Skip to main content

Advertisement

Log in

Positive Association Between Helicobacter pylori Infection and Metabolic Syndrome in a Korean Population: A Multicenter Nationwide Study

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background and Aim

Helicobacter pylori (H. pylori) infection causes extra-gastrointestinal as well as gastric diseases. This analytical cross-sectional study was performed to investigate the association between H. pylori infection and metabolic syndrome in a Korean population.

Methods

Anthropometric and metabolic data, as well as anti-H. pylori IgG antibodies, were measured in 21,106 subjects who participated in a health checkup between January 2016 and June 2017. The classification of metabolic syndrome followed the revised National Cholesterol Education Program criteria.

Results

After excluding subjects with a history of H. pylori eradication therapy, or gastric symptoms, the seropositivity of H. pylori was 43.2% in 15,195 subjects. H. pylori-positive participants had significantly higher body mass index (BMI), waist circumference, total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), and lower high-density lipoprotein (HDL-C) than did seronegative participants (P < 0.05). After adjusting for confounders, high TC, low HDL-C, and high LDL-C were associated with H. pylori seropositivity. Finally, the prevalence of metabolic syndrome was higher in H. pylori-seropositive subjects than in negative ones (27.2% vs. 21.0%, P < 0.05), and H. pylori seropositivity increased the likelihood of metabolic syndrome (OR 1.19, 95% CI 1.09–1.31, P < 0.001) after adjusting for sex, age, BMI, smoking, residence, household income, and education level. However, the association between H. pylori seropositivity and metabolic syndrome disappeared in those ≥ 65 years old.

Conclusions

H. pylori infection plays an independent role in the pathogenesis of metabolic syndrome in Koreans under 65 years old.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

H. pylori :

Helicobacter pylori

HP :

Helicobacter pylori

MS:

Metabolic syndrome

TC:

Total cholesterol

WC:

Waist circumference

WHO:

World Health Organization

BMI:

Body mass index

BP:

Blood pressure

TG:

Triglycerides

LDL-C:

Low-density lipoprotein cholesterol

HDL-C:

High-density lipoprotein cholesterol

FG:

Fasting glucose

Anti-HP IgG:

Helicobacter pylori immunoglobulin G antibody

NCEP:

National Cholesterol Education Program

OR:

Odds ratio

CI:

Confidence interval

IR:

Insulin resistance

References

  1. McColl KE. Clinical practice. Helicobacter pylori infection. N Engl J Med. 2010;362:1597–1604.

    Article  CAS  Google Scholar 

  2. de Korwin JD, Ianiro G, Gibiino G, Gasbarrini A. Helicobacter pylori infection and extra gastric diseases in 2017. Helicobacter. 2017;22:e12411.

    Article  Google Scholar 

  3. Lim JH, Kim N, Lim SH, Kwon JW, et al. Inverse relationship between Helicobacter pylori infection and asthma among adults younger than 40 years: a cross-sectional study. Medicine (Baltimore). 2016;95:e2609.

    Article  CAS  Google Scholar 

  4. Lim SH, Kim N, Kwon JW, Kim SE, et al. Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a cross-sectional nationwide multicenter study. PLoS One. 2018;13:e0204762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Watanabe S, Hojo M, Nagahara A. Metabolic syndrome and gastrointestinal diseases. J Gastroenterol. 2007;42:267–274.

    Article  PubMed  Google Scholar 

  6. Jinjuvadia R, Antaki F, Lohia P, Liangpunsakul S. The association between nonalcoholic fatty liver disease and metabolic abnormalities in the United States population. J Clin Gastroenterol. 2017;51:160–166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among US adults: NHANES III to NHANES 1999–2006. Diabetes Care. 2011;34:216–219.

    Article  PubMed  Google Scholar 

  8. Nestel P, Lyu R, Low LP, Sheu WH, et al. Metabolic syndrome: recent prevalence in East and Southeast Asian populations. Asia Pac J Clin Nutr. 2007;16:362–367.

    PubMed  Google Scholar 

  9. Lim S, Shin H, Song JH, Kwak SH, et al. Increasing prevalence of metabolic syndrome in Korea: the Korean national health and nutrition examination survey for 1998–2007. Diabetes Care. 2011;34:1323–1328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Oh SW. Obesity and metabolic syndrome in Korea. Diabetes Metab J. 2011;35:561–566.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Tran BT, Jeong BY, Oh JK. The prevalence trend of metabolic syndrome and its components and risk factors in Korean adults: results from the Korean National Health and nutrition examination survey 2008–2013. BMC Public Health. 2017;17:71.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lee SE, Han K, Kang YM, Kim S-O, et al. Trends in the prevalence of metabolic syndrome and its components in South Korea: findings from the Korean National Health Insurance Service Database (2009–2013). PLoS ONE. 2018;13:e0194490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gunji T, Matsuhashi N, Sato H, Fujibayashi K, et al. Helicobacter pylori infection is significantly associated with metabolic syndrome in the Japanese population. Am J Gastroenterol. 2008;103:3005–3010.

