Transgenerational programming of maternal behaviour by prenatal stress
Open accessAbstract
Peripartum events hold the potential to have dramatic effects in the programming of physiology and behaviour of offspring and possibly subsequent generations. Here we have characterized transgenerational changes in rat maternal behaviour as a function of gestational and prenatal stress. Pregnant dams of the parental generation were exposed to stress from days 12-18 (F0-S). Their daughters and grand-daughters were either stressed (F1-SS, F2-SSS) or non-stressed (F1-SN, F2-SNN). Maternal antepartum behaviours were analyzed at a time when pregnant dams usually show a high frequency of tail chasing behaviours. F1-SS, F2-SNN and F2-SSS groups showed a significant reduction in tail chasing behaviours when compared with controls. The effects of multigenerational stress (SSS) slightly exceeded those of transgenerational stress (SNN) and resulted in absence of tail chasing behaviour. These findings suggest that antepartum maternal behaviour in rats is programmed by transgenerational inheritance of stress responses. Thus, altered antepartum maternal behaviour may serve as an indicator of an activated stress response during gestation.
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Maternal physiology, particularly stress and nutrition, can greatly impact the neural and behavioral development of offspring.
“This is in keeping with a large body of research showing that maternal physiology, particularly stress (85–87) and nutrition (88–90), can greatly impact the neural and behavioral development of offspring.”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [85]
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Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965 · see citing works
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works
Glucocorticoids, prenatal stress and the programming of disease
Harris, A., & Seckl, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.007 · Cited by 871 · see citing works
Epigenetic transgenerational actions of environmental factors in disease etiology
Skinner, M. K., Manikkam, M., & Guerrero‐Bosagna, C. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.12.007 · Cited by 713 · see citing works
Prenatal stress and the programming of the HPA axis
Glover, V., O’Connor, T. G., & O’Donnell, K. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.008 · Cited by 567 · see citing works
Champagne, F. A., & Meaney, M. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.016 · Cited by 510 · see citing works
Weaver, I. C. G., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., Szyf, M., & Meaney, M. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4164-06.2007 · Cited by 508 · see citing works
What is an epigenetic transgenerational phenotype?
Skinner, M. K. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.09.001 · Cited by 485 · see citing works
Epigenetic programming of stress responses through variations in maternal care
FISH, E. W., SHAHROKH, D., BAGOT, R., CALDJI, C., BREDY, T., SZYF, M., & MEANEY, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.011 · Cited by 361 · see citing works
Piazza, P. V., Rougé-Pont, F., Deroche, V, Maccari, S., Simon, H., & Le Moal, M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8716 · Cited by 346 · see citing works
Epigenetic transgenerational inheritance of altered stress responses
Crews, D. P., Gillette, R., Scarpino, S. V., Manikkam, M., Savenkova, M. I., & Skinner, M. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118514109 · Cited by 322 · see citing works
Are animal models relevant to key aspects of human parturition?
Mitchell, B. F., & Taggart, M. J. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00153.2009 · Cited by 267 · see citing works
Parenting Behavior Is Associated With the Early Neurobehavioral Development of Very Preterm Children
Treyvaud, K., Anderson, V. A., Howard, K., Bear, M. J., Hunt, R. W., Doyle, L. W., Inder, T. E., Woodward, L. J., & Anderson, P. J. (2009) · PEDIATRICS · doi:10.1542/peds.2008-0477 · Cited by 249 · see citing works
Fleming, A. S., Kraemer, G. W., Gonzalez, A., Lovic, V., Rees, S., & Melo, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00793-1 · Cited by 203 · see citing works
Zucchi, F. C. R., Yao, Y., Ward, I. D., Ilnytskyy, Y., Olson, D. M., Benzies, K., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056967 · Cited by 193 · see citing works
Self-citationMATERNAL AND FOETAL CORTICOSTERONE LEVELS DURING LATE PREGNANCY IN RATS
Dupouy, J., Coffigny, H., & Magre, S. (1975) · Journal of Endocrinology · doi:10.1677/joe.0.0650347 · Cited by 188 · see citing works
Metz, G. A. S., Jadavji, N. M., & Smith, L. K. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04285.x · Cited by 151 · see citing works
Sharp, H. M., Pickles, A. R., Meaney, M. J., Marshall, K. H., Tibu, F., & Hill, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045446 · Cited by 140 · see citing works
Rubinow, D. R., Crowder, V. L., Schmidt, P. J., & Rubinow, K. B. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-375097-6.10036-8 · Cited by 136 · see citing works
Changes in Hormone Levels and Gap Junctions in the Rat Uterus During Pregnancy and Parturition
Purl, C. P., & Garfield, R. E. (1982) · Biology of Reproduction · doi:10.1095/biolreprod27.4.967 · Cited by 135 · see citing works
Piazza, P. V., Barrot, M., Rougé‐Pont, F., Marinelli, M., Maccari, S., Abrous, D. N., Simon, H., & Moal, M. L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.26.15445 · Cited by 129 · see citing works
Kuhn, C. M., Schanberg, S. M., Field, T. M., Symanski, R., Zimmerman, E. A., SCAFIDI, F. A., & Roberts, J. (1991) · The Journal of Pediatrics · doi:10.1016/s0022-3476(05)82059-1 · Cited by 110 · see citing works
Whishaw, I. Q., Metz, G. A. S., Kolb, B., & Pellis, S. M. (2001) · Developmental Psychobiology · doi:10.1002/dev.1041 · Cited by 110 · see citing works
Stress as a Modulator of Motor System Function and Pathology
Metz, G. A. S. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.3-4.209 · Cited by 106 · see citing works
Effects of early life social stress on maternal behavior and neuroendocrinology
Murgatroyd, C., & Nephew, B. C. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.05.020 · Cited by 100 · see citing works
Pauk, J. S., Kuhn, C. M., Field, T. M., & Schanberg, S. M. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90359-0 · Cited by 94 · see citing works
Transgenerational inheritance of stress pathology
Matthews, S. G., & Phillips, D. I. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.01.009 · Cited by 91 · see citing works
van Hasselt, F. N., Tieskens, J. M., Trezza, V., Krugers, H. J., Vanderschuren, L. J. M. J., & Joëls, M. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.007 · Cited by 91 · see citing works
Migicovsky, Z., & Kovalchuk, I. (2011) · Frontiers in Genetics · doi:10.3389/fgene.2011.00028 · Cited by 86 · see citing works
Maternal Behavior in the Rat: an Investigation and Quantification of Nest Building
Denenberg, V. H., Taylor, R. E., & ZARROW, M. X. (1969) · Behaviour · doi:10.1163/156853969x00369 · Cited by 51 · see citing works
Maternal Programming of Reproductive Function and Behavior in the Female Rat
Cameron, N. M. (2011) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2011.00010 · Cited by 51 · see citing works
Paris, J. J., & Frye, C. A. (2010) · Stress · doi:10.3109/10253890.2010.512375 · Cited by 48 · see citing works
The secret language of destiny: stress imprinting and transgenerational origins of disease
Zucchi, F. C. R., Yao, Y., & Metz, G. A. S. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00096 · Cited by 48 · see citing works
Maternal care associates with play dominance rank among adult female rats
Parent, C. I., Corpo, A. D., Cameron, N. M., & Meaney, M. J. (2012) · Developmental Psychobiology · doi:10.1002/dev.21070 · Cited by 43 · see citing works
ZARROW, M. X., SAWIN, P. B., ROSS, S., Denenberg, V. H., Crary, D. D., Wilson, E. D., & Farooq, A. (1961) · Reproduction · doi:10.1530/jrf.0.0020152 · Cited by 43 · see citing works
[The transgenerational mechanisms in developmental programming of metabolic diseases].
