Prenatal Maternal Stress and the Developing Fetus and Infant: A Review of Animal Models as Related to Human Research

REFERENCES

• Alder , J. , Fink , N. , Bitzer , J. , Hosli , I. and Holzgreve , W. 2007 . Depression and anxiety during pregnancy: A risk factor for obstetric, fetal and neonatal outcome? A critical review of the literature . Journal of Maternal-Fetal and Neonatal Medicine , 20 ( 3 ) : 189 – 209 .
   PubMed Web of Science ®Google Scholar
• Bakermans-Kranenburg , M. , van IJzendoorn , M. , Mesman , J. , Alink , L. and Juffer , F. 2008 . Effects of an attachment-based intervention on daily cortisol moderated by dopamine receptor D4: A randomized control trial on 1- to 3-year-olds screened for externalizing behavior . Development and Psychopathology , 20 ( 3 ) : 805 – 820 .
   PubMed Web of Science ®Google Scholar
• Baradon , T. , Fonagy , P. , Bland , K. , Lénárd , K. and Sleed , M. 2008 . New beginnings—an experience-based program addressing the attachment relationship between mothers and their babies in prisons . Journal of Child Psychotherapy , 34 ( 2 ) : 240 – 258 .
   Web of Science ®Google Scholar
• Barker , D. 1998 . In utero programming of chronic disease . Clinical Science , 95 : 115 – 128 .
   PubMed Web of Science ®Google Scholar
• Bosch , O. , Müsch , W. , Bredewold , R. , Slattery , D. and Neumann , I. 2007 . Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring: Implications for postpartum mood disorder . Psychoneuroendocrinology , 32 ( 3 ) : 267 – 278 .
   PubMed Web of Science ®Google Scholar
• Bowlby , J. 1969 . Attachment and Loss, Vol. 1 , New York , NY : Basic Books .
   Google Scholar
• Cai , Q. , Zhu , Z. , Fan , X. , Jia , N. , Bai , Z. , Song , L. and Li , X. 2006 . The effects of prenatal stress on Ca2+ channel and K+ channel of hippocampal CA3 pyramidal neurons in rat offspring . Fen Zi Xi Bao SHeng Wu Xue Bao , 39 ( 3 ) : 223 – 228 . (Chinese: English abstract available)
   PubMedGoogle Scholar
• Caldji , C. , Tannenbaum , B. , Sharma , S. , Francis , D. , Plotsky , P. and Meaney , M. 1998 . Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat . Proceedings of the National Academy of Sciences of the United States of America , 95 : 5335 – 5340 .
   PubMed Web of Science ®Google Scholar
• Cassidy , J. and Shaver , P. 1999 . Handbook of attachment: Theory, research and clinical applications , New York , NY : Guilford .
   Google Scholar
• Christiensson , K. , Nilsson , B. , Stock , S. , Matthiesen , A. and Uvnas-Moberg , K. 1989 . Effect of nipple stimulation on uterine activity and on plasma levels of oxytocin in full term, healthy, pregnant women . Acta Obstetricia et Gynecologica Scandinavica , 68 ( 3 ) : 205 – 210 .
   PubMed Web of Science ®Google Scholar
• Cicchetti , D. and Gunnar , M. 2008 . Editorial: Integrating biological measures into the design and evaluation of preventive interventions . Development and Psychopathology , 20 ( 3 ) : 737 – 743 .
   PubMed Web of Science ®Google Scholar
• Coe , C. and Lubach , G. 2000 . Prenatal influences on neuroimmune set points in infancy . Annals of the New York Academy of Sciences , 917 : 468 – 477 .
   PubMed Web of Science ®Google Scholar
• Dickerson , P. , Lally , B. , Gunnel , E. , Birkle , D. and Salm , A. 2005 . Early emergence of increased fearful behavior in prenatally stressed rats . Physiology & Behavior , 86 ( 4 ) : 586 – 593 .
   PubMed Web of Science ®Google Scholar
• Dozier , M. , Peloso , E. , Lewis , E. , Laurenceau , J. and Levine , S. 2008 . Effects of an attachment-based intervention of the cortisol production of infants and toddlers in foster care . Development and Psychopathology , 20 ( 3 ) : 845 – 859 .
   PubMed Web of Science ®Google Scholar
• Drake , A. , Tang , J. and Nyirenda , M. 2007 . Mechanisms underlying the role of glucocorticoids in the early life programming of adult disease . Clinical Science (Lond) , 113 ( 5 ) : 219 – 232 .
