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For: Ye Q, Shao X, Shen R, Chen D, Shen J. Changes in the human gut microbiota composition caused by Helicobacter pylori eradication therapy: A systematic review and meta-analysis. Helicobacter 2020;25:e12713. [PMID: 32515529 DOI: 10.1111/hel.12713] [Citation(s) in RCA: 40] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [What about the content of this article? (0)] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/11/2020] [Revised: 05/10/2020] [Accepted: 05/17/2020] [Indexed: 02/06/2023]

For:	Ye Q, Shao X, Shen R, Chen D, Shen J. Changes in the human gut microbiota composition caused by Helicobacter pylori eradication therapy: A systematic review and meta-analysis. Helicobacter 2020;25:e12713. [PMID: 32515529 DOI: 10.1111/hel.12713] [Citation(s) in RCA: 40] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [What about the content of this article? (0)] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/11/2020] [Revised: 05/10/2020] [Accepted: 05/17/2020] [Indexed: 02/06/2023]

Number

Cited by Other Article(s)

George S, Lucero Y, Cabrera C, Zabala Torres B, Fernández L, Mamani N, Lagomarcino A, Aguilera X, O'Ryan M. Protocol for a randomised 'screen-and-treat' Helicobacter pylori eradication trial in 14-18-years-old adolescents residing in three regions of Chile: effectiveness and microbiological host implications. BMJ Open 2025;15:e084984. [PMID: 39890135 PMCID: PMC11784427 DOI: 10.1136/bmjopen-2024-084984] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/02/2024] [Accepted: 01/10/2025] [Indexed: 02/03/2025] Open

Abstract

INTRODUCTION

Gastric cancer is a major global health concern, being the final stage of a long-term process, primarily associated with Helicobacter pylori (H. pylori) infection. Early childhood acquisition of H. pylori with low spontaneous eradication rates underscores the need for preventive measures. Our previous pilot treatment study revealed high eradication rates, favourable tolerance profile and a decline in serum biomarkers indicative of gastric damage in asymptomatic school-aged children. The purpose of this study is to determine the potential benefit of a 'screen-and-treat' strategy targeting persistently infected, asymptomatic adolescents. Specific aims are to assess eradication efficacy, its clinical and molecular outcomes and potential clinical and microbiological side effects.

METHODS AND ANALYSIS

The screening phase will involve testing 500-1000 asymptomatic adolescents aged 14-18 from three cities in Chile using the urea breath test (UBT) to identify 210 participants with persistent infection. They will proceed to a randomised, non-blinded, controlled trial, receiving either a sequential eradication scheme for H. pylori or no treatment. Follow-up will span up to 24 months post-treatment, involving UBT, gastroenterological assessments and blood and stool sample collections. Concurrently, a subset of 60 uninfected adolescents will undergo matched follow-up. Enzyme-linked immunosorbent assay (ELISA) commercial kits will evaluate gastric damage biomarkers in serum (pepsinogen I and II, gastrin-17, VCAM-1, CXCL13). Stool samples will be employed for Escherichia coli and Enterococcus spp-culture, assessing AMR via the disk diffusion method. H. pylori clarithromycin resistance will be determined by molecular method from stool samples. The gut microbiome will be characterised by amplifying and sequencing the 16S rRNA gene from stool samples, followed by bioinformatics analysis.

ETHICS AND DISSEMINATION

Approved by the Human Research Ethics Committee at the Faculty of Medicine, University of Chile (073-2022). Findings will be disseminated in peer-reviewed journals and scientific meetings to guide future practices.

TRIAL REGISTRATION NUMBER

NCT05926804.

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Liu Z, Xu H, You W, Pan K, Li W. Helicobacter pylori eradication for primary prevention of gastric cancer: progresses and challenges. JOURNAL OF THE NATIONAL CANCER CENTER 2024;4:299-310. [PMID: 39735441 PMCID: PMC11674435 DOI: 10.1016/j.jncc.2024.06.006] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/26/2024] [Revised: 06/20/2024] [Accepted: 06/27/2024] [Indexed: 12/31/2024] Open

Kuo YC, Ko HJ, Yu LY, Shih SC, Wang HY, Lin YC, Hu KC. Kill Two Birds with One Stone? The Effect of Helicobacter pylori Eradication in Decreased Prevalence of Gastric Cancer and Colorectal Cancer. Cancers (Basel) 2024;16:3881. [PMID: 39594836 PMCID: PMC11592957 DOI: 10.3390/cancers16223881] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2024] [Revised: 10/27/2024] [Accepted: 11/15/2024] [Indexed: 11/28/2024] Open

Affiliation(s)

Yang-Che Kuo Division of Gastroenterology, Department of Internal Medicine, MacKay Memorial Hospital, Taipei 104217, Taiwan; (Y.-C.K.); (L.-Y.Y.); (S.-C.S.); (H.-Y.W.) Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan
Hung-Ju Ko Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan
Lo-Yip Yu Division of Gastroenterology, Department of Internal Medicine, MacKay Memorial Hospital, Taipei 104217, Taiwan; (Y.-C.K.); (L.-Y.Y.); (S.-C.S.); (H.-Y.W.) Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan
Shou-Chuan Shih Division of Gastroenterology, Department of Internal Medicine, MacKay Memorial Hospital, Taipei 104217, Taiwan; (Y.-C.K.); (L.-Y.Y.); (S.-C.S.); (H.-Y.W.) Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan
Horng-Yuan Wang Division of Gastroenterology, Department of Internal Medicine, MacKay Memorial Hospital, Taipei 104217, Taiwan; (Y.-C.K.); (L.-Y.Y.); (S.-C.S.); (H.-Y.W.) Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan
Ying-Chun Lin Department of Anesthesiology, MacKay Memorial Hospital, Taipei 104217, Taiwan; Graduate Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei 106319, Taiwan
Kuang-Chun Hu Division of Gastroenterology, Department of Internal Medicine, MacKay Memorial Hospital, Taipei 104217, Taiwan; (Y.-C.K.); (L.-Y.Y.); (S.-C.S.); (H.-Y.W.) Healthy Evaluation Center, MacKay Memorial Hospital, Taipei 104217, Taiwan; MacKay Junior College of Medicine, Nursing and Management, Taipei 112021, Taiwan MacKay Medical College, Taipei 252005, Taiwan

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Mishra V, Dash D, Panda AK, Pathak SK. Efficacy of Lactobacillus spp. Supplementation in Helicobacter pylori Eradication: A Systematic Meta-Analysis of Randomized Controlled Trials With Trial Sequential Analysis. Helicobacter 2024;29:e70006. [PMID: 39722187 DOI: 10.1111/hel.70006] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/06/2024] [Revised: 10/24/2024] [Accepted: 12/12/2024] [Indexed: 12/28/2024]

Abstract

BACKGROUND

Helicobacter pylori infection is a major global health concern and has been associated with a number of gastrointestinal disorders. Probiotics, especially Lactobacillus spp., have been suggested to have beneficial effect in managing H. pylori infection. This meta-analysis of randomized control trials (RCTs) aimed to evaluate the effect of Lactobacillus spp. supplementation on H. pylori eradication rates and associated side effects when combined with standard therapy.

