Skip to main content Accessibility help
×
Home

Second-trimester maternal distress increases the risk of small for gestational age

  • A. S. Khashan (a1), C. Everard (a1), L. M. E. McCowan (a2), G. Dekker (a3), R. Moss-Morris (a4), P. N. Baker (a5), L. Poston (a6), J. J. Walker (a7) and L. C. Kenny (a1)...

Abstract

Background

The effect of prenatal distress on the risk of a small for gestational age (SGA) infant is uncertain. We have addressed the influences of prenatal stress, anxiety and depression on the risk of SGA. We also examined the effects of infant sex and timing of distress during pregnancy on any observed associations.

Method

The study population comprised 5606 healthy nulliparous pregnant women who participated in the international prospective Screening for Obstetric and Pregnancy Endpoints (SCOPE) study. Women completed the Perceived Stress Scale (PSS), the short form of the Spielberger State–Trait Anxiety Inventory (STAI) and the Edinburgh Postnatal Depression Scale (EPDS) at 15 ± 1 and 20 ± 1 weeks' gestation. SGA was defined as birthweight below the 10th customized percentile. Logistic regression was used for data analysis, adjusting for several potential confounders such as maternal age, body mass index (BMI), smoking, socio-economic status and physical exercise.

Results

The risk of SGA was increased in relation to mild [adjusted odds ratio (aOR) 1.35, 95% confidence interval (CI) 1.07–1.71], moderate (aOR 1.26, 95% CI 1.06–1.49), high (aOR 1.45, 95% CI 1.08–1.95) and very high stress scores (aOR 1.56, 95% CI 1.03–2.37); very high anxiety score (aOR 1.45, 95% CI 1.13–1.86); and very high depression score (aOR 1.14, 95% CI 1.05–1.24) at 20 ± 1 weeks' gestation. Sensitivity analyses showed that very high anxiety and very high depression increases the risk of SGA in males but not in females whereas stress increases the risk of SGA in both males and females.

Conclusions

These findings suggest that prenatal stress, anxiety and depression measured at 20 weeks' gestation increase the risk of SGA. The effects of maternal anxiety and depression on SGA were strongest in male infants.

Copyright

Corresponding author

* Address for correspondence: A. S. Khashan, Ph.D., Department of Obstetrics and Gynaecology, Cork University Maternity Hospital, Fifth Floor, University College Cork, Cork, Ireland. (Email: a.khashan@ucc.ie)

