Helicobacter pylori infection
An acceptable H pylorieradication regimen is generally defined as one that reliably offers cure rates of at least 90%.[128]Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidence-based medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol. 2014 Feb;12(2):177-86;e3;discussion e12-3.
http://www.cghjournal.org/article/S1542-3565%2813%2900773-8/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/23751282?tool=bestpractice.com
First-line treatment
Two first-line quadruple eradication regimens, recommended by guidance, have been shown to have cure rates of at least 90%:[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[130]McNicholl AG, Bordin DS, Lucendo A, et al. Combination of bismuth and standard triple therapy eradicates Helicobacter pylori infection in more than 90% of patients. Clin Gastroenterol Hepatol. 2020 Jan;18(1):89-98.
http://www.ncbi.nlm.nih.gov/pubmed/30978536?tool=bestpractice.com
[131]Fallone CA, Chiba N, van Zanten SV, et al. The Toronto consensus for the treatment of Helicobacter pylori infection in adults. Gastroenterology. 2016 Jul;151(1):51-69;e14.
http://www.ncbi.nlm.nih.gov/pubmed/27102658?tool=bestpractice.com
[132]Wang Z, Wu S. Doxycycline-based quadruple regimen versus routine quadruple regimen for rescue eradication of Helicobacter pylori: an open-label control study in Chinese patients. Singapore Med J. 2012 Apr;53(4):273-6.
http://smj.sma.org.sg/5304/5304a7.pdf
http://www.ncbi.nlm.nih.gov/pubmed/22511052?tool=bestpractice.com
[133]Akyildiz M, Akay S, Musoglu A, et al. The efficacy of ranitidine bismuth citrate, amoxicillin and doxycycline or tetracycline regimens as a first line treatment for Helicobacter pylori eradication. Eur J Intern Med. 2009 Jan;20(1):53-7.
http://www.ncbi.nlm.nih.gov/pubmed/19237093?tool=bestpractice.com
[134]Niv Y. Doxycycline in eradication therapy of Helicobacter pylori - a systematic review and meta-analysis. Digestion. 2016;93(2):167-73.
https://www.karger.com/Article/FullText/443683
http://www.ncbi.nlm.nih.gov/pubmed/26849820?tool=bestpractice.com
Proton-pump inhibitor (PPI) (e.g., omeprazole - other PPIs are also suitable) plus amoxicillin plus clarithromycin plus metronidazole
PPI plus bismuth plus metronidazole plus tetracycline (or doxycycline if tetracycline is not available).
Although some guidelines recommend 10 to 14 days of therapy, 14 days of therapy is generally recommended as increasing the duration of treatment improves the eradication rate without significantly increasing adverse events.[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[131]Fallone CA, Chiba N, van Zanten SV, et al. The Toronto consensus for the treatment of Helicobacter pylori infection in adults. Gastroenterology. 2016 Jul;151(1):51-69;e14.
http://www.ncbi.nlm.nih.gov/pubmed/27102658?tool=bestpractice.com
[135]Gisbert JP, McNicholl AG. Optimization strategies aimed to increase the efficacy of H. pylori eradication therapies. Helicobacter. 2017 Aug;22(4).
http://www.ncbi.nlm.nih.gov/pubmed/28464347?tool=bestpractice.com
[136]Alsamman MA, Vecchio EC, Shawwa K, et al. Retrospective analysis confirms tetracycline quadruple as best Helicobacter pylori regimen in the USA. Dig Dis Sci. 2019 Oct;64(10):2893-8.
http://www.ncbi.nlm.nih.gov/pubmed/31187323?tool=bestpractice.com
[137]Sun 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 Jun;15(3):233-8.
http://www.ncbi.nlm.nih.gov/pubmed/20557366?tool=bestpractice.com
[138]Calvet X, García N, López T, et al. A meta-analysis of short versus long therapy with a proton pump inhibitor, clarithromycin and either metronidazole or amoxycillin for treating Helicobacter pylori infection. Aliment Pharmacol Ther. 2000 May;14(5):603-9.
https://onlinelibrary.wiley.com/doi/full/10.1046/j.1365-2036.2000.00744.x?sid=nlm%3Apubmed
http://www.ncbi.nlm.nih.gov/pubmed/10792124?tool=bestpractice.com
[139]Ford A, Moayyedi P. How can the current strategies for Helicobacter pylori eradication therapy be improved? Can J Gastroenterol. 2003 Jun;17 suppl B:36B-40B.