MATERIALS AND METHODS

Relevant studies were retrieved from PubMed, Scopus, Google Scholar and the Cochrane Library. Comprehensive Meta-Analysis (CMA) Software 4.0 was used for all the statistical analyses. TSA 0.9.5.10 Beta software was used for the trial sequential analysis (TSA). GRADEpro GDT was used to assess the certainty of evidence.

RESULTS

An analysis of 26 selected studies showed that supplementing with Lactobacillus spp. significantly increased the rates of H. pylori eradication in per-protocol (PP) analysis (Overall risk ratio [RR] = 1.063, p = 0.000, 95% CI of -0.21 to 2.11; adults: RR = 1.050, p = 0.005, 95% CI = -0.55 to 2.03, children: RR = 1.223, p = 0.001, 95% CI = -13.35 to 4.55). In comparison to quadruple therapy, Lactobacillus spp. supplementation to triple therapy showed significant benefit (RR: 1.124; p = 0.000, 95% CI of -0.48 to 2.61). L. reuteri supplementation indicated better efficacy (RR: 1.049; p = 0.055, 95% CI of -0.56 to 3.26) than Lactobacillus GG (RR: 0.980; p = 0.595, 95% CI of -0.69 to 1.21). The 28-30 day (RR: 1.103; p = 0.003, 95% CI of -2.14 to 4.19) and 14-day supplementation periods (RR: 1.102; p = 0.003, 95% CI of -1.69 to 3.51) showed the most improvement. The analysis also revealed that Lactobacillus spp. significantly reduced gastrointestinal side effects: nausea/vomiting (RR: 0.566; p = 0.037, -3.11 to 1.45), diarrhea (RR: 0.324; p = 0.000, -5.46 to 0.48), and abdominal pain (RR: 0.438; p = 0.007, -5.65 to 4.22). The effect on bloating was non-significant (RR: 0.820; p = 0.498, -4.01 to 0.96). TSA graphs validated sufficient evidence for the conclusions.

CONCLUSION

Lactobacillus spp. significantly enhances H. pylori eradication rates and may reduce gastrointestinal side effects when used alongside standard therapy, offering a promising adjunctive treatment option. The evidence was supported by TSA and assessed using GRADEpro, indicating a high certainty of the findings.

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Lin X, Huang H, Liu Y, Zeng Y, Lu S, Xu X, Lin Y, Qiu F, Cai F, Pan J, Huang S, Lin S, Lin A, Lin Z, Huang X. Tegoprazan-Amoxicillin Dual Therapy for Helicobacter pylori Eradication: A Prospective, Randomized, Multicenter Study in Fujian, China. Helicobacter 2024;29:e13151. [PMID: 39523458 DOI: 10.1111/hel.13151] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/22/2024] [Revised: 10/09/2024] [Accepted: 10/20/2024] [Indexed: 11/16/2024]

Abstract

INTRODUCTION

Few studies have investigated the efficacy and safety of tegoprazan-amoxicillin (TA) dual therapy for Helicobacter pylori eradication. We aim to evaluate the effectiveness and safety of different dosages of TA dual therapy for H. pylori eradication.

METHODS

This prospective, randomized, open-label, multicenter study was conducted at four centers in Fujian, China. H. pylori-infective patients were randomized 1:1:1 to receive one of the following treatments: bismuth quadruple therapy (BQT, esomeprazole 20 mg twice daily + potassium bismuth citrate 240 mg twice daily + amoxicillin 1 g twice daily + clarithromycin 500 mg twice daily), tegoprazan-amoxicillin dual therapies (TA-qd, tegoprazan 50 mg once daily + amoxicillin 1 g thrice daily; TA-bid, tegoprazan 50 mg twice daily + amoxicillin 1 g thrice daily) for 14 days. The primary outcome was noninferiority in eradication rates of the different TA groups compared to the BQT group. Secondary outcomes encompassed an assessment of adverse reactions and clinical symptom relief. Additionally, exploratory outcomes were focused on the shifts in gut microbiota and a cost-effectiveness analysis.

RESULTS

A total of 321 patients were enrolled. The eradication rates in the BQT group, TA-qd group, and TA-bid group were 85.05% (91/107), 85.98% (92/107), and 85.98% (92/107) in the intention-to-treat analysis (ITT) (BQT vs. TA-qd, 95% CI -8.50% to 10.36%, noninferiority p = 0.012; BQT vs. TA-bid, 95% CI -8.50% to 10.36%, noninferiority p = 0.012); 91.00% (91/100), 91.09% (92/101), and 92.93% (92/99) in the modified intention-to-treat analysis (mITT) (BQT vs. TA-qd, 95% CI -7.81% to 7.98%, noninferiority p = 0.006; BQT vs. TA-bid, 95% CI -5.62% to 9.48%, noninferiority p < 0.001); 90.81% (89/98), 91.00% (91/100), and 93.81% (91/97) in the per-protocol analysis (PP) (BQT vs. TA-qd, 95% CI -7.83% to 8.19%, noninferiority p = 0.006; BQT vs. TA-bid, 95% CI 4.46% to 10.46%, noninferiority p < 0.001). The incidence of adverse reactions in the TA-qd and TA-bid groups was significantly lower than in the BQT group (13.33%, 14.56%, and 27.18%, respectively; p = 0.017). The complete remissions of clinical symptoms for BQT, TA-qd, and TA-bid were 36.89%, 65.71%, and 68.93%, respectively, had significant differences (p < 0.001). Two weeks of TA therapy altered gut microbiota diversity and composition, but that recovered 4 weeks after discontinuation. The cost-effectiveness ratios (CERs) for BQT, TA-qd, and TA-bid were 1.85 CNY, 2.08 CNY, and 3.69 CNY, respectively.

CONCLUSION

Both TA dual therapies provided satisfactory eradication rates of > 90% for eradicating H. pylori, fewer adverse reactions, and greater clinical symptom relief compared to BQT, with a mild, reversible impact on gut microbiota. In addition, the TA dual therapy with low doses of tegoprazan showed better cost-effectiveness.

TRIAL REGISTRATION

Chinese Clinical Trial Register and registration No.: ChiCTR2300071997.

