Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability
Abstract
Previous studies have found that stressful events during pregnancy can influence the developing fetus, resulting in attentional and neuromotor problems. This prospective study examined whether periods of vulnerability exist for neurobehavioral impairments associated with prenatal stress, using a nonhuman primate model. Twenty-eight rhesus monkey infants were born to mothers in 3 groups: (1) early gestation stress involving mild psychological stress from gestational days 45–90, (2) mid-late gestation stress from days 90–145, and (3) undisturbed controls. Infants were separated from their mothers on days 4, 9, 15, and 22 (±1) postpartum for growth and neurobehavioral assessments. Results indicated that infants from the early gestation stress condition weighed less than infants from mothers stressed during mid-late gestation. Moreover, whereas both groups scored lower than controls on measures of attention and neuromotor maturity, early gestation stress was associated with more pronounced and more pervasive motor impairments than mid-late gestation stress. These results suggest sensitivity to prenatal stress effects peaks during early gestation, tapering off during mid-late gestation. Clarifying the period of greatest vulnerability to prenatal stress moves toward elucidating the underlying mechanism for prenatal stress effects and may lead to more successful intervention and/or prevention.
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This possibility is supported by rhesus monkey observations where prenatal exposure to the same stressor had greater effects on postnatal motor development if earlier in gestation when neuronal migration peaked than mid-to-late when synaptogenesis peaked.
“This possibility has been supported by observations in rhesus monkeys, where prenatal exposure to the same stressor had greater effects on postnatal motor development if it occurred earlier in gestation, when neuronal migration was at its peak, than if it occurred in mid- to late gestation, when synaptogenesis was at its peak (Schneider et al., 1999).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Schneider et al., 1999
Brain regions undergoing the most extensive maturation are thought to be the most vulnerable to insult.
“Given that brain regions undergoing the most extensive maturation are thought to be the most vulnerable to insult (Schneider et al., 1999), we might expect differing effects of ELS based on developmental timing.”
From The effects of early life stress on reward processing (2018) · cites this paper as Schneider et al., 1999
Cites
Simultaneous Statistical Inference
Miller, R. G. (1981) · Springer series in statistics · doi:10.1007/978-1-4613-8122-8 · Cited by 5,608 · see citing works
Comparison of two modes of stress measurement: Daily hassles and uplifts versus major life events
Kanner, A. D., Coyne, J. C., Schaefer, C. A., & Lazarus, R. S. (1981) · Journal of Behavioral Medicine · doi:10.1007/bf00844845 · Cited by 3,128 · see citing works
Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys
Bourgeois, J.-P., Goldman-Rakic, P. S., & Rakic, P. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.1.78 · Cited by 687 · see citing works
Bourgeois, J., & Rakic, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02801.1993 · Cited by 567 · see citing works
Moderate Prenatal Alcohol Exposure: Effects on Child IQ and Learning Problems at Age 7 1/2 Years
Streissguth, A. P., Barr, H. M., & Sampson, P. D. (1990) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1990.tb01224.x · Cited by 547 · see citing works
Limits of Neurogenesis in Primates
RAKIC, P. T. (1985) · Science · doi:10.1126/science.3975601 · Cited by 503 · see citing works
Disorders of Neuronal Migration
Barth, P. G. (1987) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s031716710002610x · Cited by 435 · see citing works
Norbeck, J. S., & Tilden, V. P. (1983) · Journal of Health and Social Behavior · doi:10.2307/2136301 · Cited by 423 · see citing works
Sensitive periods in development: Structural characteristics and causal interpretations.
Bornstein, M. H. (1989) · Psychological Bulletin · doi:10.1037/0033-2909.105.2.179 · Cited by 377 · see citing works
Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys
Goldman‐Rakic, P. S., & Brown, R. M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90146-8 · Cited by 283 · see citing works
Conceptualizations, measurement, and effects of prenatal maternal stress on birth outcomes
Lobel, M. (1994) · Journal of Behavioral Medicine · doi:10.1007/bf01857952 · Cited by 256 · see citing works
Psychosocial stress in pregnancy and its relation to low birth weight.
