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Micronutrient status and leukocyte telomere length in school-age Colombian children

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Abstract

Purpose

Leukocyte telomere length (LTL) is a biomarker of inflammation and oxidative stress that predicts chronic disease risk. Nutritional factors are related to LTL in adulthood, but these associations are not well characterized in children. We examined whether micronutrient status biomarkers were associated with LTL in school-age children.

Methods

We conducted a cross-sectional study of 330 boys and 393 girls aged 5–12 years from Bogotá, Colombia. We quantified blood concentrations of hemoglobin, ferritin, zinc, vitamin A, folate, and vitamin B-12; and measured LTL using qPCR in DNA extracted from buffy coat. We estimated mean differences in LTL by quartiles of micronutrient status biomarkers and categories of relevant sociodemographic and anthropometric covariates with the use of linear regression.

Results

In girls, plasma vitamin B-12 was positively associated with LTL (adjusted LTL difference between extreme vitamin B-12 quartiles = 0.11; P, trend = 0.02). LTL was also positively associated with birth order in girls (P, trend = 0.02). In boys, LTL was not related to the micronutrient status biomarkers but, unexpectedly, it was positively associated with birth weight (P = 0.02), height-for-age Z score (P, trend = 0.01), and serum C-reactive protein (P, trend = 0.01).

Conclusions

LTL is associated with vitamin B-12 status among girls. LTL is also associated with birth weight, height, and C-reactive protein in boys.

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References

  1. Blackburn EH (2005) Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett 579:859–862. https://doi.org/10.1016/j.febslet.2004.11.036

    Article  CAS  PubMed  Google Scholar 

  2. Broer L, Codd V, Nyholt DR et al (2013) Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet 21:1163–1168. https://doi.org/10.1038/ejhg.2012.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dalgård C, Benetos A, Verhulst S et al (2015) Leukocyte telomere length dynamics in women and men: menopause vs age effects. Int J Epidemiol 44:1688–1695. https://doi.org/10.1093/ije/dyv165

    Article  PubMed  PubMed Central  Google Scholar 

  4. Starkweather AR, Alhaeeri AA, Montpetit A et al (2014) An integrative review of factors associated with telomere length and implications for biobehavioral research. Nurs Res 63:36–50. https://doi.org/10.1097/NNR.0000000000000009

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hjelmborg JB, Dalgard C, Moller S et al (2015) The heritability of leucocyte telomere length dynamics. J Med Genet 52:297–302. https://doi.org/10.1136/jmedgenet-2014-102736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Frenck RW, Blackburn EH, Shannon KM (1998) The rate of telomere sequence loss in human leukocytes varies with age. Proc Natl Acad Sci 95:5607–5610

    Article  CAS  Google Scholar 

  7. Paul L (2011) Diet, nutrition and telomere length. J Nutr Biochem 22:895–901. https://doi.org/10.1016/j.jnutbio.2010.12.001

    Article  CAS  PubMed  Google Scholar 

  8. Mons U, Müezzinler A, Schöttker B et al (2017) Leukocyte telomere length and all-cause, cardiovascular disease, and cancer mortality: results from individual-participant-data meta-analysis of 2 large prospective cohort studies. Am J Epidemiol 185:1317–1326. https://doi.org/10.1093/aje/kww210

    Article  PubMed  PubMed Central  Google Scholar 

  9. Haycock PC, Heydon EE, Kaptoge S et al (2014) Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ 349:g4227. https://doi.org/10.1136/bmj.g4227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Entringer S, Epel ES, Lin J et al (2015) Maternal folate concentration in early pregnancy and newborn telomere length. Ann Nutr Metab 66:202–208. https://doi.org/10.1159/000381925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kim J-H, Kim GJ, Lee D et al (2017) Higher maternal vitamin D concentrations are associated with longer leukocyte telomeres in newborns. Matern Child Nutr. https://doi.org/10.1111/mcn.12475

