Correlates of longitudinal leukocyte telomere length in the Costa Rican Longevity Study of Healthy Aging (CRELES): On the importance of DNA collection and storage procedures
Autoři:
Luis Rosero-Bixby aff001; David H. Rehkopf aff002; William H. Dow aff003; Jue Lin aff004; Elissa S. Epel aff005; Jorge Azofeifa aff006; Alejandro Leal aff006
Působiště autorů:
Centro Centroamericano de Población, Universidad de Costa Rica, San Jose, Costa Rica
aff001; School of Medicine, Division of Primary Care and Population Health, Stanford University, Stanford, CA, United States of America
aff002; Health Policy and Management, University of California Berkeley, Berkeley, CA, United States of America
aff003; Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA, United States of America
aff004; Psychiatry, University of California San Francisco, San Francisco, CA, United States of America
aff005; Escuela de Biología, Universidad de Costa Rica, San Jose, Costa Rica
aff006
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223766
Souhrn
The objective is to identify cofactors of leukocyte telomere length (LTL) in a Latin American population, specifically the association of LTL with 36 socio-demographic, early childhood, and health characteristics, as well as with DNA sample collection and storage procedures. The analysis is based on longitudinal information from a subsample of 1,261 individuals aged 60+ years at baseline from the Costa Rican Study of Longevity and Healthy Aging (CRELES): a nationally representative sample of elderly population. Random effects regression models for panel data were used to estimate the associations with LTL and its longitudinal changes. Sample collection procedures and DNA refrigerator storage time were strongly associated with LTL: telomeres are longer in blood collected in October-December, in DNA extracted from <1-year-old blood cells, and in DNA stored at 4°C for longer periods of time up to five years. The data confirmed that telomeres are shorter at older ages, as well as among males, and diabetic individuals, whereas telomeres are longer in the high-longevity Nicoya region. Most health, biomarkers, and early childhood indicators did not show significant associations with LTL. Longitudinal LTL variation over approximately two years was mainly associated with baseline LTL levels, as found in other studies. Our findings suggest that if there is unavoidable variability in season of sample collection and DNA storage time, these factors should be controlled for in all demographic and epidemiologic studies of LTL. However, due to unobserved components of measurement variation, statistical control may be inadequate as compared to standardization of data collection procedures.
Klíčová slova:
Telomeres – Telomere length – Socioeconomic aspects of health – Biomarkers – Child health – DNA extraction – Specimen storage
Zdroje
1. Epel ES, Prather AA. Stress, Telomeres, and Psychopathology: Toward a Deeper Understanding of a Triad of Early Aging. Annual review of clinical psychology. 2018;14:371–97. doi: 10.1146/annurev-clinpsy-032816-045054 29494257
2. Mathur MB, Epel E, Kind S, Desai M, Parks CG, Sandler DP, et al. Perceived stress and telomere length: A systematic review, meta-analysis, and methodologic considerations for advancing the field. Brain, behavior, and immunity. 2016;54:158–69. doi: 10.1016/j.bbi.2016.02.002 26853993
3. Needham BL, Adler N, Gregorich S, Rehkopf D, Lin J, Blackburn EH, et al. Socioeconomic status, health behavior, and leukocyte telomere length in the National Health and Nutrition Examination Survey, 1999–2002. Soc Sci Med. 2013;85:1–8. doi: 10.1016/j.socscimed.2013.02.023 23540359
4. Oliveira BS, Zunzunegui MV, Quinlan J, Fahmi H, Tu MT, Guerra RO. Systematic review of the association between chronic social stress and telomere length: A life course perspective. Ageing research reviews. 2016;26:37–52. doi: 10.1016/j.arr.2015.12.006 26732034
5. Puterman E, Lin J, Blackburn E, O'Donovan A, Adler N, Epel E. The power of exercise: buffering the effect of chronic stress on telomere length. PLoS One. 2010;5(5):e10837. doi: 10.1371/journal.pone.0010837 20520771
6. Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366(9486):662–4. doi: 10.1016/S0140-6736(05)66630-5 16112303
7. Codd V, Nelson CP, Albrecht E, Mangino M, Deelen J, Buxton JL, et al. Identification of seven loci affecting mean telomere length and their association with disease. Nature genetics. 2013;45(4):422. doi: 10.1038/ng.2528 23535734
8. Zhan Y, Song C, Karlsson R, Tillander A, Reynolds CA, Pedersen NL, et al. Telomere length shortening and Alzheimer disease—a Mendelian randomization study. JAMA neurology. 2015;72(10):1202–3. doi: 10.1001/jamaneurol.2015.1513 26457630
