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Open Access 01-11-2020 | Post-Traumatic Stress Disorder | Review

Epigenetic clocks may come out of rhythm—implications for the estimation of chronological age in forensic casework

Authors: Barbara Elisabeth Koop, Alexandra Reckert, Julia Becker, Yang Han, Wolfgang Wagner, Stefanie Ritz-Timme

Published in: International Journal of Legal Medicine | Issue 6/2020

Abstract

There is a growing perception that DNA methylation may be influenced by exogenous and endogenous parameters. Knowledge of these factors is of great relevance for the interpretation of DNA-methylation data for the estimation of chronological age in forensic casework. We performed a literature review to identify parameters, which might be of relevance for the prediction of chronological age based on DNA methylation. The quality of age predictions might particularly be influenced by lifetime adversities (chronic stress, trauma/post-traumatic stress disorder (PTSD), violence, low socioeconomic status/education), cancer, obesity and related diseases, infectious diseases (especially HIV and Cytomegalovirus (CMV) infections), sex, ethnicity and exposure to toxins (alcohol, smoking, air pollution, pesticides). Such factors may alter the DNA methylation pattern and may explain the partly high deviations between epigenetic age and chronological age in single cases (despite of low mean absolute deviations) that can also be observed with “epigenetic clocks” comprising a high number of CpG sites. So far, only few publications dealing with forensic age estimation address these confounding factors. Future research should focus on the identification of further relevant confounding factors and the development of models that are “robust” against the influence of such biological factors by systematic investigations under targeted inclusion of diverse and defined cohorts.

Ritz-Timme S, Cattaneo C, Collins MJ, Waite ER, Schutz HW, Kaatsch HJ, Borrman HI (2000) Age estimation: the state of the art in relation to the specific demands of forensic practise. Int J Legal Med 113(3):129–136PubMed

Horvath S (2013) DNA methylation age of human tissues and cell types. Genome Biol 14(10):R115. https://doi.org/10.1186/gb-2013-14-10-r115CrossRefPubMedPubMedCentral

Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, Klotzle B, Bibikova M, Fan JB, Gao Y, Deconde R, Chen M, Rajapakse I, Friend S, Ideker T, Zhang K (2013) Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell 49(2):359–367. https://doi.org/10.1016/j.molcel.2012.10.016CrossRefPubMed

Levine ME, Lu AT, Quach A, Chen BH, Assimes TL, Bandinelli S, Hou L, Baccarelli AA, Stewart JD, Li Y, Whitsel EA, Wilson JG, Reiner AP, Aviv A, Lohman K, Liu Y, Ferrucci L, Horvath S (2018) An epigenetic biomarker of aging for lifespan and healthspan. Aging (Albany NY) 10(4):573–591. https://doi.org/10.18632/aging.101414CrossRef

Weidner CI, Lin Q, Koch CM, Eisele L, Beier F, Ziegler P, Bauerschlag DO, Jockel KH, Erbel R, Muhleisen TW, Zenke M, Brummendorf TH, Wagner W (2014) Aging of blood can be tracked by DNA methylation changes at just three CpG sites. Genome Biol 15(2):R24. https://doi.org/10.1186/gb-2014-15-2-r24CrossRefPubMedPubMedCentral

Parson W (2018) Age estimation with DNA: from forensic DNA fingerprinting to forensic (epi)genomics: a mini-review. Gerontology. 64:326–332. https://doi.org/10.1159/000486239CrossRefPubMed

Koop BE, Mayer F, Gündüz T, Blum J, Becker J, Schaffrath J, Wagner W, Han Y, Boehme P, Ritz-Timme S (2020) Postmortem age estimation via DNA methylation analysis in buccal swabs from corpses in different stages of decomposition - a “proof of principle” study. Int J Legal Med (in press)

Han Y, Franzen J, Stiehl T, Gobs M, Kuo CC, Nikolic M, Hapala J, Koop BE, Strathmann K, Ritz-Timme S, Wagner W (2020) New targeted approaches for epigenetic age predictions. BMC Biol 18(1):71. https://doi.org/10.1186/s12915-020-00807-2CrossRefPubMedPubMedCentral

Cho S, Jung SE, Hong SR, Lee EH, Lee JH, Lee SD, Lee HY (2017) Independent validation of DNA-based approaches for age prediction in blood. Forensic Sci Int Genet 29:250–256. https://doi.org/10.1016/j.fsigen.2017.04.020CrossRefPubMed

10.

