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Clinical research

Adenovirus 36 seropositivity is related to obesity risk, glycemic control, and leptin levels in Chilean subjects

Abstract

Background

Adenovirus 36 (Ad-36) has been associated to adiposity in animal and in vitro studies. Ad-36 seropositivity has also been reported to contribute to obesity risk in children and adult populations. We investigated the relationship of Ad-36 serology with obesity and metabolic parameters in a Chilean population.

Subjects and methods

Clinical and anthropometric data were obtained and blood samples were drawn from 99 lean (BMI: 18.5–24.9 kg/m2) and 151 obese (BMI > 30 kg/m2) subjects. Laboratory tests included lipid profile as well as glucose, insulin, leptin, and adiponectin levels. Ad-36 seropositivity was evaluated in serum samples by enzyme-linked immunosorbent assay.

Results

Seroprevalence of Ad-36 was higher in the obese group (58%) than in lean controls (34%) demonstrating that individuals previously infected with Ad-36 have higher risk of obesity in the study population (OR: 2.67, 95%CI: 1.58–4.51, p < 0.001). Interestingly, Ad-36 was related to lower concentrations of triglycerides and VLDL cholesterol in lean subjects (p = 0.049) and lower leptin in obese individuals (p = 0.014). Previous Ad-36 infection was also related to lower glycemia, insulinemia, and HOMA-IR (p < 0.05) in obese subjects who were not under antidiabetic drugs.

Conclusions

Our results provide evidence of the contribution of previous Ad-36 infection to an increased risk of obesity in adult Chilean population. Ad-36 seropositivity was also associated to lipid profile, glycemic control, and leptin levels in adult Chilean population.

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References

  1. James WP. The epidemiology of obesity: the size of the problem. J Intern Med. 2008;263:336–52.

    CAS  Article  Google Scholar 

  2. Pasarica M, Dhurandhar NV. Infectobesity: obesity of infectious origin. Adv Food Nutr Res. 2007;52:61–102.

    CAS  Article  Google Scholar 

  3. Esposito S, Preti V, Consolo S, Nazzari E, Principi N. Adenovirus 36 infection and obesity. J Clin Virol. 2012;55:95–100.

    Article  Google Scholar 

  4. Dhurandhar NV, Whigham LD, Abbott DH, Schultz-Darken NJ, Israel BA, Bradley SM, et al. Human adenovirus Ad-36 promotes weight gain in male rhesus and marmoset monkeys. J Nutr. 2002;132:3155–60.

    CAS  Article  Google Scholar 

  5. Atkinson RL, Lee I, Shin HJ, He J. Human adenovirus-36 antibody status is associated with obesity in children. Int J Pediatr Obes. 2010;5:157–60.

    Article  Google Scholar 

  6. 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. 2010;34:89–93.

    Article  Google Scholar 

  7. Kocazeybek B, Dinc HO, Ergin S, Saribas S, Ozcabi BT, Cizmecigil U, et al. Evaluation of adenovirus-36 (Ad-36) antibody seropositivity and adipokine levels in obese children. Microb Pathog. 2017;108:27–31.

    CAS  Article  Google Scholar 

  8. Tosh AK, Wasserman MG, McLeay II MT, Tepe SK. Human adenovirus-36 seropositivity and obesity among Midwestern US adolescents. Int J Adolesc Med Health. 2017. https://doi.org/10.1515/ijamh-2017-0126.

  9. Atkinson RL, Dhurandhar NV, Allison DB, Bowen RL, Israel BA, Albu JB, et al. Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes. 2005;29:281–6.

    CAS  Article  Google Scholar 

  10. 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. 2009;33:1402–9.

    CAS  Article  Google Scholar 

  11. Karamese M, Altoparlak U, Turgut A, Aydogdu S, Karamese SA. The relationship between adenovirus-36 seropositivity, obesity and metabolic profile in Turkish children and adults. Epidemiol Infect. 2015;143:3550–6.

    CAS  Article  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. 2011;19:220–1.

    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. 2010;34:302–8.

    CAS  Article  Google Scholar 

  14. 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. 2012;36:281–5.

    CAS  Article  Google Scholar 

  15. Zhou Y, Pan Q, Wang X, Zhang L, Xiao F, Guo L. The relationship between human adenovirus 36 and obesity in Chinese Han population. Biosci Rep. 2018;38:BSR20180553.

  16. Xu MY, Cao B, Wang DF, Guo JH, Chen KL, Shi M, et al. Human adenovirus 36 infection increased the risk of obesity: a meta-analysis update. Medicine. 2015;94:e2357.

    Article  Google Scholar 

  17. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in adults (Adult Treatment Panel III) final report. Circulation. 2002;106:3143–421.

