Infectious complications following probiotic ingestion: a potentially underestimated problem? A systematic review of reports and case series
Open accessAbstract
BACKGROUND: Little is studied about complications related to probiotic ingestion. This study proposes to present a synthesis and critical evaluation of the reports and series of cases on the infectious complications related to the ingestion of probiotics, which can raise awareness for the prescribing and use of probiotics for certain groups of patients. METHODS: Systematic review of reports and series of cases researched in the PubMed, SciELO and Scopus databases published until August 2018. The references of the articles were investigated manually for the search of cross references. SPSS version 23.0 was used for descriptive statistics and univariate analysis. RESULTS: We found 60 case reports and 7 case series, making up a total of 93 patients. Fungemia was the most common infectious complications with 35 (37.6%) cases. The genus Saccharomyces was the most frequent with 47 (50.6%) cases, followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively. Adults over 60 years of age, Clostridium difficile colitis, antibiotic use and Saccharomyces infections were associated with overall mortality. HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death. CONCLUSION: The use of probiotics cannot be considered risk-free and should be carefully evaluated for some patient groups. TRIAL REGISTRATION: CRD42016042289.
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Written from the paper’s full text.
TL;DR
This systematic review of 60 case reports and 7 case series (93 patients, 1976–2018) found infectious complications after probiotic ingestion, most commonly fungemia and Saccharomyces infection. Mortality was associated with age >60 years, C. difficile colitis, antibiotic use, and Saccharomyces infection.
Key findings
- Among 93 patients, fungemia was most common at 35 (37.6%), followed by sepsis 29 (31.2%), bacteremia 19 (20.4%), endocarditis 4, and abscess 3; pneumonia, pleural empyema, and septic arthritis each occurred in 1 case.
- Saccharomyces was the most frequent genus with 47 (50.6%) cases, including S. cerevisiae 41 (44.1%), S. boulardii 5 (5.4%), and Saccharomyces spp. 1 (1.1%); Lactobacillus accounted for 26 (27.9%), Bifidobacterium 12 (12.8%), Bacillus 5 (5.4%), Pediococcus 2 (2.2%), and Escherichia coli 1 (1.1%).
- All-cause mortality was 19.6% (18 cases) and was associated with age >60 years (OR 6.25, 95% CI 1.89–20.1; p=0.003), C. difficile colitis (OR 11.8, 95% CI 2.89–48.81; p<0.001), antibiotic use (OR 9.75, 95% CI 1.51–17.11; p=0.002), and Saccharomyces spp. (OR 4.9, 95% CI 1.30–15.48; p=0.03). HIV infection, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, and enteral or parenteral nutrition were not associated with death.
- Blood was the most frequent isolation site, in 87 (93.5%) cases.
Methods
- Systematic review of case reports and case series searched in PubMed, SciELO, and Scopus from inception to August 8, 2018, with manual reference cross-checking; no language restriction; reported per PRISMA and registered at PROSPERO (CRD42016042289).
- Included infections after probiotic ingestion, including bacteremia/fungemia, sepsis, endocarditis, and abscess; 6797 records plus 55 cross-references yielded 67 articles (60 case reports, 7 case series) corresponding to 93 patients.
- Descriptive statistics and univariate analysis used SPSS version 23.0; categorical variables compared with chi-square and Fisher’s exact tests, continuous variables with Mann-Whitney test, two-tailed p<0.05; risk of bias assessed with a modified National Institutes of Health tool.
Limitations
- The paper states possible publication bias, with more serious cases more likely published, but also notes that case reports are increasingly difficult to publish, so other serious cases may not have reached public knowledge.
- The paper states that the mortality analysis did not consider other factors such as numbers and types of comorbidity, and that the review is not intended to discourage probiotic use.
- Evident from the text: case reports and case series cannot establish causality or incidence, and there is no denominator of all probiotic users; risk of bias was mostly “fair” (7/67, 10.4%, were “good”; none “poor”).
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
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- Findingown data
Adults over 60 years of age were associated with overall mortality.
“Adults over 60 years of age, Clostridium difficile colitis, antibiotic use and Saccharomyces infections were associated with overall mortality.”
- Also stated in: § Conclusion · plain
“Mortality was associated with age > 60 years, C. difficile colitis, current antimicrobial use and Saccharomyces infection.”
Quote in the paperSubstantial claim - Also stated in: § Conclusion · plain
- Findingown data
Enteral or parenteral nutrition were not associated with death.
“HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death.”
Quote in the paperNot a substantial claim - Findingown data
Endocarditis occurred in 4 cases.
“followed by endocarditis and abscess, with 4 and 3 cases, respectively.”
Quote in the paperNot a substantial claim - Findingown data
Saccharomyces infections were associated with overall mortality.
“Adults over 60 years of age, Clostridium difficile colitis, antibiotic use and Saccharomyces infections were associated with overall mortality.”
- Also stated in: § Conclusion · plain
“Mortality was associated with age > 60 years, C. difficile colitis, current antimicrobial use and Saccharomyces infection.”
Quote in the paperSubstantial claim - Also stated in: § Conclusion · plain
- Findingown data
Bifidobacterium accounted for 12 (12.8%) cases.
“followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively.”
- Also stated in: § Probiotic microorganisms involved in infectious complications · plain
“Of the 12 patients with infectious complications due to Bifidobacterium spp.”
Quote in the paperNot a substantial claim - Also stated in: § Probiotic microorganisms involved in infectious complications · plain
- Findingown data
Bacteremia was responsible for 19 (20.4%) cases.
“bacteremia was responsible for 19 (20.4%) of cases”
Quote in the paperNot a substantial claim - Findingown data
Immunosuppressive drugs were not associated with death.
“HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death.”
Quote in the paperNot a substantial claim - Findingown data
Abscess occurred in 3 cases.
“followed by endocarditis and abscess, with 4 and 3 cases, respectively.”
Quote in the paperNot a substantial claim - Findingown data
HIV infections were not associated with death.
“HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death.”
Quote in the paperNot a substantial claim - Findingown data
Sepsis was identified in 29 (31.2%) patients.
“Sepsis was identified in 29 (31.2%) patients;”
Quote in the paperNot a substantial claim - Findingown data
Solid organ transplantation was not associated with death.
“HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death.”
Quote in the paperNot a substantial claim - Findingown data
Clostridium difficile colitis was associated with overall mortality.
“Adults over 60 years of age, Clostridium difficile colitis, antibiotic use and Saccharomyces infections were associated with overall mortality.”
- Also stated in: § Conclusion · plain
“Mortality was associated with age > 60 years, C. difficile colitis, current antimicrobial use and Saccharomyces infection.”
Quote in the paperSubstantial claim - Also stated in: § Conclusion · plain
- Findingown data
Bacillus accounted for 5 (5.4%) cases.
“followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively.”
Quote in the paperNot a substantial claim - Findingown data
Antibiotic use was associated with overall mortality.
“Adults over 60 years of age, Clostridium difficile colitis, antibiotic use and Saccharomyces infections were associated with overall mortality.”
- Also stated in: § Conclusion · plain
“Mortality was associated with age > 60 years, C. difficile colitis, current antimicrobial use and Saccharomyces infection.”
Quote in the paperSubstantial claim - Also stated in: § Conclusion · plain
- Findingown data
Deep intravenous lines were not associated with death.
“HIV infections, immunosuppressive drugs, solid organ transplantation, deep intravenous lines, enteral or parenteral nutrition were not associated with death.”
