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U.S. Department of Agriculture/ARS Childrens Nutrition Research Center, Houston, TX 77030 and Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030
2To whom correspondence should be addressed at 1100 Bates. E-mail: nbutte{at}bcm.tmc.edu
| ABSTRACT |
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KEY WORDS: lactation breastfeeding energy requirements doubly labeled water humans
| INTRODUCTION |
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The purpose of this study was threefold: to estimate the energy requirements of lactation by measuring milk production and composition, body weight and composition and TEE; to compare these estimates to energy requirements in the nonpregnant, nonlactating state; and to test for energetic adaptations in BMR and physical activity during the energy-demanding process of lactation.
| SUBJECTS AND METHODS |
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Measurements of TEE, BMR, anthropometry and body composition were performed on 24 healthy women at 3 mo and again at 18 or 24 mo postpartum at the Childrens Nutrition Research Center. Subjects were recruited in their third trimester of pregnancy and were required to be healthy, normotensive, nonsmoking and nondiabetic with the intention to breastfeed exclusively for a minimum of 4 mo. At 3 mo postpartum, the women were exclusively breastfeeding and milk production was assessed. By 6 mo, 4 women were exclusively breastfeeding, 15 were partially breastfeeding and 5 had weaned. The mean duration of breastfeeding was 320 ± 154 d. At 18 or 24 mo, the women were no longer breastfeeding. Body composition measurements taken at 0.5 mo postpartum were used to compute changes in weight, fat-free mass (FFM) and fat mass (FM) during the 0.5- to 3-mo period of exclusive breastfeeding. This study was approved by the Baylor Affiliates Review Board for Human Subject Research, and informed written consent was obtained from each woman.
The women had unremarkable health histories and pregnancies. Maternal
age averaged 30.4 ± 3.2 y. Ethnic distribution consisted of
20 Caucasian, one African-American, one Hispanic and two Asian
women. Median gravidity and parity were 2 (range 15) and 0.5 (range:
03), respectively. Attained level of education was 17 ± 2 y.
Maternal prepregnancy weight (by subject recall) and body mass index
averaged 59.1 ± 9.0 kg and 22.1 ± 3.1
kg/m2, respectively. Mean gestational weight gain
was 16.0 ± 3.8 kg; 50% of the women made gains within the
Institute of Medicinerecommended ranges for gestational weight gain
(Institute of Medicine and Food and Nutrition Board
1990
). Family income was distributed as follows: 4% under
$20,000, 25% between $20,000 and $34,999, 17% between $35,000 and
$49,999 and 54% above $50,000. Infants were born healthy at full term
with mean birth weights and lengths of 3.48 ± 0.52 kg and 50.7
± 2.6 cm, respectively.
Anthropometry and body composition.
Body weight to the nearest 0.1 kg and height to the nearest 0.1 cm were
measured using an electronic balance (Healthometer, Bridgeview, IL) and
stadiometer (Holtain Limited, Crymych, U.K.), respectively.
Dual-energy x-ray absorptiometry (QDR2000; Hologic, Madison, WI;
software version 5.56) was used to measure FFM and FM. Energetic
equivalents of changes in FFM and FM were taken as 5 and 39 kJ/g,
respectively (Forbes 1987
).
Milk energy output.
Milk energy output was assessed from milk production and the energy
concentration of the milk. The amount of milk produced was assessed by
a 3-d test-weighing session at home (Butte et al. 1984
), with a correction for insensible water loss of 2
g · kg-1 · d-1 feeding time
(Butte 1996
). Infant weights were measured before and
after each feeding on electronic, integrating scales with a precision
of ±1.0 g (model 3862MP; Sartorious, Göttingen, Germany).
For the determination of milk composition, mothers expressed all their
milk during a 24-h period with an electric pump (Egnell, Cary, IL)
while in the metabolic research unit for other studies. After each
pumping session, the milk was weighed, and a 10% aliquot was
refrigerated and later pooled for the 24-h analysis. The energy
concentration of human milk was determined by adiabatic bomb
calorimetry (Parr Instruments, Moline, IL).