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Affiliation(s)

Xueyan Lin Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Huping Huang Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Yijuan Liu Department of Gastroenterology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China
Yanling Zeng Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Shiyun Lu Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Xuefeng Xu Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Yun Lin Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Feng Qiu Department of Gastroenterology, Fujian Provincial Geriatric Hospital, Fuzhou, China
Fangfang Cai Department of Gastroenterology, Fujian Provincial Geriatric Hospital, Fuzhou, China
Jie Pan Department of Gastroenterology, Pingtan Comprehensive Experimental Area Hospital, Fuzhou, China
Shaozhong Huang Department of Gastroenterology, Pingtan Comprehensive Experimental Area Hospital, Fuzhou, China
Shaowei Lin School of Public Health, Fujian Medical University, Fuzhou, China
Aiping Lin Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Zhihui Lin Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China
Xueping Huang Department of Gastroenterology, The Shengli Clinical Medical College, Fujian Medical University, Fuzhou, China Department of Gastroenterology, Fujian Provincial Hospital, Fuzhou, China Department of Gastroenterology, Fuzhou University Affiliated Provincial Hospital, Fuzhou, China

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Huang Y, Chen Y, Ma L, Guo H, Chen H, Qiu B, Yao M, Huang W, Zhu L. The toxic effects of Helicobacter pylori and benzo(a)pyrene in inducing atrophic gastritis and gut microbiota dysbiosis in Mongolian gerbils. Food Sci Nutr 2024;12:7568-7580. [PMID: 39479696 PMCID: PMC11521681 DOI: 10.1002/fsn3.4368] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/09/2024] [Revised: 07/09/2024] [Accepted: 07/15/2024] [Indexed: 11/02/2024] Open

Casado J, Olivan-Muro I, Algarate S, Chueca E, Salillas S, Velázquez-Campoy A, Piazuelo E, Fillat MF, Sancho J, Lanas Á, González A. Novel Drug-like HsrA Inhibitors Exhibit Potent Narrow-Spectrum Antimicrobial Activities against Helicobacter pylori. Int J Mol Sci 2024;25:10175. [PMID: 39337660 PMCID: PMC11432330 DOI: 10.3390/ijms251810175] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/03/2024] [Revised: 09/20/2024] [Accepted: 09/20/2024] [Indexed: 09/30/2024] Open

Affiliation(s)

Javier Casado Group of Translational Research in Digestive Disease, Institute for Health Research Aragón (IIS Aragón), San Juan Bosco 13, 50009 Zaragoza, Spain Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain
Irene Olivan-Muro Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain
Sonia Algarate Microbiology Service, University Clinic Hospital Lozano Blesa, San Juan Bosco 15, 50009 Zaragoza, Spain
Eduardo Chueca Group of Translational Research in Digestive Disease, Institute for Health Research Aragón (IIS Aragón), San Juan Bosco 13, 50009 Zaragoza, Spain Biomedical Research Networking Centre in Hepatic and Digestive Diseases (CIBERehd), Monforte de Lemos 3-5, 28029 Madrid, Spain
Sandra Salillas Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain
Adrián Velázquez-Campoy Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain Biomedical Research Networking Centre in Hepatic and Digestive Diseases (CIBERehd), Monforte de Lemos 3-5, 28029 Madrid, Spain
Elena Piazuelo Group of Translational Research in Digestive Disease, Institute for Health Research Aragón (IIS Aragón), San Juan Bosco 13, 50009 Zaragoza, Spain Biomedical Research Networking Centre in Hepatic and Digestive Diseases (CIBERehd), Monforte de Lemos 3-5, 28029 Madrid, Spain Aragón Health Sciences Institute (IACS), San Juan Bosco 13, 50009 Zaragoza, Spain
María F Fillat Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain
Javier Sancho Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain
Ángel Lanas Group of Translational Research in Digestive Disease, Institute for Health Research Aragón (IIS Aragón), San Juan Bosco 13, 50009 Zaragoza, Spain Biomedical Research Networking Centre in Hepatic and Digestive Diseases (CIBERehd), Monforte de Lemos 3-5, 28029 Madrid, Spain Department of Medicine, Psychiatry and Dermatology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Digestive Diseases Service, University Clinic Hospital Lozano Blesa, San Juan Bosco 15, 50009 Zaragoza, Spain
Andrés González Group of Translational Research in Digestive Disease, Institute for Health Research Aragón (IIS Aragón), San Juan Bosco 13, 50009 Zaragoza, Spain Department of Biochemistry and Molecular & Cellular Biology, University of Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain Institute for Biocomputation and Physics of Complex Systems (BIFI), Mariano Esquilor (Edif. I+D), 50018 Zaragoza, Spain Biomedical Research Networking Centre in Hepatic and Digestive Diseases (CIBERehd), Monforte de Lemos 3-5, 28029 Madrid, Spain

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Yao M, Cao J, Zhang L, Wang K, Lin H, Qin L, Zhang Q, Qu C, Miao J, Xue C. Indole-3-Lactic Acid Derived from Lacticaseibacillus paracasei Inhibits Helicobacter pylori Infection via Destruction of Bacteria Cells, Protection of Gastric Mucosa Epithelial Cells, and Alleviation of Inflammation. JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY 2024;72:15725-15739. [PMID: 38973111 DOI: 10.1021/acs.jafc.4c02868] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 07/09/2024]

Affiliation(s)

Mengke Yao College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Junhan Cao College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Liping Zhang Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Kai Wang Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Huan Lin College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Ling Qin Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Qing Zhang Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
Changfeng Qu Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China Laboratory for Marine Drugs and Bioproducts, Qingdao Pilot National Laboratory for Marine Science and Technology, Qingdao 266237, China Marine Natural Products R&D Laboratory, Qingdao Key Laboratory, Qingdao 266061, China
Jinlai Miao Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China Laboratory for Marine Drugs and Bioproducts, Qingdao Pilot National Laboratory for Marine Science and Technology, Qingdao 266237, China Marine Natural Products R&D Laboratory, Qingdao Key Laboratory, Qingdao 266061, China
Changhu Xue College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China

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Morin C, Verma VT, Arya T, Casu B, Jolicoeur E, Ruel R, Marinier A, Sygusch J, Baron C. Structure-based design of small molecule inhibitors of the cagT4SS ATPase Cagα of Helicobacter pylori. Biochem Cell Biol 2024;102:226-237. [PMID: 38377487 DOI: 10.1139/bcb-2023-0331] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/22/2024] Open

Shadvar N, Akrami S, Mousavi Sagharchi SMA, Askandar RH, Merati A, Aghayari M, Kaviani N, Afkhami H, Kashfi M. A review for non-antibiotic treatment of Helicobacter pylori: new insight. Front Microbiol 2024;15:1379209. [PMID: 38774508 PMCID: PMC11106852 DOI: 10.3389/fmicb.2024.1379209] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/30/2024] [Accepted: 04/12/2024] [Indexed: 05/24/2024] Open

Chen Y, Teng T, Su Y, Chen WZ. The effect of supplementing with Saccharomyces boulardii on bismuth quadruple therapy for eradicating Helicobacter pylori: a systematic review and meta-analysis of randomized controlled trials. Front Med (Lausanne) 2024;11:1344702. [PMID: 38695028 PMCID: PMC11061494 DOI: 10.3389/fmed.2024.1344702] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/26/2023] [Accepted: 04/08/2024] [Indexed: 05/04/2024] Open

Abstract

Background and objective

It remains uncertain if the addition of Saccharomyces boulardii (S. boulardii) to bismuth quadruple therapy (BQT) recommended in the current guidelines can enhance the Helicobacter pylori (H. pylori) eradication rate and decrease the incidence of adverse events. We therefore conducted a meta-analysis of randomized controlled trials (RCTs) to address this issue.