http://www.ncbi.nlm.nih.gov/pubmed/12845349?tool=bestpractice.com
[140]Fuccio L, Minardi ME, Zagari RM, et al. Meta-analysis: duration of first-line proton-pump inhibitor based triple therapy for Helicobacter pylori eradication. Ann Intern Med. 2007 Oct 16;147(8):553-62.
http://www.ncbi.nlm.nih.gov/pubmed/17938394?tool=bestpractice.com
[141]Flores HB, Salvana A, Ang ELR, et al. Duration of proton-pump inhibitor-based triple therapy for Helicobacter pylori eradication: a meta-analysis. Gastroenterology. 2010;138(S-340).[142]Yuan Y, Ford AC, Khan KJ, et al. Optimum duration of regimens for Helicobacter pylori eradication. Cochrane Database Syst Rev. 2013 Dec 11;(12):CD008337.
http://www.ncbi.nlm.nih.gov/pubmed/24338763?tool=bestpractice.com
[143]Liou JM, Chen CC, Lee YC, et al. Systematic review with meta-analysis: 10- or 14-day sequential therapy vs. 14-day triple therapy in the first line treatment of Helicobacter pylori infection. Aliment Pharmacol Ther. 2016 Feb;43(4):470-81.
https://onlinelibrary.wiley.com/doi/full/10.1111/apt.13495
http://www.ncbi.nlm.nih.gov/pubmed/26669729?tool=bestpractice.com
Second-line treatment
Patients who fail first-line therapy should be re-treated with regimens that do not include previously used antibiotics, except for amoxicillin and tetracycline as resistance to later antibiotics is rare.[21]Bhutto A, Morley JE. The clinical significance of gastrointestinal changes with aging. Curr Opin Clin Nutr Metab Care. 2008 Sep;11(5):651-60.
http://www.ncbi.nlm.nih.gov/pubmed/18685464?tool=bestpractice.com
[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
Those with a penicillin allergy should be considered for allergy testing.
Second-line regimens after first-line regimen failure include:[21]Bhutto A, Morley JE. The clinical significance of gastrointestinal changes with aging. Curr Opin Clin Nutr Metab Care. 2008 Sep;11(5):651-60.
http://www.ncbi.nlm.nih.gov/pubmed/18685464?tool=bestpractice.com
[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
PPI plus amoxicillin plus levofloxacin
High-dose PPI plus high-dose amoxicillin
PPI plus rifabutin plus amoxicillin.
Fourteen days of therapy is recommended for these regimens, although the rifabutin-based regimen may be given for 10 to 14 days.[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[144]Fiorini G, Zullo A, Vakil N, et al. Rifabutin triple therapy is effective in patients with multidrug-resistant strains of Helicobacter pylori. J Clin Gastroenterol. 2018 Feb;52(2):137-40.
http://www.ncbi.nlm.nih.gov/pubmed/27136964?tool=bestpractice.com
[145]Graham DY, Canaan Y, Maher J, et al. Rifabutin-based triple therapy (RHB-105) for Helicobacter pylori eradication: a double-blind, randomized, controlled trial. Ann Intern Med. 2020 Jun 16;172(12):795-802.
http://www.ncbi.nlm.nih.gov/pubmed/32365359?tool=bestpractice.com
Due to complexity and poor adherence, sequential non-bismuth and hybrid non-bismuth quadruple therapy are no longer recommended.[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[146]Fallone CA, Moss SF, Malfertheiner P. Reconciliation of recent Helicobacter pylori treatment guidelines in a time of increasing resistance to antibiotics. Gastroenterology. 2019 Jul;157(1):44-53.
http://www.ncbi.nlm.nih.gov/pubmed/30998990?tool=bestpractice.com
High-dose dual therapy, defined as the administration of a high dose of a PPI plus a high dose of amoxicillin, is effective following first-line therapy failure (70% to 89%), and circumvents the issue of clarithromycin, metronidazole, and levofloxacin resistance.[147]Howden CW. Emerging regimens for H. pylori infection should enhance efficacy and circumvent resistance. Dig Dis Sci. 2019 Oct;64(10):2691-2.