Zambrano, E. (2009) · PubMed · Cited by 24 · see citing works
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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
Environmental stress and epigenetic transgenerational inheritance
Skinner, M. K. (2014) · BMC Medicine · doi:10.1186/s12916-014-0153-y · Cited by 225 · see citing works
Zucchi, F. C. R., Yao, Y., Ward, I. D., Ilnytskyy, Y., Olson, D. M., Benzies, K., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056967 · Cited by 193 · see citing works
Self-citationAuriti, C., Rose, D. U. D., Santisi, A., Martini, L., Piersigilli, F., Bersani, I., Ronchetti, M. P., & Caforio, L. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166198 · Cited by 162 · see citing works
Yao, Y., Robinson, A. M., Zucchi, F. C. R., Robbins, J. C., Babenko, O., Kovalchuk, O., Kovalchuk, I., Olson, D. M., & Metz, G. A. S. (2014) · BMC Medicine · doi:10.1186/s12916-014-0121-6 · Cited by 146 · 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
Allostatic Load and Preterm Birth
Olson, D., Severson, E., Verstraeten, B. S. E., Ng, J. W. Y., McCreary, J., & Metz, G. A. S. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226209 · Cited by 115 · see citing works
Serpeloni, F., Radtke, K., de Assis, S. G., Henning, F., Nätt, D., & Elbert, T. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.153 · Cited by 98 · see citing works
Labor and delivery outcomes among young adolescents
Torvie, A. J., Callegari, L. S., Schiff, M. A., & Debiec, K. E. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.04.024 · Cited by 97 · see citing works
Prenatal noise stress impairs HPA axis and cognitive performance in mice
Jafari, Z., Mehla, J., Kolb, B. E., & Mohajerani, M. H. (2017) · Scientific Reports · doi:10.1038/s41598-017-09799-6 · Cited by 84 · see citing works
Oxytocin during Development: Possible Organizational Effects on Behavior
Miller, T. V., & Caldwell, H. K. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00076 · Cited by 79 · see citing works
Inguaggiato, E., Sgandurra, G., & Cioni, G. (2017) · Neuropsychiatrie de l Enfance et de l Adolescence · doi:10.1016/j.neurenf.2017.03.009 · Cited by 78 · see citing works
Phillips, N. L. H., & Roth, T. L. (2019) · Genes · doi:10.3390/genes10010047 · Cited by 77 · see citing works
Individual differences in the effects of prenatal stress exposure in rodents
Boersma, G. J., & Tamashiro, K. L. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.006 · Cited by 71 · see citing works
Climate change is a major stressor causing poor pregnancy outcomes and child development
Olson, D. M., & Metz, G. A. S. (2020) · F1000Research · doi:10.12688/f1000research.27157.1 · Cited by 64 · see citing works
Environmental intervention as a therapy for adverse programming by ancestral stress
McCreary, J. K., Erickson, Z. T., Hao, Y., Ilnytskyy, Y., Kovalchuk, I., & Metz, G. A. S. (2016) · Scientific Reports · doi:10.1038/srep37814 · Cited by 59 · see citing works
Self-citationZaidan, H., & Gaisler‐Salomon, I. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.04.013 · Cited by 54 · see citing works
Stress transgenerationally programs metabolic pathways linked to altered mental health
Kiss, D., Ambeskovic, M., Montina, T., & Metz, G. A. S. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2272-4 · Cited by 52 · see citing works
Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice
Garcia‐Flores, V., Romero, R. J., Furcron, A.-E., Levenson, D., Galaz, J., Zou, C., Hassan, S. S., Hsu, C., Olson, D. M., Metz, G. A. S., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00254 · Cited by 49 · see citing works
Prenatal Stress Alters Hippocampal Neuroglia and Increases Anxiety in Childhood