    Article  CAS  PubMed  Google Scholar 

  14. Chen LW, Chien CY, Yang KJ, Kuo SF, Chen CH, Chien RN. Helicobacter pylori Infection increases insulin resistance and metabolic syndrome in residents younger than 50 years old: a community-based study. PLoS ONE. 2015;10:e0128671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Naja F, Nasreddine L, Hwalla N, Moghames P, et al. Association of H. pylori infection with insulin resistance and metabolic syndrome among Lebanese adults. Helicobacter. 2012;17:444–451.

    Article  CAS  PubMed  Google Scholar 

  16. Takeoka A, Tayama J, Yamasaki H, Kobayashi M, et al. Impact of Helicobacter pylori immunoglobulin G levels and atrophic gastritis status on risk of metabolic syndrome. PLoS ONE. 2016;11:e0166588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lim SH, Kwon JW, Kim N, Kim GH, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol. 2013;13:104.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kim SY, Ahn JS, Ha YJ, Doh HJ, et al. Serodiagnosis of Helicobacter pylori infection in Korean patients using enzyme-linked immunosorbent assay. J Immunoassay. 1998;19:251–270.

    Article  CAS  PubMed  Google Scholar 

  19. Kim JH, Kim HY, Kim N, Kim SW, et al. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol. 2001;16:969–975.

    Article  CAS  PubMed  Google Scholar 

  20. Yim JY, Kim N, Choi SH, Kim YS, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007;12:333–340.

    Article  PubMed  Google Scholar 

  21. Kim N. Part III Diagnosis 8. Serology In: Kim N, editor. Helicobacter pylori. Singapore: Springer; 2016:113–118.

  22. van Der Ende A, van Der Hulst RWM, Roorda P, Tytgat GNJ, Dankert J. Evaluation of three commercial serological tests with different methodologies to assess Helicobacter pylori infection. J Clin Microbiol. 1999;37:4150–4152.

    PubMed Central  Google Scholar 

  23. Grundy SM, Cleeman JI, Daniels SR, Donato KA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112:2735–2752.

    Article  PubMed  Google Scholar 

  24. World Health Organization. Regional Office for the Western Pacific. The Asia-Pacific perspective: redefining obesity and its treatment. Sydney: Health Communications Australia. 2000:15–21. http://www.who.int/iris/handle/10665/206936. Accessed January 05, 2018.

  25. Sung KC, Rhee EJ, Ryu SH, Beck SH. Prevalence of Helicobacter pylori infection and its association with cardiovascular risk factors in Korean adults. Int J Cardiol. 2005;102:411–417.

    Article  PubMed  Google Scholar 

  26. Nam SY, Ryu KH, Park BJ, Park S. Effects of Helicobacter pylori infection and its eradication on lipid profiles and cardiovascular diseases. Helicobacter. 2015;20:125–132.

    Article  CAS  PubMed  Google Scholar 

  27. Kim TJ, Lee H, Kang M, Kim JE, et al. Helicobacter pylori is associated with dyslipidemia but not with other risk factors of cardiovascular disease. Sci Rep. 2016;6:38015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wald NJ, Law MR, Morris JK, Bagnall AM. Helicobacter pylori infection and mortality from ischaemic heart disease: negative result from a large, prospective study. BMJ. 1997;315:1199–1201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Niemelä S, Karttunen T, Korhonen T, Läärä E, et al. Could Helicobacter pylori infection increase the risk of coronary heart disease by modifying serum lipid concentrations? Heart. 1996;75:573–575.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Chen TP, Hung HF, Chen MK, Lai HH, et al. Helicobacter pylori infection is positively associated with metabolic syndrome in Taiwanese adults: a cross-sectional study. Helicobacter. 2015;20:184–191.

    Article  CAS  PubMed  Google Scholar 

  31. Shin DW, Kwon HT, Kang JM, Park JH, et al. Association between metabolic syndrome and Helicobacter pylori infection diagnosed by histologic status and serological status. J Clin Gastroenterol. 2012;46:840–845.

    Article  PubMed  Google Scholar 

  32. Polyzos SA, Kountouras J, Zavos C, Deretzi G. The association between Helicobacter pylori infection and insulin resistance: a systematic review. Helicobacter. 2011;16:79–88.

    Article  CAS  PubMed  Google Scholar 

  33. Upala S, Jaruvongvanich V, Riangwiwat T, Jaruvongvanich S, Sanguankeo A. Association between Helicobacter pylori infection and metabolic syndrome: a systematic review and meta-analysis. J Dig Dis. 2016;17:433–440. https://doi.org/10.1111/1751-2980.12367.