Quote in the paperNot a substantial claim - Findingown data
Lactobacillus accounted for 26 (27.9%) cases.
“followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively.”
- Also stated in: § Probiotic microorganisms involved in infectious complications · plain
“Lactobacillus spp. were the etiologic agents in 26 episodes of infectious complications after probiotic use”
Quote in the paperNot a substantial claim - Also stated in: § Probiotic microorganisms involved in infectious complications · plain
- Findingown data
The prevalence of antibiotic use during the infectious complication was higher in the group that died.
“The mean age was higher in the group that died, as were the prevalence of C. difficile colitis and antibiotic use during the infectious complication.”
Quote in the paperNot a substantial claim - Findingown data
Three of the 5 affected Bacillus patients died.
“Three of the 5 affected patients died.”
Quote in the paperNot a substantial claim - Findingown data
Death occurred in only 1 (3.8%) Lactobacillus case.
“Death occurred in only 1 (3.8%) case.”
Quote in the paperNot a substantial claim - Findingown data
All-cause mortality among Saccharomyces cases was 15% (14 cases).
“All-cause mortality was 15% (14 cases).”
Quote in the paperNot a substantial claim - Findingown data
In 27 cases, the probiotic microorganisms in the medications were compatible with the isolates found in the blood samples of the patient.
“In 27 cases, the probiotic microorganisms in the medications were compatible with the isolates found in the blood samples of the patient.”
Quote in the paperNot a substantial claim- Rests on an assumption: Compatibility between a microorganism isolated from a patient and the probiotic product taken indicates that the probiotic caused the infection.
- Findingown data
The group of patients with infectious complications by Saccharomyces spp. had a higher death rate.
“The group of patients with infectious complications by Saccharomyces spp. had a higher death rate (Table 3).”
Quote in the paperNot a substantial claim - Findingown data
11 (11.8%) had C. difficile colitis.
“At least 40 (43%) of the cases were on antimicrobial therapy at the time of the infectious complications and 11 (11.8%) had C. difficile colitis.”
Quote in the paperNot a substantial claim - Findingown data
Of the 12 patients with infectious complications due to Bifidobacterium spp., 10 were newborns (9 preterm).
“Of the 12 patients with infectious complications due to Bifidobacterium spp., 10 were newborns (9 preterm).”
Quote in the paperNot a substantial claim - Findingown data
The prevalence of C. difficile colitis was higher in the group that died.
“The mean age was higher in the group that died, as were the prevalence of C. difficile colitis and antibiotic use during the infectious complication.”
Quote in the paperNot a substantial claim - Findingown data
There were no deaths in the Bifidobacterium group.
“There were no deaths in this group.”
Quote in the paperNot a substantial claim - Findingown data
In 15 Lactobacillus cases, additional methods showed that the microorganisms isolated from biological samples were compatible with the probiotics taken by the patients.
“In 15 cases, additional methods showed that the microorganisms isolated from biological samples were compatible with the probiotics taken by the patients.”
Quote in the paperNot a substantial claim- Rests on an assumption: Compatibility between a microorganism isolated from a patient and the probiotic product taken indicates that the probiotic caused the infection.
- Findingown data
The mean age was higher in the group that died.
“The mean age was higher in the group that died, as were the prevalence of C. difficile colitis and antibiotic use during the infectious complication.”
Quote in the paperNot a substantial claim - Findingown data
All-cause mortality was 22.8% among the 57 cases where there was compatibility between probiotics and isolated microorganisms.
“All-cause mortality was 19.6% (18 cases) and it was 22.8% among the 57 cases where there was compatibility between probiotics and the isolated microorganisms in the biological samples.”
Quote in the paperNot a substantial claim - Findingown data
When evaluating sepsis only, 39.3% were caused by Saccharomyces.
“When evaluating sepsis only, 39.3% were caused by these fungi.”
Quote in the paperNot a substantial claim - Findingown data
Blood was the most frequent site of isolation of probiotic microorganisms.
“Blood was the most frequent site of isolation of probiotic microorganisms (Table 2).”
Quote in the paperNot a substantial claim - Findingown data
All-cause mortality was 19.6% (18 cases).
“All-cause mortality was 19.6% (18 cases) and it was 22.8% among the 57 cases where there was compatibility between probiotics and the isolated microorganisms in the biological samples.”
Quote in the paperNot a substantial claim - Findingown data
At least 40 (43%) of the cases were on antimicrobial therapy at the time of the infectious complications.
“At least 40 (43%) of the cases were on antimicrobial therapy at the time of the infectious complications and 11 (11.8%) had C. difficile colitis.”
Quote in the paperNot a substantial claim - Interpretationown data
Probiotic use cannot be considered risk-free.
“The use of probiotics cannot be considered risk-free and should be carefully evaluated for some patient groups.”
- Also stated in: § Discussion · plain
“Therefore, to assume that probiotic intake is completely risk-free is not true.”
- Also stated in: § Conclusion · plain
“the use of probiotics cannot be considered risk free and should be carefully evaluated for high- risk groups of patients.”
Quote in the paperSubstantial claim - Also stated in: § Discussion · plain
- Interpretationnone given
The cases described are infections with high mortality rates such as endocarditis and sepsis.
“However, the cases described here are infections with high mortality rates such as endocarditis and sepsis.”
Quote in the paperSubstantial claim - Study design and conductown data
Other factors, such as numbers and types of comorbidity, were not considered in the analysis of the Saccharomyces association with mortality.
“Although the analysis suggests that the genus Saccharomyces is associated with higher overall mortality, we know that other factors were not considered, such as the numbers and types of comorbidity.”
Quote in the paperSubstantial claim
- May combine two claims. 18
- Classified as probably not a substantial claim. 23
May combine two claims.
Findingown dataSaccharomyces was the most frequent genus, accounting for 47 (50.6%) cases.
“The genus Saccharomyces was the most frequent with 47 (50.6%) cases”
- Also stated in: § Probiotic microorganisms involved in infectious complications · plain
“Among the 93 cases, 47 (50.5%) were due to Saccharomyces, making it the most frequent genus in this review.”
Quote in the paperNot a substantial claim- Also stated in: § Probiotic microorganisms involved in infectious complications · plain
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataPediococcus accounted for 2 (2.2%) cases.
“followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataPneumonia, pleural empyema and septic arthritis were each present in only one case.
“Pneumonia, pleural empyema and septic arthritis were present in only one case each.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataFungemia was the most common infectious complication, occurring in 35 (37.6%) cases.
“Fungemia was the most common infectious complications with 35 (37.6%) cases.”
- Also stated in: § Occurrence of infectious complications · plain
“Fungemia was most commonly observed condition, with 35 (37.6%) of the cases.”
Quote in the paperNot a substantial claim- Also stated in: § Occurrence of infectious complications · plain
May combine two claims.
Findingown dataOf the 67 articles included, 7 (10.4%) were classified as good and the remaining as fair; none were classified as poor.
“Of the 67 articles included in the synthesis, 7 (10.4%) were classified as “good” and the remaining as “fair”. None were classified as “poor”.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataEscherichia accounted for 1 (1.1%) case.
“followed by Lactobacillus, Bifidobacterium, Bacillus, Pedioccocus and Escherichia with 26 (27.9%), 12 (12.8%), 5 (5.4%), 2 (2.2%) and 1 (1.1%) case, respectively.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe systematic review identified 60 case reports and 7 case series, totaling 93 patients.
