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Journal of the American College of Nutrition

ISSN: 0731-5724 (Print) 1541-1087 (Online) Journal homepage: http://www.tandfonline.com/loi/uacn20

Regional Body Composition Changes during


Lactation in Indian Women from the Low-Income
Group and Their Relationship to the Growth of
Their Infants

Bharati Kulkarni MBBS, DCH, MPH, Veena Shatrugna MD, Balakrishna


Nagalla PhD & K. Usha Rani BCom

To cite this article: Bharati Kulkarni MBBS, DCH, MPH, Veena Shatrugna MD, Balakrishna
Nagalla PhD & K. Usha Rani BCom (2011) Regional Body Composition Changes during
Lactation in Indian Women from the Low-Income Group and Their Relationship to the
Growth of Their Infants, Journal of the American College of Nutrition, 30:1, 57-62, DOI:
10.1080/07315724.2011.10719944

To link to this article: http://dx.doi.org/10.1080/07315724.2011.10719944

Published online: 09 Jun 2013.

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Original Research

Regional Body Composition Changes during Lactation


in Indian Women from the Low-Income Group and Their
Relationship to the Growth of Their Infants

Bharati Kulkarni, MBBS, DCH, MPH, Veena Shatrugna, MD, Balakrishna Nagalla, PhD, K. Usha Rani, BCom
National Institute of Nutrition, Indian Council of Medical Research, Hyderabad, INDIA
Key words: lactation, infant growth, regional body composition, fat mass, fat-free mass, appendicular skeletal mass, Indian
women

Background: Increased energy requirement during lactation may lead to maternal tissue depletion in women
from poor subsistence communities.
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Objectives: To examine the regional body composition changes in undernourished lactating women and to
assess the relationship of maternal body composition changes with weight gain of the infants.
Subjects and Methods: Body composition was assessed using dual energy x-ray absorptiometry in 35
lactating women at 4 time points: within 1 month after delivery (baseline) and at 6, 12, and 18 months
postpartum.
Results: The mean age, height, and body mass index of the women were 23.5 years, 150.7 cm, and 20.0 kg/
m2, respectively. There were no significant differences in body weight or whole-body lean as well as fat mass at 4
time points, but the percentage fat decreased significantly during lactation. There was selective mobilization of fat
mass from the leg region, whereas the appendicular skeletal mass (ASM) increased significantly. When the
growth of the infants in the first 6 months (proxy for the lactation performance) was assessed in relation to the
maternal body composition changes during that period, it was observed that the change in fat mass had a negative
relationship to the weight gain of the infant. Change in the ASM during this period, however, had a significant
positive relationship with the weight gain of the infants.
Conclusion: There were important differences in the lactation-related changes in the regional body
composition parameters of these undernourished women. Regional body composition changes may be related to
the weight gain of the breast-fed infants.

INTRODUCTION adaptations and body composition changes may be different


among these 2 groups of women.
Maternal energy requirements are greatest during lactation. A large number of studies have investigated body
The increased energy demand during lactation is usually met composition changes in lactating women to assess the extent
through multiple strategies such as increased energy intake, to which fat mobilization helps in subsidizing the energy cost
energy sparing through decreased physical activity, or possible of lactation [7–10]. Most of these studies were carried out in
energy-sparing adaptations [1,2], as well as mobilization of fat women from developed countries, and these studies indicated
from maternal reserves developed during pregnancy [3–5]. that fat mass changes during lactation may be highly variable
Healthy women from well-to-do families appear to meet their among women [11]. However, there have been few longitu-
extra energy demand mainly by increases in energy intake [6], dinal studies in undernourished women from developing
whereas for women from poor subsistence communities, it may countries beyond 6 months postpartum [10,12].
not be possible to increase their energy intake or decrease Studies from India have indicated that women from low-
physical activity. It is therefore possible that the metabolic income groups do not have adequate weight gain during

Address correspondence to: Bharati Kulkarni, MBBS, DCH, MPH, Scientist C, National Institute of Nutrition, Indian Council of Medical Research, Jamai Osmania P.O.,
Hyderabad 500 007, INDIA. E-mail: bharati70@yahoo.com
The authors declare no conflict of interest. This work was supported by the Indian Council of Medical Research.

