Leukocyte Methylomic Imprints of Exposure to the Genocide against the Tutsi in Rwanda: a Pilot Epigenome-Wide Analysis
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Aim & methods: We conducted a pilot epigenome-wide association study of women from Tutsi ethnicity exposed to the genocide while pregnant and their resulting offspring, and a comparison group of women who were pregnant at the time of the genocide but living outside of Rwanda.Results: Fifty-nine leukocyte-derived DNA samples survived quality control: 33 mothers (20 exposed, 13 unexposed) and 26 offspring (16 exposed, 10 unexposed). Twenty-four significant differentially methylated regions (DMRs) were identified in mothers and 16 in children. Conclusions: In utero genocide exposure was associated with CpGs in three of the 24 DMRs: BCOR, PRDM8 and VWDE, with higher DNA methylation in exposed versus unexposed offspring. Of note, BCOR and VWDE show significant correlation between brain and blood DNA methylation within individuals, suggesting these peripherally derived signals of genocide exposure may have relevance to the brain.
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There were six studies of trauma or PTSD following war, including two studies of Holocaust survivors, two on the Rwandan genocide, one from the Kosovo War, and one of Vietnam veterans.
“There were six studies of trauma or PTSD following war, including two studies of Holocaust survivors [83,94,95], two studies on the Rwandan genocide [90,91], and one each from the Kosovo War [96] and Vietnam veterans [97].”
The 22 publications come from 19 independent studies.
“These publications come from 19 independent studies, as in some cases the same study has been used to investigate different genes [87,88,89,90,91].”
Exposures occurring in utero or during early childhood, periods characterized by heightened biological plasticity, have been associated with more pronounced neurocognitive and psychological effects.
“Developmental timing appears to play an important role in shaping outcomes, as exposures occurring in utero or during early childhood, periods characterized by heightened biological plasticity, have been associated with more pronounced neurocognitive and psychological effects (7, 10, 11).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Trauma-related variation has been described in pathways relevant to neurodevelopment, immune-inflammatory signaling, circadian regulation, metabolism, and memory formation.
“Trauma-related variation has also been described in pathways relevant to neurodevelopment, immune-inflammatory signaling, circadian regulation, metabolism, and memory formation (7–9).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Across survivor populations and their descendants, research suggests coordinated involvement of stress-response regulation, neurodevelopmental signaling, and behavioral adaptation.
“Across survivor populations and their descendants, research suggests coordinated involvement of stress-response regulation, neurodevelopmental signaling, and behavioral adaptation (7, 82–100).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Evidence from multiple trauma contexts points to involvement of interacting regulatory systems, including stress-response signaling, neurodevelopmental processes, circadian and metabolic regulation, and epigenetic remodeling.
“Evidence from multiple trauma contexts points to involvement of interacting regulatory systems, including stress-response signaling, neurodevelopmental processes, circadian and metabolic regulation, and epigenetic remodeling (7, 82–124).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Across diverse forms of complex trauma, sustained exposure to interpersonal and collective adversity has been associated with cumulative biological and psychological adaptation that may extend across generations.
“Across diverse forms of complex trauma, sustained exposure to interpersonal and collective adversity has been associated with cumulative biological and psychological adaptation that may extend across generations.”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Genome-scale analyses have identified methylation changes in genes involved in embryonic and neural development, including BCOR, PRDM8, and VWDE, in offspring with in utero exposure to the Tutsi genocide.