Bennett, G. A., Palliser, H. K., Shaw, J. C., Walker, D. W., & Hirst, J. J. (2015) · Developmental Neuroscience · doi:10.1159/000437302 · Cited by 43 · see citing works
McCreary, J. K., Truica, L. S., Friesen, B., Yao, Y., Olson, D. M., Kovalchuk, I., Cross, A. R., & Metz, G. A. S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.046 · Cited by 42 · see citing works
Erickson, Z. T., Falkenberg, E. A., & Metz, G. A. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092132 · Cited by 40 · see citing works
Ambeskovic, M., Soltanpour, N., Falkenberg, E. A., Zucchi, F. C. R., Kolb, B. E., & Metz, G. A. S. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw063 · Cited by 39 · see citing works
The Adverse Effects of Auditory Stress on Mouse Uterus Receptivity and Behaviour
Jafari, Z., Faraji, J., Mirza Agha, B., Metz, G. A. S., Kolb, B. E., & Mohajerani, M. H. (2017) · Scientific Reports · doi:10.1038/s41598-017-04943-8 · Cited by 39 · see citing works
Ambeskovic, M., Babenko, O., Ilnytskyy, Y., Kovalchuk, I., Kolb, B., & Metz, G. A. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-42691-z · Cited by 36 · see citing works
Maternal Behavior in Beef Cattle: The Physiology, Assessment and Future Directions—A Review
Nevard, R. P., Pant, S. D., Broster, J., Norman, S. T., & Stephen, C. (2022) · Veterinary Sciences · doi:10.3390/vetsci10010010 · Cited by 38 · see citing works
Corticosterone response to gestational stress and postpartum memory function in mice
Jafari, Z., Mehla, J., Afrashteh, N., Kolb, B. E., & Mohajerani, M. H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180306 · Cited by 37 · see citing works
Fish as a model in social neuroscience: conservation and diversity in the social brain network
Ogawa, S., Pfaff, D. W., & Parhar, I. S. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12689 · Cited by 31 · see citing works
Asamoah, B. O., & Agardh, A. (2017) · BMJ Open · doi:10.1136/bmjopen-2016-011663 · Cited by 29 · see citing works
Verstraeten, B. S. E., McCreary, J. K., Weyers, S., Metz, G. A. S., & Olson, D. M. (2019) · Biology of Reproduction · doi:10.1093/biolre/ioy166 · Cited by 28 · see citing works
Intergenerational accumulation of impairments in maternal behavior following postnatal social stress
Nephew, B. C., Carini, L. M., Sallah, S., Cotino, C., Alyamani, R. A. S., Pittet, F., Bradburn, S., & Murgatroyd, C. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.05.011 · Cited by 28 · see citing works
Accurate diagnosis and repair of obstetric anal sphincter injuries: why and how
Hickman, L. C., & Propst, K. A. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.02.044 · Cited by 27 · see citing works
Intergenerational Sex-Specific Transmission of Maternal Social Experience
Faraji, J., Karimi, M., Soltanpour, N., Rouhzadeh, Z., Roudaki, S., Hosseini, S. A., Jafari, S. Y., Abdollahi, A. A., Soltanpour, N., Moeeini, R., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-28729-8 · Cited by 25 · see citing works
Boschen, K. E., Keller, S. M., Roth, T. L., & Klintsova, A. Y. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.12.009 · Cited by 24 · see citing works
Evidence for Ancestral Programming of Resilience in a Two-Hit Stress Model
Faraji, J., Soltanpour, N., Ambeskovic, M., Zucchi, F. C. R., Beaumier, P., Kovalchuk, I., & Metz, G. A. S. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00089 · Cited by 23 · see citing works
Govindaraj, S., Shanmuganathan, A., & Rajan, R. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171089 · Cited by 23 · see citing works
Zucchi, F. C. R., Yao, Y., Ilnytskyy, Y., Robbins, J. C., Soltanpour, N., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092130 · Cited by 20 · see citing works
