Skip to main content
Download PDF

Efficacy and safety of bifidobacterium quadruple viable tablets in the treatment of Helicobacter pylori-infected peptic ulcer or gastritis patients: a systematic review and meta-analysis

BMC Infectious Diseases volume 23, Article number: 313 (2023) Cite this article

Abstract

Background

To better understand the efficacy and safety of Bifidobacterium quadruple viable tablets in the treatment of helicobacter pylori (H. pylori)-infected peptic ulcer or gastritis patients.

Methods

A systematic review of the studies published to June 2022 was performed in English database PubMed, Embase, Chinese database CNKI, Wanfang. There were 17 studies were included in this systematic review and meta-analysis. The outcomes measured included H. pylori eradication rate, changes in clinical symptoms of epigastric pain scores, and the incidence of adverse reactions.

Results

The results of the fixed effect model showed that the eradication rate of H. pylori in the combination of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was greater than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (OR = 3.73, 95%CI (2.79,5.00), Z = 2.78, P < 0.001; I2 = 0.0%, P > 0.999). The results of random effects model showed that the epigastric pain score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (WMD=-0.70, 95%CI (-1.06,-0.34), Z = 3.82, P < 0.001; I2 = 96.7%, P < 0.001). The results of random effects model showed that the acid reflux score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (WMD=-0.98, 95%CI (-1.70,-0.26), Z = 2.66, P < 0.001; I2 = 99.7%, P < 0.001).

Conclusions

The eradication rate of H. pylori by Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing quadruple therapy is better than that of bismuth-containing quadruple therapy. The improvement of clinical symptoms of patients is better than that of bismuth-containing quadruple therapy, and the incidence of adverse reactions is lower than that of bismuth-containing quadruple therapy. Bifidobacterium quadruple viable bacteria tablet combined with bismuth-containing quadruple therapy was effective and safe. It provides a new way to treat patients with H. pylori.

Peer Review reports

Introduction

Helicobacter pylori (H. pylori) is the most common pathogen with prevalence rates of more than 80% in developing countries [1]. The cag-PAI was found to be present in more than 96% of 594 isolates in one study [2], which is similar to that reported previously for eastern populations [3,4,5]. Previous studies reported that cagA and cagE were detected in 66% and 62% H. pylori strains respectively in America [6, 7]. The presence of cagA and cagE in H. pylori were isolated from Chinese, Indian, and Malay patients in Singapore ranged from 92.3 to 100% [3]. The H. pylori was found to be associated to many diseases including chronic gastritis, peptic ulcer disease, gastric mucosa associated lymphoid tissue lymphoma, and gastric adenocarcinoma [8,9,10,11,12,13]. Antibiotics are most commonly used clinically for the treatment of diseases associated with H. pylori. The randomized controlled trial showed that probiotic did not reduce the risk of antibiotic-associated diarrhea in children when analyzed according to the most stringent definition [14]. However, it reduced the overall risk of diarrhea for 7 days after antibiotic treatment. Sheu et al. found that pretreatment of yogurt containing Lactobacillus and Bifidobacterium-containing improved the efficacy of quadruple therapy in eradicating residual H. pylori infection after failed triple therapy [15]. There was a study have shown that antibiotics used to treat H. pylori may cause microbiome disorders [16]. He et al. found the probiotic could downregulate immune-inflammatory mediators, and modify clinical symptoms in patients [17]. However, there was no significant effect on the eradication rate of H. pylori. Francesco et al. found that the treatment seem to improve the eubiosis of the gut microbial consortium [18]. But a study has shown that certain potentially pathogenic bacteria such as Fusobacterium increased after probiotic monotherapy. To better understand the efficacy and safety of Bifidobacterium quadruple viable tablets in the treatment of H. pylori-infected peptic ulcer patients. Therefore a meta-analysis was used to measure the effect of Bifidobacterium quadruple viable tablets on patients with H. pylori.