Spolnicka M, Pospiech E, Adamczyk JG, Freire-Aradas A, Peplonska B, Zbiec-Piekarska R, Makowska Z, Pieta A, Lareu MV, Phillips C, Ploski R, Zekanowski C, Branicki W (2018) Modified aging of elite athletes revealed by analysis of epigenetic age markers. Aging (Albany NY) 10(2):241–252. https://doi.org/10.18632/aging.101385CrossRef

11.

Spolnicka M, Pospiech E, Peplonska B, Zbiec-Piekarska R, Makowska Z, Pieta A, Karlowska-Pik J, Ziemkiewicz B, Wezyk M, Gasperowicz P, Bednarczuk T, Barcikowska M, Zekanowski C, Ploski R, Branicki W (2017) DNA methylation in ELOVL2 and C1orf132 correctly predicted chronological age of individuals from three disease groups. Int J Legal Med 132:1–11. https://doi.org/10.1007/s00414-017-1636-0CrossRefPubMedPubMedCentral

12.

Spolnicka M, Zbiec-Piekarska R, Karp M, Machnicki MM, Wlasiuk P, Makowska Z, Pieta A, Gambin T, Gasperowicz P, Branicki W, Giannopoulos K, Stoklosa T, Ploski R (2018) DNA methylation signature in blood does not predict calendar age in patients with chronic lymphocytic leukemia but may alert to the presence of disease. Forensic Sci Int Genet 34:e15–e17. https://doi.org/10.1016/j.fsigen.2018.02.004CrossRefPubMed

13.

Bell CG, Lowe R, Adams PD, Baccarelli AA, Beck S, Bell JT, Christensen BC, Gladyshev VN, Heijmans BT, Horvath S, Ideker T, Issa JJ, Kelsey KT, Marioni RE, Reik W, Relton CL, Schalkwyk LC, Teschendorff AE, Wagner W, Zhang K, Rakyan VK (2019) DNA methylation aging clocks: challenges and recommendations. Genome Biol 20(1):249. https://doi.org/10.1186/s13059-019-1824-yCrossRefPubMedPubMedCentral

14.

Zannas AS, Arloth J, Carrillo-Roa T, Iurato S, Roh S, Ressler KJ, Nemeroff CB, Smith AK, Bradley B, Heim C, Menke A, Lange JF, Bruckl T, Ising M, Wray NR, Erhardt A, Binder EB, Mehta D (2015) Lifetime stress accelerates epigenetic aging in an urban, African American cohort: relevance of glucocorticoid signaling. Genome Biol 16:266. https://doi.org/10.1186/s13059-015-0828-5CrossRefPubMedPubMedCentral

15.

Boks MP, van Mierlo HC, Rutten BP, Radstake TR, De Witte L, Geuze E, Horvath S, Schalkwyk LC, Vinkers CH, Broen JC, Vermetten E (2015) Longitudinal changes of telomere length and epigenetic age related to traumatic stress and post-traumatic stress disorder. Psychoneuroendocrinology 51:506–512. https://doi.org/10.1016/j.psyneuen.2014.07.011CrossRefPubMed

16.

Wolf EJ, Logue MW, Hayes JP, Sadeh N, Schichman SA, Stone A, Salat DH, Milberg W, McGlinchey R, Miller MW (2016) Accelerated DNA methylation age: associations with PTSD and neural integrity. Psychoneuroendocrinology 63:155–162. https://doi.org/10.1016/j.psyneuen.2015.09.020CrossRefPubMed

17.

Wolf EJ, Logue MW, Stoop TB, Schichman SA, Stone A, Sadeh N, Hayes JP, Miller MW (2017) Accelerated DNA methylation age: associations with PTSD and mortality. Psychosom Med 80:42–48. https://doi.org/10.1097/PSY.0000000000000506CrossRef

18.

Wolf EJ, Morrison FG (2017) Traumatic stress and accelerated cellular aging: from epigenetics to cardiometabolic disease. Curr Psychiatry Rep 19(10):75. https://doi.org/10.1007/s11920-017-0823-5CrossRefPubMedPubMedCentral

19.

Mehta D, Bruenig D, Lawford B, Harvey W, Carrillo-Roa T, Morris CP, Jovanovic T, Young RM, Binder EB, Voisey J (2018) Accelerated DNA methylation aging and increased resilience in veterans: the biological cost for soldiering on. Neurobiol Stress 8:112–119. https://doi.org/10.1016/j.ynstr.2018.04.001CrossRefPubMedPubMedCentral

20.

Wolf EJ, Maniates H, Nugent N, Maihofer AX, Armstrong D, Ratanatharathorn A, Ashley-Koch AE, Garrett M, Kimbrel NA, Lori A, Va Mid-Atlantic Mirecc W, Aiello AE, Baker DG, Beckham JC, Boks MP, Galea S, Geuze E, Hauser MA, Kessler RC, Koenen KC, Miller MW, Ressler KJ, Risbrough V, Rutten BPF, Stein MB, Ursano RJ, Vermetten E, Vinkers CH, Uddin M, Smith AK, Nievergelt CM, Logue MW (2018) Traumatic stress and accelerated DNA methylation age: a meta-analysis. Psychoneuroendocrinology 92:123–134. https://doi.org/10.1016/j.psyneuen.2017.12.007CrossRefPubMed

21.

Chen E, Miller GE, Yu T, Brody GH (2016) The great recession and health risks in African American youth. Brain Behav Immun 53:234–241. https://doi.org/10.1016/j.bbi.2015.12.015CrossRefPubMed

22.

Simons RL, Lei MK, Beach SR, Philibert RA, Cutrona CE, Gibbons FX, Barr A (2016) Economic hardship and biological weathering: the epigenetics of aging in a U.S. sample of black women. Soc Sci Med 150:192–200. https://doi.org/10.1016/j.socscimed.2015.12.001CrossRefPubMed

23.

Fiorito G, Polidoro S, Dugue PA, Kivimaki M, Ponzi E, Matullo G, Guarrera S, Assumma MB, Georgiadis P, Kyrtopoulos SA, Krogh V, Palli D, Panico S, Sacerdote C, Tumino R, Chadeau-Hyam M, Stringhini S, Severi G, Hodge AM, Giles GG, Marioni R, Karlsson Linner R, O'Halloran AM, Kenny RA, Layte R, Baglietto L, Robinson O, McCrory C, Milne RL, Vineis P (2017) Social adversity and epigenetic aging: a multi-cohort study on socioeconomic differences in peripheral blood DNA methylation. Sci Rep 7(1):16266. https://doi.org/10.1038/s41598-017-16391-5CrossRefPubMedPubMedCentral

24.

Jovanovic T, Vance LA, Cross D, Knight AK, Kilaru V, Michopoulos V, Klengel T, Smith AK (2017) Exposure to violence accelerates epigenetic aging in children. Sci Rep 7(1):8962. https://doi.org/10.1038/s41598-017-09235-9CrossRefPubMedPubMedCentral

25.

Hughes A, Smart M, Gorrie-Stone T, Hannon E, Mill J, Bao Y, Burrage J, Schalkwyk L, Kumari M (2018) Socioeconomic position and DNA methylation age acceleration across the Lifecourse. Am J Epidemiol 187:2346–2354. https://doi.org/10.1093/aje/kwy155CrossRefPubMedPubMedCentral

26.

Austin MK, Chen E, Ross KM, McEwen LM, Maclsaac JL, Kobor MS, Miller GE (2018) Early-life socioeconomic disadvantage, not current, predicts accelerated epigenetic aging of monocytes. Psychoneuroendocrinology 97:131–134. https://doi.org/10.1016/j.psyneuen.2018.07.007CrossRefPubMed

27.

Fiorito G, McCrory C, Robinson O, Carmeli C, Rosales CO, Zhang Y, Colicino E, Dugue PA, Artaud F, McKay GJ, Jeong A, Mishra PP, Nost TH, Krogh V, Panico S, Sacerdote C, Tumino R, Palli D, Matullo G, Guarrera S, Gandini M, Bochud M, Dermitzakis E, Muka T, Schwartz J, Vokonas PS, Just A, Hodge AM, Giles GG, Southey MC, Hurme MA, Young I, McKnight AJ, Kunze S, Waldenberger M, Peters A, Schwettmann L, Lund E, Baccarelli A, Milne RL, Kenny RA, Elbaz A, Brenner H, Kee F, Voortman T, Probst-Hensch N, Lehtimaki T, Elliot P, Stringhini S, Vineis P, Polidoro S, Consortium B, Lifepath C (2019) Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: a multi-cohort analysis. Aging (Albany NY) 11(7):2045–2070. https://doi.org/10.18632/aging.101900CrossRef

28.

Tajuddin SM, Hernandez DG, Chen BH, Noren Hooten N, Mode NA, Nalls MA, Singleton AB, Ejiogu N, Chitrala KN, Zonderman AB, Evans MK (2019) Novel age-associated DNA methylation changes and epigenetic age acceleration in middle-aged African Americans and whites. Clin Epigenetics 11(1):119. https://doi.org/10.1186/s13148-019-0722-1CrossRefPubMedPubMedCentral

29.

