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Epidemiology and Population Health

Adenovirus 36 prevalence and association with human obesity: a systematic review

Abstract

Introduction

Obesity has numerous etiologies and includes biological factors. Studies have demonstrated that the human adenovirus subtype 36 (Adv36) is an adipogenic agent and causes metabolic alterations. Study results on the prevalence of Adv36 and clinical effects in humans vary substantially. This was a systematic review to summarize the studies on the prevalence of Adv36 infection and its association with human obesity.

Methods

A systematic literature review was conducted using the preferred reporting items for systematic reviews and meta-analysis (PRISMA). Observational or experimental studies found in the Medline, Embase, LILACS, Science Direct and SciELO databases that presented results on the prevalence of Adv36 in humans were included.

Results

Thirty-seven studies were screened. A total of 10,300 adults aged 18–70 years and 4585 children and adolescents aged 3–18 years were assessed. The average prevalence of Adv36 among adults was 22.9%, ranging from 5.5% to 49.8%. Among children and adolescents, the average prevalence of Adv36 was 28.9%, ranging from 7.5% to 73.9%. There was a positive statistical relationship between Adv36 and weight gain, obesity, or metabolic changes in 31 studies. However, in four studies there was no association with obesity, and in one, no association was described. One of the studies showed an inverse correlation, i.e., Adv36 was a protective factor against obesity.

Conclusion

Strong evidence suggested a positive association between viral infection and obesity. However, due to the multi-causality of obesity and heterogeneity of studies, diagnostic tests should be standardized and easily accessible by the population to estimate the overall prevalence of Adv36 infection and its association with obesity.

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Fig. 1: Flowchart showing study selection process.
Fig. 2: Geographic distribution of the conducted studies.

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References

  1. Obesity: preventing and managing the global epidemic. Report of a WHO Consultation (WHO Technical Report Series 894). Authors: World Health Organization. 252. Publication date: 2000.

  2. WHO. Obesity and overweight. Updated 16 Feb 2018. Available at: http://www.who.int/news-room/factsheets/detail/obesity-and-overweight. Accessed 5 Jan 2020.

  3. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis. Lancet. 2014; 384:766–81. https://doi.org/10.1016/S0140-6736(14)60460-8.

  4. Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics. 2015;33:673–89. https://doi.org/10.1007/s40273-014-0243-x.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hainer V, Zamrazilová H, Kunešová M, Bendlová B, Aldhoon-Hainerová I. Obesity and infection: reciprocal causality. Physiol Res. 2015;64:S105–19. https://doi.org/10.33549/physiolres.933130.

    Article  CAS  PubMed  Google Scholar 

  6. Mullen JT, Moorman DW, Davenport DL. The obesity paradox: body mass index and outcomes in patients undergoing non-bariatric general surgery. Ann Surg. 2009;250:166–72. https://doi.org/10.1097/SLA.0b013e3181ad8935.

    Article  PubMed  Google Scholar 

  7. Morgan OW, Bramley A, Fowlkes A, Freedman DS, Taylor TH, Gargiullo P. et al. Morbid obesity as a risk factor for hospitalization and death due to 2009 pandemic influenza a(h1n1) disease. PLoS ONE. 2010;5:e9694 https://doi.org/10.1371/journal.pone.0009694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Arslan E, Atilgan H, Yavasoglu I. The prevalence of Helicobacter pylori in obese subjects. Eur J Intern Med. 2009;20:695–7. https://doi.org/10.1016/j.ejim.2009.07.013.

    Article  PubMed  Google Scholar 

  9. Uberos J, Molina-Carballo A, Fernandez-Puentes V, Rodriguez-Belmonte R, Munoz-Hoyos A. Overweight and obesity as risk factors for the asymptomatic carrier state of Neisseria meningitidis among a paediatric population. Eur J Clin Microbiol Infect Dis. 2010;29:333–4. https://doi.org/10.1007/s10096-009-0849-7.

    Article  CAS  PubMed  Google Scholar 

  10. Huttunen R, Syrjänen J. Obesity and the risk and outcome of infection. Int J Obes. 2013;37:333–40. https://doi.org/10.1038/ijo.2012.62.