BMR by respiration calorimetry.
Oxygen consumption (
O2), carbon dioxide production
(
CO2) and energy expenditure under basal conditions
were measured by room calorimetry. The performance of the respiration
calorimeters has been described in detail previously (Moon et al. 1995
). At 3 mo postpartum, subjects spent the night in the
calorimeter; they were awakened at 0700 h after a 12-h fast, were
asked to urinate and return to bed, and remained supine. After a 20-min
equilibration period, BMR was measured for 40 min. At 18- to 24-mo
postpartum, subjects arrived at the Childrens Nutrition Research
Center at 0700 h in the fasted state and rested supine for 30 min
before the 40-min measurement of BMR.
TEE by doubly labeled water method.
TEE was measured by the doubly labeled water method
(International Dietary Energy Consulting Group 1990
).
After the collection of a baseline saliva sample, the women received
via mouth 100 mg of 2H2O (Cambridge Isotope
Laboratories, Andover, MA) and 125 mg of H218O
(Cambridge Isotope Laboratories) per kg body weight. One daily saliva
sample was collected at home for the next 13 d. Saliva samples
were collected at least 30 min after eating or drinking. Using a small
straw, the subject expectorated approximately 1 mL of saliva directly
into an o-ringsealed vial. Samples were stored frozen at -20°C in
the o-ringsealed vials. The time of collection was recorded. Saliva
samples were analyzed for hydrogen and oxygen isotope ratio
measurements by gas-isotope-ratio mass spectrometry (Wong et al. 1987
). For hydrogen isotope ratio measurements, 10 µL of
saliva without further treatment was reduced to hydrogen gas with 200
mg zinc reagent at 500°C for 30 min (Wong et al. 1992
). The 2H/1H isotope ratios of the
hydrogen gas were measured with a Finnigan Delta-E
gas-isotope-ratio mass spectrometer (Finnigan MAT, San Jose, CA). For
oxygen isotope ratio measurements, 100 µL of saliva was allowed to
equilibrate with 300 mbar of CO2 of known 18O
content at 25°C for 10 h using a VG ISOPREP-18
water-CO2 equilibration system (VG Isogas, Limited,
Cheshire, U.K.). At the end of the equilibration, the
18O/16O isotope ratios of the CO2
were measured with a VG SIRA-12 gas-isotope-ratio mass spectrometer (VG
Isogas, Limited).
The isotope dilution spaces for 2H (NH) and
18O (NO) were calculated as follows:
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where d is the dose of 2H2O or H218O in g, A is the amount of laboratory water in g used in the dose dilution, a is the amount of 2H2O or H218O in g added to the laboratory water in the dose dilution, Ea is the rise in 2H or 18O abundance in the laboratory water after the addition of the isotopic water and Ed is obtained from the zero-time intercepts of the 2H and 18O decay curves in the saliva samples.
CO2 was calculated from the fractional
turnover rates of 2H (kH)
and 18O (kO) as follows:
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In this equation, the in vivo isotope fractionation factors of
0.945 [f1, 2H2O(liquid)
2H2O(gas)],
0.990 [f2,
H218O(liquid)
H218O(gas)]
and 1.039 [f3,
H218O(liquid)
+ C16O2(gas)
H216O(liquid)
+ C18O16O (gas)] measured at 37°C were used (Wong et al. 1988
).
CO2 was converted to
TEE using the Weir equation (de V. Weir 1949
) as
follows:
![]() |
where oxygen consumption (
O2) was
calculated from an assumed food quotient (FQ) of 0.86 using the
relationship
O2 =
CO2/FQ according to Black et al. (1986)
.
