Archives of Women's Mental Health

, Volume 19, Issue 5, pp 721–739

Prenatal stress and hemodynamics in pregnancy: a systematic review

  • Terri A. Levine
  • Fiona A. Alderdice
  • Ruth E. Grunau
  • Fionnuala M. McAuliffe
Review Article

Abstract

Maternal prenatal stress is associated with preterm birth, intrauterine growth restriction, and developmental delay. However, the impact of prenatal stress on hemodynamics during pregnancy remains unclear. This systematic review was conducted in order to assess the quality of the evidence available to date regarding the relationship between prenatal stress and maternal–fetal hemodynamics. The PubMed/Medline, EMBASE, PsycINFO, Maternity and Infant Care, Trip, Cochrane Library, and CINAHL databases were searched using the search terms pregnancy; stress; fetus; blood; Doppler; ultrasound. Studies were eligible for inclusion if prenatal stress was assessed with standardized measures, hemodynamics was measured with Doppler ultrasound, and methods were adequately described. A specifically designed data extraction form was used. The methodological quality of included studies was assessed using well-accepted quality appraisal guidelines. Of 2532 studies reviewed, 12 met the criteria for inclusion. Six reported that prenatal stress significantly affects maternal or fetal hemodynamics; six found no significant association between maternal stress and circulation. Significant relationships between prenatal stress and uterine artery resistance (RI) and pulsatility (PI) indices, umbilical artery RI, PI, and systolic/diastolic ratio, fetal middle cerebral artery PI, cerebroplacental ratio, and umbilical vein volume blood flow were found. To date, there is limited evidence that prenatal stress is associated with changes in circulation. More carefully designed studies with larger sample sizes, repeated assessments across gestation, tighter control for confounding factors, and measures of pregnancy-specific stress will clarify this relationship.

Keywords

Blood flow Doppler ultrasound Fetal well-being Hemodynamics Middle cerebral artery Pregnancy Pregnancy-specific stress Psychological distress Stress Umbilical artery Uterine artery 

