Skip to main content

Influence of Helicobacter pylori infection on metabolic parameters and body composition of dyslipidemic patients

Internal and Emergency Medicine volume 9, pages 767–772 (2014)Cite this article

Abstract

Helicobacter pylori infection may contribute to the development of extra-gastroduodenal diseases. The aim of this study was to explore whether this infection could influence metabolic parameters and body composition of dyslipidemic patients. In an 8-month period, 155 patients attended our clinic; 110 patients (48 men and 62 women, age 35–55 years) fulfilled inclusion criteria. Metabolic parameters were determined by routine tests and body composition by anthropometry and bioelectrical impedance analysis. The H. pylori and CagA infectious status were examined serologically. Sixty-one patients (55.4 %) had serum antibodies to H. pylori and 30 infected patients (49.1 %) had anti-CagA antibodies. The mean percentage of fat mass and level of high-density protein cholesterol in seropositive patients were significantly lower than those measured in seronegative ones (P = 0.008 and P < 0.001, respectively). The mean glucose concentration in patients with anti-H. pylori serum IgG was significantly higher than in uninfected patients (P = 0.021). No significant difference was observed regarding the other parameters. The CagA status did not influence any of the considered parameters. Our results are in agreement with those of other studies; however, the level of concordance of results reported in the various publications on this topic is very low, presumably from differences concerning the age, alimentary habits and possible presence of different pathologies in the groups studied. The most plausible hypothesis for the observed alterations may exist in the low-grade systemic inflammatory status of infected individuals, which may influence the fat turnover and support the insulin resistance with consequent alteration of glucose metabolism.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Graham DY (1989) Campylobacter pylori and peptic ulcer disease. Gastroenterology 96:615–625

    PubMed  CAS  Google Scholar 

  2. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG (1991) Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 338:1175–1176

    PubMed  Article  CAS  Google Scholar 

  3. Parsonnet J (1993) Helicobacter pylori and gastric cancer. Gastroenterol Clin North Am 22:89–104

    PubMed  CAS  Google Scholar 

  4. Mendall MA, Goggin PM, Molineaux N, Levy J, Toosy T, Strachan D, Camm AJ, Northfield TC (1994) Relation of Helicobacter pylori infection and coronary heart disease. Br Heart J 71:437–439

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  5. Patel P, Carrington D, Strachan DP, Leatham E, Goggin P, Northfield TC, Mendall MA (1994) Fibrinogen: a link between chronic infection and coronary heart disease. Lancet 343:1634–1635

    PubMed  Article  CAS  Google Scholar 

  6. Tebbe B, Geilen CC, Schulzke JD, Bojarski C, Radenhausen M, Orfanos CE (1996) Helicobacter pylori infection and chronic urticaria. J Am Acad Dermatol 34:685–686

    PubMed  Article  CAS  Google Scholar 

  7. Van Lente F (2000) Markers of inflammation as predictors in cardiovascular disease. Clin Chim Acta 293:31–52

    PubMed  Article  Google Scholar 

  8. Niemelä S, Karttunen T, Korhonen T, Laara E, Karttunen R, Ikaheimo M, Kesaniemi YA (1996) Could Helicobacter pylori infection increase the risk of coronary heart disease by modifying serum lipid concentrations? Heart 75:573–575

    PubMed  Article  PubMed Central  Google Scholar 

  9. Hoffmeister A, Rothenbacher D, Bode G, Persson K, März W, Nauck MA, Brenner H, Hombach V, Koenig W (2001) Current infection with Helicobacter pylori but not seropositivity to Chlamydia pneumoniae or cytomegalovirus is associated with an atherogenic modified lipid profile. Arterioscler Thromb Vasc Biol 21:427–432

    PubMed  Article  CAS  Google Scholar 

  10. Murray LJ, Bamford KB, O’Reilly DP, McCrum EE, Evans AE (1995) Helicobacter pylori infection: relation with cardiovascular risk factors, ischaemic heart disease, and social class. Br Heart J 74:497–501

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  11. Laurila A, Bloigu A, Nayha S, Hassi J, Leinonen M, Saikku P (1999) Association of Helicobacter pylori infection with elevated serum lipids. Atherosclerosis 142:207–210

    PubMed  Article  CAS  Google Scholar 

  12. Zhu J, Quyyumi AA, Muhlestein JB, Nieto FJ, Horne BD, Zalles-Ganley A, Anderson JL, Epstein SE (2002) Lack of association of Helicobacter pylori infection with coronary artery disease and frequency of acute myocardial infarction or death. Am J Cardiol 89:155–158

    PubMed  Article  CAS  Google Scholar 

  13. Arslan E, Atilgan H, Yavaşoğlu I (2009) The prevalence of Helicobacter pylori in obese subjects. Eur J Intern Med 20:695–697. doi:10.1016/j.ejim.2009.07.013

    PubMed  Article  Google Scholar 

  14. Ioannou GN, Weiss NS, Kearney DJ (2005) Is Helicobacter pylori seropositivity related to body mass index in the United States? Aliment Pharmacol Ther 21:765–772

