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Volume 31, Number 6—June 2025

Research

Prospective Multicenter Surveillance of Non–H. pylori Helicobacter Infections during Medical Checkups, Japan, 2022

Kengo Tokunaga1Comments to Author , Emiko Rimbara1Comments to Author , Toshihisa Tsukadaira, Katsuhiro Mabe, Koji Yahara, Hidekazu Suzuki, Tadashi Shimoyama, Mitsushige Sugimoto, Tadayoshi Okimoto, Hidenori Matsui, Masato Suzuki, Keigo Shibayama, Hiroyoshi Ota, Kazunari Murakami, and Mototsugu Kato
Author affiliation: Kyorin University School of Medicine, Tokyo, Japan (K. Tokunaga); National Institute of Infectious Diseases, Tokyo (E. Rimbara, K. Yahara, H. Matsui, M. Suzuki); Kenwakai Hospital, Iida, Japan (T. Tsukadaira); Mabe Goryokaku Gastrointestinal Endoscopy Clinic, Hakodate, Japan (K. Mabe); Tokai University School of Medicine, Isehara, Japan (H. Suzuki); Aomori General Health Examination Center, Aomori, Japan (T. Shimoyama); Oita University, Oita, Japan (M. Sugimoto, K. Murakami); Oita Prefectural Hospital, Oita (T. Okimoto); Nagoya University Graduate School of Medicine, Nagoya, Japan (K. Shibayama); Shinshu University School of Medicine, Matsumoto, Japan (H. Ota); Public Interest Foundation Hokkaido Cancer Society, Sapporo, Japan (M. Kato)

Main Article

Figure 3

Helicobacter suis antibody titers according to gastric Helicobacter infection status in study of NHPH infections, Japan, 2022. Antibodies were measured by using ELISA. Gastric Helicobacter infection status was categorized into 5 groups. Horizontal lines within each group indicate the median value for that group. Red dotted line indicates the threshold for diagnosing H. suis infection, as previously described (16). p value comparisons are indicated above the groups. NHPH, non–H. pylori Helicobacter.

Figure 3. Helicobacter suis antibody titers according to gastric Helicobacter infection status in study of NHPH infections, Japan, 2022. Antibodies were measured by using ELISA. Gastric Helicobacter infection status was categorized into 5 groups. Horizontal lines within each group indicate the median value for that group. Red dotted line indicates the threshold for diagnosing H. suis infection, as previously described (16). p value comparisons are indicated above the groups. NHPH, non–H. pylori Helicobacter.

Main Article

References
  1. Dent  JC, McNulty  CA, Uff  JC, Wilkinson  SP, Gear  MW. Spiral organisms in the gastric antrum. Lancet. 1987;2:96. DOIPubMedGoogle Scholar
  2. Stolte  M, Kroher  G, Meining  A, Morgner  A, Bayerdörffer  E, Bethke  B. A comparison of Helicobacter pylori and H. heilmannii gastritis. A matched control study involving 404 patients. Scand J Gastroenterol. 1997;32:28–33. DOIPubMedGoogle Scholar
  3. Morgner  A, Lehn  N, Andersen  LP, Thiede  C, Bennedsen  M, Trebesius  K, et al. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology. 2000;118:821–8. DOIPubMedGoogle Scholar
  4. Nakamura  M, Øverby  A, Michimae  H, Matsui  H, Takahashi  S, Mabe  K, et al. PCR analysis and specific immunohistochemistry revealing a high prevalence of non-Helicobacter pylori Helicobacters in Helicobacter pylori-negative gastric disease patients in Japan: High susceptibility to an Hp eradication regimen. Helicobacter. 2020;25:e12700. DOIPubMedGoogle Scholar
  5. Kadota  H, Yuge  R, Miyamoto  R, Otani  R, Takigawa  H, Hayashi  R, et al. Investigation of endoscopic findings in nine cases of Helicobacter suis-infected gastritis complicated by gastric mucosa-associated lymphoid tissue lymphoma. Helicobacter. 2022;27:e12887. DOIPubMedGoogle Scholar
  6. Haesebrouck  F, Pasmans  F, Flahou  B, Chiers  K, Baele  M, Meyns  T, et al. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev. 2009;22:202–23. DOIPubMedGoogle Scholar
  7. De Groote  D, Van Doorn  LJ, Van den Bulck  K, Vandamme  P, Vieth  M, Stolte  M, et al. Detection of non-pylori Helicobacter species in “Helicobacter heilmannii”-infected humans. Helicobacter. 2005;10:398–406. DOIPubMedGoogle Scholar
  8. Rimbara  E, Suzuki  M, Matsui  H, Nakamura  M, Morimoto  M, Sasakawa  C, et al. Isolation and characterization of Helicobacter suis from human stomach. Proc Natl Acad Sci U S A. 2021;118:e2026337118. DOIPubMedGoogle Scholar
  9. Heilmann  KL, Borchard  F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut. 1991;32:137–40. DOIPubMedGoogle Scholar
  10. Okiyama  Y, Matsuzawa  K, Hidaka  E, Sano  K, Akamatsu  T, Ota  H. Helicobacter heilmannii infection: clinical, endoscopic and histopathological features in Japanese patients. Pathol Int. 2005;55:398–404. DOIPubMedGoogle Scholar
  11. Tsukadaira  T, Hayashi  S, Ota  H, Kobayashi  N, Sekiguchi  Y, Kodaira  H, et al. Prevalence, clinical features, and esophagogastroduodenoscopy (EGD) findings of non-Helicobacter pylori Helicobacter infection: A study of 50 cases at a single facility in Japan. Helicobacter. 2021;26:e12811. DOIPubMedGoogle Scholar
  12. Taillieu  E, De Witte  C, De Schepper  H, Van Moerkercke  W, Rutten  S, Michiels  S, et al. Clinical significance and impact of gastric non-Helicobacter pylori Helicobacter species in gastric disease. Aliment Pharmacol Ther. 2023;57:1432–44. DOIPubMedGoogle Scholar
  13. Rimbara  E, Tamura  R, Tanuma  M, Noguchi  N, Kawai  T, Sasatsu  M. Evaluation of clarithromycin resistance in Helicobacter pylori obtained from culture isolates, gastric juice, and feces. Helicobacter. 2009;14:156–7. DOIPubMedGoogle Scholar
  14. Tsuda  M, Watanabe  Y, Oikawa  R, Watanabe  R, Higashino  M, Kubo  K, et al. Clinical evaluation of a novel molecular diagnosis kit for detecting Helicobacter pylori and clarithromycin-resistant using intragastric fluid. Helicobacter. 2022;27:e12933. DOIPubMedGoogle Scholar
  15. Matsui  H, Suzuki  M, Aoki  S, Shibayama  K, Tokunaga  K, Suzuki  H, et al. Protocol for detecting Helicobacter suis infection in gastric biopsies and serum by PCR and ELISA. STAR Protoc. 2023;4:102556. DOIPubMedGoogle Scholar