Abbreviations

CPR

Cerebroplacental ratio

GHQ-28

General Health Questionnaire

HADS

Hospital Anxiety and Depression Scale

HAM-A

Hamilton Rating Scale for Anxiety

IES

Impact of Event Scale

K-10

Kessler Psychological Distress Scale

MCA

Middle cerebral artery

PES-Brief

Pregnancy Experiences Scale

PI

Pulsatility index

PSS

Perceived Stress Scale by Sheldon Cohen

RI

Resistance index

S/D

Systolic/diastolic ratio

STAI

State–Trait Anxiety Inventory

UA

Umbilical artery

UtA

Uterine artery

UVVBF

Umbilical vein volume blood flow

WHO-5

World Health Organization Five Well-Being Index

References

  1. Aardema MW, Saro MC, Lander M, DeWolf BT, Oosterhof H, Aardnoudse JG (2004) Second trimester Doppler ultrasound screening of the uterine arteries differentiates between subsequent normal and poor outcomes of hypertensive pregnancy: two different pathophysiological entities? Clin Sci (Lond) 106:377–382CrossRefGoogle Scholar
  2. Adamson SL, Morrow RJ, Bascom PA, Mo LY, Ritchie JW (1989) Effect of placental resistance, arterial diameter, and blood pressure on the uterine arterial velocity waveform: a computer modelling approach. Ultrasound Med Biol 15:437–442PubMedCrossRefGoogle Scholar
  3. Alderdice F, Lynn F (2011) Factor structure of the Prenatal Distress Questionnaire. Midwifery 27:553–559PubMedCrossRefGoogle Scholar
  4. Andersson L, Sundstrom-Poromaa I, Wulff M, Astrom M, Bixo M (2004) Neonatal outcome following maternal antenatal depression and anxiety: a population-based study. Am J Epidemiol 159:872–881PubMedCrossRefGoogle Scholar
  5. Arias F (1994) Accuracy of the middle-cerebral-to-umbilical-artery resistance index ratios in the prediction of neonatal outcome in patients at high risk of fetal and neonatal outcomes. Am J Obstet Gynecol 171:1541–1545PubMedCrossRefGoogle Scholar
  6. Austin M, Hadzi-Pavlovic D, Leader L, Saint K, Parker G (2005) Maternal trait anxiety, depression and life event stress in pregnancy: relationships with infant temperament. Early Hum Dev 81:183–190PubMedCrossRefGoogle Scholar
  7. Aylard PR, Gooding JH, McKenna PJ, Snaith RP (1987) A validation study of three anxiety and depression self-assessment scales. J Psychosom Res 31:261–268PubMedCrossRefGoogle Scholar
  8. Bahado-Singh RO, Kovanci E, Jeffres A, Oz U, Deren O, Copel J, Mari G (1999) The Doppler cerebroplacental ratio and perinatal outcome in intrauterine growth restriction. Am J Obstet Gynecol 180:750–756PubMedCrossRefGoogle Scholar
  9. Bailey BA (2010) Partner violence during pregnancy: prevalence, effects, screening, and management. Int J Women's Health 2:183–197CrossRefGoogle Scholar
  10. Barker DJ (1998) In utero programming of chronic disease. Clin Sci (Lond) 95:115–128CrossRefGoogle Scholar
  11. Barker DJ, Eriksson JG, Forsen T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31(6):1235–1239PubMedCrossRefGoogle Scholar
  12. Bartha JL, Comino-Delgado R, Gonzalez-Mena C, Lopez I, Arrabal J (1998) Umbilical blood flow and neonatal morphometry: a multivariate analysis. Eur J Obstet Gynecol Reprod Biol 79:27–33PubMedCrossRefGoogle Scholar
  13. Bouthoorn SH, van Lenthe FJ, Gaillard R, Hofman A, Steegers EAP, Jaddoe VWV, Raat H (2014) Socioeconomic inequalities in placental vascular resistance: a prospective cohort study. Fertil Steril 101:1367–1374.e4PubMedCrossRefGoogle Scholar
  14. Brouwers EP, van Baar AL, Pop VJ (2001) Maternal anxiety during pregnancy and subsequent infant development. Infant Behav Dev 24:95–106CrossRefGoogle Scholar
  15. Brunton PJ, Arunachalam S, Russell JA (2008) Control of neurohypophyseal hormone secretion, blood osmolality and volume in pregnancy. J Physiol Pharmacol 59(Supplement 8):27–45PubMedGoogle Scholar
  16. Buss C, Davis EP, Hobel CJ, Sandman CA (2011) Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years of age. Stress 14(6):665–676PubMedPubMedCentralCrossRefGoogle Scholar