Materials and methods

Search of literature

We performed this meta-analysis following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (https://guides.lib.monash.edu/systematic-review/prisma). PRISMA is an evidence-based minimum set of items for reporting in systematic reviews and meta-analyses. PRISMA is an international initiative developed by relevant experts to address the ongoing issue of a lack of well documented and transparent review methods reported in published review papers. All the prospective or retrospective study published from the database inception through June 2022, were searched from two English-language databases (PubMed and Embase) and two Chinese-language databases (China National Knowledge Infrastructure and Wanfang) by 2 reviewers. Search terms were ((bifidobaeterium tetravaccine tables), AND (bifidobaeterium), AND (Helicobacter Pylori OR HP). Quadruple viable tablets: Bifidobacterium infantis, Feedadditive Lactobacillusacidophilus, Enterococcus faecalis, Bacilluscereus.

Inclusion and exclusion criteria

The inclusion criteria included: (1) randomized controlled trials; (2) Patients included in the study were patients with peptic ulcer or gastritis ulcer with H pylori infection; (3) The experimental group was Bifidobacterium quadruple viable tablet combined with bismuth-containing quadruple therapy, and the control group was bismuth-containing quadruple therapy; (4) The main indicators are Helicobacter pylori clearance rate and symptom score; the secondary indicators are the incidence of adverse reactions.

The exclusion criteria were (1) reduplicative article; (2) conference summaries, comments, letters, etc.; (3) animal studies, existing meta-analyses and systematic reviews; (4) Types of non-randomized controlled trials; (5) No primary indicator data to report.

Data extraction

Extracted information includes author’s name, publication time, sample size, age of included patients, H pylori detection method, outcome indicators, etc. Data were extracted from the literature by the first reviewer, and accuracy was confirmed by the second reviewer.

The risk of bias assessment of the included studies was performed using the Cochrane Collaboration’s RCT risk of bias assessment tool. The Cochrane collaboration risk of the bias tool considers these items for assessment: random sequences generation (for selection bias); allocation concealment (for selection bias); blinding of participants and personnel (for performance bias); blinding of outcome assessment (for detection bias); incomplete outcome data (for attrition bias); selective reporting and other bias (for reporting bias). The two authors performed the risk of bias assessment independently. If there was any disagreement, they discussed with the third author and finally reached agreement.

Statistical analysis

Data analysis was performed using Stata 15.0 software. The main indicators of Helicobacter pylori eradication rate and incidence of adverse events were estimated using indicators OR values ​​and 95%CI. Effects of symptom scores were estimated using Weighted Mean Difference (WMD) and 95% CI. According to the results of the heterogeneity test, choose a random-effects or fixed-effects model to estimate the total effect. Q-test and I2-test were used to estimate heterogeneity between studies. When P > 0.1 and I2 ≤ 50%, the fixed effect model was used. When P < 0.1 and I2 ≥ 50%, the random effect model was used. Funnel plots and Egger’s test were used to assess the primary outcome of publication bias. If the P value is < 0.05, the difference in means is considered statistically significant. Sensitivity analysis was used to identify the sources of heterogeneity, and was performed to cascade studies to observe the effect on the combined effect and the stability of the main index results.

Results

Study selection

A total of 219 studies were identified through the database search. 35 duplicated reports were excluded. 106 irrelevant studies were excluded after a title and abstract screening that. According to the inclusion and exclusion criteria, 61 studies were excluded, 17 studies met the inclusion criteria. A specific studies flowchart was shown in Fig. 1. And the selected study characteristics were listed in Table 1. The control group was quadruple viable tablets. Bifidobacterium quadruple viable tablets were added to the control group in the treatment group. The results of the risk bias evaluation of the studies were shown in Figs. 2 and 3. The method of randomization was described in 11 studies. 6 articles was used allocation concealment. None of the studies described blinded settings. All articles were unknown risk. All study data were completed. There was no selective reporting bias in any of the 17 articles. The included studies were of good quality and had a low risk of bias.