    Article  PubMed  PubMed Central  Google Scholar 

  12. Milne E, O’Callaghan N, Ramankutty P et al (2015) Plasma micronutrient levels and telomere length in children. Nutrition 31:331–336. https://doi.org/10.1016/j.nut.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  13. Arsenault JE, Mora-Plazas M, Forero Y et al (2009) Provision of a school snack is associated with vitamin B-12 status, linear growth, and morbidity in children from Bogotá, Colombia. J Nutr 139:1744–1750. https://doi.org/10.3945/jn.109.108662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Harrison GG, Stormer A, Herman DR, Winham DM (2003) Development of a spanish-language version of the U.S. household food security survey module. J Nutr 133:1192–1197

    Article  CAS  Google Scholar 

  15. Álvarez MC, Estrada A, Montoya EC, Melgar-Quiñónez H (2006) Validation of a household food security scale in Antioquia, Colombia. Salud Publica Mex 48:474–481

    Article  Google Scholar 

  16. Makino T, Takahara K (1981) Direct determination of plasma copper and zinc in infants by atomic absorption with discrete nebulization. Clin Chem 27:1445–1447

    Article  CAS  Google Scholar 

  17. Cawthon RM (2009) Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res 37:e21–e21. https://doi.org/10.1093/nar/gkn1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Eisenberg DTA, Kuzawa CW, Hayes MG (2015) Improving qPCR telomere length assays: controlling for well position effects increases statistical power. Am J Hum Biol 27:570–575. https://doi.org/10.1002/ajhb.22690

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lin J, Epel E, Cheon J et al (2010) Analyses and comparisons of telomerase activity and telomere length in human T and B cells: insights for epidemiology of telomere maintenance. J Immunol Methods 352:71–80. https://doi.org/10.1016/j.jim.2009.09.012

    Article  CAS  PubMed  Google Scholar 

  20. Needham BL, Rehkopf D, Adler N et al (2015) Leukocyte telomere length and mortality in the national health and nutrition examination survey, 1999–2002. Epidemiology 26:528–535. https://doi.org/10.1097/EDE.0000000000000299

    Article  PubMed  PubMed Central  Google Scholar 

  21. Villamor E, Bosch RJ (2015) Optimal treatment of replicate measurements in anthropometric studies. Ann Hum Biol 42:507–510. https://doi.org/10.3109/03014460.2014.969488

    Article  PubMed  Google Scholar 

  22. Joint World Health Organization/Centers for Disease Control and Prevention Technical Consultation (2004) Assessing the iron status of populations including literature reviews, 2nd edn. World Health Organization/Centers for Disease Control and Prevention, Geneva

    Google Scholar 

  23. Zimmermann MB, Hurrell RF (2007) Nutritional iron deficiency. Lancet 370:511–520. https://doi.org/10.1016/S0140-6736(07)61235-5

    Article  CAS  PubMed  Google Scholar 

  24. Villamor E, Mora-Plazas M, Forero Y et al (2008) Vitamin B-12 status is associated with socioeconomic level and adherence to an animal food dietary pattern in Colombian school children. J Nutr 138:1391–1398

    Article  CAS  Google Scholar 

  25. Sommer A, Davidson FR (2002) Assessment and control of vitamin A deficiency: the Annecy accords. J Nutr 132:2845S–2850S

    Article  CAS  Google Scholar 

  26. de Onis M (2007) Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85:660–667. https://doi.org/10.2471/BLT.07.043497

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bickel G, Nord M, Price C et al (2000) Guide to measuring household food security. USDA Food and Nutrition Service, Alexandria

    Google Scholar 

  28. Arsenault JE, Mora-Plazas M, Forero Y et al (2009) Hemoglobin concentration is inversely associated with erythrocyte folate concentrations in Colombian school-age children, especially among children with low vitamin B-12 status. Eur J Clin Nutr 63:842–849. https://doi.org/10.1038/ejcn.2008.50