“We found 60 case reports and 7 case series, making up a total of 93 patients.”
- Also stated in: § Database search · plain
“We included 60 case reports and 7 case series, corresponding to 93 patients (Additional file 1).”
Quote in the paperSubstantial claim- Also stated in: § Database search · plain
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataCentral venous access was present in 59 (63.5%) cases.
“Central venous access, enteral nutrition and parenteral nutrition were present in 59 (63.5%), 52 (56%) and 14 (15%), respectively, of all cases.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataPatients on immunosuppressive drugs accounted for 14 (15%) patients.
“Patients on immunosuppressive drugs (corticosteroids, chemotherapy and immunobiologicals) accounted for 14 (15%) patients.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe genus Saccharomyces was positively associated with mortality; 3/4 of patients who died had probiotics belonging to this genus as the etiological agent.
“The genus Saccharomyces was also positively associated with mortality, since 3/4 of patients who died had probiotics belonging to this genus as the etiological agent of the infectious complications found.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown dataTwo patients had received solid organ transplantation and 5 (5.4%) had been previously diagnosed as HIV infected.
“Two patients had received solid organ transplantation and 5 (5.4%) had been previously diagnosed as HIV infected.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataBacteremia accounted for 20.4% of infectious complications and Lactobacillus was responsible for 42% of these.
“Bacteremia accounted 20.4% of the infectious complications and the genus Lactobacillus was responsible for 42% of these.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataIn 10 patients the indication for probiotic use was to prevent necrotizing enterocolitis and at least 4 of them developed this complication despite probiotic prophylaxis.
“In 10 patients the indication for the use of probiotic was to prevent necrotizing enterocolitis (NE) and at least 4 of them ended up developing this complication, despite probiotic prophylaxis.”
Quote in the paperSubstantial claimMay combine two claims.
Findingnone givenTen preterm infants had extremely low birth weight and half had sepsis, four patients had bacteremia and only one had fungemia.
“Ten preterm infants had extremely low birth weight and half had sepsis, four patients had bacteremia and only one had fungemia.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataBetween 2011 and 2017, there were 39 cases.
“Between 2011 and 2017, there were 39 cases.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataParenteral nutrition was present in 14 (15%) cases.
“Central venous access, enteral nutrition and parenteral nutrition were present in 59 (63.5%), 52 (56%) and 14 (15%), respectively, of all cases.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe earliest case dated back to 1976, and there was a progressive increase in cases in the 1980s, 1990s and 2000s, with 4, 16 and 33 cases, respectively.
“The earliest case dated back to 1976, and we observed a progressive increase in the following decades of 80, 90 and 00, with 4,16 and 33 cases, respectively.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataEnteral nutrition was present in 52 (56%) cases.
“Central venous access, enteral nutrition and parenteral nutrition were present in 59 (63.5%), 52 (56%) and 14 (15%), respectively, of all cases.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataIn our review, 12 samples of Saccharomyces spp. had antimicrobial susceptibility testing and 10 of them were sensitive to azoles.
“In our review, 12 samples of Saccharomyces spp. had antimicrobial susceptibility testing and 10 of them were sensitive to azoles.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataEach of the five continents had at least one case.
“Each of the five continents had at least one case.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataMales had a slightly higher prevalence, corresponding to 53 (57%) of the cases.
“Males had a slightly higher prevalence, corresponding to 53 (57%) of the cases.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown dataMost cases were from Europe (61; 65.6%) and 17 (18.3%) from the United States and Canada.
“Of the 60 reports and 7 series of cases involving 93 patients, most were from Europe (61; 65.6%) and 17 (18.3%) from the United States and Canada.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataElderly (adults over 60 years) were reported in 33 (35.5%) cases.
“Elderly (defined as adults over 60 years of age) and children younger than 1 year were reported in 33 (35.5%) and 25 (26.7%) cases, respectively.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataOf the 8 patients with Lactobacillus bacteremia, 4 were immunosuppressed (2 with HIV infection), 3 underwent intestinal invasive procedures, and 1 had diverticular disease of the colon.
“We observed that of the 8 patients with Lactobacillus bacteremia, 4 were immunosuppressed - 2 with HIV infection; 3 underwent intestinal invasive procedures and 1 had diverticular disease of the colon.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataOf patients younger than 1 year, 17 (68%) were premature.
“Of patients younger than 1 year, 17 (68%) were premature (Additional file 1: Table S8).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataIn our review, 26.7% of patients were younger than 1 year and practically two-thirds of them premature.
“In our review, 26.7% of the patients were younger than 1 year of age and practically two-thirds of them premature.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataChildren younger than 1 year were reported in 25 (26.7%) cases.
“Elderly (defined as adults over 60 years of age) and children younger than 1 year were reported in 33 (35.5%) and 25 (26.7%) cases, respectively.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataNeoplasia was described in 10 (10.7%) cases, of which 4 (40%) were hematologic malignancies.
“Neoplasia was described in 10 (10.7%) and of these, 4 (40%) were of hematologic malignancies.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductcitationThe systematic review was based on PRISMA.
“The description of this systematic review was based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyzes – PRISMA [9].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [9] Liberati A, Altman DG, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):1–34. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductcitationA modified National Institutes of Health Tool was used to evaluate risk of bias in the retrieved articles.
“A modified National Institutes of Health Tool [14] was to use to evaluate the risk of bias in the retrieved articles (see Additional file 1).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [14] NIH. Quality assessment tool for case series studies. In: National Heart, Lung, and Blood Institute; 2014. https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools . Acessed 28 June 2016.
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenPotentially relevant titles and abstracts were selected and articles evaluated independently by two reviewers, with divergences resolved by consensus and a third reviewer if necessary.
“Potentially relevant titles and abstracts were selected and their articles evaluated independently by Rafael Lessa da Costa and Jose Moreira. The divergences were resolved by consensus and, whenever necessary, by a third reviewer (Cristiane Lamas or Andrea De Lorenzo).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenData extraction divergences were resolved by consensus and, when necessary, by a third reviewer.
“At this stage, the divergences were resolved by consensus and, when necessary, by the third reviewer.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe study was registered at PROSPERO (CRD42016042289).
“The study was registered at PROSPERO (CRD42016042289).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S2 (checkable).
InterpretationreasoningDue to the limitation for publication of case reports, several other serious cases may not have reached public knowledge.
“on the other, due to the mentioned limitation for the publication of case reports, several other serious cases may not have reached public knowledge.”
Quote in the paperNot a substantial claim- Rests on an assumption: Case reports are increasingly difficult to publish.
Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone givenThe proportion of cases of infectious complications is small when the total number of people who use probiotics is considered.
“The proportion of cases of infectious complications is small when the total number of people who use probiotics is considered.”
Quote in the paperNot a substantial claim- Rests on an assumption: The total number of people who use probiotics is large enough that the proportion of infectious complications is small.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThere is a possibility of publication bias, with more serious cases having been published.
“So, although on one hand there is the possibility of publication bias, with more serious cases having been published”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone givenProbiotics were often used in the context of excessive antibiotic use.
“Probiotics were often used in the context of excessive antibiotic use, and a more judicious use of antibiotics is critical”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Compatibility between a microorganism isolated from a patient and the probiotic product taken indicates that the probiotic caused the infection.
