Energy stress during pregnancy and lactation: consequences for ...

European Journal of Clinical Nutrition (2003) 57, 151–156 ß 2003 Nature Publishing Group All rights reserved 0954–3007/03 $25.00 www.nature.com/ejcn

ORIGINAL COMMUNICATION Energy stress during pregnancy and lactation: consequences for maternal nutrition in rural Bangladesh DS Alam1,2*, JMA van Raaij2, JGAJ Hautvast2, M Yunus1 and GJ Fuchs1,3 1

ICDDRB Centre for Health and Population Research, Dhaka, Bangladesh; 2Division of Human Nutrition and Epidemiology, Wageningen University, Wageningen, The Netherlands; and 3Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, USA Objective: To assess the relationship of energy stress during pregnancy and lactation to maternal body stores in marginally nourished rural Bangladeshi women. Subjects and methods: Two-hundred and fifty-two women were followed from 5 – 7 months of pregnancy until 6 months postpartum. Energy intake was estimated during pregnancy and at 1, 3 and 6 month(s) postpartum using 24 h dietary recall. Body weight was measured on enrollment, another once or twice during pregnancy, and at 1, 3 and 6 month(s) postpartum. The weekly rates of pregnancy weight gain and postpartum weight changes were determined. Weight and length of the infants were measured at birth and at approximately 1, 3 and 6 month(s). Results: Maternal energy intake at 5 – 7 months of gestation was 1464 416 kcal=day (mean s.d.). Women gained a mean of 200 g=week or a total of 4 kg during the second half of pregnancy. An analysis of maternal weight showed no indication of accrual of fat stores during pregnancy. Dietary energy during lactation exceeded the intake during pregnancy by 248 – 354 kcal=day. Mothers lost an estimated average of 1 kg of weight during the first 6 months of lactation. The mean ( s.d.) birth weight was 2.55 0.38 kg, and the prevalence of low birth weight ( < 2500 g) was 48%. Infants exhibited some catch-up growth only during the first 3 months but overall growth during the first 6 months did not change from their relative status at birth when compared with NCHS reference. Conclusions: These rural Bangladeshi women failed to gain sufficient weight during the last half of pregnancy to maintain body weight during lactation when the energy demand is high. Poor growth of their primarily breastfed infants raises concern about the adequacy of lactation in this community. European Journal of Clinical Nutrition (2003) 57, 151 – 156. doi:10.1038=sj.ejcn.1601514 Keywords: energy intake; pregnancy weight gain; postpartum weight; birth weight; infant growth; rural Bangladesh

Introduction Maternal energy balance during pregnancy is a complex and widely variable physiological process (Goldberg et al, 1991) and is recognized as an important determinant of pregnancy

*Correspondence: DS Alam, ICDDRB Centre for Health and Population Research, GPO Box 128, Dhaka-1000, Bangladesh. E-mail: [email protected] Guarantor: DS Alam. Contributors: DSA, GJF, MY and JMAVR developed the study design. DSA, GJF and DY were responsible for the implementation of the field work. DSA, JMAVR, JGAJH and GJF designed the analysis. DSA drafted the manuscript which was then revised by all investigators. Received 31 January 2001; revised 16 April 2002; accepted 18 April 2002

outcome (Kramer 1987). Women should be in positive energy balance during pregnancy to support the energy demands of pregnancy and to build adequate fat reserves to support additional energy requirements during late pregnancy and lactation (Institute of Medicine, 1990). Major determinants of energy balance are energy intake and energy expenditure, and the degree of positive energy balance during pregnancy is reflected in pregnancy weight gain. Although data from high-income countries are abundant, very little is known about dietary energy and weight gain during pregnancy in poor developing countries. In healthy Western populations, weight at 4 weeks postpartum closely approximates weight at mid-pregnancy, and the weight in excess of pre-pregnant weight primarily repre-