Newton, R., & Hunt, L. P. (1984) · BMJ · doi:10.1136/bmj.288.6425.1191 · Cited by 256 · see citing works
Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life
Zecevic, N., Bourgeois, J.-P., & Rakic, P. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90124-7 · Cited by 253 · see citing works
Long‐term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys
Clarke, A. S., Wittwer, D. J., Abbott, D. H., & Schneider, M. L. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270502 · Cited by 245 · see citing works
Self-citationStress, anxiety, and birth outcomes: A critical review of the evidence.
Istvan, J. A. (1986) · Psychological Bulletin · doi:10.1037/0033-2909.100.3.331 · Cited by 216 · see citing works
Timing of Neuroblast Multiplication in Developing Human Brain
Dobbing, J., & Sands, J. (1970) · Nature · doi:10.1038/226639a0 · Cited by 207 · see citing works
Prenatal alcohol exposure and infant information processing ability.
Jacobson, S., Jacobson, J. L., Sokol, R. J., Martier, S., & Ager, J. W. (1993) · PubMed · Cited by 196 · see citing works
Prenatal stress has long‐term effects on behavioral responses to stress in juvenile rhesus monkeys
Clarke, A. S., & Schneider, M. L. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260506 · Cited by 187 · see citing works
Self-citationPhysical growth of the rhesus monkey (Macaca mulatta)
WAGENEN, G. V., & CATCHPOLE, H. R. (1956) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330140219 · Cited by 180 · see citing works
Psychosocial influences on new born outcomes: A controlled prospective study
Pagel, M. D., SMILKSTEIN, G., Regen, H., & Montano, D. (1990) · Social Science & Medicine · doi:10.1016/0277-9536(90)90158-o · Cited by 180 · see citing works
Abnormalities of Pregnancy as a Function of Anxiety and Life Stress
Gorsuch, R. L., & Key, M. K. (1974) · Psychosomatic Medicine · doi:10.1097/00006842-197407000-00009 · Cited by 178 · see citing works
Schneider, M. L. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250706 · Cited by 158 · see citing works
Self-citationSchneider, M. L., Coe, C. L., & Lubach, G. R. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250604 · Cited by 145 · see citing works
Self-citationSchneider, M. L., & Suomi, S. J. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80021-l · Cited by 141 · see citing works
Self-citationRepeated Social Stress during Pregnancy Impairs Neuromotor Development of the Primate Infant
Schneider, M. L., & Coe, C. L. (1993) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-199304000-00002 · Cited by 139 · see citing works
Self-citationNeonatal Behavioral Assessment Scale, 2nd ed.
Pavlakis, S. G. (1986) · Neurology · doi:10.1212/wnl.36.6.877 · Cited by 131 · see citing works
Experimental studies on congenital malformations
WILSON, J. G. (1959) · Journal of Chronic Diseases · doi:10.1016/0021-9681(59)90026-8 · Cited by 128 · see citing works
Synaptogenesis in Monkey Somatosensory Cortex
Zečević, N., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.6.510 · Cited by 122 · see citing works
Schneider, M. L. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80009-j · Cited by 109 · see citing works
Self-citationEyler, F. D., Behnke, M., Conlon, M., Woods, N. S., & Wobie, K. (1998) · PEDIATRICS · doi:10.1542/peds.101.2.237 · Cited by 104 · see citing works
Psychobiological Aspects of Life Stress
Frankenhaeuser, M. (1980) · Springer eBooks · doi:10.1007/978-1-4684-1042-6_10 · Cited by 103 · see citing works
Mechanism of nitrofen teratogenesis.
