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Epidemiology and Population Health

Association of adiposity, telomere length and mortality: data from the NHANES 1999–2002

International Journal of Obesity volume 42, pages 198–204 (2018)Cite this article

Subjects

Abstract

Background/Objectives:

Telomere shortening is associated with age and risk of medical comorbidity. We assessed the relationship between measures of adiposity, leukocyte telomere length, and mortality and whether it is modified by age.

Subjects/Methods:

Subjects with dual-energy X-ray absorptiometry measures were identified using the National Health and Nutrition Examination Survey 1999–2002. Obesity was categorized using two body fat definitions (BF1%: men ⩾25%; females ⩾35%; BF2% ⩾28% and ⩾38%, respectively), body mass index (BMI) and waist circumference (WC; men ⩾102 cm; females ⩾88 cm). Telomere length relative to standard reference DNA (T/S ratio) was assessed using quantitative PCR. Weighted multivariable regression models evaluated the association of telomere length with adiposity, both continuously and categorically (low/normal BF%, low/high WC and standard BMI categories). Differences in telomere length by age and adiposity were ascertained and subsequent models were stratified by age. Proportional hazard models assessed the risk of mortality by adiposity status. A telomere by adiposity interaction was tested in the entire cohort and by age category (<60 vs ⩾60 years; <70 vs ⩾70 years).

Results:

We identified 7827 subjects. Mean age was 46.1 years. Overall telomere length was 1.05±0.01 (s.e.) that differed by BF1% (low/high: 1.12±0.02 vs 1.03±0.02; P<0.001), BF2% (1.02±0.02 vs 1.11±0.02; P<0.001), BMI (underweight 1.08±0.03; normal 1.09±0.02; overweight 1.04±0.02; and obese 1.03±0.02;P<0.001) and WC (low/high 1.09±0.02 vs 1.02±0.02; P<0.001). Adjusted β-coefficients evaluating the relationship between telomere length and adiposity (measured continuously) were as follows: BF1% (β=−0.0033±0.0008; P<0.001), BF2% (−0.041±0.008; P<0.001), BMI (β=−0.025±0.0008; P=0.005) and WC (β=−0.0011±0.0004; P=0.007). High BF% (BF1%: β=−0.035±0.011; P=0.002; BF2%: β=−0.041±0.008; P<0.001) and WC (β=−0.035±0.011; P=0.008) were inversely related to telomere length (TL). Stratifying by age, high BF1% (−0.061±0.013), BF2% (−0.065±0.01), BMI-obesity (−0.07±0.015) and high WC (−0.048±0.013) were significant (all P<0.001). This association diminished with increasing age. In older participants, TL was inversely related to mortality (hazard ratio 0.36 (0.27, 0.49)), as were those classified by BF1% (0.68 (0.56, 0.81)), BF2% (0.75 (0.65, 0.80)), BMI (0.50 (0.42, 0.60)) and WC (0.72 (0.63, 0.83)). No interaction was observed between adiposity status, telomere length and mortality.

Conclusions:

Obesity is associated with shorter telomere length in young participants, a relationship that diminishes with increasing age. It does not moderate the relationship with mortality.

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References

  1. Gregg EW, Cheng YJ, Cadwell BL, Imperatore G, Williams DE, Flegal KM et al. Secular trends in cardiovascular disease risk factors according to body mass index in US adults. JAMA 2005; 293: 1868–1874.

    Article  CAS  PubMed  Google Scholar 

  2. Blaum CS, Xue QL, Michelon E, Semba RD, Fried LP . The association between obesity and the frailty syndrome in older women: the Women's Health and Aging Studies. J Am Geriatr Soc 2005; 53: 927–934.

    Article  PubMed  Google Scholar 

  3. Zizza CA, Herring A, Stevens J, Popkin BM . Obesity affects nursing-care facility admission among whites but not blacks. Obes Res 2002; 10: 816–823.

    Article  PubMed  Google Scholar 

  4. Flegal KM, Graubard BI, Williamson DF, Gail MH . Excess deaths associated with underweight, overweight, and obesity. JAMA 2005; 293: 1861–1867.

    Article  CAS  PubMed  Google Scholar 

  5. Forsythe LK, Wallace JM, Livingstone MB . Obesity and inflammation: the effects of weight loss. Nutr Res Rev 2008; 21: 117–133.

    Article  CAS  PubMed  Google Scholar 

  6. Schrager MA, Metter EJ, Simonsick E, Ble A, Bandinelli S, Lauretani F et al. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol (1985) 2007; 102: 919–925.

    Article  Google Scholar 

  7. Haver VG, Mateo Leach I, Kjekshus J, Fox JC, Wedel H, Wikstrand J et al. Telomere length and outcomes in ischaemic heart failure: data from the COntrolled ROsuvastatin multiNAtional Trial in Heart Failure (CORONA). Eur J Heart Fail 2015; 17: 313–319.

    Article  CAS  PubMed  Google Scholar 

  8. Nielsen BR, Linneberg A, Bendix L, Harboe M, Christensen K, Schwarz P . Association between leukocyte telomere length and bone mineral density in women 25-93 years of age. Exp Gerontol 2015; 66: 25–31.

