. Res. source

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    Premisecitation

    The gut microbial population plays a key role in training, functioning and stimulating the host immune system, developing tolerance towards beneficial microbiota and eliciting immune response against gut pathogens.

    “The gut microbial population plays a key role in training, functioning and stimulating the host immune system, with the final effect of developing tolerance towards beneficial microbiota and eliciting immune response against gut pathogens [76].”
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    • cites [76] Belkaid, 2014, Role of the microbiota in immunity and inflammation, Cell source

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    Premisecitation

    LGG triggers the immune response within normal not transformed gut epithelium, protecting against inflammation that can support formation of a cancer-favorable milieu.

    “LGG triggers the immune response also within the normal not transformed gut epithelium, thus protecting towards inflammation, which can support the formation of a cancer-favorable milieu [112].”
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    • cites [112] Suzuki, C., Aoki-Yoshida, A., Aoki, R., Sasaki, K., Takayama, Y., and Mizumachi, K. (2017). The distinct effects of orally administered Lactobacillus rhamnosus GG and Lactococcus lactis subsp. lactis C59 on gene expression in the murine small intestine. PLoS ONE, 12. source

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    Premisecitation

    LGG is one of the first probiotic species studied specifically in oncology.

    “Among these probiotic species, LGG is one of the first studied specifically in oncology [87].”
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    • cites [87] Goldin, 1996, The effect of Lactobacillus GG on the initiation and promotion of DMH-induced intestinal tumors in the rat, Nutr. Cancer source

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    Premisecitation

    The mechanism of improved cisplatin response with probiotics involves induction of pro-apoptotic genes within the tumor mass and enhancement of the host immune response.

    “The mechanism involves the induction of pro-apoptotic genes within the tumor mass and the enhancement of host’s immune response [166].”
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    • cites [166] Gui, 2015, Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model, Genet. Mol. Res. source

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    Premisecitation

    CpG oligodeoxynucleotides mimic bacterial DNA, strongly stimulate the immune system, and show anti-tumor activity in several cancers.

    “With reference to immunotherapy, the administration of CpG oligodeoxynucleotides, synthetic molecules mimicking bacterial DNA, strongly stimulate the immune system, therefore showing anti-tumor activity in several cancers [169].”
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    • cites [169] Weiner, 2008, CpG oligodeoxynucleotides as immunotherapy in cancer, Update Cancer Ther. source

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    Interpretationcitation

    Interventions on the microbiome may be pivotal to ameliorate anti-cancer therapy-related toxicity and improve anti-cancer therapy efficacy.

    “Specifically, interventions on microbiome may be pivotal to ameliorate anti-cancer therapy-related toxicity, as well as to improve anti-cancer therapy efficacy [151,152].”
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    • cites [151] Nayak, R.R., and Turnbaugh, P.J. (2016). Mirror, mirror on the wall: Which microbiomes will help heal them all?. BMC Med., 14. source

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    • cites [152] Fessler, 2017, The Microbiota: A New Variable Impacting Cancer Treatment Outcomes, Clin. Cancer Res. source

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    Interpretationreasoning

    The patient's microbiome composition affects the efficacy of both chemotherapy and immunotherapy.

    “These two effects combined together may explain the strong involvement of the patient’s microbiome composition in affecting the efficacy of both chemotherapy and immunotherapy [19].”
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    • cites [19] Gopalakrishnan, 2018, The Influence of the Gut Microbiome on Cancer, Immunity, and Cancer Immunotherapy, Cancer Cell source

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    Interpretationreasoning

    Dysbiosis of the gut microbiota can influence both cancer pathogenesis and therapeutic outcome.

    “The microbiota, when affected by dysbiosis, can deeply influence both cancer pathogenesis (as reported in Section 2) and its therapeutic outcome.”
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    Premisecitation

    Intra-tumoral injection of CpG oligodeoxynucleotides together with an anti-IL-10R antibody induces TNF production from tumor-infiltrating myeloid cells and reduces growth of several tumor types in mice.

