Maternal stress and distress and child nutritional status - Nature

European Journal of Clinical Nutrition (2013) 67, 348–352 & 2013 Macmillan Publishers Limited All rights reserved 0954-3007/13 www.nature.com/ejcn

ORIGINAL ARTICLE

Maternal stress and distress and child nutritional status PHC Rondo´1, G Rezende1, JO Lemos1 and JA Pereira2 BACKGROUND/OBJECTIVE: To assess the relationship between maternal stress and distress in pregnancy and 5–8 years postpartum and child nutritional status. SUBJECTS/METHODS: Longitudinal cohort study carried out in Jundiai city, Southeast Brazil, involving 409 women followed throughout pregnancy to 5–8 years postpartum, and respective children. Measures of stress and distress were obtained three times in pregnancy (at gestational ages lower than 16 weeks, from 20 to 26 weeks and from 30 to 36 weeks) and 5–8 years postpartum by the Perceived Stress Scale (PSS), General Health Questionnaire (GHQ) and the State-Trait Anxiety Inventories (STAI). The nutritional status of the children was assessed by the World Health Organization body mass index (BMI) z-score for age. The relationship between child BMI z-score for age and scores of the PSS, GHQ and STAI was evaluated by multivariate linear regression, controlling for confounding variables. RESULTS: BMI z-score for age of the children was negatively associated with maternal scores of the PSS 5–8 years postpartum and scores of the GHQ in the second trimester of pregnancy. BMI of the children was positively associated with maternal BMI and birthweight (R2 ¼ 0.13). There was 0.04 (confidence interval 0.07 to 0.9 10 2) decrease in child BMI per score unit of the PSS increase, and 0.09 (confidence interval 0.18 to 0.6 10 3) decrease in child BMI per score unit of the GHQ increase. CONCLUSIONS: This study detected a relationship between maternal mental and nutritional status and child nutritional status, implying that if the mother is not physically or mentally well, her capacity for caring for her child may be impaired. European Journal of Clinical Nutrition (2013) 67, 348–352; doi:10.1038/ejcn.2013.28; published online 13 February 2013 Keywords: maternal stress; maternal distress; child nutritional status; birthweight

INTRODUCTION Mental disorders (stress and distress) represent an important health problem, accounting for more than 10% of disability worldwide and around one-third of years lost due to disability among adults aged 15 years and over,1 more than is attributable to cardiovascular diseases or cancer. Depression, probably the most well-known type of distress,2 is the fourth leading contributor to global disease burden,1 and is more prevalent in women, especially during their childbearing ages.3,4 Although maternal depression has received reasonable research and clinical attention, stress, and other forms of distress like anxiety, has been less investigated.5 Stress has been cited as the preceding factor in 85% of the cases of depression, by depressed patients.6 It is also widely acknowledged that symptoms of anxiety and depression co-occur and that this comorbidity may be an indicator of the severity of distress.7 Malnutrition and overweight/obesity, the extremes of the nutritional status, seem to be more likely to occur in children of mothers with stress and distress.8,9 However, the number of studies in this area is still limited, and most of them investigated the issue in the perinatal and early postpartum period,10 and very few of them later in infancy and childhood.11–14 Therefore, the objective of this study was to assess the relationship between maternal stress and distress throughout pregnancy and 5–8 years postpartum and child nutritional status. MATERIALS AND METHODS This is an epidemiological cohort study involving 409 women and respective children in Jundiai city, Brazil. Originally, 865 women were

