Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
BMC Pregnancy and Childbirth
Published in: BMC Pregnancy and Childbirth 1/2019

Open Access 01-12-2019 | Research article

Prenatal maternal stress and birth outcomes in rural Ghana: sex-specific associations

Authors: Kenneth Ayuurebobi Ae-Ngibise, Blair J. Wylie, Ellen Boamah-Kaali, Darby W. Jack, Felix Boakye Oppong, Steven N. Chillrud, Stephaney Gyaase, Seyram Kaali, Oscar Agyei, Patrick L. Kinney, Mohammed Mujtaba, Rosalind J. Wright, Kwaku Poku Asante, Alison G. Lee

Published in: BMC Pregnancy and Childbirth | Issue 1/2019

Login to get access

Abstract

Background

In developed countries, prenatal maternal stress has been associated with poor fetal growth, however this has not been evaluated in rural sub-Saharan Africa. We evaluated the effect of prenatal maternal stress on fetal growth and birth outcomes in rural Ghana.

Methods

Leveraging a prospective, rural Ghanaian birth cohort, we ascertained prenatal maternal negative life events, categorized scores as 0-2 (low stress; referent), 3-5 (moderate), and > 5 (high) among 353 pregnant women in the Kintampo North Municipality and Kintampo South District located within the middle belt of Ghana. We employed linear regression to determine associations between prenatal maternal stress and infant birth weight, head circumference, and length. We additionally examined associations between prenatal maternal stress and adverse birth outcome, including low birth weight, small for gestational age, or stillbirth. Effect modification by infant sex was examined.

Results

In all children, high prenatal maternal stress was associated with reduced birth length (β = − 0.91, p = 0.04; p-value for trend = 0.04). Among girls, moderate and high prenatal maternal stress was associated with reduced birth weight (β = − 0.16, p = 0.02; β = − 0.18, p = 0.04 respectively; p-value for trend = 0.04) and head circumference (β = − 0.66, p = 0.05; β = − 1.02, p = 0.01 respectively; p-value for trend = 0.01). In girls, high prenatal stress increased odds of any adverse birth outcome (OR 2.41, 95% CI 1.01-5.75; p for interaction = 0.04). Sex-specific analyses did not demonstrate significant effects in boys.

Conclusions

All infants, but especially girls, were vulnerable to effects of prenatal maternal stress on birth outcomes. Understanding risk factors for impaired fetal growth may help develop preventative public health strategies.

Trial registration

NCT01335490 (prospective registration).
Date of Registration: April 14, 2011.
Status of Registration: Completed.
Appendix
Available only for authorised users
Literature
1.
Katz J, Lee AC, Kozuki N, Lawn JE, Cousens S, Blencowe H, et al. Mortality risk in preterm and small-for-gestational-age infants in low-income and middle-income countries: a pooled country analysis. Lancet. 2013;382(9890):417–25.CrossRefPubMedPubMedCentral
2.
UNICEF. Low birthweight: country, regional and global estimates. In: Organization WH, editor. New York 2004.
3.
Organization WH. World health statistics 2017: monitoring health for the SDGs, Sustainable Development Goals. Geneva: World Health Organization; 2017. Contract No.: License CC BY-NC-SA 3.0 IGO
4.
Lawn JE, Cousens S, Zupan J. 4 million neonatal deaths: when? Where? Why? Lancet. 2005;365(9462):891–900.CrossRefPubMed
5.
Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;327(8489):1077–81.CrossRef
6.
Barker DJ, Godfrey KM, Osmond C, Bull A. The relation of fetal length, ponderal index and head circumference to blood pressure and the risk of hypertension in adult life. Paediatr Perinat Epidemiol. 1992;6(1):35–44.CrossRefPubMed
7.
Pike KC, Crozier SR, Lucas JS, Inskip HM, Robinson S, Roberts G, et al. Patterns of fetal and infant growth are related to atopy and wheezing disorders at age 3 years. Thorax. 2010;65(12):1099–106.CrossRefPubMed
8.
Rondó PH, Ferreira RF, Nogueira F, Ribeiro M, Lobert H, Artes R. Maternal psychological stress and distress as predictors of low birth weight, prematurity and intrauterine growth retardation. Eur J Clin Nutr. 2003;57(2):266.CrossRefPubMed
9.
Su Q, Zhang H, Zhang Y, Zhang H, Ding D, Zeng J, et al. Maternal stress in gestation: birth outcomes and stress-related hormone response of the neonates. Pediatr Neonatol. 2015;56(6):376–81.CrossRefPubMed
10.
Schetter CD, Tanner L. Anxiety, depression and stress in pregnancy: implications for mothers, children, research, and practice. Curr Opin Psychiatry. 2012;25(2):141.CrossRef
11.
Koen N, Brittain K, Donald KA, Barnett W, Koopowitz S, Maré K, et al. Psychological trauma and posttraumatic stress disorder: risk factors and associations with birth outcomes in the Drakenstein child health study. Eur J Psychotraumatol. 2016;7(1):28720.CrossRefPubMed
12.
Wainstock T, Shoham-Vardi I, Glasser S, Anteby E, Lerner-Geva L. Fetal sex modifies effects of prenatal stress exposure and adverse birth outcomes. Stress. 2015;18(1):49–56.CrossRefPubMed
13.
Torche F, Kleinhaus K. Prenatal stress, gestational age and secondary sex ratio: the sex-specific effects of exposure to a natural disaster in early pregnancy. Hum Reprod. 2012;27(2):558–67.CrossRefPubMed
14.
Carpenter T, Grecian SM, Reynolds RM. Sex differences in early-life programming of the hypothalamic-pituitary-adrenal axis in humans suggest increased vulnerability in females: a systematic review. J Dev Orig Health Dis. 2017;8(2):244–55.CrossRefPubMed
15.
Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31(Suppl):S33–9.CrossRefPubMed
16.
Navara KJ. Programming of offspring sex ratios by maternal stress in humans: assessment of physiological mechanisms using a comparative approach. J Comp Physiol B. 2010;180(6):785–96.CrossRefPubMed
17.
Jack DW, Asante KP, Wylie BJ, Chillrud SN, Whyatt RM, Ae-Ngibise KA, et al. Ghana randomized air pollution and health study (GRAPHS): study protocol for a randomized controlled trial. Trials. 2015;16:420.CrossRefPubMedPubMedCentral
18.
Boamah EA, Asante K, Ae-Ngibise K, Kinney PL, Jack DW, Manu G, et al. Gestational age assessment in the Ghana randomized air pollution and health study (GRAPHS): ultrasound capacity building, fetal biometry protocol development, and ongoing quality control. JMIR Res Protoc. 2014;3(4):e77.CrossRefPubMedPubMedCentral
19.
Shalowitz MU, Berry CA, Rasinski KA, Dannhausen-Brun CA. A new measure of contemporary life stress: development, validation, and reliability of the CRISYS. Health Serv Res. 1998;33(5 Pt 1):1381–402.PubMedPubMedCentral
20.
Mathilda Chiu Y-H, Coull BA, Cohen S, Wooley A, Wright RJ. Prenatal and postnatal maternal stress and wheeze in urban children: effect of maternal sensitization. Am J Respir Crit Care Med. 2012;186(2):147–54.CrossRefPubMedCentral
21.
Myers HF. Ethnicity-and socio-economic status-related stresses in context: an integrative review and conceptual model. J Behav Med. 2009;32(1):9–19.CrossRefPubMed
22.
Alison CT, Rich-Edwards JW, Koenen K, Wright RJ. Cumulative stress and maternal prenatal corticotropin-releasing hormone in an urban US cohort. Psychoneuroendocrinology. 2012;37(7):970–9.CrossRef
23.
Berry C, Quinn K, Shalowitz M, Wolf R. Validation of the crisis in family systems–revised, a contemporary measure of life stressors. Psychol Rep. 2001;88(3):713–24.CrossRefPubMed
24.
Mikolajczyk RT, Zhang J, Betran AP, Souza JP, Mori R, Gulmezoglu AM, et al. A global reference for fetal-weight and birthweight percentiles. Lancet. 2011;377(9780):1855–61.CrossRefPubMed
25.
26.
Wahabi HA, Alzeidan RA, Fayed AA, Mandil A, Al-Shaikh G, Esmaeil SA. Effects of secondhand smoke on the birth weight of term infants and the demographic profile of Saudi exposed women. BMC Public Health. 2013;13:341.CrossRefPubMedPubMedCentral
27.
Andres RL, Day MC. Perinatal complications associated with maternal tobacco use. Semin Neonatol. 2000;5(3):231–41.CrossRefPubMed
28.
Services USDoHaH. The health benefits of smoking cessation: a report of the surgeon general. Rockville: US Department of Health and Human Services; 1990.
29.
Seth S, Lewis AJ, Saffery R, Lappas M, Galbally M. Maternal prenatal mental health and placental 11beta-HSD2 gene expression: initial findings from the mercy pregnancy and emotional wellbeing study. Int J Mol Sci. 2015;16(11):27482–96.CrossRefPubMedPubMedCentral
30.
Fowden AL, Szemere J, Hughes P, Gilmour RS, Forhead AJ. The effects of cortisol on the growth rate of the sheep fetus during late gestation. J Endocrinol. 1996;151(1):97–105.CrossRefPubMed
31.
Lee JY, Yun HJ, Kim CY, Cho YW, Lee Y, Kim MH. Prenatal exposure to dexamethasone in the mouse induces sex-specific differences in placental gene expression. Develop Growth Differ. 2017;59(6):515–25.CrossRef
32.
French NP, Hagan R, Evans SF, Godfrey M, Newnham JP. Repeated antenatal corticosteroids: size at birth and subsequent development. Am J Obstet Gynecol. 1999;180(1 Pt 1):114–21.CrossRefPubMed
33.
Murphy VE, Gibson PG, Giles WB, Zakar T, Smith R, Bisits AM, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003;168(11):1317–23.CrossRefPubMed
34.
Dean F, Matthews SG. Maternal dexamethasone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal Guinea pig brain. Brain Res. 1999;846(2):253–9.CrossRefPubMed
35.
Quesada AA, Tristao RM, Pratesi R, Wolf OT. Hyper-responsiveness to acute stress, emotional problems and poorer memory in former preterm children. Stress. 2014;17(5):389–99.CrossRefPubMed
36.
Alexander N, Rosenlocher F, Stalder T, Linke J, Distler W, Morgner J, et al. Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. J Clin Endocrinol Metab. 2012;97(10):3538–44.CrossRefPubMed
37.
38.
Mina TH, Raikkonen K, Riley SC, Norman JE, Reynolds RM. Maternal distress associates with placental genes regulating fetal glucocorticoid exposure and IGF2: role of obesity and sex. Psychoneuroendocrinology. 2015;59:112–22.CrossRefPubMed
39.
Saif Z, Hodyl N, Stark M, Fuller P, Cole T, Lu N, et al. Expression of eight glucocorticoid receptor isoforms in the human preterm placenta vary with fetal sex and birthweight. Placenta. 2015;36(7):723–30.CrossRefPubMedPubMedCentral
40.
Mericq V, Medina P, Kakarieka E, Marquez L, Johnson MC, Iniguez G. Differences in expression and activity of 11beta-hydroxysteroid dehydrogenase type 1 and 2 in human placentas of term pregnancies according to birth weight and gender. Eur J Endocrinol. 2009;161(3):419–25.CrossRefPubMed
41.
Stark MJ, Wright IM, Clifton VL. Sex-specific alterations in placental 11beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone. Am J Physiol Regul Integr Comp Physiol. 2009;297(2):R510–4.CrossRefPubMed
42.
Shams M, Kilby MD, Somerset DA, Howie AJ, Gupta A, Wood PJ, et al. 11Beta-hydroxysteroid dehydrogenase type 2 in human pregnancy and reduced expression in intrauterine growth restriction. Hum Reprod. 1998;13(4):799–804.CrossRefPubMed
43.
Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489):1077–81.CrossRefPubMed
44.
Robinson SM, Batelaan SF, Syddall HE, Sayer AA, Dennison EM, Martin HJ, et al. Combined effects of dietary fat and birth weight on serum cholesterol concentrations: the Hertfordshire cohort study. Am J Clin Nutr. 2006;84(1):237–44.CrossRefPubMed
Metadata
Title
Prenatal maternal stress and birth outcomes in rural Ghana: sex-specific associations
Authors
Kenneth Ayuurebobi Ae-Ngibise
Blair J. Wylie
Ellen Boamah-Kaali
Darby W. Jack
Felix Boakye Oppong
Steven N. Chillrud
Stephaney Gyaase
Seyram Kaali
Oscar Agyei
Patrick L. Kinney
Mohammed Mujtaba
Rosalind J. Wright
Kwaku Poku Asante
Alison G. Lee
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pregnancy and Childbirth / Issue 1/2019
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-019-2535-9

Other articles of this Issue 1/2019

BMC Pregnancy and Childbirth 1/2019 Go to the issue

Research article

Midwives’ perceptions of being ‘with woman’: a phenomenological study

Study protocol

Client-tailored maternity care to increase maternal empowerment: cluster randomized controlled trial protocol; the healthy pregnancy 4 All-2 program

Research article

Complications and adverse outcomes in pregnancy and childbirth among women who conceived by assisted reproductive technologies: a nationwide birth cohort study of Japan environment and children’s study

Research article

Acceptability of a text message-based intervention for obesity prevention in infants from Hawai‘i and Puerto Rico WIC

Research article

What factors influence midwives to provide obstetric high dependency care on the delivery suite or request care be escalated away from the obstetric unit? Findings of a focus group study

Research article

Maternal BMI mediates the impact of crop-related agricultural work during pregnancy on infant length in rural Pakistan: a mediation analysis of cross-sectional data