“Genome-scale analyses have further identified methylation changes in genes involved in embryonic and neural development, including BCOR, PRDM8, and VWDE, in offspring with in utero exposure to the Tutsi genocide (7).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [7]
Cites
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
Greedy function approximation: A gradient boosting machine
Friedman, J. H. (2001) · The Annals of Statistics · doi:10.1214/aos/1013203451 · Cited by 30,731 · see citing works
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658 · see citing works
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U. E., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 8,501 · see citing works
DNA methylation age of human tissues and cell types
Horvath, S. (2013) · Genome Biology · doi:10.1186/gb-2013-14-10-r115 · Cited by 7,075 · see citing works
Leek, J. T., Johnson, W. E., Parker, H. S., Jaffe, A. E., & Storey, J. D. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts034 · Cited by 6,231 · see citing works
Aryee, M. J., Jaffe, A. E., Bravo, H. C., Ladd‐Acosta, C., Feinberg, A. P., Hansen, K. D., & Irizarry, R. A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu049 · Cited by 4,423 · see citing works
Fast gene set enrichment analysisPreprint
Korotkevich, G., Sukhov, V., Budin, N., Shpak, B., Artyomov, M. N., & Sergushichev, A. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/060012 · Cited by 3,742 · see citing works
eQTLGen, Wray, N. R., 23andMe, the Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium, Ripke, S., Mattheisen, M., Trzaskowski, M., Byrne, E. M., Abdellaoui, A., Adams, M. J., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0090-3 · Cited by 3,005 · see citing works
Meinshausen, N., & Bühlmann, P. (2010) · Journal of the Royal Statistical Society Series B (Statistical Methodology) · doi:10.1111/j.1467-9868.2010.00740.x · Cited by 2,314 · see citing works
Effects of perinatal mental disorders on the fetus and child
Stein, A., Pearson, R. M., Goodman, S. H., Rapa, E., Rahman, A., McCallum, M., Howard, L. M., & Pariante, C. M. (2014) · The Lancet · doi:10.1016/s0140-6736(14)61277-0 · Cited by 2,166 · see citing works
DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis
Joubert, B. R., Felix, J. F., Yousefi, P., Bakulski, K. M., Just, A. C., Breton, C., Reese, S. E., Markunas, C. A., Richmond, R. C., Xu, C.-J., et al. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.02.019 · Cited by 886 · see citing works
Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation
Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N., Klengel, T., Holsboer, F., & Binder, E. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.005 · Cited by 782 · see citing works
Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms
Yehuda, R., & Lehrner, A. (2018) · World Psychiatry · doi:10.1002/wps.20568 · Cited by 730 · see citing works
Intergenerational Transmission of Stress in Humans
Bowers, M. E., & Yehuda, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.247 · Cited by 564 · see citing works
Teschendorff, A. E., Breeze, C. E., Zheng, S., & Beck, S. (2017) · BMC Bioinformatics · doi:10.1186/s12859-017-1511-5 · Cited by 548 · see citing works
Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513 · see citing works
Mapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex
Jaffe, A. E., Gao, Y., Deep-Soboslay, A., Tao, R., Hyde, T. M., Weinberger, D. R., & Kleinman, J. E. (2016) · Nature Neuroscience · doi:10.1038/nn.4181 · Cited by 511 · see citing works
Braun, P. R., Han, S., Hing, B., Nagahama, Y., Gaul, L. N., Heinzman, J. T., Grossbach, A. J., Close, L., Dlouhy, B. J., Howard, M. A., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0376-y · Cited by 467 · see citing works
Kubzansky, L. D., Koenen, K. C., Spiro, A., Vokonas, P., & Sparrow, D. (2007) · Archives of General Psychiatry · doi:10.1001/archpsyc.64.1.109 · Cited by 425 · see citing works
Dysregulation of the fibroblast growth factor system in major depression
Evans, S. J., Choudary, P. V., Neal, C. R., Li, J. Z., Vawter, M. P., Tomita, H., Lopez, J. F., Thompson, R. C., Meng, F., Stead, J. D., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406788101 · Cited by 424 · see citing works
Salas, L. A., Koestler, D. C., Butler, R. A., Hansen, H. M., Wiencke, J. K., Kelsey, K. T., & Christensen, B. C. (2018) · Genome biology · doi:10.1186/s13059-018-1448-7 · Cited by 418 · see citing works
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012) · Epigenetics · doi:10.4161/epi.21180 · Cited by 342 · see citing works
Perroud, N., Rutembesa, E., Paoloni-Giacobino, A., Mutabaruka, J., Mutesa, L., Stenz, L., Malafosse, A., & Karege, F. (2014) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2013.866693 · Cited by 336 · see citing works
Self-citationGroßmann, V., Tiacci, E., Holmes, A. B., Kohlmann, A., Martelli, M. P., Kern, W., Rosseto, A. S., Klein, H., Dugas, M., Schindela, S., et al. (2011) · Blood · doi:10.1182/blood-2011-07-365320 · Cited by 265 · see citing works
Prenatal stress and epigenetics
Cao-Lei, L., de Rooij, S. R., King, S., Matthews, S. G., Metz, G. A. S., Roseboom, T. J., & Moshe Szyf, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.016 · Cited by 230 · see citing works
Kertes, D. A., Kamin, H. S., Hughes, D. A., Rodney, N. C., Bhatt, S., & Mulligan, C. J. (2016) · Child Development · doi:10.1111/cdev.12487 · Cited by 219 · see citing works
A prospective study of posttraumatic stress disorder symptoms and coronary heart disease in women.
Kubzansky, L. D., Koenen, K. C., Jones, C. C., & Eaton, W. W. (2009) · Health Psychology · doi:10.1037/0278-6133.28.1.125 · Cited by 203 · see citing works
Epigenetic dysregulation of HTR2A in the brain of patients with schizophrenia and bipolar disorder
Abdolmaleky, H. M., Yaqubi, S., Papageorgis, P., Lambert, A. W., Ozturk, S., Sivaraman, V., & Thiagalingam, S. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.04.007 · Cited by 192 · see citing works
Vukojevic, V., Kolassa, I.-T., Fastenrath, M., Gschwind, L., Spalek, K., Milnik, A., Heck, A., Vogler, C., Wilker, S., Demougin, P., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1526-14.2014 · Cited by 168 · see citing works
Self-citationMental and physical health in Rwanda 14 years after the genocide
Munyandamutsa, N., Mahoro Nkubamugisha, P., Gex-Fabry, M., & Eytan, A. (2012) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s00127-012-0494-9 · Cited by 149 · see citing works
Rutten, B. P. F., Vermetten, E., Vinkers, C. H., Ursini, G., Daskalakis, N. P., Pishva, E., de Nijs, L., Houtepen, L. C., Eijssen, L., Jaffe, A. E., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.120 · Cited by 142 · see citing works
Transgenerational epigenetics of traumatic stress
Jawaid, A., Roszkowski, M., & Mansuy, I. M. (2018) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2018.03.003 · Cited by 134 · see citing works