    “Along this line, the intra-tumoral injection of CpG oligodeoxynucleotides administered together with an anti-interleukin-10 receptor (IL-10R) antibody, induce TNF production from tumor infiltrating myeloid cells and, in turn, reduce the growth several types of tumors in mice [165].”
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    Premisecitation

    In 1890, heat-inactivated Streptococci were injected intratumorally in humans for the first time as an attempt to cure cancer.

    “Back in 1890 two heat-inactivated microorganisms (Streptococci) were injected intratumorally for the very first time in humans as an attempt to cure cancer [153,154].”
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    Premisecitation

    Almost every available anti-cancer treatment is toxic also towards normal cells, and their use may be coupled with side effects, some of which can compromise overall survival of patients.

    “Because almost every available anti-cancer treatment is toxic also towards normal cells, their use may be coupled with side effects, some of which can compromise the overall survival of the patients [140].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [140] Dy, 2013, Understanding, recognizing, and managing toxicities of targeted anticancer therapies, CA Cancer J. Clin. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The gut microbiota regulates therapeutic outcome by metabolizing anti-tumoral compounds and by modulating the host immune response and inflammation pathways.

    “In particular, the regulation of such therapeutic outcome is tightly connected with the ability of the gut microbiota to metabolize anti-tumoral compounds, as well as to modulate host’s immune response and inflammation pathways [164].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [164] Schwabe, 2013, The microbiome and cancer, Nat. Rev. Cancer source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Mice bearing lung tumors treated with cisplatin plus antibiotics survive less and develop bigger tumors.

    “Consistently, mice bearing lung tumors treated with cisplatin coupled with antibiotics, survive less and develop bigger tumors.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [166] Gui, 2015, Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model, Genet. Mol. Res. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Radiotherapy, chemotherapy and immunotherapy treatments can all modify patients' microbiome and microbiome composition can deeply affect patients' response to such therapies.

    “In fact, radiotherapy, chemotherapy and immunotherapy treatments can all modify patients’ microbiome and, at the same time, microbiome composition can deeply affect patients’ response to such therapies [150].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [150] Roy, 2017, Microbiota: A key orchestrator of cancer therapy, Nat. Rev. Cancer source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    NLRP6 plays a key role in colorectal carcinogenesis and regulates susceptibility to intestinal inflammation through its microbiome-modulatory activity.

    “Regarding the correlation between inflammasomes, microbiome and cancer, NRPL6 plays a key role in colorectal carcinogenesis and, in particular, NLRP6 regulates susceptibility to intestinal inflammation through its microbiome-modulatory activity [139].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [139] Elinav, 2018, NLRP6 and Dysbiosis: Avoiding the Luring Attraction of Over-Simplification, Immunity source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In colorectal cancer, inflammasome activation has a protective role; in breast and skin cancers, their triggering leads to detrimental outcomes.

    “In CRC inflammasomes activation has a protective role, on the contrary in breast and skin cancers their triggering leads to detrimental outcomes [119].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [119] Kantono, 2017, Inflammasomes and Cancer: The Dynamic Role of the Inflammasome in Tumor Development, Front. Immunol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    NLRP6 KO mice show dysbiosis and increased incidence of inflammation-associated colorectal cancer.

    “NLRP6 KO mice show dysbiosis and increased incidence of inflammation-associated CRC [135,136,137].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [135] Elinav, 2011, NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis, Cell source

      Not checked in the free run.

    • cites [136] Levy, 2015, Microbiota-Modulated Metabolites Shape the Intestinal Microenvironment by Regulating NLRP6 Inflammasome Signaling, Cell source

      Not checked in the free run.

    • cites [137] Levy, 2017, NLRP6: A Multifaceted Innate Immune Sensor, Trends Immunol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Intra-tumoral variety is tightly linked with development of resistance to therapy, considered the first cause of failure of available anti-cancer treatments, as well as subsequent tumor relapses.