    Article  CAS  Google Scholar 

  11. Nadeau KJ, Maahs DM, Daniels SR, Eckel RH. Childhood obesity and cardiovascular disease: links and prevention strategies. Nat Rev Cardiol. 2011;8:513–25. https://doi.org/10.1038/nrcardio.2011.86.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Jubber AS. Respiratory complications of obesity. Int J Clin Pract. 2004;58:573–80. https://doi.org/10.1111/j.1368-5031.2004.00166.x.

    Article  CAS  PubMed  Google Scholar 

  13. Roswall N, Li Y, Sandin S, Ström P, Adami HO, Weiderpass E. Changes in body mass index and waist circumference and concurrent mortality among Swedish women. Obesity. 2017;25:215–22. https://doi.org/10.1002/oby.21675.

    Article  PubMed  Google Scholar 

  14. Hill JO, Wyatt HR, Melanson EL. Genetic and environmental contributions to obesity. Med Clin North Am. 2000;84:333–45. https://doi.org/10.1016/s0025-7125(05)70224-8.

    Article  CAS  PubMed  Google Scholar 

  15. Campbell AMLV. Genetics of obesity. Aust Fam Phys. 2017;46:456–9.

    Google Scholar 

  16. Aveyard P, Lewis A, Tearne S, Hood K, Christian-Brown A, Adab P. et al. Screening and brief intervention for obesity in primary care: a parallel, two-arm, randomized trial. Lancet. 2016;356:2492–500. https://doi.org/10.1016/S0140-6736(16)31893-1.

    Article  Google Scholar 

  17. Zhang Y, Liu JU, Yao J, Ji G, Qian L, Wang J. et al. Obesity: pathophysiology and Intervention. Nutrients.2014;6:5153–83. https://doi.org/10.3390/nu6115153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. English WJ, Williams DB. Metabolic and bariatric surgery: an effective treatment option for obesity and cardiovascular disease. Prog Cardiovasc Dis. 2018;61:253–69. https://doi.org/10.1016/j.pcad.2018.06.003.

    Article  PubMed  Google Scholar 

  19. Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: Causes and therapeutic strategies. Metab Syndr Relat Disord. 2015;13:423–44. https://doi.org/10.1089/met.2015.0095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Dhurandhar NV. Is obesity caused by an adenovirus?. Expert Rev Anti-Infect Ther. 2012;10:521–4. https://doi.org/10.1586/eri.12.41.

    Article  CAS  PubMed  Google Scholar 

  21. Kim JY, Van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM. et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Investig. 2007;117:2621–37. https://doi.org/10.1172/JCI31021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lyons MJ, Faust IM, Hemmes RB, Buskirk DR, Hirsch J, Zabriskie JB. A virally induced obesity syndrome in mice. Science. 1982;216:82–5. https://doi.org/10.1126/science.7038878.

    Article  CAS  PubMed  Google Scholar 

  23. Verlaeten O, Griffond B, Khuth ST, Giraudon P, Akaoka H, Belin MF. et al. Down regulation of melanin concentrating hormone in virally induced obesity. Mol Cell Endocrinol. 2001;181:207–19. https://doi.org/10.1016/s0303-7207(01)00488-9.

    Article  CAS  PubMed  Google Scholar 

  24. Herden C, Herzog S, Richt JA, Nesseler A, Christ M, Failing K. et al. Distribution of borna disease virus in the brain of rats infected with an obesity-inducing virus strain. Brain Pathology. 2000;10:39–48. https://doi.org/10.1111/j.1750-3639.2000.tb00241.x.

    Article  CAS  PubMed  Google Scholar 

  25. So PW, Herlihy AH, Bell JD. Adiposity induced by adenovirus 5 inoculations. Int J Obes. 2005;29:603–6. https://doi.org/10.1038/sj.ijo.0802917.

    Article  CAS  Google Scholar 

  26. Pasarica M, Shin AC, Yu M, Ou Yang HM, Rathod M, Jen KL. et al. Human adenovirus 36 induces adiposity, increases insulin sensitivity, and alters hypothalamic monoamines in rats. Obesity. 2006;14:1905–13. https://doi.org/10.1038/oby.2006.222.

