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A Helicobacter pylori screening and treatment program to eliminate gastric cancer among junior high school students in Saga Prefecture: a preliminary report

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Abstract

Background

To present the strategies and preliminary findings of the first 3 years after implementing a Helicobacter pylori screening and eradication program to prevent gastric cancer in Saga Prefecture.

Methods

A screening and treatment program to eradicate H. pylori from third-grade junior high students was started in Saga Prefecture in 2016, using local governmental grants. Screening was with urinary anti-H. pylori antibody tests, followed by H. pylori stool antigen tests for students who were antibody positive. Those positive on both tests underwent H. pylori eradication by triple therapy based on a potassium-competitive acid blocker.

Results

From 2016 to 2018, the participation rate was 83.1% and the H. pylori infection rate was 3.1% (660/21,042). The participation rates were higher in 2017 (85.4%) and 2018 (85.9%) compared with 2016 (78.5%) (P < 0.0001), and the infection rate also decreased in a time-dependent manner (2016: 3.6%, 2017: 3.3%, 2018: 2.5%, P = 0.0001). In total, 501 students positive for H. pylori received eradication therapy (85.1% success) and adverse events occurred in 20 of these (4.0%). However, no serious complications occurred.

Conclusions

The H. pylori screening and eradication project for school students in Saga Prefecture has started successfully and we have seen both a steady increase in the participation rate and a steady decrease in the infection rate, without major safety concerns.

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References

  1. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.

    Article  CAS  PubMed  Google Scholar 

  2. Park JY, Forman D, Waskit LA, et al. Epidemiology of Helicobacter pylori and CagA-positive infections and global variations in gastric cancer. Toxins. 2018;10:e163.

    Article  CAS  PubMed  Google Scholar 

  3. Suzuki H, Mori H. World trends for H. pylori eradication therapy and gastric cancer prevention strategy by H. pylori test-and-treat. J Gastroenterol. 2018;53:354–61.

    Article  PubMed  Google Scholar 

  4. Hatakeyama H. Helicobacter pylori CagA and cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 2014;15:306–16.

    Article  CAS  PubMed  Google Scholar 

  5. Kikuchi S, Nakajima T, Kobayashi O, et al. Effect of age on the relationship between gastric cancer and Helicobacter pylori. Jpn J Cancer Res. 2000;91:774–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ekstom AM, Held M, Hansson LE, et al. Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology. 2001;121:784–91.

    Article  Google Scholar 

  7. Horiuchi Y, Fujisaki J, Yamamoto N, et al. Biological behavior of the intramucosal Helicobacter pylori-negative undifferentiated-type early gastric cancer: comparison with helicobacter pylori-positive early gastric cancer. Gastric Cancer. 2016;19:160–5.

    Article  CAS  PubMed  Google Scholar 

  8. Tsuda M, Asaka M, Kato M, et al. Effect on Helicobacter pylori eradication therapy against gastric cancer in Japan. Helicobacter. 2017;22:e12415.

    Article  PubMed Central  Google Scholar 

  9. Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2018. https://doi.org/10.1007/s10120-018-0876-0

    Article  PubMed  Google Scholar 

  10. Asaka M, Mabe K, Matsushima R, et al. Helicobacter pylori eradication to eliminate gastric cancer: the Japanese strategy. Gastroenterol Clin N Am. 2015;44:639–48.

    Article  Google Scholar 

  11. Tsutsumi K, Kusano C, Suzuki S, et al. Diagnostic accuracy of latex agglutination turbidimetric immunoassay in screening adolescents for Helicobacter pylori infection in Japan. Digestion. 2018;98:75–80.

    Article  CAS  PubMed  Google Scholar 

  12. Take S, Mizuno M, Ishiki 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;42:21–7.

    Article  PubMed  Google Scholar 

  13. Wong 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;291:187–94.

    Article  CAS  PubMed  Google Scholar 

  14. Sugano K, Tack J, Kuipers EJ, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64:1353–67.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kato S, Kikuchi S, Nakajima S. When does gastric atrophy develop in Japanese children? Helicobacter. 2008;13:278–81.

    Article  PubMed  Google Scholar 

  16. Nozaki K, Shimizu N, Ikehara Y, et al. Eradication diminishes enhancing effects of Helicobacter pylori infection on glandular stomach carcinogenesis in Mongolian gerbils. Cancer Sci. 2003;94:235–9.