Energy stress during pregnancy and lactation DS Alam et al

152 sents fat mass accrued during the first half of pregnancy (Hytten, 1991). This amount of additional fat accrual corresponds to about 2 kg in high-income countries (van Raaij et al, 1987; Institute of Medicine, 1990). Pregnancy weight gain in developing countries is about half or less compared with that in developed countries, and there are indications that these women often lose weight during the course of pregnancy (Lawrence et al, 1987; Krasovec 1991; Kramer, 1998). Maternal energy requirements are greatest during lactation because of additional requirements ( 600 kcal) for milk production (FAO=WHO=UNU, 1985). The energy demand during lactation is usually met through various strategies including increased energy intake, mobilization of fat from maternal reserves developed during pregnancy and energy sparing through reduced physical activity or possible energysparing adaptations (Sadurskis et al, 1988; van Raaij et al, 1991). However, in poor subsistence developing communities such options are not often met because of social and economic constraints. Energy cost of lactation is presumed to be similar in welland poorly-nourished women since the quantity and quality of breast milk from different populations with diverse socioeconomic and nutritional status have been shown to be comparable (Brown et al, 1986). However, as women in developing countries more often enter lactation without additional fat stores, they are likely to be at risk of adverse nutritional consequences unless the extra energy demand is met through enhanced dietary intake. While adequacy of lactation is difficult to measure, breastfed infant growth provides an indirect measure of adequacy, particularly during the early months. Evidence from poor developing countries suggests maternal lactation can support adequate infant growth during the first 6 months (Dewey, 1998), although the consequences for maternal nutrition are not clearly known. In this study we examined the extent to which energy stress during pregnancy and lactation affects maternal energy stores by analyzing maternal weight during pregnancy and weight changes during lactation in relation to their dietary energy intake.

Subjects and methods Subjects and study design This study was conducted between November 1995 and October 1997 in eight villages in Matlab, a sub-district in Chandpur district that is typical of the rural and riverine delta of Bangladesh (van Ginneken et al, 1998). Pregnant women at 5 – 7 months of gestation without any apparent chronic illness were eligible for the study. Trained Community Health Workers (CHWs) identified eligible subjects and new pregnancies. Written informed consent was obtained from each woman before enrollment. An interview was conducted on socioeconomic, demographic and household characteristics. The responses, along European Journal of Clinical Nutrition

with obstetric history, were recorded on precoded questionnaires. Weight, height and mid-upper-arm circumference were measured. Maternal weight was again measured once to twice during pregnancy, and at 1, 3 and 6 month(s) postpartum. Maternal dietary intake was assessed by 24 h dietary recall at entry, and at 1, 3 and 6 month(s) postpartum. Weight and length were measured soon after birth ( > 80% within 72 h after birth) and at about 1, 3 and 6 month(s) of age. In total, 335 women were enrolled during the study period of which 315 women delivered live singleton babies (one false pregnancy, three miscarriages, two twin deliveries, 10 still births, and four unknown). Out of these 315 mothers, 252 had complete baseline anthropometric and dietary data and infant anthropometric data taken at birth (19 migrated out, 22 refused to continue and another 22 had no maternal=infant anthropometric measurements). Characteristics of these 252 women are presented in Table 1. Baseline characteristics of the 83 women who were not included in the study were comparable with those included in the analysis.

Maternal anthropometry Anthropometric measurements were taken by trained workers following standard procedures (Gibson 1990). Weight of the women was measured on portable battery-operated SECA electronic scales (model 770) with digital displays accurate to the nearest 100 g. The scales were calibrated daily before use. Maternal height to the nearest 0.1 cm was measured using a locally made wooden measuring stick fixed to a flat wooden platform and a movable head plate. Mid-upper-arm circumference (MUAC) was measured to the nearest 1 mm at the mid-point between the shoulder and elbow on the women’s bare left arm with a non-stretchable MUAC tape. Body mass index (BMI; kg=m2) was calculated from weight and height data. Weekly pregnancy weight gain was calculated for each mother by subtracting the weight at entry from the last weight measured in pregnancy and then dividing the difference by the number of weeks between the measurements. Pregnancy weights of all the mothers were plotted against gestational age. Weight gain during pregnancy was also estimated using the slope of linear regression of maternal weight on gestational age. For each individual mother, monthly weight changes during the postpartum period were calculated by subtracting the weight measured at 6 months postpartum from that at 1 month postpartum. The pattern of maternal weight change during postpartum was also examined by plotting all the postpartum weights on the weeks of postpartum.

