ORIGINAL ARTICLE
Fifth Chinese National Consensus Report on the management of Helicobacter pylori infection
Wen Zhong Liu,
Yong Xie,
Hong Lu,
Hong Cheng,
Zhi Rong Zeng,
Li Ya Zhou,
Ye Chen,
Jiang Bin Wang,
Yi Qi Du,
Nong Hua Lu,
on behalf of
Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer,
Wen Zhong Liu
Department of Gastroenterology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorYong Xie
Department of Gastroenterology, First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China
Search for more papers by this authorHong Lu
Department of Gastroenterology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorHong Cheng
Department of Gastroenterology, Peking University First Hospital, Beijing, China
Search for more papers by this authorZhi Rong Zeng
Division of Gastroenterology, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, Guangdong Province, China
Search for more papers by this authorLi Ya Zhou
Department of Gastroenterology, Peking University Third Hospital, Beijing, China
Search for more papers by this authorYe Chen
Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China
Search for more papers by this authorJiang Bin Wang
Department of Gastroenterology, China-Japan Friendship Hospital, Jilin University, Changchun, Jilin Province, China
Search for more papers by this authorYi Qi Du
Department of Gastroenterology, Changhai Hospital, Second Military Medical University, Shanghai, China
Search for more papers by this authorCorresponding Author
Nong Hua Lu
Department of Gastroenterology, First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China
Correspondence
Nong Hua Lu, Department of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China.
Email: lunonghua@163.com
Search for more papers by this authorChinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer
Search for more papers by this authorWen Zhong Liu,
Yong Xie,
Hong Lu,
Hong Cheng,
Zhi Rong Zeng,
Li Ya Zhou,
Ye Chen,
Jiang Bin Wang,
Yi Qi Du,
Nong Hua Lu,
on behalf of
Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer,
Wen Zhong Liu
Department of Gastroenterology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorYong Xie
Department of Gastroenterology, First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China
Search for more papers by this authorHong Lu
Department of Gastroenterology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorHong Cheng
Department of Gastroenterology, Peking University First Hospital, Beijing, China
Search for more papers by this authorZhi Rong Zeng
Division of Gastroenterology, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, Guangdong Province, China
Search for more papers by this authorLi Ya Zhou
Department of Gastroenterology, Peking University Third Hospital, Beijing, China
Search for more papers by this authorYe Chen
Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China
Search for more papers by this authorJiang Bin Wang
Department of Gastroenterology, China-Japan Friendship Hospital, Jilin University, Changchun, Jilin Province, China
Search for more papers by this authorYi Qi Du
Department of Gastroenterology, Changhai Hospital, Second Military Medical University, Shanghai, China
Search for more papers by this authorCorresponding Author
Nong Hua Lu
Department of Gastroenterology, First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China
Correspondence
Nong Hua Lu, Department of Gastroenterology, The First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China.
Email: lunonghua@163.com
Search for more papers by this authorChinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer
Search for more papers by this authorAbstract
Background
Since the ‘Fourth Chinese National Consensus Report on the management of H. pylori infection’ was published in 2012, three important consensuses (Kyoto global consensus report on H. pylori gastritis, The Toronto Consensus for the Treatment of H. pylori Infection in Adults and Management of H. pylori infection—the Maastricht V/Florence Consensus Report) have been published regarding the management of H. pylori infection.
Materials and Methods
A Delphi method was adopted to develop the consensus of relevant ‘statements’. First, the established ‘statements’ were sent to experts via email. Second, after undergoing two rounds of consultation, the initial statements were discussed face to face and revised in the conference item by item on 16 December 2016. Finally, 21 core members of conferees participated in the final vote of statements. Voting for each statement was performed using an electronic system with levels of agreements shown on the screen in real time.
Results
Consensus contents contained a total of 48 “statements” and related 6 parts, including indications for H. pylori eradication, diagnosis, treatment, H. pylori and gastric cancer, H. pylori infection in special populations, H. pylori and gastrointestinal microbiota.
Conclusions
Recommendations are provided on the basis of the best available evidence.
REFERENCES
- 1 Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer. Fourth Chinese National Consensus Report on the management of Helicobacter pylori infection. Chin J Dig Dis. 2012; 32: 655-661.
- 2Sugano K, Tack J, Kuipers EJ, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015; 64: 1353-1367.
- 3Fallone CA, Chiba N, van Zanten SV, et al. The Toronto consensus for the treatment of Helicobacter pylori infection in adults. Gastroenterology. 2016; 151: 51-69.
- 4Malfertheiner P, Megraud F, O'Morain CA, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence consensus report. Gut. 2017; 66: 6-30.
- 5 Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer. The conference summary regarding Kyoto global consensus report on Helicobacter pylori gastritis. Chin J Dig Dis. 2016; 36: 53-57.
- 6Jiang ZM, Zhan SY, Jia XW, et al. The basic approach and process of formulating guidelines about clinical diagnosis and treatment. Chinese J Med. 2016; 96: 250253.