Activity energy expenditure (AEE) was estimated as TEE - (BMR +
0.1 x TEE), assuming that 10% of TEE was due to the thermic
effect of feeding (TEF). There is no clear evidence that TEF is
either increased or decreased in lactation (Illingworth et al. 1986
, Motil et al. 1990
, Spaaij et al. 1994
); therefore, the assumption that TEF remains
constant during lactation seems reasonable. Physical activity level
(PAL) was defined as the ratio of TEE to BMR. Participation in physical
activities of moderate, hard and very hard intensity was assessed by
the 7-d recall method published by Blair (1984)
.
Energy requirements.
At 3 mo postpartum, energy requirements during lactation were defined as the sum of TEE and milk energy output; net energy requirements during lactation were defined as the sum of TEE, milk energy output and the energy mobilization from tissues. At 1824 mo postpartum, the energy requirements were taken as TEE.
Statistics.
Minitab (release 13; Minitab, College Station, PA, 1998) was used for
data description and statistical analysis, including Pearsons
correlation, paired t test,
2 and linear
regression. ANOVA was used to test for differences in outcome variables
between the lactating and nonlactating states; the model included
subjects, time postpartum and covariates of weight, FFM and FM in some
applications. Differences were considered statistically significant at
P
0.05.
| RESULTS |
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The isotope dilution spaces, NH and
NO, did not change significantly between 3 and
1824 mo postpartum (Table 2
). Fractional turnover rates of 18O and
2H were significantly higher during lactation
than afterward (P = 0.001).
CO2 and
O2
were not significantly different between lactating and nonlactating
states.
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| DISCUSSION |
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The changes in weight and, therefore, energy mobilization from tissues
(-0.65 MJ/d) of these lactating women were typical of other
well-nourished women (Butte and Hopkinson 1998
,
Institute of Medicine and Subcommittee on Nutrition During
Lactation 1991
). On average, these women achieved their nadir
weight at 12 mo postpartum (60.5 kg), which was close to their
prepregnancy weight, and then regained between 12 and 24 mo (61.6 kg).
Well-nourished lactating women experience a mild, gradual weight
loss in the first 6 mo postpartum, averaging -0.8 kg/mo, whereas
undernourished women experience negligible weight loss.
Sadurskis et al. (1988)
monitored FM in 23 Swedish women
for 6 mo postpartum; FM decreased from 30.4 to 29.6% by
18O dilution and from 32.9 to 31.9% by total
body potassium counting. Consistent with a minor weight loss and
sedentary lifestyle, British women (n = 10) displayed a
nonsignificant increase (30.331.4% between 1 and 3 mo postpartum) in
FM estimated by 2H and 18O
dilution (Goldberg et al. 1991
). In U.S. women
(n = 45), FM decreased from 28.0% at 1 mo to 26.3% at
4 mo postpartum by underwater weighing (Butte et al. 1984
). Changes in adipose tissue volume in 15 Swedish women
were measured by magnetic resonance imaging (Sohlström and Forsum 1995
). In the first 6 mo postpartum, the subcutaneous
region accounted for the entire reduction in adipose tissue volume,
which decreased from 30.6 to 27.4 L; nonsubcutaneous adipose tissue
volume actually increased. Mobilization of tissue reserves is a
general, but not obligatory, feature of lactation.
Milk production and milk energy content were within normal limits for
exclusively breastfeeding women at 3 mo postpartum (Institute of
Medicine and Subcommittee on Nutrition During Lactation 1991
,
Jensen 1995
, Prentice and Prentice 1988
).
We avoided the common difficulties of estimating the energy content of
human milk due to diurnal, within-feed and between-breast
variation in milk fat by obtaining a complete 24-h milk expression.
Lactation performance may also be judged by infant growth, which was
adequate in these infants (Butte et al. 2000
).
Interestingly, milk energy output tended to be lower in women with
higher TEE and AEE.
