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Published in: Journal of Gastroenterology 6/2012

01-06-2012 | Original Article—Alimentary Tract

Reinfection rate of Helicobacter pylori after eradication treatment: a long-term prospective study in Japan

Authors: Susumu Take, Motowo Mizuno, Kuniharu Ishiki, Takayuki Imada, Tetsuji Okuno, Tomowo Yoshida, Kenji Yokota, Keiji Oguma, Masahide Kita, Hiroyuki Okada, Kazuhide Yamamoto

Published in: Journal of Gastroenterology | Issue 6/2012

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Abstract

Background

We previously reported that the reinfection rate with Helicobacter pylori in Japan was low despite a high prevalence of infection. In the present study, we extended our previous work to more accurately determine the reinfection rate.

Methods

We enrolled 1625 patients (219 women and 1406 men, mean age 50.8 years) who had received H. pylori eradication therapy. After documentation of eradication, bacterial culture and urea breath test were carried out yearly. H. pylori strains were analyzed by using random amplification of polymorphic DNA fingerprinting.

Results

A total of 1609 patients were followed for up to 12.5 years (mean 4.7 years); H. pylori became re-positive in 26 patients. In 13 of the 26 patients, H. pylori became positive at the first-year follow up. Stored H. pylori isolates were available for analysis from ten of the 13 patients; four of the isolates were genetically different from the initial strain, but the other six were identical to the initial strain. In the other 13 patients, H. pylori became positive at later follow up (mean 4.8 years; range 1.8–8.0 years). In all of the four of these patients whose isolates could be analyzed, the H. pylori strains were different from the initial strain. Assuming that reinfection occurred in the four patients positive for different strains of H. pylori at the first-year follow up and in the 13 positive at later follow up, the reinfection rate was 0.22% per year.