Methods

We performed comprehensive searches in PubMed, Embase, Web of Science, and Cochrane library databases from the inception of the databases through to November 1, 2023. A meta-analysis was conducted to determine the pooled relative risk (RR) with 95% confidence intervals (CI) using a random-effects model. We utilized the revised Cochrane Risk of Bias Tool to assess the risk of bias of included studies.

Results

A total of six RCTs (1,404 patients) included in this meta-analysis. The results of the intention-to-treat analysis showed that the combination of S. boulardii with BQT had a higher eradication rate than BQT alone (87.0% versus 83.3%), with a pooled RR of 1.05 (95% CI: 1.00-1.10, p = 0.03). In the per-protocol analysis, however, there was no statistical significance between the two groups in the eradication rate (93.7% versus 91.0%, RR = 1.03, 95% CI: 1.00-1.06, p = 0.07). The combination of S. boulardii and BQT had a significantly lower rate of overall adverse events (22% vs. 39%, RR = 0.56, 95% CI: 0.44-0.70, p < 0.00001), diarrhea (7.9% vs. 25.7%, RR = 0.29, 95% CI: 0.17-0.48, p < 0.00001), constipation (2.9% vs. 8.4%, RR = 0.35, 95% CI: 0.14-0.88, p = 0.03) and abdominal distention (4.9% vs. 12.7%, RR = 0.41, 95% CI: 0.23-0.72, p = 0.002) than BQT alone. For the assessment of risk of bias, five studies were deemed to have some concerns, while one study was judged to have a low risk.

Conclusion

Current evidence suggests that supplementation with S. boulardii in BQT may not have a major effect on the H. pylori eradication rate, but significantly reduces the incidence of overall adverse events, diarrhea, abdominal distention and constipation. Combining S. Boulardii with BQT can help alleviate symptoms, potentially improving patient adherence.

Systematic review registration

https://osf.io/n9z7c.

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Law SR, Mathes F, Paten AM, Alexandre PA, Regmi R, Reid C, Safarchi A, Shaktivesh S, Wang Y, Wilson A, Rice SA, Gupta VVSR. Life at the borderlands: microbiomes of interfaces critical to One Health. FEMS Microbiol Rev 2024;48:fuae008. [PMID: 38425054 PMCID: PMC10977922 DOI: 10.1093/femsre/fuae008] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2023] [Revised: 02/12/2024] [Accepted: 02/27/2024] [Indexed: 03/02/2024] Open

Liu M, Wang Y, Du B. Update on the association between Helicobacter pylori infection and asthma in terms of microbiota and immunity. ALLERGY, ASTHMA, AND CLINICAL IMMUNOLOGY : OFFICIAL JOURNAL OF THE CANADIAN SOCIETY OF ALLERGY AND CLINICAL IMMUNOLOGY 2024;20:4. [PMID: 38221621 PMCID: PMC10788013 DOI: 10.1186/s13223-024-00870-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/25/2023] [Accepted: 01/01/2024] [Indexed: 01/16/2024]

Li Y, Ouyang Y, He C. Research trends on the relationship between Helicobacter pylori and microbiota: A bibliometric analysis. Helicobacter 2023;28:e13021. [PMID: 37697432 DOI: 10.1111/hel.13021] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/13/2023] [Revised: 07/27/2023] [Accepted: 08/29/2023] [Indexed: 09/13/2023]

Abstract

BACKGROUND

Increasing evidence has indicated that Helicobacter pylori infection is associated with the complex microbiota in the digestive tract of the human body. We aimed to assess the research trends and hotspots in the field of H. pylori and microbiota using a quantitative method.

MATERIALS AND METHODS

The clinical studies on H. pylori and microbiota published from 2001 to 2022 were extracted from the Web of Science database. We visualized and analyzed countries/regions, institutions, authors, journals, and keywords through VOSviewer and CiteSpace software. The test techniques, specimen type, as well as microbiota variation after H. pylori infection and eradication were also evaluated.

RESULTS

A total of 98 publications were finally identified, and the number of annual papers increased gradually. China showed its dominant position in the publication outputs, and Nanchang University was the most productive institution. Cong He, Xu Shu, and Yin Zhu published the highest number of papers, whereas Helicobacter was the most productive journal. "Helicobacter pylori" ranked highest in the keyword occurrences. 16S rRNA gene sequencing was the most frequently used method for microbiota analysis. Fecal samples had the highest frequency of use, followed by gastric mucosa and saliva. H. pylori infection was associated with the alterations of microbiota through the digestive tract, characterized by the enrichment of Helicobacter in the stomach. Triple and quadruple therapy were the most utilized eradication regimens, and probiotics supplementation therapy has been proven to reduce side effects and restore microbial diversity.

CONCLUSIONS

This bibliometric analysis provides an overview of advancements in the field of H. pylori and microbiota. While numerous studies have been conducted on the correlation between H. pylori and the alterations of microbiota, future research is warranted to investigate the mechanisms underlying the interplay between H. pylori and other microbes in the development of related diseases.

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Sharma P, Phatak SM, Warikoo P, Mathur A, Mahant S, Das K, Das R. Crosstalk between Helicobacter pylori and gastrointestinal microbiota in various gastroduodenal diseases-A systematic review. 3 Biotech 2023;13:303. [PMID: 37588796 PMCID: PMC10425313 DOI: 10.1007/s13205-023-03734-5] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/20/2022] [Accepted: 07/21/2023] [Indexed: 08/18/2023] Open

Wang X, Teng G, Dong X, Dai Y, Wang W. Efficacy and safety of vonoprazan-amoxicillin dual therapy for Helicobacter pylori first-line treatment: a single-center, randomized, controlled trial. Therap Adv Gastroenterol 2023;16:17562848231190976. [PMID: 37664169 PMCID: PMC10469240 DOI: 10.1177/17562848231190976] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/12/2023] [Accepted: 07/13/2023] [Indexed: 09/05/2023] Open

Abstract

Background

With the increase in antibiotic resistance, the success rate of Helicobacter pylori (H. pylori) eradication therapy has declined in recent years. Vonoprazan-amoxicillin (VA) dual therapy has been reported to be a promising regimen.

Objectives

To compare the efficacy and safety of VA dual therapy and bismuth quadruple therapy containing amoxicillin and clarithromycin for H. pylori first-line eradication, and to further analyze the effects of clarithromycin resistance on eradication rate.

Design

This study was a single-center, open-label, randomized controlled trial.