- 7Qaseem A, Snow V, Owens DK, et al. The development of clinical practice guidelines and guidance statements of the American College of Physicians: summary of methods. Ann Intern Med. 2010; 153: 194-199.
- 8Sipponen P. Natural history of gastritis and its relationship to peptic ulcer disease. Digestion. 1992; 51(Suppl 1): 70-75.
- 9Moayyedi P, Forman D, Braunholtz D, et al. The proportion of upper gastrointestinal symptoms in the community associated with Helicobacter pylori, lifestyle factors, and nonsteroidal anti-inflammatory drugs. Leeds HELP Study Group. Am J Gastroenterol. 2000; 95: 1448-1455.
- 10Sugano K. Screening of gastric cancer in Asia. Best Pract Res Clin Gastroenterol. 2015 Dec; 29: 895-905.
- 11Sonnenberg A, Lash RH, Genta RM. A national study of Helicobacter pylori infection in gastric biopsy specimens. Gastroenterology. 2010; 139: 1894-1901.
- 12Warren JR. Gastric pathology associated with Helicobacter pylori. Gastroenterol Clin North Am. 2000; 29: 705-751.
- 13Marshall BJ, Armstrong JA, McGechie DB, et al. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust. 1985; 142: 436-439.
- 14Morris A, Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol. 1987; 82: 192-199.
- 15Leja M, Axon A, Brenner H. Epidemiology of Helicobacter pylori infection. Helicobacter. 2016; 21(Suppl 1): 3-7.
- 16Van der Hulst RW, Tytgat GN. Helicobacter pylori and peptic ulcer disease. Scand J Gastroenterol Suppl. 1996; 220: 10-18 Review.
- 17Nakamura S, Sugiyama T, Matsumoto T, et al. Long-term clinical outcome of gastric MALT lymphoma after eradication of Helicobacter pylori: a multicentre cohort follow-up study of 420 patients in Japan. Gut. 2012; 61: 507-513.
- 18Nagy P, Johansson S, Molloy-Bland M. Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut Pathog. 2016; 8: 8.
- 19Gisbert JP, Calvet X. Helicobacter pylori “Test-and-Treat” strategy for management of dyspepsia: a comprehensive review. Clin Transl Gastroenterol. 2013; 4: e32.
- 20Ford AC, Qume M, Moayyedi P, et al. Helicobacter pylori “test and treat” or endoscopy for managing dyspepsia: an individual patient data meta-analysis. Gastroenterology. 2005; 128: 1838-1844.
- 21Liu WZ. The importance of H. pylori eradication in the management of dyspepsia. Chin J Dig Dis. 2016; 36: 2-4.
- 22Chen SL, Gwee KA, Lee JS, et al. Systematic review with meta-analysis: prompt endoscopy as the initial management strategy for uninvestigated dyspepsia in Asia. Aliment Pharmacol Ther. 2015; 41: 239-252.
- 23Talley NJ, Vakil NB, Moayyedi P. American gastroenterological association technical review on the evaluation of dyspepsia. Gastroenterology. 2005; 129: 1756-1780.
- 24Suzuki H, Moayyedi P. Helicobacter pylori infection in functional dyspepsia. Nat Rev Gastroenterol Hepatol. 2013; 10: 168-174.
- 25Sugano K. Should we still subcategorize Helicobacter pylori -associated dyspepsia as functional disease? J Neurogastroenterol Motil. 2011; 17: 366-371.
- 26Stanghellini V, Chan FK, Hasler WL, et al. Gastroduodenal disorders. Gastroenterology. 2016; 150: 1380-1392.
- 27Yamada T, Searle JG, Ahnen D. NIH Consensus conference. Helicobacter pylori in peptic ulcer disease. NIH consensus development panel on Helicobacter pylori in peptic ulcer disease. JAMA. 1994; 272: 65-69.
- 28Gisbert JP, Calvet X, Cosme A, et al. Long-term follow-up of 1000 patients cured of Helicobacter pylori infection following an episode of peptic ulcer bleeding. Am J Gastroenterol. 2012; 107: 1197-1204.
- 29Enserink M. Physiology or medicine. Triumph of the ulcer-bug theory. Science. 2005; 310: 34-35.
- 30Nakamura S, Matsumoto T. Treatment strategy for gastric mucosa-associated lymphoid tissue lymphoma. Gastroenterol Clin North Am. 2015; 44: 649-660.
- 31Fischbach W. Gastric MALT lymphoma – update on diagnosis and treatment. Best Pract Res Clin Gastroenterol. 2014; 28: 1069-1077.
- 32Huang JQ, Sridhar S, Hunt RH. Role of Helicobacter pylori infection and non-steroidal anti-inflammatory drugs in peptic-ulcer disease: a meta-analysis. Lancet. 2002; 359: 14-22.