Infant anthropometry Weights of the infants were measured using a portable pediatric SECA beam balance (accurate to 10 g). The scale was calibrated daily by senior field staff and checked care-


153 fully before each measurement. Infants were weighed nude during hot weather or with light clothes on during cold weather; in the latter situation, the weight subtracting the weight of the clothes was recorded. Weight measured within 72 h or sooner after birth was recorded as the birth weight because there is no significant difference in birth weight and weight measured within the first 3 days of birth (Arifeen et al, 2000). Infants’ length was measured using a locally constructed wooden length board and measured to the nearest 0.1 cm. Weight and length were compared with the NCHS reference and converted to age- and sex-specific Z-scores using the ANTHRO software (Centre for Disease Control & WHO Nutrition Unit, 1992).

Maternal energy intake Energy intake was estimated by the 24 h dietary recall method following standardized procedures (Gibson, 1990). Nutrient intake was calculated using a computerized food composition table for Bangladeshi foods that was developed using nutrient data from regional food composition databases (National Institute of Nutrition, 1989; Helen Keller International, 1988). This computerized database was updated and supplemented for this study with the nutrient composition of multi-ingredient foods commonly consumed in the Matlab community. All commonly used local household measures were standardized (ml or g=unit) for respective food items during the initial phase of the study. Nutrient intake data were calculated using the computer package KOMEET, developed at the Wageningen University in Wageningen, The Netherlands.

Data analysis and statistics Results are presented as mean and standard deviation except where otherwise indicated. Group means were compared by Student’s t-test or one-way analysis of variance (ANOVA) when more than two group means were compared. Withinsubject repeated-measure ANOVA was used to examine whether there was any significant within-subject difference in energy intakes during pregnancy and postpartum measurements. If the F-statistic was significant in ANOVA, the Bonferroni test, which takes account of multiple comparisons, was used post-hoc to identify the individual means that were significantly different from one another. A P-value < 0.05 was considered statistically significant. All data analyses were performed using SPSS PC (version 7.5) for Windows.

Results During late pregnancy, mean ( s.d.) daily energy intake was 1464 416 kcal=day or 33 10 kcal=kg=day (Table 2). Postpartum energy intake increased significantly compared with intake during late pregnancy. The difference in mean ( s.d.) daily energy intake between late pregnancy and the post-

partum period ranged between 248 590 and 354 555 kcal=day (or 9 14 and 12 14 kcal=kg=day, respectively). Mean daily energy intake at 3 months postpartum was significantly greater than at 1 or 6 months postpartum. Pregnancy weight gain during the later half of pregnancy was 0.20 kg=week. The amount of weekly weight gain did not differ when calculated from changes in weight of individual women (Table 1) or estimated from the regression slope (Figure 1). As most women were measured more than once during pregnancy the data points used in the scatter plot were not truly independent. However, measurements on the same women were well balanced throughout the pregnancy period. This rate of weight gain means that women gained an estimated 4 kg during the second half of pregnancy in that population (ie 44.3 kg, and 48.3 kg at 20 and 40 weeks of gestation, respectively). During the postpartum period, mothers’ weight tended to decline. The mean weight loss between 1 and 6 months postpartum when calculated from the difference in weight of individual mothers was 1.07 kg (P < 0.005; Table 1). The regression slope derived from plotting maternal weight on postpartum week indicated a weekly weight loss of 46 g,

Table 1 Characteristics of the mothers at 5 – 7 months of pregnancy (n ¼ 252) Age (y) Gestational age (weeks) Education (y)a Parity Family size b Income (Taka) Weight (kg) Height (cm) MUAC (mm) BMIc (kg=m2) Pregnancy weight gain (g=week)d Postpartum weight loss (kg)e

26 6 25 3 3 3 2.2 1.5 5.7 2.8 36 000 (22 000 – 48 000) 45.2 5.4 149.5 5.3 227 18 20.2 1.9 200 120 1.07 2.20

All values are mean s.d. except where noted. Number of years attended at school. b Household annual income in Taka (1 US$ ¼ 57.3 Taka): median (25th and 75th percentiles). c BMI calculated based on weight measured at 5 – 7 months of pregnancy. d Pregnancy weight gain calculated from weight change in individual women (P < 0.001). e Weight loss calculated from change in weight in individual women between 1 and 6 month postpartum (P < 0.005). a

Table 2 Maternal energy intake during pregnancy and lactation Energy intake (kcal=day) Pregnancy 1 month postpartum 3 months postpartum 6 months postpartum

1464 416 1732 398 1800 421 1713 479

(252) a (189) a,b (145) a (199)

Energy intake (kcal=kg=day) 33 10 42 11 45 12 42 13

a

(252) (158) b (120) (136)

Values are mean s.d. (n). a Significantly higher than pregnancy intakes (P < 0.01). b Significantly different from 1 and 6 month(s) postpartum (P < 0.05).