    PubMed  Article  CAS  Google Scholar 

  15. Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, Massone A, Papini E, Xiang Z, Figura N, Rappuoli R (1993) Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA 90:5791–5795

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  16. Xiang Z, Bugnoli M, Ponzetto A, Morgando A, Figura N, Covacci A, Petracca R, Pennatini C, Censini S, Armellini D, Rappuoli R (1993) Detection in an enzyme immunoassay of an immune response to a recombinant fragment of the 128 kilodalton protein (CagA) of Helicobacter pylori. Eur J Clin Microbiol Infect Dis 12:739–745

    PubMed  Article  CAS  Google Scholar 

  17. Kosunen TU, Seppälä K, Sarna S, Sipponen P (1992) Diagnostic value of decreasing IgG, IgA, and IgM antibody titres after eradication of Helicobacter pylori. Lancet 339:893–895

    PubMed  Article  CAS  Google Scholar 

  18. Ching CK, Wong BC, Kwok E, Ong L, Covacci A, Lam SK (1996) Prevalence of CagA-bearing Helicobacter pylori strains detected by the anti-CagA assay in patients with peptic ulcer disease and in controls. Am J Gastroenterol 91:949–953

    PubMed  CAS  Google Scholar 

  19. Figura N, Franceschi F, Santucci A, Bernardini G, Gasbarrini G, Gasbarrini A (2010) Extragastric manifestations of Helicobacter pylori infection. Helicobacter 15:60–68

    PubMed  Article  Google Scholar 

  20. Jia EZ, Zhao FJ, Hao B, Zhu TB, Wang LS, Chen B, Cao KJ, Huang J, Ma WZ, Yang ZJ, Zhang G (2009) Helicobacter pylori infection is associated with decreased serum levels of high density lipoprotein, but not with the severity of coronary atherosclerosis. Lipids Health Dis 8:59. doi:10.1186/1476-511X-8-59

    PubMed  Article  PubMed Central  Google Scholar 

  21. Kanbay M, Gür G, Yücel M, Yilmaz U, Boyacioğlu S (2005) Does eradication of Helicobacter pylori infection help normalize serum lipid and CRP levels? Dig Dis Sci 50:1228–1231

    PubMed  Article  CAS  Google Scholar 

  22. Gallin JL, Kaye D, O’Leary WM (1969) Serum lipid in infection. N Engl J Med 281:1081–1086

    PubMed  Article  CAS  Google Scholar 

  23. Alvarez C, Ramos A (1986) Lipids, lipoproteins, and apoproteins in serum during infection. Clin Chem Res 32:142–145

    CAS  Google Scholar 

  24. Grunfeld C, Gulli R, Moser AH, Gavin LA, Feingold KR (1989) Effect of tumour necrosis factor administration in vivo on lipoprotein lipase activity in various tissues of the rat. J Lipid Res 30:579–585

    PubMed  CAS  Google Scholar 

  25. Ekesbo R, Nilsson PM, Lindholm LH, Persson K, Wadstrom T (2000) Combined seropositivity for H. pylori and C. pneumoniae is associated with age, obesity and social factors. J Cardiovasc Risk 7:191–195

    PubMed  CAS  Google Scholar 

  26. Crabtree JE, Farmery SM, Lindley IJD, Figura N, Peichl P, Tompkins DS (1994) CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J Clin Pathol 47:945–950

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  27. Rasmi Y, Raeisi S, Seyyed Mohammadzad MH (2012) Association of inflammation and cytotoxin-associated gene A positive strains of Helicobacter pylori in cardiac syndrome x. Helicobacter 17:116–120

    PubMed  Article  CAS  Google Scholar 

  28. Perri F, Clemente R, Festa V, De Ambrosio CC, Quitadamo M, Fusillo M, Grossi E, Andriulli A (1999) Serum tumour necrosis factor-alpha is increased in patients with Helicobacter pylori infection and CagA antibodies. Ital J Gastroenterol Hepatol 31:290–294

    PubMed  CAS  Google Scholar 

  29. Chimienti G, Russo F, Lamanuzzi BL, Nardulli M, Messa C, Di Leo A, Correale M, Pepe G (2003) Helicobacter pylori is associated with modified lipid profile: impact on Lipoprotein(a). Clin Biochem 36:359–365

    PubMed  Article  CAS  Google Scholar 

  30. Lopes-Virella MF (1993) Interactions between bacterial lipopolysaccharide and serum lipoproteins and their possible role in coronary heart disease. Eur Heart J 14:118–124

    PubMed  CAS  Google Scholar 

  31. Manco M, Putignani L, Bottazzo GF (2010) Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev 31:817–844

    PubMed  Article  CAS  Google Scholar 

  32. Oshima T, Ozono R, Yano Y, Oishi Y, Teragawa H, Higashi Y, Yoshizumi M, Masayuki Kambe M (2005) Association of Helicobacter pylori infection with systemic inflammation and endothelial dysfunction in healthy male subjects. JACC 45:1219–1222