Manson, J. M. (1986) · Environmental Health Perspectives · doi:10.1289/ehp.8670137 · Cited by 93 · see citing works
Schneider, M. L., Moore, C. F., Suomi, S. J., & Champoux, M. (1991) · American Journal of Primatology · doi:10.1002/ajp.1350250302 · Cited by 86 · see citing works
Self-citationHormonal Response to Stress in the Squirrel Monkey (Saimiri sciureus)
Coe, C. L., Mendoza, S. P., Davidson, J. M., Smith, E. R., Dallman, M. F., & Levine, S. D. (2008) · Neuroendocrinology · doi:10.1159/000122792 · Cited by 83 · see citing works
Prenatal stress alters brain biogenic amine levels in primates
Schneider, M. L., Clarke, A. S., Kraemer, G. W., Roughton, E. C., Lubach, G. R., Rimm‐Kaufman, S. E., Schmidt, D. E., & Ebert, M. H. (1998) · Development and Psychopathology · doi:10.1017/s0954579498001679 · Cited by 81 · see citing works
Self-citationMaternal anxiety and neonatal wellbeing
Crandon, A. J. (1979) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(79)90015-1 · Cited by 80 · see citing works
Childbirth education, maternal attitudes, and delivery
Zax, M., Sameroff, A. J., & Farnum, J. E. (1975) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(75)90525-6 · Cited by 74 · see citing works
Delayed Object Permanence Development in Prenatally Stressed Rhesus Monkey Infants (Macaca Mulatta)
Schneider, M. L. (1992) · The Occupational Therapy Journal of Research · doi:10.1177/153944929201200203 · Cited by 70 · see citing works
Self-citationNewell‐Morris, L. L., Fahrenbruch, C. E., & Sackett, G. P. (2009) · Biology of the Neonate · doi:10.1159/000243104 · Cited by 66 · see citing works
Schneider, M. L., Roughton, E. C., & Lubach, G. R. (1997) · Child Development · doi:10.1111/j.1467-8624.1997.tb01959.x · Cited by 63 · see citing works
Self-citationPsychological factors in preterm labor: critical review and theoretical synthesis
Omer, H., & Everly, G. S. (1988) · American Journal of Psychiatry · doi:10.1176/ajp.145.12.1507 · Cited by 55 · see citing works
Clarke, A. S., Soto, A. A., Bergholz, T. M., & Schneider, M. L. (1996) · Infant Behavior and Development · doi:10.1016/s0163-6383(96)90006-5 · Cited by 50 · see citing works
Self-citationSurvey of Protocols for Nursery-Rearing Infant Macaques
Ruppenthal, G. C. (1979) · Springer eBooks · doi:10.1007/978-1-4684-3477-4_13 · Cited by 49 · see citing works
Neonatal behavioral assessment.
Rs, I. (1990) · PubMed · Cited by 32 · see citing works
Farber, E. A., Vaughn, B. E., & Egeland, B. R. (1981) · Early Human Development · doi:10.1016/0378-3782(81)90034-7 · Cited by 28 · see citing works
The development of the frontal lobe. A view from the rear of the brain.
RAKIC, P. T. (1995) · PubMed · Cited by 28 · see citing works
Maternal Endocrine Activation During Pregnancy Alters Neurobehavioral State in Primate Infants
Roughton, E. C., Schneider, M. L., Bromley, L. J., & Coe, C. L. (1998) · American Journal of Occupational Therapy · doi:10.5014/ajot.52.2.90 · Cited by 26 · see citing works
Self-citationNeurophysiology: Plasticity in the visual cortex
Sillito, A. M. (1983) · Nature · doi:10.1038/303477a0 · Cited by 17 · see citing works
Maternal Stress during Pregnancy and the Behavior of the Offspring
HUTTUNEN, M. O. (1989) · Springer eBooks · doi:10.1007/978-1-4684-5634-9_15 · Cited by 12 · see citing works
Toward a more temporal view of organism-environment interaction.
Sackett, G. P. (2004) · American Psychological Association eBooks · doi:10.1037/10100-001 · Cited by 7 · see citing works
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Antenatal maternal stress and long‐term effects on child neurodevelopment: how and why?