Adjusted for weight or FFM and FM, BMR did not differ in these women
during and after lactation. This stands in contrast to the higher 24-h
energy expenditure, sleeping metabolic rate and BMR, adjusted
for FFM and FM, that we observed in lactating than nonlactating women
at 3 mo postpartum estimated by room calorimetry (Butte et al. 1999
). The discrepancy in our own results might be attributed
to the different conditions under which BMR was measured at 1824 mo.
Although the women had fasted and rested before the measurement, they
did not sleep overnight in the calorimeter. If lactation is a
continuous, inefficient process, BMR would be expected to be elevated
due to the energy cost of milk synthesis. However, there is no
consensus as to whether BMR is elevated (Forsum et al. 1992
, Sadurskis et al. 1988
, Spaaij et al. 1994
), depressed (Guillermo-Tuazon et al. 1992
, Lawrence et al. 1986
) or unchanged
(Goldberg et al. 1991
, Illingworth et al. 1986
, Madhavapeddi and Rao1992
, Motil et al. 1990
, Piers et al. 1995
, Schutz et al. 1980
, Singh et al. 1989
, van Raaij et al. 1991
) during lactation. Interpretation of these studies is
difficult because BMR was not always adjusted for differences in body
weight or body composition between comparison groups. In general, it
would appear that BMR is unchanged or slightly elevated during
lactation; there is little evidence of energy conservation.
TEE of lactating women has been measured by the doubly labeled water
(DLW) method in five other studies (Butte et al. 1997
, Forsum et al. 1992
, Goldberg et al. 1991
, Lovelady et al. 1993
, Singh et al. 1989
). Potential sources of error in the DLW method
unique to lactation are isotope exchange and sequestration during de
novo synthesis of milk fat and lactose and increased water flux into
milk. Theoretically, the export of exchangeable hydrogen bound to
solids in milk may result in a 1.01.3% underestimation of
CO2 (International Dietary Energy Consulting Group 1990
). 2H sequestration
may increase this underestimation to 1.53.4%. Mean TEE values of
10.0 MJ/d (PAL = 1.79) in our subjects are higher than values
reported for British (8.9 MJ/d, PAL = 1.54) (Goldberg et al. 1991
) and lactating Otomi women (9.2 MJ/d, PAL = 1.6)
(Butte et al. 1997
), similar to those reported for U.S.
women (10.1 MJ/d, PAL = 1.76) (Lovelady et al. 1993
) and slightly lower than those reported for Gambian (10.4
MJ/d, PAL = 1.95) (Singh et al. 1989
) and Swedish
(10.7 MJ/d, PAL = 1.80) (Forsum et al. 1992
) women
during lactation. The physical activity of our women would be assessed
as "moderate" or "heavy" according to the FAO/WHO/UNU
classification (FAO/WHO/UNU Expert Consultation 1985
),
consistent with the active lives of these working mothers.
Theoretically, the energy cost of lactation could be met by a reduction
in the time spent in physical activity or an increase in the efficiency
of performing routine tasks. Adaptations in the level of physical
activity were not seen in these lactating women; AEE and PAL did not
differ significantly during and after lactation. Reductions in physical
activity have been reported in early lactation (45 wk postpartum) in
Swedish (van Raaij et al. 1991
) and British
(Goldberg et al. 1991
) women. By 27 wk, the activity of
the Swedish women, however, was similar to prepregnancy levels. By 3 mo
postpartum, the majority of the women in our study had resumed their
characteristic occupational and recreational lifestyles, with
additional child-rearing responsibilities.