- 33Vergara M, Catalán M, Gisbert JP, et al. Meta-analysis: role of Helicobacter pylori eradication in the prevention of peptic ulcer in NSAID users. Aliment Pharmacol Ther. 2005; 21: 1411-1418.
- 34Melcarne L, García-Iglesias P, Calvet X. Management of NSAID-associated peptic ulcer disease. Expert Rev Gastroenterol Hepatol. 2016; 10: 723-733.
- 35Sostres C, Carrera-Lasfuentes P, Benito R, et al. Peptic ulcer bleeding risk. The role of Helicobacter pylori infection in NSAID/low-dose aspirin users. Am J Gastroenterol. 2015; 110: 684-689.
- 36Hunt RH, Bazzoli F. Review article: should NSAID/low-dose aspirin takers be tested routinely for H. pylori infection and treated if positive? Implications for primary risk of ulcer and ulcer relapse after initial healing. Aliment Pharmacol Ther. 2004; 19(Suppl 1): 9-16 Review.
- 37Chan FKL, Ching JYL, Suen BY, et al. Effects of Helicobacter pylori infection on long-term risk of peptic ulcer bleeding in low-dose aspirin users. Gastroenterology. 2013; 144: 528-535.
- 38Kuipers EJ, Uyterlinde AM, Peña AS, et al. Increase of Helicobacter pylori -associated corpus gastritis during acid suppressive therapy: implications for long-term safety. Am J Gastroenterol. 1995; 90: 1401-1406.
- 39Lundell L, Havu N, Miettinen P, et al. Changes of gastric mucosal architecture during long-term omeprazole therapy: results of a randomized clinical trial. Aliment Pharmacol Ther. 2006; 23: 639-647.
- 40Schenk BE, Kuipers EJ, Nelis GF, et al. Effect of Helicobacter pylori eradication on chronic gastritis during omeprazole therapy. Gut. 2000; 46: 615-621.
- 41Yuan W, Li Y, Yang K, et al. Iron deficiency anemia in Helicobacter pylori infection: meta-analysis of randomized controlled trials. Scand J Gastroenterol. 2010; 45: 665-676.
- 42Queiroz DMM, Harris PR, Sanderson IR, et al. Iron status and Helicobacter pylori infection in symptomatic children: an international multi-centered study. PLoS ONE. 2013; 8: e68833.
- 43Goddard AF, James MW, McIntyre AS, et al. Guidelines for the management of iron deficiency anaemia. Gut. 2011; 60: 1309-1316.
- 44Stasi R, Sarpatwari A, Segal JB, et al. Effects of eradication of Helicobacter pylori infection in patients with immune thrombocytopenic purpura: a systematic review. Blood. 2009; 113: 1231-1240.
- 45Russo G, Miraglia V, Branciforte F, et al. Effect of eradication of Helicobacter pylori in children with chronic immune thrombocytopenia: a prospective, controlled, multicenter study. Pediatr Blood Cancer. 2011; 56: 273-278.
- 46Provan D, Stasi R, Newland AC, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010; 115: 168-186.
- 47Neunert C, Lim W, Crowther M, et al. The American Society of Hematology 2011 evidence-based practice guideline for immune thrombocytopenia. Blood. 2011; 117: 4190-4207.
- 48Stabler SP. Clinical practice. Vitamin B12 deficiency. N Engl J Med. 2013; 368: 149-160.
- 49Malfertheiner P. The intriguing relationship of Helicobacter pylori infection and acid secretion in peptic ulcer disease and gastric cancer. Dig Dis. 2011; 29: 459-464.
- 50Haruma K, Mihara M, Okamoto E, et al. Eradication of Helicobacter pylori increases gastric acidity in patients with atrophic gastritis of the corpus-evaluation of 24-h pH monitoring. Aliment Pharmacol Ther. 1999; 13: 155-162.
- 51Iijima K, Ohara S, Sekine H, et al. Changes in gastric acid secretion assayed by endoscopic gastrin test before and after Helicobacter pylori eradication. Gut. 2000; 46: 20-26.
- 52Kandulski A, Malfertheiner P. Helicobacter pylori and gastroesophageal reflux disease. Curr Opin Gastroenterol. 2014; 30: 402-407.
- 53Franceschi F, Tortora A, Gasbarrini G, et al. Helicobacter pylori and extragastric diseases. Helicobacter. 2014; 19(Suppl 1): 52-58.
- 54Hughes WS. An hypothesis: the dramatic decline in heart attacks in the United States is temporally related to the decline in duodenal ulcer disease and Helicobacter pylori infection. Helicobacter. 2014; 19: 239-241.
- 55Bu XL, Yao XQ, Jiao SS, et al. A study on the association between infectious burden and Alzheimer's disease. Eur J Neurol. 2015; 22: 1519-1525.
- 56Bu XL, Wang X, Xiang Y, et al. The association between infectious burden and Parkinson's disease: a case-control study. Parkinsonism Relat Disord. 2015; 21: 877-881.