Talge, N. M., Neal, C., Glover, V., & the Early Stress, T. R. A. P. S. N. F. A. N. E. O. C. A. A. M. H. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01714.x · Cited by 1,349 · see citing works
Van den Bergh, B. R. H., Mulder, E. J. H., Mennes, M., & Glover, V. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.007 · Cited by 1,104 · see citing works
Prenatal maternal stress: effects on pregnancy and the (unborn) child
Mulder, E. J. H., Robles de Medina, P. G., Huizink, A. C., Van den Bergh, B. R. H., Buitelaar, J. K., & Visser, G. H. A. (2002) · Early Human Development · doi:10.1016/s0378-3782(02)00075-0 · Cited by 779 · see citing works
Davis, E. P., & Sandman, C. A. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01385.x · Cited by 704 · see citing works
Stress during pregnancy is associated with developmental outcome in infancy
Huizink, A. C., Robles de Medina, P. G., Mulder, E. J. H., Visser, G. H. A., & Buitelaar, J. K. (2003) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00166 · Cited by 651 · see citing works
Alterations induced by gestational stress in brain morphology and behaviour of the offspring
Weinstock, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00018-1 · Cited by 791 · see citing works
den Bergh, B. R. H. V., & Marcoen, A. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00727.x · Cited by 636 · see citing works
Prenatal stress and brain development
Charil, A., Laplante, D. P., Vaillancourt, C., & King, S. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.06.002 · Cited by 554 · see citing works
Oberlander, T. F., Warburton, W., Misri, S., Aghajanian, J., & Hertzman, C. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.8.898 · Cited by 551 · see citing works
When stress happens matters: Effects of earthquake timing on stress responsivity in pregnancy
Glynn, L. M., Wadhwa, P. D., Dunkel-Schetter, C., Chicz-DeMet, A., & Sandman, C. A. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.111066 · Cited by 508 · see citing works
Prenatal Stress and Neurodevelopment of the Child: Focus on the HPA Axis and Role of the Placenta
O’Donnell, K. J., O’Connor, T. G., & Glover, V. A. S. (2009) · Developmental Neuroscience · doi:10.1159/000216539 · Cited by 509 · see citing works
Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys
Coe, C. L., Kramer, M., Czéh, B., Gould, E., Reeves, A. J., Kirschbaum, C., & Fuchs, E. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00698-x · Cited by 477 · see citing works
Huizink, A. C., Mulder, E. J. H., & Buitelaar, J. K. (2004) · Psychological Bulletin · doi:10.1037/0033-2909.130.1.115 · Cited by 473 · see citing works
Monk, C. E., Spicer, J., & Champagne, F. A. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000764 · Cited by 458 · see citing works
Prenatal stress and risk for autism
KINNEY, D., MUNIR, K., CROWLEY, D., & MILLER, A. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.06.004 · Cited by 440 · see citing works
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.010 · Cited by 435 · see citing works
Maternal Stress During Pregnancy Predicts Cognitive Ability and Fearfulness in Infancy
Bergman, K., Sarkar, P., O’Connor, T. G., Modi, N., & Glover, V. A. S. (2007) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e31814a62f6 · Cited by 430 · see citing works
Psychological measures of prenatal stress as predictors of infant temperament
HUIZINK, A. C., ROBLES DE MEDINA, P. G., MULDER, E. J. H., VISSER, G. H. A., & BUITELAAR, J. K. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200209000-00008 · Cited by 409 · see citing works
Beydoun, H. A., & Saftlas, A. F. (2008) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2008.00951.x · Cited by 413 · see citing works
Maternal psychological distress during pregnancy in relation to child development at age two
DiPietro, J. A., Novak, M. F. S. X., Costigan, K. A., Atella, L. D., & Reusing, S. P. (2006) · Child Development · doi:10.1111/j.1467-8624.2006.00891.x · Cited by 390 · see citing works
The Price We Pay: Economic and Social Consequences of Inadequate Education
Belfield, C., & Levin, H. (2008) · Choice Reviews Online · doi:10.5860/choice.45-6317 · Cited by 369 · see citing works
Prenatal stress and cognitive development and temperament in infants
Buitelaar, J. K., Huizink, A. C., Mulder, E. J. H., de Medina, P. R., & Visser, G. H. A. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00050-2 · Cited by 332 · see citing works
