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Department of Nutrition and Food Science, University of Maryland, College Park, MD 20742;
*
Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892; and
U.S. Department of Agriculture, Beltsville Human Nutrition Research Center, Beltsville, MD 20705
2To whom correspondence and reprint requests should be addressed. E-mail: pv6{at}umail.umd.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • calcium • postpartum • lactation • fractional absorption • stable isotopes • humans
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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not to be significantly different at absorptions
<25%. Smith et al. (2)
gave small amounts of calcium
tracers and found that isotope incorporation into blood, urine and
saliva yielded similar results for calcium absorption. Theoretically,
the incorporation of Ca stable isotopes into breast milk can also be
used to determine the absorption of Ca.
Calcium absorption using the incorporation of isotopes into urine
has been used for studies of girls (3
4
5)
, pregnant women
(6
7
8)
and lactating women (6
7
8
9
10
11)
. One group
that has not received attention is postpartum nonlactating women
(PPNL).
This study was undertaken to compare the fractional absorption of Ca as measured by stable isotope incorporation into urine, serum and milk of lactating women. In addition, the incorporation of Ca from oral and IV stable isotopes into serum and urine was compared among postpartum lactating (LACT), PPNL and never pregnant (NP) women. This study is unique because of the controlled calcium intake of the subjects.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This study was approved by the Institutional Review Boards (IRB) for human studies at the University of Maryland and the USDA. Written informed consent was obtained from each subject before beginning the study.
At 2–3 mo postpartum, LACT (n = 6) and PPNL
(n = 6) as well as NP women (n
= 7) were recruited from the greater Baltimore-Washington, DC
area. None of the women used supplements containing minerals for 
2 mo
before the study or oral contraceptives for 6 mo before the study.
All subjects and their infants were in good health. All infants
exhibited normal growth with appropriate weights for age, lengths for
age and weights for length. A description of the subjects was published
previously (12)
.
Before beginning the study each woman kept a 7-d food and drink intake
record. These records were analyzed using the University of Maryland
database and Food 8 program (13)
. Figure 1
summarizes the study design.
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Subjects remained free living but were fed a controlled diet for a 21-d
study period. This diet was similar in nutrient composition to diets of
healthy lactating women during previous studies (13
14
15)
.
Energy intake was adjusted to maintain subject weight by supplementing
the diet with mineral-free beverages. One of the lactating subjects
also increased her intake by an additional glass of skim milk. All food
was purchased in lots, prepared and packaged at the USDA, Beltsville,
MD. Food was frozen until use and was delivered daily to subjects. A
3-d rotating menu was used. A composite for each of the 3-d menus,
including all food and beverages, was weighed, digested and analyzed by
atomic absorption spectrometry to determine calcium content
(16)
. Mean daily calcium content for the LACT subjects
averaged 32.8 mmol/d (1316 mg/d) with the inclusion of the one subject
that consumed the extra milk and 30.1 mmol/d (1206 mg/d) when she was
excluded, and 30.1 mmol/d (1206 mg/d) for the PPNL and NP women.
After consuming the diet for a 6-d equilibration period and after an overnight fast, subjects were brought to the University of Maryland Hospital, a blood sample was collected and they then received an injection of 0.05 mmol (2 mg) 42Ca as calcium carbonate. Immediately after the injection, the subjects consumed a standardized breakfast that contained 377 mg of Ca, and 90 mL of milk to which 0.25 mmol (10 mg) 44Ca as calcium carbonate had been added the previous day and allowed to equilibrate with the calcium in milk overnight at 4°C. The stable isotopes were obtained from Oak Ridge National Laboratory (Oak Ridge, TN). Sterile solutions of 42Ca and 44Ca were prepared by the NIH pharmacy and tested for sterility and pyrogenicity.
Sample collection.
Venous blood samples were collected from fasting subjects immediately before and 24 and 48 h after receiving the oral and IV calcium doses. Trace element–free syringes were used. Samples of serum were frozen at -80°C for later analysis.