    Article  CAS  PubMed  Google Scholar 

  27. Carter JK, Ow CL, Smith RE. Rous-associated virus type 7 induces a syndrome in chickens characterized by stunting and obesity. Infect Immunol. 1983;39:410–22.

    Article  CAS  Google Scholar 

  28. Dhurandhar NV, Kulkarni P, Ajinkya SM, Sherikar A. Effect of adenovirus infection on adiposity in chicken. Vet Microbiol. 1992;31:101–7. https://doi.org/10.1016/0378-1135(92)90068-5.

    Article  CAS  PubMed  Google Scholar 

  29. Dhurandhar NV, Israel BA, Kolesar JM, Mayhew G, Cook ME, Atkinson RL. Transmissibility of adenovirus-induced adiposity in a chicken model. Int J Obes Relat Metab Disord. 2001;25:990–6. https://doi.org/10.1038/sj.ijo.0801668.

    Article  CAS  PubMed  Google Scholar 

  30. Whigham LD, Israel BA, Atkinson RL. Adipogenic potential of multiple human adenoviruses in vivo and in vitro in animals. Am J Physiol Regul Integr Comput Physiol. 2006;290:R190–4. https://doi.org/10.1152/ajpregu.00479.2005.

    Article  CAS  Google Scholar 

  31. 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. https://doi.org/10.1093/jn/131.10.3155.

    Article  CAS  PubMed  Google Scholar 

  32. Kapila M, Khosla P, Dhurandhar NV. Novel short-term effects of adenovirus ad-36 on hamster lipoproteins. Int J Obes Relat Metab Disord. 2004;28:1521–7. https://doi.org/10.1038/sj.ijo.0802710.

    Article  CAS  PubMed  Google Scholar 

  33. 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. https://doi.org/10.1038/sj.ijo.0801319.

    Article  CAS  PubMed  Google Scholar 

  34. Krishnapuram R, Dhurandhar EJ, Dubuisson O, Kirk-Ballard H, Bajpeyi S, Butte N, et al. Template to improve glycemic control without reducing adiposity or dietary fat. Am J Physiol Endocrinol Metab. 2011;300:E779–89. https://doi.org/10.1152/ajpendo.00703.2010. May

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Dhurandhar NV, Kulkarni PR, Ajinkya SM, Sherikar AA, Atkinson RL. Association of adenovirus infection with human obesity. Obes Res. 1997;5:464–9. https://doi.org/10.1002/j.1550-8528.1997.tb00672.x.

    Article  CAS  PubMed  Google Scholar 

  36. 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. https://doi.org/10.1038/sj.ijo.0802830.

    Article  CAS  Google Scholar 

  37. 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. https://doi.org/10.1038/ijo.2009.196.

    Article  CAS  Google Scholar 

  38. Trovato GM, Martines GF, Garozzo A, Tonzudo A, Timpanaro R, Pirri C. et al. Ad36 adipogenic adenovirus in human non‐alcoholic fatty liver disease. Liver Int. 2010;30:184–90. https://doi.org/10.1111/j.1478-3231.2009.02127.x.

    Article  CAS  PubMed  Google Scholar 

  39. 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 https://doi.org/10.1371/journal.pone.0041652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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. https://doi.org/10.1038/ijo.2011.102.

    Article  CAS  Google Scholar 

  41. 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. https://doi.org/10.1007/s10620-011-1903-8.

    Article  CAS  PubMed  Google Scholar 

  42. 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. https://doi.org/10.2337/dc12-1089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Almgren M, Atkinson RL, Hilding A, He J, Brismar K, Schalling M. et al. Human adenovirus-36 is uncommon in type 2 diabetes and is associated with increased insulin sensitivity in adults in Sweden. Ann Med. 2014;46:539–46. https://doi.org/10.3109/07853890.2014.935469.

    Article  CAS  PubMed  Google Scholar 

  44. Bil-Lula I, Stapor S, Sochocka M, Wolyniec M, Zatonska K, Ilow R. et al. Infectobesity in the polish population—evaluation of an association between adenoviruses type 5, 31, 36 and human obesity. Int J Virol Mol Biol. 2014;3:1–8. https://doi.org/10.5923/j.ijvmb.20140301.01.