    Article  CAS  PubMed  Google Scholar 

  9. Liu M, Huo YR, Wang J, Wang C, Liu S, Liu S et al. Telomere shortening in Alzheimer's disease patients. Ann Clin Lab Sci 2016; 46: 260–265.

    CAS  PubMed  Google Scholar 

  10. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA . Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 2003; 361: 393–395.

    Article  CAS  PubMed  Google Scholar 

  11. Collaborators GBDO Collaborators GBDO Afshin A, Collaborators GBDO Forouzanfar MH, Collaborators GBDO Reitsma MB, Collaborators GBDO Sur P, Collaborators GBDO Estep K et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med 2017; 377: 13–27.

    Article  Google Scholar 

  12. Muezzinler A, Zaineddin AK, Brenner H . Body mass index and leukocyte telomere length in adults: a systematic review and meta-analysis. Obes Rev 2014; 15: 192–201.

    Article  CAS  PubMed  Google Scholar 

  13. Mundstock E, Sarria EE, Zatti H, Mattos Louzada F, Kich Grun L, Herbert Jones M et al. Effect of obesity on telomere length: systematic review and meta-analysis. Obesity (Silver Spring) 2015; 23: 2165–2174.

    Article  Google Scholar 

  14. McAuley PA, Artero EG, Sui X, Lee DC, Church TS, Lavie CJ et al. The obesity paradox, cardiorespiratory fitness, and coronary heart disease. Mayo Clin Proc 2012; 87: 443–451.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ . Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin Nutr 2014; 68: 1001–1007.

    Article  CAS  PubMed  Google Scholar 

  16. Dickey R, Bartuska C, Bray G, Callaway W, Davidson E, Feld S et al. AACE/ACE position statement on the prevention, diagnosis, and treatment of obesity (1998 revision). Endocr Pract 1998; 4: 300.

    Google Scholar 

  17. Baumgartner RN . Body composition in healthy aging. Ann N Y Acad Sci 2000; 904: 437–448.

    Article  CAS  PubMed  Google Scholar 

  18. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA . Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 2002; 76: 473–481.

    Article  CAS  PubMed  Google Scholar 

  19. Tian S, Morio B, Denis JB, Mioche L . Age-related changes in segmental body composition by ethnicity and history of weight change across the adult lifespan. Int J Environ Res Public Health 2016; 13: E821.

    Article  PubMed  Google Scholar 

  20. Angleman SB, Harris TB, Melzer D . The role of waist circumference in predicting disability in periretirement age adults. Int J Obes (Lond) 2006; 30: 364–373.

    Article  CAS  Google Scholar 

  21. Cerhan JR, Moore SC, Jacobs EJ, Kitahara CM, Rosenberg PS, Adami HO et al. A pooled analysis of waist circumference and mortality in 650,000 adults. Mayo Clin Proc 2014; 89: 335–345.

    Article  PubMed  Google Scholar 

  22. Jun ES, Lee TH, Cho HH, Suh SY, Jung JS . Expression of telomerase extends longevity and enhances differentiation in human adipose tissue-derived stromal cells. Cell Physiol Biochem 2004; 14: 261–268.

    Article  CAS  PubMed  Google Scholar 

  23. Ogura F, Wakao S, Kuroda Y, Tsuchiyama K, Bagheri M, Heneidi S et al. Human adipose tissue possesses a unique population of pluripotent stem cells with nontumorigenic and low telomerase activities: potential implications in regenerative medicine. Stem Cells Dev 2014; 23: 717–728.

    Article  CAS  PubMed  Google Scholar 

  24. Bischoff C, Petersen HC, Graakjaer J, Andersen-Ranberg K, Vaupel JW, Bohr VA et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology 2006; 17: 190–194.

    Article  PubMed  Google Scholar 

  25. Lee M, Martin H, Firpo MA, Demerath EW . Inverse association between adiposity and telomere length: The Fels Longitudinal Study. Am J Hum Biol 2011; 23: 100–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Houston DK, Ding J, Nicklas BJ, Harris TB, Lee JS, Nevitt MC et al. Overweight and obesity over the adult life course and incident mobility limitation in older adults: the health, aging and body composition study. Am J Epidemiol 2009; 169: 927–936.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Herbert KE, Mistry Y, Hastings R, Poolman T, Niklason L, Williams B . Angiotensin II-mediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways. Circ Res 2008; 102: 201–208.

    Article  CAS  PubMed  Google Scholar 

  28. Newsholme P, de Bittencourt PI Jr . The fat cell senescence hypothesis: a mechanism responsible for abrogating the resolution of inflammation in chronic disease. Curr Opin Clin Nutr Metab Care 2014; 17: 295–305.

    Article  CAS  PubMed  Google Scholar 

  29. Ottinger MA . Mechanisms of reproductive aging: conserved mechanisms and environmental factors. Ann N Y Acad Sci 2010; 1204: 73–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Diaz VA, Mainous AG, Player MS, Everett CJ . Telomere length and adiposity in a racially diverse sample. Int J Obes (Lond) 2010; 34: 261–265.