King, S. E., Schatz, N. A., Babenko, O., Ilnytskyy, Y., Kovalchuk, I., & Metz, G. A. S. (2025) · Communications Biology · doi:10.1038/s42003-024-07444-3 · Cited by 22 · see citing works
Social Isolation Stress Modulates Pregnancy Outcomes and the Inflammatory Profile of Rat Uterus
Lopes, N. A., Falkenberg, E. A., Wiley, C., Patel, V., Serrano-Lomelin, J. A., Fang, X., Weiler, A. M., McCreary, J. K., Metz, G. A. S., & Olson, D. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116169 · Cited by 16 · see citing works
Skelin, I., Needham, M., Molina, L., Metz, G. A. S., & Gruber, A. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.009 · Cited by 16 · see citing works
Adverse effects of paternal chemotherapy exposure on the progeny brain: intergenerational chemobrain
KOVALCHUK, A. V., Ilnytskyy, Y., Wóycicki, R. K., Rodriguez‐Juarez, R., Metz, G. A. S., & Kovalchuk, O. (2018) · Oncotarget · doi:10.18632/oncotarget.24311 · Cited by 15 · see citing works
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Nwogueze, B. C., Ojieh, A. E., Ovuakporaye, S. I., Iju, W. J., Godsday, O. U., Olowe, G. T., Nneamaka, E. C., & Peter, A. C. (2020) · Biomedical & Pharmacology Journal · doi:10.13005/bpj/2038 · Cited by 14 · see citing works
Macrosomia and its predictors in pregnant women with diabetes in Ethiopia
Belay, D. M., Bayih, W. A., Alemu, A. Y., Endalamaw, A., Mekonen, D. K., Ayele, A. S., Aytenew, T. M., Aynew, Y. E., Hailemichael, W., Getu, S., et al. (2021) · Tropical Medicine & International Health · doi:10.1111/tmi.13684 · Cited by 14 · see citing works
Effects of maternal social isolation on adult rodent offspring cognition
McDonald, R. J., Hong, N. S., Trow, J., Kaupp, C., Balog, R. J., Gokarn, L., Falkenberg, E. A., McCreary, K. J. K., Soltanpour, N., Witbeck, C., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-34834-0 · Cited by 14 · see citing works
Multiple prenatal stresses increase sexual dimorphism in adult offspring behavior
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Environmental influences on the female epigenome and behavior
Keller, S. M., & Roth, T. L. (2016) · Current Zoology · doi:10.1093/eep/dvw007 · Cited by 12 · see citing works
Effects of sleep restriction during pregnancy on postpartum maternal behavior in female rats
Pires, G. N., Tufik, S., & Andersen, M. L. (2020) · Behavioural Processes · doi:10.1016/j.beproc.2020.104200 · Cited by 10 · see citing works
Influence of gestational exercise practice and litter size reduction on maternal care
August, P. M., RODRIGUES, K. D. S., Klein, C. P., dos Santos, B. G., & Matté, C. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135454 · Cited by 9 · see citing works
Robillard, P., Hulsey, T. C., Boukerrou, M., Bonsante, F., Dekker, G., & Iacobelli, S. (2017) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2017.1334049 · Cited by 8 · see citing works
Animal Models of Transgenerational Epigenetic Effects
Rosenfeld, C. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00011-8 · Cited by 7 · see citing works
Rebnord, T., Østbye, T., Mmbaga, B. T., Mchome, B. L., Lie, R. T., & Daltveit, A. K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184362 · Cited by 6 · see citing works
Commodification of usada bali: between profit-oriented and negotiation of sasana balian
Suatama, I. B., Kumbara, A. A. N. A., & Dewi, A. A. (2019) · International Journal of Social Sciences and Humanities · doi:10.29332/ijssh.v3n2.300 · Cited by 6 · see citing works
Reporting of ethics in peer-reviewed verbal autopsy studies: a systematic review