Subjects collected all urine from 1 d before and for 2 wk after receiving the isotope doses. Urine collections (24-h) were made daily into opaque polyethylene containers (Fisher Scientific, Springfield, NJ), previously shown to be free from trace element contamination. Samples from each 24-h urine collection were frozen until analysis.
Lactating women hand-expressed milk samples into acid-washed
plastic vials at the beginning of each feeding beginning 24 h
before receiving the stable isotopes and for 48 h immediately
after stable isotope dosing. Infants were fed on demand throughout the
study. Milk samples were frozen at -80°C until analysis.
Infants were weighed by their mothers with a portable infant balance
(Toledo Scale, Columbus, OH) before and after each feeding on those
days on which milk samples were collected. Time of feeding and weights
were recorded and the difference between final and initial infant
weight was used to estimate milk intake. The daily weight of milk
consumed was averaged and adjusted for insensible weight loss
(17)
.
Sample analysis.
Serum and milk samples and aliquots of the 24-h urine samples were collected from 1 d before receiving the isotopes and for 48 h after dosing and were analyzed for 44Ca and 42Ca enrichment.
Urine samples were prepared using a method similar to that described by
Turnlund et al. (18)
and described in more detail
elsewhere (19)
. Briefly, small urine samples were
centrifuged (6,500 x g for 5 min) to remove
precipitates and the calcium separated from the supernatant using a
saturated solution of ammonium oxalate (pH 8). Serum and milk samples
(0.2 and 0.05 mL, respectively) were dry-ashed at 480°C and the
calcium separated using ammonium oxalate. The calcium oxalate
precipitate was dissolved in 0.1 mol/L nitric acid and diluted to the
desired concentration. The isotope ratios were determined using a
PlasmaQuad II+ (VG Elemental) modified to operate in the cool plasma
mode (19)
. Total calcium was determined by atomic
absorption spectrometry (Model 5000, Perkin-Elmer, Norwalk, CT).
Calculations.
The amount of the tracer was determined using the following
equation, based on the equations of Turnlund et al. (20)
 |
where T is the total amount of calcium in the sample; mt is the amount of enriched calcium tracer; Wn is the atomic weight of natural or unenriched calcium; Wt is the atomic weight of the enriched calcium tracer; A is used to designate atomic abundance with the subscripts indicating the isotope and the source of the isotope; i is the tracer (42Ca or 44Ca) isotope; x is the reference (43Ca) isotope; n is the natural element; t is the enriched stable isotope tracer; and Ri/x is the ratio of reference to tracer isotope.
Calculation of fractional absorption.
The fractional absorption (%FA) of the oral calcium dose was
determined by the relative amounts of the two tracers in the IV and
oral doses, and in the samples using the following equation:
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where 42Caiv is the IV dose, 44Caoral is the oral dose, and 42Ca and 44Ca are the amounts of the two tracers in the biological sample, all expressed in molar or mass terms.
Statistical analysis.
ANOVA was used to compare fractional absorption determined from urine, serum and milk as well as to compare calcium fractional absorption and calcium losses among the three groups of women. Unpaired t test was used to compare the postpartum women (lactating and nonlactating) and NP women. The Least Significant Difference procedure was performed to determine differences among group means. Data are reported as means ± SEM. Differences were considered significant when P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. The three groups of women did not differ in height, weight or body
mass index. The two groups of postpartum women did not differ in the
length of the postpartum period. Before the controlled feeding study,
the LACT women consumed significantly more (P < 0.05)
energy and calcium than the PPNL and NP women.
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).
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. The postpartum women who had resumed menses (n = 7)
tended to have a greater (P < 0.07) fractional calcium
absorption, 27.5 ± 2.8%, than the postpartum women who were
amenorrheic (n = 5), 21.0 ± 1.2%. When the two
postpartum groups were separated and compared with the NP group, there
was a significant difference (P < 0.046) in the NP
women compared with the PPNL, but not with the LACT women (P
< 0.085) (Table 2)
.