9. Sanders JL, Newman AB. Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiologic reviews. 2013;35(1):112–31.
10. Fernández-Eulate G, Alberro A, Muñoz-Culla M, Zulaica M, Zufiria M, Barandiaran M, et al. Blood markers in Healthy-aged Nonagenarians: A combination of high telomere length and low amyloidβ are strongly associated with healthy ageing in the oldest old. Frontiers in aging neuroscience. 2018;10:380. doi: 10.3389/fnagi.2018.00380 30546303
11. Belsky DW, Caspi A, Houts R, Cohen HJ, Corcoran DL, Danese A, et al. Quantification of biological aging in young adults. Proc Natl Acad Sci U S A. 2015;112(30):E4104–10. doi: 10.1073/pnas.1506264112 26150497
12. Wang X-b, Cui N-h, Zhang S, Liu Z-j, Ma J-f, Ming L. Leukocyte telomere length, mitochondrial DNA copy number, and coronary artery disease risk and severity: A two-stage case-control study of 3064 Chinese subjects. Atherosclerosis. 2019;284:165–72. doi: 10.1016/j.atherosclerosis.2019.03.010 30921599
13. Dean SG, Zhang C, Gao J, Roy S, Shinkle J, Sabarinathan M, et al. The association between telomere length and mortality in Bangladesh. Aging (Albany NY). 2017;9(6):1537. doi: 10.18632/aging.101246 28630379
14. Yu R, Tang N, Leung J, Woo J. Telomere length is not associated with frailty in older Chinese elderly: Cross-sectional and longitudinal analysis. Mechanisms of ageing and development. 2015;152:74–9. doi: 10.1016/j.mad.2015.10.002 26483096
15. Glei DA, Goldman N, Weinstein M, Risques RA. Shorter ends, faster end? Leukocyte telomere length and mortality among older Taiwanese. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences. 2014;70(12):1490–8.
16. Lapham K, Kvale MN, Lin J, Connell S, Croen LA, Dispensa BP, et al. Automated assay of telomere length measurement and informatics for 100,000 subjects in the genetic epidemiology research on adult health and aging (GERA) cohort. Genetics. 2015;200(4):1061–72. doi: 10.1534/genetics.115.178624 26092717
17. Rode L, Nordestgaard BG, Bojesen SE. Peripheral blood leukocyte telomere length and mortality among 64 637 individuals from the general population. Journal of the National Cancer Institute. 2015;107(6):djv074.
18. Madrid AS, Rode L, Nordestgaard BG, Bojesen SE. Short telomere length and ischemic heart disease: observational and genetic studies in 290 022 individuals. Clinical chemistry. 2016;62(8):1140–9. doi: 10.1373/clinchem.2016.258566 27259814
19. Wium-Andersen MK, Ørsted DD, Rode L, Bojesen SE, Nordestgaard BG. Telomere length and depression: prospective cohort study and Mendelian randomisation study in 67 306 individuals. The British Journal of Psychiatry. 2017;210(1):31–8. doi: 10.1192/bjp.bp.115.178798 27810892
20. Al‐Attas O, Al‐Daghri N, Bamakhramah A, Shaun Sabico S, McTernan P, Huang TK. Telomere length in relation to insulin resistance, inflammation and obesity among Arab youth. Acta paediatrica. 2010;99(6):896–9. doi: 10.1111/j.1651-2227.2010.01720.x 20178511
21. Kark JD, Nassar H, Shaham D, Sinnreich R, Goldberger N, Aboudi V, et al. Leukocyte telomere length and coronary artery calcification in Palestinians. Atherosclerosis. 2013;229(2):363–8. doi: 10.1016/j.atherosclerosis.2013.05.030 23880188
22. Flannagan KS, Jansen EC, Rozek LS, Rentschler KM, Roman AV, Ramirez‐Zea M, et al. Sociodemographic correlates and family aggregation of leukocyte telomere length in adults and children from Mesoamerica. American Journal of Human Biology. 2017;29(3):e22942.
23. Rehkopf DH, Needham BL, Lin J, Blackburn EH, Zota AR, Wojcicki JM, et al. Leukocyte Telomere Length in Relation to 17 Biomarkers of Cardiovascular Disease Risk: A Cross-Sectional Study of US Adults. PLoS Med. 2016;13(11):e1002188. doi: 10.1371/journal.pmed.1002188 27898678
24. Patel CJ, Manrai AK, Corona E, Kohane IS. Systematic correlation of environmental exposure and physiological and self-reported behaviour factors with leukocyte telomere length. International journal of epidemiology. 2016:dyw043.