    “Importantly, this intra-tumoral variety is tightly linked with the development of the resistance to therapy, considered the first cause of failure of the available anti-cancer treatments, as well as subsequent tumor relapses [146].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [146] McGranahan, 2015, Biological and therapeutic impact of intratumor heterogeneity in cancer evolution, Cancer Cell source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Immune checkpoint inhibitors have success in treating various malignancies, but a significant number of patients can use such therapy only for a limited time due to strong toxic side effects including gut inflammation from immune dysregulation.

    “Although the immune checkpoint inhibitors have success in treating various malignancies, there is still a significant number of patients that can use such therapy only for a limited amount of time, given the occurrence of strong toxic side effects, including gut inflammation, due to the subsequent immune-dysregulation (i.e., autoimmunity) [177].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [177] Larkin, 2015, Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma, N. Engl. J. Med. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In a double-blind study, a mixture of Bifidobacterium longum BB536 and Lactobacillus johnsonii La1 was administered to patients; La1 adhered to the colonic mucosa, reducing gut pathogen concentration and modulating local immunity.

    “A mixture of two probiotic species Bifidobacterium longum (BB536) and Lactobacillus johnsonii (La1) was administered to the patients in the double-blind study, finding that one of that, La1, was able to adhere to the colonic mucosa, thereby reducing the concentration of gut pathogens and modulating the local immunity [95].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [95] Gianotti, 2010, A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients, World J. Gastroenterol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    FMT in germ-free mice with the identified bacteria along with anti-PD1 therapy enhanced anti-cancer effects and reduced melanoma growth.

    “Functional studies performed with FMT in germ free mice further demonstrated how treating mice with the identified bacteria, along with the anti-PD1 therapy, enhanced the anti-cancer effects and reduces the melanoma growth [171].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [171] Gopalakrishnan, 2018, Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients, Science source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Immune checkpoint inhibition blocks the immune-inhibitory pathway, thereby modulating T cell activation against tumor target cells.

    “Immune checkpoint inhibition consists in the administration of therapeutic agents able to block the immune-inhibitory pathway, thus modulating T cell activation against tumor target cells.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [173] Chen, 2018, Delivery Strategies for Immune Checkpoint Blockade, Adv. Healthc. Mater. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    FMT from patients to germ-free mice showed that Akkermansia muciniphila alone or with Enterococcus hirae increased intra-tumoral cytotoxic T cell infiltrates, thereby increasing PD-1 blockade response in mice.

    “Performing FMT from patients to germ free mice, the authors found that Akkermansia muciniphila (alone or in combination with Enterococcus hirae) was able to increase intra-tumoral cytotoxic T cell infiltrates, thus increasing the PD-1 blockade response in mice [170].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [170] Routy, 2018, Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors, Science source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Administration of Alistipes shahii to antibiotic-treated tumor-bearing mice restores TNF production and improves therapeutic outcome.

    “Moreover, the administration of a specific bacteria, Alistipes shahii, to antibiotic-treated tumor bearing mice, restores TNF production with a notable improvement in the therapeutic outcome [165].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [165] Iida, 2013, Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment, Science source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In 2017, randomized administration of Bifidobacterium lactis and Lactobacillus acidophilus to CRC patients can change the epigenetic patterns of tumor tissue from baseline, with potential therapeutic benefits in CRC by manipulation of the gut microbiota.

    “Moreover, according to the result of a trial published in 2017, the randomized administration of Bifidobacterium lactis and Lactobacillus acidophilus to CRC patients, can change the epigenetic patterns of tumor tissue from its baseline, with potential therapeutic benefits in CRC by manipulation of the gut microbiota [100].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [100] Hibberd, 2017, Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention, BMJ Open Gastroenterol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    MASCC/ISOO and ESMO guidelines suggest probiotics containing Lactobacillus species be used to prevent diarrhea in patients receiving chemotherapy and/or radiation therapy for a pelvic malignancy (Level of evidence III).