Conclusions

When probable recrudescence (H. pylori positivity with identical strains) was excluded, the reinfection rate of H. pylori in this Japanese population was very low, but we note that reinfection can occur over many years.
Literature
1.
go back to reference Infection with Helicobacter pylori. IARC Monogr Eval Carcinog Risks Hum 1994;61:177–240. Infection with Helicobacter pylori. IARC Monogr Eval Carcinog Risks Hum 1994;61:177–240.
3.
go back to reference Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.PubMedCrossRef Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.PubMedCrossRef
4.
go back to reference Rauws EA, Tytgat GN. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet. 1990;335:1233–5.PubMedCrossRef Rauws EA, Tytgat GN. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet. 1990;335:1233–5.PubMedCrossRef
5.
go back to reference Graham DY, Lew GM, Klein PD, Evans DG, Evans DJ Jr, Saeed ZA, et al. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann Intern Med. 1992;116:705–8.PubMed Graham DY, Lew GM, Klein PD, Evans DG, Evans DJ Jr, Saeed ZA, et al. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann Intern Med. 1992;116:705–8.PubMed
6.
go back to reference Hopkins RJ, Girardi LS, Turney EA. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: a review. Gastroenterology. 1996;110:1244–52.PubMedCrossRef Hopkins RJ, Girardi LS, Turney EA. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: a review. Gastroenterology. 1996;110:1244–52.PubMedCrossRef
7.
go back to reference Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993;342:575–7.PubMedCrossRef Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993;342:575–7.PubMedCrossRef
8.
go back to reference Gasbarrini A, Franceschi F, Tartaglione R, Landolfi R, Pola P, Gasbarrini G. Regression of autoimmune thrombocytopenia after eradication of Helicobacter pylori. Lancet. 1998;352:878.PubMedCrossRef Gasbarrini A, Franceschi F, Tartaglione R, Landolfi R, Pola P, Gasbarrini G. Regression of autoimmune thrombocytopenia after eradication of Helicobacter pylori. Lancet. 1998;352:878.PubMedCrossRef
9.
go back to reference Inaba T, Mizuno M, Take S, Suwaki K, Honda T, Kawai K, et al. Eradication of Helicobacter pylori increases platelet count in patients with idiopathic thrombocytopenic purpura in Japan. Eur J Clin Invest. 2005;35:214–9.PubMedCrossRef Inaba T, Mizuno M, Take S, Suwaki K, Honda T, Kawai K, et al. Eradication of Helicobacter pylori increases platelet count in patients with idiopathic thrombocytopenic purpura in Japan. Eur J Clin Invest. 2005;35:214–9.PubMedCrossRef
10.
go back to reference Uemura N, Mukai T, Okamoto S, Yamaguchi S, Mashiba H, Taniyama K, et al. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev. 1997;6:639–42.PubMed Uemura N, Mukai T, Okamoto S, Yamaguchi S, Mashiba H, Taniyama K, et al. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev. 1997;6:639–42.PubMed
11.
go back to reference Uemura N, Okamoto S. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer in Japan. Gastroenterol Clin North Am. 2000;29:819–27.PubMedCrossRef Uemura N, Okamoto S. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer in Japan. Gastroenterol Clin North Am. 2000;29:819–27.PubMedCrossRef
12.
go back to reference Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. The effect of eradicating Helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol. 2005;100:1037–42.PubMedCrossRef Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. The effect of eradicating Helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol. 2005;100:1037–42.PubMedCrossRef
13.
go back to reference Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. Baseline gastric mucosal atrophy is a risk factor associated with the development of gastric cancer after Helicobacter pylori eradication therapy in patients with peptic ulcer diseases. J Gastroenterol. 2007;42(Suppl 17):21–7.PubMedCrossRef Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. Baseline gastric mucosal atrophy is a risk factor associated with the development of gastric cancer after Helicobacter pylori eradication therapy in patients with peptic ulcer diseases. J Gastroenterol. 2007;42(Suppl 17):21–7.PubMedCrossRef
14.
go back to reference Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008;372:392–7.PubMedCrossRef Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008;372:392–7.PubMedCrossRef
15.
go back to reference Miyoshi M, Mizuno M, Ishiki K, Nagahara Y, Maga T, Torigoe T, et al. A randomized open trial for comparison of proton pump inhibitors, omeprazole versus rabeprazole, in dual therapy for Helicobacter pylori infection in relation to CYP2C19 genetic polymorphism. J Gastroenterol Hepatol. 2001;16:723–8.PubMedCrossRef Miyoshi M, Mizuno M, Ishiki K, Nagahara Y, Maga T, Torigoe T, et al. A randomized open trial for comparison of proton pump inhibitors, omeprazole versus rabeprazole, in dual therapy for Helicobacter pylori infection in relation to CYP2C19 genetic polymorphism. J Gastroenterol Hepatol. 2001;16:723–8.PubMedCrossRef
16.