“In 27 cases, the probiotic microorganisms in the medications were compatible with the isolates found in the blood samples of the patient.”
“In 15 cases, additional methods showed that the microorganisms isolated from biological samples were compatible with the probiotics taken by the patients.”
The paper relies on this without support.
Case reports are increasingly difficult to publish.
“We believe that these cases represent only a small proportion of existing cases, since case reports are increasingly difficult to publish.”
The paper relies on this without support.
The total number of people who use probiotics is large enough that the proportion of infectious complications is small.
“The proportion of cases of infectious complications is small when the total number of people who use probiotics is considered.”
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?
One report described 93 cases of serious infections with a 15% mortality rate, including fungemia (37.6%), sepsis (31.2%), bacteremia (20.4%), endocarditis, and abscesses.
“For example, one report on observational results described 93 cases of serious infections (with a 15% mortality rate), with fungemia (37.6% of cases), sepsis (31.2%), bacteremia (20.4%), endocarditis, and abscesses [74,75].”
From Current Concepts in Probiotic Safety and Efficacy (2026) · cites this paper as [74]
The Results (Occurrence of infectious complications) report 93 cases and the stated percentages for fungemia, sepsis, and bacteremia, as well as endocarditis and abscesses. But the Results (Gender and age distribution, and associated conditions) give overall all-cause mortality as 19.6% (18 cases). The 15% figure appears in the Saccharomyces subgroup, not for all 93 cases. (LLM, conf=0.92)
Experimental — accuracy not yet measuredAge over 60 years, infections such as Clostridioides difficile, antibiotic exposure, immunosuppression, and use of Saccharomyces or Lactobacillus (especially L. rhamnosus) appear to increase the risk of probiotic-related adverse effects.
“Age over 60 years, infections such as Clostridioides difficile, antibiotic exposure, immunosuppression, and the use of Saccharomyces or Lactobacillus (especially L. rhamnosus) all appear to increase the risk [74].”
From Current Concepts in Probiotic Safety and Efficacy (2026) · cites this paper as [74]
The Conclusion and Results (pages not specified) associate age over 60, C. difficile colitis, antibiotic use, and Saccharomyces infection with mortality among patients who already had probiotic-related infectious complications—not with an increased risk of developing adverse effects. The Discussion describes immunosuppression as a risk factor for lactobacillemia, and the Results identify L. rhamnosus in 14 cases, but neither establishes increased adverse-effect risk from using Lactobacillus, especially L. rhamnosus. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSome findings on probiotic safety are isolated and based on single clinical cases, such as sepsis development in patients with established intravenous catheters.
“Some findings are isolated, based on single clinical cases, such as sepsis development in patients with established intravenous catheters [74].”
From Current Concepts in Probiotic Safety and Efficacy (2026) · cites this paper as [74]
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.
Saccharomyces mortality percentage does not match its case count
MajorThis section identifies 47 Saccharomyces cases. Fourteen deaths among those cases represent 29.8%, not the reported 15%.
Reported 15 · recomputed 29.787234
“All-cause mortality was 15% (14 cases).”
Solid-organ transplant patient counts conflict
MinorThe narrative says two patients had received transplants, whereas Table 3 assigns two to the no-death group and one to the death group.
“Two patients had received solid organ transplantation”
“| Solid organ transplant | 2 (2.7) | 1 (5.5) | 0.55 | – |”
Immunosuppressive-drug patient counts conflict
MinorThe narrative gives 14 patients, but Table 3 lists 15 without death and five with death, totaling 20.
“Patients on immunosuppressive drugs (corticosteroids, chemotherapy and immunobiologicals) accounted for 14 (15%) patients.”
“| Immunosuppressive drugs | 15 (20.2) | 5 (27.8) | 0.89 | – |”
Cites
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000100 · Cited by 28,164 · see citing works
Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X., & Zhang, T. (2017) · Neonatology · doi:10.1159/000454668 · Cited by 24,577 · see citing works
Bone, R. C., BALK, R. A., Cerra, F. B., Dellinger, R. P., Fein, A. M., Knaus, W. A., Schein, R. M. H., & Sibbald, W. J. (1992) · CHEST Journal · doi:10.1378/chest.101.6.1644 · Cited by 13,192 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2009.06.006 · Cited by 10,578 · see citing works
American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference
(1992) · Critical Care Medicine · doi:10.1097/00003246-199206000-00025 · Cited by 5,091 · see citing works
Severe Sepsis and Septic Shock
Angus, D. C., & van der Poll, T. (2013) · New England Journal of Medicine · doi:10.1056/nejmra1208623 · Cited by 3,993 · see citing works
Durack, D. T., Lukes, A. S., Bright, D. K., & Service, D. E. (1994) · The American Journal of Medicine · doi:10.1016/0002-9343(94)90143-0 · Cited by 2,572 · see citing works
Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial
Kalliomäki, M. A., Salminen, S., Arvilommi, H. S., Kero, P. O., Koskinen, P. J., & Isolauri, E. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04259-8 · Cited by 2,434 · see citing works
Principles and Practice of Infectious Diseases.
(1985) · Annals of Internal Medicine · doi:10.7326/0003-4819-103-1-169_2 · Cited by 1,576 · see citing works
Probiotic use in clinical practice: what are the risks?
Boyle, R. J., Robins-Browne, R. M., & Tang, M. L. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.6.1256 · Cited by 776 · see citing works
Arendrup, M. C., Boekhout, T., Akova, M., Meis, J. F. G. M., Cornely, O. A., & Lortholary, O. (2013) · Clinical Microbiology and Infection · doi:10.1111/1469-0691.12360 · Cited by 533 · see citing works
A randomized synbiotic trial to prevent sepsis among infants in rural India
Panigrahi, P., Parida, S., Nanda, N. C., Satpathy, R., Pradhan, L., Chandel, D. S., Baccaglini, L., Mohapatra, A., Mohapatra, S. S., Misra, P. R., et al. (2017) · Nature · doi:10.1038/nature23480 · Cited by 526 · see citing works
Saccharomyces cerevisiae Fungemia: An Emerging Infectious Disease
Munoz, P., Bouza, E., Cuenca-Estrella, M., Eiros, J. M., Perez, M. J., Sanchez-Somolinos, M., Rincon, C., Hortal, J., & Pelaez, T. (2005) · Clinical Infectious Diseases · doi:10.1086/429916 · Cited by 462 · see citing works
Salminen, M. K., Tynkkynen, S., Rautelin, H., Saxelin, M., Vaara, M., Ruutu, P., Sarna, S., Valtonen, V., & Järvinen, A. (2002) · Clinical Infectious Diseases · doi:10.1086/342912 · Cited by 419 · see citing works
Probiotics for treating infectious diarrhoea
Allen, S. J., Okoko, B. J., Martinez, E. G., Gregorio, G. V., & Dans, L. F. (2003) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003048.pub2 · Cited by 400 · see citing works
GUYONNET, D., CHASSANY, O., DUCROTTE, P., PICARD, C., MOURET, M., MERCIER, C. ‐., & MATUCHANSKY, C. (2007) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2007.03362.x · Cited by 365 · see citing works
Necrotising enterocolitis hospitalisations among neonates in the United States
Holman, R. C., Stoll, B. J., Curns, A. T., Christensen, K. L. Y., Steiner, C., & Schonberger, L. B. (2006) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2006.00756.x · Cited by 345 · see citing works
Probiotic and synbiotic therapy in critical illness: a systematic review and meta-analysis
Manzanares, W., Lemieux, M., Langlois, P. L., & Wischmeyer, P. E. (2016) · Critical Care · doi:10.1186/s13054-016-1434-y · Cited by 295 · see citing works
Safety of probiotics used to reduce risk and prevent or treat disease.