  17. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA (2010) High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology 35:141–153PubMedPubMedCentralCrossRefGoogle Scholar
  18. Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA, Sandman CA (2012) Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci 109(20):E1312–E1319PubMedPubMedCentralCrossRefGoogle Scholar
  19. Caliskan E, Ozkan S, Cakiroglu Y, Yalcinkaya O, Polat A, Corakci A (2009) The effects of maternal anxiety prior to amniocentesis on uterine and fetal umbilical blood flow. J Turkish German Gynecol Assoc 10:162–167Google Scholar
  20. Calkins K, Devaskar SU (2011) Fetal origins of adult disease. Curr Probl Pediatr Adolesc Health Care 41(6):158–176PubMedPubMedCentralCrossRefGoogle Scholar
  21. Campbell JC (1998) Abuse during pregnancy: progress, policy, and potential. Am J Public Health 88:185–187PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMedCrossRefGoogle Scholar
  23. Cohen S, Williamson G (1988) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health: Claremont Symposium on Applied Social Psychology. Sage, Newbury Park, CA, pp 31–67Google Scholar
  24. Davis EP, Glynn LM, Dunkel-Schetter C, Hobel C, Chicz-Demet A, Sandman CA (2005) Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Dev Neurosci 27:299–305PubMedCrossRefGoogle Scholar
  25. Davis EP, Glynn LM, Dunkel-Schetter C, Hobel C, Chicz-Demet A, Sandman CA (2007) Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry 46:737–746PubMedCrossRefGoogle Scholar
  26. Davis EP, Glynn LM, Waffarn F, Sandman CA (2011) Prenatal maternal stress programs infant stress regulation. J Child Psychol Psychiatry 52(2):119–129PubMedCrossRefGoogle Scholar
  27. Davis EP, Snidman N, Wadhwa P, Dunkel-Schetter C, Glynn LM, Sandman CA (2004) Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy 6:319–331CrossRefGoogle Scholar
  28. Davis EP, Sandman CA (2010) The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev 81(1):131–148PubMedPubMedCentralCrossRefGoogle Scholar
  29. Diego MA, Jones NA, Field T, Hernandez-Reif M, Schanberg S, Kuhn C, Gonzalez-Garcia A (2006) Maternal psychological distress, prenatal cortisol, and fetal weight. Psychosom Med 68:747–753PubMedCrossRefGoogle Scholar
  30. DiPietro JA, Costigan KA, Sipsma HL (2008) Continuity in self-report measures of maternal anxiety, stress, and depressive symptoms from pregnancy through two years postpartum. J Psychosom Obstetr Gynecol 29:115–124CrossRefGoogle Scholar
  31. DiPietro JA, Ghera MM, Costigan K, Hawkins M (2004) Measuring the ups and downs of pregnancy stress. J Psychosom Obstetr Gynecol 25:189–201CrossRefGoogle Scholar
  32. DiPietro JA, Hilton SC, Hawkins M, Costigan KA, Pressman EK (2002) Maternal stress and affect influence fetal neurobehavioral development. Dev Psychol 38:659–668PubMedCrossRefGoogle Scholar
  33. DiPietro JA, Novak MF, Costigan KA, Atella LD, Reusing SP (2006) Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev 77:573–587PubMedCrossRefGoogle Scholar
  34. Dole N, Savitz DA, Hertz-Picciotto I, Siega-Riz AM, McMahon MJ, Buekens P (2003) Maternal stress and preterm birth. Am J Epidemiol 157(1):14–24PubMedCrossRefGoogle Scholar
  35. Duncan AF, Watterberg KL, Nolen TL, Vohr BR, Adams-Chapman I, Das A (2012) Effect of ethnicity and race on cognitive and language testing at age 18–22 months in extremely preterm infants. J Pediatr 160(6):966–971PubMedPubMedCentralCrossRefGoogle Scholar
  36. Duvekot JJ, Peeters LL (1994) Maternal cardiovascular hemodynamic adaptation to pregnancy. Obstetr Gynecol Survey 49(Supplement 12):S1–S14CrossRefGoogle Scholar
  37. Ellman LM, Schetter CD, Hobel CJ, Chicz-Demet A, Glynn LM, Sandman CA (2008) Timing of fetal exposure to stress hormones: effects on newborn physical and neuromuscular maturation. Dev Psychobiol 50(3):232–241PubMedPubMedCentralCrossRefGoogle Scholar