Thurston RC, Carroll JE, Levine M, Chang Y, Crandall C, Manson JE, Pal L, Hou L, Shadyab AH, Horvath S (2020) Vasomotor symptoms and accelerated epigenetic aging in the Women’s Health Initiative (WHI). J Clin Endocrinol Metab 105(4):1221–1227. https://doi.org/10.1210/clinem/dgaa081CrossRefPubMedCentral

30.

Marini S, Davis KA, Soare TW, Zhu Y, Suderman MJ, Simpkin AJ, Smith A, Wolf EJ, Relton CL, Dunn EC (2020) Adversity exposure during sensitive periods predicts accelerated epigenetic aging in children. Psychoneuroendocrinology 113:104484. https://doi.org/10.1016/j.psyneuen.2019.104484CrossRefPubMed

31.

Linner RK, Marioni RE, Rietveld CA, Simpkin AJ, Davies NM, Watanabe K, Armstrong NJ, Auro K, Baumbach C, Bonder MJ, Buchwald J, Fiorito G, Ismail K, Iurato S, Joensuu A, Karell P, Kasela S, Lahti J, Mcrae AF, Mandaviya PR, Seppala I, Wang Y, Baglietto L, Binder EB, Harris SE, Hodge AM, Horvath S, Hurme M, Johannesson M, Latvala A, Mather KA, Medland SE, Metspalu A, Milani L, Milne RL, Pattie A, Pedersen NL, Peters A, Polidoro S, Raikkonen K, Severi G, Starr JM, Stolk L, Waldenberger M, Eriksson JG, Esko T, Franke L, Gieger C, Giles GG, Hagg S, Jousilahti P, Kaprio J, Kahonen M, Lehtimaki T, Martin NG, van Meurs JBC, Ollikainen M, Perola M, Posthuma D, Raitakari OT, Sachdev PS, Taskesen E, Uitterlinden AG, Vineis P, Wijmenga C, Wright MJ, Relton C, Smith GD, Deary IJ, Koellinger PD, Benjamin DJ, Consortium B (2017) An epigenome-wide association study meta-analysis of educational attainment. Mol Psychiatry 22(12):1680–1690. https://doi.org/10.1038/mp.2017.210CrossRef

32.

McCartney DL, Stevenson AJ, Walker RM, Gibson J, Morris SW, Campbell A, Murray AD, Whalley HC, Porteous DJ, McIntosh AM, Evans KL, Deary IJ, Marioni RE (2018) Investigating the relationship between DNA methylation age acceleration and risk factors for Alzheimer’s disease. Alzheimers Dement (Amst) 10:429–437. https://doi.org/10.1016/j.dadm.2018.05.006CrossRef

33.

Quach A, Levine ME, Tanaka T, Lu AT, Chen BH, Ferrucci L, Ritz B, Bandinelli S, Neuhouser ML, Beasley JM, Snetselaar L, Wallace RB, Tsao PS, Absher D, Assimes TL, Stewart JD, Li Y, Hou L, Baccarelli AA, Whitsel EA, Horvath S (2017) Epigenetic clock analysis of diet, exercise, education, and lifestyle factors. Aging (Albany NY) 9(2):419–446. https://doi.org/10.18632/aging.101168CrossRef

34.

Sumner JA, Colich NL, Uddin M, Armstrong D, McLaughlin KA (2018) Early experiences of threat, but not deprivation, are associated with accelerated biological aging in children and adolescents. Biol Psychiatry 85:268–278. https://doi.org/10.1016/j.biopsych.2018.09.008CrossRefPubMedPubMedCentral

35.

Brody GH, Miller GE, Yu T, Beach SR, Chen E (2016) Supportive family environments ameliorate the link between racial discrimination and epigenetic aging: a replication across two longitudinal cohorts. Psychol Sci 27(4):530–541. https://doi.org/10.1177/0956797615626703CrossRefPubMedPubMedCentral

36.

Dugue PA, Bassett JK, Joo JE, Jung CH, Ming Wong E, Moreno-Betancur M, Schmidt D, Makalic E, Li S, Severi G, Hodge AM, Buchanan DD, English DR, Hopper JL, Southey MC, Giles GG, Milne RL (2018) DNA methylation-based biological aging and cancer risk and survival: pooled analysis of seven prospective studies. Int J Cancer 142(8):1611–1619. https://doi.org/10.1002/ijc.31189CrossRefPubMed

37.

