Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Clinical and laboratory characteristics of 1179 Czech adolescents evaluated for antibodies to human adenovirus 36

International Journal of Obesity volume 38, pages 285–291 (2014)Cite this article

Subjects

Abstract

Background:

Human adenovirus 36 (Adv36) is associated with obesity in children. Most prior studies have been small and the association of Adv36 status with markers of metabolic risks has been inconsistent.

Objectives:

To determine the prevalence of Adv36 antibodies in different weight categories of adolescents and to evaluate the association of Adv36 infection with anthropometric parameters and cardiometabolic health risks.

Subjects and methods:

In 1179 Czech adolescents (85 underweight, 506 normal weight, 160 overweight and 428 obese), the following variables were evaluated: anthropometric (body weight, height, body mass index, circumferences, fat mass), blood pressure, biochemical and hormonal (lipid profile, glucose, insulin, liver enzymes, adiponectin) and Adv36 antibodies (enzyme-linked immunosorbent assay).

Results:

Of the total cohort, 26.5% were positive for Adv36 antibodies (underweight: 22.3%; normal weight: 21.5%; overweight: 40.0% and obese: 28.0%). The odds ratio for Adv36 antibody positivity evaluated vs normal weight was 2.61 for overweight (95% confidence interval (CI): 1.77–3.86, P<0.001) and 1.46 for obesity (95% CI: 1.07–1.99, P=0.016). A significantly higher prevalence of Adv36 infection was observed in female subjects (32.5%) in comparison to male subjects (19.7%; P<0.001). Adv36 positivity of the whole cohort was significantly related to body weight (P=0.042), body mass index (P=0.015), hip circumference (P=0.004), body height z-score (P=0.029), and total body fat (P=0.000) and trunk fat (P=0.000). Adv36 antibody-positive girls demonstrated significantly higher body height (167.8 vs 165.0 cm, P=0.01) and waist circumference (77.0 vs 72.0 cm, P=0.01). Infected adolescents exhibited significantly higher levels of total cholesterol (TC) and low-density lipoprotein cholesterol (LDL-C), but lower levels of blood glucose. Liver enzymes were significantly increased only in Adv36-positive boys.

Conclusion:

These results demonstrated an association of Adv36 antibodies with obesity and an even greater association with overweight. Adv36 positivity was related to increased fat mass, levels of TC and LDL-C, but to decreased level of blood glucose. No relation to adiponectin levels was revealed.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Lobstein T, Baur L, Uauy R, IASO International Obesity Task Force. Obesity in children and young people: a crisis in public health. Obes Rev 2004; 5 (Suppl 1): 4–104.

    Article  PubMed  Google Scholar 

  2. McAllister EJ, Dhurandhar NV, Keith SW, Aronne LJ, Barger J, Baskin M et al. Ten putative contributors to the obesity epidemic. Crit Rev Food Sci Nutr 2009; 49: 868–913.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Dhurandar NV . Infectobesity: obesity of infectious origin. J Nutr 2001; 131: 2794S–2797S.

    Article  Google Scholar 

  4. Pasarica M, Mashtalir N, McAllister EJ, Kilroy GE, Koska J, Permana P et al. Adipogenic human adenovirus Ad-36 induces commitment, differentiation, and lipid accumulation in human adipose-derived stem cells. Stem Cells 2008; 26: 969–978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Atkinson RL, Dhurandhar NV, Allison DB, Bowen RL, Israel BA, Albu JB et al. Human adenovirus AD-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes (Lond) 2005; 29: 281–286.

    Article  CAS  Google Scholar 

  6. Yamada T, Hara K, Kadowaki T . Association of adenovirus 36 infection with obesity and metabolic markers in humans: a meta-analysis of observational studies. PLoS One 2012; 7: e42031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Almgren M, Atkinson R, He J, Hilding A, Hagman E, Wolk A et al. Adenovirus-36 is associated with obesity in children and adults in Sweden as determined by rapid ELISA. PLoS One 2012; 7: e41652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Atkinson RL . Prevalence of infection with adenovirus-36 in Belgium and Holland and association with obesity. Obesity (Silver Spring, MD) 2011; 19: 2.

