Abstract
Infection with adenovirus 36 (Ad36) has been associated with risk of obesity in youth in some studies, but the seroprevalence of this virus has not been examined among all populations. As Hispanic-American youth are of greater risk for obesity than other American youth, we sought to determine the proportion of Ad36 seropositive (Ad36+) students in an urban middle school serving a Hispanic population. We further examined if Ad36+ students were more likely to have obesity, and if Ad36 serostatus impacted changes in weight status following a health intervention. We determined body mass index (BMI) at the beginning and end of a 16-week health intervention among 40 Hispanic-American middle-school students. Ad36 serostatus was determined by enzyme-linked immunsorbent assay (ELISA). Seventy percent of the students were Ad36+. Ad36+ and Ad36 seronegative (Ad36−) did not differ before or after the intervention in body weight measures. The odds of being classified as obese was 1.4 times greater among Ad36+ than Ad36− at baseline, and 2.4 times greater post-intervention, but these were not statistically significant. We report a high seroprevalence of Ad36 among a population of Hispanic-American students. Ad36 seropositivity was associated with a trend for a greater likelihood of having obesity, but did not impact response to a health intervention.
Acknowledgments
The authors gratefully recognize the time of the participants, and thank Kyle Stallard for his assistance.
Funding: This work was partially funded by the Texas Obesity Research Center at the University of Houston. Funders were not involved in the study design; collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
Conflict of interest: None.
References
[1] Lion T. Adenovirus infections in immunocompetent and immunocompromised patients. Clin Microbiol Rev. 2014;27:441–62.10.1128/CMR.00116-13Search in Google Scholar PubMed PubMed Central
[2] 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;24:989–96.10.1038/sj.ijo.0801319Search in Google Scholar PubMed
[3] 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;26:969–78.10.1634/stemcells.2007-0868Search in Google Scholar PubMed PubMed Central
[4] Vangipuram SD, Sheele J, Atkinson RL, Holland TC, Dhurandhar NV. A human adenovirus enhances preadipocyte differentiation. Obes Res. 2004;12:770–7.10.1038/oby.2004.93Search in Google Scholar PubMed
[5] 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:e41652.10.1371/journal.pone.0041652Search in Google Scholar PubMed PubMed Central
[6] 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;29:281–6.10.1038/sj.ijo.0802830Search in Google Scholar PubMed
[7] Sabin MA, Burgner D, Atkinson RL, Pei-Lun Lee Z, 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;39:1644–50.10.1038/ijo.2015.108Search in Google Scholar PubMed
[8] 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;22:895–900.10.1002/oby.20533Search in Google Scholar PubMed
[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. 2009;33:1402–9.10.1038/ijo.2009.196Search in Google Scholar PubMed
[10] Aldhoon-Hainerova I, Zamrazilová 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;38:285–91.10.1038/ijo.2013.72Search in Google Scholar PubMed
[11] Atkinson RL, Lee I, Shin HJ, He J. Human adenovirus-36 antibody status is associated with obesity in children. Int J Pediatr Obes. 2010;5:157–60.10.3109/17477160903111789Search in Google Scholar PubMed
[12] 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;99:3240–6.10.1210/jc.2014-1780Search in Google Scholar PubMed PubMed Central
[13] Gabbert C, Donohue M, Arnold J, Schwimmer JB. Adenovirus 36 and obesity in children and adolescents. Pediatrics. 2010;126:721–6.10.1542/peds.2009-3362Search in Google Scholar PubMed
[14] 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;62:821–4.10.2310/JIM.0000000000000084Search in Google Scholar PubMed
[15] 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;28:489–96.10.1002/jbmr.1776Search in Google Scholar PubMed PubMed Central
[16] Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014;311:806–14.10.1001/jama.2014.732Search in Google Scholar PubMed PubMed Central
[17] Must A, Jacques PF, Dallal GE, Bajema CJ, Dietz WH. Long-term morbidity and mortality of overweight adolescents. A follow-up of the Harvard Growth Study of 1922 to 1935. N Engl J Med. 1992;327:1350–5.10.1056/NEJM199211053271904Search in Google Scholar PubMed
[18] Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics–2013 update: a report from the American Heart Association. Circulation. 2013;127:e6-e245.10.1161/CIR.0b013e31828124adSearch in Google Scholar PubMed PubMed Central
