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Salivary telomere length and the risks of prediabetes and diabetes among middle-aged and older adults: findings from the Health and Retirement Study

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Abstract

Aim

To assess the association of telomere length (TL) with prediabetes/diabetes and to explore the potential factors affecting TL among individuals with prediabetes/diabetes by weight status.

Methods

This study included 3,379 eligible adults (aged 45–85 years, males: 42%) from the US Health and Retirement Study in 2008. TL was assayed using quantitative PCR of saliva (T/S ratio). Linear and nonlinear associations between TL and prediabetes/diabetes were assessed using the logistic regression and restricted cubic spline model, respectively, adjusting for TL-plate numbers, age, sex, race, body mass index, lifestyles, diabetes medications, and cardiometabolic parameters (blood pressure, C-reactive protein, and total cholesterol). Multiple linear regression was used for testing any factors associated with TL.

Results

Among 3,379 participants, 868 (25.7%) had prediabetes with a mean TL of 1.34 ± 0.37 (T/S ratio) and 858 (25.4%) had diabetes with a mean TL of 1.36 ± 0.43 (T/S ratio). Neither linear nor nonlinear association of TL with prediabetes/diabetes was significant by weight status. Age was negatively associated with TL in both normal-weight (β = − 0.002, p = 0.025) and overweight/obese (β = − 0.002, p = 0.006) prediabetes, but non-significant in normal-weight and overweight/obese diabetes. BMI and cardiometabolic parameters were not associated with TL in prediabetes/diabetes by weight status.

Conclusions

Salivary TL was not associated with prediabetes/diabetes among the US middle-aged and older adults. Further longitudinal studies are required to establish the link between TL and diabetes development and to identify potential factors affecting TL shortening, particularly in normal-weight diabetic patients.

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References

  1. Cheng F, Carroll L, Joglekar MV et al (2021) Diabetes, metabolic disease, and telomere length. Lancet Diabetes Endocrinol 9(2):117–126. https://doi.org/10.1016/S2213-8587(20)30365-X

    Article  CAS  Google Scholar 

  2. Smith L, Luchini C, Demurtas J et al (2019) Telomere length and health outcomes: an umbrella review of systematic reviews and meta-analyses of observational studies. Ageing Res Rev 51:1–10. https://doi.org/10.1016/j.arr.2019.02.003

    Article  CAS  Google Scholar 

  3. Cheng F, Luk AO, Tam CHT et al (2020) Shortened relative leukocyte telomere length is associated with prevalent and incident cardiovascular complications in type 2 diabetes: analysis from the Hong Kong diabetes register. Diabetes Care 43(9):2257–2265. https://doi.org/10.2337/dc20-0028

    Article  CAS  Google Scholar 

  4. Testa R, Olivieri F, Sirolla C et al (2011) Leukocyte telomere length is associated with complications of type 2 diabetes mellitus. Diabet Med 28(11):1388–1394. https://doi.org/10.1111/j.1464-5491.2011.03370.x

    Article  CAS  Google Scholar 

  5. Menke A, Casagrande S, Cowie CC (2015) Leukocyte telomere length and diabetes status, duration, and control: the 1999–2002 national health and nutrition examination survey. BMC Endocr Disord 15:52. https://doi.org/10.1186/s12902-015-0050-1

    Article  CAS  Google Scholar 

  6. Hovatta I, de Mello VD, Kananen L et al (2012) Leukocyte telomere length in the finnish diabetes prevention study. PLoS ONE 7(4):e34948. https://doi.org/10.1371/journal.pone.0034948

    Article  CAS  Google Scholar 

  7. You NC, Chen BH, Song Y et al (2012) A prospective study of leukocyte telomere length and risk of type 2 diabetes in postmenopausal women. Diabetes 61(11):2998–3004. https://doi.org/10.2337/db12-0241

    Article  CAS  Google Scholar 

  8. Cao L, Li ZQ, Shi YY, Liu Y (2020) Telomere length and type 2 diabetes: mendelian randomization study and polygenic risk score analysis. Yi Chuan 42(9):882–888. https://doi.org/10.16288/j.yczz.20-077

