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Basic Research Article

Community and domestic violence are associated with DNA methylation GrimAge acceleration and heart rate variability in adolescents

La violencia doméstica y comunitaria están asociadas con la aceleración de la metilación del ADN GrimAge y la variabilidad de la frecuencia cardíaca en adolescentes

社区和家庭暴力与青少年 DNA 甲基化 GrimAge 加速和心率变异性有关

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Article: 2202054 | Received 23 Nov 2022, Accepted 03 Apr 2023, Published online: 05 May 2023

References

  • Aghagoli, G., Conradt, E., Padbury, J. F., Sheinkopf, S. J., Tokadjian, H., Dansereau, L. M., Tronick, E. Z., Marsit, C. J., & Lester, B. M. (2020). Social stress-related epigenetic changes associated with increased heart rate variability in infants. Frontiers in Behavioral Neuroscience, 13, 1–7. https://doi.org/10.3389/fnbeh.2019.00294
  • Alcantara, J. M. A., Plaza-Florido, A., Amaro-Gahete, F. J., Acosta, F. M., Migueles, J. H., Molina-Garcia, P., Sacha, J., Sanchez-Delgado, G., & Martinez-Tellez, B. (2020). Impact of using different levels of threshold-based artefact correction on the quantification of heart rate variability in three independent human cohorts. Journal of Clinical Medicine, 9(2). https://doi.org/10.3390/jcm9020325
  • Bahari, A., Hasani, J., & Boojar, M. M. A. (2021). Childhood trauma and type D personality: The endocrine and cardiovascular effects on stress reactivity. Journal of Health Psychology, 26(14), 2861–2875. https://doi.org/10.1177/1359105320934181
  • Barber, A. D., John, M., DeRosse, P., Birnbaum, M. L., Lencz, T., & Malhotra, A. K. (2020). Parasympathetic arousal-related cortical activity is associated with attention during cognitive task performance. NeuroImage, 208, Article 116469. https://doi.org/10.1016/j.neuroimage.2019.116469
  • Barfield, R. T., Kilaru, V., Smith, A. K., & Conneely, K. N. (2012). CpGassoc: An R function for analysis of DNA methylation microarray data. Bioinformatics, 28(9), 1280–1281. https://doi.org/10.1093/bioinformatics/bts124
  • Beauchaine, T. (2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13(2), 183–214. https://doi.org/10.1017/s0954579401002012
  • Berntson, G. G., Norman, G. J., Hawkley, L. C., & Cacioppo, J. T. (2008). Cardiac autonomic balance versus cardiac regulatory capacity. Psychophysiology, 45(4), 643–652. https://doi.org/10.1111/j.1469-8986.2008.00652.x
  • Catai, A. M., Pastre, C. M., de Godoy, M. F., da Silva, E., de Takahashi, A. C. M., & Vanderlei, L. C. M. (2020). Heart rate variability: Are you using it properly? Standardisation checklist of procedures. Brazilian Journal of Physical Therapy, 24(2), 91–102. https://doi.org/10.1016/j.bjpt.2019.02.006
  • Chen, Y., Lemire, M., Choufani, S., Butcher, D. T., Grafodatskaya, D., Zanke, B. W., Gallinger, S., Hudson, T. J., & Weksberg, R. (2013). Discovery of cross-reactive probes and polymorphic CpGs in the illumina infinium HumanMethylation450 microarray. Epigenetics, 8(2), 203–209. https://doi.org/10.4161/epi.23470
  • Chou, C. Y., La Marca, R., Steptoe, A., & Brewin, C. R. (2018). Cardiovascular and psychological responses to voluntary recall of trauma in posttraumatic stress disorder. European Journal of Psychotraumatology, 9(1), 1–13. https://doi.org/10.1080/20008198.2018.1472988
  • D’Addario, C., Dell’Osso, B., Palazzo, M. C., Benatti, B., Lietti, L., Cattaneo, E., Galimberti, D., Fenoglio, C., Cortini, F., Scarpini, E., Arosio, B., Di Francesco, A., Di Benedetto, M., Romualdi, P., Candeletti, S., Mari, D., Bergamaschini, L., Bresolin, N., Maccarrone, M., & Altamura, A. C. (2012). Selective DNA methylation of BDNF promoter in bipolar disorder: Differences among patients with BDI and BDII. Neuropsychopharmacology, 37(7), 1647–1655. https://doi.org/10.1038/npp.2012.10