    Article  CAS  Google Scholar 

  31. Moverare-Skrtic S, Svensson J, Karlsson MK, Orwoll E, Ljunggren O, Mellstrom D et al. Serum insulin-like growth factor-I concentration is associated with leukocyte telomere length in a population-based cohort of elderly men. J Clin Endocrinol Metab 2009; 94: 5078–5084.

    Article  CAS  PubMed  Google Scholar 

  32. Farzaneh-Far R, Lin J, Epel E, Lapham K, Blackburn E, Whooley MA . Telomere length trajectory and its determinants in persons with coronary artery disease: longitudinal findings from the heart and soul study. PLoS One 2010; 5: e8612.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Romero-Corral A, Somers VK, Sierra-Johnson J, Thomas RJ, Collazo-Clavell ML, Korinek J et al. Accuracy of body mass index in diagnosing obesity in the adult general population. Int J Obes (Lond) 2008; 32: 959–966.

    Article  CAS  Google Scholar 

  34. Batsis JA, Mackenzie TA, Bartels SJ, Sahakyan KR, Somers VK, Lopez-Jimenez F . Diagnostic accuracy of body mass index to identify obesity in older adults: NHANES 1999-2004. Int J Obes (Lond) 2016; 40: 761–767.

    Article  CAS  Google Scholar 

  35. An R, Yan H . Body weight status and telomere length in U.S. middle-aged and older adults. Obes Res Clin Pract 2017; 11: 51–62.

    Article  PubMed  Google Scholar 

  36. Njajou OT, Cawthon RM, Blackburn EH, Harris TB, Li R, Sanders JL et al. Shorter telomeres are associated with obesity and weight gain in the elderly. Int J Obes (Lond) 2012; 36: 1176–1179.

    Article  CAS  Google Scholar 

  37. Batsis JA, Lopez-Jimenez F . Cardiovascular risk assessment—from individual risk prediction to estimation of global risk and change in risk in the population. BMC Med 2010; 8: 29.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pahor M, Guralnik JM, Ambrosius WT, Blair S, Bonds DE, Church TS et al. Effect of structured physical activity on prevention of major mobility disability in older adults: the LIFE study randomized clinical trial. JAMA 2014; 311: 2387–2396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

JAB’s research reported in this publication was supported in part by the National Institute on Aging of the National Institutes of Health under Award Number K23AG051681. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Support was also provided by the Dartmouth Health Promotion and Disease Prevention Research Center supported by Cooperative Agreement Number U48DP005018 from the Centers for Disease Control and Prevention. The findings and conclusions in this journal article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. JAB received funding from Health Resources Services Administration (UB4HP19206-01-00) for medical geriatric teaching, the Junior Faculty Career Development Award, the Department of Medicine, Dartmouth-Hitchcock Medical Center, and the Dartmouth Centers for Health and Aging. SJB receives funding from the National Institute of Mental Health (K12 HS0217695 (AHRQ); NIMH: T32 MH073553, R01 MH078052, R01 MH089811; R24 MH102794 CDC U48DP005018). RTE is supported by The Dartmouth Clinical and Translational Science Institute, under award number UL1TR001086 from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH).

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Authors and Affiliations

  1. Section of General Internal Medicine, Dartmouth-Hitchcock Medical Center, Lebanon, NH, USA

    J A Batsis

  2. Geisel School of Medicine at Dartmouth, Hanover, NH, USA,

    J A Batsis, T A Mackenzie, R T Emeny & S J Bartels

  3. The Dartmouth Institute for Health Policy & Clinical Practice, Lebanon, Hanover, NH, USA,

    J A Batsis, T A Mackenzie, R T Emeny & S J Bartels

  4. Dartmouth Centers for Health and Aging, Dartmouth College, Hanover, NH, USA

    J A Batsis & S J Bartels

  5. Health Promotion Research Center at Dartmouth, Lebanon, NH, USA

    J A Batsis & S J Bartels

  6. Dartmouth Weight & Wellness Center, Lebanon, NH, USA

    J A Batsis

  7. Department of Biomedical Data Science, Geisel School of Medicine at Dartmouth Practice, Lebanon, NH, USA

    T A Mackenzie

  8. Department of Epidemiology, School of Public Health, SUNY Albany, Albany, NY, USA

    E Vasquez

  9. Department of Family and Community Nursing, University of North Carolina School of Nursing, Greensboro, NC, USA,

    C M Germain

  10. University of New England College of Osteopathic Medicine, Biddeford, ME, USA

    P Rippberger

  11. Division of Cardiovascular Disease, Department of Medicine, Mayo Clinic, Rochester, MN, USA

    F Lopez-Jimenez

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  1. J A Batsis
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Correspondence to J A Batsis.

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Work to be presented in part to the 2017 International Association of Geriatrics and Gerontology, San Francisco, CA, USA, July 2017.

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Batsis, J., Mackenzie, T., Vasquez, E. et al. Association of adiposity, telomere length and mortality: data from the NHANES 1999–2002. Int J Obes 42, 198–204 (2018). https://doi.org/10.1038/ijo.2017.202

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