There was no difference in the cumulative incorporation of the IV and
oral stable isotope doses into either milk or urine when the oral dose
was corrected for absorption (data not shown). There was significantly
more (P < 0.001) of the 44Ca
oral dose incorporated into the milk of LACT women compared with urine
(Table 3
). The two groups of postpartum women, LACT and PPNL, had significantly
less (P < 0.01) of the oral dose excreted into urine
than the NP women.
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shows the pattern of IV and oral isotope incorporation into milk
48 h after isotope dosing for a typical subject. The IV dose was
detected in the first feeding after the dosing and the oral in the
second feeding after dosing. Both the oral and IV doses appeared to
peak 
10 h after dosing, with the IV dose showing a more rapid
decline than the oral dose over the next 30 h.
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). The total calcium loss from urine and milk for the lactating women
was 6.7 mmol/d (268 mg/d). Using the analyzed Ca intake for the
controlled feeding and the percentage of Ca fractional absorption, the
lactating women were absorbing 7.8 ± 0.94 mmol/d (313 ± 37.8 mg/d) of Ca. This Ca intake would more than cover the total
urinary and milk losses of these women. An estimated mean calcium
balance, which did not include endogenous Ca losses, was calculated for
the three groups of women (Table 4
). The PPNL women had a significantly higher (P < 0.002) positive estimated Ca balance (5.2 ± 1.21 mmol/d; 212
± 48.6 mg/d) than the LACT women (1.1 + 1.50 mmol/d; 45 ± 60.1mg/d) or the NP women (1.1 + 0.51; 45 ± 20.4 mg/d).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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showed that fractional calcium
absorptions determined from isotopic ratios in blood, urine and saliva
were similar. They concluded that saliva samples could be used to
determine calcium kinetic parameters for compartmental modeling and
fractional absorption, thereby eliminating the need to collect blood
and urine samples. We found that milk samples also gave values similar
to those of blood and urine for isotopic ratios of Ca enrichment. Thus,
during lactation, milk samples can be used to determine fractional
calcium absorption and eliminate the need for the collection of urine
or blood.
The fractional calcium absorptions for the lactating and nonlactating
women in our study were in the same range as those reported when the
oral isotope was given in milk (9)
and slightly lower than
what has been reported when the isotope is given in a water solution
(6
,8)
. Heaney et al. (21)
reported that the
oral calcium load influences fractional calcium absorption
measurements. Thus, if the oral dose of stable isotope is given with
milk, which has a high calcium content, it would be expected that the
fractional calcium absorption measurement would be lower than when the
oral isotope is given in a water solution.
Our observation of no significant difference in the FA of calcium
between LACT and PPNL is consistent with the results of longitudinal
studies of calcium absorption during reproduction that have not shown
an increase in calcium absorption during lactation
(6
,7
,8)
. Our observation is also consistent with studies
that compared lactating women with nonlactating postpartum controls
(11)
and found no difference in the FA of calcium.
However, increases have been observed postlactation after weaning and
the resumption of menses (8
,11)
. We also observed a
nonsignificant increase in calcium FA with the resumption of menses.
Our result that postpartum women have a higher calcium FA than the NP
women is surprising given the results of the longitudinal and
controlled studies of FA during lactation (6
7
8
9
10
11)
. The
main difference in our study compared with these other investigations
of calcium absorption during lactation is that ours was a controlled
feeding study in which all subjects received 30–33 mmol/d Ca from food
sources for 6 d before the measure of absorption. The differences
in FA detected in our study could be due to the fact that the women had
been adapted to a standard calcium diet; this allowed us to measure a
difference that was not seen in other studies because the women in
previous studies did not consume a controlled diet. The NP women
absorbed less calcium, indicating that they did not need as much
calcium, whereas the postpartum women did not show this adaptation,
indicating they had a greater need for calcium.