    Article  CAS  Google Scholar 

  9. Wang J, Dong X, Cao L et al (2016) Association between telomere length and diabetes mellitus: a meta-analysis. J Int Med Res 44(6):1156–1173. https://doi.org/10.1177/0300060516667132

    Article  Google Scholar 

  10. Zhao J, Miao K, Wang H, Ding H, Wang DW (2013) Association between telomere length and type 2 diabetes mellitus: a meta-analysis. PLoS ONE 8(11):e79993. https://doi.org/10.1371/journal.pone.0079993

    Article  Google Scholar 

  11. D’Mello MJ, Ross SA, Briel M, Anand SS, Gerstein H, Pare G (2015) Association between shortened leukocyte telomere length and cardiometabolic outcomes: systematic review and meta-analysis. Circ Cardiovasc Genet 8(1):82–90. https://doi.org/10.1161/CIRCGENETICS.113.000485

    Article  CAS  Google Scholar 

  12. Yu HJ, Ho M, Liu X, Yang J, Chau PH, Fong DYT (2022) Association of weight status and the risks of diabetes in adults: a systematic review and meta-analysis of prospective cohort studies. Int J Obes (Lond). https://doi.org/10.1038/s41366-022-01096-1

    Article  Google Scholar 

  13. Welendorf C, Nicoletti CF, Pinhel MAS, Noronha NY, de Paula BMF, Nonino CB (2019) Obesity, weight loss, and influence on telomere length: new insights for personalized nutrition. Nutrition 66:115–121. https://doi.org/10.1016/j.nut.2019.05.002

    Article  CAS  Google Scholar 

  14. Zhao J, Zhu Y, Lin J et al (2014) Short leukocyte telomere length predicts risk of diabetes in american indians: the strong heart family study. Diabetes 63(1):354–362. https://doi.org/10.2337/db13-0744

    Article  CAS  Google Scholar 

  15. Gujral UP, Narayan KMV (2019) Diabetes in normal-weight individuals: high susceptibility in nonwhite populations. Diabetes Care 42(12):2164–2166. https://doi.org/10.2337/dci19-0046

    Article  Google Scholar 

  16. Olaogun I, Farag M, Hamid P (2020) The pathophysiology of type 2 diabetes mellitus in non-obese individuals: an overview of the current understanding. Cureus 12(4):e7614. https://doi.org/10.7759/cureus.7614

    Article  Google Scholar 

  17. Stout SA, Lin J, Hernandez N et al (2017) Validation of minimally-invasive sample collection methods for measurement of telomere length. Front Aging Neurosci 9:397. https://doi.org/10.3389/fnagi.2017.00397

    Article  CAS  Google Scholar 

  18. Mitchell C, Hobcraft J, McLanahan SS et al (2014) Social disadvantage, genetic sensitivity, and children’s telomere length. Proc Natl Acad Sci U S A 111(16):5944–5949. https://doi.org/10.1073/pnas.1404293111

    Article  CAS  Google Scholar 

  19. Tabák AG, Herder C, Rathmann W, Brunner EJ, Kivimäki M (2012) Prediabetes: a high-risk state for diabetes development. Lancet 379(9833):2279–2290. https://doi.org/10.1016/S0140-6736(12)60283-9

    Article  Google Scholar 

  20. Sonnega A, Faul JD, Ofstedal MB, Langa KM, Phillips JW, Weir DR (2014) Cohort profile: the Health and Retirement Study (HRS). Int J Epidemiol 43(2):576–585. https://doi.org/10.1093/ije/dyu067

    Article  Google Scholar 

  21. Health and Retirement Study, 2008 Telomere data set. Produced and distributed by the University of Michigan with funding from the National Institute on Aging (grant number NIAU01AG009740). Ann Arbor, MI, (2013)

  22. Eileen MC, Jessica DF, Jung Ki K, et al. (2013) Documentation of biomarkers in the 2006 and 2008 Health and Retirement Study. In: Institute for Social Research, University of Michigan, Ann Arbor, Michigan