Genome-Wide DNA Methylation Scan in Major Depressive Disorder
Sabunciyan, S., Aryee, M. J., Irizarry, R. A., Rongione, M. A., Webster, M. J., Kaufmann, W. E., Murakami, P. N., Lessard, A., Yolken, R. H., Feinberg, A. P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034451 · Cited by 132 · see citing works
Rieder, H., & Elbert, T. (2013) · Conflict and Health · doi:10.1186/1752-1505-7-6 · Cited by 112 · see citing works
Maternal prenatal stress and infant DNA methylation: A systematic review
Sosnowski, D. W., Booth, C., York, T. P., Amstadter, A. B., & Kliewer, W. (2018) · Developmental Psychobiology · doi:10.1002/dev.21604 · Cited by 111 · see citing works
Hilton, E. N., Johnston, J. J., Whalen, S., Okamoto, N., Hatsukawa, Y., NISHIO, J., Kohara, H., Hirano, Y., Mizuno, S., Torii, C., et al. (2009) · European Journal of Human Genetics · doi:10.1038/ejhg.2009.52 · Cited by 108 · see citing works
Wamstad, J. A., Corcoran, C. M., Keating, A. M., & Bardwell, V. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002814 · Cited by 104 · see citing works
the Traumatic Stress Brain Study Group, Logue, M. W., Miller, M. W., Wolf, E. J., Huber, B. R., Morrison, F. G., Zhou, Z., Zheng, Y., Smith, A. K., Daskalakis, N. P., et al. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-0820-0 · Cited by 102 · see citing works
Self-citationAntidepressants during pregnancy and autism in offspring: population based cohort study
Rai, D., Lee, B. K., Dalman, C., Newschaffer, C., Lewis, G., & Magnusson, C. (2017) · BMJ · doi:10.1136/bmj.j2811 · Cited by 93 · see citing works
Intergenerational Effects of Maternal Holocaust Exposure on <i>FKBP5</i> Methylation
Bierer, L. M., Bader, H. N., Daskalakis, N. P., Lehrner, A., Provençal, N., Wiechmann, T., Klengel, T., Makotkine, I., Binder, E. B., & Yehuda, R. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19060618 · Cited by 86 · see citing works
Fibroblast Growth Factors in Schizophrenia
van Scheltinga, A. F. T., Bakker, S. C., & Kahn, R. S. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp033 · Cited by 77 · see citing works
Serpeloni, F., Radtke, K. M., Hecker, T., Sill, J., Vukojevic, V., Assis, S. G. D., Schauer, M., Elbert, T., & Nätt, D. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00269 · Cited by 77 · see citing works
Husarewycz, M. N., El-Gabalawy, R., Logsetty, S., & Sareen, J. (2014) · General Hospital Psychiatry · doi:10.1016/j.genhosppsych.2013.06.003 · Cited by 76 · see citing works
Fibroblast Growth Factors in Depression
Deng, Z. H., Deng, S., Zhang, M.-R., & Tang, M. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00060 · Cited by 68 · see citing works
c060 : Extended Inference with Lasso and Elastic-Net Regularized Cox and Generalized Linear Models
Sill, M., Hielscher, T., Becker, N., & Zucknick, M. (2014) · Journal of Statistical Software · doi:10.18637/jss.v062.i05 · Cited by 66 · see citing works
Keyes, K. M., McLaughlin, K. A., Demmer, R. T., Cerdá, M., Koenen, K. C., Uddin, M., & Galea, S. (2013) · Depression and Anxiety · doi:10.1002/da.22090 · Cited by 60 · see citing works
Self-citationmCSEA: detecting subtle differentially methylated regions
Martorell‐Marugán, J., González‐Rumayor, V., & Carmona‐Sáez, P. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz096 · Cited by 59 · see citing works