Perna L, Zhang Y, Mons U, Holleczek B, Saum KU, Brenner H (2016) Epigenetic age acceleration predicts cancer, cardiovascular, and all-cause mortality in a German case cohort. Clin Epigenetics 8:64. https://doi.org/10.1186/s13148-016-0228-zCrossRefPubMedPubMedCentral

38.

Zheng Y, Joyce BT, Colicino E, Liu L, Zhang W, Dai Q, Shrubsole MJ, Kibbe WA, Gao T, Zhang Z, Jafari N, Vokonas P, Schwartz J, Baccarelli AA, Hou L (2016) Blood epigenetic age may predict cancer incidence and mortality. EBioMedicine 5:68–73. https://doi.org/10.1016/j.ebiom.2016.02.008CrossRefPubMedPubMedCentral

39.

Ambatipudi S, Horvath S, Perrier F, Cuenin C, Hernandez-Vargas H, Le Calvez-Kelm F, Durand G, Byrnes G, Ferrari P, Bouaoun L, Sklias A, Chajes V, Overvad K, Severi G, Baglietto L, Clavel-Chapelon F, Kaaks R, Barrdahl M, Boeing H, Trichopoulou A, Lagiou P, Naska A, Masala G, Agnoli C, Polidoro S, Tumino R, Panico S, Dolle M, Peeters PHM, Onland-Moret NC, Sandanger TM, Nost TH, Weiderpass E, Quiros JR, Agudo A, Rodriguez-Barranco M, Huerta Castano JM, Barricarte A, Fernandez AM, Travis RC, Vineis P, Muller DC, Riboli E, Gunter M, Romieu I, Herceg Z (2017) DNA methylome analysis identifies accelerated epigenetic ageing associated with postmenopausal breast cancer susceptibility. Eur J Cancer 75:299–307. https://doi.org/10.1016/j.ejca.2017.01.014CrossRefPubMedPubMedCentral

40.

Levine ME, Hosgood HD, Chen B, Absher D, Assimes T, Horvath S (2015) DNA methylation age of blood predicts future onset of lung cancer in the women's health initiative. Aging (Albany NY) 7(9):690–700. https://doi.org/10.18632/aging.100809CrossRef

41.

Durso DF, Bacalini MG, Sala C, Pirazzini C, Marasco E, Bonafe M, do Valle IF, Gentilini D, Castellani G, Faria AMC, Franceschi C, Garagnani P, Nardini C (2017) Acceleration of leukocytes’ epigenetic age as an early tumor and sex-specific marker of breast and colorectal cancer. Oncotarget 8(14):23237–23245. https://doi.org/10.18632/oncotarget.15573CrossRefPubMedPubMedCentral

42.

Nevalainen T, Kananen L, Marttila S, Jylhava J, Mononen N, Kahonen M, Raitakari OT, Hervonen A, Jylha M, Lehtimaki T, Hurme M (2017) Obesity accelerates epigenetic aging in middle-aged but not in elderly individuals. Clin Epigenetics 9:20. https://doi.org/10.1186/s13148-016-0301-7CrossRefPubMedPubMedCentral

43.

Simpkin AJ, Cooper R, Howe LD, Relton CL, Davey Smith G, Teschendorff A, Widschwendter M, Wong A, Kuh D, Hardy R (2017) Are objective measures of physical capability related to accelerated epigenetic age? Findings from a British birth cohort. BMJ Open 7(10):e016708. https://doi.org/10.1136/bmjopen-2017-016708CrossRefPubMedPubMedCentral

44.

Li C, Wang Z, Hardy T, Huang Y, Hui Q, Crusto CA, Wright ML, Taylor JY, Sun YV (2019) Association of Obesity with DNA methylation age acceleration in African American mothers from the InterGEN study. Int J Mol Sci 20(17). https://doi.org/10.3390/ijms20174273

45.

Horvath S, Levine AJ (2015) HIV-1 infection accelerates age according to the epigenetic clock. J Infect Dis 212(10):1563–1573. https://doi.org/10.1093/infdis/jiv277CrossRefPubMedPubMedCentral

46.

Gross AM, Jaeger PA, Kreisberg JF, Licon K, Jepsen KL, Khosroheidari M, Morsey BM, Swindells S, Shen H, Ng CT, Flagg K, Chen D, Zhang K, Fox HS, Ideker T (2016) Methylome-wide analysis of chronic HIV infection reveals five-year increase in biological age and epigenetic targeting of HLA. Mol Cell 62(2):157–168. https://doi.org/10.1016/j.molcel.2016.03.019CrossRefPubMedPubMedCentral

47.