   PubMed Web of Science ®Google Scholar
• Dunn , E. , Owen , D. , Kostaki , A. and Matthews , S. 2005 . Prenatal glucocorticoid exposure affects reproductive capacity and adrenocortical function in mature female guinea pig offspring . Pediatric Research , 58 : 0 – 008 . (Abstract)
   Web of Science ®Google Scholar
• Emack , J. , Kostaki , A. , Walker , C. and Matthews , S. 2008 . Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring . Hormones and Behavior , 54 ( 4 ) : 514 – 520 .
   PubMed Web of Science ®Google Scholar
• Feldman , R. and Eidelman , A. 2009 . Biological and environmental initial conditions shape the trajectories of cognitive and social-emotional development across the first years of life . Developmental Science , 12 ( 1 ) : 194 – 200 .
   PubMed Web of Science ®Google Scholar
• Feldman , R. , Weller , A. , Zagoory-Sharon , O. and Levine , A. 2007 . Evidence for a neuroendocrinological foundation of human affiliation: Plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding . Psychological Science , 18 ( 11 ) : 965 – 970 .
   PubMed Web of Science ®Google Scholar
• Francis , D. , Champagne , F. , Liu , D. and Meaney , M. 1999 . “ Maternal care, gene expression, and the development of individual differences in stress reactivity ” . In Socioeconomic status and health in industrial nations: Social, psychological, and biological pathways , Edited by: Adler , N. , Marmot , M. , McEwen , B. and Stewart , J. 66 – 84 . New York , NY : New York Academy of Sciences .
   Google Scholar
• Francis , D. , Champagne , F. and Meaney , M. 2000 . Variations in maternal behavior are associated with differences in oxytocin receptor levels in the rat . Journal of Neuroendocrinology , 12 ( 12 ) : 1145 – 1148 .
   PubMed Web of Science ®Google Scholar
• Francis , D. , Diorio , J. , Liu , D. and Meaney , M. 1999 . Nongenomic transmission across generations of maternal behavior and stress responses in the rat . Science , 286 ( 5442 ) : 1155 – 1158 .
   PubMed Web of Science ®Google Scholar
• Fumagalli , F. , Bedogni , F. , Perez , J. , Racagni , G. and Riva , M. 2004 . Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress . European Journal of Neuroscience , 20 ( 5 ) : 1348 – 1354 .
   PubMed Web of Science ®Google Scholar
• Gwynne , K. , Blick , B. and Duffy , G. 2009 . Pilot evaluation of an early intervention programme for children at risk . Journal of Paediatrics and Child Health , 45 ( 3 ) : 118 – 124 .
   PubMed Web of Science ®Google Scholar
• Hane , A. and Fox , N. 2006 . Ordinary variations in maternal caregiving influence human infants’ stress reactivity . Psychological Science , 17 ( 6 ) : 550 – 556 .
   PubMed Web of Science ®Google Scholar
• Harding , R. and Bocking , A. 2001 . Fetal growth and development , Cambridge , MA : Cambridge University Press .
   Google Scholar
• Harper , L. 2005 . Epigenetic inheritance and the intergenerational transfer of experience . Psychological Bulletin , 131 ( 3 ) : 340 – 360 .
   PubMed Web of Science ®Google Scholar
• Hofer , M. 2006 . Psychobiological roots of early attachment . Current Directions in Psychological Science , 15 ( 2 ) : 84 – 88 .
   Web of Science ®Google Scholar
• Hofer , M. 1994 . Early relationships as regulators of infant physiology and behavior . Acta Paediatrica , 397 ( Suppl ) : 9 – 18 .
   Web of Science ®Google Scholar
• Huizink , A. , Mulder , E. and Buitelaar , J. 2004 . Prenatal stress and risk for psychopathology: Specific effects or induction of general susceptibility? . Psychological Bulletin , 130 ( 1 ) : 115 – 142 .
   PubMed Web of Science ®Google Scholar
• Juffer , F. , Bakermans-Kranenburg , M. and van IJzendoorn , M. 2008 . Promoting positive parenting: An attachment-based intervention , New York , NY : Taylor & Francis .
   Google Scholar
• Kapoor , A. , Dunn , E. , Kostaki , A. , Andrews , M. and Matthews , S. 2006 . Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids . Journal of Physiology , 572 ( 1 ) : 31 – 44 .