  • Denson, T. F., Grisham, J. R., & Moulds, M. L. (2011). Cognitive reappraisal increases heart rate variability in response to an anger provocation. Motivation and Emotion, 35(1), 14–22. https://doi.org/10.1007/s11031-011-9201-5
  • Etzel, L., Hastings, W. J., Hall, M. A., Heim, C. M., Meaney, M. J., Noll, J. G., O'Donnell, K., Pokhvisneva, I., Rose, E. J., Schreier, H. M. C., Shenk, C.E., & Shalev, I. (2022). Obesity and accelerated epigenetic aging in a high-risk cohort of children. Scientific Reports, 12(1), 8328. https://doi.org/10.1038/s41598-022-11562-5
  • Giurgescu, C., Nowak, A. L., Gillespie, S., Nolan, T. S., Anderson, C. M., Ford, J. L., Hood, D. B., & Williams, K. P. (2019). Neighborhood environment and DNA methylation: Implications for cardiovascular disease risk. Journal of Urban Health, 96(1, SI), 23–34. https://doi.org/10.1007/s11524-018-00341-1
  • Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S., Klotzle, B., Bibikova, M., Fan, J.-B., 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. Molecular Cell, 49(2), 359–367. https://doi.org/10.1016/j.molcel.2012.10.016
  • Held, J., Vîslă, A., Wolfer, C., Messerli-Bürgy, N., & Flückiger, C. (2021). Heart rate variability change during a stressful cognitive task in individuals with anxiety and control participants. BMC Psychology, 9(1), 44. https://doi.org/10.1186/s40359-021-00551-4
  • Hill, L. K., & Siebenbrock, A. (2009). Are all measures created equal? Heart rate variability and respiration – biomed 2009. Biomedical Sciences Instrumentation, 45, 71–76.
  • Hoare, J., Stein, D. J., Heany, S. J., Fouche, J. P., Phillips, N., Er, S., Myer, L., Zar, H. J., Horvath, S., & Levine, A. J. (2020). Accelerated epigenetic aging in adolescents from low-income households is associated with altered development of brain structures. Metab Brain Dis, 35(8), 1287–1298. https://doi.org/10.1007/s11011-020-00589-0
  • Horvath, S. (2013). DNA methylation age of human tissues and cell types. Genome Biology, 14(10), R115. https://doi.org/10.1186/gb-2013-14-10-r115
  • Jovanovic, T., Vance, L. A., Cross, D., Knight, A. K., Kilaru, V., Michopoulos, V., Klengel, T., & Smith, A. K. (2017). Exposure to violence accelerates epigenetic aging in children. Scientific Reports, 7(1). https://doi.org/10.1038/s41598-017-09235-9
  • Joyce, B. T., Gao, T., Zheng, Y., Ma, J., Hwang, S. J., Liu, L., Nannini, D., Horvath, S., Lu, A. T., Bai Allen, N., Jacobs, D. R., Gross, M., Krefman, A., Ning, H., Liu, K., Lewis, C. E., Schreiner, P. J., Sidney, S., Shikany, J. M., … Lloyd-Jones, D. (2021). Epigenetic age acceleration reflects long-term cardiovascular health. Circulation Research, 770–781. https://doi.org/10.1161/CIRCRESAHA.121.318965
  • Katrinli, S., Stevens, J., Wani, A. H., Lori, A., Kilaru, V., van Rooij, S. J. H., Hinrichs, R., Powers, A., Gillespie, C. F., Michopoulos, V., Gautam, A., Jett, M., Hammamieh, R., Yang, R., Wildman, D., Qu, A., Koenen, K., Aiello, A. E., Jovanovic, T., … Smith, A. K. (2020). Evaluating the impact of trauma and PTSD on epigenetic prediction of lifespan and neural integrity. Neuropsychopharmacology, 45(10), 1609–1616. https://doi.org/10.1038/s41386-020-0700-5
  • Keary, T. A., Hughes, J. W., & Palmieri, P. A. (2009). Women with posttraumatic stress disorder have larger decreases in heart rate variability during stress tasks. International Journal of Psychophysiology, 73(3), 257–264. https://doi.org/10.1016/j.ijpsycho.2009.04.003
  • Kim, H. G., Cheon, E. J., Bai, D. S., Lee, Y. H., & Koo, B. H. (2018). Stress and heart rate variability: A meta-analysis and review of the literature. Psychiatry Investigation, 15(3), 235–245. https://doi.org/10.30773/pi.2017.08.17
  • Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of cognitive neuroscience, 16(8), 1412–1425.