  16. Matsui  H, Rimbara  E, Suzuki  M, Tokunaga  K, Suzuki  H, Sano  M, et al. Development of serological assays to identify Helicobacter suis and H. pylori infections. iScience. 2023;26:106522. DOIPubMedGoogle Scholar
  17. Kimura  K, Takemoto  T. An endoscopic recognition of the atrophic border and its significance in chronic gastritis. Endoscopy. 1969;1:87–97. DOIGoogle Scholar
  18. Shiratori  S, Mabe  K, Yoshii  S, Takakuwa  Y, Sato  M, Nakamura  M, et al. Two cases of chronic gastritis with non-Helicobacter pylori Helicobacter infection. Intern Med. 2016;55:1865–9. DOIPubMedGoogle Scholar
  19. Yagi  K, Nakamura  A, Sekine  A. Characteristic endoscopic and magnified endoscopic findings in the normal stomach without Helicobacter pylori infection. J Gastroenterol Hepatol. 2002;17:39–45. DOIPubMedGoogle Scholar
  20. Haruma  K, Kato  M, Inoue  K, Murakami  K, Kamada  T, editors. Kyoto classification of gastritis. Tokyo: Nihon Medical Center; 2017.
  21. Okuda  M, Osaki  T, Kikuchi  S, Ueda  J, Lin  Y, Yonezawa  H, et al. Evaluation of a stool antigen test using a mAb for native catalase for diagnosis of Helicobacter pylori infection in children and adults. J Med Microbiol. 2014;63:1621–5. DOIPubMedGoogle Scholar
  22. Wang  C, Nishiyama  T, Kikuchi  S, Inoue  M, Sawada  N, Tsugane  S, et al. Changing trends in the prevalence of H. pylori infection in Japan (1908-2003): a systematic review and meta-regression analysis of 170,752 individuals. Sci Rep. 2017;7:15491. DOIPubMedGoogle Scholar
  23. Sano  M, Rimbara  E, Suzuki  M, Matsui  H, Hirai  M, Aoki  S, et al. Helicobacter ailurogastricus in patient with multiple refractory gastric ulcers, Japan. Emerg Infect Dis. 2023;29:833–5. DOIPubMedGoogle Scholar
  24. Wüppenhorst  N, von Loewenich  F, Hobmaier  B, Vetter-Knoll  M, Mohadjer  S, Kist  M. Culture of a gastric non-Helicobacter pylori Helicobacter from the stomach of a 14-year-old girl. Helicobacter. 2013;18:1–5. DOIPubMedGoogle Scholar
  25. Jalava  K, On  SL, Harrington  CS, Andersen  LP, Hänninen  ML, Vandamme  P. A cultured strain of “Helicobacter heilmannii,” a human gastric pathogen, identified as H. bizzozeronii: evidence for zoonotic potential of Helicobacter. Emerg Infect Dis. 2001;7:1036–8. DOIPubMedGoogle Scholar
  26. Kivistö  R, Linros  J, Rossi  M, Rautelin  H, Hänninen  ML. Characterization of multiple Helicobacter bizzozeronii isolates from a Finnish patient with severe dyspeptic symptoms and chronic active gastritis. Helicobacter. 2010;15:58–66. DOIPubMedGoogle Scholar
  27. Kikuchi  M, Iwaya  O, Endo  H, Sigeta  F, Une  M, Osaka  S, et al. The presence of Helicobacter infection in sows. Nippon Juishikai Zasshi. 2004;57:310–2. DOIGoogle Scholar
  28. Kubota-Aizawa  S, Ohno  K, Kanemoto  H, Nakashima  K, Fukushima  K, Uchida  K, et al. Epidemiological study on feline gastric Helicobacter spp. in Japan. J Vet Med Sci. 2017;79:876–80. DOIPubMedGoogle Scholar
  29. Kubota-Aizawa  S, Ohno  K, Fukushima  K, Kanemoto  H, Nakashima  K, Uchida  K, et al. Epidemiological study of gastric Helicobacter spp. in dogs with gastrointestinal disease in Japan and diversity of Helicobacter heilmannii sensu stricto. Vet J. 2017;225:56–62. DOIPubMedGoogle Scholar
  30. Liu  J, He  L, Haesebrouck  F, Gong  Y, Flahou  B, Cao  Q, et al. Prevalence of coinfection with gastric non-Helicobacter pylori Helicobacter (NHPH) species in Helicobacter pylori-infected patients suffering from gastric disease in Beijing, China. Helicobacter. 2015;20:284–90. DOIPubMedGoogle Scholar
  31. 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. DOIPubMedGoogle Scholar

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1These authors contributed equally to this article.

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