Fig. 1
figure 1

The process of selecting articles for the meta-analysis

Full size image
Table 1 Characteristics of Studies Included in the Meta-Analysis.
Full size table
Fig. 2
figure 2

Methodological quality evaluation of included studies

Full size image
Fig. 3
figure 3

Risk of bias summary

Full size image
Fig. 4
figure 4

The combined effect results of eradication rate in each study.

Full size image

Helicobacter pylori eradication rate

The results of the fixed effect model showed that the eradication rate of H pylori in the combination of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was greater than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (OR = 3.73, 95%CI (2.79,5.00), Z = 2.78, P < 0.001; I2 = 0.0%, P = 0.859). The H pylori eradication rate was analyzed by treatment duration as a subgroup (Fig. 4). There was no heterogeneity among studies. The publication bias analysis was shown in Fig. 5. The funnel plot has poor symmetry. Combined with Egger’s test, P < 0.001, there was publication bias. Sensitivity analysis was used to evaluate the stability of the combined effect. By excluding each study step by step, the combined effect was within the 95% CI (1.06, 1.38), and the study results were stable and reliable (Fig. 6).

Fig. 5
figure 5

Analysis of publication bias with the funnel plot about the eradication rate

Full size image
Fig. 6
figure 6

Sensitivity analysis of eradication rate.

Full size image
Fig. 7
figure 7

The combined effect results of epigastric pain scores in each study.

Full size image

Changes in clinical symptoms of epigastric pain scores

The results of random effects model showed that the epigastric pain score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (WMD=-0.70, 95%CI (-1.06,-0.34), Z = 3.82, P < 0.001; I2 = 96.7%, P < 0.001) (Fig. 7). There was heterogeneity among the studies. The results of random effects model showed that the acid reflux score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (WMD=-0.98, 95%CI (-1.70,-0.26), Z = 2.66, P < 0.001; I2 = 99.7%, P < 0.001) (Fig. 8). There was heterogeneity among the studies. There was heterogeneity among the studies. The results of random effects model showed that the nausea and vomiting score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (WMD=-1.02, 95%CI(-1.66,-0.39), Z = 3.15, P = 0.002; I2 = 97.1%, P < 0.001) (Fig. 9). Types of adverse reactions were analyzed in Table 2. There was heterogeneity among the studies.

Fig. 8
figure 8

The combined effect results of acid reflux score in each study.

Full size image
Fig. 9
figure 9

The combined effect results of nausea and vomiting score in each study

Full size image
Table 2 Types of adverse reactions were analyzed
Full size table

The incidence of adverse reactions

The results of the fixed effect model showed that the incidence of adverse reactions of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant (OR = 0.37, 95%CI (0.27,0.50), Z = 5.37, P < 0.001; I2 = 0.0%, P = 0.782) (Fig. 10). There was no heterogeneity among studies.

Fig. 10
figure 10

The combined effect results of incidence of adverse reactions in each study

Full size image

Discussion

The gastric pathogen H. pylori is one of the most successful pathogens [19]. H. pylori infection is closely related to the pathogenesis of chronic gastritis, peptic ulcer, gastric cancer and gastric mucosa-associated lymphoid tissue lymphoma [20]. The eradication effect of H. pylori treatment has decreased owing to increasing its antimicrobial resistance [21]. H. pylori eradication therapy includes a variety of drugs, and adverse reactions are common during treatment, especially intestinal flora imbalance [22]. Therefore, many clinical treatment programs use probiotics to regulate the disturbance of intestinal flora while using antibiotics [23]. And some studies have shown that probiotics have an inhibitory effect on the reproduction of HP and can significantly reduce the adverse reactions of drugs and improve the healing rate of gastric mucosal damage [17]. Timely supplementation of probiotics can effectively improve the dysbiosis of the gastrointestinal tract in patients. At the same time, it can effectively protect the gastrointestinal mucosal barrier of patients, so that it can play a better therapeutic effect.