  • Koenig, J., & Thayer, J. F. (2016). Sex differences in healthy human heart rate variability: A meta-analysis. Neuroscience & Biobehavioral Reviews, 64, 288–310. https://doi.org/10.1016/j.neubiorev.2016.03.007
  • Laborde, S., Mosley, E., & Mertgen, A. (2018). Vagal tank theory: The three Rs of cardiac vagal control functioning – resting, reactivity, and recovery. Frontiers in Neuroscience, 12, 1–14. https://doi.org/10.3389/fnins.2018.00458
  • Lancaster, K., Goldbeck, L., Puglia, M. H., Morris, J. P., & Connelly, J. J. (2018). DNA methylation of OXTR is associated with parasympathetic nervous system activity and amygdala morphology. Social Cognitive and Affective Neuroscience, 13(11), 1155–1162. https://doi.org/10.1093/scan/nsy086
  • Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical Report A-8. https://doi.org/10.1016/j.epsr.2006.03.016
  • Leek, J. T., Johnson, W. E., Parker, H. S., Jaffe, A. E., & Storey, J. D. (2012). The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics, 28(6), 882–883. https://doi.org/10.1093/bioinformatics/bts034
  • Lima, C. N. C., Suchting, R., Scaini, G., Cuellar, V. A., Del Favero-Campbell, A., Walss-Bass, C., Soares, J. C., Quevedo, J., & Fries, G. R. (2022). Epigenetic GrimAge acceleration and cognitive impairment in bipolar disorder. European Neuropsychopharmacology, 62, 10–21. https://doi.org/10.1016/j.euroneuro.2022.06.007
  • Lu, A. T., Quach, A., Wilson, J. G., Reiner, A. P., Aviv, A., Raj, K., Hou, L., Baccarelli, A. A., Li, Y., Stewart, J. D., Whitsel, E. A., Assimes, T. L., Ferrucci, L., & Horvath, S. (2019). DNA methylation GrimAge strongly predicts lifespan and healthspan. Aging, 11(2), 303–327. https://doi.org/10.18632/aging.101684
  • Marini, S., Davis, K. A., Soare, T. W., Zhu, Y., Suderman, M. J., Simpkin, A. J., Smith, A. D. A. C., Wolf, E. J., Relton, C. L., & Dunn, E. C. (2020). Adversity exposure during sensitive periods predicts accelerated epigenetic aging in children. Psychoneuroendocrinology, 113, Article 104484. https://doi.org/10.1016/j.psyneuen.2019.104484
  • Marioni, R. E., Shah, S., McRae, A. F., Chen, B. H., Colicino, E., Harris, S. E., Gibson, J., Henders, A. K., Redmond, P., Cox, S. R., Pattie, A., Corley, J., Murphy, L., Martin, N. G., Montgomery, G. W., Feinberg, A. P., Fallin, M. D., Multhaup, M. L., Jaffe, A. E., … Deary, I. J. (2015). DNA methylation age of blood predicts all-cause mortality in later life. Genome Biology, 16(1), 1–12. https://doi.org/10.1186/s13059-015-0584-6
  • McCrory, C., Fiorito, G., Hernandez, B., Polidoro, S., O’Halloran, A. M., Hever, A., Ni Cheallaigh, C., Lu, A. T., Horvath, S., Vineis, P., & Kenny, R. A. (2021). Grimage outperforms other epigenetic clocks in the prediction of age-related clinical phenotypes and all-cause mortality. The Journals of Gerontology: Series A, 76(5), 741–749. https://doi.org/10.1093/gerona/glaa286
  • Mehta, D., Bruenig, D., Pierce, J., Sathyanarayanan, A., Stringfellow, R., Miller, O., Mullens, A. B., & Shakespeare-Finch, J. (2021). Recalibrating the epigenetic clock after exposure to trauma: The role of risk and protective psychosocial factors. Journal of Psychiatric Research. https://doi.org/10.1016/j.jpsychires.2021.11.026