[19] Day JC. Population Projections of the United States by Age, Sex, Race, and Hispanic Origin: 1995–2050, U.S. Bureau of the Cenus, Current Populations Reports. Washington, DC: U.S. Government Printing Office, pp. 25–1130, 1996.Search in Google Scholar
[20] Johnston CA, Moreno JP, Hernandez DC, Reichek B, Foreyt, JP. Dissemination of a school-based obesity intervention for Mexican Americans: A randomized controlled trial. Health Behav Policy Rev. 2017;4:454–65.10.14485/HBPR.4.5.5Search in Google Scholar
[21] Na HN, Hong YM, Ye MB, Park S, Kim IB, Nam JH. Adenovirus 36 attenuates weight loss from exercise but improves glycemic control by increasing mitochondrial activity in the liver. PLoS One. 2014;9:e114534.10.1371/journal.pone.0114534Search in Google Scholar PubMed PubMed Central
[22] 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;6:269–78.10.1159/000353109Search in Google Scholar PubMed PubMed Central
[23] Zamrazilova 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;39:1757–60.10.1038/ijo.2015.167Search in Google Scholar PubMed
[24] Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC growth charts for the United States: methods and development. Vital Health Stat 11. 2002;246:1–190.Search in Google Scholar
[25] Atkinson RL. Human adenovirus-36 and childhood obesity. Int J Pediatr Obes. 2011;1:2–6.10.3109/17477166.2011.590200Search in Google Scholar PubMed
[26] Altman DG. Practical statistics for medical research. London: Chapman and Hall, pp. 269, 1991.10.1201/9780429258589Search in Google Scholar
[27] 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;34:89–93.10.1038/ijo.2009.207Search in Google Scholar PubMed
[28] Parra-Rojas I, Del Moral-Hernández O, Salgado-Bernabé AB, Guzmán-Guzmán IP, Salgado-Goytia L, Muñoz-Valle JF. Adenovirus-36 seropositivity and its relation with obesity and metabolic profile in children. Int J Endocrinol. 2013;2013:463194.10.1155/2013/463194Search in Google Scholar PubMed PubMed Central
[29] 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;34:302–8.10.1038/ijo.2009.224Search in Google Scholar PubMed
[30] Zajacova A, Dowd JB, Aiello AE. Socioeconomic and race/ethnic patterns in persistent infection burden among U.S. adults. J Gerontol A Biol Sci Med Sci. 2009;64:272–9.10.1093/gerona/gln012Search in Google Scholar PubMed PubMed Central
[31] Rubicz R, Leach CT, Kraig E, Dhurandhar NV, Grubbs B, Blangero J, et al. Seroprevalence of 13 common pathogens in a rapidly growing U.S. minority population: Mexican Americans from San Antonio, TX. BMC Res Notes. 2011;4:433.10.1186/1756-0500-4-433Search in Google Scholar PubMed PubMed Central
[32] 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;19:220–1.10.1038/oby.2009.452Search in Google Scholar PubMed
[33] 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:e42031.10.1371/journal.pone.0042031Search in Google Scholar PubMed PubMed Central
©2018 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Editorial
- Close-in-age exemption laws: focusing on the best interests of children and adolescents
- Review
- Literature review: nutritional factors influencing academic achievement in school age children
- Original Articles
- Appointed by young people – a qualitative study on young patients recruiting hospital staff in Denmark
- Child labor and mental health status of in-school adolescents in a municipal local government area of Lagos state, Nigeria
- Usefulness of hematological parameters for differential diagnosis of endometriomas in adolescents/young adults and older women
- Assessment of the WHO Health Promoting Schools Framework among schools in selected villages of rural Puducherry, South India – a mixed method study
- The development and psychometric evaluation of a new instrument to market healthy breakfast and snacks among adolescents
- Awareness of bicycle light use of young adults
- A brief study on the knowledge and choice of contraception methods in married adolescent girls
- Coverage of and compliance to iron supplementation under the National Iron Plus Initiative among reproductive age-group women in urban Puducherry – a cross-sectional study
- Adolescents’ smartphone use at night, sleep disturbance and depressive symptoms
- Prevalence and determinants of poor quality of sleep among adolescents in rural Puducherry, South India
- Health awareness, lifestyle and dietary behavior of university students in the northeast part of Bangladesh
- The effectiveness of group counseling on prenatal care knowledge and performance of pregnant adolescents in a Kurdish region of Iran
- High adenovirus 36 seroprevalence among a population of Hispanic American youth
- Development and psychometric properties of the female adolescents’ sexual reproductive self-care scale
- “Decide Now, Buy Marlboro”: Examining the influence and appeal of Marlboro’s new brand architecture among Filipino adolescents
- Knowledge, attitude and practice of cigarette smoking among senior secondary school students in Depok, Indonesia
- Factors associated with knowledge of where to access health care among youth in juvenile detention: a mixed methods study
- Association between a vegetarian diet and emotional symptoms: a cross-sectional study among adolescents in four developing countries
- A prospective 1-year study on load reduction of school backpacks shows reversible changes of body posture in schoolchildren
- Level, motivation and barriers to participate in physical activity among late adolescents in Puducherry
- A pilot study to improve sugar and water consumption in Maltese school children
- Deep venous thrombosis of lower limbs in adolescents: a study in a tertiary hospital
- Prevalence and determinants of condom use among male adolescents in Indonesia
- Iranian mothers’ needs for reproductive health education of their adolescent daughters: a qualitative study
- Short Communication
- Psychosocial determinants of stress among adolescents in an urban slum in a city of Western Maharashtra: a cross-sectional study
Articles in the same Issue
- Frontmatter
- Editorial
- Close-in-age exemption laws: focusing on the best interests of children and adolescents
- Review
- Literature review: nutritional factors influencing academic achievement in school age children
- Original Articles
- Appointed by young people – a qualitative study on young patients recruiting hospital staff in Denmark
- Child labor and mental health status of in-school adolescents in a municipal local government area of Lagos state, Nigeria
- Usefulness of hematological parameters for differential diagnosis of endometriomas in adolescents/young adults and older women
- Assessment of the WHO Health Promoting Schools Framework among schools in selected villages of rural Puducherry, South India – a mixed method study
- The development and psychometric evaluation of a new instrument to market healthy breakfast and snacks among adolescents
- Awareness of bicycle light use of young adults
- A brief study on the knowledge and choice of contraception methods in married adolescent girls
- Coverage of and compliance to iron supplementation under the National Iron Plus Initiative among reproductive age-group women in urban Puducherry – a cross-sectional study
- Adolescents’ smartphone use at night, sleep disturbance and depressive symptoms
- Prevalence and determinants of poor quality of sleep among adolescents in rural Puducherry, South India
- Health awareness, lifestyle and dietary behavior of university students in the northeast part of Bangladesh
- The effectiveness of group counseling on prenatal care knowledge and performance of pregnant adolescents in a Kurdish region of Iran
- High adenovirus 36 seroprevalence among a population of Hispanic American youth
- Development and psychometric properties of the female adolescents’ sexual reproductive self-care scale
- “Decide Now, Buy Marlboro”: Examining the influence and appeal of Marlboro’s new brand architecture among Filipino adolescents
- Knowledge, attitude and practice of cigarette smoking among senior secondary school students in Depok, Indonesia
- Factors associated with knowledge of where to access health care among youth in juvenile detention: a mixed methods study
- Association between a vegetarian diet and emotional symptoms: a cross-sectional study among adolescents in four developing countries
- A prospective 1-year study on load reduction of school backpacks shows reversible changes of body posture in schoolchildren
- Level, motivation and barriers to participate in physical activity among late adolescents in Puducherry
- A pilot study to improve sugar and water consumption in Maltese school children
- Deep venous thrombosis of lower limbs in adolescents: a study in a tertiary hospital
- Prevalence and determinants of condom use among male adolescents in Indonesia
- Iranian mothers’ needs for reproductive health education of their adolescent daughters: a qualitative study
- Short Communication
- Psychosocial determinants of stress among adolescents in an urban slum in a city of Western Maharashtra: a cross-sectional study