    Article  Google Scholar 

  18. Chang X, Jiao Y, Lu J-F, Nurbiya N, Guan Y-Q. The regulation of adenovirus type 36 infection and progranulin expression in Uygur obese patients. J Xian Jiaotong Univ (Med Sci). 2015;36:219–24.

  19. 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.

    CAS  Article  Google Scholar 

  20. 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.

    CAS  Article  Google Scholar 

  21. Dhurandhar NV, Israel BA, Kolesar JM, Mayhew GF, Cook ME, Atkinson RL. Increased adiposity in animals due to a human virus. Int J Obes Relat Metab Disord. 2000;24:989–96.

    CAS  Article  Google Scholar 

  22. Ponterio E, Cangemi R, Mariani S, Casella G, De Cesare A, Trovato FM, et al. Adenovirus 36 DNA in human adipose tissue. Int J Obes. 2015;39:1761–4.

    CAS  Article  Google Scholar 

  23. 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;26:969–78.

    CAS  Article  Google Scholar 

  24. Vangipuram SD, Sheele J, Atkinson RL, Holland TC, Dhurandhar NV. A human adenovirus enhances preadipocyte differentiation. Obes Res. 2004;12:770–7.

    CAS  Article  Google Scholar 

  25. Vangipuram SD, Yu M, Tian J, Stanhope KL, Pasarica M, Havel PJ, et al. Adipogenic human adenovirus-36 reduces leptin expression and secretion and increases glucose uptake by fat cells. Int J Obes. 2007;31:87–96.

    CAS  Article  Google Scholar 

  26. Rogers PM, Fusinski KA, Rathod MA, Loiler SA, Pasarica M, Shaw MK, et al. Human adenovirus Ad-36 induces adipogenesis via its E4 orf-1 gene. Int J Obes. 2008;32:397–406.

    CAS  Article  Google Scholar 

  27. 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;57:535–44.

    CAS  Article  Google Scholar 

  28. 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;30:184–90.

    CAS  Article  Google Scholar 

  29. Trovato FM, Catalano D, Garozzo A, Martines GF, Pirri C, Trovato GM. ADV36 adipogenic adenovirus in human liver disease. World J Gastroenterol. 2014;20:14706–16.

    CAS  Article  Google Scholar 

  30. Wang ZQ, Cefalu WT, Zhang XH, Yu Y, Qin J, Son L, et al. Human adenovirus type 36 enhances glucose uptake in diabetic and nondiabetic human skeletal muscle cells independent of insulin signaling. Diabetes. 2008;57:1805–13.

    CAS  Article  Google Scholar 

  31. Lin WY, Dubuisson O, Rubicz R, Liu N, Allison DB, Curran JE, et al. Long-term changes in adiposity and glycemic control are associated with past adenovirus infection. Diabetes Care. 2013;36:701–7.

    Article  Google Scholar 

  32. Dhurandhar NV. Insulin sparing action of adenovirus 36 and its E4orf1 protein. J Diabetes Complications. 2013;27:191–9.

    Article  Google Scholar 

  33. Dhurandhar EJ, Dubuisson O, Mashtalir N, Krishnapuram R, Hegde V, Dhurandhar NV. E4orf1: a novel ligand that improves glucose disposal in cell culture. PLoS One. 2011;6:e23394.

    CAS  Article  Google Scholar 

  34. McMurphy TB, Huang W, Xiao R, Liu X, Dhurandhar NV, Cao L. Hepatic expression of adenovirus 36 E4ORF1 improves glycemic control and promotes glucose metabolism through AKT activation. Diabetes. 2017;66:358–71.

    CAS  Article  Google Scholar 

  35. Ergin S, Altan E, Pilanci O, Sirekbasan S, Cortuk O, Cizmecigil U, et al. The role of adenovirus 36 as a risk factor in obesity: the first clinical study made in the fatty tissues of adults in Turkey. Microb Pathog. 2015;80:57–62.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank the volunteers for their participation in this research. The authors also thank physicians, nurses, and administrative staff from the Centro de Tratamiento de la Obesidad (CTO) and the Laboratorio Clinico of the Clinica Alemana de Temuco. The authors thank Dr. Soledad Reyes and Lilian Saravia for the support in obtaining biological samples. This research was funded by FONDECYT, grant number 11150445.

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Correspondence to Alvaro Cerda.

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Sapunar, J., Fonseca, L., Molina, V. et al. Adenovirus 36 seropositivity is related to obesity risk, glycemic control, and leptin levels in Chilean subjects. Int J Obes 44, 159–166 (2020). https://doi.org/10.1038/s41366-019-0321-4

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