- 57Papastergiou V, Karatapanis S, Georgopoulos SD. Helicobacter pylori and colorectal neoplasia: is there a causal link? World J Gastroenterol. 2016; 22: 649-658.
- 58Zhang Y, Du T, Chen X, Yu X, Tu L, Zhang C. Association between Helicobacter pylori infection and overweight or obesity in a Chinese population. J Infect Dev Ctries. 2015; 9: 945-953.
- 59Daugule I, Zavoronkova J, Santare D. Helicobacter pylori and allergy: update of research. World J Methodol. 2015; 5: 203-211.
- 60Rokkas T, Pistiolas D, Sechopoulos P, et al. Relationship between Helicobacter pylori infection and esophageal neoplasia: a meta-analysis. Clin Gastroenterol Hepatol. 2007; 5: 1413-1417.
- 61Lender N, Talley NJ, Enck P, et al. Review article: associations between Helicobacter pylori and obesity–an ecological study. Aliment Pharmacol Ther. 2014; 40: 24-31.
- 62Hojo M, Miwa H, Ohkusa T, et al. Alteration of histological gastritis after cure of Helicobacter pylori infection. Aliment Pharmacol Ther. 2002; 16: 1923-1932.
- 63Asaka M, Sugiyama T, Nobuta A, Kato M, Takeda H, Graham DY. Atrophic gastritis and intestinal metaplasia in Japan: results of a large multicenter study. Helicobacter. 2001; 6: 294-299.
- 64Venerito M, Malfertheiner P. Preneoplastic conditions in the stomach: always a point of no return? Dig Dis. 2015; 33: 5-10.
- 65Zhou L, Lin S, Ding S, et al. Relationship of Helicobacter pylori eradication with gastric cancer and gastric mucosal histological changes: a 10-year follow-up study. Chin Med J (Engl). 2014; 127: 1454-1458.
- 66Wang J, Xu L, Shi R, et al. Gastric atrophy and intestinal metaplasia before and after Helicobacter pylori eradication: a meta-analysis. Digestion 2011; 83: 253.
- 67Liu KS, Wong IO, Leung WK. Helicobacter pylori associated gastric intestinal metaplasia: treatment and surveillance. World J Gastroenterol. 2016; 22: 1311-1320.
- 68Ferwana M, Abdulmajeed I, Alhajiahmed A, et al. Accuracy of urea breath test in Helicobacter pylori infection: meta-analysis. World J Gastroenterol. 2015; 21: 1305-1314.
- 69Wang YK, Kuo FC, Liu CJ, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015; 21: 11221-11235.
- 70Gisbert JP, Pajares JM. Review article: 13C-urea breath test in the diagnosis of Helicobacter pylori infection—a critical review. Aliment Pharmacol Ther. 2004; 20: 1001-1017.
- 71Tian XY, Zhu H, Zhao J, et al. Diagnostic performance of urea breath test, rapid urea test, and histology for Helicobacter pylori infection in patients with partial gastrectomy: a meta-analysis. J Clin Gastroenterol. 2012; 46: 285-292.
- 72Gisbert JP, de la Morena F, Abraira V. Accuracy of monoclonal stool antigen test for the diagnosis of H. pylori infection: a systematic review and meta-analysis. Am J Gastroenterol 2006; 101: 1921-1930.
- 73Atkinson NS, Braden B. Helicobacter pylori infection: diagnostic strategies in primary diagnosis and after therapy. Dig Dis Sci. 2016; 61: 19-24.
- 74Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med. 2015; 3: 9.
- 75 Chinese Society of Gastroenterolog, Fang JY, Liu WZ, et al. The management of chronic gastritis in China. Chin J Dig Dis. 2013; 33: 5-16
- 76Lahner E, Esposito G, Zullo A, et al. Gastric precancerous conditions and Helicobacter pylori infection in dyspeptic patients with or without endoscopic lesions. Scand J Gastroenterol. 2016; 51: 1294-1298.
- 77Yang YX, Brill J, Krishnan P, et al. American gastroenterological association institute guideline on the role of upper gastrointestinal biopsy to evaluate dyspepsia in the adult patient in the absence of visible mucosal lesions. Gastroenterology. 2015; 149: 1082-1087.
- 78Sipponen P, Price AB. The Sydney System for classification of gastritis 20 years ago. J Gastroenterol Hepatol. 2011; 26(Suppl 1): 31-34.
- 79Lash JG, Genta RM. Adherence to the Sydney System guidelines increases the detection of Helicobacter gastritis and intestinal metaplasia in 400738 sets of gastric biopsies. Aliment Pharmacol Ther. 2013; 38: 424-431.
- 80Panarelli NC, Ross DS, Bernheim OE, et al. Utility of ancillary stains for Helicobacter pylori in near-normal gastric biopsies. Hum Pathol. 2015; 46: 397-403.
- 81Batts KP, Ketover S, Kakar S, et al. Appropriate use of special stains for identifying Helicobacter pylori: recommendations from the Rodger C. Haggitt Gastrointestinal Pathology Society. Am J Surg Pathol. 2013; 37: e12-e22.