    Article  CAS  PubMed  Google Scholar 

  17. Furuta T, El-Omar EM, Xiao F, et al. Interleukin 1beta polymorphisms increase risk of hypochlorhydria and atrophic gastritis and reduce risk of duodenal ulcer recurrence in Japan. Gastroenterology. 2002;123:92–105.

    Article  CAS  PubMed  Google Scholar 

  18. Akamatsu T, Ichikawa S, Okada S, et al. Introduction of an examination and treatment for Helicobacter pylori infection in high school health screening. J Gastroenterol. 2011;46:1353–60.

    Article  PubMed  Google Scholar 

  19. Kusano C, Gotoda T, Ishikawa H, et al. The administrative project of Helicobacter pylori infection screening among junior high school students in an area of Japan with a high incidence of gastric cancer. Gastric Cancer. 2017;20:S16–9.

    Article  Google Scholar 

  20. Okuda M, Kamiya S, Booka M, et al. Diagnostic accuracy of urine-based kits for detection of Helicobacter pylori antigen in children. Pediatr Int. 2013;55:337–41.

    Article  CAS  PubMed  Google Scholar 

  21. Yamamoto T, Ishii T, Kawakami T, et al. Reliability of urinary tests for antibody to Helicobacter pylori in patients with pulmonary tuberculosis. World J Gastroenterol. 2005;11:412–4.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Tamamura T, Morita E, Kondo T, et al. Prevalence of Helicobacter pylori infection measured with urinary antibody in an urban area of Japan, 2008–2010. Nagoya J Med Sci. 2012;74:63–70.

    Google Scholar 

  23. Shimoyama T. Stool antigen tests for the management of Helicobacter pylori infection. World J Gastroenterol. 2013;19:818–91.

    Google Scholar 

  24. Fukuda Y, Tomita T, Hori K, et al. Evaluation of a novel Helicobacter pylori stool antigen detection kit, Testmate rapid pylori antigen, for rapid diagnosis of Helicobacter pylori infection. Jpn J Med Pharm Sci. 2004;52:469–74.

    Google Scholar 

  25. Zebala Torrres B, Luceno Y, Lagomarcino AJ, et al. Review: prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter. 2017;22:e12399.

    Article  Google Scholar 

  26. Tanaka Y, Sakata Y, Hara M, et al. Risk factors for Helicobacter pylori infection and endoscopic reflux esophagitis in healthy young Japanese volunteers. Intern Med. 2017;56:2979–83.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Takeshita E, Sakata Y, Hara M, et al. Higher frequency of reflux symptoms and acid-related dyspepsia in females than males regardless of endoscopic esophagitis: cross sectional analysis of 3,505 Japanese subjects undergoing medical health checkups. Digestion. 2016;93:266–71.

    Article  PubMed  Google Scholar 

  28. Fujimoto Y, Furusyo N, Toyoda K, et al. Intrafamilial transmission of Helicobacter pylori among the population of endemic areas in Japan. Helicobacter. 2007;12:170–6.

    Article  PubMed  Google Scholar 

  29. Asaka M, Kimura T, Kudo M, et al. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992;102:760–6.

    Article  CAS  PubMed  Google Scholar 

  30. Okuda M, Osaki T, Lin Y, et al. Low prevalence and incidence of Helicobacter pylori infection in children: a population-based study in Japan. Helicobacter. 2014;20:133–8.

    Article  PubMed  Google Scholar 

  31. Schwarz S, Morelli G, Kusecek B, et al. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog. 2008;4:e1000180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Rogers AH. The source of infection in the intrafamilial transfer of Streptococcus mutans. Caries Res. 1981;15:26–31.

    Article  CAS  PubMed  Google Scholar 

  33. Seow WK. Early childhood caries. Pesiatr Clin N Am. 2019;65:941–54.

    Article  Google Scholar 

  34. Murakami K, Sakurai Y, Shiino M, et al. Vonoprazan, a novel potassium-competitive acid blocker, as a component of first-line and second-line triple therapy for Helicobacter pylori eradication: a phase III, randomized, double-blind study. Gut. 2016;65:1439–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Tanabe H, Ando K, Sato K, et al. Efficacy of vonoprazan-based triple therapy for Helicobacter pylori eradication: a multicenter study and a review of the literature. Dig Dis Sci. 2017;62:3069–76.