  38. Entringer S, Epel ES, Lin J, Buss C, Shahbaba B, Blackburn EH, Wadhwa PD (2013) Maternal psychosocial stress during pregnancy is associated with newborn leukocyte telomere length. Am J Obstetr Gynecol 208:134.e1–134.e7CrossRefGoogle Scholar
  39. Entringer S, Buss C, Wadhwa PD (2010) Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings. Curr Opinion Endocrinol Diabetes Obes 17(6):507–516CrossRefGoogle Scholar
  40. Galjaard S, Devlieger R, Van Assche FA (2013) Fetal growth and developmental programming. J Perinat Med 41(1):101–105PubMedCrossRefGoogle Scholar
  41. Giscombe CL, Lobel M, Giscombé CL, Lobel M (2005) Explaining disproportionately high rates of adverse birth outcomes among African Americans: the impact of stress, racism, and related factors in pregnancy. Psychol Bull 131(5):662–683PubMedCrossRefGoogle Scholar
  42. Glynn LM, Schetter CD, Hobel CJ, Sandman CA, Glynn LM, Schetter CD, Sandman CA (2008) Pattern of perceived stress and anxiety in pregnancy predicts preterm birth. Health Psychol 27(1):43–51PubMedCrossRefGoogle Scholar
  43. Goldberg D (1978) Manual of the General Health Questionnaire. NFER-Nelson, WindsorGoogle Scholar
  44. Gramellini D, Folli MC, Raboni S, Vadora E, Merialdi A (1992) Cerebral–umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 74:416–420CrossRefGoogle Scholar
  45. Gurung RA, Dunkel-Schetter C, Collins N, Rini C, Hobel CJ (2005) Psychosocial predictors of prenatal anxiety. J Soc Clin Psychol 14:41–51Google Scholar
  46. Gutteling BM, de Weerth C, Willemsen-Swinkels SH, Huizink AC, Mulder EJ, Visser GH, Buitelaar JK (2005) The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry 14:41–51PubMedCrossRefGoogle Scholar
  47. Haelterman E, Qvist R, Barlow P, Alexander S (2003) Social deprivation and poor access to care as risk factors for severe pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 111:25–32PubMedCrossRefGoogle Scholar
  48. Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55PubMedCrossRefGoogle Scholar
  49. Harville EW, Savitz DA, Dole N, Herring AH, Thorp JM, Light KC (2008) Stress and placental resistance measured by Doppler ultrasound in early and mid-pregnancy. Ultrasound Obstet Gynecol 32:23–30PubMedCrossRefGoogle Scholar
  50. Hayden JA, Cote P, Bombardier C (2006) Evaluation of the quality of prognosis studies in systematic reviews. Ann Intern Med 144(6):427–437PubMedCrossRefGoogle Scholar
  51. Helbig A, Kaasen A, Malt UF, Haugen G (2011) Psychological distress after recent detection of fetal malformation: short-term effect on second-trimester uteroplacental and fetoplacental circulation. BJOG Int J Obstetr Gynecol 118:1653–1657CrossRefGoogle Scholar
  52. Helbig A, Kaasen A, Malt UF, Haugen G (2013) Does antenatal maternal psychological distress affect placental circulation in the third trimester? PLoS ONE 8(2):e57071PubMedPubMedCentralCrossRefGoogle Scholar
  53. Henrichs J, Schenk JJ, Roza SJ, van den Berg MP, Schmidt HG, Steegers EA, Tiemeier H (2010) Maternal psychological distress and fetal growth trajectories: the Generation R Study. Psychol Med 40(4):633–643PubMedCrossRefGoogle Scholar
  54. Hilmert CJ, Dominguez TP, Schetter CD, Srinivas SK, Glynn LM, Hobel CJ, Sandman CA (2014) Lifetime racism and blood pressure changes during pregnancy: implications for fetal growth. Health Psychol 33(1):43–51PubMedCrossRefGoogle Scholar
  55. Hollis B, Prefumo F, Bhide A, Ra S, Thilaganathan B (2003) First-trimester uterine artery blood flow and birth weight. Ultrasound Obstet Gynecol 22:373–376PubMedCrossRefGoogle Scholar
  56. Horowitz M, Wilner N, Alvarez W (1979) Impact of Event Scale: a measure of subjective stress. Psychosom Med 41(3):209–218PubMedCrossRefGoogle Scholar
  57. Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK (2002) Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry 41:1078–1085PubMedCrossRefGoogle Scholar
  58. Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK (2003) Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry 44(6):810–818PubMedCrossRefGoogle Scholar