   PubMed Web of Science ®Google Scholar
• Kapoor , A. , Petropoulos , S. and Matthews , S. 2008 . Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids . Brain Research Reviews , 57 ( 2 ) : 586 – 595 .
   PubMedGoogle Scholar
• Keverne , E. and Kendrick , K. 1994 . Maternal behaviour in sheep and its neuroendocrine regulation . Acta Paediatric Supplement , 397 : 47 – 56 .
   PubMedGoogle Scholar
• Kofman , O. 2002 . The role of prenatal stress in the etiology of developmental behavioral disorders . Neuroscience & Biobehavioral Reviews , 26 ( 4 ) : 457 – 470 .
   PubMed Web of Science ®Google Scholar
• Kostaki , A. , Owen , D. , Li , D. and Matthews , S. 2005 . Transgenerational effects of prenatal glucocorticoid exposure on growth, endocrine function and behaviour in the guinea pig . Pediatric Research , 58 : P1 – P052 . (Abstract)
   PubMed Web of Science ®Google Scholar
• Kraszpulski , M. , Dickerson , P. and Salm , A. 2006 . Prenatal stress affects the developmental trajectory of the rat amygdala . Stress: The International Journal on the Biology of Stress , 9 ( 2 ) : 85 – 95 .
   PubMed Web of Science ®Google Scholar
• Ladd , C. , Huot , R. , Thrivikraman , K. , Nemeroff , C. , Meaney , M. and Plotsky , P. 2000 . Long-term behavioral and neuroendocrine adaptations to adverse early experience . Progress in Brain Research , 122 : 81 – 103 .
   PubMed Web of Science ®Google Scholar
• Ladd , C. , Huot , R. , Thrivikraman , K. , Nemeroff , C. and Plotsky , P. 2004 . Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor MRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation . Biological Psychiatry , 55 ( 4 ) : 367 – 375 .
   PubMed Web of Science ®Google Scholar
• Lephard , E. , Watson , M. , Jacobson , N. , Rhees , R. and Ladel , D. 1997 . Calbindin-D28K is regulated by adrenal steroids in the hypothalamic tissue during prenatal development . Developmental Brain Research , 100 : 117 – 120 .
   PubMedGoogle Scholar
• Liu , D. , Diorio , J. , Tannenbaum , B. , Caldji , C. , Francis , D. , Freedman , A. … and Meaney , M. J. 1997 . Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress . Science , 277 : 1659 – 1662 .
   PubMed Web of Science ®Google Scholar
• Lumey , L. , Ravelli , A. , Wiessing , L. , Koppe , J. , Treffers , P. and Stein , Z. 1993 . The Dutch famine birth cohort study: Design, validation of exposure, and selected characteristics of subjects after 43 years follow-up . Paediatric and Perinatal Epidemiology , 7 ( 4 ) : 354 – 367 .
   PubMedGoogle Scholar
• Lupien , S. and Lepage , M. 2001 . Stress, memory, and the hippocampus: Can't live with it, can't live without it . Behavioral Brain Research , 127 : 137 – 158 .
   PubMed Web of Science ®Google Scholar
• Mayers , H. , Hager-Budny , M. and Buckner , E. 2008 . The chances for children teen parent-infant project: Results of a pilot intervention for teen mothers and their infants in inner city high schools . Infant Mental Health Journal , 29 ( 4 ) : 320 – 342 .
   PubMed Web of Science ®Google Scholar
• Manjarrez , G. , Cisneros , I. , Herrera , R. , Vazquez , F. , Robles , A. and Hernandez , J. 2005 . Prenatal impairment of brain serotonergic transmission in infants . Journal of Pediatrics , 147 ( 5 ) : 592 – 596 .
   PubMed Web of Science ®Google Scholar
• McEwen , B. 1998 . Stress, adaptation, and disease: Allostasis and allostatic load . Annals of the New York Academy of Science , 840 : 33 – 44 .
   PubMed Web of Science ®Google Scholar
• Mrazek , P. and Haggert , R. 1994 . Reducing risks for mental disorders: Frontiers for prevention research , Washington , DC : National Academy Press .
   Google Scholar
• Nathanielsz , P. and Padmanabhan , V. 2006 . Developmental origins of health and disease . Journal of Physiology , 572 ( 1 ) : 3 – 4 .
   PubMed Web of Science ®Google Scholar
• Ogden , P. , Minton , K. and Pain , C. 2006 . Trauma and the body: A sensorimotor approach to psychotherapy , New York , NY : Norton .