recruited from 1997 to 2000 at 12 health units and 5 hospitals in the city, and followed throughout pregnancy to evaluate stress and distress as predictors of low birthweight, prematurity and intrauterine growth retardation.15 Afterwards, the women and their children 5–8 years of age were followed from 2004 to 2006 to investigate the relationship between maternal stress and distress and child nutritional status. All women included in the cohort were insured by the National Health Service (Sistema Unico de Saude) and were apparently healthy, considering that those who present any problem in pregnancy are usually reported to specialized antenatal services. Women with chronic infectious diseases, metabolic diseases, cardiopathy, mental diseases, hypertension/preeclampsia/ eclampsia, vaginal bleeding and multiple deliveries were excluded from the study. Measures of stress and distress were obtained by four psychologists who interviewed the women at a gestational age lower than 16 weeks, from 20 to 26 weeks, from 30 to 36 weeks and from 5 to 8 years postpartum. Stress was assessed by the 14-item Perceived Stress Scale (PSS),16 an instrument designed for use with community samples that determines the degree to which situations in the last month had been estimated as stressful. The PSS is rated on a five-point scale ranging from ‘never’ to ‘very often’. Distress was investigated by the 12-item version of the General Health Questionnaire (GHQ),17 a screening instrument conceived for use in general population surveys. The questionnaire has been validated and tested in a Brazilian population.18 According to the GHQ scores, the women have been classified in two groups (low, 0–3 and high, X4). Anxiety was assessed using the State-Trait Anxiety Inventories (STAI).19 The STAI has 40 items, and is a self-report instrument designed to measure both state and trait anxiety. For state anxiety, subjects are asked how they feel at the time of being questioned, and for trait anxiety, subjects are asked how they feel generally. A cut-off point of scores 440 is used for both state anxiety and trait anxiety. Gestational age was determined by a combination of ultrasonography performed up to the 20th week of gestation, the Capurro method20

1 Department of Nutrition, School of Public Health, University of Saõ Paulo, Saõ Paulo, Brazil and 2Federal University of Piauı´, Campus Senador Helvı´dio Nunes de Barros, Rua Cıćero Eduardo s/n, Bairro Junco, Picos, Brazil. Correspondence: Professor PHC Rondo´, Department of Nutrition, School of Public Health, University of Saõ Paulo, Avenida Dr Arnaldo 715, Saõ Paulo CEP 01246-904, Brazil. E-mail: [email protected] Received 22 October 2012; revised 14 January 2013; accepted 15 January 2013; published online 13 February 2013

Maternal stress and distress and child nutrition PH Rondo´ et al

349 assessed from 12 to 48 h of birth and information on the date of the last menstrual period. When there was less than or a week discrepancy between at least two of the gestational age determinations, assessed by the three different methods, one of them was chosen, giving preference to the order of the methods cited above. Birthweight was collected from the medical records.15 Demographic and socioeconomic characteristics and information on breastfeeding were assessed by a general questionnaire. The nutritional status of the women and respective children was determined by the body mass index (BMI) and was classified according to the World Health Organization International Classification of BMI for adults,21 and to the World Health Organization BMI z-score for age growth reference for children and adolescents from 5 to 19 years.22 The participants were weighed on a portable Sohnle electronic scale (model 7500; Sohnle, Murrhardt, Germany), with a precision of 100 g. Height was measured with a Seca wall-mounted stadiometer (Leicester Portable Height measure model; Hamburg, Germany), with a precision of 0.1 cm. The anthropometric measurements were performed according to the recommendations of Jelliffe and Jelliffe.23 The Stata version 10 software (College Station, TX, USA) was used for storage and statistical analysis of the data. The relationship between child BMI z-score for age (dependent variable) and scores of the PSS, GHQ and STAI (independent variables) in the three trimesters of pregnancy and 5–8 years postpartum, and the other independent variables investigated— confounding variables (maternal age, maternal education, per capita income, family size, maternal work, marital status, maternal BMI, length of breastfeeding, child gender, age, birthweight and gestational age) were determined using univariate linear regression. The variables with a P–value p0.20 in the univariate analysis (scores of the PSS, GHQ and STAI in the three trimesters of pregnancy and 5–8 years postpartum, maternal education, maternal BMI and length of breastfeeding) were selected for entry into a multivariate linear regression model, using the backward stepwise selection method. In the final model, the variables with a Pp0.05 were considered as being statistically significant. Informed written consent was obtained from all subjects, and the protocol was approved by the Research Ethics Committee of the School of Public Health, University of Saõ Paulo and the Health Secretariat of Jundiai, Saõ Paulo, Brazil. The present study was carried out in accordance with the Declaration of Helsinki of the World Medical Association.

RESULTS There was a loss of 33.6% children, considering all the mothers who were located (n ¼ 745) in the first phase of the study, and a loss of 42.7% children, considering the mothers who participated in the original cohort (n ¼ 865).15 Comparison of some characteristics between the children included in the cohort and those who did not conclude the study showed a significant difference in age, the youngest children did not conclude the study (P ¼ 0.01), whereas no differences were observed for birthweight, per capita income or maternal education. The characteristics of the women included in the present study are shown in Table 1. Most of the women were from 26 to 35 years of age (50.6%), had X8 years of formal education (52.7%), received more than half minimum Brazilian wage (1 minimum Brazilian wage ¼ R$350.00 ¼ approximately US$77) (72.1%), had a family size p4 persons (64%), did not work outside home (72.1%) and were married or with a partner (76.5%). Almost 70% of the women were overweight or obese, and 42.8% breastfed their children for a periodp6 months. Table 2 presents the scores of the PSS, GHQ and STAI. There is no clear cut-off point for the scores of the PSS; therefore, they are presented in quartiles. Comparing the mean scores of the women in the highest quartile with the mean scores of the whole population, and the mean scores of the populations studied by Cohen et al.,16 we considered that those women had stress in pregnancy and 5–8 years postpartum. The prevalences of maternal distress, assessed by the GHQ and STAI, varied between 25.7 and 58.4% in the three trimesters of pregnancy and 5–8 years postpartum. The characteristics of the children included in the study are presented in Table 3. Most of the children were female (56%) and & 2013 Macmillan Publishers Limited

Table 1.

Characteristics of the women included in the study (n ¼ 409) N

%

Age (years) 19–25 26–35 X35

91 207 111

22.3 50.6 30.7

Educationa (years) p4 5–8 X8

79 113 214

19.5 27.8 52.7

114 158 137

27.9 38.6 33.5

109 153 87 60

26.6 37.4 21.3 14.7

Work Yes No

114 295

27.9 72.1

Marital status Married/with partner Single/separated/divorced/widow

313 96

76.5 23.5

BMI (weight/height2) 18.5–24.9 (normal) 25.0–29.9 (overweight) 30.0–34.9 (obese I) 35.0–39.9 (obese II)

124 201 63 21

30.3 49.1 15.4 5.2

Length of breastfeeding (months) p1 2–6 7–12 13–24 25–60

49 126 92 92 50

12 30.8 22.5 22.5 12.2

Mean (s.d.) 30.7 (6.06)

Per capita income (MBW)b o½ ½–1 X1 Family size (number of persons) p3 4 5 X6

7.7 (3.1)

0.92 (0.67)

4.3 (1.4)

27.3 (4.1)

12.3 (12.2)

a

n ¼ 406. bMinimum Brazilian wage (MBW) (1 MBW ¼ R$350.00 ¼ approximately US$77).

from 6 to 7 years of age (51.1%). Only 5.6% of the children had low birthweight, and the majority (67.3%) had a birthweight X3000 g. Almost 4% of the children were born preterm and 1.2% postterm. In relation to their nutritional status, 4.6% were malnourished (BMI z-score o 2), 4.2% were obese (BMI z-score for age 4 þ 2) and 20% were overweight (BMI z-score for age from þ 1 to þ 2). According to Table 4, BMI z-score for age of the children was negatively associated with maternal scores of the PSS 5–8 years postpartum and scores of the GHQ in the second trimester of pregnancy. BMI z-score for age was positively associated with maternal BMI and birthweight (R2 ¼ 0.13). There was 0.04 (confidence interval 0.07 to 0.9 10 2) decrease in child BMI z-score for age per score of the PSS increase, and 0.09 (confidence interval 0.18 to 0.6 10 3) decrease in child BMI z-score for age per score of the GHQ increase. DISCUSSION The results of this study showed a negative relationship between maternal mental and nutritional status and child nutritional status at 5–8 years, implying that if the mother is not physically or mentally well, her capacity for caring for her child may be impaired. The study also showed positive associations between child nutritional status and birthweight. European Journal of Clinical Nutrition (2013) 348 – 352


350 Table 2. Maternal PSS, GHQ and STAI scores in the three trimesters of pregnancy and 5–8 years postpartum (n ¼ 409)

Table 3.