Methods

Treatment-naïve H. pylori-infected patients were randomly allocated 1:1 to the VA group (vonoprazan 20 mg twice daily and amoxicillin 750 mg four times daily, for 14 days) or the RBAC group (rabeprazole 10 mg, bismuth potassium citrate 220 mg, amoxicillin 1000 mg and clarithromycin 500 mg twice daily, for 14 days). H. pylori clarithromycin resistance and CYP2C19 gene polymorphisms were detected with real-time polymerase chain reaction (PCR) technique. The eradication rates and adverse events were analyzed.

Results

A total of 151 patients were enrolled. The intention-to-treat (ITT), modified intention-to-treat (mITT), and per-protocol (PP) eradication rates and their 95% confidence intervals (95% CIs) were 94.6% (86.0-98.3%), 98.6% (91.3-99.9%), and 98.5% (90.9-99.9%) for VA group and 87.0% (77.0-93.3%), 91.8% (82.3-96.6%), and 93% (83.7-97.4%) for RBAC group. The eradication rate of the VA group was noninferior to the RBAC group in ITT, mITT, and PP analyses (p < 0.0001). In patients infected with strains of clarithromycin resistance point mutation, the eradication rate of the RBAC group decreased to lower than 90%, but the difference from the VA group did not achieve statistical significance (ITT eradication rate: 81.5% in the RBAC group and 96.2% in the VA group, p = 0.192). The incidence of adverse events in the VA group was 39.2%, which was significantly lower than that in the RBAC group (79.2%, p = 0.000).

Conclusion

The efficacy of VA dual therapy is noninferior to RBAC in H. pylori first-line eradication, with fewer adverse reactions.

Registration

This study was registered at the Chinese Clinical Trial Registry (ChiCTR2100052550) on 30 October 2021.

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Fiorani M, Tohumcu E, Del Vecchio LE, Porcari S, Cammarota G, Gasbarrini A, Ianiro G. The Influence of Helicobacter pylori on Human Gastric and Gut Microbiota. Antibiotics (Basel) 2023;12:765. [PMID: 37107126 PMCID: PMC10135037 DOI: 10.3390/antibiotics12040765] [Citation(s) in RCA: 9] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/15/2023] [Revised: 04/12/2023] [Accepted: 04/14/2023] [Indexed: 04/29/2023] Open

Duan M, Liu J, Zuo X. Dual therapy for Helicobacter pylori infection. Chin Med J (Engl) 2023;136:13-23. [PMID: 36805362 PMCID: PMC10106215 DOI: 10.1097/cm9.0000000000002565] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2022] [Indexed: 02/22/2023] Open

Maev IV, Andreev DN, Sokolov PS, Fomenko AК, Devkota MK, Andreev NG, Zaborovsky AV. Efficacy of <i>Saccharomyces boulardii</i> CNCM I-745 probiotic drug in the prevention and treatment of diarrhea in hospitalized patients with new coronavirus infection COVID-19. TERAPEVT ARKH 2022;94:1163-1170. [PMID: 36468990 DOI: 10.26442/00403660.2022.10.201881] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2022] [Accepted: 11/22/2022] [Indexed: 11/23/2022]

Abstract Aim. To evaluate the efficacy of Saccharomyces boulardii (S. boulardii) CNCM I-745 probiotic drug in preventing and treating diarrhea in hospitalized patients with COVID-19. Materials and methods. A prospective comparative study was conducted in two parallel groups. The study included males and females aged 18 to 60 with the following diagnosis confirmed by polymerase chain reaction: U07.2 Coronavirus infection COVID-19, caused by SARS-CoV-2 virus (grade 13 pneumonia according to CT scan). All patients received antibiotic therapy. The patients were subdivided into two equal groups (n=60) depending on the administration of S. boulardii CNCM I-745 probiotic drug in addition to standard treatment. The probiotic was prescribed by the attending physician; the dose was 2 capsules per day (500 mg/day) 30 min before the meal for 10 days. All patients were monitored for main clinical, laboratory, and instrumental parameters during the study. In addition, the symptom of diarrhea (stool with a frequency of more than 3 times a day of type 6 and 7 according to the Bristol stool scale), including its frequency, duration, and the number of bowel movements of loose stool per day were precisely evaluated in both groups. Results. In the overall patient pool, diarrhea was reported in 21.7% of in-patients during the observation period (95% confidence interval [CI] 14.229.1) with a mean duration of 4.6154 days (95% CI 3.7910-5.4398). The incidence of diarrhea in group 1 was 13.3% (95% CI 4.522.2), and in group 2, it was 30.0% (95% CI 18.141.9). Relative risk showed that the use of the S. boulardii CNCM I-745 probiotic drug leads to a significant reduction in the risk of diarrhea in hospitalized patients with COVID-19 infection receiving antibiotic therapy (odds ratio [OR] 0.3590, 95% CI 0.14210.9069; p=0.0303). In group 1, the duration of diarrhea was 3.1250 days (95% CI 2.58923.6608) versus 5.2778 days (95% CI 4.22906.3265) in group 2, p=0.0112. The mean daily frequency of loose stools in patients with diarrhea in group 1 was 3.2500 (95% CI 2.65883.8412) versus 4.3889 (95% CI 3.72525.0525) in group 2, p=0.0272. The secondary endpoint, duration of hospital stay, was also significantly shorter in group 1 patients 11.6833 days (95% CI 11.204212.1625) versus 12.7333 days (95% CI 12.135713.3309) in group 2, p=0.0120. Conclusion. The present prospective comparative study demonstrated that adding S. boulardii CNCM I-745 probiotic drug into the standard treatment regimen of patients with new coronavirus infection COVID-19 receiving antibiotic therapy helps reduce the incidence of diarrhea and its severity during hospitalization, as well as the duration of hospital stay. Collapse

He C, Xie Y, Zhu Y, Zhuang K, Huo L, Yu Y, Guo Q, Shu X, Xiong Z, Zhang Z, Lyu B, Lu N. Probiotics modulate gastrointestinal microbiota after Helicobacter pylori eradication: A multicenter randomized double-blind placebo-controlled trial. Front Immunol 2022;13:1033063. [PMID: 36426355 PMCID: PMC9679295 DOI: 10.3389/fimmu.2022.1033063] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2022] [Accepted: 10/21/2022] [Indexed: 08/10/2023] Open

Abstract

BACKGROUND

Helicobacter pylori (H. pylori) eradication has been reported to cause short-term disruption of gut microbiota. It is acknowledged that probiotics supplementation mitigates side effects induced by H. pylori eradication, yet its role on alleviating dysbiosis of microbiota is obscure.

OBJECTIVES

To evaluate the impact of probiotics on gastrointestinal microbiota after eradication therapy.

METHODS

This was a multicenter, double-blinded, randomized trial done at seven centers in China. A total of 276 treatment-naïve H. pylori-positive patients were randomly assigned to receive 14-day bismuth-containing quadruple therapy (esomeprazole, bismuth, amoxicillin, furazolidone) combined with probiotics (Bifidobacterium Tetragenous viable Bacteria Tablets) (n=140) or placebo (n=136) for 28 days. Saliva, gastric mucosa and fecal samples were collected before and after therapy for 16S rRNA gene sequencing.