  • Melo, H. M., Martins, T. C., Nascimento, L. M., Hoeller, A. A., Walz, R., & Takase, E. (2018). Ultra-short heart rate variability recording reliability: The effect of controlled paced breathing. Annals of Noninvasive Electrocardiology, 23(5), 1–9. https://doi.org/10.1111/anec.12565
  • Messerli-Bürgy, N., Meyer, A. H., Kakebeeke, T. H., Stülb, K., Arhab, A., Zysset, A. E., Leeger-Aschmann, C. S., Schmutz, E. A., Thayer, J. F., Groene, M., Kriemler, S., Jenni, O. G., Puder, J. J., & Munsch, S. (2020). Cardiac vagal tone in preschool children: Interrelations and the role of stress exposure. International Journal of Psychophysiology, 152, 102–109. https://doi.org/10.1016/j.ijpsycho.2020.04.006
  • Mestanikova, A., Mestanik, M., Ondrejka, I., Hrtanek, I., Cesnekova, D., Jurko, A., Visnovcova, Z., Sekaninova, N., & Tonhajzerova, I. (2019). Complex cardiac vagal regulation to mental and physiological stress in adolescent major depression. Journal of Affective Disorders, 249, 234–241. https://doi.org/10.1016/j.jad.2019.01.043
  • Murali, R., & Chen, E. (2005). Exposure to violence and cardiovascular and neuroendocrine measures in adolescents. Annals of Behavioral Medicine, 30(2), 155–163. https://doi.org/10.1207/s15324796abm3002_8
  • Nwanaji-Enwerem, J. C., Laan, L. V. D., Avakame, E. F., Scott, K. A., Burris, H. H., & Cardenas, A. (2021). Associations of DNA methylation mortality risk markers with congenital microcephaly from zika virus: A study of brazilian children less than 4 years of age. Journal of Tropical Pediatrics, 67(1). https://doi.org/10.1093/tropej/fmab020
  • Oblak, L., van der Zaag, J., Higgins-Chen, A. T., Levine, M. E., & Boks, M. P. (2021). A systematic review of biological, social and environmental factors associated with epigenetic clock acceleration. Ageing Research Reviews, 69, Article 101348. https://doi.org/10.1016/j.arr.2021.101348
  • Okazaki, S., Otsuka, I., Shinko, Y., Horai, T., Hirata, T., Yamaki, N., Sora, I., & Hishimoto, A. (2021). Epigenetic clock analysis in children with fetal alcohol spectrum disorder. Alcohol: Clinical and Experimental Research, 45(2), 329–337. https://doi.org/10.1111/acer.14532
  • Oliveira, N. C. S., Serpeloni, F., & Assis, S. G. (2021). The interplay between DNA methylation and cardiac autonomic system functioning: A systematic review. International Journal of Environmental Health Research, 33(1), 54–70. https://doi.org/10.1080/09603123.2021.2000590
  • Penttilä, J., Helminen, A., Jartti, T., Kuusela, T., Huikuri, H. V., Tulppo, M. P., Coffeng, R., & Scheinin, H. (2001). Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: Effects of various respiratory patterns. Clinical Physiology, 21(3), 365–376. https://doi.org/10.1046/j.1365-2281.2001.00337.x
  • Pinto, L. W., & Gonçalves de Assis, S. (2013). Family and community violence of schoolchildren from the city of São Gonçalo, Rio de Janeiro, Brazil. Revista Brasileira de Epidemiologia = Brazilian Journal of Epidemiology, 16(2), 288–300. https://doi.org/10.1590/S1415-790X2013000200006