    PubMed  Article  CAS  Google Scholar 

  33. Jin W, Sun G-S, Marchadier D, Octaviani E, Glick JM, Rader DJ (2003) Endothelial cells secrete triglyceride lipase and phospholipase activities in response to cytokines as a result of endothelial lipase. Circ Res 92:644–650

    PubMed  Article  CAS  Google Scholar 

  34. Riwanto M, Landmesser U (2013) High-density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J Lipid Res [Epub ahead of print]

  35. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM (1995) Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 95:2409–2415

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  36. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111–1119

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  37. Ojetti V, Pellicano R, Fagoonee S, Migneco A, Berrutti M, Gasbarrini A (2010) Helicobacter pylori infection and diabetes. Minerva Med 101:115–119

    PubMed  CAS  Google Scholar 

  38. Burghen GA, Murrell LR, Whitington GL, Klyce MK, Burstein S (1992) Acid peptic disease in children with type I diabetes mellitus: a complicating relationship. Am J Dis Child 146:718–722

    PubMed  Article  CAS  Google Scholar 

  39. Nweneka CV, Prentice AM (2011) Helicobacter pylori infection and circulating ghrelin levels: a systematic review. BMC Gastroenterol 11:7–25

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  40. Lane JA, Murray LJ, Harvey IM, Donovan JL, Nair P, Harvey RF (2011) Randomised clinical trial: Helicobacter pylori eradication is associated with a significantly increased body mass index in a placebo-controlled study. Aliment Pharmacol Ther 33:922–929

    PubMed  Article  CAS  Google Scholar 

  41. Vahdat K, Azizi F, Zandi K, Assadi M, Nabipour I (2012) Chronic inflammation is correlated with percentage of body fat independent of the burden of infection. Inflammation 35:1322–1329

    PubMed  Article  CAS  Google Scholar 

  42. Kebapcilar L, Sari I, Renkal AH, Alacacioglu A, Yuksel A, Ilhan E, Alkan B, Yuksel D, Kozaci DL, Gunay N (2009) The influence of Helicobacter pylori eradication on leptin, soluble CD40 ligand, oxidative stress and body composition in patients with peptic ulcer disease. Intern Med 48:2055–2059

    PubMed  Article  Google Scholar 

  43. Menchine MD, Arora S, Camargo CA, Ginde AA (2011) Prevalence of undiagnosed and suboptimally controlled diabetes by point-of-care HbA1C in unselected emergency department patients. Acad Emerg Med 18:326–329

    PubMed  Article  PubMed Central  Google Scholar 

  44. Danesh J, Peto R (1998) Risk factors for coronary heart disease and infection with Helicobacter pylori: meta-analysis of 18 studies. BMJ 7138:1130–1132

    Article  Google Scholar 

  45. Cho I, Blaser MJ, François F, Mathew JP, Ye XY, Goldberg JD, Bini EJ (2005) Helicobacter pylori and overweight status in the United States: data from the Third National Health and Nutrition Examination Survey. Am J Epidemiol 162:79–84

    Article  Google Scholar 

  46. Furuta T, Shirai N, Xiao F, Takashima M, Hanai H (2002) Effect of Helicobacter pylori infection and its eradication on nutrition. Aliment Pharmacol Ther 16:799–806

    PubMed  Article  CAS  Google Scholar 

  47. Azuma T, Suto H, Ito Y, Muramatsu A, Ohtani M, Dojo M, Yamazaki Y, Kuriyama M, Kato T (2002) Eradication of Helicobacter pylori infection induces an increase in body mass index. Aliment Pharmacol Ther 16:240–244

    PubMed  Article  Google Scholar 

  48. Kagawa M, Kerr D, Uchida H, Binns C (2009) Differences in the relationship between BMI and percentage body fat between Japanese and Australian-Caucasian young men. Br J Nutr 95:1002–1007

    Article  Google Scholar 

Download references

Conflict of interest

None.

Author information

Affiliations

  1. Department of Molecular and Developmental Medicine, University of Siena, Siena, Italy

    Elena Moretti & Giulia Collodel

  2. Department of Medical, Surgical and Neurological Sciences, University of Siena and Policlinico S. Maria alle Scotte, Viale Bracci, Siena, Italy

    Stefano Gonnelli, Mariastella Campagna, Ranuccio Nuti & Natale Figura

Authors
  1. Elena Moretti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefano Gonnelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariastella Campagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ranuccio Nuti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Giulia Collodel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natale Figura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natale Figura.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Moretti, E., Gonnelli, S., Campagna, M. et al. Influence of Helicobacter pylori infection on metabolic parameters and body composition of dyslipidemic patients. Intern Emerg Med 9, 767–772 (2014). https://doi.org/10.1007/s11739-013-1043-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11739-013-1043-6

Keywords

  • BMI
  • CagA
  • Dyslipidemia
  • Fat mass
  • Glucose
  • H. pylori infection
  • HDL-cholesterol