Viuff, A. F., Sharp, G. C., Rai, D., Henriksen, T. B., Pedersen, L. H., Kyng, K. J., Staunstrup, N. H., Hidalgo, A. P. C., Neumann, A., Felix, J. F., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0286-4 · Cited by 56 · see citing works
Cediel-Ulloa, A., Gliga, A. R., Love, T., Pineda, D., Mruzek, D. W., Watson, G. E., Davidson, P. W., Shamlaye, C. F., Strain, J., MYERS, G. J., et al. (2020) · Environment International · doi:10.1016/j.envint.2020.106321 · Cited by 46 · see citing works
Conrad, D., Wilker, S., Schneider, A., Karabatsiakis, A., Pfeiffer, A., Kolassa, S., Freytag, V., Vukojević, V., Vogler, C., Milnik, A., et al. (2018) · Psychophysiology · doi:10.1111/psyp.13288 · Cited by 45 · see citing works
Schaal, S., Dusingizemungu, J., Jacob, N., & Elbert, T. R. (2011) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v2i0.6343 · Cited by 41 · see citing works
Expression of the mouse PR domain protein Prdm8 in the developing central nervous system
Komai, T., Iwanari, H., Mochizuki, Y., Hamakubo, T., & Shinkai, Y. (2009) · Gene Expression Patterns · doi:10.1016/j.gep.2009.07.005 · Cited by 37 · see citing works
Wani, A. H., Aiello, A. E., Kim, G. S., Xue, F., Martin, C. L., Ratanatharathorn, A. D., Qu, A., Koenen, K. C., Galea, S., Wildman, D. E., et al. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.12.076 · Cited by 37 · see citing works
Self-citationDNA methylation from germline cells in veterans with PTSD
Mehta, D., Pelzer, E. S., Bruenig, D., Lawford, B., McLeay, S., Morris, C. P., Gibson, J. N., Young, R. M., Voisey, J., McLeay, S., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.06.001 · Cited by 37 · see citing works
Cook, T. L., Shannon, P. J., Vinson, G. A., Letts, J., & Dwee, E. (2015) · BMC International Health and Human Rights · doi:10.1186/s12914-015-0046-y · Cited by 36 · see citing works
Epigenetic modifiers DNMT3A and BCOR are recurrently mutated in CYLD cutaneous syndrome
Davies, H. R., Hodgson, K., Schwalbe, E. C., Coxhead, J. M., Sinclair, N., Zou, X., Cockell, S., Husain, A., Nik‐Zainal, S., & Rajan, N. (2019) · Nature Communications · doi:10.1038/s41467-019-12746-w · Cited by 35 · see citing works
Mutuyimana, C., Sezibera, V., Nsabimana, E., Mugabo, L., Cassady, C., Musanabaganwa, C., & Kayiteshonga, Y. (2019) · BMC Psychology · doi:10.1186/s40359-019-0362-4 · Cited by 33 · see citing works
Self-citationWalker, R. M., Christoforou, A., McCartney, D. L., Morris, S. W., Kennedy, N. A., Morten, P., Anderson, S. M., Torrance, H. S., Macdonald, A., Sussmann, J. E., et al. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0171-z · Cited by 30 · see citing works
Prenatal lead exposure and cord blood DNA methylation in the Korean Exposome Study
Park, J., Kim, J., Kim, E., Kim, W. J., & Won, S. (2021) · Environmental Research · doi:10.1016/j.envres.2021.110767 · Cited by 30 · see citing works
Impact of environmental conditions and chemicals on the neuronal epigenome
del Blanco, B., & Barco, Á. (2018) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2018.06.003 · Cited by 29 · see citing works
Lowe, S. R., Joshi, S., Galea, S., Aiello, A. E., Uddin, M., Koenen, K. C., & Cerdá, M. (2017) · Psychological Medicine · doi:10.1017/s0033291717001143 · Cited by 27 · see citing works
Self-citationGenetic variant in CACNA1C is associated with PTSD in traumatized police officers
Krzyzewska, I., Ensink, J., Nawijn, L., Mul, A., Koch, S., Venema, A., Shankar, V., Frijling, J., Veltman, D., Lindauer, R., et al. (2018) · European Journal of Human Genetics · doi:10.1038/s41431-017-0059-1 · Cited by 25 · see citing works