The role of prenatal stress in the etiology of developmental behavioural disorders
Kofman, O. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00015-5 · Cited by 331 · see citing works
Autism Prevalence Following Prenatal Exposure to Hurricanes and Tropical Storms in Louisiana
Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-007-0414-0 · Cited by 295 · see citing works
Sandman, C. A., Davis, E. P., Buß, C., & Glynn, L. M. (2011) · Neuroendocrinology · doi:10.1159/000327017 · Cited by 293 · see citing works
Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age
Buss, C., Davis, E. P., Hobel, C. J., & Sandman, C. A. (2011) · Stress · doi:10.3109/10253890.2011.623250 · Cited by 289 · see citing works
The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming
Bronson, S. L., & Bale, T. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.231 · Cited by 285 · see citing works
The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm
King, S., & Laplante, D. P. (2005) · Stress · doi:10.1080/10253890500108391 · Cited by 286 · see citing works
(2012) · Springer eBooks · doi:10.1007/springerreference_75865 · Cited by 285 · see citing works
Parental Depression: Animal Models of an Adverse Life Event
Newport, D. J., Stowe, Z. N., & Nemeroff, C. B. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.8.1265 · Cited by 265 · see citing works
Hompes, T., Izzi, B., Gellens, E., Morreels, M., Fieuws, S., Pexsters, A., Schops, G., Dom, M., Van Bree, R., Freson, K., et al. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.03.009 · Cited by 262 · see citing works
Monk, C. E., Georgieff, M., & Osterholm, E. A. (2012) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12000 · Cited by 260 · see citing works
Armed conflict and birth weight: Evidence from the al-Aqsa Intifada
Mansour, H., & Rees, D. I. (2011) · Journal of Development Economics · doi:10.1016/j.jdeveco.2011.12.005 · Cited by 245 · see citing works
de Vries, A., Holmes, M. C., Heijnis, A., Seier, J. V., van Heerden, J., Louw, J., Wolfe‐Coote, S. A., Meaney, M. J., Levitt, N. S., & Seckl, J. R. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30982 · Cited by 238 · see citing works
Neuroactive steroids: State of the art and new perspectives
Melcangi, R. C., García‐Segura, L. M., & Mensah‐Nyagan, A. G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7403-5 · Cited by 232 · see citing works
Maternal stress and affect influence fetal neurobehavioral development
DiPietro, J. A., Hilton, S. C., Hawkins, M., Costigan, K. A., & Pressman, E. K. (2002) · Developmental Psychology · doi:10.1037/0012-1649.38.5.659 · Cited by 218 · see citing works
Acute maternal stress in pregnancy and schizophrenia in offspring: A cohort prospective study
Malaspina, D., Corcoran, C. M., Kleinhaus, K., Perrin, M., Fennig, S., Nahon, D., Friedlander, Y., & Harlap, S. (2008) · BMC Psychiatry · doi:10.1186/1471-244x-8-71 · Cited by 214 · see citing works
Owen, D., Andrews, M. H., & Matthews, S. G. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.004 · Cited by 207 · see citing works
RetractedOsborne, S., Biaggi, A., Chua, T.-E., Preez, A. D., Hazelgrove, K. M., Nikkheslat, N., Previti, G., Zunszain, P. A., Conroy, S., & Pariante, C. M. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.06.017 · Cited by 207 · see citing works
Anesthesia for Cesarean Delivery and Learning Disabilities in a Population-based Birth Cohort
Šprung, J., Flick, R. P., Wilder, R. T., Katusic, S. K., Pike, T. L., Dingli, M., Gleich, S. J., Schroeder, D. R., Barbaresi, W. J., Hanson, A. C., et al. (2009) · Anesthesiology · doi:10.1097/aln.0b013e3181adf481 · Cited by 203 · see citing works
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
“Given that brain regions undergoing the most extensive maturation are thought to be the most vulnerable to insult (Schneider et al., 1999), we might expect differing effects of ELS based on developmental timing.”
BackgroundPregnant women become insensitive to cold stress
Kammerer, M. H., Adams, D., von Castelberg, B., & Glover, V. A. S. (2002) · BMC Pregnancy and Childbirth · doi:10.1186/1471-2393-2-8 · Cited by 201 · see citing works
Schneider, M. L., Moore, C. F., Kraemer, G. W., Roberts, A. D., & DeJesus, O. T. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00050-6 · Cited by 197 · see citing works