The bifidobacteria in the bifidobacteria quadruple viable tablet can secrete thermostable active protein and have inhibitory effect on Hp. Bifidobacterium is the normal flora of the healthy human gut. Direct supplementation can enhance the biological barrier function of the intestinal mucosa, inhibit the growth and reproduction of pathogenic bacteria, and regulate the intestinal microecological balance. Consistent with our findings, the results of the fixed effect model showed that the eradication rate of H. pylori in the combination of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was greater than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant. More interestingly, studies have shown that supplementation with yogurt containing bifidobacteria improves H. pylori eradication [24].

Fang et al. found Lactobacillus as an adjunct to triple therapy improves H. pylori eradication and reduces the incidence of treatment-related diarrhea in children [25]. Results of a meta-analysis of 10 clinical trials showed that lactobacillus- and bifidobacteria-containing probiotic combinations may have a beneficial effect on eradication rates and overall side-effect rates during initial H. pylori eradication therapy in adults [26]. Similarity, the results of random effects model showed that the epigastric pain score of Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing conventional quadruple therapy was lower than that of bismuth-containing conventional quadruple therapy, and the difference was statistically significant. And we found that the Bifidobacterium quadruple viable bacteria tablets could reduce the incidence of adverse reactions.

Conclusion

The eradication rate of H. pylori by Bifidobacterium quadruple viable bacteria tablets combined with bismuth-containing quadruple therapy was better than that of bismuth-containing quadruple therapy. The improvement of clinical symptoms of patients is better than that of bismuth-containing quadruple therapy, and the incidence of adverse reactions was lower than that of bismuth-containing quadruple therapy. Bifidobacterium quadruple viable bacteria tablet combined with bismuth-containing quadruple therapy was effective and safe.

Data Availability

Data is obtained with the permission of the corresponding author.

References

  1. Camilo V, Sugiyama T, Touati E. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2017;22(Suppl 1):32–5.

    Google Scholar 

  2. Lai CH, Perng CL, Lan KH, Lin HJ. Association of IS605 and cag-PAI of Helicobacter pylori isolated from patients with gastrointestinal Diseases in Taiwan. Gastroenterol Res Pract. 2013;2013:356217.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Schmidt HM, Andres S, Nilsson C, Kovach Z, Kaakoush NO, Engstrand L, Goh KL, Fock KM, Forman D, Mitchell H. The cag PAI is intact and functional but HP0521 varies significantly in Helicobacter pylori isolates from Malaysia and Singapore. Eur J Clin Microbiol Infect diseases: official publication Eur Soc Clin Microbiol. 2010;29(4):439–51.

    Article  CAS  Google Scholar 

  4. Sheu SM, Sheu BS, Yang HB, Li C, Chu TC, Wu JJ. Presence of iceA1 but not cagA, cagC, cagE, cagF, cagN, cagT, or orf13 genes of Helicobacter pylori is associated with more severe gastric inflammation in taiwanese. J Formos Med Association = Taiwan yi zhi. 2002;101(1):18–23.

    CAS  PubMed  Google Scholar 

  5. Perng CL, Lin HJ, Lo WC, Tseng GY, Sun IC, Ou YH. Genotypes of Helicobacter pylori in patients with peptic ulcer bleeding. World J Gastroenterol. 2004;10(4):602–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Podzorski RP, Podzorski DS, Wuerth A, Tolia V. Analysis of the vacA, cagA, cagE, iceA, and babA2 genes in Helicobacter pylori from sixty-one pediatric patients from the midwestern United States. Diagn Microbiol Infect Dis. 2003;46(2):83–8.