    Article  Google Scholar 

  45. Jiao Y, Mao X, Chang X, Abudureyimu K, Zhang C, Lu J. et al. Adenovirus 36 infection expresses cellular APMI and Visfatin genes in overweight Uygur individuals. Diagn Pathol. 2014;9:83–9. https://doi.org/10.1186/1746-1596-9-83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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. https://doi.org/10.1016/j.micpath.2015.02.008.

    Article  CAS  PubMed  Google Scholar 

  47. 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. https://doi.org/10.1017/S0950268815000679.

    Article  CAS  PubMed  Google Scholar 

  48. Kocazeybek B, Saribas S, Ergin S. The role of Ad-36 as a risk factor in males with gynecomastia. Med Hypotheses. 2015;85:992–6. https://doi.org/10.1016/j.mehy.2015.08.020.

    Article  CAS  PubMed  Google Scholar 

  49. Sabin MA, Burgner D, Atkinson RL, Pei-Lun LZ, Magnussen CG, Cheung M. et al. Longitudinal investigation of adenovirus 36 seropositivity and human obesity: the cardiovascular risk in young finns study. Int J Obes. 2015;39:1644–50. https://doi.org/10.1038/ijo.2015.108.

    Article  CAS  Google Scholar 

  50. Waye MM, Chan JC, Tong PC, Ma R, Chan PK. Association of human adenovirus-36 with diabetes, adiposity, and dyslipidaemia in Hong Kong Chinese. Hong Kong Med J. 2015;21:45–7.

    PubMed  Google Scholar 

  51. Sapunar J, Fonseca L, Molina, Ortiz E, Barra MI, Reimer C. et al. Adenovirus 36 seropositivity is related to obesity risk, glycemic control, and leptin levels in Chilean subjects. Int J Obes. 2020;44:159–66. https://doi.org/10.1038/s41366-019-0321-4.

    Article  Google Scholar 

  52. 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. https://doi.org/10.3109/17477160903111789.

    Article  PubMed  Google Scholar 

  53. Gabbert C, Donohue M, Arnold J, Schwimmer JB. Adenovirus 36 and obesity in children and adolescents. Pediatrics. 2010;126:721–6. https://doi.org/10.1542/peds.2009-3362.

    Article  PubMed  Google Scholar 

  54. Na HN, Hong YM, Kim J, Kim HK, Jo I, Nam JH. Association between human adenovirus-36 and lipid disorders in Korean school children. Int J Obes. 2010;34:89–93. https://doi.org/10.1038/ijo.2009.207.

    Article  Google Scholar 

  55. Tosh AK, Broy-Aschenbrenner A, El Khatib J, Ge B. Adenovirus-36 antibody status & BMI comparison among obese Missouri adolescents. Mol Med. 2012;109:402–3. PMCID: PMC6179760

    Google Scholar 

  56. Aldhoon-Hainerova I, Zamrazilova H, Atkinson RL, Dušátková L, Sedláčková B, Hlavatý P. et al. Clinical and laboratory characteristics of 1179 Czech adolescents evaluated for antibodies to human adenovirus 36. Int J Obes. 2014;38:285–91. https://doi.org/10.1038/ijo.2013.72.

    Article  CAS  Google Scholar 

  57. Laing EM, Tripp RA, Pollock NK, Baile CA, Della-Fera MA, Rayalam S. et al. Adenovirus 36, adiposity, and bone strength in late-adolescent females. J Bone Miner Res. 2013;28:489–96. https://doi.org/10.1002/jbmr.1776.

    Article  PubMed  Google Scholar 

  58. Parra-Rojas I, Del Moral-Hernandez O, Salgado-Bernabe AB, Guzman-Guzman IP, Salgado-Goytia L, Munoz-Valle JF. Adenovirus 36 seropositivity and its relation with obesity and metabolic profile in children. Int J Endocrinol. 2013;2013:463194 https://doi.org/10.1155/2013/463194.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Vander Wal JS, Huelsing J, Dubuisson O, Dhurandhar NV. An observational study of the association between adenovirus 36 antibody status and weight loss among youth. Obes Facts. 2013;6:269–78. https://doi.org/10.1159/000353109.