   Google Scholar
• Oppenheim , D. and Goldsmith , D. 2007 . Attachment theory in clinical work with children: Bridging the gap between research and practice , New York , NY : Guilford Press .
   Google Scholar
• Palleres , M. , Scacchi Bernasconi , P. , Feleder , C. and Cutrera , R. 2007 . Effects of prenatal stress on motor performance and anxiety behavior in Swiss mice . Physiology & Behavior , 92 ( 5 ) : 951 – 956 .
   PubMed Web of Science ®Google Scholar
• Peleg , D. , Kennedy , C. and Hunter , S. 1998 . Intrauterine growth restriction: Identification and management . American Family Physician , 58 : 453 – 460 .
   PubMed Web of Science ®Google Scholar
• Perez-Laso , C. , Segovia , S. , Martin , J. , Ortega , E. , Gomez , F. and Del Cerro , M. 2007 . Environmental prenatal stress alters sexual dimorphism of maternal behavior in rats . Behavioral Brain Research , 187 ( 2 ) : 284 – 288 .
   PubMed Web of Science ®Google Scholar
• Pryce , C. , Bettschen , D. and Feldon , J. 2001 . Comparison of the effects of early handling and early deprivation on maternal care in the rat . Developmental Psychobiology , 38 ( 4 ) : 239 – 251 .
   PubMed Web of Science ®Google Scholar
• Roseboom , T. , Rooij , S. and Painter , R. 2006 . The Dutch famine and its long-term consequences for adult health . Early Human Development , 82 : 485 – 491 .
   PubMed Web of Science ®Google Scholar
• Sadler , L. , Slade , A. and Mayes , L. 2006 . “ Minding the baby: A mentalization-based parenting program ” . In Handbook of Mentalization-Based Treatment , Edited by: Allen , J. G. and Fonagy , P. 271 – 288 . Chichester , , UK : Wiley .
   Google Scholar
• Sapolsky , R. 2000 . Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders . Archives of General Psychiatry , 57 ( 10 ) : 925 – 935 .
   PubMed Web of Science ®Google Scholar
• Sapolsky , R. 2004 . Why zebras don't get ulcers: A guide to stress, stress-related diseases and coping , New York , NY : Holt .
   Google Scholar
• Sapolsky , R. , Krey , L. and McEwen , B. 1986 . The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis . Endocrinology Review , 7 ( 3 ) : 284 – 301 .
   PubMed Web of Science ®Google Scholar
• Santos , K. , Mazzola , T. and Carvalho , H. 2005 . The prima donna of epigenetics: The regulation of gene expression by DNA methylation . Brazilian Journal of Medical and Biological Research , 38 ( 10 ) : 1531 – 1541 .
   PubMed Web of Science ®Google Scholar
• Schneider , M. , Moore , C. , Roberts , A. and Dejesus , O. 2001 . Prenatal stress alters early neurobehavior, stress reactivity and learning in non-human primates: A brief review . Stress , 4 : 183 – 193 .
   PubMedGoogle Scholar
• Seckl , J. and Holmes , M. 2007 . Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology . Nature Clinical Practice Endocrinology & Metabolism , 3 ( 6 ) : 479 – 488 .
   PubMedGoogle Scholar
• Skinner , H. , White , D. and Birkle , D. 1999 . The effects of maternal stress on plasma corticosterone and ACTH levels in rats . Social Neuroscience Abstracts , 857
   Google Scholar
• Slade , A. , Sadler , L. , de Dios-Kenn , C. , Webb , D. , Ezepchick , J. and Mayes , L. 2005 . Minding the baby: A reflective parenting program . Psychoanalytic Study of the Child , 60 : 74 – 100 .
   PubMed Web of Science ®Google Scholar
• Son , G. , Geum , D. , Chung , S. , Kim , E. , Jo , J. , Kikm , C. … and Kim , K. 2006 . Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity . Journal of Neuroscience , 26 ( 12 ) : 3309 – 3318 .
   PubMed Web of Science ®Google Scholar
• Sroufe , L. 2005 . Attachment and development: A prospective, longitudinal study from birth to adulthood . Attachment & Human Development , 7 ( 4 ) : 349 – 367 .
   PubMed Web of Science ®Google Scholar
• Sroufe , L. , Carlson , E. , Levy , A. and Egeland , B. 1999 . Implications of attachment theory for developmental psychopathology . Development and Psychopathology , 11 ( 1 ) : 1 – 13 .