    Article  CAS  PubMed  Google Scholar 

  36. Takara Y, Endo H, Nakano R, et al. Smoking and drinking did not increase the failure of therapeutic Helicobacter pylori eradication by vonoprazan, clarithromycin, and amoxicillin. Digestion. 2018;4:1–7.

    Google Scholar 

  37. Ozaki H, Harada S, Takeuchi T, et al. Vonoprazan, a novel potassium-competitive acid blocker, should be used for the Helicobacter pylori eradication therapy as first choice: a large sample study of vonoprazan in real world compared with our randomized control trial using second-generation proton pump inhibitors for Helicobacter pylori eradication therapy. Digestion. 2018;97:212–8.

    Article  CAS  PubMed  Google Scholar 

  38. Suzuki S, Gotoda T, Kusano C, et al. The efficacy and tolerability of a triple therapy containing a potassium-competitive acid blocker compared with a 7-day PPI-based low dose clarithromycin triple therapy. Am J Gastroenterol. 2016;111:949–56.

    Article  CAS  PubMed  Google Scholar 

  39. Khurana R, Fischbach L, Chiba N, et al. Meta-analysis: Helicobacter pylori eradication treatment efficacy in children. Aliment Pharmacol Ther. 2007;25:423–36.

    Article  CAS  Google Scholar 

  40. Jones NL, Koletzko S, Goodman K, et al. Joint ESPGHAN/NASPGHAN guideline for the management of Helicobacter pylori in children and adolescents (update 2016). J Pediatr Gastroenterol Nutr. 2017;23:2453–8.

    Google Scholar 

  41. Kotilea K, Mekhael J, Salame A, et al. Eradication rate of Helicobacter pylori infection is directly influenced by adherence to therapy in children. Helicobacter. 2017;22:e12383.

    Article  CAS  Google Scholar 

  42. Kato S, Konno M, Maisawa S, et al. Results of triple eradication therapy in Japanese children: a retrospective multicenter study. J Gastroenterol. 2004;39:838–43.

    Article  PubMed  Google Scholar 

  43. Kato S, Fujimura S. Primary antimicrobial resistance of Helicobacter pylori in children during the past 9 years. Pediatr Int. 2010;52:18–90.

    Article  CAS  Google Scholar 

  44. 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;55:1372–82.

    Article  Google Scholar 

  45. Montes M, Villalon FN, Eizaguirre FJ, et al. Helicobacter pylori infection in children. Antimicrobial resistance and treatment response. Helicobacter. 2015;20:169–75.

    Article  CAS  PubMed  Google Scholar 

  46. Ogata SK, Godoy AP, da Silva Patricio FR, et al. High Helicobacter pylori resistance to metronidazole and clarithromycin in Brazilian children and adolescents. J Pediatr Gastroenterol Nutr. 2013;56:645–8.

    Article  CAS  PubMed  Google Scholar 

  47. Okamura T, Suga T, Nagaya T, et al. Antimicrobial resistance and characteristics of eradication therapy of Helicobacter pylori in Japan: a multi-generational comparison. Helicobacter. 2014;19:214–20.

    Article  CAS  PubMed  Google Scholar 

  48. Okuda M, Kikuchi S, Mabe K, et al. Nationwide survey of Helicobacter pylori treatment for children and adolescents in Japan. Pediatr Int. 2017;59:57–61.

    Article  PubMed  Google Scholar 

  49. Mabe K, Okuda M, Kikuchi S, et al. Randomized controlled trial: PPI-based triple therapy containing metronidazole versus clarithromycin as first-line treatment for Helicobacter pylori in adolescents and young adults in Japan. J Infect Chemother. 2018;24:538–43.

    Article  CAS  PubMed  Google Scholar 

  50. Adachi T, Matsui S, Watanabe T, et al. Comparative study of clarithromycin- versus metronidazole-based triple therapy as first-line eradication for Helicobacter pylori. Oncology. 2017;93:15–9.

    Article  PubMed  Google Scholar 

  51. Kusano C, Gotoda T, Suzuki S, et al. Safety of first-line triple therapy with a potassium-competitive acid blocker for Helicobacter pylori eradication in children. J Gastroenterol. 2018;53:718–24.