    Article  CAS  PubMed  Google Scholar 

  29. Morris MS, Jacques PF, Rosenberg IH, Selhub J (2007) Folate and vitamin B-12 status in relation to anemia, macrocytosis, and cognitive impairment in older Americans in the age of folic acid fortification. Am J Clin Nutr 85:193–200. https://doi.org/10.1093/ajcn/85.1.193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. White H (1980) A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica 48:817–838. https://doi.org/10.2307/1912934

    Article  Google Scholar 

  31. Schafer JL (1997) Analysis of incomplete multivariate data. CRC Press, Boca Raton

    Book  Google Scholar 

  32. Liu JJ, Prescott J, Giovannucci E et al (2013) One-carbon metabolism factors and leukocyte telomere length. Am J Clin Nutr 97:794–799. https://doi.org/10.3945/ajcn.112.051557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nomura SJ, Robien K, Zota AR (2017) Serum folate, vitamin B-12, vitamin A, γ-tocopherol, α-tocopherol, and carotenoids do not modify associations between cadmium exposure and leukocyte telomere length in the general US adult population. J Nutr 147:538–548. https://doi.org/10.3945/jn.116.243162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Shin C, Baik I (2016) Leukocyte telomere length is associated with serum vitamin B-12 and homocysteine levels in older adults with the presence of systemic inflammation. Clin Nutr Res 5:7–14. https://doi.org/10.7762/cnr.2016.5.1.7

    Article  PubMed  PubMed Central  Google Scholar 

  35. Bull CF, O’Callaghan NJ, Mayrhofer G, Fenech MF (2009) Telomere length in lymphocytes of older south Australian men may be inversely associated with plasma homocysteine. Rejuvenation Res 12:341–349. https://doi.org/10.1089/rej.2009.0868

    Article  CAS  PubMed  Google Scholar 

  36. Rane G, Koh W-P, Kanchi MM et al (2015) Association between leukocyte telomere length and plasma homocysteine in a Singapore Chinese population. Rejuvenation Res 18:203–210. https://doi.org/10.1089/rej.2014.1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zhang D, Wen X, Wu W et al (2013) Homocysteine-related hTERT DNA demethylation contributes to shortened leukocyte telomere length in atherosclerosis. Atherosclerosis 231:173–179. https://doi.org/10.1016/j.atherosclerosis.2013.08.029

    Article  CAS  PubMed  Google Scholar 

  38. Zhang D, Wen X, Zhang L, Cui W (2014) DNA methylation of human telomerase reverse transcriptase associated with leukocyte telomere length shortening in hyperhomocysteinemia-type hypertension in humans and in a rat model. Circ J 78:1915–1923. https://doi.org/10.1253/circj.CJ-14-0233

    Article  CAS  PubMed  Google Scholar 

  39. Xu Q, Parks CG, DeRoo LA et al (2009) Multivitamin use and telomere length in women. Am J Clin Nutr 89:1857–1863. https://doi.org/10.3945/ajcn.2008.26986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Fretts AM, Howard BV, Siscovick DS et al (2016) Processed meat, but not unprocessed red meat, is inversely associated with leukocyte telomere length in the strong heart family study. J Nutr 146:2013–2018. https://doi.org/10.3945/jn.116.234922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Paul L, Cattaneo M, D’Angelo A et al (2009) Telomere length in peripheral blood mononuclear cells is associated with folate status in men. J Nutr 139:1273–1278. https://doi.org/10.3945/jn.109.104984

    Article  CAS  PubMed  Google Scholar 

  42. Lee J-Y, Shin C, Baik I (2017) Longitudinal associations between micronutrient consumption and leukocyte telomere length. J Hum Nutr Diet Off J Br Diet Assoc 30:236–243. https://doi.org/10.1111/jhn.12403

    Article  Google Scholar 

  43. de Zegher F, Díaz M, Lopez-Bermejo A, Ibáñez L (2016) Recognition of a sequence: more growth before birth, longer telomeres at birth, more lean mass after birth. Pediatr Obes 12:274–279. https://doi.org/10.1111/ijpo.12137