    Article  Google Scholar 

  9. Trovato GM, Castro A, Tonzuso A, Garozzo A, Martines GF, Pirri C et al. Human obesity relationship with Ad36 adenovirus and insulin resistance. Int J Obes (Lond) 2009; 33: 1402–1409.

    Article  CAS  Google Scholar 

  10. Trovato GM, Martines GF, Garozzo A, Tonzuso A, Timpanaro R, Pirri C et al. AD36 adipogenic adenovirus in human non-alcoholic fatty liver disease. Liver Int 2010; 30: 184–190.

    Article  CAS  PubMed  Google Scholar 

  11. Na HN, Kim J, Lee HS, Shim KW, Kimm H, Jee SH et al. Association of human adenovirus-36 in overweight Korean adults. Int J Obes (Lond) 2012; 36: 281–255.

    Article  CAS  Google Scholar 

  12. Goossens VJ, deJager SA, Grauls GE, Gielen M, Vlietinck RF, Derom CA et al. Lack of evidence for the role of human adenovirus-36 in obesity in a European cohort. Obesity (Silver Spring, MD) 2011; 19: 220–221.

    Article  Google Scholar 

  13. Broderick MP, Hansen CJ, Irvine M, Metzgar D, Campbell K, Baker C et al. Adenovirus 36 seropositivity is strongly associated with race and gender, but not obesity, among US military personnel. Int J Obes (Lond) 2010; 34: 302–308.

    Article  CAS  Google Scholar 

  14. Atkinson RL, Lee I, Shin HJ, He J . Human adenovirus-36 antibody status is associated with obesity in children. Int J Pediatr Obes 2010; 5: 157–160.

    Article  PubMed  Google Scholar 

  15. Na HN, Hong YM, Kim J, Kim HK, Jo I, Nam JH . Association between human adenovirus-36 and lipid disorders in Korean schoolchildren. Int J Obes (Lond) 2010; 34: 89–93.

    Article  Google Scholar 

  16. Gabbert C, Donohue M, Arnold J, Schwimmer JB . Adenovirus 36 and obesity in children and adolescents. Pediatrics 2010; 126: 721–726.

    Article  PubMed  Google Scholar 

  17. Dhurandhar NV, Israel BA, Kolesar JM, Mayhew G, Cook ME, Atkinson RL . Transmisibility of adenovirus-induced adiposity in a chicken model. Int J Obes 2001; 25: 990–996.

    Article  CAS  Google Scholar 

  18. Trovato GM, Martines GF, Trovato FM, Pirri C, Pace P, Garozzo A et al. Adenovirus-36 seropositivity enhances effects of nutritional intervention on obesity, bright liver, and insulin resistance. Dig Dis Sci 2012; 57: 535–544.

    Article  CAS  PubMed  Google Scholar 

  19. Trovato GM, Martines GF, Garozzo A, Tonzuso A, Timpanaro R, Pirri C et al. AD36 adipogenic adenovirus in human non-alcoholic fatty liver disease. Liver Int 2010; 30: 184–190.

    Article  CAS  PubMed  Google Scholar 

  20. Kobzova J, Vignerova J, Blaha P, Krejcovsky L, Riedlova J . The 6th nationwide anthropological survey of children and adolescents in the Czech Republic in 2001. Cent Eur J Public Health 2004; 12: 126–130.

    CAS  PubMed  Google Scholar 

  21. Report of a WHO Expert Committee. Physical status: the use and interpretation of anthropometry. World Health Organ Tech Rep Ser 1995; 854: 429–431.

    Google Scholar 

  22. Bergman RN, Stefanovski D, Buchanan TA, Sumner AE, Reynolds JC, Sebring NG et al. A better index of body adiposity. Obesity (Silver Spring, MD) 2011; 19: 1083–1089.