Self-citationLi, J., Olsen, J., Vestergaard, M., & Obel, C. (2010) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-010-0113-9 · Cited by 190 · see citing works
Behavior genetics and postgenomics
Charney, E. (2012) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11002226 · Cited by 207 · see citing works
Oberlander, T. F., GRUNAU, R. E., Fitzgerald, C., Papsdorf, M., Rurak, D. W., & Riggs, W. K. (2005) · PEDIATRICS · doi:10.1542/peds.2004-0420 · Cited by 164 · see citing works
Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity
MUELLER, B., & Bale, T. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.019 · Cited by 162 · see citing works
In Utero Exposure to Ischemic-Hypoxic Conditions and Attention-Deficit/Hyperactivity Disorder
Getahun, D., Rhoads, G., Demissie, K., Lu, S.-E., Quinn, V. P., Fassett, M., Wing, D., & Jacobsen, S. (2013) · Pediatrics · doi:10.1542/peds.2012-1298 · Cited by 132 · see citing works
Sarkar, P., Bergman, K., O’Connor, T. G., & Glover, V. A. S. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01659.x · Cited by 138 · see citing works
Maternal immune activation in nonhuman primates alters social attention in juvenile offspring
Machado, C. J., Whitaker, A. M., Smith, S. E. P., Patterson, P. H., & Bauman, M. D. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.035 · Cited by 136 · see citing works
Prenatal maternal mood is associated with altered diurnal cortisol in adolescence
O’Donnell, K. J., Glover, V. A. S., Jenkins, J., Browne, D. T., Ben‐Shlomo, Y., Golding, J., & O’Connor, T. G. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.01.008 · Cited by 136 · see citing works
Stanton, A. L., Lobel, M., Sears, S. R., & DeLuca, R. S. (2002) · Journal of Consulting and Clinical Psychology · doi:10.1037//0022-006x.70.3.751 · Cited by 125 · see citing works
Egliston, K.-A., McMahon, C. A., & Austin, M. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.10.003 · Cited by 123 · see citing works
Effects of maternal prenatal stress on offspring development: a commentary
Lazinski, M. J., Shea, A. K., & Steiner, M. S. (2008) · Archives of Women s Mental Health · doi:10.1007/s00737-008-0035-4 · Cited by 120 · see citing works
Childbirth and mental disorders
Leight, K. L., Fitelson, E. M., Weston, C. A., & Wisner, K. L. (2010) · International Review of Psychiatry · doi:10.3109/09540261.2010.514600 · Cited by 115 · see citing works
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Li, J., Vestergaard, M., Obel, C., Christensen, J., Precht, D. H., Lu, M., & Olsen, J. (2009) · PEDIATRICS · doi:10.1542/peds.2008-1734 · Cited by 111 · see citing works
Antenatal maternal anxiety is linked with atypical handedness in the child
Glover, V. A. S., O’Connor, T. G., Heron, J., & Golding, J. (2004) · Early Human Development · doi:10.1016/j.earlhumdev.2004.04.012 · Cited by 110 · see citing works
Behavioral perinatology: Biobehavioral processes in human fetal development
Wadhwa, P. D., Glynn, L. M., Hobel, C. J., Garite, T. J., Porto, M., Chicz-DeMet, A., Wiglesworth, A., & Sandman, C. A. (2002) · Regulatory Peptides · doi:10.1016/s0167-0115(02)00102-7 · Cited by 110 · see citing works
The evolutionary paradox and the missing heritability of schizophrenia
van Dongen, J., & Boomsma, D. I. (2013) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32135 · Cited by 106 · see citing works
Robinson, M., Mattes, E., Oddy, W. H., Pennell, C. E., van Eekelen, A., McLean, N. J., Jacoby, P., Li, J., de Klerk, N. H., Zubrick, S. R., et al. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000241 · Cited by 103 · see citing works
Mastorci, F., Vicentini, M., Viltart, O., Manghi, M., Graiani, G., Quaini, F., Meerlo, P., Nalivaiko, E., Maccari, S., & Sgoifo, A. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.001 · Cited by 99 · see citing works
Meyer, J. S., & Hamel, A. F. (2014) · ILAR Journal · doi:10.1093/ilar/ilu023 · Cited by 96 · see citing works
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2004) · Stress · doi:10.1080/10253890500044521 · Cited by 96 · see citing works
Wurmser, H., Rieger, M., Domogalla, C., Kahnt, A., Buchwald, J., Kowatsch, M., Kuehnert, N., Buske-Kirschbaum, A., Papoušek, M., Pirke, K., et al. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2005.09.016 · Cited by 95 · see citing works
Pryce, C. R., Aubert, Y., Maier, C., Pearce, P. C., & Fuchs, E. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1989-2 · Cited by 94 · see citing works