(2011) · PubMed Central · Cited by 242 · see citing works
Wolf, B. W., WHEELER, K. B., Ataya, D. G., & Garleb, K. A. (1998) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(98)00090-8 · Cited by 173 · see citing works
In defense of Pierre Louis who pioneered the epidemiological approach to good medicine
Morabia, A. (2008) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2008.07.007 · Cited by 149 · see citing works
Prevention of necrotizing enterocolitis with probiotics: a systematic review and meta-analysis
Sawh, S. C., Deshpande, S., Jansen, S., Reynaert, C. J., & Jones, P. M. (2016) · PeerJ · doi:10.7717/peerj.2429 · Cited by 133 · see citing works
Zhang, Q., Wu, Y., & Fei, X. (2016) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2016.1181156 · Cited by 122 · see citing works
Salminen, M. K., Tynkkynen, S., Rautelin, H., Poussa, T., Saxelin, M., Ristola, M., Valtonen, V., & Järvinen, A. (2004) · HIV Clinical Trials · doi:10.1310/6f83-n39q-9ppp-lmvv · Cited by 103 · see citing works
LeDoux, D., LaBombardi, V. J., & Karter, D. L. (2006) · International Journal of STD & AIDS · doi:10.1258/095646206776253507 · Cited by 81 · see citing works
Antony, S. J. (2000) · PubMed Central · Cited by 59 · see citing works
Sepsis, Severe Sepsis, and Septic Shock
Munford, R. S., & Suffredini, A. F. (2010) · Elsevier eBooks · doi:10.1016/b978-0-443-06839-3.00070-9 · Cited by 55 · see citing works
Bifidobacterium breveSepsis in Child with High-Risk Acute Lymphoblastic Leukemia
Avčin, S. L., Pokorn, M., Kitanovski, L., Premru, M. M., & Jazbec, J. (2015) · Emerging infectious diseases · doi:10.3201/eid2109.150097 · Cited by 36 · see citing works
National Heart, Lung, and Blood Institute
Hall, M. H. (2012) · Springer eBooks · doi:10.1007/978-1-4419-1005-9_817 · Cited by 13 · see citing works
van der Horst, H. E. (2004) · Huisarts en Wetenschap · doi:10.1007/bf03083732 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- FAO/WHO. Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report, 2001.
Cited by
Sorted by citations
(BIOHAZ), E. P. O. B. H., Koutsoumanis, K., Allende, A., Álvarez‐Ordóñez, A., Bolton, D., Bover‐Cid, S., Chemaly, M., Davies, R., Cesare, A. D., Hilbert, F., et al. (2021) · EFSA Journal · doi:10.2903/j.efsa.2021.6377 · Cited by 443 · see citing works
Paraprobiotics: A New Perspective for Functional Foods and Nutraceuticals
Siciliano, R. A., Reale, A., Mazzeo, M. F., Morandi, S., Silvetti, T., & Brasca, M. (2021) · Nutrients · doi:10.3390/nu13041225 · Cited by 244 · see citing works
Probiotics and Preterm Infants
van den Akker, C. H. P., van Goudoever, J. B., Shamir, R., Domellöf, M., Embleton, N. D., Hojsak, I., Lapillonne, A., Mihatsch, W., Canani, R. B., Bronský, J., et al. (2020) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002655 · Cited by 239 · see citing works
Reappraisal of probiotics’ safety in human
Sotoudegan, F., Daniali, M., Hassani, S., Nikfar, S., & Abdollahi, M. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.04.032 · Cited by 154 · see citing works
Members of the Lactobacillus Genus Complex (LGC) as Opportunistic Pathogens: A Review
Rossi, F., Amadoro, C., & Colavita, G. (2019) · Microorganisms · doi:10.3390/microorganisms7050126 · Cited by 97 · see citing works
Use of Probiotics for the Management of Acute Gastroenteritis in Children: An Update
Szajewska, H., Guarino, A., Hojsak, I., Indrio, F., Kolacek, S., Orel, R., Salvatore, S., Shamir, R., van Goudoever, J. B., Vandenplas, Y., et al. (2020) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002751 · Cited by 90 · see citing works
The opportunistic nature of gut commensal microbiota
Dey, P., & Chaudhuri, S. R. (2022) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2022.2133987 · Cited by 82 · see citing works
Bacteriocins: potentials and prospects in health and agrifood systems
Reuben, R. C., & Torres, C. (2024) · Archives of Microbiology · doi:10.1007/s00203-024-03948-y · Cited by 88 · see citing works
Probiotics, Photobiomodulation, and Disease Management: Controversies and Challenges
Ailioaie, L. M., & Litscher, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094942 · Cited by 68 · see citing works
Liu, Y., Yu, X., Yu, L.-L., Tian, F., Zhao, J.-X., Zhang, H., Qian, L., Wang, Q., Xue, Z.-K., Zhai, Q., et al. (2020) · Engineering · doi:10.1016/j.eng.2020.06.026 · Cited by 55 · see citing works
Invasive Infections Associated with the Use of Probiotics in Children: A Systematic Review
D’Agostin, M., Squillaci, D., Lazzerini, M., Barbi, E., Wijers, L., & Lozzo, P. D. (2021) · Children · doi:10.3390/children8100924 · Cited by 56 · see citing works
Batista, K. S., de Albuquerque, J. G., de Vasconcelos, M. H. A., Bezerra, M. L. R., Barbalho, M. B. D. S., Pinheiro, R. O., & Aquino, J. D. S. (2021) · Nutrition Research Reviews · doi:10.1017/s0954422421000317 · Cited by 54 · see citing works
Charoensappakit, A., Sae‐khow, K., & Leelahavanichkul, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158223 · Cited by 50 · see citing works
Lista, S., Munafò, A., Caraci, F., Imbimbo, C., Emanuele, E., Minoretti, P., Pinto-Fraga, J., Merino-País, M., Crespo‐Escobar, P., López‐Ortiz, S., et al. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102659 · Cited by 48 · see citing works
Probiotics and their applications in functional foods: a health perspective
Amin, M. R., Biswas, A. P., Tasnim, M., Islam, M. N., & Azam, M. S. (2025) · Applied Food Research · doi:10.1016/j.afres.2025.101193 · Cited by 46 · see citing works
Lee, Z., Lew, C. C. H., Ortiz‐Reyes, L., Patel, J. J., Wong, Y. J., Loh, C. T. I., Martindale, R. G., & Heyland, D. K. (2023) · Clinical Nutrition · doi:10.1016/j.clnu.2023.01.019 · Cited by 42 · see citing works
Clostridium butyricum Bacteremia Associated with Probiotic Use, Japan
Sada, R. M., Matsuo, H., Motooka, D., Kutsuna, S., Hamaguchi, S., Yamamoto, G., & Ueda, A. (2024) · Emerging infectious diseases · doi:10.3201/eid3004.231633 · Cited by 37 · see citing works
IUPHAR review: Microbiota-gut-brain axis and its role in neuropsychiatric disorders