   PubMed Web of Science ®Google Scholar
• Suomi , S. J. and Levine , S. 1998 . “ Psychobiology of intergenerational effects of trauma. Evidence from animal studies ” . In International handbook of multigenerational legacies of trauma , Edited by: Danieli , Y. 623 – 637 . New York , NY : Plenum Press .
   Google Scholar
• Swain , J. , Thomas , P. , Leckman , J. and Mayes , L. 2008 . “ Parent-infant attachment systems: Neural circuits and early-life programming ” . In Mind to mind: Infant research, neuroscience and psychoanalysis , Edited by: Jurist , E. , Slade , A. and Bergner , S. 264 – 303 . New York , NY : Other Press .
   Google Scholar
• Toth , S. , Rogosch , F. and Cicchetti , D. 2008 . Attachment-theory-informed intervention and reflective functioning in depressed mothers. In Clinical applications of the adult attachment interview , 154 – 172 . New York , NY : Guilford Press .
   Google Scholar
• Uvnas-Moberg , K. 1996 . Neuroendocrinology of the mother-child interaction . Trends in Endocrinology and Metabolism , 7 ( 4 ) : 126 – 131 .
   PubMed Web of Science ®Google Scholar
• Uvnas-Moberg , K. 1997 . Physological and endocrine effects of social contact . Annals of the New York Academy of Science , 807 : 146 – 163 .
   PubMed Web of Science ®Google Scholar
• Uvnas-Moberg , K. and Winberg , J. 1989 . “ Role of sensory stimulation in the energy economy in mother and infant with particular regard to the gastrointestinal endocrine system ” . In Textbook of gastroenterology and nutrition in infancy , 2nd , Edited by: Lebenthal , E. 53 – 62 . New York , NY : Raven Press .
   Google Scholar
• Van den Hove , D. , Steinbusch , H. , Scheepens , A. , Van de Berg , W. , Kooiman , L. , Boosten , B. , Prickaerts , J. and Blanco , C. 2006 . Prenatal stress and neonatal rat brain development . Neuroscience , 137 ( 1 ) : 145 – 155 .
   PubMed Web of Science ®Google Scholar
• Vashadze , S. 2007 . Insomnia, serotonin and depression . Georgian Medical News , 150 : 22 – 24 .
   Google Scholar
• Viltart , O. and Vanbesien-Mailliot , C. 2007 . Impact of prenatal stress on neuroendocrine programming . Scientific World Journal , 7 : 1493 – 1537 .
   Google Scholar
• Wadhwa , P. 1998 . “ Prenatal stress and life-span development ” . In Encyclopedia of Mental Health , Edited by: Friedman , H. Vol. 3 , 265 – 280 . San Diego : Academic Press .
   Google Scholar
• Wadhwa , P. 2005 . Psychoneuroendocrine processes in human pregnancy influence fetal development and health . Psychoneuroendocrinology , 30 ( 8 ) : 724 – 743 .
   PubMed Web of Science ®Google Scholar
• Weinstock , M. 2001a . Alterations induced by gestational stress in brain morphology and behaviour of the offspring . Progress in Neurobiology , 65 ( 5 ) : 427 – 451 .
   PubMed Web of Science ®Google Scholar
• Weinstock , M. 2001b . Alterations induced by gestational stress in brain morphology and behaviour of the offspring . Progress in Neurobiology , 63 : 427 – 452 .
   Google Scholar
• Winberg , J. 2005 . Mother and newborn baby: Mutual regulation of physiology and behavior–a selective review . Developmental Psychobiology , 47 ( 3 ) : 217 – 229 .
   PubMed Web of Science ®Google Scholar
• Winslow , J. 2005 . Neuropeptides and non-human primate social deficits associated with pathogenic rearing experience . International Journal of Developmental Neuroscience , 23 ( 2–3 ) : 245 – 251 .
   PubMed Web of Science ®Google Scholar
• Yaka , R. , Salomon , S. , Matzner , H. and Weinstock , M. 2007 . Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats . Behavioral Brain Research , 179 ( 1 ) : 126 – 132 .
   PubMed Web of Science ®Google Scholar
• Yang , J. , Han , H. , Cao , J. , Li , L. and Xu , L. 2006 . Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring . Hippocampus , 16 ( 5 ) : 431 – 436 .
   PubMed Web of Science ®Google Scholar