  • Pius-Sadowska, E., & Machaliński, B. (2017). BDNF – a key player in cardiovascular system. Journal of Molecular and Cellular Cardiology, 110, 54–60. https://doi.org/10.1016/j.yjmcc.2017.07.007
  • Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74(2), 116–143. https://doi.org/10.1016/j.biopsycho.2006.06.009
  • Protsenko, E., Yang, R., Nier, B., Reus, V., Hammamieh, R., Rampersaud, R., Wu, G. W. Y., Hough, C. M., Epel, E., Prather, A. A., Jett, M., Gautam, A., Mellon, S. H., & Wolkowitz, O. M. (2021). “Grimage,” an epigenetic predictor of mortality, is accelerated in major depressive disorder. Translational Psychiatry, 11(1), 193. https://doi.org/10.1038/s41398-021-01302-0
  • Rampersaud, R., Protsenko, E., Yang, R., Reus, V., Hammamieh, R., Wu, G. W. Y., Epel, E., Jett, M., Gautam, A., Mellon, S. H., & Wolkowitz, O. M. (2022). Dimensions of childhood adversity differentially affect biological aging in major depression. Translational Psychiatry, 12(1), 431. https://doi.org/10.1038/s41398-022-02198-0
  • Richters, J. E., & Martinez, P. (1990). Things I have seen and heard: A structured interview for assessing young children’s violence exposure.
  • Ross, K. M., Carroll, J. E., Horvath, S., Hobel, C. J., Coussons-Read, M. E., & Dunkel Schetter, C. (2020). Epigenetic age and pregnancy outcomes: GrimAge acceleration is associated with shorter gestational length and lower birthweight. Clinical Epigenetics, 12(1), 120. https://doi.org/10.1186/s13148-020-00909-2
  • Schauer, M., & Elbert, T. (2010). Dissociation following traumatic stress: Etiology and treatment. Zeitschrift für Psychologie/Journal of Psychology, 218(2), 109–127. https://doi.org/10.1027/0044-3409/a000018
  • Schauer, M., Neuner, F., & Elbert, T. (2011). Narrative exposure therapy: A short-term treatment for traumatic stress disorders. Hogrefe Publishing.
  • Seddon, J. A., Rodriguez, V. J., Provencher, Y., Raftery-Helmer, J., Hersh, J., Labelle, P. R., & Thomassin, K. (2020). Meta-analysis of the effectiveness of the Trier Social Stress Test in eliciting physiological stress responses in children and adolescents. Psychoneuroendocrinology, 116, 104582. https://doi.org/10.1016/j.psyneuen.2020.104582
  • Serpeloni, F., Natt, D., de Assis, S. G., Wieling, E., & Elbert, T. (2020). Experiencing community and domestic violence is associated with epigenetic changes in DNA methylation of BDNF and CLPX in adolescents. Psychophysiology, 57(1), e13382. https://doi.org/10.1111/psyp.13382
  • Serpeloni, F., Radtke, K., de Assis, S., Henning, F., Natt, D., & Elbert, T. (2017). Grandmaternal stress during pregnancy and DNA methylation of the third generation: An epigenome-wide association study. Translational Psychiatry, 7(8), e1202. https://doi.org/10.1038/tp.2017.153
  • Shaffer, F., & Ginsberg, J. P. (2017). An overview of heart rate variability metrics and norms. Frontiers in Public Health, 5. https://doi.org/10.3389/fpubh.2017.00258
  • Shaffer, F., McCraty, R., & Zerr, C. L. (2014). A healthy heart is not a metronome: An integrative review of the heart’s anatomy and heart rate variability. Frontiers in Psychology, 5, 1040. https://doi.org/10.3389/fpsyg.2014.01040