    Article  CAS  PubMed  Google Scholar 

  34. Park MJ, Choi SH, Kim D, Kang SJ, et al. Association between Helicobacter pylori seropositivity and the coronary artery calcium score in a screening population. Gut Liver. 2011;5:321–327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gallin JI, Kaye D, O’Leary WM. Serum lipids in infection. N Engl J Med. 1969;281:1081–1086.

    Article  CAS  PubMed  Google Scholar 

  36. Feingold KR, Grunfeld C. Role of cytokines in inducing hyperlipidemia. Diabetes. 1992;41:97–101.

    Article  CAS  PubMed  Google Scholar 

  37. Memon RA, Grunfeld C, Moser AH, Feingold KR. Tumor necrosis factor mediates the effects of endotoxin on cholesterol and triglyceride metabolism in mice. Endocrinology. 1993;132:2246–2253.

    Article  CAS  PubMed  Google Scholar 

  38. Migneco A, Ojetti V, Specchia L, Franceschi F, et al. Eradication of Helicobacter pylori infection improves blood pressure values in patients affected by hypertension. Helicobacter. 2003;8:585–589.

    Article  PubMed  Google Scholar 

  39. Gobert AP, Mersey BD, Cheng Y, Blumberg D, Newton JC, Wilson KT. Cutting edge: urease release by Helicobacter pylori stimulates macrophage inducible nitric oxide synthase. J Immunol. 2002;168:6002–6006.

    Article  CAS  PubMed  Google Scholar 

  40. Cammarota G, Figura N, Cianci R, Pasceri V, et al. Is there an antigenic mimicry between arteriosclerotic lesions and H. pylori antigens? Clin Biochem. 2000;33:419–421.

    Article  CAS  PubMed  Google Scholar 

  41. Zhou X, Liu W, Gu M, Zhou H, Zhang G. Helicobacter pylori infection causes hepatic insulin resistance by the c-Jun/miR-203/SOCS3 signaling pathway. J Gastroenterol. 2015;50:1027–1040.

    Article  CAS  PubMed  Google Scholar 

  42. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111–1119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gillum RF. Infection with Helicobacter pylori, coronary heart disease, cardiovascular risk factors, and systemic inflammation: the Third National Health and Nutrition Examination Survey. J Natl Med Assoc. 2004;96:1470–1476.

    PubMed  PubMed Central  Google Scholar 

  44. Nabipour I, Vahdat K, Jafari SM, Pazoki R, Sanjdideh Z. The association of metabolic syndrome and Chlamydia pneumoniae, Helicobacter pylori, cytomegalovirus, and herpes simplex virus type 1: the Persian Gulf Healthy Heart Study. Cardiovasc Diabetol. 2006;5:25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Malamug LR, Karnchanasorn R, Samoa R, Chiu KC. The role of Helicobacter pylori seropositivity in insulin sensitivity, beta cell function, and abnormal glucose tolerance. Scientifica (Cairo). 2014;2014:870165.

    Google Scholar 

  46. Gerig R, Ernst B, Wilms B, Thurnheer M, Schultes B. Gastric Helicobacter pylori infection is associated with adverse metabolic traits in severely obese subjects. Obesity (Silver Spring). 2013;21:535–537.

    Article  CAS  Google Scholar 

  47. Lee JH, Kim N, Chung JI, Kang KP, et al. Long-term follow up of Helicobacter pylori IgG serology after eradication and reinfection rate of H. pylori in South Korea. Helicobacter. 2008;13:288–294.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant (No. 2011-0030001) of the National Research Foundation (NRF) for the Global Core Research Center (GCRC) funded by the Ministry of Science, ICT and Future Planning (MSIP), Republic of Korea.

Author information

Authors and Affiliations

Authors

Contributions

SHL collected and analyzed the data and drafted the article. NK designed and supervised this study and edited this manuscript. JWK provided statistical support and helped to provide the table and figures. NK, SHL, SEK, GHP, JYL, KSP, JES, HJS, DSM, SCC, HJK and JHL helped to collect the data and edited the manuscript. JYY and JSK reviewed the manuscript. All authors have read and approved the final draft of this manuscript.

Corresponding author

Correspondence to Nayoung Kim.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee, the 1964 Declaration of Helsinki, and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all participants in this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lim, S.H., Kim, N., Kwon, J.W. et al. Positive Association Between Helicobacter pylori Infection and Metabolic Syndrome in a Korean Population: A Multicenter Nationwide Study. Dig Dis Sci 64, 2219–2230 (2019). https://doi.org/10.1007/s10620-019-05544-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-019-05544-3

Keywords

Navigation