Lee, S.-H., Han, C., & Shin, C. (2025) · Pharmacological Research · doi:10.1016/j.phrs.2025.107749 · Cited by 36 · see citing works
Beyond probiotics: a narrative review on an era of revolution
Sharma, N., Kang, D., Paik, H., & Park, Y. (2022) · Food Science and Biotechnology · doi:10.1007/s10068-022-01212-x · Cited by 30 · see citing works
Quality of probiotic products for preterm infants: Contamination and missing strains
Vermeulen, M. J., Luijendijk, A., van Toledo, L., van Kaam, A. H., & Reiss, I. K. M. (2019) · Acta Paediatrica · doi:10.1111/apa.14976 · Cited by 29 · see citing works
Health-Promoting Effects and Safety Aspects of Lactobacillus delbrueckii: A Food Industry Species
de Jesus, L. C. L., Santos, R. C. V., Quaresma, L. S., Américo, M. F., Rodrigues, T. V., Freitas, A. D. S., Campos, G. M., Dutra, J. D. C. F., Barroso, F. A. L., Laguna, J. G., et al. (2024) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2024.104605 · Cited by 28 · see citing works
Alruwaili, R. F., Alsadaan, N., Alruwaili, A. N., & Alrumayh, A. G. R. (2023) · Sustainability · doi:10.3390/su152215728 · Cited by 24 · see citing works
Current Concepts in Probiotic Safety and Efficacy
Churin, A. A., Sokolyanskaya, L. O., Lukina, A. P., & Karnachuk, O. V. (2026) · Nutrients · doi:10.3390/nu18040696 · Cited by 31 · see citing works
Probiotics in the Management of Mental and Gastrointestinal Post-COVID Symptomes
Łoniewski, I., Skonieczna‐Żydecka, K., Sołek-Pastuszka, J., & Marlicz, W. M. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11175155 · Cited by 22 · see citing works
Imre, A., Rácz, H. V., Antunovics, Z., Rádai, Z., Kovács, R., Lopandić, K., Pócsi, I., & Pfliegler, W. P. (2019) · Microbiological Research · doi:10.1016/j.micres.2019.126298 · Cited by 21 · see citing works
Lo, C. K. L., & Sheth, P. M. (2021) · BMC Infectious Diseases · doi:10.1186/s12879-021-06095-7 · Cited by 19 · see citing works
Safety of probiotics in humans: A dark side revealed?
Pace, F., Macchini, F., & Castagna, V. M. (2020) · Digestive and Liver Disease · doi:10.1016/j.dld.2020.04.029 · Cited by 17 · see citing works
Infectious complications of probiotic use: A matched case-control study
Tom, F. S., Tucker, K. J., McCracken, C. M., McGregor, J. C., & Gore, S. J. (2022) · Infection Control & Hospital Epidemiology · doi:10.1017/ice.2021.261 · Cited by 14 · see citing works
CRISPR-engineered microbiome: living therapeutics revolutionize blood cancer immunotherapy
Cheng, F., Samarkhazan, H. S., & Khazaei, Y. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00882-9 · Cited by 14 · see citing works
Bacterial Meningitis Caused by Bacillus subtilis var. natto
Tokano, M., Tarumoto, N., Imai, K., Sakai, J., Maeda, T., Kawamura, T., Seo, K., Takahashi, K., Yamamoto, T., & Maesaki, S. (2022) · Internal Medicine · doi:10.2169/internalmedicine.0768-22 · Cited by 14 · see citing works
Maleki-Hajiagha, A., Karimi, R., abbasi, S., Emami, N., & Amidi, F. (2025) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-025-07338-0 · Cited by 13 · see citing works
Wang, Y., Zhang, Z., Chen, Q., & Chen, T. (2024) · npj Biofilms and Microbiomes · doi:10.1038/s41522-024-00521-9 · Cited by 16 · see citing works
Probiotic-related bacteremia after major hepatectomy for biliary cancer: a report of two cases
Shimura, M., Mizuma, M., Nakagawa, K., Aoki, S., Miura, T., Takadate, T., Ariake, K., Maeda, S., Kawaguchi, K., Masuda, K., et al. (2021) · Surgical Case Reports · doi:10.1186/s40792-021-01216-5 · Cited by 12 · see citing works
Influence of biotic interventions on the immune response to vaccines in young and older adults
Spacova, I., Patusco, R., Lebeer, S., & Jensen, M. G. (2023) · Clinical Nutrition · doi:10.1016/j.clnu.2023.01.001 · Cited by 12 · see citing works
Rare Yeasts in Latin America: Uncommon Yet Meaningful
Gil, Ó., Hernández-Pabón, J. C., Tabares, B., Lugo-Sánchez, C., & Firacative, C. (2023) · Journal of Fungi · doi:10.3390/jof9070747 · Cited by 11 · see citing works
Imre, A., Kovács, R., Pázmándi, K., Nemes, D., Jakab, Á., Fekete, T., Rácz, H. V., Dóczi, I., Bácskay, I., Gácser, A., et al. (2021) · Journal of Fungi · doi:10.3390/jof7090746 · Cited by 11 · see citing works
Matin, M., Rad, A. H., Gharehbaghi, M. M., Mirghafourvand, M., & Mohammad‐Alizadeh‐Charandabi, S. (2022) · European Journal of Nutrition · doi:10.1007/s00394-022-02905-z · Cited by 11 · see citing works
Autoprobiotics in the Treatment of Patients with Colorectal Cancer in the Early Postoperative Period
Ермоленко, Е. И., Baryshnikova, N. V., Alekhina, G., Zakharenko, A., Тен, О. А., Кащенко, В. А., Lavrenova, N. S., Gushchina, O. O., Сергеевич, О. Т., MOROZOVA, A. D., et al. (2024) · Microorganisms · doi:10.3390/microorganisms12050980 · Cited by 10 · see citing works
Immunosuppressant Drugs and Their Effects on Children Undergoing Solid Organ Transplant
Spinner, J. A., & Denfield, S. W. (2022) · Pediatrics in Review · doi:10.1542/pir.2020-000620 · Cited by 9 · see citing works
Pinto, G., de Lima, L. L. P., Pedra, T., Assumpção, A. M., Morgado, S. M., & Mascarenhas, L. A. (2021) · Access Microbiology · doi:10.1099/acmi.0.000250 · Cited by 9 · see citing works
Haziri, D., Prechter, F., & Stallmach, A. (2020) · Zeitschrift für Gastroenterologie · doi:10.1055/a-1168-7577 · Cited by 9 · see citing works
Dairy Propionibacteria: Probiotic Properties and Their Molecular Bases
Rossi, F., Santonicola, S., Giaccone, V., Truant, A., & Colavita, G. (2025) · Biomolecules · doi:10.3390/biom15060886 · Cited by 8 · see citing works
Successful treatment of canine infective endocarditis caused by Bacillus amyloliquefaciens
Bae, H., Hwang, T. S., Lee, H., Jung, D., Kim, S., & Yu, D. (2022) · Veterinary Quarterly · doi:10.1080/01652176.2022.2033879 · Cited by 8 · see citing works
Siddiqui, A., Haider, R., Aaqil, S. I., Vohra, L. I., Qamar, K., Jawed, A., Fatima, N., Adnan, A., Parikh, V., Ochani, S., et al. (2024) · Annals of Medicine and Surgery · doi:10.1097/ms9.0000000000002007 · Cited by 9 · see citing works
Role of Probiotics in the Treatment and Prevention of Common Gastrointestinal Conditions in Children