https://link.springer.com/article/10.1007%2Fs10620-019-05747-8
http://www.ncbi.nlm.nih.gov/pubmed/31346952?tool=bestpractice.com
[148]Yang X, Wang JX, Han SX, et al. High dose dual therapy versus bismuth quadruple therapy for Helicobacter pylori eradication treatment: a systematic review and meta-analysis. Medicine (Baltimore). 2019 Feb;98(7):e14396.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408008
http://www.ncbi.nlm.nih.gov/pubmed/30762742?tool=bestpractice.com
Rifabutin-based regimens are effective rescue therapies as H pyloriresistance to this commonly used anti-tuberculosis drug is uncommon.[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[98]Stenstrom B, Mendis A, Marshall B. Helicobacter pylori - the latest in diagnosis and treatment. Aus Fam Physician. 2008 Aug;37(8):608-12.
http://www.ncbi.nlm.nih.gov/pubmed/18704207?tool=bestpractice.com
[73]Malfertheiner P. Helicobacter pylori infection - management from a European perspective. Dig Dis. 2014;32(3):275-80.
http://www.ncbi.nlm.nih.gov/pubmed/24732193?tool=bestpractice.com
[128]Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidence-based medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol. 2014 Feb;12(2):177-86;e3;discussion e12-3.
http://www.cghjournal.org/article/S1542-3565%2813%2900773-8/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/23751282?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[131]Fallone CA, Chiba N, van Zanten SV, et al. The Toronto consensus for the treatment of Helicobacter pylori infection in adults. Gastroenterology. 2016 Jul;151(1):51-69;e14.
http://www.ncbi.nlm.nih.gov/pubmed/27102658?tool=bestpractice.com
[149]Liang 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 Jul;11(7):802-7;e1.
http://www.cghjournal.org/article/S1542-3565%2813%2900116-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/23376004?tool=bestpractice.com
[150]Vakil N. H. pylori treatment: new wine in old bottles? Am J Gastroenterol. 2009 Jan;104(1):26-30.
http://www.ncbi.nlm.nih.gov/pubmed/19098845?tool=bestpractice.com
[151]Vakil N, Megraud F. Eradication therapy for Helicobacter pylori. Gastroenterology. 2007 Sep;133(3):985-1001.
http://www.ncbi.nlm.nih.gov/pubmed/17854602?tool=bestpractice.com
[152]Graham DY, Rimbara E. Understanding and appreciating sequential therapy for Helicobacter pylori eradication. J Clin Gastroenterol. 2011 Apr;45(4):309-13.
http://www.ncbi.nlm.nih.gov/pubmed/21389810?tool=bestpractice.com
[153]Hsu PI, Wu DC, Wu JY, et al. Modified sequential Helicobacter pylori therapy: proton pump inhibitor and amoxicillin for 14 days with clarithromycin and metronidazole added as a quadruple (hybrid) therapy for the final 7 days. Helicobacter. 2011 Apr;16(2):139-45.
http://www.ncbi.nlm.nih.gov/pubmed/21435092?tool=bestpractice.com
[154]Hu Y, Zhu Y, Lu N-H. Novel and effective therapeutic regimens for Helicobacter pylori in an era of increasing antibiotic resistance front cell. Infect Microbiol. 2017 May 5;7:168.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5418237
http://www.ncbi.nlm.nih.gov/pubmed/28529929?tool=bestpractice.com
Although myelotoxicity was observed in 2% of treated patients, all of them recovered without increased susceptibility to infection.[155]Gisbert JP, Calvet X. Review article: rifabutin in the treatment of refractory Helicobacter pylori infection. Aliment Pharmacol Ther. 2012 Jan;35(2):209-21.
https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-2036.2011.04937.x
http://www.ncbi.nlm.nih.gov/pubmed/22129228?tool=bestpractice.com
Antibiotic resistance
Standard first-line empirical initial treatment for H pylori infection is triple therapy consisting of a PPI, amoxicillin, and clarithromycin for 14 days.[91]Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection - the Maastricht V/Florence Consensus Report. Gut. 2017 Jan;66(1):6-30.
https://gut.bmj.com/content/66/1/6.long
http://www.ncbi.nlm.nih.gov/pubmed/27707777?tool=bestpractice.com
[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
However, treatment success with this regimen is presently <80%, in both the US and Europe, primarily related to an increase in the prevalence of clarithromycin resistance and poor treatment adherence; evidence suggests that this regimen should no longer be recommended.[130]McNicholl AG, Bordin DS, Lucendo A, et al. Combination of bismuth and standard triple therapy eradicates Helicobacter pylori infection in more than 90% of patients. Clin Gastroenterol Hepatol. 2020 Jan;18(1):89-98.