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154

Figure 1

Maternal weight during pregnancy. Figure 3 Infant growth pattern (0 – 6 months). WAZ ¼ weight for age Z-score; LAZ ¼ length for age Z-score; WLZ ¼ weight for length Z-score. Compared with Z-score at birth: *P < 0.05, **P < 0.01.

Figure 2

Maternal weight during postpartum.

although it did not reach statistical significance (Figure 2). Maternal weights in the scatter plot were clustered around 5, 15 and 28 weeks; however, each woman contributed a maximum of once in each of those clusters of measurements. According to the obtained regression line, maternal weight was estimated to be 41.8 and 40.8 kg at 1 and 6 months, respectively, indicating a weight loss of 1 kg between 1 and 6 month(s) postpartum, which is, consistent with that obtained from the changes in weight of individual mothers. European Journal of Clinical Nutrition

The mean ( s.d.) weight of the infants at birth was 2.55 0.38 kg and 48% had low birth weight (less than 2.50 kg at birth). At birth the infants were relatively shorter and thinner compared to those in the NCHS reference population (Figure 3). There was a small but significant increase in length-for-age Z-scores (LAZ) at 1 month of age compared with that at birth, at which their catch-up in length plateaud approximately at 7 1.4 s.d. Infants performed relatively better by weight for length Z-scores (WLZ) which were significantly higher at 1 and 3 month(s) compared with that at birth. At 6 months WLZ declined slightly and tended to be lower than at 3 months and fell below the reference median. Although always remaining far below the reference median, infants’ weight for age Z-scores (WAZ) were significantly higher at 1 and 3 month(s) compared with that at birth, but this catch-up in weight gain was not sustained in the following months. Although breastmilk was the main source of nutrients up to 6 months of age, 70% and 37% were exclusively breastfed up to 3 and 6 months, respectively (data not presented).

Discussion The main aim of this study was to examine the response of women in rural Bangladesh to the energy demanding periods of pregnancy and lactation, and its effect on maternal energy stores (body weight). This study has clearly demonstrated that poorly nourished rural women fail to compensate during these critical periods of energy demand. This is reflected by low pregnancy weight gain and substantial


155 postpartum weight loss. This low maternal energy intake and low pregnancy weight gain is also consistent with low mean birth weight and high prevalence of low birth weight. Of interest and potentially significant programmatic relevance, the growth performance of the infants who were primarily breastfed up to 6 months of age showed only an inadequate catch-up growth, which was not sustained beyond 3 months. Since there was no obvious indication of increased maternal fat stores during pregnancy, a decline in maternal body weight during lactation indicates a compromised maternal ability to deal with energy stress during lactation in this community. Maternal energy intake during 5 – 7 months of pregnancy was only 1464 kcal=day. Studies have shown that energy intake during pregnancy either remain unchanged or increased only slightly in late pregnancy (van Raaij et al, 1987; Tuazon et al, 1987). Although low, the energy intake observed in this study may be considered as the usual intake by pregnant women in rural Bangladesh. This pattern of intake is consistent with the intake pattern reported previously (Hassan et al, 1985). Energy intake assessment is often subject to under-reporting by the subjects (Carter & Whiting, 1998). However, energy intake observed in these poor and non-obese women is unlikely to be under-reported because dietary data and our observation suggest that their dietary pattern consists of a limited number of food items, a fairly fixed meal pattern (two to three meals per day), a virtual lack of snack foods or drinks and no tradition or facilities for the women to eat out. A key question is whether or not the observed energy intake in these women is adequate in relation to their energy requirements. However, a major and direct outcome of energy balance during pregnancy is pregnancy weight gain, which we measured in this study. These women gained about 4 kg during the second half of pregnancy, which is less than half the usual weight gain by well-nourished Western women in this same period (Hytten, 1991; van Raaij et al, 1987; Institute of Medicine, 1990). This low pregnancy weight gain itself is a clear indication of a gross inadequacy of dietary energy intake during pregnancy. In well-nourished Western mothers, weights at mid-pregnancy are nearly on the same level as that at 1 month postpartum (Hytten, 1991). Weights at these two periods represent prepregnancy weight plus additional weight mainly attributable to fat mass gained during early pregnancy and that retained after delivery, respectively. Recent review has shown that the amount of gain in fat mass is about 2 – 2.5 kg in high-income Western countries (Prentice et al, 1996). The extrapolated weight at mid-pregnancy was estimated to be 44.3 kg and at 1 month postpartum was 41.8 kg in those study women, a difference of 7 2.5 kg. This lower weight at 1 month postpartum compared with that at mid-pregnancy suggests that mothers in this study did not possibly accrue any fat during the first half of pregnancy, and that their 1 month postpartum weight represented their approximate prepregnancy weight.