    “probiotics containing Lactobacillus species are suggested be used to prevent diarrhea in patients receiving chemotherapy and/or radiation therapy for a pelvic malignancy (Level of evidence III) [193,194].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [193] Peterson, 2015, Management of oral and gastrointestinal mucosal injury: ESMO Clinical Practice Guidelines for diagnosis, treatment, and follow-up, Ann. Oncol. source

      Not checked in the free run.

    • cites [194] Lalla, 2014, MASCC/ISOO clinical practice guidelines for the management of mucositis secondary to cancer therapy, Cancer source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Probiotics are generally regarded as safe, but administering them to immunocompromised cancer patients carries potential risk of opportunistic infection development and transfer of antibiotics resistance.

    “Although probiotics are generally regarded as safe, the main concerns of administering them to immunocompromised cancer patients are both the potential risk of opportunistic infection development and the transfer of antibiotics resistance [190,191].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [190] Vanderhoof, 2008, Probiotics in the United States, Clin. Infect. Dis. source

      Not checked in the free run.

    • cites [191] Redman, 2014, The efficacy and safety of probiotics in people with cancer: A systematic review, Ann. Oncol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    CTLA-4 regulates T cell proliferation early in the immune response within lymph nodes, while PD-1 suppresses T-cell activation later in the body periphery.

    “While CTLA-4 regulates T cells proliferation early in the immune response within the lymph nodes, PD-1 suppresses T-cell activation later, within the body periphery [174].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [174] Buchbinder, 2016, CTLA-4 and PD-1 Pathways: Similarities, Differences, and Implications of Their Inhibition, Am. J. Clin. Oncol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Oral administration of a cocktail of Bifidobacterium species combined with anti-PD-L1 antibody boosts T cell response and blocks melanoma growth in mice.

    “In fact, they demonstrated that oral administration of a cocktail of Bifidobacterium species combined with the anti-PD-L1 antibody, specifically boosts T cell response and blocks the melanoma growth [176].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [176] Sivan, 2015, Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy, Science source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Probiotics administration in multiple trials has shown beneficial effects on ameliorating diarrhea and other gut-related damages following anti-cancer therapy, re-establishing a healthy intestinal microbiota composition.

    “Despite of that, probiotics administration in multiple trials has shown beneficial effects on ameliorating diarrhea and other gut-related damages following anti-cancer therapy, thus re-establishing a healthy intestinal microbiota composition [192].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [192] Mego, 2013, Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy, Complement. Ther. Med. source

      Not checked in the free run.

  • The quote only partly states this claim.

    Premisecitation

    Metagenomics analysis of patients' fecal gut microbiome showed a difference in composition between anti-PD1 responders and non-responders.

    “Importantly, metagenomics analysis of patients’ fecal gut microbiome showed a difference in the composition of their gut microbiome.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [170] Routy, 2018, Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors, Science source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Gut microbiota composition modulates both immunotherapy response and toxicity.

    “Altogether, these data provide a strong evidence of the role of gut microbiota composition in modulating the effect of both immunotherapy response and toxicity.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationnone given

    LGG is a probiotic well studied in cancer and often administered as a complementary therapeutic to cure dysbiosis.

    “LGG is a very good example of a probiotic well studied in cancer, often administered as complementary therapeutic to cure dysbiosis.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    There are still many obstacles for translating basic microbiome research into therapeutic applications.

    “Even if the last decade witnessed massive advances in unveiling the role of gut microbiome in cancer and other diseases, there are still many obstacles for translating basic microbiome research into therapeutic applications.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Potential pathogens can develop among gut bacteria and could limit or slow down the translation of in vitro and in vivo results to the clinic.

  • May combine two claims.

    Premisecitation

    Preclinical studies in mice demonstrated efficacy of FMT in reducing colon tumorigenesis, although efficacy in clinical trials still needs to be proven.

    “Regarding anti-tumor therapeutic applications, preclinical studies performed in mice demonstrated the efficacy of FMT in reducing colon tumorigenesis, although the efficacy in clinical trials still needs to be further proven [198].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [198] Bel, 2014, Reprogrammed and transmissible intestinal microbiota confer diminished susceptibility to induced colitis in TMF−/− mice, Proc. Natl. Acad. Sci. USA source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    FMT has been used to cure recurrent Clostridium difficile duodenal infection.

    “For example, FMT has been used to cure recurrent Clostridium difficile duodenal infection [195,196].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [195] Dijkgraaf, 2013, Duodenal infusion of feces for recurrent Clostridium difficile, N. Engl. J. Med.

      Not checked in the free run.

    • cites [196] Khoruts, 2016, Inflammatory Bowel Disease Affects the Outcome of Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection, Clin. Gastroenterol. Hepatol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Some bacterial subpopulations rise during gut dysbiosis and trigger formation of an inflammatory and pro-cancerogenic environment.

    “Some bacterial subpopulations are able to rise during gut dysbiosis and, in turn, to trigger the formation of an inflammatory and pro-cancerogenic environment.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Many gut-derived probiotics protect the host by re-establishing conditions of a healthy intestinal microbiota within dysbiotic patients, including cancer patients.

    “On the other hand, many gut derived probiotics are able to protect the host, re-establishing the conditions of a healthy intestinal microbiota within dysbiotic patients, including cancer patients.”
    Quote in the paperNot a substantial claim
61 of 61

  • The paper relies on this without support.

    The gut microbial balance is required for the correct fulfilment of the gut microbiota's metabolic functions.

    “The gut microbial balance has a key role in the correct fulfilment of all these pivotal metabolic functions.”

  • The paper relies on this without support.

    Potential pathogens can develop among gut bacteria and could limit or slow down the translation of in vitro and in vivo results to the clinic.

    “Among the gut bacteria can develop potential pathogens and that could limit, or at least slow down, the translation of the in vitro and in vivo results to the clinic.”

  • The paper relies on this without support.

    Each individual inherits a specific gut microbiota footprint since birth, and their intestinal microbiota develops and changes with aging, diet, and lifetime exposure to the heterogeneous environment.

    “Each individual inherited a specific gut microbiota footprint since their birth, and their intestinal microbiota develops and changes with aging, diet and lifetime exposure to the heterogeneous environment.”
3 of 3

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Authors
Vivarelli, S., Salemi, R., Candido, S., Falzone, L., Santagati, M., Stefani, S., Torino, F., Banna, G. L., Tonini, G., & Libra, M.
Affiliations
  • University of Catania (IT)
  • University of Rome Tor Vergata (IT)
  • Ospedale Cannizzaro (IT)
  • Università Campus Bio-Medico (IT)
Corresponding author
Libra, Massimo
ORCID
Venue
Cancers
Publisher
MDPI AG
Published
2019-01-03
Volume
11
Issue
1
Pages
38
ISSN
2072-6694 (ISSN-L)
DOI
10.3390/cancers11010038
PMC
PMC6356461
OpenAlex
W2906724057
Semantic Scholar
d102bbd36de209be8b4873bf86615a75268252ab
Cited by
586
References
204
Citations by year
2026: 41 · 2025: 59 · 2024: 84 · 2023: 79 · 2022: 103 · 2021: 92 · 2020: 91 · 2019: 37
FWCI
7.11
Type
journal article
Language
en
Open access
Licence
Locations
  • Cancers (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
Keywords
gut microbiota, cancer, carcinogenesis, dysbiosis, probiotics, Lactobacillus rhamnosus GG, cancer immunotherapy, chemotherapy, radiotherapy, intestinal homeostasis, inflammation, microbiota metabolites, host-microbe interactions

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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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-07.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-07.

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