    Article  Google Scholar 

  60. Cakmakliogullari EK, Sanlidag T, Ersoy B, Akcali S, Var A, Cicek C. Are human adenovirus-5 and 36 associated with obesity in children?. J Investig Med. 2014;62:821–4. https://doi.org/10.2310/JIM.0000000000000084.

    Article  CAS  PubMed  Google Scholar 

  61. Dusatkova L, Zamrazilova H, Aldhoon-Hainerova I, Atkinson RL, Sedlackova B, Lee ZP, et al. Association of adenovirus 36 infection with obesity-related gene variants in adolescents. Physiol Res 2015;64:S197–S202. https://doi.org/10.33549/physiolres.933131. Suppl 2

    Article  CAS  PubMed  Google Scholar 

  62. Park S, Kim J, Shin HJ, Hong YM, Sheen YH, Park HL. et al. Tracking study about adenovirus 36 infection: increase of adiposity. J Microbiol Biotechnol. 2015;25:2169–72. https://doi.org/10.4014/jmb.1509.09003.

    Article  CAS  PubMed  Google Scholar 

  63. Zamrazilová H, Aldhoon-Hainerová I, Atkinson RL, Dušátková L, Sedláčková B, Lee ZP. et al. Adenovirus 36 infection: a role in dietary intake and response to inpatient weight management in obese girls. Int J Obes. 2015;39:1757–60. https://doi.org/10.1038/ijo.2015.167.

    Article  CAS  Google Scholar 

  64. Kocazeybek B, Dinc HO, Ergin S. Evaluation of adenovirus-36 (Ad-36) antibody seropositivity and adipokine levels in obese children. Microb Pathog. 2017;108:27–31. https://doi.org/10.1016/j.micpath.2017.04.034.

    Article  CAS  PubMed  Google Scholar 

  65. Tosh AK, Wasserman MG, McLeay li 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.

  66. Lavoy EC, Arlinghaus KR, Rooney BV, Gupta P, Atkinson R, Johnston CA. High adenovirus 36 seroprevalence among a population of Hispanic American youth. Int J Adolesc Med Health. 2018. https://doi.org/10.1515/ijamh-2018-0110.

  67. 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. https://doi.org/10.1038/ijo.2009.224.

    Article  CAS  Google Scholar 

  68. Goossens VJ, de Jager 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. https://doi.org/10.1038/oby.2009.452.

    Article  PubMed  Google Scholar 

  69. Voss JD, Burnett DG, Olsen CH, Haverkos HW, Atkinson RL. Adenovirus 36 Antibodies associated with clinical diagnosis of overweight/obesity but not BMI gain: a military cohort study. J Clin Endocrinol Metab.2014;99:E1708–12. https://doi.org/10.1210/jc.2014-1863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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.https://doi.org/10.3390/v7072787.

    Article  CAS  Google Scholar 

  71. 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. https://doi.org/10.1042/BSR20180553.

  72. Berger PK, Pollock NK, Laing EM, Warden SJ, Hill-Gallant KM, Hausman DB. et al. Association of adenovirus 36 infection with adiposity and inflammatory-related markers in children. J Clin Endocrinol Metab. 2014;99:3240–6. https://doi.org/10.1210/jc.2014-1780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dhurandhar NV. A framework for identification of infections that contribute to human obesity. Lancet Infect. Dis. 2011;11:963–69.https://doi.org/10.1016/S1473-3099(11)70274-2.

    Article  PubMed  Google Scholar 

  74. Hegde V, Dhurandhar NV. Microbes and obesity: interrelationship between infection, adipose tissue and the immune system. Clin Microbiol Infect. 2013;19:314–20.https://doi.org/10.1111/1469-0691.12157.

    Article  CAS  PubMed  Google Scholar 

  75. Rathod MA, Rogers PM, Vangipuram SD, McAllister EJ, Dhurandhar NV. Adipogenic cascade can be induced without adipogenic media by a human adenovirus. Obesity. 2009;17:657–64.https://doi.org/10.1038/oby.2008.630.