25. Price LH, Kao H-T, Burgers DE, Carpenter LL, Tyrka AR. Telomeres and early-life stress: an overview. Biological psychiatry. 2013;73(1):15–23. doi: 10.1016/j.biopsych.2012.06.025 22831981
26. Weischer M, Bojesen SE, Nordestgaard BG. Telomere shortening unrelated to smoking, body weight, physical activity, and alcohol intake: 4,576 general population individuals with repeat measurements 10 years apart. PLoS genetics. 2014;10(3):e1004191. doi: 10.1371/journal.pgen.1004191 24625632
27. Verhulst S, Aviv A, Benetos A, Berenson GS, Kark JD. Do leukocyte telomere length dynamics depend on baseline telomere length? An analysis that corrects for ‘regression to the mean’. European Journal of Epidemiology. 2013;28(11):859–66. doi: 10.1007/s10654-013-9845-4 23990212
28. Goglin SE, Farzaneh-Far R, Epel ES, Lin J, Blackburn EH, Whooley MA. Change in Leukocyte Telomere Length Predicts Mortality in Patients with Stable Coronary Heart Disease from the Heart and Soul Study. PloS one. 2016;11(10):e0160748. doi: 10.1371/journal.pone.0160748 27783614
29. Duggan C, Risques RA, Alfano C, Prunkard D, Imayama I, Holte S, et al. Change in peripheral blood leukocyte telomere length and mortality in breast cancer survivors. JNCI: Journal of the National Cancer Institute. 2014;106(4).
30. Farzaneh-Far R, Cawthon RM, Na B, Browner WS, Schiller NB, Whooley MA. Prognostic value of leukocyte telomere length in patients with stable coronary artery disease: data from the Heart and Soul Study. Arteriosclerosis, thrombosis, and vascular biology. 2008;28(7):1379–84. doi: 10.1161/ATVBAHA.108.167049 18467646
31. Rehkopf DH, Dow WH, Rosero-Bixby L, Lin J, Epel ES, Blackburn EH. Seasonal variation of peripheral blood leukocyte telomere length in Costa Rica: A population-based observational study. Am J Hum Biol. 2014;26(3):367–75. doi: 10.1002/ajhb.22529 24615938
32. Campos-Sánchez R, Raventós H, Barrantes R. Ancestry informative markers clarify the regional admixture variation in the Costa Rican population. Human biology. 2014;85(5):721–40.
33. CRELES: Costa Rican Longevity and Health Aging Study, 2005 (Costa Rica Estudio de Longevidad y Envejecimiento Saludable): Sampling and Methods No. ICPSR26681-v2) [Internet]. Inter-university Consortium for Political and Social Research. http://www.icpsr.umich.edu/icpsrweb/NACDA/studies/26681/documentation. Retrieved January 15, 2013.
34. Hermann BG, Frischauf AM. Isolation of genomic DNA. Methods in Enzymology. 1987;152:180–3. doi: 10.1016/0076-6879(87)52018-3 3657568
35. Folstein ME, Folstein SE. Mini-Mental State. A practical method for grading the conitive state of patients for the clinician. Journal of Psychiatric Research. 1975;12(2):189–95.
36. Sheikh JL, Yesavage JA. Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. Clinical Gerontology: A Guide to Assessment and Intervention. New York: The Haworth Press; 1986.
37. Rosero-Bixby L, Dow WH. Predicting mortality with biomarkers: a population-based prospective cohort study for elderly Costa Ricans. Population Health Metrics 2012;10(11).
38. Schafer JL. Multiple imputation: a primer. Statistical methods in medical research. 1999;8(1):3–15. doi: 10.1177/096228029900800102 10347857
39. Royston P, Carlin JB, White IR. Multiple imputation of missing values: new features for mim. Stata Journal. 2009;9(2):252–64.
40. Allison PD. Fixed effects regression models. Thousand Oaks, CA: SAGE publications; 2009.
41. Lin J, Epel E, Cheon J, Kroenke C, Sinclair E, Bigos M, et al. Analyses and comparisons of telomerase activity and telomere length in human T and B cells: insights for epidemiology of telomere maintenance. J Immunol Methods. 2010;352(1–2):71–80. doi: 10.1016/j.jim.2009.09.012 19837074
42. McEwen LM, Morin AM, Edgar RD, MacIsaac JL, Jones MJ, Dow WH, et al. Differential DNA methylation and lymphocyte proportions in a Costa Rican high longevity region. Epigenetics & Chromatin. 2017;10(1).