  • Steinberg, A. M., Brymer, M. J., Decker, K. B., & Pynoos, R. S. (2004). The University of California at Los Angeles post-traumatic stress disorder reaction index. Current Psychiatry Reports, 6(2), 96–100. https://doi.org/10.1007/s11920-004-0048-2
  • Suglia, S. F., Sapra, K. J., & Koenen, K. C. (2015). Violence and cardiovascular health: A systematic review. American Journal of Preventive Medicine, 48(2), 205–212. https://doi.org/10.1016/j.amepre.2014.09.013
  • Sumner, J. A., Colich, N. L., Uddin, M., Armstrong, D., & McLaughlin, K. A. (2019). Early experiences of threat, but not deprivation, are associated with accelerated biological aging in children and adolescents. Biol Psychiatry, 85(3), 268–278. https://doi.org/10.1016/j.biopsych.2018.09.00
  • Tang, R., Howe, L. D., Suderman, M., Relton, C. L., Crawford, A. A., & Houtepen, L. C. (2020). Adverse childhood experiences, DNA methylation age acceleration, and cortisol in UK children: a prospective population-based cohort study. Clinical Epigenetics, 12(1), 55. https://doi.org/10.1186/s13148-020-00844-2
  • Tarvainen, M. P., Niskanen, J. P., Lipponen, J. A., Ranta-aho, P. O., & Karjalainen, P. A. (2014). Kubios HRV – heart rate variability analysis software. Computer Methods and Programs in Biomedicine, 113(1), 210–220. https://doi.org/10.1016/j.cmpb.2013.07.024
  • Thayer, J. F., Yamamoto, S. S., & Brosschot, J. F. (2010). The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. International Journal of Cardiology, 141(2), 122–131. https://doi.org/10.1016/j.ijcard.2009.09.543
  • Thomas, B. L., Claassen, N., Becker, P., & Viljoen, M. (2019). Validity of commonly used heart rate variability markers of autonomic nervous system function. Neuropsychobiology, 78(1), 14–26. https://doi.org/10.1159/000495519
  • Triche, T. J., Weisenberger, D. J., van den Berg, D., Laird, P. W., & Siegmund, K. D. (2013). Low-level processing of illumina infinium DNA methylation BeadArrays. Nucleic Acids Research, 41(7), e90. https://doi.org/10.1093/nar/gkt090
  • Tyra, A. T., Cook, T. E., Young, D. A., Hurley, P. E., Oosterhoff, B. J., John-Henderson, N. A., & Ginty, A. T. (2021). Adverse childhood experiences, sex, and cardiovascular habituation to repeated stress. Biological Psychology, 165, Article 108175. https://doi.org/10.1016/j.biopsycho.2021.108175
  • Zannas, A. S., Jia, M., Hafner, K., Baumert, J., Wiechmann, T., Pape, J. C., Arloth, J., Ködel, M., Martinelli, S., Roitman, M., Röh, S., Haehle, A., Emeny, R. T., Iurato, S., Carrillo-Roa, T., Lahti, J., Räikkönen, K., Eriksson, J. G., Drake, A. J., … Binder, E. B. (2019). Epigenetic upregulation of FKBP5 by aging and stress contributes to NF-κB-driven inflammation and cardiovascular risk. Proceedings of the National Academy of Sciences of the United States of America, 116(23), 11370–11379. https://doi.org/10.1073/pnas.1816847116
  • Zheng, S. C., Webster, A. P., Dong, D., Feber, A., Graham, D. G., Sullivan, R., Jevons, S., Lovat, L. B., Beck, S., Widschwendter, M., & Teschendorff, A. E. (2018). A novel cell-type deconvolution algorithm reveals substantial contamination by immune cells in saliva, buccal and cervix. Epigenomics, 10(7), 925–940. https://doi.org/10.2217/epi-2018-0037