  59. Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK (2004) Is pregnancy anxiety a distinctive syndrome? Early Hum Dev 79:81–91PubMedCrossRefGoogle Scholar
  60. James SA (1994) John Henryism and the health of African Americans. Cult Med Psychiatry 18:163–182PubMedCrossRefGoogle Scholar
  61. Japundzic-Zigon N (2013) Vasopressin and oxytocin in control of the cardiovascular system. Curr Neuropharmacol 11:218–230PubMedPubMedCentralCrossRefGoogle Scholar
  62. Johnson P, Stojilkovic T, Sarkar P (2001) Middle cerebral artery Doppler in severe intrauterine growth restriction. Ultrasound Obstet Gynecol 17:416–420PubMedCrossRefGoogle Scholar
  63. Kent A, Hughes P, Ormerod L, Jones G, Thilaganathan B (2002) Uterine artery resistance and anxiety in the second trimester of pregnancy. Ultrasound Obstet Gynecol 19:177–179PubMedCrossRefGoogle Scholar
  64. Kessler RC (2003) Epidemiology of women and depression. J Affect Disord 74:5–13PubMedCrossRefGoogle Scholar
  65. Kessler RC, Andrews G, Colpe LJ, Hiripi E, Mroczek DK, Normand SL, Zaslavsky AM (2002) Short screening scales to monitor population prevalences and trends in non-specific psychological distress. Psychol Med 32:959–976PubMedCrossRefGoogle Scholar
  66. King S, Laplante DP (2005) The effects of prenatal maternal stress on children’s cognitive development: Project Ice Storm. Stress 8(1):35–45PubMedCrossRefGoogle Scholar
  67. Kinsella MT, Monk C (2009) Impact of maternal stress, depression, & anxiety on fetal neurobehavioral development. Clin Obstet Gynecol 52(3):425–440PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kivlighan KT, DiPietro JA, Costigan KA, Laudenslager ML (2008) Diurnal rhythm of cortisol during late pregnancy: associations with maternal psychological well-being and fetal growth. Psychoneuroendocrinology 33(9):1225–1235PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kochenour NK (1993) Doppler velocimetry in pregnancy. Seminars in Ultrasound, CT, and MRI 14:249–266PubMedCrossRefGoogle Scholar
  70. Kramer MS, Lydon J, Seguin L, Goulet L, Kahn SR, McNamara H, Platt RW (2009) Stress pathways to spontaneous preterm birth: the role of stressors, psychological distress, and stress hormones. Am J Epidemiol 169(11):1319–1326PubMedCrossRefGoogle Scholar
  71. Laplante DP, Barr RG, Brunet A, Du Fort GG, Meaney ML, Saucier J, King S (2004) Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res 56(3):400–410PubMedCrossRefGoogle Scholar
  72. Littleton H, Breitkopf C, Berenson A (2007) Correlates of anxiety symptoms during pregnancy and association with perinatal outcomes: a meta-analysis. Am J Obstet Gynecol 196:424–432PubMedCrossRefGoogle Scholar
  73. Lobel M (1994) Conceptualizations, measurement, and effects of prenatal maternal stress on birth outcomes. J Behav Med 17(3):225–272PubMedCrossRefGoogle Scholar
  74. Lobel M, Hamilton JG, Cannella DT (2008) Psychosocial perspectives on pregnancy: prenatal maternal stress and coping. Soc Personal Psychol Compass 2(4):1600–1623CrossRefGoogle Scholar
  75. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Lai M, Taylor K, Baron-Cohen S (2012) Fetal programming effects of testosterone on the reward system and behavioral approach tendencies in humans. Biol Psychiatry 72:839–847PubMedPubMedCentralCrossRefGoogle Scholar
  76. Maina G, Saracco P, Giolito MR, Danelon D, Bogetto F, Todros T (2008) Impact of maternal psychological distress on fetal weight, prematurity and intrauterine growth retardation. J Affect Disord 111(2–3):214–220PubMedCrossRefGoogle Scholar
  77. McFarlane J, Soeken K, Wiist WH (2000) An evaluation of interventions to decrease intimate partner violence in pregnant women. Public Health Nurs 17(6):443–451PubMedCrossRefGoogle Scholar
  78. Mendelson T, DiPietro JA, Costigan KA, Chen P, Henderson J (2011) Associations of maternal psychological factors on umbilical and uterine blood flow. J Psychosom Obstetr Gynecol 32(1):3–9CrossRefGoogle Scholar