go back to reference Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Inaba T, et al. Interleukin-1beta genetic polymorphism influences the effect of cytochrome P 2C19 genotype on the cure rate of 1-week triple therapy for Helicobacter pylori infection. Am J Gastroenterol. 2003;98:2403–8.PubMed Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Inaba T, et al. Interleukin-1beta genetic polymorphism influences the effect of cytochrome P 2C19 genotype on the cure rate of 1-week triple therapy for Helicobacter pylori infection. Am J Gastroenterol. 2003;98:2403–8.PubMed
17.
go back to reference Ishiki K, Mizuno M, Take S, Nagahara Y, Yoshida T, Yamamoto K, et al. Helicobacter pylori eradication improves pre-existing reflux esophagitis in patients with duodenal ulcer disease. Clin Gastroenterol Hepatol. 2004;2:474–9.PubMedCrossRef Ishiki K, Mizuno M, Take S, Nagahara Y, Yoshida T, Yamamoto K, et al. Helicobacter pylori eradication improves pre-existing reflux esophagitis in patients with duodenal ulcer disease. Clin Gastroenterol Hepatol. 2004;2:474–9.PubMedCrossRef
18.
go back to reference Ishioka H, Mizuno M, Take S, Ishiki K, Nagahara Y, Yoshida T, et al. A better cure rate with 800 mg than with 400 mg clarithromycin regimens in one-week triple therapy for Helicobacter pylori infection in cigarette-smoking peptic ulcer patients. Digestion. 2007;75:63–8.PubMedCrossRef Ishioka H, Mizuno M, Take S, Ishiki K, Nagahara Y, Yoshida T, et al. A better cure rate with 800 mg than with 400 mg clarithromycin regimens in one-week triple therapy for Helicobacter pylori infection in cigarette-smoking peptic ulcer patients. Digestion. 2007;75:63–8.PubMedCrossRef
19.
go back to reference Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. Helicobacter pylori eradication may induce de novo, but transient and mild, reflux esophagitis: prospective endoscopic evaluation. J Gastroenterol Hepatol. 2009;24:107–13.PubMedCrossRef Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, et al. Helicobacter pylori eradication may induce de novo, but transient and mild, reflux esophagitis: prospective endoscopic evaluation. J Gastroenterol Hepatol. 2009;24:107–13.PubMedCrossRef
20.
go back to reference Take S, Mizuno M, Ishiki K, Yoshida T, Ohara N, Yokota K, et al. The long-term risk of gastric cancer after the successful eradication of Helicobacter pylori. J Gastroenterol 2010. Take S, Mizuno M, Ishiki K, Yoshida T, Ohara N, Yokota K, et al. The long-term risk of gastric cancer after the successful eradication of Helicobacter pylori. J Gastroenterol 2010.
21.
go back to reference Adachi M, Mizuno M, Yokota K, Miyoshi M, Nagahara Y, Maga T, et al. Reinfection rate following effective therapy against Helicobacter pylori infection in Japan. J Gastroenterol Hepatol. 2002;17:27–31.PubMedCrossRef Adachi M, Mizuno M, Yokota K, Miyoshi M, Nagahara Y, Maga T, et al. Reinfection rate following effective therapy against Helicobacter pylori infection in Japan. J Gastroenterol Hepatol. 2002;17:27–31.PubMedCrossRef
22.
go back to reference Nakajima S, Nishiyama Y, Yamaoka M, Yasuoka T, Cho E. Changes in the prevalence of Helicobacter pylori infection and gastrointestinal diseases in the past 17 years. J Gastroenterol Hepatol. 2010;25(Suppl 1):S99–110.PubMedCrossRef Nakajima S, Nishiyama Y, Yamaoka M, Yasuoka T, Cho E. Changes in the prevalence of Helicobacter pylori infection and gastrointestinal diseases in the past 17 years. J Gastroenterol Hepatol. 2010;25(Suppl 1):S99–110.PubMedCrossRef
23.
go back to reference Nagahara Y, Mizuno M, Maga T, Ishiki K, Okuno T, Yoshida T, et al. Outcome of patients with inconsistent results from 13C-urea breath test and bacterial culture at the time of assessment of Helicobacter pylori eradication therapy in Japan. Hepatogastroenterology. 2003;50:1700–3.PubMed Nagahara Y, Mizuno M, Maga T, Ishiki K, Okuno T, Yoshida T, et al. Outcome of patients with inconsistent results from 13C-urea breath test and bacterial culture at the time of assessment of Helicobacter pylori eradication therapy in Japan. Hepatogastroenterology. 2003;50:1700–3.PubMed
24.
go back to reference Akopyanz N, Bukanov NO, Westblom TU, Kresovich S, Berg DE. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 1992;20:5137–42.PubMedCrossRef Akopyanz N, Bukanov NO, Westblom TU, Kresovich S, Berg DE. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 1992;20:5137–42.PubMedCrossRef
25.
go back to reference Jorgensen M, Daskalopoulos G, Warburton V, Mitchell HM, Hazell SL. Multiple strain colonization and metronidazole resistance in Helicobacter pylori-infected patients: identification from sequential and multiple biopsy specimens. J Infect Dis. 1996;174:631–5.PubMedCrossRef Jorgensen M, Daskalopoulos G, Warburton V, Mitchell HM, Hazell SL. Multiple strain colonization and metronidazole resistance in Helicobacter pylori-infected patients: identification from sequential and multiple biopsy specimens. J Infect Dis. 1996;174:631–5.PubMedCrossRef
26.
go back to reference Drumm B, Perez–Perez GI, Blaser MJ, Sherman PM. Intrafamilial clustering of Helicobacter pylori infection. N Engl J Med. 1990;322:359–63.PubMedCrossRef Drumm B, Perez–Perez GI, Blaser MJ, Sherman PM. Intrafamilial clustering of Helicobacter pylori infection. N Engl J Med. 1990;322:359–63.PubMedCrossRef
27.
go back to reference Schutze K, Hentschel E, Dragosics B, Hirschl AM. Helicobacter pylori reinfection with identical organisms: transmission by the patients’ spouses. Gut. 1995;36:831–3.PubMedCrossRef Schutze K, Hentschel E, Dragosics B, Hirschl AM. Helicobacter pylori reinfection with identical organisms: transmission by the patients’ spouses. Gut. 1995;36:831–3.PubMedCrossRef