    Article  CAS  PubMed  Google Scholar 

  52. Gibbons TE, Gold BD. The use of proton pump inhibitors in children: a comprehensive review. Paediatr Drugs. 2003;5:25–40.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work is supported by public grants of Saga Prefecture. We would like to thank Mr. Daisuke Yoshihara, Mr. Shuichi Furukawa, and Ms. Aiko Ikegami of the department of Health and Welfare in Saga Prefecture. The authors thank Professor Takuji Gotoda, Dr. Tsugio Furukawa, Dr. Chika Kusano, Dr. Mototsugu Kato, Dr. Katsuhiro Mabe, and Mr. Hiroo Sashiyama for their excellent suggestions, as well as Professor Masahiro Asaka for their role as safety evaluation committee chairman for this project. We also want to acknowledge Dr. Yamaguchi D, Dr. Takeshita E, Dr. Hanada K, Dr. Kawakubo Y, Dr. Imamura I, Dr. Taniguchi K, Dr. Yamamoto K, Dr. Kajiwara T, Dr. Kuwahara A, Dr. Akiyama M, Dr. Yamaguchi S, Dr. Mizoe A, Dr. Muro E, Dr. Nishimura S, Dr. Noda T, Dr. Ogata S, Dr. Matsunaga K, Dr. Watanabe S, Dr. Inutsuka S, Dr. Fukuyama K, Dr. Ooi J, Dr. Fujioka Y, Takayanagi T and Dr. Fukuda K, the head of the department in charge of the cooperating medical institution. Finally, we thank Ms. Kozue Kakiuchi, Ms. Tomomi Ito, and Ms. Hiromi Beppu, the project business center’s staff, for their support.

Funding

This project was supported by public grants from the government of Saga Prefecture.

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Authors and Affiliations

  1. Department of Pediatrics, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Toshihiko Kakiuchi, Muneaki Matsuo & Aiko Nakayama

  2. Department of Internal Medicine, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Yasuhisa Sakata, Yuichiro Eguchi, Hirokazu Takahashi, Keizo Anzai & Kazuma Fujimoto

  3. Department of Prevention Medicine, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Megumi Hara

  4. Department of Internal Medicine, Saiseikai Karatsu Hospital, 817 Motohata-machi, Karatsu-shi, 847-0852, Japan

    Hiroyoshi Endo

  5. Clinical Research Center, Saga University Hospital, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Keiko Sato & Ayako Takamori

  6. Saga Cancer Center, Saga University Hospital, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Kazumi Sasaki

  7. Medical Informatics, Saga University Hospital, 5-1-1 Nabeshima, Saga-shi, 849-8501, Saga, Japan

    Mitsuhiro Takasaki

  8. Department of Pediatrics, Aichi Medical University School of Medicine, 1-1 Yazakokarimata, Nagakute-shi, 480-1195, Aichi, Japan

    Masumi Okuda

  9. Department of Public Health, Aichi Medical University School of Medicine, 1-1 Yazakokarimata, Nagakute-shi, 480-1195, Aichi, Japan

    Shogo Kikuchi

Authors
  1. Toshihiko Kakiuchi
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  2. Muneaki Matsuo
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  3. Hiroyoshi Endo
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  4. Aiko Nakayama
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  7. Kazumi Sasaki
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  8. Mitsuhiro Takasaki
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  9. Megumi Hara
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  10. Yasuhisa Sakata
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  11. Masumi Okuda
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  12. Shogo Kikuchi
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  13. Yuichiro Eguchi
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  16. Kazuma Fujimoto
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Contributions

Guarantor of the article: TK. Conceptualization, data analysis, and manuscript preparation: TK, HE, and KF. Data collection: TK. Critical review of the manuscript: MM, KA, and KF. All authors have read and approved the submitted version.

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Correspondence to Toshihiko Kakiuchi.

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Kakiuchi, T., Matsuo, M., Endo, H. et al. A Helicobacter pylori screening and treatment program to eliminate gastric cancer among junior high school students in Saga Prefecture: a preliminary report. J Gastroenterol 54, 699–707 (2019). https://doi.org/10.1007/s00535-019-01559-9

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  • DOI: https://doi.org/10.1007/s00535-019-01559-9

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