RESULTS

The incidence of gastrointestinal adverse events was lower in probiotics group compared to placebo group (23.6% vs 37.7%, p=0.016), while there was no significant difference in eradication rate. We found dramatic perturbations of gut microbiota immediately following eradication, with the predominance of Proteobacteria in replacement of commensal Firmicutes and Bacteroidetes, and gradually restored after two weeks. The reduction of gut Bacteroidetes caused by eradication drugs was neutralized with probiotics supplementation. The gastric microbiota was completely reconstituted with H. pylori depleted and other taxa flourished. Of note, patients treated with probiotics showed smaller fluctuations of gastric microbiota compared to those with placebo. We also observed changes of saliva microbiota after H. pylori eradication, illustrated by the overgrowth of Neisseria and depletion of Streptococcus. The expansion of some pathogenic genera, including Porphyromonas, Leptotrichia, in the mouth was suppressed by probiotics.

CONCLUSION

This study not only demonstrated the beneficial effect of probiotics implementation on side events during H. pylori eradication but also provided a comprehensive profile of microbiome alterations along gastrointestinal tract that modulated by probiotics.

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Affiliation(s)

Cong He Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China
Yong Xie Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China
Yin Zhu Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China
Kun Zhuang Department of Gastroenterology, Xi’an Central Hospital, Shaanxi, China
Lijuan Huo Department of Gastroenterology, First Affiliated Hospital of Shanxi Medical University, Taiyuan, China
Yong Yu Department of Gastroenterology, Fifth Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Qiang Guo Department of Gastroenterology, First People’s Hospital of Yunnan Province, Kunming, China
Xu Shu Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China
Zhijuan Xiong Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China
Zhenyu Zhang Department of Gastroenterology, Nanjing First Hospital, Nanjing Medical University, Jiangsu, China
Bin Lyu Department of Gastroenterology, First Affiliated Hospital of Zhejiang Chinese Medical University, Hangzhou, China
Nonghua Lu Department of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Jiangxi, China Jiangxi Clinical Research Center for Gastroenterology, Nanchang, China

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Du L, Chen B, Cheng F, Kim J, Kim JJ. Effects of Helicobacter pylori Therapy on Gut Microbiota: A Systematic Review and Meta-Analysis. Dig Dis 2022;42:102-112. [PMID: 36228588 DOI: 10.1159/000527047] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/11/2021] [Accepted: 09/04/2022] [Indexed: 02/02/2023]

Kononova AG, Kolbasnikov SV, Beldiev SN. The role of probiotics in <i>Helicobacter pylori</i> eradication therapy regimens: current evidence of eff ectiveness. EXPERIMENTAL AND CLINICAL GASTROENTEROLOGY 2022:160-168. [DOI: 10.31146/1682-8658-ecg-200-4-160-168] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/04/2025]

Hu Y, Xu X, Ouyang YB, He C, Li NS, Xie C, Peng C, Zhu ZH, Xie Y, Shu X, Lu NH, Zhu Y. Analysis of oral microbiota alterations induced by Helicobacter pylori infection and vonoprazan-amoxicillin dual therapy for Helicobacter pylori eradication. Helicobacter 2022;27:e12923. [PMID: 36036087 DOI: 10.1111/hel.12923] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/07/2022] [Revised: 07/22/2022] [Accepted: 07/27/2022] [Indexed: 12/09/2022]

Affiliation(s)

Yi Hu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Xin Xu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yao-Bin Ouyang Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Cong He Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Nian-Shuang Li Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Chuan Xie Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Chao Peng Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Zhen-Hua Zhu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yong Xie Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Xu Shu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Nong-Hua Lu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yin Zhu Department Of Gastroenterology, Digestive Disease Hospital, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China

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Gut Microbiota Dysbiosis in the Development and Progression of Gastric Cancer. JOURNAL OF ONCOLOGY 2022;2022:9971619. [PMID: 36072968 PMCID: PMC9441395 DOI: 10.1155/2022/9971619] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 05/04/2022] [Accepted: 07/29/2022] [Indexed: 12/12/2022]

Hu Y, Xu X, Ouyang YB, He C, Li NS, Xie C, Peng C, Zhu ZH, Shu X, Xie Y, Lu NH, Zhu Y. Altered Gut Microbiota and Short-Chain Fatty Acids After Vonoprazan-Amoxicillin Dual Therapy for Helicobacter pylori Eradication. Front Cell Infect Microbiol 2022;12:881968. [PMID: 35719338 PMCID: PMC9201212 DOI: 10.3389/fcimb.2022.881968] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2022] [Accepted: 05/09/2022] [Indexed: 12/17/2022] Open

Affiliation(s)

Yi Hu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Xin Xu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yao-Bin Ouyang Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Cong He Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Nian-Shuang Li Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Chuan Xie Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Chao Peng Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Zhen-Hua Zhu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Xu Shu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yong Xie Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Nong-Hua Lu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China
Yin Zhu Department Of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, China JiangXi Clinical Research Center for Gastroenterology, Nanchang, China

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Guo Y, Cao XS, Guo GY, Zhou MG, Yu B. Effect of Helicobacter Pylori Eradication on Human Gastric Microbiota: A Systematic Review and Meta-Analysis. Front Cell Infect Microbiol 2022;12:899248. [PMID: 35601105 PMCID: PMC9114356 DOI: 10.3389/fcimb.2022.899248] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2022] [Accepted: 04/11/2022] [Indexed: 12/24/2022] Open

Abstract

Background

Helicobacter pylori (H. pylori) infection is a major risk factor for gastric cancer and eradication of H. pylori is recommended as an effective gastric cancer prevention strategy. The infected individuals show microbial dysbiosis of gastric microbiota. In recent years, agrowing number of studies have focused on gastric microbiota changes following H. pylori eradication. In the present study, we aim to evaluate the influence of successful H. pylori eradication on the short-term and long-term alterations of human gastric microbiota using a method of systematic review and meta-analysis.

Methods

We did a systematic search based on three databases (PubMed, EMBASE, and Web of Science) in November 2021. Additional articles were also identified by reviewing references cited in the included papers. Human studies that reported changes in gastric microbiota following successful H. pylori eradication were enrolled. PROSPERO registration number: CRD42021293796.

Results

In total, nine studies enrolling 546 participants were included. Regarding quadruple therapy, alpha diversity indexes increased within 1 month after eradication; significant differences in gastric microbial community structure between before and after eradication were also seen within 1 month. The trends of the above-mentioned diversity changes persisted with a follow-up of 6 months. The microbial composition altered significantly after eradication and the relative abundance of H. pylori-related taxa decreased. Accordingly, gastric commonly dominant commensals were enriched. Bioinformatic analyses of microbiota functions showed that bacteria reproduction-related pathways were down-regulated and pathways of gastric acid secretion, etc. were up-regulated. For triple therapy, similar trends of alpha diversity and beta diversity changes were observed in the short-term and long-term follow-up. Also, after eradication, H. pylori was not the gastric dominant bacteria and similar changes in gastric microbial composition were found. For gastric microbial interactions, a decrease in microbial interactions was seen after eradication. Additionally, regarding whether successful H. pylori eradication could restore gastric microbiota to uninfected status, the results remain controversial.