Journal of the American College of Nutrition, Vol. 30, No. 1, 57–62 (2011)
Published by the American College of Nutrition

57
Regional Body Composition Changes during Lactation

pregnancy with probably low fat mass accrual [13]. Thus, these Procedures
women start lactation without adequate energy reserves. In
Anthropometry. Maternal weight was measured without
addition, they breast-feed their infants for a period of 18–24
footwear to the nearest 0.1 kg on lever type SECA balance
months postpartum and have short interpregnancy intervals. It
(Hamburg, Germany). Heights were measured to the nearest
is possible that the energy stress during lactation leads to
0.1 cm with a stadiometer (SECA, UK). The infant’s weight
maternal tissue depletion.
was measured with a lever-type SECA mechanical baby beam
A few studies that have explored regional body fat changes
balance (Hamburg, Germany), and length was measured with
in lactating women indicated that there are regional differences
an infantometer made in house at our institute. Quality control
in mobilization of body fat during this period [14], which may
checks were carried out every 3 months.
alter the regional fat distribution. Since regional fat distribution
Body Composition Measurements. Body composition
is important for evaluating the health risks of an individual
measurements including whole-body lean mass, fat mass, and
[15], it is necessary to assess the lactation-related changes in
percentage of fat mass as well as regional fat and lean mass
regional fat distribution. This descriptive longitudinal study were assessed using dual energy x-ray absorptiometry (DXA;
was therefore carried out to examine the regional body Hologic 4500W, Waltham, MA). Standard Hologic software
composition changes in undernourished lactating women for options were used to define regions of the body (head, arms,
18 months postpartum. In addition, we also assessed whether trunk, and legs). Appendicular skeletal muscle mass (ASM)
the weight gain of the infants was related to the body was calculated as the sum of lean mass in both the right and left
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composition changes in their mothers. arms and legs [17].


The scanner was calibrated daily, and its performance was
monitored as per the quality assurance protocol. All of the
SUBJECTS AND METHODS scans and analyses were carried out by a trained technician
according to the manufacturer’s instructions. No sign of
Details regarding subjects, study design, sample size scanner drift was observed during the study period. The in
estimation, and procedures are published elsewhere [16]. Some vivo precision (coefficient of variation) for percentage body fat
of the relevant details are described below. Forty consecutive estimation was 1.7%.
women who had undergone tubal ligation and attended the
postpartum follow-up clinic in a large government maternity Statistical Analyses
hospital (Hyderabad, India) were recruited for this study during
the period of June 2002 to September 2002. Only the women SPSS Windows version 14.0 was used for statistical
who had undergone tubal ligation were enrolled in this study so analysis. Descriptive statistics were calculated for all of the
that it would be possible to follow up with them and repeat body composition parameters and anthropometric measure-
body composition assessment until 18 months postpartum. All ments of mother and offspring at different time points. Mean
of the women had established breast-feeding and visited the values of body composition parameters at different time points
clinic for their first follow-up within 1 month postpartum. The were compared by repeated measures analysis of variance with
study was approved by the institutional ethics committee. post hoc test for each site. Regression models were built to
Informed consent was obtained from all the subjects. study the relationship of weight gain of the breast-fed infants in
the first 6 months of the study as a dependent variable and
change in maternal fat mass and ASM, maternal weight at
Study Design
baseline, infant’s birth weight, and interval between the baseline
Subjects were examined at 4 time points during the study and 6-month follow-up examinations as independent variables.
period: within 1 month after delivery (baseline) and at 6, 12,
and 18 months after delivery. At each time point, the following
were assessed: maternal anthropometry (height at baseline and RESULTS
weight), infant’s weight and length, and maternal body
composition including lean mass, fat mass, and percentage A total of 40 women were recruited for the study. However,
fat. Information regarding resumption of menstruation and 35 women completed follow-up until 18 months. The reasons
introduction of complementary foods was collected at each for loss to follow-up were a change of residence (in 3 women)
time point. However, the amount of complementary foods and cessation of breast-feeding consequent to child’s illness (in
consumed by the infants as well as the frequency of breast- 2 women). Characteristics of the women who were lost to
feeding were not measured. Customary medical care and follow-up were not different from the study women. The
nutrition advice were provided to all of the subjects. The women belonged to the low-income group, and their mean
women breast-fed as long as they wished. They were advised to (SE) age, height, weight, and body mass index were 23.5 (0.5)
start energy-dense complementary foods at 6 months of age as years, 150.7 (0.8) cm, 45.5 (0.9) kg, and 20.0 (0.4) kg/m2,
per the World Health Organization (WHO) guidelines. respectively. The mean (SE) birth weight was 2.8 (0.6) kg, and