    Article  CAS  PubMed  Google Scholar 

  7. Hsu PI, Hwang IR, Cittelly D, Lai KH, El-Zimaity HM, Gutierrez O, Kim JG, Osato MS, Graham DY, Yamaoka Y. Clinical presentation in relation to diversity within the Helicobacter pylori cag pathogenicity island. Am J Gastroenterol. 2002;97(9):2231–8.

    Article  CAS  PubMed  Google Scholar 

  8. Fischbach W, Malfertheiner P. Helicobacter Pylori infection. Deutsches Arzteblatt international. 2018;115(25):429–36.

    PubMed  PubMed Central  Google Scholar 

  9. Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H, et al. Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer. 2004;109(1):138–43.

    Article  CAS  PubMed  Google Scholar 

  10. Hill R, Pearman J, Worthy P, Caruso V, Goodwin S, Blincow E. Campylobacter pyloridis and gastritis in children. Lancet (London England). 1986;1(8477):387.

    Article  CAS  PubMed  Google Scholar 

  11. Sabbagh P, Mohammadnia-Afrouzi M, Javanian M, Babazadeh A, Koppolu V, Vasigala VR, Nouri HR, Ebrahimpour S. Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations. Eur J Clin Microbiol Infect diseases: official publication Eur Soc Clin Microbiol. 2019;38(1):55–66.

    Article  CAS  Google Scholar 

  12. Nejati S, Karkhah A, Darvish H, Validi M, Ebrahimpour S, Nouri HR. Influence of Helicobacter pylori virulence factors CagA and VacA on pathogenesis of gastrointestinal disorders. Microb Pathog. 2018;117:43–8.

    Article  CAS  PubMed  Google Scholar 

  13. Tokudome S, Hosono A, Suzuki S, Ghadimi R, Tanaka T, Ichikawa H, Miyata M, Marumoto M, Agawa H, Arakawa K, et al. Helicobacter pylori infection as an essential factor for stomach cancer. Asian Pac J cancer prevention: APJCP. 2006;7(1):163.

    Google Scholar 

  14. Lukasik J, Dierikx T, Besseling-van der Vaart I, de Meij T, Szajewska H. Multispecies Probiotic for the Prevention of Antibiotic-Associated Diarrhea in Children: a Randomized Clinical Trial. JAMA Pediatr. 2022;176(9):860–6.

    Article  PubMed  Google Scholar 

  15. Sheu BS, Cheng HC, Kao AW, Wang ST, Yang YJ, Yang HB, Wu JJ. Pretreatment with Lactobacillus- and Bifidobacterium-containing yogurt can improve the efficacy of quadruple therapy in eradicating residual Helicobacter pylori infection after failed triple therapy. Am J Clin Nutr. 2006;83(4):864–9.

    Article  CAS  PubMed  Google Scholar 

  16. Yildiz SS, Yalinay M, Karakan T. Bismuth-based quadruple Helicobacter pylori eradication regimen alters the composition of gut microbiota. Le Infezioni in Medicina. 2018;26(2):115–21.

    PubMed  Google Scholar 

  17. He C, Kong F, Chai X, Zou C, Zhu X, Zhao D. Effect of Probiotic-Assisted Eradication of cagA+/vacA s1m1 Helicobacter pylori on Intestinal Flora. BioMed research international 2022, 2022:8607671.

  18. Di Pierro F, Bertuccioli A, Saponara M, Ivaldi L. Impact of a two-bacterial-strain formula, containing Bifidobacterium animalis lactis BB-12 and Enterococcus faecium L3, administered before and after therapy for Helicobacter pylori eradication. Minerva Gastroenterol Dietol. 2020;66(2):117–23.

    Article  PubMed  Google Scholar 

  19. Nagy P, Johansson S, Molloy-Bland M. Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut pathogens. 2016;8:8.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kuo YT, Liou JM, El-Omar EM, Wu JY, Leow AHR, Goh KL, Das R, Lu H, Lin JT, Tu YK, et al. Primary antibiotic resistance in Helicobacter pylori in the Asia-Pacific region: a systematic review and meta-analysis. lancet Gastroenterol Hepatol. 2017;2(10):707–15.