    Article  PubMed Central  Google Scholar 

  23. Haas GM, Liepold E, Schwandt P . Percentile curves for fat patterning in German adolescents. World J Pediatr 2011; 7: 16–23.

    Article  PubMed  Google Scholar 

  24. Zamrazilová H, Hlavatý P, Dušátková L, Sedláčková B, Aldhoon Hainerová I, Kunešová M et al. A new simple method for estimating trunk and visceral fat by bioelectrical impedance: comparison with magnetic resonance imaging and dual X-ray absorptiometry in Czech adolescents. Cas Lek Cesk 2010; 149: 417–422.

    PubMed  Google Scholar 

  25. National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescent. The fourth report on the diagnosis, evaluation and treatment of high blood pressure in children and adolescents. Pediatrics 2004; 114: 555–576.

    Article  Google Scholar 

  26. Chapman SJ, Hill AVS. Human genetic susceptibility to infectious disease. Nat Rev Genet 2012; 13: 175–188.

    Article  CAS  PubMed  Google Scholar 

  27. James CB, Vanderpool EA, Roane P . Acceleration of adenovirus replication and increased virion production by treatment with the steroid hormone 17 beta-estradiol. Microbiol Immunol 1992; 36: 99–103.

    Article  CAS  PubMed  Google Scholar 

  28. Vindrieux D, Le Corre L, Hsieh JT, Métivier R, Escobar P, Caicedo A et al. Coxsackie and adenovirus receptor is a target and a mediator of estrogen action in breast cancer. Endocr Relat Cancer 2011; 18: 311–321.

    Article  CAS  PubMed  Google Scholar 

  29. Wolfrum N, Greber UF . Adenovirus signalling in entry. Cell Microbiol 2013; 15: 53–62.

    Article  CAS  PubMed  Google Scholar 

  30. Rogers PM, Mashtalir N, Rathod MA, Dubuisson O, Wang Z, Dasuri K et al. Metabolically favorable remodeling of human adipose tissue by human adenovirus type 36. Diabetes 2008; 57: 2321–2331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the grant: NT/13792-4 Internal Grant Agency of the Ministry of Health of the Czech Republic.

Author information

Author notes

  1. I Aldhoon-Hainerová and H Zamrazilová: These authors contributed equally to this work.

Authors and Affiliations

  1. Obesity Management Center, Institute of Endocrinology, Prague, Czech Republic

    I Aldhoon-Hainerová, H Zamrazilová, L Dušátková, B Sedláčková, P Hlavatý, M Kunešová & V Hainer

  2. Department of Pediatrics and Center for Research of Diabetes, Metabolism and Nutrition, Third Faculty of Medicine, Charles University, Prague, Czech Republic

    I Aldhoon-Hainerová

  3. Obetech Obesity Research Center, Richmond, VA, USA

    R L Atkinson & Z P Lee

  4. Faculty of Science, Charles University, Prague, Czech Republic

    L Dušátková & B Sedláčková

Authors
  1. I Aldhoon-Hainerová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H Zamrazilová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R L Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L Dušátková
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B Sedláčková
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P Hlavatý
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Z P Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M Kunešová
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. V Hainer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I Aldhoon-Hainerová.

Ethics declarations

Competing interests

Dr R Atkinson is the owner and Dr Z Lee is Laboratory Director of Obetech, LLC, a company that provides assays for adenoviruses associated with obesity and has several patents in the area of virus-induced obesity. Dr Atkinson also is Co-Editor of the International Journal of Obesity. Dr IA Hainerová, Dr H Zamrazilová, Dr L Dušátková, Dr B Sedláčková, Dr P Hlavatý, Dr M Kunešová and Dr V Hainer declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aldhoon-Hainerová, I., Zamrazilová, H., Atkinson, R. et al. Clinical and laboratory characteristics of 1179 Czech adolescents evaluated for antibodies to human adenovirus 36. Int J Obes 38, 285–291 (2014). https://doi.org/10.1038/ijo.2013.72

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2013.72

Keywords

This article is cited by

Search

Advanced search

Quick links