58 VOL. 30, NO. 1


Regional Body Composition Changes during Lactation

Table 1. Changes in Maternal Regional Body Composition Parameters and Infant Growth during 18 Months Postpartum (N ¼ 35)

Baseline 6 Months 12 Months 18 Months


Mean SE Mean SE Mean SE Mean SE p Value
Arm
Fat mass 1.26 0.07 1.35 0.08 1.28 0.09 1.25 0.09 0.171
Lean mass 2.84a 0.06 2.89ab 0.05 2.95b 0.05 3.00c 0.06 ,0.001
Leg
Fat mass 5.40a 0.26 5.23a 0.27 5.03b 0.29 5.06ab 0.28 0.039
Lean mass 8.79a 0.17 9.08b 0.17 9.16bc 0.17 9.20c 0.17 ,0.001
Trunk
Fat mass 5.36 0.32 5.62 0.39 5.19 0.41 5.15 0.42 0.070
Lean mass 15.70a 0.22 15.19b 0.23 14.98b 0.20 15.13b 0.20 ,0.001
Whole body
Fat mass 12.73 6.25 12.90 6.96 12.21 7.63 12.15 7.43 0.112
Lean mass 30.04 0.43 29.86 0.42 29.78 0.40 30.00 0.41 0.491
% Fat 28.3ab 0.90 28.5a 1.01 27.3b 1.10 27.1b 1.07 0.025
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Weight 45.8 0.95 45.4 1.01 45.0 1.07 44.6 1.14 0.180
Weight of infant 3.1a 0.07 6.5b 0.13 7.9c 0.15 8.6d 0.17 ,0.001
WAZ 0.9a 0.13 0.83a 0.15 1.58b 0.15 1.94c 0.15 0.020
Length of infant 50.6a 0.36 65.4b 0.53 72.8c 0.50 77.4d 0.58 ,0.001
LAZ 0.33a 0.17 0.20ab 0.20 0.54b 0.19 1.15c 0.21 0.027
Lean mass and fat mass in kilograms; weight and weight of infant in kilograms; length of infant in centimeters. Different superscripts within a row indicate significant
differences (p , 0.05) at different time points. A p value of ,0.05 indicates the overall significant difference between 4 time points.
WAZ ¼ weight for age Z score; LAZ ¼ length for age Z score.

the mean (SE) duration of postpartum amenorrhea was 7.0 6 months (proxy for the lactation performance of a woman)
(0.8) months. Their dietary intakes have been published was related to the body composition changes during that
elsewhere [16]. Diets were typically cereal based, and intake period. Weight gain of the infant during the period between
of all of the major nutrients was below the recommended daily baseline and 6-month follow-up was the dependent variable,
allowance. All of the women except 2 breast-fed their infants and maternal weight at baseline, birth weight of the infant,
throughout the study period. One woman stopped breast- change in fat mass, and change in ASM in 6 months were
feeding at 6 months and the other at 12 months postpartum. included as independent variables (Table 2). While the lean
mass in the arms and legs increased, the lean mass in the trunk
Body Composition Changes during Lactation regions reduced significantly during lactation. Since changes in
the whole-body lean mass did not reflect these regional
Regional body composition estimates during follow-up are differences, only the ASM was included in the regression
presented in Table 1. Although the whole-body fat mass and model. It may be observed that loss of 1 kg maternal fat mass
lean mass did not show significant changes during lactation,
there were significant changes in the regional body composi-
Table 2. Multiple Linear Regression of Weight Gain of the
tion parameters. Fat mass in the arm region did not change,
Breast-Fed Infants in the First 6 Months of the Study on
whereas fat mass in the leg region reduced significantly at 1 Change in Maternal Fat Mass and Appendicular Skeletal Mass
year after delivery. There was also a significant increase in the (ASM), Maternal Weight at Baseline, and Infant’s Birth
lean mass of the arms and legs, whereas the lean mass in the Weight
trunk region reduced significantly. Although the mean body
weight reduced by 1.2 kg from baseline to 18 months, this Weight Gain of the
Infant in 6 Months (kg)
change was not statistically significant. Percentage body fat,
however, reduced significantly by 1 year. Infant weight and b Coefficient SE p Value
length measurements during the 18-month period showed Constant 1.666
progressive growth faltering. Change in fat mass in 6 months 0.107 0.050 0.039
(kg)
Change in ASM in 6 months (kg) 0.580 0.216 0.013
Regression Analysis Maternal weight at baseline (kg) 0.031 0.297 0.176
Multiple linear regression analysis was performed to Birth weight of the infant (kg) 0.390 0.313 0.202
explore if the weight gain of the breast-fed infants in the first R2 ¼ 0.325, p ¼ 0.011.