The women in our study increased their energy intake quite substantially (248 – 354 kcal=day) during lactation compared to their intake during 5 – 7 months of pregnancy. Such increases are expected because of higher energy demand during lactation to support the energy cost of breast milk, and these amounts are comparable with those observed in other populations (van Raaij et al, 1991; Sadurskis et al, 1988). We also observed significantly higher energy intake at 3 months postpartum compared with 1 or 6 month(s) postpartum, which coincides with peak lactation (Prentice et al, 1996). However, the increase in energy intake during lactation over that during pregnancy is only about half the estimated extra energy required for lactation (FAO= WHO=UNU, 1985). This means that, if other sources of energy were not available, women would undergo a negative energy balance. Our observation is supported by a recent study in a small number of malnourished Bangladeshi women, which reported a negative energy balance at 3 and 10 months of lactation (Vinoy et al, 2000). Breast milk has been shown to be adequate for growth during the first 6 months of age even in poor communities (Dewey, 1998). Both WHO and UNICEF currently recommend exclusive breastfeeding until 6 months of age. Therefore, growth of breastfed infant can be considered as a proxy indicator of adequacy of lactation. In this community prolonged breastfeeding is traditional and breast milk serves as an exclusive or predominant source of nutrients for infants up to 6 months (Huffman et al, 1980). Infants in this study were born relatively shorter and thinner and had lower mean birth weight compared to the reference population. They showed only limited catch-up in both linear and ponderal growth, which was not sustained beyond 3 months. This is a growth pattern almost similar to WHO breastfed cohort, although these infants’ growth curve followed a lower level compared with a reference as well as the WHO breastfed cohort (WHO Working Group on Infant Growth, 1995). This pattern of infant growth raises concern about the adequacy of lactation in malnourished women who live on very low dietary energy. However, it is clearly evident from maternal pregnancy weight gain that there are few possibilities for mothers to enter lactation with any additional energy reserves. Therefore, 1 kg weight loss in these mothers during lactation suggests substantial depletion of maternal stores. More importantly, the mothers’ very poor nutritional status is likely to have greater implications for subsequent pregnancies, particularly if the next pregnancy occurs soon. From these findings we conclude that mothers in this poor rural community failed to gain sufficient weight during the last half of pregnancy to maintain maternal body weight during lactation when the energy demand is high. Although basic data on energy expenditure are not available for this population, it is clear that to protect maternal stores a substantial increase in energy intake and a reduction in physical activity or, preferably, a combination of both, should be achieved during these periods. Further studies should be undertaken to quantify health and nutritional European Journal of Clinical Nutrition


156 consequences both for mothers and infants in situations such as this with critical energy balances. The situation of pregnant Bangladeshi women is really critical and needs immediate intervention to protect maternal nutrition and to prevent extremely high occurrence of low birth weight in this population.

Acknowledgements This study was conducted at ICDDRB: Centre for Health and Population Research with support from a grant USAID=OMNI HNI’s CA no. HRN-5122-A-00-3046-00-(‘CA’). ICDDRB acknowledges with gratitude the commitment of USAID=OMNI to the Centre’s research efforts. We are thank˚ ke Persson for his valuable suggestions ful to Professor Lars A on the initial version of this manuscript. Financial support from the Division of Human Nutrition and Epidemiology at Wageningen University during analysis and write-up is gratefully acknowledged.

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