29.
go back to reference Malaty HM, Kumagai T, Tanaka E, Ota H, Kiyosawa K, Graham DY, et al. Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J Clin Microbiol. 2000;38:1971–3.PubMed Malaty HM, Kumagai T, Tanaka E, Ota H, Kiyosawa K, Graham DY, et al. Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J Clin Microbiol. 2000;38:1971–3.PubMed
30.
go back to reference Miyaji H, Azuma T, Ito S, Abe Y, Gejyo F, Hashimoto N, et al. Helicobacter pylori infection occurs via close contact with infected individuals in early childhood. J Gastroenterol Hepatol. 2000;15:257–62.PubMedCrossRef Miyaji H, Azuma T, Ito S, Abe Y, Gejyo F, Hashimoto N, et al. Helicobacter pylori infection occurs via close contact with infected individuals in early childhood. J Gastroenterol Hepatol. 2000;15:257–62.PubMedCrossRef
31.
go back to reference Bell GD, Powell KU. Helicobacter pylori reinfection after apparent eradication—the Ipswich experience. Scand J Gastroenterol Suppl. 1996;215:96–104.PubMedCrossRef Bell GD, Powell KU. Helicobacter pylori reinfection after apparent eradication—the Ipswich experience. Scand J Gastroenterol Suppl. 1996;215:96–104.PubMedCrossRef
32.
go back to reference Okimoto T, Murakami K, Sato R, Miyajima H, Nasu M, Kagawa J, et al. Is the recurrence of Helicobacter pylori infection after eradication therapy resultant from recrudescence or reinfection, in Japan. Helicobacter. 2003;8:186–91.PubMedCrossRef Okimoto T, Murakami K, Sato R, Miyajima H, Nasu M, Kagawa J, et al. Is the recurrence of Helicobacter pylori infection after eradication therapy resultant from recrudescence or reinfection, in Japan. Helicobacter. 2003;8:186–91.PubMedCrossRef
33.
go back to reference Karczewska E, Konturek JE, Konturek PC, Czesnikiewicz M, Sito E, Bielanski W, et al. Oral cavity as a potential source of gastric reinfection by Helicobacter pylori. Dig Dis Sci. 2002;47:978–86.PubMedCrossRef Karczewska E, Konturek JE, Konturek PC, Czesnikiewicz M, Sito E, Bielanski W, et al. Oral cavity as a potential source of gastric reinfection by Helicobacter pylori. Dig Dis Sci. 2002;47:978–86.PubMedCrossRef
34.
go back to reference Gurbuz AK, Ozel AM, Yazgan Y, Celik M, Yildirim S. Oral colonization of Helicobacter pylori: risk factors and response to eradication therapy. South Med J. 2003;96:244–7.PubMedCrossRef Gurbuz AK, Ozel AM, Yazgan Y, Celik M, Yildirim S. Oral colonization of Helicobacter pylori: risk factors and response to eradication therapy. South Med J. 2003;96:244–7.PubMedCrossRef
35.
go back to reference Mocek FW, Ward WW Jr, Wolfson SE, Rumage WT Jr, Wieman TJ. Elimination of recurrent hyperplastic polyps by eradication of Helicobacter pylori. Ann Intern Med. 1994;120:1007–8.PubMed Mocek FW, Ward WW Jr, Wolfson SE, Rumage WT Jr, Wieman TJ. Elimination of recurrent hyperplastic polyps by eradication of Helicobacter pylori. Ann Intern Med. 1994;120:1007–8.PubMed
36.
go back to reference Wedi B, Wagner S, Werfel T, Manns MP, Kapp A. Prevalence of Helicobacter pylori-associated gastritis in chronic urticaria. Int Arch Allergy Immunol. 1998;116:288–94.PubMedCrossRef Wedi B, Wagner S, Werfel T, Manns MP, Kapp A. Prevalence of Helicobacter pylori-associated gastritis in chronic urticaria. Int Arch Allergy Immunol. 1998;116:288–94.PubMedCrossRef
37.
go back to reference Dufour C, Brisigotti M, Fabretti G, Luxardo P, Mori PG, Barabino A. Helicobacter pylori gastric infection and sideropenic refractory anemia. J Pediatr Gastroenterol Nutr. 1993;17:225–7.PubMedCrossRef Dufour C, Brisigotti M, Fabretti G, Luxardo P, Mori PG, Barabino A. Helicobacter pylori gastric infection and sideropenic refractory anemia. J Pediatr Gastroenterol Nutr. 1993;17:225–7.PubMedCrossRef
38.
go back to reference Kimura K, Takemoto T. An endoscopic recognition of the atrophic border and its significance in chronic gastritis. Endoscopy. 1969;3:87–97.CrossRef Kimura K, Takemoto T. An endoscopic recognition of the atrophic border and its significance in chronic gastritis. Endoscopy. 1969;3:87–97.CrossRef
39.
go back to reference Sakaki N, Arakawa T, Katou H, Momma K, Egawa N, Kamisawa T, et al. Relationship between progression of gastric mucosal atrophy and Helicobacter pylori infection: retrospective long-term endoscopic follow-up study. J Gastroenterol. 1997;32:19–23.PubMedCrossRef Sakaki N, Arakawa T, Katou H, Momma K, Egawa N, Kamisawa T, et al. Relationship between progression of gastric mucosal atrophy and Helicobacter pylori infection: retrospective long-term endoscopic follow-up study. J Gastroenterol. 1997;32:19–23.PubMedCrossRef
Metadata
Title
Reinfection rate of Helicobacter pylori after eradication treatment: a long-term prospective study in Japan
Authors
Susumu Take
Motowo Mizuno
Kuniharu Ishiki
Takayuki Imada
Tetsuji Okuno
Tomowo Yoshida
Kenji Yokota
Keiji Oguma
Masahide Kita
Hiroyuki Okada
Kazuhide Yamamoto
Publication date
01-06-2012
Publisher
Springer Japan
Published in
Journal of Gastroenterology / Issue 6/2012
Print ISSN: 0944-1174
Electronic ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-012-0536-9

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