References

Hide All
Akram, SK, Carlsson-Skwirut, C, Bhutta, ZA, Soder, O (2011). Placental IGF-I, IGFBP-1, zinc, and iron, and maternal and infant anthropometry at birth. Acta Paediatrica 100, 15041509.
Barker, DJ (1995). Fetal origins of coronary heart disease. British Medical Journal 311, 171174.
Barker, DJ, Osmond, C, Forsen, TJ, Kajantie, E, Eriksson, JG (2007). Maternal and social origins of hypertension. Hypertension 50, 565571.
Carrel, L, Willard, HF (2005). X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434, 400404.
Chang, TC, Robson, SC, Boys, RJ, Spencer, JA (1992). Prediction of the small for gestational age infant: which ultrasonic measurement is best? Obstetrics and Gynecology 80, 10301038.
Class, QA, Khashan, AS, Lichtenstein, P, Langstrom, N, D'Onofrio, BM (2013). Maternal stress and infant mortality: the importance of the preconception period. Psychological Science 24, 13091316.
Class, QA, Lichtenstein, P, Langstrom, N, D'Onofrio, BM (2011). Timing of prenatal maternal exposure to severe life events and adverse pregnancy outcomes: a population study of 2.6 million pregnancies. Psychosomatic Medicine 73, 234241.
Cohen, S, Kamarck, T, Mermelstein, R (1983). A global measure of perceived stress. Journal of Health and Social Behaviour 24, 385396.
Cox, JL, Chapman, G, Murray, D, Jones, P (1996). Validation of the Edinburgh Postnatal Depression Scale (EPDS) in non-postnatal women. Journal of Affective Disorders 39, 185189.
Davis, EP, Waffarn, F, Uy, C, Hobel, CJ, Glynn, LM, Sandman, CA (2009). Effect of prenatal glucocorticoid treatment on size at birth among infants born at term gestation. Journal of Perinatology 29, 731737.
Diaz, R, Brown, RW, Seckl, JR (1998). Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11 beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. Journal of Neuroscience 18, 25702580.
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. Psychosomatic Medicine 68, 747753.
Galligan, JJ, Parkman, H (2007). Recent advances in understanding the role of serotonin in gastrointestinal motility and functional bowel disorders. Neurogastroenterology and Motility 19, 14.
Gardosi, J, Kady, SM, McGeown, P, Francis, A, Tonks, A (2005). Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. British Medical Journal 331, 11131117.
Glover, V, Hill, J (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiology and Behavior 106, 736740.
Godfrey, KM, Barker, DJ (2000). Fetal nutrition and adult disease. American Journal of Clinical Nutrition 71, 1344S1352S.
Grote, NK, Bridge, JA, Gavin, AR, Melville, JL, Iyengar, S, Katon, WJ (2010). A meta-analysis of depression during pregnancy and the risk of preterm birth, low birth weight, and intrauterine growth restriction. Archives of General Psychiatry 67, 10121024.
Hadlock, FP, Harrist, RB, Sharman, RS, Deter, RL, Park, SK (1985). Estimation of fetal weight with the use of head, body, and femur measurements – a prospective study. American Journal of Obstetrics and Gynecology 151, 333337.
Hedegaard, M, Henriksen, TB, Sabroe, S, Secher, NJ (1996). The relationship between psychological distress during pregnancy and birth weight for gestational age. Acta Obstetricia Gynecologica Scandinavica 75, 3239.
Henrichs, J, Schenk, JJ, Roza, SJ, van den Berg, MP, Schmidt, HG, Steegers, EA, Hofman, A, Jaddoe, VW, Verhulst, FC, Tiemeier, H (2010). Maternal psychological distress and fetal growth trajectories: the Generation R Study. Psychological Medicine 40, 633643.
Kaaij, MW, Struijk, PC, Lotgering, FK (1999). Accuracy of sonographic estimates of fetal weight in very small infants. Ultrasound in Obstetrics and Gynecology 13, 99102.
Kapoor, A, Dunn, E, Kostaki, A, Andrews, MH, Matthews, SG (2006). Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. Journal of Physiology 572, 3144.
Khashan, A, McNamee, R, Abel, K, Pedersen, M, Webb, R, Kenny, L, Mortensen, P, Baker, P (2008). Reduced infant birthweight consequent upon maternal exposure to severe life events. Psychosomatic Medicine 70, 688694.
Khashan, AS, McNamee, R, Henriksen, TB, Pedersen, MG, Kenny, LC, Abel, KM, Mortensen, PB (2011). Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. Journal of Psychiatric Research 45, 879885.
Lederman, SA, Rauh, V, Weiss, L, Stein, JL, Hoepner, LA, Becker, M, Perera, FP (2004). The effects of the World Trade Center event on birth outcomes among term deliveries at three lower Manhattan hospitals. Environmental Health Perspectives 112, 17721778.