  79. Monk C, Newport DJ, Korotkin JH, Long Q, Knight B, Stowe ZN (2012) Uterine blood flow in a psychiatric population: impact of maternal depression, anxiety, and psychotropic medication. Biol Psychiatry 72:483–490PubMedPubMedCentralCrossRefGoogle Scholar
  80. Moser K, Li L, Power C (2003) Social inequalities in low birth weight in England and Wales: trends and implications for future population health. J Epidemiol Community Health 57:687–691PubMedPubMedCentralCrossRefGoogle Scholar
  81. Niederhofer H, Reiter A (2004) Prenatal maternal stress, prenatal fetal movements, and perinatal temperament factors influence behaviour and school marks at the age of 6 years. Fetal Diagn Ther 19:160–162PubMedCrossRefGoogle Scholar
  82. O’Connor TG, Heron J, Golding J, Glover V (2003) Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J Child Psychol Psychiatry 44(7):1025–1036PubMedCrossRefGoogle Scholar
  83. Odibo AO, Riddick C, Pare E, Stamilio DM, Macones GA (2005) Cerebroplacental Doppler ratio and adverse perinatal outcomes in intrauterine growth restriction. J Ultrasound Med 24(9):1223–1228PubMedGoogle Scholar
  84. Peacock JL, Bland JM, Anderson HR (1995) Preterm delivery: effects of socioeconomic factors, psychological stress, smoking, alcohol, and caffeine. Br Med J 311:531–535CrossRefGoogle Scholar
  85. Perkin M, Bland J, Peacock J, Anderson H (1993) The effect of anxiety and depression during pregnancy on obstetric complications. Br J Obstet Gynaecol 100:629–634PubMedCrossRefGoogle Scholar
  86. Qiu A, Rifkin-Graboi A, Chen H, Chong Y, Kwek K, Gluckman PD, Meaney MJ (2013) Maternal anxiety and infants’ hippocampal development: timing matters. Transl Psychiatry 3, e306PubMedPubMedCentralCrossRefGoogle Scholar
  87. Raum E, Arabin B, Schlaud M, Walter U, Schwartz FW (2001) The impact of maternal education on intrauterine growth: a comparison of former West and East Germany. Int J Epidemiol 30:81–87PubMedCrossRefGoogle Scholar
  88. Roesch SC, Dunkel-Schetter C, Woo G, Hobel CJ (2004) Modeling the types and timing of stress in pregnancy. Anxiety Stress Coping 17(1):87–102CrossRefGoogle Scholar
  89. Rondo PH, Ferreira RF, Nogueira F, Ribeiro MC, Lobert H, Artes R (2003) Maternal psychological stress and distress as predictors of low birth weight, prematurity, and intrauterine growth restriction. Eur J Clin Nutr 57:266–272PubMedCrossRefGoogle Scholar
  90. Roos A, Geerts L, Koen N, Faure SC, Vythilingum B, Stein DJ (2015) Psychosocial predictors of fetoplacental blood flow during pregnancy. Compr Psychiatry 57:125–131PubMedCrossRefGoogle Scholar
  91. Ross MG, Beall MH (2008) Adult sequelae of intrauterine growth restriction. Semin Perinatol 32(3):213–218PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sandman CA, Davis EP, Buss C, Glynn LM (2012) Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 95(1):7–21PubMedCrossRefGoogle Scholar
  93. Sandman CA, Glynn L, Dunkel-Schetter C, Wadhwa P, Garite T, Chicz-DeMet A, Hobel C (2006) Elevated maternal cortisol early in pregnancy predicts third trimester levels of placental corticotropin releasing hormone (CRH): priming the placental clock. Peptides 27:1457–1463PubMedCrossRefGoogle Scholar
  94. Sandman CA, Wadhwa PD, Chicz-DeMet A, Dunkel-Schetter C, Porto M (1997) Maternal stress, HPA activity, and fetal/infant outcome. Ann N Y Acad Sci 814:266–275Google Scholar
  95. Sarason IG, Johnson JH, Siegel JM (1978) Assessing the impact of life changes: development of the life experiences survey. J Consult Clin Psychol 46:932–946PubMedCrossRefGoogle Scholar
  96. Scheyer K, Urizar GG (2016) Altered stress patterns and increased risk for postpartum depression among low-income pregnant women. Arch Womens Ment Health 19:3017–328Google Scholar
  97. Silva LM, Coolman M, Steegers EA, Jaddoe VW, Moll HA, Hofman A, Raat H (2008) Low socioeconomic status is a risk factor for preeclampsia: the Generation R Study. J Hypertens 26:1200–1208PubMedCrossRefGoogle Scholar