Kananen L, Nevalainen T, Jylhava J, Marttila S, Hervonen A, Jylha M, Hurme M (2015) Cytomegalovirus infection accelerates epigenetic aging. Exp Gerontol 72:227–229. https://doi.org/10.1016/j.exger.2015.10.008CrossRefPubMed

48.

Gao X, Zhang Y, Brenner H (2017) Associations of helicobacter pylori infection and chronic atrophic gastritis with accelerated epigenetic ageing in older adults. Br J Cancer 117(8):1211–1214. https://doi.org/10.1038/bjc.2017.314CrossRefPubMedPubMedCentral

49.

Rosen AD, Robertson KD, Hlady RA, Muench C, Lee J, Philibert R, Horvath S, Kaminsky ZA, Lohoff FW (2018) DNA methylation age is accelerated in alcohol dependence. Transl Psychiatry 8(1):182. https://doi.org/10.1038/s41398-018-0233-4CrossRefPubMedPubMedCentral

50.

Luo A, Jung J, Longley M, Rosoff DB, Charlet K, Muench C, Lee J, Hodgkinson CA, Goldman D, Horvath S, Kaminsky ZA, Lohoff FW (2020) Epigenetic aging is accelerated in alcohol use disorder and regulated by genetic variation in APOL2. Neuropsychopharmacology 45(2):327–336. https://doi.org/10.1038/s41386-019-0500-yCrossRefPubMed

51.

Gao X, Zhang Y, Breitling LP, Brenner H (2016) Relationship of tobacco smoking and smoking-related DNA methylation with epigenetic age acceleration. Oncotarget 7(30):46878–46889. https://doi.org/10.18632/oncotarget.9795CrossRefPubMedPubMedCentral

52.

Vidal-Bralo L, Lopez-Golan Y, Gonzalez A (2016) Simplified assay for epigenetic age estimation in whole blood of adults. Front Genet 7:126. https://doi.org/10.3389/fgene.2016.00126CrossRefPubMedPubMedCentral

53.

Yang Y, Gao X, Just AC, Colicino E, Wang C, Coull BA, Hou L, Zheng Y, Vokonas P, Schwartz J, Baccarelli AA (2019) Smoking-related DNA methylation is associated with DNA methylation phenotypic age acceleration: the veterans affairs normative aging study. Int J Environ Res Public Health 16(13). https://doi.org/10.3390/ijerph16132356

54.

Ward-Caviness CK, Nwanaji-Enwerem JC, Wolf K, Wahl S, Colicino E, Trevisi L, Kloog I, Just AC, Vokonas P, Cyrys J, Gieger C, Schwartz J, Baccarelli AA, Schneider A, Peters A (2016) Long-term exposure to air pollution is associated with biological aging. Oncotarget 7(46):74510–74525. https://doi.org/10.18632/oncotarget.12903CrossRefPubMedPubMedCentral

55.

Li J, Zhu X, Yu K, Jiang H, Zhang Y, Wang B, Liu X, Deng S, Hu J, Deng Q, Sun H, Guo H, Zhang X, Chen W, Yuan J, He M, Bai Y, Han X, Liu B, Liu C, Guo Y, Zhang B, Zhang Z, Hu FB, Gao W, Li L, Lathrop M, Laprise C, Liang L, Wu T (2018) Exposure to polycyclic aromatic hydrocarbons and accelerated DNA methylation aging. Environ Health Perspect 126(6):067005. https://doi.org/10.1289/EHP2773CrossRefPubMedPubMedCentral

56.

Nwanaji-Enwerem JC, Colicino E, Trevisi L, Kloog I, Just AC, Shen J, Brennan K, Dereix A, Hou L, Vokonas P, Schwartz J, Baccarelli AA (2016) Long-term ambient particle exposures and blood DNA methylation age: findings from the VA normative aging study. Environ Epigenet 2(2). https://doi.org/10.1093/eep/dvw006

57.

Nwanaji-Enwerem JC, Dai L, Colicino E, Oulhote Y, Di Q, Kloog I, Just AC, Hou L, Vokonas P, Baccarelli AA, Weisskopf MG, Schwartz JD (2017) Associations between long-term exposure to PM2.5 component species and blood DNA methylation age in the elderly: the VA normative aging study. Environ Int 102:57–65. https://doi.org/10.1016/j.envint.2016.12.024CrossRefPubMedPubMedCentral

58.