The hidden costs of terrorism: The effects on health at birth
Quintana‐Domeque, C., & Ródenas-Serrano, P. (2017) · Journal of Health Economics · doi:10.1016/j.jhealeco.2017.08.006 · Cited by 95 · see citing works
Prenatal stress alters cardiovascular responses in adult rats
Igosheva, N., Klimova, O. A., Анищенко, Т. Г., & Glover, V. A. S. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.056911 · Cited by 92 · see citing works
Prenatal maternal stress affects motor function in 5½‐year‐old children: Project Ice Storm
Cao, X., Laplante, D. P., Brunet, A., Ciampi, A., & King, S. (2012) · Developmental Psychobiology · doi:10.1002/dev.21085 · Cited by 92 · see citing works
Pain and stress in the human fetus
Smith, R. P., Gitau, R., Glover, V. A. S., & Fisk, N. M. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00441-3 · Cited by 91 · see citing works
Hurricane Katrina-Related Maternal Stress, Maternal Mental Health, and Early Infant Temperament
Tees, M. T., Harville, E. W., Xiong, X., Buekens, P. M., Pridjian, G. C., & Elkind-Hirsch, K. E. (2009) · Maternal and Child Health Journal · doi:10.1007/s10995-009-0486-x · Cited by 87 · see citing works
Chernobyl exposure as stressor during pregnancy and behaviour in adolescent offspring
Huizink, A. C., Dick, D. M., Sihvola, E., Pulkkinen, L., Rose, R. J., & Kaprio, J. A. (2007) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2007.01050.x · Cited by 86 · see citing works
First-Trimester Working Conditions and Birthweight: A Prospective Cohort Study
Vrijkotte, T. G. M., van der Wal, M. F., van Eijsden, M., & Bonsel, G. J. (2009) · American Journal of Public Health · doi:10.2105/ajph.2008.138412 · Cited by 83 · see citing works
Prenatal Stress and Immune Recognition of Self and Nonself in the Primate Neonate
Coe, C. L., Lubach, G. R., & Karaszewski, J. W. (1999) · Neonatology · doi:10.1159/000014172 · Cited by 82 · see citing works
Self-citationDoes prenatal stress affect the motoric development of rat pups?
Patin, V., Vincent, A., Lordi, B., & Caston, J. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.12.008 · Cited by 77 · see citing works
Environmental enrichment for primates in laboratories
Buchanan‐Smith, H. M. (2011) · Advances in science and research · doi:10.5194/asr-5-41-2010 · Cited by 73 · see citing works
Behavioural effects of fetal antidepressant exposure in a Norwegian cohort of discordant siblings
Brandlistuen, R. E., Ystrøm, E., Eberhard‐Gran, M., Nulman, I., Koren, G., & Nordeng, H. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyv030 · Cited by 72 · see citing works
Costa, L. G., Steardo, L., & Cuomo, V. (2004) · Pharmacological Reviews · doi:10.1124/pr.56.1.5 · Cited by 73 · see citing works
Sandman, C. A., Glynn, L. M., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. (2003) · Developmental Neuroscience · doi:10.1159/000071467 · Cited by 73 · see citing works
Neurobehavioral development of common marmoset monkeys
SCHULTZ‐DARKEN, N. J., Braun, K. M., & Emborg, M. E. (2015) · Developmental Psychobiology · doi:10.1002/dev.21360 · Cited by 71 · see citing works
The Impact of Corticosteroids on the Developing Animal
Edwards, H. E., & Burnham, W. M. (2001) · Pediatric Research · doi:10.1203/00006450-200110000-00003 · Cited by 71 · see citing works
Maternal sensitivity moderates the impact of prenatal anxiety disorder on infant mental development
Grant, K., McMahon, C. A., Reilly, N. M., & Austin, M. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2010.07.004 · Cited by 70 · see citing works
Kranendonk, G., van der Mheen, H., Fillerup, M., & Hopster, H. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-074 · Cited by 70 · see citing works
Armed conflict and birth weight
Le, K. T., & Nguyen, M. (2020) · Economics & Human Biology · doi:10.1016/j.ehb.2020.100921 · Cited by 69 · see citing works
Igarashi, T. (2013) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2012.0103 · Cited by 69 · see citing works
Schneider, M. L., Moore, C. F., Gajewski, L. L., Larson, J. A., Roberts, A. D., Converse, A. K., & DeJesus, O. T. (2008) · Child Development · doi:10.1111/j.1467-8624.2007.01113.x · Cited by 69 · see citing works
Self-citationKranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., Wiegant, V. M., & Taverne, M. A. M. (2005) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2005.07.001 · Cited by 67 · see citing works