    Article  CAS  PubMed  Google Scholar 

  76. Ponterio E, Gnessi L. Adenovirus 36 and obesity: an overview. Viruses. 2015;7:3719–40. https://doi.org/10.3390/v7072787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1 https://doi.org/10.1186/2046-4053-4-1

    Article  PubMed  PubMed Central  Google Scholar 

  78. Kolesar JM, Miller JA, Dhurandhar NV, Atkinson RL. Direct quantification of AD36 adenovirus DNA by capillary electrophoresis with laser-induced fluorescence. J Chromatogr B Biomed Sci Appl. 2000;744:1–8.

    Article  CAS  PubMed  Google Scholar 

  79. Yeung R, Eshaghi A, Lombos E, Blair J, Mazzulli T, Burton L, et al. Characterization of culture-positive adenovirus serotypes from respiratory specimens in Toronto, Ontario, Canada: September 2007–June 2008. Virol J. 2009;6:11.

  80. Chappell CL, Dickerson M, Day RS, Dubuisson O, Dhurandhar NV. Adenovirus 36 antibody detection: Improving the standard serum neutralization assay. J Virol Methods. 2017;239:69–74.

    Article  CAS  PubMed  Google Scholar 

  81. Dubuisson O, Day RS, Dhurandhar NV. Accurate identification of neutralizing antibodies to adenovirus Ad36—a putative contributor of obesity in humans. J Diabet Compl. 2015;29:83–7.

    Article  Google Scholar 

  82. Nam JH, Na HN, Atkinson RL, Dhurandhar NV. Genomic stability of adipogenic human adenovirus 36. Int J Obes. 2014;38:321–4.

    Article  CAS  Google Scholar 

  83. Atkinson RL. Adenovirus and obesity. Chapter 9. In. Haslam DW, Sharma AM, Roux CW. Controversies in obesity. London: Springer-Verlag, 2014. p.75–78.

  84. Lessan N, Saradalekshmi KR, Alkaf B, Majeed M, Barakat MT, Lee ZPL. et al. Obesity and diabetes in an arab population: role of adenovirus 36 infection. Sci Rep. 2020;10:8107https://doi.org/10.1038/s41598-020-65008-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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:e42031https://doi.org/10.1371/journal.pone.0042031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Shang Q, Wang H, Song Y, Wei L, Lavebratt C, Zhang F. et al. Serological data analyses show that adenovirus 36 infection is associated with obesity: a meta-analysis involving 5739 subjects. Obesity. 2014;22:895–900.https://doi.org/10.1002/oby.20533.

    Article  PubMed  Google Scholar 

  87. 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:e2357https://doi.org/10.1097/MD.0000000000002357.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Akheruzzaman M, Hegde V, Dhurandhar NV. Twenty-five years of research about adipogenic adenoviruses: a systematic review. Obes Rev. 2019;20:499–509.https://doi.org/10.1111/obr.12808. Apr.

    Article  PubMed  Google Scholar 

  89. 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.https://doi.org/10.1038/sj.ijo.0803748.

    Article  CAS  Google Scholar 

  90. Thai M, Graham NA, Braas D, Nehil M, Komisopoulou E, Kurdistani SK. et al. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab. 2014;19:694–701.https://doi.org/10.1016/j.cmet.2014.03.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Dhurandhar NV. Insulin sparing action of adenovirus 36 and its E4orf1 protein. J Diabet Compl. 2013;27:191–9.https://doi.org/10.1016/j.jdiacomp.2012.09.006.

    Article  Google Scholar 

  92. Kusminski CM, Gallardo-Montejano VI, Wang ZV, Hegde V, Bickel PE, Dhurandhar NV. et al. E4orf1 induction in adipose tissue promotes insulin-independent signaling in the adipocyte. Mol Metab. 2015;4:653–64.https://doi.org/10.1016/j.molmet.2015.07.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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.https://doi.org/10.1038/sj.ijo.0803366.

    Article  CAS  Google Scholar 

  94. 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;57:2321–31.https://doi.org/10.2337/db07-1311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 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.https://doi.org/10.1634/stemcells.2007-0868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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da Silva Fernandes, J., Schuelter-Trevisol, F., Cancelier, A.C.L. et al. Adenovirus 36 prevalence and association with human obesity: a systematic review. Int J Obes 45, 1342–1356 (2021). https://doi.org/10.1038/s41366-021-00805-6

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