Lind PM, Salihovic S, Lind L (2018) High plasma organochlorine pesticide levels are related to increased biological age as calculated by DNA methylation analysis. Environ Int 113:109–113. https://doi.org/10.1016/j.envint.2018.01.019CrossRefPubMed

59.

White AJ, Kresovich JK, Keller JP, Xu Z, Kaufman JD, Weinberg CR, Taylor JA, Sandler DP (2019) Air pollution, particulate matter composition and methylation-based biologic age. Environ Int 132:105071. https://doi.org/10.1016/j.envint.2019.105071CrossRefPubMedPubMedCentral

60.

Horvath S, Gurven M, Levine ME, Trumble BC, Kaplan H, Allayee H, Ritz BR, Chen B, Lu AT, Rickabaugh TM, Jamieson BD, Sun D, Li S, Chen W, Quintana-Murci L, Fagny M, Kobor MS, Tsao PS, Reiner AP, Edlefsen KL, Absher D, Assimes TL (2016) An epigenetic clock analysis of race/ethnicity, sex, and coronary heart disease. Genome Biol 17(1):171. https://doi.org/10.1186/s13059-016-1030-0CrossRefPubMedPubMedCentral

61.

Simpkin AJ, Hemani G, Suderman M, Gaunt TR, Lyttleton O, McArdle WL, Ring SM, Sharp GC, Tilling K, Horvath S, Kunze S, Peters A, Waldenberger M, Ward-Caviness C, Nohr EA, Sorensen TI, Relton CL, Smith GD (2016) Prenatal and early life influences on epigenetic age in children: a study of mother-offspring pairs from two cohort studies. Hum Mol Genet 25(1):191–201. https://doi.org/10.1093/hmg/ddv456CrossRefPubMed

62.

Javed R, Chen W, Lin F, Liang H (2016) Infant's DNA methylation age at birth and epigenetic aging accelerators. Biomed Res Int 2016:4515928–4515910. https://doi.org/10.1155/2016/4515928CrossRefPubMedPubMedCentral

63.

Zbiec-Piekarska R, Spolnicka M, Kupiec T, Parys-Proszek A, Makowska Z, Paleczka A, Kucharczyk K, Ploski R, Branicki W (2015) Development of a forensically useful age prediction method based on DNA methylation analysis. Forensic Sci Int Genet 17:173–179. https://doi.org/10.1016/j.fsigen.2015.05.001CrossRefPubMed

64.

Carroll JE, Irwin MR, Levine M, Seeman TE, Absher D, Assimes T, Horvath S (2017) Epigenetic aging and immune senescence in women with insomnia symptoms: findings from the Women’s Health Initiative study. Biol Psychiatry 81(2):136–144. https://doi.org/10.1016/j.biopsych.2016.07.008CrossRefPubMed

65.

White AJ, Kresovich JK, Xu Z, Sandler DP, Taylor JA (2019) Shift work, DNA methylation and epigenetic age. Int J Epidemiol 48:1536–1544. https://doi.org/10.1093/ije/dyz027CrossRefPubMedPubMedCentral

66.

Brody GH, Yu T, Chen E, Beach SR, Miller GE (2016) Family-centered prevention ameliorates the longitudinal association between risky family processes and epigenetic aging. J Child Psychol Psychiatry 57(5):566–574. https://doi.org/10.1111/jcpp.12495CrossRefPubMed

67.

Horvath S, Ritz BR (2015) Increased epigenetic age and granulocyte counts in the blood of Parkinson's disease patients. Aging (Albany NY) 7(12):1130–1142. https://doi.org/10.18632/aging.100859CrossRef

68.

Horvath S, Oshima J, Martin GM, Lu AT, Quach A, Cohen H, Felton S, Matsuyama M, Lowe D, Kabacik S, Wilson JG, Reiner AP, Maierhofer A, Flunkert J, Aviv A, Hou L, Baccarelli AA, Li Y, Stewart JD, Whitsel EA, Ferrucci L, Matsuyama S, Raj K (2018) Epigenetic clock for skin and blood cells applied to Hutchinson Gilford Progeria syndrome and ex vivo studies. Aging (Albany NY) 10(7):1758–1775. https://doi.org/10.18632/aging.101508CrossRef

69.

Martin-Herranz DE, Aref-Eshghi E, Bonder MJ, Stubbs TM, Choufani S, Weksberg R, Stegle O, Sadikovic B, Reik W, Thornton JM (2019) Screening for genes that accelerate the epigenetic aging clock in humans reveals a role for the H3K36 methyltransferase NSD1. Genome Biol 20(1). https://doi.org/10.1186/s13059-019-1753-9

70.