Conclusion

In conclusion, successful H. pylori eradication could reverse the gastric microbiota dysbiosis and show beneficial effects on gastric microbiota. Our findings may provide new insight for exploring the role of H. pylori and the whole gastric microbiota in gastric carcinogenesis.

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The impact of Saccharomyces boulardii adjuvant supplementation on alternation of gut microbiota after H. pylori eradication; a metagenomics analysis. GENE REPORTS 2022. [DOI: 10.1016/j.genrep.2022.101499] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/05/2023]

Helicobacter pylori may participate in the development of inflammatory bowel disease by modulating the intestinal microbiota. Chin Med J (Engl) 2022;135:634-638. [PMID: 35234697 PMCID: PMC9276318 DOI: 10.1097/cm9.0000000000002008] [Citation(s) in RCA: 13] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/17/2021] [Indexed: 12/04/2022] Open

Transcriptome Analysis of the Response of Mature Helicobacter pylori Biofilm to Different Doses of Lactobacillus salivarius LN12 with Amoxicillin and Clarithromycin. Antibiotics (Basel) 2022;11:antibiotics11020262. [PMID: 35203863 PMCID: PMC8868532 DOI: 10.3390/antibiotics11020262] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/07/2022] [Revised: 02/13/2022] [Accepted: 02/15/2022] [Indexed: 02/04/2023] Open

Nabavi-Rad A, Sadeghi A, Asadzadeh Aghdaei H, Yadegar A, Smith SM, Zali MR. The double-edged sword of probiotic supplementation on gut microbiota structure in Helicobacter pylori management. Gut Microbes 2022;14:2108655. [PMID: 35951774 PMCID: PMC9373750 DOI: 10.1080/19490976.2022.2108655] [Citation(s) in RCA: 41] [Impact Index Per Article: 13.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/14/2022] [Revised: 07/13/2022] [Accepted: 07/29/2022] [Indexed: 02/04/2023] Open

Abstract

As Helicobacter pylori management has become more challenging and less efficient over the last decade, the interest in innovative interventions is growing by the day. Probiotic co-supplementation to antibiotic therapies is reported in several studies, presenting a moderate reduction in drug-related side effects and a promotion in positive treatment outcomes. However, the significance of gut microbiota involvement in the competence of probiotic co-supplementation is emphasized by a few researchers, indicating the alteration in the host gastrointestinal microbiota following probiotic and drug uptake. Due to the lack of long-term follow-up studies to determine the efficiency of probiotic intervention in H. pylori eradication, and the delicate interaction of the gut microbiota with the host wellness, this review aims to discuss the gut microbiota alteration by probiotic co-supplementation in H. pylori management to predict the comprehensive effectiveness of probiotic oral administration.Abbreviations: acyl-CoA- acyl-coenzyme A; AMP- antimicrobial peptide; AMPK- AMP-activated protein kinase; AP-1- activator protein 1; BA- bile acid; BAR- bile acid receptor; BCAA- branched-chain amino acid; C2- acetate; C3- propionate; C4- butyrate; C5- valeric acid; CagA- Cytotoxin-associated gene A; cAMP- cyclic adenosine monophosphate; CD- Crohn's disease; CDI- C. difficile infection; COX-2- cyclooxygenase-2; DC- dendritic cell; EMT- epithelial-mesenchymal transition; FMO- flavin monooxygenases; FXR- farnesoid X receptor; GPBAR1- G-protein-coupled bile acid receptor 1; GPR4- G protein-coupled receptor 4; H2O2- hydrogen peroxide; HCC- hepatocellular carcinoma; HSC- hepatic stellate cell; IBD- inflammatory bowel disease; IBS- irritable bowel syndrome; IFN-γ- interferon-gamma; IgA immunoglobulin A; IL- interleukin; iNOS- induced nitric oxide synthase; JAK1- janus kinase 1; JAM-A- junctional adhesion molecule A; LAB- lactic acid bacteria; LPS- lipopolysaccharide; MALT- mucosa-associated lymphoid tissue; MAMP- microbe-associated molecular pattern; MCP-1- monocyte chemoattractant protein-1; MDR- multiple drug resistance; mTOR- mammalian target of rapamycin; MUC- mucin; NAFLD- nonalcoholic fatty liver disease; NF-κB- nuclear factor kappa B; NK- natural killer; NLRP3- NLR family pyrin domain containing 3; NOC- N-nitroso compounds; NOD- nucleotide-binding oligomerization domain; PICRUSt- phylogenetic investigation of communities by reconstruction of unobserved states; PRR- pattern recognition receptor; RA- retinoic acid; RNS- reactive nitrogen species; ROS- reactive oxygen species; rRNA- ribosomal RNA; SCFA- short-chain fatty acids; SDR- single drug resistance; SIgA- secretory immunoglobulin A; STAT3- signal transducer and activator of transcription 3; T1D- type 1 diabetes; T2D- type 2 diabetes; Th17- T helper 17; TLR- toll-like receptor; TMAO- trimethylamine N-oxide; TML- trimethyllysine; TNF-α- tumor necrosis factor-alpha; Tr1- type 1 regulatory T cell; Treg- regulatory T cell; UC- ulcerative colitis; VacA- Vacuolating toxin A.

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Keikha M, Karbalaei M. Probiotics as the live microscopic fighters against Helicobacter pylori gastric infections. BMC Gastroenterol 2021;21:388. [PMID: 34670526 PMCID: PMC8527827 DOI: 10.1186/s12876-021-01977-1] [Citation(s) in RCA: 40] [Impact Index Per Article: 10.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/06/2021] [Accepted: 10/15/2021] [Indexed: 02/07/2023] Open

Iino C, Shimoyama T. Impact of Helicobacter pylori infection on gut microbiota. World J Gastroenterol 2021;27:6224-6230. [PMID: 34712028 PMCID: PMC8515792 DOI: 10.3748/wjg.v27.i37.6224] [Citation(s) in RCA: 20] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/16/2021] [Revised: 05/13/2021] [Accepted: 09/02/2021] [Indexed: 02/06/2023] Open

Guillemard E, Poirel M, Schäfer F, Quinquis L, Rossoni C, Keicher C, Wagner F, Szajewska H, Barbut F, Derrien M, Malfertheiner P. A Randomised, Controlled Trial: Effect of a Multi-Strain Fermented Milk on the Gut Microbiota Recovery after Helicobacter pylori Therapy. Nutrients 2021;13:nu13093171. [PMID: 34579049 PMCID: PMC8466689 DOI: 10.3390/nu13093171] [Citation(s) in RCA: 24] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2021] [Revised: 08/27/2021] [Accepted: 09/07/2021] [Indexed: 12/21/2022] Open