Hojsak, I., & Kolaček, S. (2024) · Pediatric Gastroenterology Hepatology & Nutrition · doi:10.5223/pghn.2024.27.1.1 · Cited by 11 · see citing works
Wang, A. Y. L., Aviña, A. E., Liu, Y., & Kao, H. (2025) · Burns & Trauma · doi:10.1093/burnst/tkaf068 · Cited by 8 · see citing works
Actualización sobre infección por Clostridium difficile en el paciente mayor
Boixareu, C. B., Tutor‐Ureta, P., & Ramos, A. (2020) · Revista Española de Geriatría y Gerontología · doi:10.1016/j.regg.2019.12.003 · Cited by 8 · see citing works
Du, M., Xie, X., Yang, S., Li, Y., Jiang, T., Yang, J., Li, L., Huang, Y., Wu, Q., Chen, W., et al. (2021) · Molecules · doi:10.3390/molecules26216480 · Cited by 7 · see citing works
Ranjbar, M., Naeini, F., Rostamian, A., Djafarian, K., & Mohammadi, H. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e36230 · Cited by 6 · see citing works
Lang, J. M., Shostak, E. S., Quinn, W. K., Chervinskaya, V. D., Fioraso, E., Smith, E., Kotarsky, C. J., DeBlauw, J. A., Lloyd, J. L., & Ives, S. J. (2025) · The Journal of Clinical Hypertension · doi:10.1111/jch.14972 · Cited by 5 · see citing works
Probiotics, postbiotics and paraprobiotics
Корниенко, Е. А. (2022) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-205-9-240-250 · Cited by 5 · see citing works
Atak, E. S., Yıldız, D., Kocatürk, R. R., Temizyürek, A., Özcan, Ö. Ö., Erguzel, T. T., Karahan, M., & Tarhan, N. (2021) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.2022.3665.1 · Cited by 5 · see citing works
Castro-López, C., Pascacio‐Villafán, C., Aluja, M., Garcia, H. S., González-Córdova, A. F., Vallejo‐Córdoba, B., & Hernández‐Mendoza, A. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-10034-6 · Cited by 5 · see citing works
Bénéfices et risques des compléments alimentaires
Crenn, P. P. (2020) · Nutrition Clinique et Métabolisme · doi:10.1016/j.nupar.2020.04.006 · Cited by 5 · see citing works
Shostak, E. S., Lang, J. M., Quinn, W. K., Chervinskaya, V. D., Fioraso, E., Smith, E., Kotarsky, C. J., DeBlauw, J. A., Lloyd, J. L., & Ives, S. J. (2025) · Physiological Reports · doi:10.14814/phy2.70285 · Cited by 2 · see citing works
An Unusual Case of Acute Cholecystitis Caused by Lactobacillus paracasei
Kim, H. U., Choo, B., Pyakuryal, A., & Shah, M. (2023) · Cureus · doi:10.7759/cureus.40334 · Cited by 4 · see citing works
Dey, U., Madabhushi, L. P., Chacko, A. A., Gopalakrishnan, A. V., Santhanam, R. K., & Gajendran, B. (2026) · Cellular Signalling · doi:10.1016/j.cellsig.2026.112726 · Cited by 3 · see citing works
DO PROBIOTICS HAVE A FUTURE IN NEONATOLOGY?
Знаменська, Т. К., & Vorobiova, O. V. (2021) · Neonatology surgery and perinatal medicine · doi:10.24061/2413-4260.xi.3.41.2021.7 · Cited by 3 · see citing works
Clostridioides difficile in transplant patients: early diagnosis, treatment, and prevention
Revolinski, S., & Munoz-Price, L. S. (2019) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0000000000000560 · Cited by 3 · see citing works
(FEEDAP), E. P. O. A. A. P. O. S. U. I. A. F., Bampidis, V., Azimonti, G., Bastos, M. D. L., Christensen, H. K., Dusemund, B., Durjava, M. F., Kouba, M., López‐Alonso, M., Puente, S. L., et al. (2020) · EFSA Journal · doi:10.2903/j.efsa.2020.6167 · Cited by 2 · see citing works
When to use probiotics in luminal gastrointestinal disorders?
Elangovan, A., & Fischer, M. (2020) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000674 · Cited by 3 · see citing works
Complementary and alternative medicine
Bellanger, R. A., & Seeger, C. (2020) · Side effects of drugs annual · doi:10.1016/bs.seda.2020.08.004 · Cited by 3 · see citing works
Probiotic Yeasts and Bacteria: A Complementary Approach to Gut Health
Cicero, A. F. G., Bartoli, C., Lluís-Ganella, C., & Fabrizzi, P. (2026) · Microorganisms · doi:10.3390/microorganisms14081763 · Cited by 2 · see citing works
Mohajeri, M., & Abedi, N. (2024) · Nutrition & Food Science · doi:10.1108/nfs-12-2023-0293 · Cited by 2 · see citing works
Ермоленко, Е. И., Baryshnikova, N. V., Kovalis, S. A., Novilova, N. S., Orlova, V. V., Ilyina, A. S., Кащенко, В. А., Leontieva, G., & Suvorov, A. N. (2025) · World Journal of Clinical Cases · doi:10.12998/wjcc.v13.i27.107704 · Cited by 1 · see citing works
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Jangra, N., Chahar, N., Parmar, A., & Gulati, P. (2025) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-025-10690-4 · Cited by 1 · see citing works
Balaji, Y., & Ravi, S. N. (2025) · Food and Humanity · doi:10.1016/j.foohum.2025.100960 · Cited by 1 · see citing works
Liu, H., Yang, L., Huang, S., He, Y., Xie, Y., Jing, Y., Hu, B., Li, Z., Li, Z., & Li, Z. (2026) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-026-10952-9 · Cited by 1 · see citing works
Gut microbiome in sepsis: from dysbiotic biomarker to precision and palliative decision-making
Wang, L.-M., Chen, C., Danzheng, J., & Zhao, J. (2026) · Frontiers in Medicine · doi:10.3389/fmed.2026.1811304 · Cited by 1 · see citing works
Mahooti, M., Ahmad, S., Ahmadbeigi, G., Abdolalipour, E., Safaei, F., Mahooti, K., Eslami, M., Yaghmayee, S., Sanami, S., & Pajand, O. (2026) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-026-11075-x · Cited by 1 · see citing works
The role of probiotics in restoring and maintaining vaginal microbiome health: a review
Sahu, B. K., Panda, S. K., Mallick, U., Panda, S. H., & Sahu, M. C. (2026) · Infection and Immunity · doi:10.1128/iai.00011-26 · Cited by 2 · see citing works
Safety and Effectiveness of Probiotic Preparations: A Contemporary Review
Shorabaev, E., Sadanov, A. K., Baimakhanova, B. B., Ратникова, И. А., Xetayeva, G., Akhelova, S., & Turgumbayeva, A. (2026) · Diseases · doi:10.3390/diseases14090316 · Cited by 1 · see citing works
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Lamas, C. D. C. (2019) · Heart Vessels and Transplantation · doi:10.24969/hvt.2019.137 · Cited by 1 · see citing works
Self-citationDesai, S. P., Kurian, C., Das, S., Rebello, S. J., Acharyya, S., & Paari, K. A. (2023) · Journal of Health Science and Medical Research · doi:10.31584/jhsmr.20231015 · Cited by 1 · see citing works
Estrategias de prevención de infecciones tardías en unidades de cuidados intensivos neonatales
Milos, A. A. T., & Baquedano, M. S. U. (2019) · ARS MEDICA Revista de Ciencias Médicas · doi:10.11565/arsmed.v44i3.1586
Raina, S. (2020) · Journal of Global Infectious Diseases · doi:10.4103/jgid.jgid_12_20
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Özmen, H., & Aydınlı, B. (2020) · Mersin Üniversitesi Tıp Fakültesi Lokman Hekim Tıp Tarihi ve Folklorik Tıp Dergisi · doi:10.31020/mutftd.730594
Roeske, K., Kuryłek, A., Cieślik, J., Wróblewska, M., & Jagielski, T. (2020) · Postępy Mikrobiologii - Advancements of Microbiology · doi:10.21307/pm-2020.59.3.21
Чепур, С. В., Nn, P., Chubar, O. V., Cygan, V. N., Сергеевна, Б. Л., Sidorov, S. P., Bazhenov, M. V., Mosin, A. V., Vinogradov, M. V., & Семакин, Р. В. (2020) · Reviews on Clinical Pharmacology and Drug Therapy · doi:10.17816/rcf183197-212
Prophylaxis of post-antibiotherapy complications. New insights
Blejan, I. E., Arsene, A. L., & Drăgănescu, D. (2020) · Farmacist ro · doi:10.26416/farm.196.5.2020.3929
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Arassi, M. B., Karcher, N., Zeller, G., Zimmermann, M., & Tönshoff, B. (2021) · Der Nephrologe · doi:10.1007/s11560-021-00492-4
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do Nascimento, W. M., Machiavelli, A., Ferreira, F. A., Sincero, T. C. M., Zárate-Bladés, C. R., & Pinto, A. R. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819265-8.00054-1
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Dobryanskyy, D. O., & Dobryk, D. S. (2021) · Neonatology surgery and perinatal medicine · doi:10.24061/2413-4260.xi.1.39.2021.6
Doffou, É., Kamenan, B. A. T., & Abrogoua, D. P. (2021) · Annales Pharmaceutiques Françaises · doi:10.1016/j.pharma.2021.10.001
Probiotics in Pediatric Gastroenterology
Szajewska, H. (2021) · Springer eBooks · doi:10.1007/978-3-030-80068-0_54
Gut microbiota in the combined treatment of colorectal cancer using autoprobiotics
Ермоленко, Е. И., Alekhina, G., Кащенко, В. А., Захаренко, А. А., Тен, О. А., Morozova, A. S., Tsapieva, A., Ilyina, A. S., Сергеевич, О. Т., Евгеньевна, П. О., et al. (2024) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-218-10-63-76
Ito, T., Okuyama, M., Takahashi, Y., Ohkusu, K., & Yokota, K. (2024) · Cureus · doi:10.7759/cureus.68056
Butel, M. J., Waligora‐Dupriet, A., & Aires, J. (2025) · EMC - Biologie Médicale · doi:10.1016/s2211-9698(24)48051-5
Ермоленко, Е. И., Baryshnikova, N. V., Kovalis, S. A., Novikova, N. S., Orlova, V. V., Ilyina, A. S., Кащенко, В. А., & Suvorov, A. N. (2024) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-231-11-170-177
Clinical features of restrictive cardiomyopathy and constrictive pericarditis
Spinner, J. A., & Denfield, S. W. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-13279-7.00031-6
Genomic characteristics of Lacticaseibacillus rhamnosus strains isolated from blood
Jarocki, P., Sadurski, J., Siuda, M., Romanowicz, M., Panek, J., Frąc, M., & Waśko, A. D. (2025) · PLoS ONE · doi:10.1371/journal.pone.0335843
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Gomes, A. R. D., Gonçalves, C. A. F., Santos, N. M. D. S., Costa, C. D. S., & Calou, I. B. F. (2025) · Cuadernos de Educación y Desarrollo · doi:10.55905/cuadv17n11-013
Lo, C. K.-L., & Sheth, P. M. (2021) · Figshare · doi:10.6084/m9.figshare.14526495
Lo, C. K.-L., & Sheth, P. M. (2021) · Figshare · doi:10.6084/m9.figshare.14526498
The Gut Microbiome in the IgE-Mediated Food-Allergic Patient—A Narrative Review
Singh, N., Hosein, E., Virkud, Y. V., Keet, C. A., & Kulis, M. D. (2026) · Nutrients · doi:10.3390/nu18040593
ZHULDUZBAYEVA, A. Z., MUKAZHANOV, A. N., Tekebayeva, Z. B., Теmirbekova, A., Бегманович, А. А., Kulzhanova, K., Аманбаев, А. А., Shoaib, N., Nurbekova, Z., & Temirkhanov, A. Z. (2026) · МИКРОБИОЛОГИЯ ЖӘНЕ ВИРУСОЛОГИЯ · doi:10.53729/mv-as.2026.01.02
Katchhi, M. S., Ming, L. C., Tay, J. E. F., Gew, L. T., Ser, H. L., & Ali, R. A. R. (2026) · Research Square · doi:10.21203/rs.3.rs-10288995/v1
Zakrzewska, Z., Boruta, O., Skupień, D., & Skoczen, S. P. (2026) · Discover Oncology · doi:10.1007/s12672-026-05551-7
Balboa, M. J., Álvarez, M. N., Porta, M., Ricote, M., Recio, N., Bodas, A., Valenti, M., & Guarner, F. (2026) · Medicina de Familia SEMERGEN · doi:10.1016/j.semerg.2026.102800
Leonov, G. E., & Starodubova, A. V. (2026) · Rational Pharmacotherapy in Cardiology · doi:10.20996/1819-6446-2026-3365
- Authors
- Costa, R. L., Moreira, J., Lorenzo, A., & Lamas, C. C.
- Affiliations
- Instituto Nacional de Cardiologia (BR)
- Corresponding author
- Costa, Rafael Lessa
- Venue
- BMC Complementary and Alternative Medicine
- Published
- 2018-12
- Volume
- 18
- Issue
- 1
- Pages
- 329-329
- ISSN
- 1472-6882 (ISSN-L)
- PMC
- PMC6292120
- OpenAlex
- W2905075966
- Semantic Scholar
- a43371345fa412734a8f54d6d0ca41882d8de45d
- Cited by
- 105
- References
- 31
- Citations by year
- 2026: 20 · 2025: 15 · 2024: 12 · 2023: 6 · 2022: 10 · 2021: 20 · 2020: 15 · 2019: 7
- FWCI
- 1.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- BMC Complementary and Alternative Medicine (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arca - Repositório Institucional da Fiocruz (publishedVersion, other-oa)
- Americanae (AECID Library) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (202.782/2015)
- National Institutes of Health
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Health Sciences › Medicine › Complementary and alternative medicine › Complementary and Alternative Medicine Studies
- Keywords
- probiotics, infectious complications, fungemia, Saccharomyces, Lactobacillus, Bifidobacterium, Bacillus, Clostridium difficile colitis, mortality, antibiotic use, immunosuppression, elderly patients, probiotic safety
- MeSH terms
- Administration, Oral, Adolescent, Adult, Aged, Aged, 80 and over, Bifidobacterium, Child, Child, Preschool, Female, Humans, Infant, Infant, Newborn, Lactobacillus, Male, Middle Aged, Mycoses, Saccharomyces, Gram-Positive Bacterial Infections, Probiotics, Young Adult
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