The energy requirements of lactating women were estimated from
measurements of TEE, milk energy output and energy mobilization from
tissue stores in the following five studies in which doubly labeled
water was used (Butte et al. 1997
, Forsum et al. 1992
, Goldberg et al. 1991
, Lovelady et al. 1993
, Singh et al. 1989
). In 10 lactating
British women, the total energy requirements (and net energy
requirements, because there was no fat mobilization) were 11.1, 11.3
and 11.2 MJ/d at 1, 2 and 3 mo postpartum, respectively. Milk energy
output averaged 2.2 MJ/d (Goldberg et al. 1991
). In 23
lactating Swedish women, the total energy requirement at 2 mo
postpartum was 12.7 MJ/d, offset by 0.3 MJ/d from tissue stores to
yield a net requirement of 12.4 MJ/d (Forsum et al. 1992
). In nine lactating U.S. women, the total energy
requirement was 12.4 MJ/d, with 2.2 MJ/d exported into milk; 1.2 MJ/d
was mobilized from tissues, yielding a net requirement of 11.2 MJ/d
(Lovelady et al. 1993
). In 14 fully lactating Gambian
women, the total energy requirement was 12.5 MJ/d, subsidized by 0.4
MJ/d to yield a net energy requirement of 12.1 MJ/d at 56 mo
postpartum (Singh et al. 1989
). The energy requirements
of Otomi women from Mexico were determined by the same approach. Total
energy requirements were 11.2 MJ/d, of which 2.2 MJ/d was exported into
milk (Butte et al. 1997
). In the Otomi women, the energy
cost of lactation was subsidized minimally by mobilization of tissue
stores (0.1 MJ/d) to yield a net energy requirement of 11.1 MJ/d.
Across these diverse populations, mean milk energy outputs during full
lactation were similar (2.12.2 MJ/d). These values are less than
estimates used in the FAO/WHO/UNU and U.S. RDA recommendations, which
assume a milk energy concentration of 2.93 MJ/L and milk production
rates of 819848 and 750 mL/d, respectively [FAO/WHO/UNU Expert Consultation 1985
, National Research Council (U.S.) and Subcommittee on the Tenth Edition of the RDAs 1989
]. The FAO/WHO/UNU and U.S. RDA recommendations also
entail an 80% energetic efficiency of milk synthesis, which is
encompassed in our TEE. TEE, body size and energy mobilization from
tissues displayed the expected variability among these populations,
resulting in net energy requirements of fully lactating women ranging
from 11.1 to 12.4 MJ/d. Our estimates of the total and net energy
requirements of lactating women at 3 mo postpartum are in line with
estimates of other U.S. women (Lovelady et al. 1993
) and
British women (Goldberg et al. 1991
). The women in these
studies were fully breastfeeding their infants, who were <6 mo of age.
Naturally, the stage and extent of breastfeeding affect the incremental
energy requirements for lactation. Milk production rates increase
during the first 6 mo of full lactation. Beyond 6 mo postpartum,
typical milk production rates are variable and depend on weaning
practices.
In conclusion, total energy requirements were augmented during lactation compared with the nonpregnant, nonlactating state (12.0 ± 1.4 versus 10.6 ± 2.1 MJ/d). Energy mobilization from tissue stores (-0.65 ± 0.97 MJ/d) subsidized the energy cost of lactation, resulting in net energy requirements of 11.4 ± 1.8 MJ/d. Because adaptations in basal metabolism and physical activity were not evident in these well-nourished women, energy requirements were met in part by mobilization of tissue stores but primarily from the diet.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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3 Abbreviations used: AEE, activity energy
expenditure; BMR, basal metabolic rate; DLW, doubly labeled water;
FAO/WHO/UNU, Food and Agriculture Organization/World Health
Organization/United Nations University; FFM, fat-free mass; FM, fat
mass; FQ, food quotient; kH, deuterium fractional turnover
rate; kO, oxygen-18 fractional turnover rate;
NH, deuterium dilution space; NO, oxygen-18
dilution space; PAL, physical activity level; RDA, Recommended Dietary
Allowance; TEE, total energy expenditure;
CO2,
carbon dioxide production;
O2, oxygen consumption. ![]()
Manuscript received June 22, 2000. Initial review completed July 24, 2000. Revision accepted September 22, 2000.
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