Characteristics of the children included in the study (n ¼ 409) N

N PSS First trimester 7–18 19–23 24–27 28–43 Second trimester 4–18 19–23 24–27 28–46 Third trimester 2–17 18–22 23–27 28–53 5–8 Years postpartum 15–34 35–39 40–43 44–55 GHQ First trimester p3 4–12 Second trimester p3 4–12 Third trimester p3 4–12 5–8 Years postpartum p3 4–12 SAI First trimester o40 X40 Second trimester o40 X40 Third trimester o40 X40 5–8 Years postpartum o40 X40 TAI First trimester o40 X40 Second trimester o40 X40 Third trimester o40 X40 5–8 Years postpartum o40 X40

%

22.7 (6.6) 110 108 95 96

26.8 26.4 23.2 23.6

115 105 92 97

28 25.6 22.5 23.8

109 105 106 89

26.7 25.7 25.9 21.8

120 102 94 93

29.3 24.9 23 22.7

22.8 (6.9)

22.1 (7.2)

38.1 (7.4)

2.8 (3.1) 273 136

66.7 33.3

303 106

74.1 25.9

304 105

74.3 25.7

2.3 (2.6) 2.5 (2.7)

252 157

61.6 38.4

282 127

68.9 31.1

314 95

76.7 23.3

302 107

73.8 26.2

228 181

55.7 44.3

199 210

48.7 51.3

227 182

55.6 44.4

224 185

54.8 45.2

170 239

41.6 58.4

Gender Male Female

180 229

44 56

Age (years) 5–6 6–7 7–8

102 209 98

24.9 51.1 24

Birthweight (g) o2500 2500–3000 3000–3500 X3500

23 111 168 107

5.6 27.1 41.1 26.2

Gestational age (weeks) o37 37–42 X42

16 387 5

3.9 94.9 1.2

BMI (z-score)a o2 2 to 1 1 to 0 0 to þ 1 þ 1 to þ 2 4þ2

19 66 118 107 82 17

4.6 16.1 28.9 26.2 20 4.2

BMI (kg/m2)

Mean (s.d.)

6.5 (0.6)

3207.8 (476.5)

39.1 (1.3)

0 (1.27)

15.96 (2.33)

3.2 (3.2)

Abbreviation: BMI, body mass index. aWorld Health Organization BMI z-score for age.22

37.3 (8.8)

lower BMI at third grade, but only for girls. For boys, there was a positive association between maternal depression at kindergarten and higher BMI at fifth grade. In a study from India,24 infants of 37 depressed mothers were compared with those of 134 nondepressed mothers. Maternal depression was strongly associated with being underweight at 6 months, and these associations remained statistically significant after adjustment for birthweight and parental education. Harpham et al.25 also observed a relationship between maternal mental health and poor nutritional status, assessed by BMI z-scores for age, in children from 6 to 18 months in India and Vietnam. Rahman et al.26 reported that the relative risks of infants being underweight were 4.0 (2.1–7.7) at 6 months of age and 2.6 (1.7– 4.1) at 12 months of age, and the relative risks for stunting were 4.4 (1.7–11.4) at 6 months of age and 2.5 (1.6–4.0) at 12 months of age, if the mothers were depressed in the third trimester of pregnancy. Stewart et al.27 carried out a cross-sectional study to investigate the association between maternal common mental disorder (CMD) (considered by the authors as depression, anxiety and somatic manifestations of distress) and infant growth in rural Malawi. Mean length-for-age z-score for infants of mothers with CMD was significantly lower than that for infants of mothers without CMD, demonstrating an association between maternal CMD and infant growth impairment in rural sub-Saharan Africa. Avan et al.13 assessed the association between maternal postnatal depression and child growth and behavior problems at age 2 years in a socioeconomically deprived urban South African setting. The authors observed that the association between postnatal depression and child behavior problems was primarily mediated by poor child growth. A case–control study carried out in Northeast Brazil detected that maternal CMD doubled the risk of moderate/severe malnutrition in children aged 0–5 years.9 Surkan et al.28 found that maternal depressive symptoms were