http://www.ncbi.nlm.nih.gov/pubmed/30978536?tool=bestpractice.com
[156]Savoldi A, Carrara E, Graham DY, et al. Prevalence of antibiotic resistance in Helicobacter pylori: a systematic review and meta-analysis in World Health Organization regions. Gastroenterology. 2018 Nov;155(5):1372-82;e17.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6905086
http://www.ncbi.nlm.nih.gov/pubmed/29990487?tool=bestpractice.com
Resistance to other antibiotics, traditionally used in H pylorieradication regimens, has also increased. In the US, resistance to metronidazole is 20% and to levofloxacin 31%. Fortunately, antibiotic resistance to tetracycline and amoxicillin is low to rare.[156]Savoldi A, Carrara E, Graham DY, et al. Prevalence of antibiotic resistance in Helicobacter pylori: a systematic review and meta-analysis in World Health Organization regions. Gastroenterology. 2018 Nov;155(5):1372-82;e17.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6905086
http://www.ncbi.nlm.nih.gov/pubmed/29990487?tool=bestpractice.com
[157]Shiota S, Reddy R, Alsarraj A, et al. Antibiotic resistance of Helicobacter pylori among male United States veterans. Clin Gastroenterol Hepatol. 2015 Sep;13(9):1616-24.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6905083
http://www.ncbi.nlm.nih.gov/pubmed/25681693?tool=bestpractice.com
Poor treatment adherence is related to complex treatment regimens and adverse effects to antibiotics.
Confirmation of treatment efficacy
Treatment success (or failure) should be confirmed using urea breath test, stool antigen test, or biopsy with immunohistochemistry or rapid urease test.[128]Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidence-based medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol. 2014 Feb;12(2):177-86;e3;discussion e12-3.
http://www.cghjournal.org/article/S1542-3565%2813%2900773-8/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/23751282?tool=bestpractice.com
The tests should be performed at least four weeks after completion of the eradication regimen. PPIs, which are bacteriostatic against H pylori, should be withheld for one to two weeks prior to testing.[129]Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017 Feb;112(2):212-39.
https://gi.org/wp-content/uploads/2017/02/ACGManagementofHpyloriGuideline2017.pdf
http://www.ncbi.nlm.nih.gov/pubmed/28071659?tool=bestpractice.com
[158]Wang YK, Kuo FC, Liu CJ, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015 Oct 28;21(40):11221-35.
https://www.wjgnet.com/1007-9327/full/v21/i40/11221.htm
http://www.ncbi.nlm.nih.gov/pubmed/26523098?tool=bestpractice.com
[159]El-Serag HB, Kao JY, Kanwal F, et al. Houston Consensus Conference on testing for Helicobacter pylori infection in the United States. Clin Gastroenterol Hepatol. 2018 Jul;16(7):992-1002;e6.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913173
http://www.ncbi.nlm.nih.gov/pubmed/29559361?tool=bestpractice.com
[160]Laine L, Estrada R, Trujillo M, et al. Effect of proton-pump inhibitor therapy on diagnostic testing for Helicobacter pylori. Ann Intern Med. 1998 Oct 1;129(7):547-50.
http://www.ncbi.nlm.nih.gov/pubmed/9758575?tool=bestpractice.com
There is some evidence that certain stool antigen tests that use monoclonal antibodies may be reliable even in the presence of PPIs.[161]Kodama M, Murakami K, Okimoto T, et al. Influence of proton pump inhibitor treatment on Helicobacter pylori stool antigen test. World J Gastroenterol. 2012 Jan 7;18(1):44-8.
https://www.wjgnet.com/1007-9327/full/v18/i1/44.htm
http://www.ncbi.nlm.nih.gov/pubmed/22228969?tool=bestpractice.com
Individualised treatment
Patient management should be individualised and tailored. It is the view of the contributors that a one-size-fits-all approach to H pylori eradication is not necessarily in the best interest of patients. The decision whether or not to undertake H pylorieradication therapy should be based upon the clinical indication, age, family history, and underlying comorbidities of the patient, as well as potential benefits versus harms of first-line and second-line antibiotic regimens. Good antibiotic stewardship enhances patient health outcomes and reduces antibiotic resistance.