Human active X-specific DNA methylation events showing stability across time and tissues
Joo, J. E., Novakovic, B., Cruickshank, M. N., Doyle, L. W., Craig, J. M., & Saffery, R. (2014) · European Journal of Human Genetics · doi:10.1038/ejhg.2014.34 · Cited by 23 · see citing works
Regularized Multiple Regression Methods to Deal with Severe Multicollinearity
Herawati, N., Nisa, K., Setiawan, E., Nusyirwan, N., & Tiryono, T. (2018) · International journal of statistics and applications · Cited by 20 · see citing works
Wang, T., Zeng, Z., Hu, Z., Zheng, L., Li, T., Li, Y., Liu, J., Li, J., Feng, G., He, L., et al. (2012) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.650203 · Cited by 19 · see citing works
Kabakambira, J. D., Uwera, G., Hategeka, M., Kayitesi, M. L., Kalala Malu, C. K., & Hategeka, C. (2018) · Pan African Medical Journal · doi:10.11604/pamj.2018.30.216.15663 · Cited by 16 · see citing works
Etzel, L., Hastings, W., Mattern, B. C., Oxford, M., Heim, C. M., Putnam, F., Noll, J. G., & Shalev, I. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104781 · Cited by 12 · see citing works
Ensink, J. B. M., Keding, T. J., Henneman, P., Venema, A., Papale, L. A., Alisch, R. S., Westerman, Y., van Wingen, G. A., Zantvoord, J. B., Middeldorp, C. M., et al. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.04.016 · Cited by 12 · see citing works
Rescaling the Post-Traumatic Stress Disorder Checklist for Use in Primary Care
McCutchan, P. K., Freed, M. C., Low, E. C., Belsher, B. E., & Engel, C. C. (2016) · Military Medicine · doi:10.7205/milmed-d-15-00444 · Cited by 6 · see citing works
Flagged first, then by citations
1 of the 71 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Zhou, A., & Ryan, J. (2023) · Genes · doi:10.3390/genes14081639 · Cited by 57 · see citing works
“There were six studies of trauma or PTSD following war, including two studies of Holocaust survivors [83,94,95], two studies on the Rwandan genocide [90,91], and one each from the Kosovo War [96] and Vietnam veterans [97].”
BackgroundH3Africa: a model for implementing biobank-based genomic research in resource-constrained settings
Sengupta, D., Choudhury, A., & Ramsay, M. (2025) · Human Molecular Genetics · doi:10.1093/hmg/ddaf113 · Cited by 34 · see citing works
Katrinli, Ş., Wani, A. H., Maihofer, A. X., Ratanatharathorn, A. D., Daskalakis, N. P., Montalvo‐Ortiz, J. L., Núñez-Ríos, D. L., Zannas, A. S., Zhao, X., Aiello, A. E., et al. (2024) · Genome Medicine · doi:10.1186/s13073-024-01417-1 · Cited by 35 · see citing works
Self-citationEpigenetic Echoes: Bridging Nature, Nurture, and Healing Across Generations
Banushi, B., Collova, J. R., & Milroy, H. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26073075 · Cited by 27 · see citing works
Anisman, H., Doubad, D., Asokumar, A., & Matheson, K. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105859 · Cited by 25 · see citing works
Gonçalves, C., Ip, K. I., Stanton, C. A., Bamwine, P., Williams, D. R., Rao, U., & Murry, V. M. (2026) · Neuropsychopharmacology · doi:10.1038/s41386-025-02239-4 · Cited by 11 · see citing works
“Musanabaganwa et al. [161] identi fi ed methylation changes in BCOR , PRDM8 , and VWDE , with some patterns present in both blood and brain tissue, suggesting potential neurodevelopmental relevance [161].”