35.9 (7.9) 36.8 (8.4) 40.2 (10.1)

41.8 (10.6) 40 (9.9) 39.5 (9.8) 43.7 (10.8)

Abbreviations: GHQ, General Health Questionnaire; PSS, Perceived Stress Scale; STAI, State-Trait Anxiety Inventories (SAI, State-Anxiety Inventory; TAI, TraitAnxiety Inventory).

Most of the studies that investigated the association between maternal mental status and child nutritional status are restricted to the periods of pregnancy and early postpartum,10 and very few of them investigated this issue later in infancy and childhood. Duarte et al.14 examined the association between maternal depression and child BMI from kindergarten to fifth grade. Similar to our results, the authors reported a negative association between maternal depression at kindergarten and European Journal of Clinical Nutrition (2013) 348 – 352

%

Mean (s.d.)

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351 Table 4. Multivariate linear regression analysis considering BMI (z-scores) of the children as the dependent variable and maternal scores of the PSS, GHQ and STAI as independent variables BMI (z-scores) PSS (5–8 years postpartum) GHQ (second trimester) Maternal BMI Birthweight

Coefficient 0.04 0.09 0.13 0.6 10 3

S.e.

CI (95%)

0.02 0.04 0.03 0.2 10 3

0.07 to 0.9 10 2 0.18 to 0.6 10 3 0.07–0.18 0.1 10 3 to 0.1 10 2

P 0.011 0.048 o0.001 0.013

Abbreviations: BMI, body mass index; CI, confidence interval; GHQ, General Health Questionnaire; PSS, Perceived Stress Scale. R2 ¼ 0.13; adjusted R2 ¼ 0.12.

related to short stature in infants aged 6–24 months from lowincome urban communities in Northeast Brazil. When another statistical analysis was performed, considering overweight as the outcome, the authors observed a relationship between maternal depressive symptoms and overweight.8 Ajslev et al.12 investigated the associations between maternal anxiety, depression and stress (assessed 6 months postpartum) and overweight in a prospective cohort study, including 21 121 mother–child from the Danish National Birth. The authors have controlled for a range of confounding factors and concluded that maternal mental status assessed 6 months postpartum did not predict nutritional status of the children at 7 years of age. Milgrom et al.29 carried out a literature review to investigate the relationship between ante- and postnatal maternal depressive symptoms and childhood obesity, and found that data are limited, of low quality and inconclusive. The authors selected only five studies assessing this association, and two of them used the same population of children. A crosssectional study from Brazil8 found an association between maternal depressive symptoms and obesity, but the other four studies from developing countries10,12,30,31 did not confirm the association. In fact, it would be interesting to develop a study in a region where the prevalence of malnutrition and obesity is high, considering that in our study, 4.2% and 4.6% of the children presented BMI z-scores for age o 2 and 4 þ 2, respectively. It is quite difficult to compare the results of the studies that investigated the associations between maternal mental status and child nutritional status, considering that few of them have controlled for confounding variables, and most of them have assessed maternal mental health just during pregnancy or in the early postpartum period. Based on the association between maternal mental status and low birthweight,2,10,15 Stewart et al.32 hypothesized that the lower postnatal weight and length observed in infants of depressed mothers probably reflects no postnatal growth impairment, but adequate growth starting from a lower baseline mediated in pregnancy. Tomlinson et al.33 conducted a prospective cohort study in South Africa involving 147 mothers/infants and found that the association between maternal depression and child nutritional status disappeared once birthweight was accounted for. However, similar to our results, in cohort studies from Pakistan26 and India,34 the association remained significant after birthweight was included in the multivariate analysis. The relationship between child and maternal nutritional status has been cited in some studies.35–39 Amorim et al.35 showed that maternal nutritional status together with poor socioeconomic conditions were the most important determinants of the nutritional status of children at school age. Bjeland et al.36 investigated in a sample of 1483 adolescents, 1156 mothers and 1016 fathers, the relationship between overweight and waist circumference in children and parents. The authors observed associations between children and mothers for both genders, and associations between children and fathers just for boys. McDonald et al.37 measured height and weight in 3075 Colombian children between 5 and 12 years of age who attended public primary schools, and reported an association between maternal and child BMI. Rosenkranz et al.38 related mother–daughter resemblance in BMI & 2013 Macmillan Publishers Limited