    Article  PubMed  Google Scholar 

  21. Liou JM, Chen CC, Chang CM, Fang YJ, Bair MJ, Chen PY, Chang CY, Hsu YC, Chen MJ, Chen CC, et al. Long-term changes of gut microbiota, antibiotic resistance, and metabolic parameters after Helicobacter pylori eradication: a multicentre, open-label, randomised trial. Lancet Infect Dis. 2019;19(10):1109–20.

    Article  CAS  PubMed  Google Scholar 

  22. Lou JG, Chen J, Huang XL, Zhao ZY. Changes in the intestinal microflora of children with Helicobacter pylori infection and after Helicobacter pylori eradication therapy. Chin Med J. 2007;120(10):929–31.

    Article  PubMed  Google Scholar 

  23. Zhou Y, Ye Z, Lu J, Miao S, Lu X, Sun H, Wu J, Wang Y, Huang Y. Long-term changes in the gut microbiota after 14-day bismuth quadruple therapy in penicillin-allergic children. Helicobacter. 2020;25(5):e12721.

    Article  CAS  PubMed  Google Scholar 

  24. Sheu BS, Wu JJ, Lo CY, Wu HW, Chen JH, Lin YS, Lin MD. Impact of supplement with Lactobacillus- and Bifidobacterium-containing yogurt on triple therapy for Helicobacter pylori eradication. Aliment Pharmacol Ther. 2002;16(9):1669–75.

    Article  PubMed  Google Scholar 

  25. Fang HR, Zhang GQ, Cheng JY, Li ZY. Efficacy of Lactobacillus-supplemented triple therapy for Helicobacter pylori infection in children: a meta-analysis of randomized controlled trials. Eur J Pediatrics. 2019;178(1):7–16.

    Article  CAS  Google Scholar 

  26. Wang ZH, Gao QY, Fang JY. Meta-analysis of the efficacy and safety of Lactobacillus-containing and Bifidobacterium-containing probiotic compound preparation in Helicobacter pylori eradication therapy. J Clin Gastroenterol. 2013;47(1):25–32.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Digestive Disease Center, Second Affiliated Hospital of Shandong University of Traditional Chinese Medicine, Shandong, 250000, P.R. China

    Xueliang Jiang

  2. Department of Gastroenterology, First People’s Hospital of Shangqiu City, Henan, 475000, P.R. China

    Chunjin Xu

  3. Department of Gastroenterology, First People’s Hospital of the city of Xiangyang, Hubei, 441000, P.R. China

    Bo Liu

  4. Gastroenterology Department, Chongqing University Three Gorges Hospital, Chongqing, 404100, P. R. China

    Ping Chen

  5. Hangzhou Grand Biologics Pharmaceutical Co. LTD., Hangzhou, 310000, P. R. China

    Qinchang Xu & Lu Zhang

Authors
  1. Xueliang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunjin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ping Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qinchang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Xueliang Jiang and Chunjin Xu conceived the study. Xueliang Jiang and Lu Zhang performed the literature search and writing of the manuscript. Xueliang Jiang and Bo Liu analyzed and interpreted the data. Xueliang Jiang, Ping Chen and Qinchang Xu collected and assembled the data. Lu Zhang submitted the manuscript and is the corresponding author. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lu Zhang.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no conflict of interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, X., Xu, C., Liu, B. et al. Efficacy and safety of bifidobacterium quadruple viable tablets in the treatment of Helicobacter pylori-infected peptic ulcer or gastritis patients: a systematic review and meta-analysis. BMC Infect Dis 23, 313 (2023). https://doi.org/10.1186/s12879-023-08211-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12879-023-08211-1

Keywords

BMC Infectious Diseases

ISSN: 1471-2334

Contact us