Horvath S, Pirazzini C, Bacalini MG, Gentilini D, Di Blasio AM, Delledonne M, Mari D, Arosio B, Monti D, Passarino G, De Rango F, D'Aquila P, Giuliani C, Marasco E, Collino S, Descombes P, Garagnani P, Franceschi C (2015) Decreased epigenetic age of PBMCs from Italian semi-supercentenarians and their offspring. Aging (Albany NY) 7(12):1159–1170. https://doi.org/10.18632/aging.100861CrossRef

71.

Kresovich JK, Harmon QE, Xu Z, Nichols HB, Sandler DP, Taylor JA (2019) Reproduction, DNA methylation and biological age. Hum Reprod 34(10):1965–1973. https://doi.org/10.1093/humrep/dez149CrossRefPubMedPubMedCentral

72.

Stringhini S, Sabia S, Shipley M, Brunner E, Nabi H, Kivimaki M, Singh-Manoux A (2010) Association of socioeconomic position with health behaviors and mortality. JAMA 303(12):1159–1166. https://doi.org/10.1001/jama.2010.297CrossRefPubMedPubMedCentral

73.

Geronimus AT, Hicken M, Keene D, Bound J (2006) "Weathering" and age patterns of allostatic load scores among blacks and whites in the United States. Am J Public Health 96(5):826–833. https://doi.org/10.2105/AJPH.2004.060749CrossRefPubMedPubMedCentral

74.

Abbott A (2018) European scientists seek ‘epigenetic clock’ to determine age of refugees. Nature 561(7721):15. https://doi.org/10.1038/d41586-018-06121-wCrossRefPubMed

75.

Eipel M, Bozic T, Mies A, Beier F, Jost E, Brummendorf TH, Platzbecker U, Wagner W (2019) Tracking myeloid malignancies by targeted analysis of successive DNA methylation at neighboring CG dinucleotides. Haematologica 104(8):e349–e351. https://doi.org/10.3324/haematol.2018.209734CrossRefPubMedPubMedCentral

76.

Lin Q, Wagner W (2015) Epigenetic aging signatures are coherently modified in cancer. PLoS Genet 11(6):e1005334. https://doi.org/10.1371/journal.pgen.1005334CrossRefPubMedPubMedCentral

77.

Adland E, Klenerman P, Goulder P, Matthews PC (2015) Ongoing burden of disease and mortality from HIV/CMV coinfection in Africa in the antiretroviral therapy era. Front Microbiol 6:1016. https://doi.org/10.3389/fmicb.2015.01016CrossRefPubMedPubMedCentral

78.

Gao X, Jia M, Zhang Y, Breitling LP, Brenner H (2015) DNA methylation changes of whole blood cells in response to active smoking exposure in adults: a systematic review of DNA methylation studies. Clin Epigenetics 7:113. https://doi.org/10.1186/s13148-015-0148-3CrossRefPubMedPubMedCentral

79.

Sillanpaa E, Ollikainen M, Kaprio J, Wang X, Leskinen T, Kujala UM, Tormakangas T (2019) Leisure-time physical activity and DNA methylation age-a twin study. Clin Epigenetics 11(1):12. https://doi.org/10.1186/s13148-019-0613-5CrossRefPubMedPubMedCentral

80.

Han Y, Franzen J, Stiehl T, Gobs M, Chao-Chung Kuo J, Nikolić M, Hapala J, Koop B, Strathmann K, Ritz-Timme S, Wagner W (2020) New targeted approaches for epigenetic age predictions. BMC Biology (in press):https://www.biorxiv.org/content/10.1101/799031v799031.full

Title: Epigenetic clocks may come out of rhythm—implications for the estimation of chronological age in forensic casework
Authors: Barbara Elisabeth Koop
Alexandra Reckert
Julia Becker
Yang Han
Wolfgang Wagner
Stefanie Ritz-Timme
Publication date: 01-11-2020
Publisher: Springer Berlin Heidelberg
Keywords: Post-Traumatic Stress Disorder
Epigenetics
Published in: International Journal of Legal Medicine / Issue 6/2020
Print ISSN: 0937-9827
Electronic ISSN: 1437-1596
DOI: https://doi.org/10.1007/s00414-020-02375-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Epigenetic clocks may come out of rhythm—implications for the estimation of chronological age in forensic casework

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

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