- 82Smith SM, O'Morain C, McNamara D. Antimicrobial susceptibility testing for Helicobacter pylori in times of increasing antibiotic resistance. World J Gastroenterol. 2014; 20: 9912-9921.
- 83Ji R, Li YQ. Diagnosing Helicobacter pylori infection in vivo by novel endoscopic techniques. World J Gastroenterol. 2014; 20: 9314-9320.
- 84Qi Q, Guo C, Ji R, et al. Diagnostic performance of magnifying endoscopy for Helicobacter pylori infection: a meta-analysis. PLoS ONE. 2016; 11: e0168201.
- 85Zhang YX, Zhou LY, Song ZQ, et al. Primary antibiotic resistance of Helicobacter pylori strains isolated from patients with dyspeptic symptoms in Beijing: a prospective serial study. World J Gastroenterol. 2015; 21: 2786-2792.
- 86Su P, Li Y, Li H, et al. Antibiotic resistance of Helicobacter pylori isolated in the Southeast Coastal Region of China. Helicobacter. 2013; 18: 274-279.
- 87Bai P, Zhou LY, Xiao XM, et al. Susceptibility of Helicobacter pylori to antibiotics in Chinese patients. J Dig Dis. 2015; 16: 464-470.
- 88Zhou L, Zhang J, Chen M, et al. A comparative study of sequential therapy and standard triple therapy for Helicobacter pylori infection: a randomized multicenter trial. Am J Gastroenterol. 2014; 109: 535-541.
- 89Zhou L, Zhang J, Song Z, et al. Tailored versus triple plus bismuth or concomitant therapy as initial Helicobacter pylori treatment: a randomized trial. Helicobacter. 2016; 21: 91-99.
- 90Song Z, Zhou L, Zhang J, He L, Bai P, Xue Y. Hybrid therapy as first-line regimen for Helicobacter pylori eradication in populations with high antibiotic resistance rates. Helicobacter. 2016; 21: 382-388.
- 91Zhang W, Chen Q, Liang X, et al. Bismuth, lansoprazole, amoxicillin and metronidazole or clarithromycin as first-line Helicobacter pylori therapy. Gut. 2015; 64: 1715-1720.
- 92Xie C, Lu NH. Review: clinical management of Helicobacter pylori infection in China. Helicobacter. 2015; 20: 1-10.
- 93Liang X, Xu X, Zheng Q, et al. Efficacy of bismuth-containing quadruple therapies for clarithromycin-, metronidazole-, and fluoroquinolone-resistant Helicobacter pylori infections in a prospective study. Clin Gastroenterol Hepatol. 2013; 11: 802-807.
- 94Chen Q, Zhang W, Fu Q, et al. Rescue therapy for Helicobacter pylori eradication: a randomized non-inferiority trial of amoxicillin or tetracycline in bismuth quadruple therapy. Am J Gastroenterol. 2016; 111: 1736-1742.
- 95Malfertheiner P, Megraud F, O'Morain CA, et al. Management of Helicobacter pylori infection–the Maastricht IV/Florence Consensus Report. Gut. 2012; 61: 646-664.
- 96Graham DY, Dore MP. Helicobacter pylori therapy: a paradigm shift. Expert Rev Anti Infect Ther. 2016; 14: 577-585.
- 97Graham DY, Lee SY. How to effectively use bismuth quadruple therapy: the good, the bad, and the ugly. Gastroenterol Clin North Am. 2015; 44: 537-563.
- 98Lind T, Veldhuyzen van Zanten S, Unge P, et al. Eradication of Helicobacter pylori using one-week triple therapies combining omeprazole with two antimicrobials: the MACH I Study. Helicobacter. 1996; 1: 138-144.
- 99Current European concepts in the management of Helicobacter pylori infection. The Maastricht Consensus Report. European Helicobacter pylori Study Group. Gut 1997; 41: 8-13.
- 100Graham DY, Fischbach L. Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut. 2010; 59: 1143-1153.
- 101Wang B, Lv ZF, Wang YH, et al. Standard triple therapy for Helicobacter pylori infection in China: a meta-analysis. World J Gastroenterol. 2014; 20: 14973-14985.
- 102Sun Q, Liang X, Zheng Q, et al. High efficacy of 14-day triple therapy-based, bismuth-containing quadruple therapy for initial Helicobacter pylori eradication. Helicobacter. 2010; 15: 233-238.
- 103Liao J, Zheng Q, Liang X, et al. Effect of fluoroquinolone resistance on 14-day levofloxacin triple and triple plus bismuth quadruple therapy. Helicobacter. 2013; 18: 373-377.
- 104Lu H, Zhang W, Graham DY. Bismuth-containing quadruple therapy for Helicobacter pylori: lessons from China. Eur J Gastroenterol Hepatol. 2013; 25: 1134-1140.
- 105Xie Y, Zhu Y, Zhou H, et al. Furazolidone-based triple and quadruple eradication therapy for Helicobacter pylori infection. World J Gastroenterol. 2014; 20: 11415-11421.
- 106Liu WZ, Xie Y, Cheng H, et al. Fourth Chinese National Consensus Report on the management of Helicobacter pylori infection. J Dig Dis. 2013; 14: 211-221.
- 107Lv ZF, Wang FC, Zheng HL, et al. Meta-analysis: is combination of tetracycline and amoxicillin suitable for Helicobacter pylori infection? World J Gastroenterol. 2015; 21: 2522-2533.
- 108Gisbert JP, Romano M, Gravina AG, et al. Helicobacter pylori second-line rescue therapy with levofloxacin- and bismuth-containing quadruple therapy, after failure of standard triple or non-bismuth quadruple treatments. Aliment Pharmacol Ther. 2015; 41: 768-775.
- 109Ergül B, Doğan Z, Sarikaya M, et al. The efficacy of two-week quadruple first-line therapy with bismuth, lansoprazole, amoxicillin, clarithromycin on Helicobacter pylori eradication: a prospective study. Helicobacter. 2013; 18: 454-458.
- 110Srinarong C, Siramolpiwat S, Wongcha-um A, et al. Improved eradication rate of standard triple therapy by adding bismuth and probiotic supplement for Helicobacter pylori treatment in Thailand. Asian Pac J Cancer Prev. 2014; 15: 9909-9913.
- 111Dore MP, Lu H, Graham DY. Role of bismuth in improving Helicobacter pylori eradication with triple therapy. Gut. 2016; 65: 870-878.
- 112Ford AC, Malfertheiner P, Giguere M, et al. Adverse events with bismuth salts for Helicobacter pylori eradication: systematic review and meta-analysis. World J Gastroenterol. 2008; 14: 7361-7370.
- 113Lim SG, Park RW, Shin SJ, et al. The relationship between the failure to eradicate Helicobacter pylori and previous antibiotics use. Dig Liver Dis. 2016; 48: 385-390.
- 114Chen PY, Wu MS, Chen CY, et al. Systematic review with meta-analysis: the efficacy of levofloxacin triple therapy as the first- or second-line treatments of Helicobacter pylori infection. Aliment Pharmacol Ther. 2016; 44: 427-437.
- 115Cosme A, Lizasoan J, Montes M, et al. Antimicrobial susceptibility-guided therapy versus empirical concomitant therapy for eradication of Helicobacter pylori in a region with high rate of clarithromycin resistance. Helicobacter. 2016; 21: 29-34.
- 116Graham DY, Laine L. The Toronto Helicobacter pylori consensus in context. Gastroenterology. 2016; 151: 9-12.
- 117López-Góngora S, Puig I, Calvet X, et al. Systematic review and meta-analysis: susceptibility-guided versus empirical antibiotic treatment for Helicobacter pylori infection. J Antimicrob Chemother. 2015; 70: 2447-2455.
- 118Puig I, López-Góngora S, Calvet X, et al. Systematic review: third-line susceptibility-guided treatment for Helicobacter pylori infection. Therap Adv Gastroenterol. 2016; 9: 437-448.
- 119Chen H, Dang Y, Zhou X, Liu B, Liu S, Zhang G. Tailored therapy versus empiric chosen treatment for Helicobacter pylori eradication: a meta-analysis. Medicine (Baltimore). 2016; 95: e2750.
- 120Labenz J. Current role of acid suppressants in Helicobacter pylori eradication therapy. Best Pract Res Clin Gastroenterol. 2001; 15: 413-431.
- 121Gisbert JP. Potent gastric acid inhibition in Helicobacter pylori eradication. Drugs. 2005; 65(Suppl 1): 83-96.
- 122Kuo CH, Lu CY, Shih HY, et al. CYP2C19 polymorphism influences Helicobacter pylori eradication. World J Gastroenterol. 2014; 20: 16029-16036.
- 123Uotani T, Miftahussurur M, Yamaoka Y. Effect of bacterial and host factors on Helicobacter pylori eradication therapy. Expert Opin Ther Targets. 2015; 19: 1637-1650.
- 124Sahara S, Sugimoto M, Uotani T, et al. Twice-daily dosing of esomeprazole effectively inhibits acid secretion in CYP2C19 rapid metabolisers compared with twice-daily omeprazole, rabeprazole or lansoprazole. Aliment Pharmacol Ther. 2013; 38: 1129-1137.
- 125Hong J, Shu X, Liu D. Antibiotic resistance and CYP2C19 polymorphisms affect the efficacy of concomitant therapies for Helicobacter pylori infection: an open-label, randomized, single-centre clinical trial. J Antimicrob Chemother. 2016; 71: 2280-2285.
- 126Anagnostopoulos GK, Tsiakos S, Margantinis G, et al. Esomeprazole versus omeprazole for the eradication of Helicobacter pylori infection: results of a randomized controlled study. J Clin Gastroenterol. 2004; 38: 503-506.
- 127McNicholl AG, Linares PM, Nyssen OP, et al. Meta-analysis: esomeprazole or rabeprazole vs. first-generation pump inhibitors in the treatment of Helicobacter pylori infection. Aliment Pharmacol Ther. 2012; 36: 414-425.
- 128Akazawa Y, Fukuda D, Fukuda Y. Vonoprazan-based therapy for Helicobacter pylori eradication: experience and clinical evidence. Therap Adv Gastroenterol. 2016; 9: 845-852 Review.
- 129Hsu PI, Chen WC, Tsay FW, et al. Ten-day Quadruple therapy comprising proton-pump inhibitor, bismuth, tetracycline, and levofloxacin achieves a high eradication rate for Helicobacter pylori infection after failure of sequential therapy. Helicobacter. 2014; 19: 74-79.
- 130Liu WZ, Lyu BM, Xiao SD, et al. Clarithromycin-containing triple therapy in eradicating H. pylori. Chin J Internal Med. 1996; 35: 803-806.
- 131Malfertheiner P, Megraud F, O'Morain C, et al. Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut. 2007; 56: 772-781.
- 132Assem M, El Azab G, Rasheed MA, et al. Efficacy and safety of Levofloxacin, Clarithromycin and Esomeprazol as first line triple therapy for Helicobacter pylori eradication in Middle East. Prospective, randomized, blind, comparative, multicenter study. Eur J Intern Med 2010; 21: 310-314.
- 133Fock KM, Talley N, Moayyedi P, et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol. 2008; 23: 351-365.
- 134Shiotani A, Cen P, Graham DY. Eradication of gastric cancer is now both possible and practical. Semin Cancer Biol. 2013; 23: 492-501.
- 135Herrero R, Park JY, Forman D. The fight against gastric cancer – the IARC Working Group report. Best Pract Res Clin Gastroenterol. 2014; 28: 1107-1114.
- 136Plummer M, de Martel C, Vignat J, et al. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health. 2016; 4: e609-e616.
- 137Tan RY, Ngeow J. Hereditary diffuse gastric cancer: what the clinician should know. World J Gastrointest Oncol. 2015; 7: 153-160.
- 138Wong BC, Lam SK, Wong WM, et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004; 291: 187-194.
- 139Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta analysis of randomised controlled trials. BMJ. 2014; 348: g3174.
- 140Mansour S, Pee D, Blot WJ, et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst. 2012; 104: 488-492.
- 141Li WQ, Ma JL, Zhang L, et al. Effects of Helicobacter pylori treatment on gastric cancer incidence and mortality in subgroups. J Natl Cancer Inst. 2014; 106:pii: dju116. https://doi.org/10.1093/jnci/dju116
10.1093/jnci/dju116 Google Scholar
- 142Agréus L, Kuipers EJ, Kupcinskas L, et al. Rationale in diagnosis and screening of atrophic gastritis with stomach-specific plasma biomarkers. Scand J Gastroenterol. 2012; 47: 136-147.
- 143Cao Q, Ran Z, Xiao S. Screening of atrophic gastritis and gastric cancer using serum Pepsinogen, Gastrin-17 and Helicobacter pylori IgG antibodies. Chin J Gastroenterol. 2006; 11: 388-394.
- 144Yamaguchi Y, Nagata Y, Hiratsuka R, et al. Gastric cancer screening by combined assay for serum anti- Helicobacter pylori IgG antibody and serum pepsinogen levels-the ABC method. Digestion. 2016; 93: 13-18.
- 145Lee YC, Chen TH, Chiu HM, et al. The benefit of mass eradication of Helicobacter pylori infection: a community-based study of gastric cancer prevention. Gut. 2013; 62: 676-682.
- 146Ford AC, Forman D, Hunt R, Yuan Y, Moayyedi P. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev 2015; 7: CD005583.
- 147 Chinese Society of Gastrointestinal Endoscopy, Chinese Anti-Cancer Association, Committee on tumor endoscopy. Consensus reports on the early gastric cancer screening and management of endoscopy. Chin J Dig Dis. 2014; 34: 433-448
- 148Shichijo S, Hirata Y, Niikura R, et al. Histologic intestinal metaplasia and endoscopic atrophy are predictors of gastric cancer development after Helicobacter pylori eradication. Gastrointest Endosc. 2016; 84: 618-624.
- 149Rugge M. Gastric cancer risk in patients with Helicobacter pylori infection and following its eradication. Gastroenterol Clin North Am 2015; 44: 609-624.
- 150Zhou Y, Li HY, Zhang JJ, et al. Operative link on gastritis assessment stage is an appropriate predictor of early gastric cancer. World J Gastroenterol 2016; 7: 22.
- 151Rugge M, de Boni M, Pennelli G, et al. Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther. 2010; 31: 1104-1111.