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 59


Regional Body Composition Changes during Lactation

during lactation was associated with about 107 g higher weight nonlactating state. However, additional requirement for the
gain in the infant. However, increase in ASM by 1 kg was growth of maternal tissues in these young women have not
associated with about 580 g higher weight gain in the infant. been considered. It is reassuring that there was an increase in
Overall, the model explained 32.5% variation in the weight lean body mass during lactation in this group of undernour-
gain of the infants and was highly significant. ished women despite their poor diets and extra demands
imposed by breast-feeding. It is important to investigate
whether energy-protein supplementation during lactation
DISCUSSION enhances the lean mass in young lactating women. In contrast,
a study in undernourished Bangladeshi women indicated that
This is one of the few studies that have investigated regional these women lost fat-free mass during lactation [12]. It is
body composition changes in undernourished lactating women difficult to compare the results of these 2 studies because body
who breast-fed their infants for a prolonged time. composition was assessed using different methods, and women
Surprisingly, despite prolonged lactation and poor dietary in the Bangladesh study were older and suffered from a more
intakes of almost all of the nutrients including energy, severe form of chronic energy deficiency. It is possible that the
prolonged lactation was not associated with significant loss women in the present study were able to lay down lean body
of weight or lean mass in these women, although their body fat mass as they were younger and had not attained peak lean body
percentage decreased significantly. This is in contrast to earlier mass.
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studies in undernourished women from India, Bangladesh, and Regression analysis in Table 2 indicates some important
Gambia that have reported that women underwent moderate findings about the relationship of maternal body composition
weight loss [5,12,18]. Data collected from the women showed changes in lactating women to the weight gain of the breast-fed
that they probably conserved energy by opting out of the labor infants in the first 6 months. Weight gain of the infants in 6
force for a period of 1 to 1.5 years. months may be considered as proxy for the lactation
Changes in regional body composition parameters reveal performance of the mothers as the infants were nearly
important differences in the fat mobilization from different exclusively breast-fed. Since birth weight of the infant may
regions. It appears that there was selective mobilization of fat have a positive relationship to the infant’s weight gain as well
from the leg region. A number of previous studies have as breast milk output, birth weight was included as an
indicated that lactating women lose lower body fat [14,19]. The independent variable in the model. It is interesting to note that
concentration of long-chain fatty acids, which are critical for after adjusting for the maternal weight at baseline, change in fat
growing fetal and infant brain, is higher in lower-body fat than mass from baseline to 6 months had a negative relationship
in abdominal fat [20]. Mobilization of lower-body fat during with the weight gain of the infant. Change in lean body mass,
lactation may be a mechanism to ensure that the fatty acids however, had a positive relationship with the weight gain of the
necessary for the brain development of the infant are available. infants.
Since different fat stores respond differently during lactation, It may be speculated that mobilization of body fat in women
body composition measurements providing only the whole- may be associated with higher weight gain in the infants due to
body estimates may be inadequate. higher energy content of the breast milk of those women. A
Changes in the lean body mass in the study women show number of studies have demonstrated that breast milk fat
interesting patterns. There was significant reduction in the lean content is related to maternal body fat [22,23]. It is possible
mass in the trunk region, whereas the lean mass in the arm and that the mobilized fat was transferred to the breast milk,
leg regions increased significantly. As lean tissue in the arms improving the energy density of the milk and, therefore, the
and legs is mainly skeletal muscle, it is interesting to note that growth of the baby.
these undernourished women are laying down muscle mass Change in the ASM, on the other hand, had a positive
during lactation. An earlier study on the bone density changes relationship with the weight gain of the infants. This has not
during lactation in this group of women indicated absence of been reported earlier, although the relationship of maternal lean
bone loss at the lumbar spine region, possibly because these mass with birth weight has been reported in a number of
women had not attained their peak bone mass. Therefore, studies. Studies from our institute have also indicated that
despite substantial losses of calcium in breast milk, it was maternal lean body mass was the most important determinant
possible for them to resist the bone loss in an attempt to achieve of the infant’s birth weight [24].
peak bone mass. A similar phenomenon may explain the It may be speculated that women who managed to accrue
increase in the lean body mass in this group as the growth of lean body mass during lactation had better intakes of nutrients
lean body mass and bone density are thought to be coupled [21]. such as protein and certain micronutrients that are required for
Nutrient requirements of lactating women are calculated muscle tissue synthesis. The better nutrient intakes may have
using the factorial approach (i.e., by adding the nutrient affected the concentration of these nutrients in breast milk and
requirement for milk synthesis to the requirements during the thereby infant growth. One may also speculate about an