  23. An R, Yan H (2017) Body weight status and telomere length in U.S. middle-aged and older adults. Obes Res Clin Pract 11(1):51–62. https://doi.org/10.1016/j.orcp.2016.01.003

    Article  Google Scholar 

  24. Li FR, Zhang XR, Zhong WF et al (2019) Glycated hemoglobin and all-cause and cause-specific mortality among adults with and without diabetes. J Clin Endocrinol Metab 104(8):3345–3354. https://doi.org/10.1210/jc.2018-02536

    Article  Google Scholar 

  25. Sherwani SI, Khan HA, Ekhzaimy A, Masood A, Sakharkar MK (2016) Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights 11:95–104. https://doi.org/10.4137/BMI.S38440

    Article  CAS  Google Scholar 

  26. Mozaffarian D, Kamineni A, Carnethon M, Djousse L, Mukamal KJ, Siscovick D (2009) Lifestyle risk factors and new-onset diabetes mellitus in older adults: the cardiovascular health study. Arch Intern Med 169(8):798–807. https://doi.org/10.1001/archinternmed.2009.21

    Article  Google Scholar 

  27. Latifovic L, Peacock SD, Massey TE, King WD (2016) The influence of alcohol consumption, cigarette smoking, and physical activity on leukocyte telomere length. Cancer Epidemiol Biomark Prev 25(2):374–380. https://doi.org/10.1158/1055-9965.EPI-14-1364

    Article  CAS  Google Scholar 

  28. Centers for Disease Control and Prevention (2022) How much physical activity do older adults need? Available from https://www.cdc.gov/physicalactivity/basics/older_adults/index.htm. Accessed 1 April 2022

  29. Huzen J, Wong LS, van Veldhuisen DJ et al (2014) Telomere length loss due to smoking and metabolic traits. J Intern Med 275(2):155–163. https://doi.org/10.1111/joim.12149

    Article  CAS  Google Scholar 

  30. Harrell FE (2001) General aspects of fitting regression models. In: Harrell FE (ed) Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. Springer, New York, pp 11–40

    Chapter  Google Scholar 

  31. James G, Witten D, Hastie T, Tibshirani R (2021) Linear regression. In: James G, Witten D, Hastie T, Tibshirani R (eds) An introduction to statistical learning: with applications in R. Springer, New York, pp 59–128

    Chapter  Google Scholar 

  32. Shen Q, Zhao X, Yu L et al (2012) Association of leukocyte telomere length with type 2 diabetes in mainland Chinese populations. J Clin Endocrinol Metab 97(4):1371–1374. https://doi.org/10.1210/jc.2011-1562

    Article  CAS  Google Scholar 

  33. Hunt SC, Chen W, Gardner JP et al (2008) Leukocyte telomeres are longer in African Americans than in whites: the national heart, lung, and blood institute family heart study and the Bogalusa heart study. Aging Cell 7(4):451–458. https://doi.org/10.1111/j.1474-9726.2008.00397.x

    Article  CAS  Google Scholar 

  34. Gurung RL et al (2019) Ethnic disparities in relationships of obesity indices with telomere length in Asians with type 2 diabetes. J Diabetes 11(5):386–393. https://doi.org/10.1111/1753-0407.12864

    Article  CAS  Google Scholar 

  35. Martin-Ruiz CM, Gussekloo J, van Heemst D, von Zglinicki T, Westendorp RG (2005) Telomere length in white blood cells is not associated with morbidity or mortality in the oldest old: a population-based study. Aging Cell 4(6):287–290. https://doi.org/10.1111/j.1474-9726.2005.00171.x

    Article  CAS  Google Scholar 

  36. Khalangot M, Krasnienkov D, Vaiserman A et al (2017) Leukocyte telomere length is inversely associated with post-load but not with fasting plasma glucose levels. Exp Biol Med (Maywood) 242(7):700–708. https://doi.org/10.1177/1535370217694096