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Maternal stress effects across generations in a precocial bird
Charrier, M., Lumineau, S., George, I., Meurisse, M., Georgelin, M., Palme, R., Angelier, F., Coustham, V., Nicolle, C., Bertin, A., et al. (2024) · Royal Society Open Science · doi:10.1098/rsos.231826 · Cited by 3 · see citing works
Epigenetics and the Impact of Early-Life Stress Across Generations
van Steenwyk, G., & Mansuy, I. M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813156-5.00029-7 · Cited by 4 · see citing works
Sunaga, Y., Takahashi, M. K., Anan, M., & Shinkoda, K. (2020) · International Journal of Industrial Ergonomics · doi:10.1016/j.ergon.2020.103057 · Cited by 3 · see citing works
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Dias, B. G. (2024) · Chemical Senses · doi:10.1093/chemse/bjae002 · Cited by 2 · see citing works
Hoover, T. D., & Metz, G. A. S. (2020) · Springer eBooks · doi:10.1007/978-3-030-41716-1_6 · Cited by 3 · see citing works
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Yen, E., Asis‐Cruz, J. D., & Rasmussen, J. M. (2026) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2026.101697 · Cited by 1 · see citing works
Caddick, R. A., & Isles, A. R. (2015) · Journal of Clinical Epigenetics · Cited by 1 · see citing works
The Human Toll of Collective Trauma: The Ravages of War and Persecution
Gouni, O., & Verny, T. R. (2023) · The International Journal of Prenatal & Life Sciences · doi:10.24946/ijpls/20231010 · Cited by 3 · see citing works
Schierding, W. S., Vickers, M. H., O'Sullivan, J. M., & Cutfield, W. S. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-35214-7.00009-3 · Cited by 1 · see citing works
Kiss, D. (2016)
Importance of considering methodological variables in rat studies
Joshi, N. (2013) · Health Science Inquiry · doi:10.29173/hsi132
Postpartum Mood Disorders: Prevention by Prenatal Bonding (BA)
Schroth, G. (2020) · Springer eBooks · doi:10.1007/978-3-030-41716-1_41
von Lüpke, H. (2020) · Springer eBooks · doi:10.1007/978-3-030-41716-1_9
Towards understanding and halting legacies of traumaPreprint
Taylor, W. F., Korobkova, L., Bhinderwala, N., & Dias, B. G. (2024) · doi:10.31234/osf.io/7jxat
Bapat, V. A., Waters, R. C., Gordon, J. K., & Gould, E. (2026) · Neurobiology of Stress · doi:10.1016/j.ynstr.2026.100788
Hernandez, L. P., Main, A. R. H., & Salak‐Johnson, J. L. (2026) · Animals · doi:10.3390/ani16101435
- Authors
- Ward, I. D., Zucchi, F. C., Robbins, J. C., Falkenberg, E. A., Olson, D. M., Benzies, K., & Metz, G. A.
- Affiliations
- University of Lethbridge (CA)
- University of Alberta (CA)
- University of Calgary (CA)
- Corresponding author
- Metz, Gerlinde A
- Venue
- BMC Pregnancy and Childbirth
- Published
- 2013-01
- Volume
- 13
- Issue
- S1
- Pages
- S9-S9
- ISSN
- 1471-2393 (ISSN-L)
- PMC
- PMC3561190
- OpenAlex
- W2097619644
- Cited by
- 73
- References
- 39
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 11 · 2019: 4 · 2018: 5 · 2017: 12 · 2016: 7 · 2015: 7 · 2014: 7 · 2013: 3
- FWCI
- 7.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Pregnancy and Childbirth (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Open ULeth Scholarship (OPUS) (University of Lethbridge) (submittedVersion, cc-by)
- Funders
- Alberta Innovates (200700595)
- Canadian Institutes of Health Research
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- prenatal stress, maternal behavior, stress response, rats, offspring behavior
- MeSH terms
- Analysis of Variance, Animals, Behavior, Animal, Female, Maternal Behavior, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Rats, Long-Evans, Models, Animal, Rats, Peripartum Period
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