43. Martin-Ruiz CM, Baird D, Roger L, Boukamp P, Krunic D, Cawthon R, et al. Reproducibility of telomere length assessment: an international collaborative study. International journal of epidemiology. 2015;44(15):1673–83.
44. Verhulst S, Susser E, Factor-Litvak PR, Simons M, Benetos A, Steenstrup T, et al. Response to: Reliability and validity of telomere length measurements. International Journal of Epidemiology. 2016;45(4):1298–301. doi: 10.1093/ije/dyw194 27880696
45. Cunningham JM, Johnson RA, Litzelman K, Skinner HG, Seo S, Engelman CD, et al. Telomere length varies by DNA extraction method: implications for epidemiologic research. Cancer Epidemiology Biomarkers & Prevention. 2013;22(11):2047–54.
46. Richardson AJ, Narendran N, Guymer RH, Vu H, Baird PN. Blood storage at 4 degrees C-factors involved in DNA yield and quality. J Lab Clin Med. 2006;147(6):290–4. doi: 10.1016/j.lab.2006.01.005 16750666
47. Dagnall CL, Hicks B, Teshome K, Hutchinson AA, Gadalla SM, Khincha PP, et al. Effect of pre-analytic variables on the reproducibility of qPCR relative telomere length measurement. PloS one. 2017;12(9):e0184098. doi: 10.1371/journal.pone.0184098 28886139
48. Blackburn EH, Epel ES, Lin J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science, 350(6265), pp1193–1198. 2015;350(6265):1193–8. doi: 10.1126/science.aab3389 26785477
49. von Zglinicki T, Bürkle A, Kirkwood TB. Stress, DNA damage and ageing—an integrative approach. Experimental gerontology. 2001;36(7):1049–62. doi: 10.1016/s0531-5565(01)00111-5 11404050
50. Mather KA, Jorm AF, Parslow RA, Christensen H. Is telomere length a biomarker of aging? A review. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2011;22(2):202–13.
51. Rehkopf D, Dow WH, Rosero-Bixby L, Epel E, Lin J, Blackburn E. Telomere Length in Costa Rica’s Nicoyan Penninsula: A population-based study. Experimental Gerontology. 2013;48(11):1266–73. doi: 10.1016/j.exger.2013.08.005 23988653
52. Rehkopf DH, Dow WH, Rosero-Bixby L. Differences in the association of cardiovascular risk factors with education: a comparison of Costa Rica (CRELES) and the USA (NHANES). Journal of Epidemiology and Community Health. 2010;64(9):821–8. doi: 10.1136/jech.2009.086926 19822554
53. Rosero-Bixby L, Dow WH. Surprising SES Gradients in mortality, health, and biomarkers in a Latin American population of adults. J Gerontol B Psychol Sci Soc Sci. 2009;64(1):105–17. doi: 10.1093/geronb/gbn004 19196695
54. Puterman E, Gemmill A, Karasek D, Weir D, Adler NE, Prather AA, et al. Lifespan adversity and later adulthood telomere length in the nationally representative US Health and Retirement Study. Proceedings of the National Academy of Sciences. 2016;113(42):E6335–E42.
55. Aviv A, Chen W, Gardner JP, Kimura M, Brimacombe M, Cao X, et al. Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa Heart Study. American journal of epidemiology. 2009;169(3):323–9. doi: 10.1093/aje/kwn338 19056834
56. Verhulst S, Aviv A, Benetos A, Berenson GS, Kark JD. Do leukocyte telomere length dynamics depend on baseline telomere length? An analysis that corrects for 'regression to the mean'. Eur J Epidemiol. 2013;28(11):859–66. doi: 10.1007/s10654-013-9845-4 23990212
57. Bendix L, Thinggaard M, Fenger M, Kolvraa S, Avlund K, Linneberg A, et al. Longitudinal changes in leukocyte telomere length and mortality in humans The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2014;69A(2):231–9.
58. Steenstrup T, Hjelmborg J.V.B., Kark J.D., Christensen K. and Aviv A. The telomere lengthening conundrum—artifact or biology? Nucleic acids research. 2013;41(13):e131–e. doi: 10.1093/nar/gkt370 23671336
59. Chen W, Kimura M, Kim S, Cao X, Srinivasan SR, Berenson GS, et al. Longitudinal versus cross-sectional evaluations of leukocyte telomere length dynamics: age-dependent telomere shortening is the rule. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2011;66A(3):312–9.
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Eliquis (apixaban) nově hrazen ze zdravotního pojištění
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs