Original Article
Contrasting effects of prenatal life stress on blood pressure and body mass index in young adults Sunil K. Bhat a, Lawrence J. Beilin a, Monique Robinson b, Sally Burrows a, and Trevor A. Mori a
Background: Various environmental stressors in pregnancy have been reported to affect high blood pressure (BP) in adult offspring. However, few studies have examined the effect of prenatal maternal psychological stress on offspring BP and BMI in early adulthood. Method: In 957 Raine cohort participants, regression analyses were used to examine the association between the count of maternal life stress events experienced during pregnancy and offspring BP and BMI at age 20. Results: Prenatal life stress associated positively with offspring BMI but inversely with SBP. After adjustment for confounders each additional prenatal life stress event reduced offspring SBP by 0.66 mmHg (P ¼ 0.013) in those with an average BMI and lowered the odds of systolic (pre)hypertension by 17% (odds ratio ¼ 0.83; P ¼ 0.008). The inverse relationship between prenatal life stress and adult SBP was stronger in offspring with higher BMI. On the contrary, each unit increase in prenatal life stress score predicted a BMI increase of 0.37 kg/m2 (P ¼ 0.022). Longitudinal analysis showed similar effects of prenatal life stress for offspring BMI from age 8 and SBP from age 14. Conclusion: This study has shown that maternal stress in pregnancy significantly associated with BMI from early childhood, but contrary to our hypothesis predicted lower resting SBP and lower odds of systolic (pre)hypertension in young adult offspring. The effect of prenatal life stress on BP was accentuated by a higher BMI. Fetal programming events as a result of prenatal stress may underpin some of these relationships. Keywords: blood pressure, BMI, early life stress, psychosocial, Raine Study Pregnancy Cohort Abbreviations: BP, blood pressure; CI, confidence interval; PregLSE, pregnancy life stress events
in animals leading to offspring obesity and associated metabolic disorders [11–13]. The association between extremes of birth weight and adult blood pressure (BP) has been well documented following original observations of Barker and coworkers [14–18]. However, the few studies of the relation between commonly experienced forms of human psychosocial stress in pregnancy and higher BP in offspring have been restricted to children and with inconsistent findings [19–22]. Given the associations between severe maternal stressors and offspring obesity, it might be expected that there would be similar associations between maternal psychosocial stress and offspring BP, mediated either via BMI or independent mechanisms such as fetal programming of the hypothalamic pituitary axis [23–27]. We have, therefore, sought to test the hypotheses that prenatal life stress will be associated with higher BP and higher BMI in a young adult population using data from a well characterized pregnancy cohort first studied when the mothers were 18 weeks pregnant. The Western Australian Pregnancy Cohort (Raine) study is one of the longest running prospective studies on child health and development [28]. To the best of our knowledge, no other longitudinal study has examined the association between prenatal stress events exposure on BP and BMI in young adults.
METHODS This study was conducted using data from the Raine Study, a prospective longitudinal follow-up study of 2868 live births followed from 1989. All pregnant women attending King Edward Memorial Hospital were enrolled at 18 weeks of gestation between August 1989 and April 1992, with details published elsewhere [28]. The study is based on the 20-year follow-up of the offspring, conducted from January 2010 to April 2012.
INTRODUCTION
S
everal types of human maternal stress in pregnancy have been associated with offspring obesity and associated metabolic disorder [1,2]. Such studies include maternal starvation, as in the Dutch famine in the World War II [3,4], the Chinese famine [5], maternal exposure to the events of the Holocaust [6,7], environmental disasters such as the Canadian Ice blackout [8], and psychosocial stress in the form of maternal bereavement [9,10]. These human observational studies have been complemented by an extensive literature on a variety of experimental pregnancy stressors
Journal of Hypertension
Journal of Hypertension 2015, 33:711–719 a School of Medicine and Pharmacology, Royal Perth Hospital Unit, University of Western Australia, Perth and bTelethon Kids Institute, University of Western Australia, Subiaco, Western Australia, Australia
Correspondence to Sunil K. Bhat, MD MPH, Royal Perth Hospital Unit, School of Medicine and Pharmacology, GPO Box X2213, Perth, WA 6847, Australia. Tel: +61 43123 4330; fax: +61 8 9224 0246; e-mail: [email protected];sunil.kbhat@ gmail.com Received 7 August 2014 Revised 30 October 2014 Accepted 30 October 2014 J Hypertens 33:711–719 Copyright ß 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI:10.1097/HJH.0000000000000476
www.jhypertension.com
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
711
Bhat et al.
The Raine Study has ethics approval from the Human Research Ethics Committees at King Edward Memorial Hospital, Princess Margaret Hospital for Children, or The University of Western Australia. Informed written consent was obtained from the adult participants. This analysis includes the data collected during pregnancy and when their offspring were young adults.
Prenatal life stress events Antenatal women were asked in the 18-week gestation questionnaire whether they had experienced any of the 10 pregnancy life stress events (PregLSEs) since becoming pregnant and, in the 34-week gestation questionnaire, whether any of the events had been experienced within the last 4 months [29]. The response was ‘yes’ or ‘no’ to each of the PregLSE relating to pregnancy problems, death of a close relative, death of a close friend, separation or divorce, marital problems, problems with their children, own job loss (not voluntary), partner’s job loss (not voluntary), money problems, and residential move [29]. As a number of PregLSEs were related to commonly themed experiences, the 10 PregLSEs were collapsed into six categories. The two PregLSEs related to death of a close relative or a close friend were collapsed into one and the two PregLSEs relating to separation or divorce and marital problems were taken together. Similarly, the mother’s or partner’s job loss and money problems were combined into a single PregLSE reflecting money insufficiency. As a result, the maximum PregLSE score for any participant was six. It was noted that although some PregLSEs were recorded at both 18 and 34 weeks of gestation, the nature of the PregLSE suggested they were likely to have occurred only once and the stress perceived was sustained. To remove potential double counting, the number of new PregLSEs at 34 weeks (previously unreported) was added to the sum of PregLSEs at 18 weeks to obtain a total score of PregLSEs experienced from conception to 34 weeks of pregnancy.
Offspring blood pressure and anthropometric measurements BP and anthropometry were measured at ages 1, 3, 5, 8, 10, 14, 17, and 20 years. Resting supine BP and heart rate were recorded using an oscillometric sphygmomanometer (Dinamap ProCare 100; Soma Technology, Bloomfield, Connecticut, USA) with an appropriate cuff size. After resting quietly for 5 min, BP recordings were taken sequentially every 2 min. At age 14, 17, and 20 years the last five of six readings were averaged whereas at earlier ages the last two of three readings were averaged and used for the study analyses. Systolic and diastolic (pre)hypertension (SBP-PH/H and DBP-PH/H. respectively) were defined using the adult ‘Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High BP (JNC-7)’ criteria (www.nhlbi.nih.gov/guidelines/hypertension): SBP-PH as SBP 120–139 mmHg; DBP-PH as DBP 80–89 mmHg and SBP-H as SBP 140 mmHg at least; DBP-H as DBP 90 mmHg at least. Participants were weighed with a Wedderburn Chair Scale (nearest 100 g) after fasting and wearing minimal 712
www.jhypertension.com
clothing. Height was measured without shoes (nearest 0.1 cm) using a Holtain Stadiometer (Crosswell, UK). BMI was calculated as weight (kg)/height (m)2 and was categorized as normal/underweight (
Contrasting effects of prenatal life stress on blood pressure and body mass index in young adults Sunil K. Bhat a, Lawrence J. Beilin a, Monique Robinson b, Sally Burrows a, and Trevor A. Mori a
Background: Various environmental stressors in pregnancy have been reported to affect high blood pressure (BP) in adult offspring. However, few studies have examined the effect of prenatal maternal psychological stress on offspring BP and BMI in early adulthood. Method: In 957 Raine cohort participants, regression analyses were used to examine the association between the count of maternal life stress events experienced during pregnancy and offspring BP and BMI at age 20. Results: Prenatal life stress associated positively with offspring BMI but inversely with SBP. After adjustment for confounders each additional prenatal life stress event reduced offspring SBP by 0.66 mmHg (P ¼ 0.013) in those with an average BMI and lowered the odds of systolic (pre)hypertension by 17% (odds ratio ¼ 0.83; P ¼ 0.008). The inverse relationship between prenatal life stress and adult SBP was stronger in offspring with higher BMI. On the contrary, each unit increase in prenatal life stress score predicted a BMI increase of 0.37 kg/m2 (P ¼ 0.022). Longitudinal analysis showed similar effects of prenatal life stress for offspring BMI from age 8 and SBP from age 14. Conclusion: This study has shown that maternal stress in pregnancy significantly associated with BMI from early childhood, but contrary to our hypothesis predicted lower resting SBP and lower odds of systolic (pre)hypertension in young adult offspring. The effect of prenatal life stress on BP was accentuated by a higher BMI. Fetal programming events as a result of prenatal stress may underpin some of these relationships. Keywords: blood pressure, BMI, early life stress, psychosocial, Raine Study Pregnancy Cohort Abbreviations: BP, blood pressure; CI, confidence interval; PregLSE, pregnancy life stress events
in animals leading to offspring obesity and associated metabolic disorders [11–13]. The association between extremes of birth weight and adult blood pressure (BP) has been well documented following original observations of Barker and coworkers [14–18]. However, the few studies of the relation between commonly experienced forms of human psychosocial stress in pregnancy and higher BP in offspring have been restricted to children and with inconsistent findings [19–22]. Given the associations between severe maternal stressors and offspring obesity, it might be expected that there would be similar associations between maternal psychosocial stress and offspring BP, mediated either via BMI or independent mechanisms such as fetal programming of the hypothalamic pituitary axis [23–27]. We have, therefore, sought to test the hypotheses that prenatal life stress will be associated with higher BP and higher BMI in a young adult population using data from a well characterized pregnancy cohort first studied when the mothers were 18 weeks pregnant. The Western Australian Pregnancy Cohort (Raine) study is one of the longest running prospective studies on child health and development [28]. To the best of our knowledge, no other longitudinal study has examined the association between prenatal stress events exposure on BP and BMI in young adults.
METHODS This study was conducted using data from the Raine Study, a prospective longitudinal follow-up study of 2868 live births followed from 1989. All pregnant women attending King Edward Memorial Hospital were enrolled at 18 weeks of gestation between August 1989 and April 1992, with details published elsewhere [28]. The study is based on the 20-year follow-up of the offspring, conducted from January 2010 to April 2012.
INTRODUCTION
S
everal types of human maternal stress in pregnancy have been associated with offspring obesity and associated metabolic disorder [1,2]. Such studies include maternal starvation, as in the Dutch famine in the World War II [3,4], the Chinese famine [5], maternal exposure to the events of the Holocaust [6,7], environmental disasters such as the Canadian Ice blackout [8], and psychosocial stress in the form of maternal bereavement [9,10]. These human observational studies have been complemented by an extensive literature on a variety of experimental pregnancy stressors
Journal of Hypertension
Journal of Hypertension 2015, 33:711–719 a School of Medicine and Pharmacology, Royal Perth Hospital Unit, University of Western Australia, Perth and bTelethon Kids Institute, University of Western Australia, Subiaco, Western Australia, Australia
Correspondence to Sunil K. Bhat, MD MPH, Royal Perth Hospital Unit, School of Medicine and Pharmacology, GPO Box X2213, Perth, WA 6847, Australia. Tel: +61 43123 4330; fax: +61 8 9224 0246; e-mail: [email protected];sunil.kbhat@ gmail.com Received 7 August 2014 Revised 30 October 2014 Accepted 30 October 2014 J Hypertens 33:711–719 Copyright ß 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI:10.1097/HJH.0000000000000476
www.jhypertension.com
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
711
Bhat et al.
The Raine Study has ethics approval from the Human Research Ethics Committees at King Edward Memorial Hospital, Princess Margaret Hospital for Children, or The University of Western Australia. Informed written consent was obtained from the adult participants. This analysis includes the data collected during pregnancy and when their offspring were young adults.
Prenatal life stress events Antenatal women were asked in the 18-week gestation questionnaire whether they had experienced any of the 10 pregnancy life stress events (PregLSEs) since becoming pregnant and, in the 34-week gestation questionnaire, whether any of the events had been experienced within the last 4 months [29]. The response was ‘yes’ or ‘no’ to each of the PregLSE relating to pregnancy problems, death of a close relative, death of a close friend, separation or divorce, marital problems, problems with their children, own job loss (not voluntary), partner’s job loss (not voluntary), money problems, and residential move [29]. As a number of PregLSEs were related to commonly themed experiences, the 10 PregLSEs were collapsed into six categories. The two PregLSEs related to death of a close relative or a close friend were collapsed into one and the two PregLSEs relating to separation or divorce and marital problems were taken together. Similarly, the mother’s or partner’s job loss and money problems were combined into a single PregLSE reflecting money insufficiency. As a result, the maximum PregLSE score for any participant was six. It was noted that although some PregLSEs were recorded at both 18 and 34 weeks of gestation, the nature of the PregLSE suggested they were likely to have occurred only once and the stress perceived was sustained. To remove potential double counting, the number of new PregLSEs at 34 weeks (previously unreported) was added to the sum of PregLSEs at 18 weeks to obtain a total score of PregLSEs experienced from conception to 34 weeks of pregnancy.
Offspring blood pressure and anthropometric measurements BP and anthropometry were measured at ages 1, 3, 5, 8, 10, 14, 17, and 20 years. Resting supine BP and heart rate were recorded using an oscillometric sphygmomanometer (Dinamap ProCare 100; Soma Technology, Bloomfield, Connecticut, USA) with an appropriate cuff size. After resting quietly for 5 min, BP recordings were taken sequentially every 2 min. At age 14, 17, and 20 years the last five of six readings were averaged whereas at earlier ages the last two of three readings were averaged and used for the study analyses. Systolic and diastolic (pre)hypertension (SBP-PH/H and DBP-PH/H. respectively) were defined using the adult ‘Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High BP (JNC-7)’ criteria (www.nhlbi.nih.gov/guidelines/hypertension): SBP-PH as SBP 120–139 mmHg; DBP-PH as DBP 80–89 mmHg and SBP-H as SBP 140 mmHg at least; DBP-H as DBP 90 mmHg at least. Participants were weighed with a Wedderburn Chair Scale (nearest 100 g) after fasting and wearing minimal 712
www.jhypertension.com
clothing. Height was measured without shoes (nearest 0.1 cm) using a Holtain Stadiometer (Crosswell, UK). BMI was calculated as weight (kg)/height (m)2 and was categorized as normal/underweight (
