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Rare Helicobacter pylori Infection May Explain Low Stomach Cancer Incidence: Ecological Observations in Bali, Indonesia

  • Tanaka, Tsutomu (Department of Health and Nutrition Policy, Nagoya City University Graduate School of Medical Sciences) ;
  • Mulyadi, I Ketut (Department of Anatomical Pathology, Faculty of Medicine, Udayana University) ;
  • Moestikaningsih, Moestikaningsih (Department of Anatomical Pathology, Faculty of Medicine, Udayana University) ;
  • Oka, Tjok Gede (Department of Clinical Pathology, Faculty of Medicine, Udayana University) ;
  • Soeripto, Soeripto (Department of Anatomic Pathology, Faculty of Medicine, Gadjah Mada University) ;
  • Triningsih, FX Ediati (Department of Anatomic Pathology, Faculty of Medicine, Gadjah Mada University) ;
  • Triyono, Teguh (Department of Clinical Pathology, Faculty of Medicine, Gadjah Mada University) ;
  • Heriyanto, Didik Setyo (Department of Anatomic Pathology, Faculty of Medicine, Gadjah Mada University) ;
  • Hosono, Akihiro (Department of Public Health, Nagoya City University Graduate School of Medical Sciences) ;
  • Suzuki, Sadao (Department of Public Health, Nagoya City University Graduate School of Medical Sciences) ;
  • Tokudome, Shinkan (Department of Health and Nutrition Policy, Nagoya City University Graduate School of Medical Sciences)
  • Published : 2016.04.11

Abstract

The incidence rate of stomach cancer in Bali, Indonesia, is estimated to be strikingly lower than that in Japan. We conducted an on-site ecological study to investigate the association between the stomach cancer incidence and Helicobacter pylori (H. pylori) infection. Recruiting 291 healthy persons (136 men and 155 women) from the general population in Bali, Indonesia, we conducted a urea breath test (UBT) to examine H. pylori infection, along with a pepsinogen test to detect chronic atrophic gastritis and urine analysis to estimate sodium and potassium excretion. UBT positivities were 9% (2-15, 95% confidence interval) for men and 7% (1-12) for women, and positive cases for H. pylori IgG antibodies were 1% (0-3) for men and 3% (0-5) for women, significantly lower than the respective values in Japan. Positive pepsinogen tests in Bali were 0% (0-0) for men and 1% (0-4) for women, also significantly lower than the Japanese figures. Computed values for daily salt excretion were $13.3{\pm}4.1g$ (mean${\pm}$SD) for men and $11.1{\pm}3.1g$ for women, as high as corresponding Japanese consumption values. Moreover, the estimated potassium excretion was $3.2{\pm}0.7g$ for men and $2.8{\pm}0.6g$ for women in Bali, significantly higher than the figures in Japan. There were no associations across genetic polymorphisms of IL-beta, TNF-alpha, and PTPN11 with UBT positivity. The low incidence of stomach cancer in Bali may thus mainly be due to the rare H. pylori infection. Namely, the bacterium infection seems to be a critical factor for gastric cancer rather than host or other environmental factors.