The controlled calcium intake during the study was similar to what the lactating group had been consuming before the study, 30 mmol/d (1209 mg/d), but was significantly greater than the 19.9 mmol/d (798 mg/d) consumed by the NP women and 15.9 mmol/d (636 mg/d) by the PPNL women. Another possible explanation for the lower FA of the NP group is that it reflects an increased calcium intake compared with their usual intake. Although the PPNL women also had a lower Ca intake before the study period, their FA was not reduced compared with the LACT group. Possibly they had only recently reduced their intake of energy and calcium compared with what it had been during pregnancy and had not adjusted to a lower intake before beginning the greater intake of the study period.
The significantly greater (P < 0.046) FA of the PPNL women compared with the NP group could reflect a greater calcium need by the PPNL group to restore bone calcium. The lack of a significant difference (P < 0.085) between the LACT and the NP groups could be related to the sample size.
The LACT women incorporated 3 times more of the oral
44Ca dose into milk than was excreted in urine.
Also, the orally ingested 44Ca was detected in
breast milk <2 h after dosing, suggesting that there is a relatively
rapid incorporation of calcium into milk. The amount of calcium
incorporated into milk was equivalent to the urinary calcium excretion
of NP women consuming the same amount of calcium. The observation of
reduced urinary calcium excretion by LACT and PPNL women is consistent
with the findings of many other investigators (7
8
9
,15
,22)
and has been suggested as a means for providing more calcium for
incorporation into breast milk for the lactating women. Klein et al.
(15)
estimated that this reduced urinary excretion of
calcium could provide 30–40% of calcium incorporated into breast
milk. On the basis of the difference found between urinary calcium
excretion in NP and LACT women, an additional 3.0 mmol/d Ca was
conserved. This amount represents 50% of the milk calcium for these
women. The calcium conserved by a reduced urinary excretion of the PPNL
women was reflected in the higher positive calcium balance compared
with the LACT or NP group. On the basis of the difference observed
between the urinary excretion in NP and PPNL women, an additional 1.8
mmol/d of Ca would be conserved.
Our estimated balances of the three groups did not include endogenous
fecal or integumental losses. Data for these losses in postpartum women
are limited. There is one earlier study by Heaney and Skillman
(23)
that estimated the fecal endogenous loss for four
postpartum women, two of whom were lactating, using injections of
48Ca and its appearance in feces. The mean
estimated fecal endogenous loss of these women was 3.42 mmol/d (137
mg/d). Using this estimate of fecal endogenous loss for our two
postpartum groups, the PPNL women would still be in a positive calcium
balance, whereas the LACT women would be in a negative balance. This
increased calcium retention by the PPNL group may be used to increase
bone calcium stores. Hopkins et al. (24)
recently reported
that in PPNL women, bone mineral content increased within the first 3
mo postpartum. This would be expected to be the result of increased
calcium retention in these postpartum women. Numerous studies
(8
,24
25
26
27
28
29
30)
have shown that bone mineral density decreases
in the first 6 mo of lactation with recovery within 6 mo of weaning
(8
,25
26
27
28
29
30)
. Thus, lactation delays the bone mineral
recovery that occurs earlier in PPNL women. The more positive calcium
balance in the PPNL group compared with the LACT women reflects this
earlier bone mineral recovery.
Fractional calcium absorption during lactation can be determined from the incorporation of stable isotopes into milk samples, eliminating the need for the collection of urine or blood samples. During lactation, orally ingested calcium is preferentially incorporated into breast milk rather than being excreted in urine, providing a mechanism for calcium redistribution to meet maternal needs. PPNL women metabolize calcium in the same way as LACT women with similar absorption and urinary excretion but with no calcium loss through milk, resulting in a greater calcium retention than that of LACT women.
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FOOTNOTES |
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3 Abbreviations used: FA, fractional absorption; IV, intravenous; LACT, lactating; NP, never pregnant, nonlactating women; PPNL, postpartum nonlactating women.
Manuscript received February 12, 2001. Initial review completed April 24, 2001. Revision accepted June 12, 2001.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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