and obesity-related behaviors in a group of 67 girls aged 9–13 years. Lourenço et al.39 reported in a longitudinal study involving 255 children that socioeconomic background and maternal nutritional status are important predictors of BMI z-score throughout childhood. In the present study, a considerable percentage of mothers presented high scores on the GHQ (range: 25.7–38.4%) and STAI (range: 23.3–58.4%). Scores of the highest quartiles of the PSS, especially 5–8 years postpartum, were also high, compared with the scores of other populations.16 The results demonstrate that mothers were stressed and distressed in pregnancy and later in life. Paffer et al.40 investigated the association between maternal mental disorders and child malnutrition in rural and urban environments in Northeast Brazil, and observed a high prevalence of CMD (56.2% rural and 43.8% urban, respectively) in mothers of children aged up to 2 years. Maternal depression in pregnancy and in the early postpartum period is probably one of the most underrecognized and untreated conditions.3 The number of women with stress and distress in this period of life is probably higher than the observed, because of the reluctance of mothers to admit these problems during a time of presumed happiness. The possible mechanisms by which maternal stress and distress affect child nutritional status include a less healthy lifestyle, poor psychosocial stimulation of the child and reduced care-seeking for herself and for the child. Patel et al.41 found that depressed mothers in Goa were more likely to have difficulties with breastfeeding or to cease breastfeeding early, and Rondo´ et al.42 found that distressed women had less intention to breastfeed their children than not distressed women. When weaning, women with stress and distress may be less successful in preparing foods. It might also be expected that disability in those women could increase morbidity and mortality of their children. Despite the importance of maternal mental disorders and their impact on child growth and development, maternal mental health is not a component of the primary health-care system in many parts of the world (Engle43). Patel44 has suggested some strategies to improve access to psychological treatment, considering that the vast majority of potential beneficiaries are unable to access these treatments. This author addressed the human resource barrier by training lay or community health workers to deliver the treatments, and addressed the acceptability barrier by systematically adapting the treatment to contextual factors. CONCLUSION This cohort study found a relationship between maternal mental and nutritional status and child nutritional status, implying that if the mother is not physically or mentally well, her capacity for caring for her child may be impaired. Besides giving evidence of maternal mental problems, the results of the study suggest that there is a need to provide resources to cope with the high prevalence of maternal stress and distress among mothers of preschool/school children, in order to reduce the damage to both the mother and the child. The authors advise further studies to assess maternal stress and distress throughout pregnancy and European Journal of Clinical Nutrition (2013) 348 – 352


352 subsequently in life, and its relationship with child nutritional status, especially in regions with high prevalence of malnutrition and/or obesity. CONFLICT OF INTEREST The authors declare no conflict of interest.

ACKNOWLEDGEMENTS We thank Fundaçaõ de Amparo a` Pesquisa do Estado de Saõ Paulo (FAPESP), Saõ Paulo, Brazil, for financing this study (grants: 1998/00321-0; 2004/04109-8), and the field workers Rosemary F Ferreira, Alessandra L Santos and Josimara F Moura.

AUTHORS CONTRIBUTIONS PHCR designed the study protocol, secured funding, and participated in the statistical analysis, interpretation of data and writing of the paper. GR participated in the statistical analysis and interpretation of data. JOL and JAP collected data, and participated in the interpretation of data and writing of the paper. All authors approved the final version of the paper.

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