    Article  CAS  Google Scholar 

  37. Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444(7121):840–846. https://doi.org/10.1038/nature05482

    Article  CAS  Google Scholar 

  38. Bhatt SP, Misra A, Pandey RM, Upadhyay AD (2022) Shortening of leucocyte telomere length is independently correlated with high body mass index and subcutaneous obesity (predominantly truncal), in Asian Indian women with abnormal fasting glycemia. BMJ Open Diabetes Res Care. https://doi.org/10.1136/bmjdrc-2021-002706

    Article  Google Scholar 

  39. Canudas S, Hernandez-Alonso P, Galie S et al (2019) Pistachio consumption modulates DNA oxidation and genes related to telomere maintenance: a crossover randomized clinical trial. Am J Clin Nutr 109(6):1738–1745. https://doi.org/10.1093/ajcn/nqz048

    Article  Google Scholar 

  40. Mundstock E, Sarria EE, Zatti H et al (2015) Effect of obesity on telomere length: systematic review and meta-analysis. Obesity (Silver Spring) 23(11):2165–2174. https://doi.org/10.1002/oby.21183

    Article  Google Scholar 

  41. Du M, Prescott J, Cornelis MC et al (2013) Genetic predisposition to higher body mass index or type 2 diabetes and leukocyte telomere length in the nurses’ health study. PLoS ONE 8(2):e52240. https://doi.org/10.1371/journal.pone.0052240

    Article  CAS  Google Scholar 

  42. Krasnienkov DS, Khalangot MD, Kravchenko VI et al (2018) Hyperglycemia attenuates the association between telomere length and age in Ukrainian population. Exp Gerontol 110:247–252. https://doi.org/10.1016/j.exger.2018.06.027

    Article  CAS  Google Scholar 

  43. Astuti Y, Wardhana A, Watkins J, Wulaningsih W, Network PR (2017) Cigarette smoking and telomere length: a systematic review of 84 studies and meta-analysis. Environ Res 158:480–489. https://doi.org/10.1016/j.envres.2017.06.038

    Article  CAS  Google Scholar 

  44. Yun M, Li S, Yan Y et al (2019) Suppression effect of body weight on the association between cigarette smoking and telomere length: the Bogalusa heart study. Aging (Albany NY) 11(21):9893–9900. https://doi.org/10.18632/aging.102439

    Article  Google Scholar 

  45. Kirkman MS, Briscoe VJ, Clark N et al (2012) Diabetes in older adults. Diabetes Care 35(12):2650–2664. https://doi.org/10.2337/dc12-1801

    Article  Google Scholar 

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Acknowledgements

We thank the University of Michigan for providing the HRS data. The HRS data were sponsored by the National Institute on Aging (Grant Number: U01AG009740) and conducted by the University of Michigan.

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Authors and Affiliations

  1. School of Nursing, The University of Hong Kong, 3 Sassoon Road, Pokfulam, Hong Kong SAR, China

    Hong-jie Yu, Mandy Ho, Pui Hing Chau & Daniel Yee Tak Fong

  2. State Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong SAR, China

    Leiluo Geng

  3. Department of Medicine, The University of Hong Kong, Hong Kong SAR, China

    Leiluo Geng

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Contributions

YHJ and HM conceptualized and designed the study. YHJ extracted and checked the data, performed the analyses, visualized the results, and drafted the manuscript. All authors revised the manuscript critically and approved the version to be submitted. HM and YHJ are the guarantors of this work and, as such, had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

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Correspondence to Mandy Ho.

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The authors declare that they have no conflict of interest.

Ethical approval

The HRS was supported by a cooperative agreement (Grant U01AG09740) between the National Institute on Aging and the University of Michigan.

Informed consent

The informed consent for enrollment and Medicare link was obtained from participants before they enrolled in the study.

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Yu, Hj., Ho, M., Chau, P.H. et al. Salivary telomere length and the risks of prediabetes and diabetes among middle-aged and older adults: findings from the Health and Retirement Study. Acta Diabetol 60, 273–283 (2023). https://doi.org/10.1007/s00592-022-02004-9

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