Park JM, Han YM, Hahm KB. Rejuvenation of Helicobacter pylori-Associated Atrophic Gastritis Through Concerted Actions of Placenta-Derived Mesenchymal Stem Cells Prevented Gastric Cancer. Front Pharmacol 2021;12:675443. [PMID: 34483897 PMCID: PMC8416416 DOI: 10.3389/fphar.2021.675443] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2021] [Accepted: 06/22/2021] [Indexed: 01/06/2023] Open

Abstract

Chronic Helicobacter pylori infection causes gastric cancer via the progression of precancerous chronic atrophic gastritis (CAG). Therefore, repairing gastric atrophy could be a useful strategy in preventing H. pylori-associated gastric carcinogenesis. Although eradication of the bacterial pathogen offers one solution to this association, this study was designed to evaluate an alternative approach using mesenchymal stem cells to treat CAG and prevent carcinogenesis. Here, we used human placenta-derived mesenchymal stem cells (PD-MSCs) and their conditioned medium (CM) to treat H. pylori-associated CAG in a mice/cell model to explore their therapeutic effects and elucidate their molecular mechanisms. We compared the changes in the fecal microbiomes in response to PD-MSC treatments, and chronic H. pylori-infected mice were given ten treatments with PD-MSCs before being sacrificed for end point assays at around 36 weeks of age. These animals presented with significant reductions in the mean body weights of the control group, which were eradicated following PD-MSC treatment (p < 0.01). Significant changes in various pathological parameters including inflammation, gastric atrophy, erosions/ulcers, and dysplastic changes were noted in the control group (p < 0.01), but these were all significantly reduced in the PD-MSC/CM-treated groups. Lgr5+, Ki-67, H⁺/K⁺-ATPase, and Musashi-1 expressions were all significantly increased in the treated animals, while inflammatory mediators, MMP, and apoptotic executors were significantly decreased in the PD-MSC group compared to the control group (p < 0.001). Our model showed that H. pylori-initiated, high-salt diet-promoted gastric atrophic gastritis resulted in significant changes in the fecal microbiome at the phylum/genus level and that PD-MSC/CM interventions facilitated a return to more normal microbial communities. In conclusion, administration of PD-MSCs or their conditioned medium may present a novel rejuvenating agent in preventing the progression of H. pylori-associated premalignant lesions.

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Watanabe J, Hamasaki M, Kotani K. The Effect of Helicobacter pylori Eradication on Lipid Levels: A Meta-Analysis. J Clin Med 2021;10:jcm10050904. [PMID: 33668848 PMCID: PMC7956592 DOI: 10.3390/jcm10050904] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/25/2020] [Revised: 02/18/2021] [Accepted: 02/21/2021] [Indexed: 12/23/2022] Open

Andreev DN, Kucheryavyy YA, Maev IV. [Efficacy of butyric acid inclusion in eradication regimens for Helicobacter pylori infection: a meta-analysis of controlled trials]. TERAPEVT ARKH 2021;93:158-163. [PMID: 36286629 DOI: 10.26442/00403660.2021.02.200608] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2021] [Accepted: 04/05/2021] [Indexed: 12/11/2022]

Kakiuchi T, Yamamoto K, Imamura I, Hashiguchi K, Kawakubo H, Yamaguchi D, Fujioka Y, Okuda M. Gut microbiota changes related to Helicobacter pylori eradication with vonoprazan containing triple therapy among adolescents: a prospective multicenter study. Sci Rep 2021;11:755. [PMID: 33436953 PMCID: PMC7804423 DOI: 10.1038/s41598-020-80802-3] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/13/2020] [Accepted: 12/29/2020] [Indexed: 12/14/2022] Open

Martin-Nuñez GM, Cornejo-Pareja I, Clemente-Postigo M, Tinahones FJ. Gut Microbiota: The Missing Link Between Helicobacter pylori Infection and Metabolic Disorders? Front Endocrinol (Lausanne) 2021;12:639856. [PMID: 34220702 PMCID: PMC8247771 DOI: 10.3389/fendo.2021.639856] [Citation(s) in RCA: 28] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/10/2020] [Accepted: 05/17/2021] [Indexed: 12/14/2022] Open

Abstract

Helicobacter pylori (H. pylori) is a gram-negative bacterium that infects approximately 4.4 billion individuals worldwide. Although the majority of infected individuals remain asymptomatic, this bacterium colonizes the gastric mucosa causing the development of various clinical conditions as peptic ulcers, chronic gastritis and gastric adenocarcinomas and mucosa-associated lymphoid tissue lymphomas, but complications are not limited to gastric ones. Extradigestive pathologies, including metabolic disturbances such as diabetes, obesity and nonalcoholic fatty liver disease, have also been associated with H. pylori infection. However, the underlying mechanisms connecting H. pylori with extragastric metabolic diseases needs to be clarified. Notably, the latest studies on the topic have confirmed that H. pylori infection modulates gut microbiota in humans. Damage in the gut bacterial community (dysbiosis) has been widely related to metabolic dysregulation by affecting adiposity, host energy balance, carbohydrate metabolism, and hormonal modulation, among others. Taking into account that Type 2 diabetic patients are more prone to be H. pylori positive, gut microbiota emerges as putative key factor responsible for this interaction. In this regard, the therapy of choice for H. pylori eradication, based on proton pump inhibitor combined with two or more antibiotics, also alters gut microbiota composition, but consequences on metabolic health of the patients has been scarcely explored. Recent studies from our group showed that, despite decreasing gut bacterial diversity, conventional H. pylori eradication therapy is related to positive changes in glucose and lipid profiles. The mechanistic insights explaining these effects should also be addressed in future research. This review will deal with the role of gut microbiota as the linking factor between H. pylori infection and metabolic diseases, and discussed the impact that gut bacterial modulation by H. pylori eradication treatment can also have in host's metabolism. For this purpose, new evidence from the latest human studies published in more recent years will be analyzed.

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Chen CC, Liou JM, Lee YC, Hong TC, El-Omar EM, Wu MS. The interplay between Helicobacter pylori and gastrointestinal microbiota. Gut Microbes 2021;13:1-22. [PMID: 33938378 PMCID: PMC8096336 DOI: 10.1080/19490976.2021.1909459] [Citation(s) in RCA: 90] [Impact Index Per Article: 22.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/02/2020] [Revised: 03/10/2021] [Accepted: 03/19/2021] [Indexed: 02/07/2023] Open

Diagnosis of Helicobacter pylori infection: Progress and challenges. Enferm Infecc Microbiol Clin 2020;38:407-409. [DOI: 10.1016/j.eimc.2020.09.008] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2020] [Revised: 09/03/2020] [Accepted: 09/17/2020] [Indexed: 02/07/2023]