Rivera, L. M., Uwizeye, G., Stolrow, H. G., Christensen, B. C., Rutherford, J. N., & Thayer, Z. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-78035-9 · Cited by 13 · see citing works
Mattonet, K., Scharpf, F., Block, K., Kumsta, R., & Hecker, T. (2023) · European Journal of Psychotraumatology · doi:10.1080/20008066.2023.2228155 · Cited by 12 · see citing works
Li, Y., Lu, Y., Xie, Q., Zeng, X., Zhang, R., Dang, W., Zhu, Y., & Zhang, J. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06141-5 · Cited by 8 · see citing works
Uwizeye, G., Rivera, L. M., Stolrow, H. G., Christensen, B. C., Rutherford, J. N., & Thayer, Z. M. (2025) · Communications Medicine · doi:10.1038/s43856-025-01065-5 · Cited by 6 · see citing works
Musanabaganwa, C., Jansen, S., Wani, A. H., Rugamba, A., Mutabaruka, J., Rutembesa, E., Uwineza, A., Fatumo, S., Hermans, E. J., Souopgui, J., et al. (2022) · Epigenomics · doi:10.2217/epi-2022-0079 · Cited by 6 · see citing works
Self-citationDahrendorff, J., Pages, K. P., Currier, G. W., Sarker, M. H., Graham, Z., Louis‐Jacques, A. F., Dagne, G. A., & Uddin, M. (2025) · BMC Medical Genomics · doi:10.1186/s12920-025-02240-2 · Cited by 3 · see citing works
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Anisman, H., Bombay, A., & Matheson, K. (2025) · Frontiers in Environmental Health · doi:10.3389/fenvh.2025.1720326 · Cited by 4 · see citing works
Rivera, L. M., Uwizeye, G., Stolrow, H. G., Christensen, B. C., Rutherford, J. N., & Thayer, Z. M. (2024) · medRxiv · doi:10.1101/2024.06.12.24308615 · Cited by 2 · see citing works
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Kac, E., Qi, Q., & Ryznar, R. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1769422 · Cited by 1 · see citing works
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Džaferović, N., & Ašić, A. (2026) · Mammalian Genome · doi:10.1007/s00335-025-10192-2 · Cited by 1 · see citing works
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Uwizeye, G., Rivera, L. M., Stolrow, H. G., Christensen, B. C., Rutherford, J. N., & Thayer, Z. M. (2024) · medRxiv · doi:10.1101/2024.10.01.24314372
(2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23565-8.09996-8
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Anisman, H., Hayley, S. P., & Kusnecov, A. W. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23565-8.00008-9
Emery, O., Carmeli, C., Gonseth-Nusslé, S., Juster, R., Kinnaer, C., Nanchen, D., Nusslé, S., Stringhini, S., & Chamberlain, J. D. (2025) · Epigenetics · doi:10.1080/15592294.2025.2578552
Szyf, M. (2026) · Springer eBooks · doi:10.1007/978-3-032-24295-2_2
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Raviola, G. J., Nguyen, V.-S., & Stoddard, F. J. (2024) · American Psychiatric Association Publishing eBooks · doi:10.1176/appi.books.9780873182539.lg10
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MEIJER, M., & Kobor, M. S. (2026) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19043-8.00001-3
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CHEISHVILI, D., Yaakov, H., & Shrira, A. (2026) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19043-8.00027-x
- Authors
- Musanabaganwa, C., Wani, A. H., Donglasan, J., Fatumo, S., Jansen, S., Mutabaruka, J., Rutembesa, E., Uwineza, A., Hermans, E. J., Roozendaal, B., Wildman, D. E., Mutesa, L., & Uddin, M.
- Affiliations
- Radboud University Nijmegen (NL)
- University of South Florida (US)
- London School of Hygiene & Tropical Medicine (GB)
- University of Rwanda (RW)
- Department of Clinical Psychology, College of Medicine & Health Sciences, University of Rwanda, Huye, Rwanda
- Centre for Human Genetics, College of Medicine & Health Sciences, University of Rwanda, Kigali, Rwanda
- ORCID
- Venue
- Epigenomics
- Publisher
- Informa UK Limited
- Published
- 2021-12-08
- Volume
- 14
- Issue
- 1
- Pages
- 11-25
- ISSN
- 1750-1911 (ISSN-L)
- 1750-192X
- PMC
- PMC8672329
- OpenAlex
- W4200381659
- Cited by
- 35
- References
- 71
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 11 · 2023: 5 · 2022: 3
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Epigenomics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institute of Healt (U01MH115485)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- Tutsi, prenatal exposure, DNA methylation, differentially methylated regions, BCOR, PRDM8, leukocyte DNA, Rwandan genocide
- MeSH terms
- Epigenome, Child, Female, Humans, Leukocytes, Pregnancy, Rwanda, Stress Disorders, Post-Traumatic, Survivors, DNA Methylation, Genocide
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