  98. Silva LM, Jansen PW, Steegers EA, Jaddoe VW, Arends LR, Tiemeier H, Raat H (2010) Mother's educational level and fetal growth: the genesis of health inequalities. Int J Epidemiol 39:1250–1261PubMedCrossRefGoogle Scholar
  99. Sjostrom K, Valentin L, Thelin T, Marsal K (1997) Maternal anxiety in late pregnancy and fetal hemodynamics. Eur J Obstet Gynecol Reprod Biol 74:149–155PubMedCrossRefGoogle Scholar
  100. Spielberger CD (1983) Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press, Palo AltoGoogle Scholar
  101. Spies G, Stein DJ, Roos A, Faure SC, Mostert J, Seedat S, Vythilingum B (2009) Validity of the Kessler 10 (K-10) in detecting DSM-IV defined mood and anxiety disorders among pregnant women. Arch Womens Ment Health 12:69–74PubMedCrossRefGoogle Scholar
  102. Teixeira JM, Fisk NM, Glover V (1999) Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study. Br Med J 318:153–157CrossRefGoogle Scholar
  103. van den Bergh BR, Mennes M, Oosterlaan J, Stevens V, Stiers P, Marcoen A, Lagae L (2005) High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehavioural Rev 29:259–269CrossRefGoogle Scholar
  104. van den Bergh BR, van Calster B, Smits T, van Huffel S, Lagae L (2008) Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33:536–545PubMedCrossRefGoogle Scholar
  105. Vythilingum B, Geerts L, Fincham D, Roos A, Faure S, Jonkers J, Stein DJ (2010) Association between antenatal distress and uterine artery pulsatility index. Archiv Women's Mental Health 13:359–364CrossRefGoogle Scholar
  106. Wadhwa PD, Entringer S, Buss C, Lu MC (2011) The contribution of maternal stress to preterm birth: issues and considerations. Clin Perinatol 38:351–384PubMedPubMedCentralCrossRefGoogle Scholar
  107. Wadhwa PD, Sandman CA, Porto M, Dunkel-Schetter C, Garite TJ (1993) The association between prenatal stress and infant birth weight and gestational age at birth: a prospective investigation. Am J Obstetr Gynecol 169(4):858–865CrossRefGoogle Scholar
  108. Wadhwa PD, Garite TJ, Porto M, Glynn L, Chicz-DeMet A, Dunkel-Schetter C, Sandman CA (2004) Placental corticotropin-releasing hormone (CRH), spontaneous preterm birth, and fetal growth restriction: a prospective investigation. Am J Obstet Gynecol 191(4):1063–1069PubMedCrossRefGoogle Scholar
  109. Wilkinson MJB, Barczak P (1988) Psychiatric screening in general practice, comparison of the General Health Questionnaire and the Hospital Anxiety and Depression Scale. J Royal College Gen Pract 38:311–313Google Scholar
  110. Winn N, Records K, Rice M (2003) The relationship between abuse, sexually transmitted diseases, and group B streptococcus in childbearing women. Am J Matern Child Nurs 28(2):106–110CrossRefGoogle Scholar
  111. Wisborg K, Barklin A, Hedegaard M, Henriksen TB (2008) Psychological stress during pregnancy and stillbirth: prospective study. BJOG Int J Obstetr Gynecol 115:882–885CrossRefGoogle Scholar
  112. Wright RJ, Visness CM, Calatroni A, Grayson MH, Gold DR, Sandel MT, Gern JE (2010) Prenatal maternal stress and cord blood innate and adaptive cytokine responses in an inter-city cohort. Am J Respir Crit Care Med 182:25–33PubMedPubMedCentralCrossRefGoogle Scholar
  113. Zigmond AS, Snaith RP (1983) The Hospital Anxiety and Depression scale. Acta Psychiatr Scand 67:361–370PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Terri A. Levine
    • 1
  • Fiona A. Alderdice
    • 1
  • Ruth E. Grunau
    • 1
    • 2
    • 3
  • Fionnuala M. McAuliffe
    • 4
  1. 1.School of Nursing and MidwiferyQueen’s University BelfastBelfastNorthern Ireland
  2. 2.Department of PediatricsUniversity of British ColumbiaVancouverCanada
  3. 3.Child and Family Research InstituteVancouverCanada
  4. 4.UCD Obstetrics and Gynaecology, School of Medicine and Medical ScienceUniversity College Dublin, National Maternity HospitalDublinNorthern Ireland

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