Keywords

References

  1. Ang TL, Fock KM, Dhamodaran S, et al (2005). Racial differences in Helicobacter pylori, serum pepsinogen and gastric cancer incidence in an urban Asian population. J Gastroenterol Hepatol, 20, 1603-9. https://doi.org/10.1111/j.1440-1746.2005.03898.x
  2. Cohen H, Rose S, Lewin DN, et al (1999). Accuracy of four commercially available serologic tests, including two office-based tests and a commercially available 13C urea breath test, for diagnosis of Helicobacter pylori. Helicobacter, 4, 49-53. https://doi.org/10.1046/j.1523-5378.1999.09025.x
  3. Fiore AE (2004). Hepatitis A transmitted by food. Clin Infect Dis, 38, 705-15. https://doi.org/10.1086/381671
  4. Furuta T, Kamata T, Takashima M, et al (1997). Study of transmission routes of Helicobacter pylori in relation to seroprevalence of hepatitis A virus. J Clin Microbiol, 35, 1891-3.
  5. Goh KL, Parasakthi N (2001). The racial cohort phenomenon: seroepidemiology of Helicobacter pylori infection in a multiracial South-East Asian country. Eur J Gastroenterol Hepatol, 13, 177-83. https://doi.org/10.1097/00042737-200102000-00014
  6. Goh KL, Cheah PL, Noorfaridah MD, et al (2007). Ethnicity and H. pylori as risk factors for gastric cancer in Malaysia: a prospective case control study. Am J Gastroenterol, 102, 40-5. https://doi.org/10.1111/j.1572-0241.2006.00885.x
  7. Goto Y, Ando T, Yamamoto K, et al (2006). Association between serum pepsinogens and polymorphism of PTPN11 encoding SHP-2 among Helicobacter pylori seropositive Japanese. Int J Cancer, 118, 203-8. https://doi.org/10.1002/ijc.21338
  8. Graham DY, Klein PD, Evans DJ Jr, et al (1987). Campylobacter pylori detected noninvasively by the 13C-urea breath test. Lancet, 1, 1174-7.
  9. Graham KS, Graham DY (2002). H. pylori-associated Gastrointestinal Disease, 2nd ed, Handbooks in Health Care, Newton, PA.
  10. Hamajima N, Rahimov B, Malikov Y, et al (2008). Associations between a PTPN11 polymorphism and gastric atrophy-opposite in Uzbekistan to that in Japan. Asian Pac J Cancer Prev, 9, 217-20.
  11. International Agency for Research on Cancer (IARC) (1994). Schistosomes, liver flukes, and Helicobacter pylori. IARC monographs programme on the evaluation of carcinogenic risks to humans, Vol. 61, IARC, Lyon.
  12. IARC (2002). Cancer incidence in five continents, Vol.8, IARC, Lyon.
  13. IARC (2003). World cancer report, IARC, Lyon.
  14. Inoue M, Tajima K, Hirose K, et al (1994). Life-style and subsite of gastric cancer - joint effect of smoking and drinking habits. Int J Cancer, 56, 494-9. https://doi.org/10.1002/ijc.2910560407
  15. Ishida Y, Goto Y, Kondo T, et al (2006). Eradication rate of Helicobacter pylori according to genotypes of CYP2C19, IL-1B, and TNF-A. Int J Med Sci, 3, 135-40.
  16. Kato I, Tominaga S, Ito Y, et al (1990). A comparative casecontrol analysis of stomach cancer and atrophic gastritis. Cancer Res, 50, 6559-64.
  17. Kawasaki T, Itoh K, Uezono K, et al (1993). Estimation of 24-hour urinary sodium and potassium excretion from predicted value of 24-hour urinary creatinine excretion and fractional urine sodium/creatinine and potassium/creatinine ratio. Seventh Symposium Salt, 2, 257-62.
  18. Kikuchi S, Nakajima T, Kobayashi O, et al (2000). Effect of age on the relationship between gastric cancer and H. pylori. Jpn J Cancer Res, 91, 774-9. https://doi.org/10.1111/j.1349-7006.2000.tb01012.x
  19. Kiyohara T, Sato T, Totsuka A, et al (2007). Shifting seroepidemiology of hepatitis A in Japan, 1973-2003. Microbiol Immunol, 51, 185-91.
  20. Migita K, Maeda Y, Abiru S, et al (2007). Polymorphisms of interleukin-1beta in Japanese patients with hepatitis B virus infection. J Hepatol, 46, 381-6. https://doi.org/10.1016/j.jhep.2006.09.015
  21. Miki K, Morita M, Sasajima M, et al (2003). Usefulness of gastric cancer screening using the serum pepsinogen test method. Am J Gastroenterol, 98, 735-9. https://doi.org/10.1111/j.1572-0241.2003.07410.x
  22. Ministry of Health, Labour and Welfare, Japan [website on the internet]. The National Health and Nutrition Survey in Japan, 2006 (in Japanese).
  23. Ministry of Health, Labour and Welfare, Japan (2008). The National Health and Nutrition Survey in Japan, 2005 (in Japanese), Daiichi Shuppan, Tokyo.
  24. Ministry of Health, Malaysia. [website on the internet]. The First Report of the National Cancer Registry Cancer Incidence in Malaysia 2002.
  25. Nishimoto IN, Hamada GS, Kowalski LP, et al (2002). Risk factors for stomach cancer in Brazil (1): a case-control study among non-Japanese Brazilians in Sao Paulo. Jpn J Clin Oncol, 32, 277-83. https://doi.org/10.1093/jjco/hyf060
  26. Ohata H, Kitauchi S, Yoshimura N, et al (2004). Progression of chronic atrophic gastritis associated with H. pylori infection increases risk of gastric cancer. Int J Cancer, 109, 138-43. https://doi.org/10.1002/ijc.11680
  27. Oishi Y, Kiyohara Y, Kubo M, et al (2006). The serum pepsinogen test as a predictor of gastric cancer: the Hisayama Study. Am J Epidemiol, 163, 629-37. https://doi.org/10.1093/aje/kwj088
  28. El-omar EM, Cariington M, Chow WH, et al (2000). Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature, 404, 398-402. https://doi.org/10.1038/35006081
  29. Parsonnet J, Friedman GD, Vandersteen DP, et al (1991). H. pylori infection and the risk of gastric carcinoma. N Engl J Med, 325, 1127-31. https://doi.org/10.1056/NEJM199110173251603
  30. Parsonnet J, Friedman GD, Orentreich N, et al (1997). Risk for gastric cancer in people with CagA positive or CagA negative H. pylori infection. Gut, 40, 297-301. https://doi.org/10.1136/gut.40.3.297
  31. Research Group for Population-based Cancer Registration in Japan (RGPCRJ) (2003). Cancer incidence and incidence rates in Japan in 1998: Estimates Based on Data from 12 Population-based Cancer Registries. Jpn J Clin Oncol, 33, 241-5. https://doi.org/10.1093/jjco/hyg044
  32. Santos JC, Ladeira MS, Pedrazzoli J Jr, et al (2012). Relationship of IL-1 and TNF-${\alpha}$ polymorphisms with Helicobacter pylori in gastric diseases in a Brazilian population. Braz J Med Biol Res, 45, 811-7. https://doi.org/10.1590/S0100-879X2012007500099
  33. Sasazuki S, Inoue M, Iwasaki M, et al (2006). Effect of Helicobacter pylori infection combined with CagA and pepsinogen status on gastric cancer development among Japanese men and women: a nested case-control study. Cancer Epidemiol Biomarkers Prev, 15, 1341-7. https://doi.org/10.1158/1055-9965.EPI-05-0901
  34. Serres GD, Cromeans TL, Levesque B, et al (1999). Molecular confirmation of hepatitis A virus from well water: epidemiology and public health implications. JID, 179, 37-43. https://doi.org/10.1086/314565
  35. Soeripto, Indrawati, Indrayanti (2003). Gastro-intestinal cancer in Indonesia. Asian Pac J Cancer Prev, 4, 289-96.
  36. Sugimoto M, Furuta T, Shirai N, et al (2007). Different effects of polymorphisms of tumor necrosis factor-alpha and interleukin-1 beta on development of peptic ulcer and gastric cancer. J Gastroenterol Hepatol, 22, 51-9. https://doi.org/10.1111/j.1440-1746.2006.04442.x
  37. Tahara T, Shibata T, Yamashita H, et al (2012). Synergistic effect of IL-$1{\beta}$ and TNF-${\alpha}$ polymorphisms on the H. pylori-related gastric pre-malignant condition. Hepatogastroenterol, 59, 2416-20.
  38. Tan DS, Fang R, Collett D, et al (1986). A seroepidemiologic study of hepatitis A in Malaysia. Southeast Asian J Trop Med Public Health, 17, 201-4.
  39. Tokudome S, Soeripto, Triningsih FXE, et al (2005a). Rare Helicobacter pylori infection as a factor for the very low stomach cancer incidence in Yogyakarta, Indonesia. Cancer Letters, 219, 57-61. https://doi.org/10.1016/j.canlet.2004.09.043
  40. Tokudome S, Samsuria WD, Soeripto, et al (2005b). Helicobacter pylori infection appears essential for stomach carcinogenesis: observations in Semarang, Indonesia. Cancer Sci, 96, 873-5. https://doi.org/10.1111/j.1349-7006.2005.00122.x
  41. Tsugane S, Sasazuki S, Kobayashi M, et al (2004). Salt and salted food intake and subsequent risk of gastric cancer among middle-aged Japanese men and women. Br J Cancer, 90, 128-34. https://doi.org/10.1038/sj.bjc.6601511
  42. Watase H, Inagaki T, Yoshikawa I, et al (2004). Five years' follow-up study of gastric cancer screening using the serum pepsinogen test method in Adachi City, Japan. Jpn Assoc Cancer Detect Diag, 11, 77-81.
  43. World Cancer Research Fund in association with American Institute for Cancer Research (WCRF/AICR) (2007). Food, nutrition, physical activity, and the prevention of cancer: a global perspective, AICR, Washington, D.C.
  44. Zhao Y, Wang JW, Tanaka T, et al (2013). Association between TNF-${\alpha}$ and IL-$1{\beta}$ genotypes vs Helicobacter pylori infection in Indonesia. World J Gastroenterol, 19, 8758-63. https://doi.org/10.3748/wjg.v19.i46.8758

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