Relation between Prenatal Maternal Mood and Anxiety and Neonatal Health
Misri, S. K., Oberlander, T. F., Fairbrother, N., Carter, D., Ryan, D. M., Kuan, A. J., & Reebye, P. N. (2004) · The Canadian Journal of Psychiatry · doi:10.1177/070674370404901006 · Cited by 68 · see citing works
Suzumori, N., Ebara, T., Matsuki, T., Yamada, Y., Kato, S., Omori, T., Saitoh, S., Kamijima, M., Sugiura‐Ogasawara, M., & the Japan Environment & Children’s Study Group (2019) · Birth · doi:10.1111/birt.12463 · Cited by 67 · see citing works
Neuraxial Labor Analgesia for Vaginal Delivery and Its Effects on Childhood Learning Disabilities
Flick, R. P., Kunmoo, L., Hofer, R. E., Beinborn, C. W., Hambel, E. M., Klein, M. K., Gunn, P. W., Wilder, R. T., Katusic, S. K., Schroeder, D. R., et al. (2010) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e3181f2ecdd · Cited by 65 · see citing works
Doyle, C., Werner, E. A., Feng, T., Lee, S., Altemus, M. M., Isler, J. R., & Monk, C. E. (2015) · Developmental Psychobiology · doi:10.1002/dev.21317 · Cited by 63 · see citing works
Culot, L., Lledo-Ferrer, Y., Hölscher, O., Lazo, F. J. J. M., Huynen, M., & Heymann, E. W. (2011) · Primates · doi:10.1007/s10329-011-0238-6 · Cited by 63 · see citing works
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., & Taverne, M. A. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.008 · Cited by 63 · see citing works
Prenatal stress decreases spatial learning and memory retrieval of the adult male offspring of rats
Modir, F., Salmani, M. E., Goudarzi, I., Lashkarboluki, T., & Abrari, K. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.040 · Cited by 57 · see citing works
Antidepressants during pregnancy and lactation: Defining exposure and treatment issues
Newport, D. J., Wilcox, M. M., & Stowe, Z. N. (2001) · Seminars in Perinatology · doi:10.1053/sper.2001.24901 · Cited by 56 · see citing works
Schneider, M. L., Moore, C. F., & Becker, E. F. (2001) · Alcoholism Clinical and Experimental Research · doi:10.1097/00000374-200108000-00021 · Cited by 56 · see citing works
Self-citationAlkon, A., Boyce, W. T., Tran, L., Harley, K. G., Neuhaus, J. M., & Eskenazi, B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086283 · Cited by 53 · see citing works
van Batenburg‐Eddes, T., de Groot, L., Huizink, A. C., Steegers, E. A. P., Albert Hofman, D., Jaddoe, V. W. V., Verhulst, F. C., & Tiemeier, H. W. (2009) · Developmental Neuropsychology · doi:10.1080/87565640902964508 · Cited by 54 · see citing works
Coe, C. L., & Crispen, H. R. (2000) · Health Psychology · doi:10.1037/0278-6133.19.6.554 · Cited by 54 · see citing works
Pesonen, A., Räikkönen, K., Strandberg, T. E., & Järvenpää, A. (2004) · Infant Behavior and Development · doi:10.1016/j.infbeh.2004.09.001 · Cited by 54 · see citing works
Stress and Mood Disorders During Pregnancy: Implications for Child Development
Monk, C. E. (2001) · Psychiatric Quarterly · doi:10.1023/a:1010393316106 · Cited by 52 · see citing works
- Authors
- Schneider, M. L., Roughton, E. C., Koehler, A. J., & Lubach, G. R.
- Affiliations
- University of Wisconsin–Madison (US)
- ORCID
- Lubach, Gabriele R
- Venue
- Child Development
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-03-01
- Volume
- 70
- Issue
- 2
- Pages
- 263-274
- ISSN
- 0009-3920 (ISSN-L)
- 1467-8624
- OpenAlex
- W1991706811
- Cited by
- 267
- References
- 50
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 11 · 2018: 10 · 2017: 5 · 2016: 7 · 2015: 13 · 2014: 12 · 2013: 12 · 2012: 21
- FWCI
- 12.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Child Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r03mh048417-02)
- U.S. Public Health Service (MCJ-009102)
- National Institute on Alcohol Abuse and Alcoholism (AA10079, R01AA010079)
- National Institute of Mental Health (MH48417)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal stress, rhesus monkeys, infant growth, neurobehavioral development, attention, neuromotor development, early pregnancy, maternal stress, maternal separation
- MeSH terms
- Animals, Animals, Newborn, Animals, Suckling, Birth Weight, Developmental Disabilities, Female, Handling, Psychological, Hydrocortisone, Macaca mulatta, Male, Motor Skills, Orientation, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Maternal Exposure
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