Professional Documents
Culture Documents
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
Article views: 29
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.
Downloaded by [Emory University] at 09:02 18 February 2016
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.
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
Downloaded by [Emory University] at 09:02 18 February 2016
Table 1. Changes in Maternal Regional Body Composition Parameters and Infant Growth during 18 Months Postpartum (N ¼ 35)
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.
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.
Downloaded by [Emory University] at 09:02 18 February 2016
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
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
Downloaded by [Emory University] at 09:02 18 February 2016
5. Rah JH, Christian P, Shamim AA, Arju UT, Labrique AB, Rashid 22. Barbosa L, Butte NF, Villalpando S, Wong WW, Smith EO:
M: Pregnancy and lactation hinder growth and nutritional status of Maternal energy balance and lactation performance of Mesoamer-
adolescent girls in rural Bangladesh. J Nutr 138:1505–1511, 2008. indians as a function of body mass index. Am J Clin Nutr 66:575–
6. Piers LS, Diggavi SN, Thangam S, van Raaij JM, Shetty PS, 583, 1997.
Hautvast JG: Changes in energy expenditure, anthropometry, and 23. Martin JC, Bougnoux P, Fignon A, Theret V, Antoine JM,
energy intake during the course of pregnancy and lactation in well- Lamisse F, Couet C: Dependence of human milk essential fatty
nourished Indian women. Am J Clin Nutr 61:501–513, 1995. acids on adipose stores during lactation. Am J Clin Nutr 58:653–
7. Brewer MM, Bates MR, Vannoy LP: Postpartum changes in 659, 1993.
maternal weight and body fat depots in lactating vs nonlactating 24. Bharati K, Shatrugna V, Balakrishna N: Maternal lean body mass
women. Am J Clin Nutr 49:259–265, 1989. may be the major determinant of birth weight—a study from India.
8. Forsum E, Sadurskis A, Wager J: Estimation of body fat in healthy Eur J Clin Nutr 60:1341–1344, 2006.
Swedish women during pregnancy and lactation. Am J Clin Nutr 25. Vandenburgh HH, Karlisch P, Shansky J, Feldstein R: Insulin and
50:465–473, 1989. IGF-I induce pronounced hypertrophy of skeletal myofibers in
9. Chou TW, Chan GM, Moyer-Mileur L: Postpartum body tissue culture. Am J Physiol 260:C475–C484, 1993.
composition changes in lactating and non-lactating primiparas. 26. O’Brien KO, Donangelo CM, Zapata CL, Abrams SA, Spencer
Nutrition 15:481–484, 1999. EM, King JC: Bone calcium turnover during pregnancy and
10. González HF, Malpeli A, Mansur JL, De Santiago S, Etchegoyen lactation in women with low calcium diets is associated with
GS: Changes in body composition in lactating adolescent mothers. calcium intake and circulating insulin-like growth factor 1
Arch Latinoam Nutr 55:252–256, 2005. concentrations. Am J Clin Nutr 83:317–323, 2006.
Downloaded by [Emory University] at 09:02 18 February 2016
11. Butte NF, Hopkinson JM: Body composition changes during 27. Fruchtman S, Jackson L, Borski R: Insulin-like growth factor I
lactation are highly variable among women. J Nutr 128:381S– disparately regulates prolactin and growth hormone synthesis and
385S, 1998. secretion: studies using the teleost pituitary model. Endocrinology
12. Vinoy S, Rosetta L, Mascie-Taylor CG: Repeated measurements of 141:2886–2894, 2000.
energy intake, energy expenditure and energy balance in lactating 28. Thrailkill KM, Golander A, Underwood LE, Handwerger S:
Bangladeshi mothers. Eur J Clin Nutr 54:579–585, 2000. Insulin-like growth factor I stimulates the synthesis and release of
13. National Institute of Nutrition: ‘‘Annual Report (2002).’’ New prolactin from human decidual cells. Endocrinology 123:2930–
Delhi/Hyderabad, India: Indian Council of Medical Research, 2934, 1988.
2002. 29. Hull KL, Harvey S: Growth hormone: roles in female reproduc-
14. Kramer FM, Stunkard AJ, Marshall KA, McKinney S, Liebschutz tion. J Endocrinology 168:1–23, 2001.
J: Breast-feeding reduces maternal lower-body fat. J Am Diet 30. Tauer LW, Knoblauch WA: The empirical impact of bovine
Assoc 93:429–433, 1993. somatotropin on New York dairy farms. J Dairy Sci 80:1092–
15. Piché ME, Lapointe A, Weisnagel SJ, Corneau L, Nadeau A, 1097, 1997.
Bergeron J, Lemieux S: Regional body fat distribution and 31. Etherton TD, Bauman DE: Biology of somatotropin in growth and
metabolic profile in postmenopausal women. Metabolism lactation of domestic animals. Physiol Rev 78:745–761, 1998.
57:1101–1107, 2008. 32. Milsom SR, Breier BH, Gallaher BW, Cox VA, Gunn AJ,
16. Kulkarni B, Shatrugna V, Nagalla B, Ajeya Kumar P, Usha Rani Gluckman PD: Growth hormone stimulates galactopoiesis in
K, Chandrakala Omkar A: Maternal weight and lean body mass healthy lactating women. Acta Endocrinol 127:337–343, 1992.
may influence the lactation-related bone changes in young 33. Gunn AJ, Gunn TR, Rabone DL, Breier BH, Blum WF, Gluckman
undernourished Indian women. Br J Nutr 101:1527–1533, 2009. PD: Growth hormone increases breast milk volumes in mothers of
17. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D: preterm infants. Pediatrics 98:279–282, 1996.
Total-body skeletal muscle mass: estimation by a new dual-energy 34. Kaplan W, Sunehag AL, Dao H, Haymond MW: Short-term
x-ray absorptiometry method. Am J Clin Nutr 76:378–383, 2002. effects of recombinant human growth hormone and feeding on
18. Prema K, Madhavapeddi R, Ramalakshmi BA: Changes in gluconeogenesis in humans. Metabolism 57:725–732, 2008.
35. Bauman DE, Vernon RG: Effects of exogenous bovine somato-
anthropometric indices of nutritional status in lactating women.
tropin on lactation. Annu Rev Nutr 13:437–461, 1993.
Nutr Rep Int 24:893–900, 1982.
36. Quandt SA: Changes in maternal postpartum adiposity and infant
19. Lassek WD, Gaulin SJ: Changes in body fat distribution in relation
feeding patterns. Am J Phys Anthropol 60:455–461, 1983.
to parity in American women: a covert form of maternal depletion.
37. Barbosa L, Butte NF, Villalpando S, Wong WW, Smith EO:
Am J Phys Anthropol 13:295–302, 2006.
Maternal energy balance and lactation performance of Mesoamer-
20. Phinney SD, Stern JS, Burke KE, Tang AB, Miller G, Holman RT:
indians as a function of body mass index. Am J Clin Nutr 66:575–
Human subcutaneous adipose tissue shows site-specific differences
853, 1997.
in fatty acid composition. Am J Clin Nutr 60:725–729, 1994.
21. Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R: The
‘‘muscle-bone unit’’ during the pubertal growth spurt. Bone
34:771–775, 2004. Received August 5, 2009; revision accepted January 4, 2010.