    Article  PubMed  Google Scholar 

  44. Smeets CCJ, Codd V, Denniff M et al (2017) Effects of size at birth, childhood growth patterns and growth hormone treatment on leukocyte telomere length. PLoS One. https://doi.org/10.1371/journal.pone.0171825

    Article  PubMed  PubMed Central  Google Scholar 

  45. Akkad A, Hastings R, Konje J et al (2006) Telomere length in small-for-gestational-age babies. BJOG Int J Obstet Gynaecol 113:318–323. https://doi.org/10.1111/j.1471-0528.2005.00839.x

    Article  CAS  Google Scholar 

  46. Pearce MS, Mann KD, Martin-Ruiz C et al (2012) Childhood growth, IQ and education as predictors of white blood cell telomere length at age 49–51 years: the newcastle thousand families study. PLoS One 7:e40116. https://doi.org/10.1371/journal.pone.0040116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Cui Y, Gao Y-T, Cai Q et al (2013) Associations of leukocyte telomere length with body anthropometric indices and weight change in chinese women. Obesity 21:2582–2588. https://doi.org/10.1002/oby.20321

    Article  PubMed  Google Scholar 

  48. Flannagan KS, Jansen EC, Rozek LS et al (2017) Sociodemographic correlates and family aggregation of leukocyte telomere length in adults and children from Mesoamerica. Am J Hum Biol. https://doi.org/10.1002/ajhb.22942

    Article  PubMed  Google Scholar 

  49. Cole TJ (2000) Secular trends in growth. Proc Nutr Soc 59:317–324. https://doi.org/10.1017/S0029665100000355

    Article  CAS  PubMed  Google Scholar 

  50. Al-Attas O, Al-Daghri N, Bamakhramah A et al (2010) Telomere length in relation to insulin resistance, inflammation and obesity among Arab youth. Acta Paediatr 99:896–899. https://doi.org/10.1111/j.1651-2227.2010.01720.x

    Article  CAS  PubMed  Google Scholar 

  51. Sanders JL, Newman AB (2013) Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiol Rev 35:112–131. https://doi.org/10.1093/epirev/mxs008

    Article  PubMed  PubMed Central  Google Scholar 

  52. Rehkopf DH, Needham BL, Lin J et al (2016) Leukocyte telomere length in relation to 17 biomarkers of cardiovascular disease risk: a cross-Sectional study of US adults. PLoS Med. https://doi.org/10.1371/journal.pmed.1002188

    Article  PubMed  PubMed Central  Google Scholar 

  53. Gielen M, Hageman G, Pachen D et al (2014) Placental telomere length decreases with gestational age and is influenced by parity: a study of third trimester live-born twins. Placenta 35:791–796. https://doi.org/10.1016/j.placenta.2014.05.010

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Asistencia Sanitaria Interprovincial S.A. (ASISA) Research Fund at the University of Michigan.

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Authors and Affiliations

  1. Department of Epidemiology, University of Michigan School of Public Health, Room 5507 SPH II, 1415 Washington Heights, Ann Arbor, MI, 48109, USA

    Kerry S. Flannagan, Alison A. Bowman & Eduardo Villamor

  2. Foundation for Research in Nutrition and Health, FINUSAD, Bogotá, Colombia

    Mercedes Mora-Plazas & Constanza Marín

  3. University of La Sabana Medical School, Chía, Colombia

    Constanza Marín

  4. Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA

    Katie M. Rentschler & Laura S. Rozek

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  1. Kerry S. Flannagan
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  2. Alison A. Bowman
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Correspondence to Eduardo Villamor.

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On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standards

This study was conducted according to the guidelines laid down in the Declaration of Helsinki. The Ethics Committee of the National University of Colombia Medical School approved the study procedures, and the Health and Behavioral Sciences Institutional Review Board at the University of Michigan approved the use of data and samples from the study.

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Flannagan, K.S., Bowman, A.A., Mora-Plazas, M. et al. Micronutrient status and leukocyte telomere length in school-age Colombian children. Eur J Nutr 59, 1055–1065 (2020). https://doi.org/10.1007/s00394-019-01966-x

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