- 152Graham DY. Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology. 2015; 148: 719-731.
- 153Lage J, Uedo N, Dinis-Ribeiro M, et al. Surveillance of patients with gastric precancerous conditions. Best Pract Res Clin Gastroenterol. 2016; 30: 913-922.
- 154Forman D, Sierra MS. The current and projected global burden of gastric cancer (IARC Working Group Reports, No. 8). In: IARC Helicobacter pylori Working Group. Helicobacter pylori Eradication as a Strategy for Preventing Gastric Cancer (pp. 5-15). Lyon, France: International Agency for Research on Cancer; 2014.
- 155Kamada T, Haruma K, Ito M, et al. Time trends in Helicobacter pylori infection and atrophic gastritis over 40 years in Japan. Helicobacter. 2015; 20: 192-198.
- 156Wang T, Cai H, Sasazuki S, et al. Fruit and vegetable consumption, Helicobacter pylori antibodies, and gastric cancer risk: A pooled analysis of prospective studies in China, Japan, and Korea. Int J Cancer. 2017; 140: 591-599.
- 157Zeng M, Mao XH, Li JX, et al. Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2015; 386: 1457-1464.
- 158Razavi A, Bagheri N, Azadegan-Dehkordi F, et al. Comparative immune response in children and adults with H. pylori infection. J Immunol Res. 2015; 2015: 315957.
- 159 Chinese Society of Pediatrics, Chinese Study Group on Gastroenterology. Consensus reports on the management of H. pylori infection in Children. Chin J Pediatr. 2015; 53: 496-498.
- 160Malaty HM, Graham DY, Wattigney WA, et al. Natural history of Helicobacter pylori infection in childhood: 12-year follow-up cohort study in a biracial community. Clin Infect Dis. 1999; 28: 279-282.
- 161Sivapalasingam S, Rajasingham A, Macy JT, et al. Recurrence of Helicobacter pylori infection in Bolivian children and adults after a population-based “screen and treat” strategy. Helicobacter. 2014; 19: 343-348.
- 162Vanderpas J, Bontems P, Miendje Deyi VY, Cadranel S. Follow-up of Helicobacter pylori infection in children over two decades (1988–2007): persistence, relapse and acquisition rates. Epidemiol Infect. 2014; 142: 767-775.
- 163Koletzko S, Jones NL, Goodman KJ, et al. Evidence-based guidelines from ESPGHAN and NASPGHAN for Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr. 2011; 53: 230-243.
- 164Matsuzaki J, Hayashi R, Arakawa T, et al. Questionnaire-based survey on diagnostic and therapeutic endoscopies and H. pylori eradication for elderly patients in East Asian countries. Digestion. 2016; 93: 93-102.
- 165Salles N, Mégraud F. Current management of Helicobacter pylori infections in the elderly. Expert Rev Anti Infect Ther. 2007; 5: 845-856.
- 166Pea F. Antimicrobial treatment of bacterial infections in frail elderly patients: the difficult balance between efficacy, safety and tolerability. Curr Opin Pharmacol. 2015; 24: 18-22.
- 167Yap TW, Gan HM, Lee YP, et al. Helicobacter pylori eradication causes perturbation of the human gut microbiome in young adults. PLoS ONE. 2016; 11: e0151893.
- 168Ladirat SE, Schols HA, Nauta A, et al. High-throughput analysis of the impact of antibiotics on the human intestinal microbiota composition. J Microbiol Methods. 2013; 92: 387-397.
- 169Blaser MJ. Antibiotic use and its consequences for the normal microbiome. Science. 2016; 352: 544-545.
- 170Imase K, Takahashi M, Tanaka A, et al. Efficacy of Clostridium butyricum preparation concomitantly with Helicobacter pylori eradication therapy in relation to changes in the intestinal microbiota. Microbiol Immunol. 2008; 52: 156-161.
- 171Oh B, Kim JW, Kim BS. Changes in the functional potential of the gut microbiome following probiotic supplementation during Helicobacter pylori treatment. Helicobacter. 2016; 21: 493-503.
- 172Zhang MM, Qian W, Qin YY, He J, Zhou YH. Probiotics in Helicobacter pylori eradication therapy: a systematic review and meta-analysis. World J Gastroenterol. 2015; 21: 4345-4357.
- 173Lu C, Sang J, He H, et al. Probiotic supplementation does not improve eradication rate of Helicobacter pylori infection compared to placebo based on standard therapy: a meta-analysis. Sci Rep. 2016; 21: 23522.
- 174Goli YD, Moniri R. Efficacy of probiotics as an adjuvant agent in eradication of Helicobacter pylori infection and associated side effects. Benef Microbes. 2016; 7: 519.
- 175McFarland LV, Huang Y, Wang L, Malfertheiner P. Systematic review and meta-analysis: multi-strain probiotics as adjunct therapy for Helicobacter pylori eradication and prevention of adverse events. United Eur Gastroenterol J. 2016; 4: 546-561.