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Regional Body Composition Changes during Lactation

underlying hormonal mechanism that could explain the body composition changes to the infant growth. For this
observed association between increase in maternal ASM and analysis, weight gain of the infants during first 6 months was
the growth of the breast-fed infants. It is well established that considered as a proxy for the lactation performance since most
growth hormone (GH) and insulin-like growth factor-I (IGF1) of the infants did not receive any complementary feeds during
levels have a positive association with muscle mass [25]. the first 6 months.
Studies in lactating Brazilian women have demonstrated that This study thus provides important information regarding
higher circulating IGF1 levels were associated with higher the lactation-related changes in the regional body composition
bone mineral deposition [26]. On the other hand, animal of young Indian women from the low socioeconomic group.
experiments have indicated that IGF1 is a potent and specific The study raises important questions regarding recommended
secretagogue of prolactin in vertebrates [27]. IGF1 is also dietary allowances of the lactating women who may have not
known to stimulate the synthesis and release of prolactin from completed their tissue growth. The study also indicates
human decidual cells [28]. In addition, the stimulatory effect of interesting relationships between maternal tissue growth and
GH on mammogenesis and lactogenesis has been well the growth of the breast-fed infants. The significance of
established by numerous in vitro and in vivo studies [29]. maternal lean body mass during the nutritionally demanding
GH is the major galactopoietic hormone in cows and is phase of lactation for maternal and infant well-being is an
commonly used to increase milk yield in commercial dairy unexplored area and requires investigation.
herds [30,31]. Experimental studies in mothers of preterm as
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well as term infants indicated that supplementation of human


recombinant growth hormone to lactating women resulted in a ACKNOWLEDGMENTS
significant increase in their breast milk output [32–34]. GH
stimulates milk production during lactation, and it has been This study was funded by the Indian Council of Medical
proposed that this is mediated indirectly via the production of Research. The sponsor of the study had no role in study design,
IGF1 [35]. Therefore, it is possible that the women who had data collection, data analysis, data interpretation, or writing of
higher circulating levels of GH and IGF1 demonstrated a the article. The authors declare that they have no conflict of
higher increase in ASM and also had increased milk output that interest. Bharati Kulkarni and Veena Shatrugna contributed to
resulted in higher weight gain of their breast-fed infants. the study design, subject recruitment, interpretation of the
However, we did not estimate IGF1 and GH levels in these results, and article preparation. N. Balakrishna carried out
women. Further studies are necessary to test this hypothesis. statistical analysis of the data, and K. Usha Rani was
The strengths of this study include assessment of regional responsible for the body composition measurements by DXA.
body composition using DXA and examination of the All of the authors reviewed and approved the final version of
relationship of maternal body composition changes with the the article. The authors would like to thank the directors of the
growth of the breast-fed infants. The study is unique, with National Institute of Nutrition, Hyderabad, India, who provided
subjects having grossly inadequate intakes of all the nutrients, the facilities and support system to carry out this work. We are
prolonged breast-feeding with little complementary foods, and grateful to Ms B. Prema Kumai, Ms K. Sundaramma, and Mr
prolonged follow-up. The limitations of this study may be R. Sambasiva Rao for their help during the course of the study.
related to the lack of information on IGF1 and growth hormone This study would not have been possible without the unstinting
levels and breast milk output in the study women. It is possible cooperation of the women who were subjects of the study, and
that the frequency and intensity of breast-feeding may affect we are grateful to them.
the body composition changes in lactating women. A study in
Caucasian women found that fat loss was linked to more
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