Li, J, Olsen, J, Vestergaard, M, Obel, C (2010). Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. European Child and Adolescent Psychiatry 19, 747753.
Lingas, RI, Matthews, SG (2001). A short period of maternal nutrient restriction in late gestation modifies pituitary-adrenal function in adult guinea pig offspring. Neuroendocrinology 73, 302311.
Littleton, HL, Breitkopf, CR, Berenson, AB (2007). Correlates of anxiety symptoms during pregnancy and association with perinatal outcomes: a meta-analysis. American Journal of Obstetrics and Gynecology 196, 424432.
Marteau, TM, Bekker, H (1992). The development of a six-item short-form of the state scale of the Spielberger State-Trait Anxiety Inventory (STAI). British Journal of Clinical Psychology 31, 301306.
McCowan, LM, Roberts, CT, Dekker, GA, Taylor, RS, Chan, EH, Kenny, LC, Baker, PN, Moss-Morris, R, Chappell, LC, North, RA (2010). Risk factors for small-for-gestational-age infants by customised birthweight centiles: data from an international prospective cohort study. British Journal of Obstetrics and Gynaecology 117, 15991607.
McIntire, DD, Bloom, SL, Casey, BM, Leveno, KJ (1999). Birth weight in relation to morbidity and mortality among newborn infants. New England Journal of Medicine 340, 12341238.
Mueller, BR, Bale, TL (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience 28, 90559065.
Nordentoft, M, Lou, HC, Hansen, D, Nim, J, Pryds, O, Rubin, P, Hemmingsen, R (1996). Intrauterine growth retardation and premature delivery: the influence of maternal smoking and psychosocial factors. American Journal of Public Health 86, 347354.
North, RA, McCowan, LM, Dekker, GA, Poston, L, Chan, EH, Stewart, AW, Black, MA, Taylor, RS, Walker, JJ, Baker, PN, Kenny, LC (2011). Clinical risk prediction for pre-eclampsia in nulliparous women: development of model in international prospective cohort. British Medical Journal 342, d1875.
Peindl, KS, Wisner, KL, Hanusa, BH (2004). Identifying depression in the first postpartum year: guidelines for office-based screening and referral. Journal of Affective Disorders 80, 3744.
Randhawa, RS (2008). The insulin-like growth factor system and fetal growth restriction. Pediatric Endocrinology Reviews 6, 235240.
Rawn, SM, Cross, JC (2008). The evolution, regulation, and function of placenta-specific genes. Annual Review of Cell and Developmental Biology 24, 159181.
Reynolds, RM (2013). Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis – 2012 Curt Richter Award Winner. Psychoneuroendocrinology 38, 111.
Rondo, PHC, Ferreira, RF, Nogueira, F, Ribeiro, MCN, Lobert, H, Artes, R (2003). Maternal psychological stress and distress as predictors of low birthweight, prematurity and intrauterine growth retardation. European Journal of Clinical Nutrition 57, 266272.
Rossant, J, Cross, JC (2001). Placental development: lessons from mouse mutants. Nature Reviews. Genetics 2, 538548.
Seckl, JR (2008). Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Progress in Brain Research 167, 1734.
Seckl, JR, Holmes, MC (2007). Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nature Clinical Practice. Endocrinology and Metabolism 3, 479488.
Stark, MJ, Wright, IM, Clifton, VL (2009). Sex-specific alterations in placental 11 beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 297, R510R514.
Stewart, PM, Murry, BA, Mason, JI (1994). Type 2 11 beta-hydroxysteroid dehydrogenase in human fetal tissues. Journal of Clinical Endocrinology and Metabolism 78, 15291532.
Stroebe, M, Schut, H, Stroebe, W (2007). Health outcomes of bereavement. Lancet 370, 19601973.
Tan, CE, Li, HJ, Zhang, XG, Zhang, H, Han, PY, An, Q, Ding, WJ, Wang, MQ (2009). The impact of the Wenchuan earthquake on birth outcomes. PloS One 4, e8200.
Weinstock, M (2011). Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: an update. Stress 14, 604613.
Welberg, LA, Seckl, JR (2001). Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology 13, 113128.
Witt, W, Cheng, E, Wisk, L, Litzelman, K, Chatterjee, D, Mandell, K, Wakeel, F (2014). Maternal stressful life events prior to conception and the impact on infant birth weight in the United States. American Journal of Public Health 104, S81S99.
Zhu, P, Tao, FB, Hao, JH, Sun, Y, Jiang, XM (2010). Prenatal life events stress: implications for preterm birth and infant birthweight. American Journal of Obstetrics and Gynecology 203, 34e134e8.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed