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Laboratório de Bioquímica Nutricional e de Alimentos, Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil and * USDA-Western Human Nutrition Research Center, Davis, CA 95616
3To whom correspondence should be addressed. E-mail: donangel{at}iq.ufrj.br.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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500 mg/d, in three different physiologic states, i.e., control (nonpregnant, nonlactating; NPNL), pregnant and lactating. Markers of calcium metabolism [serum Ca, P and intact parathyroid hormone (iPTH); urinary Ca and P] and of bone turnover [urinary deoxypyridinoline (D-Pyr) and plasma bone alkaline phosphatase (BAP)] were measured in NPNL (adolescents, n = 12 and adults, n = 25), pregnant (adolescents, n = 30 and adults, n = 36) and lactating (adolescents, n = 19 and adults, n = 26) women. In the NPNL women, iPTH, D-Pyr and BAP were higher (P < 0.001) and urinary Ca was lower (P < 0.001) in adolescents than in adults. Serum iPTH was higher (P < 0.001) and urinary Ca was lower (P < 0.01) in adolescents than in adults also in pregnancy and lactation. Compared with NPNL women, serum Ca decreased (P < 0.001) with pregnancy in adolescents but not in adults. The increase in D-Pyr with pregnancy and lactation was very pronounced in adults (130%, P < 0.001) but less in adolescents (<25%, P < 0.01). BAP increased (P < 0.001) with pregnancy and lactation in adults (60%) but decreased (P < 0.001) with pregnancy in adolescents (13%). Pregnancy and lactation appear to affect bone turnover in adolescent and adult women with low calcium intake differently.
KEY WORDS: • calcium • adolescence • pregnancy • lactation • bone turnover
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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,2
). The achievement of optimal peak bone mass is dependent on the rapid rate of bone accretion, mainly during the adolescence growth spurt, and on genetic and environmental factors including diet composition and calcium intake (1
,3
). However, in many developing countries including Brazil, calcium intake of adolescents is frequently lower than recommendations (4
). In this situation, meeting calcium demands depends on the capacity for physiologic adaptations in calcium metabolism.
There are few studies comparing calcium metabolism between adolescent and adult females and no studies evaluating possible differences in women with habitually low calcium intakes. Kinetic and metabolic studies have shown that adolescent women absorb more calcium from the diet, excrete less calcium into urine and feces, have higher bone turnover rates and higher daily net calcium retention than do adults with similar high calcium intakes (2
,3
,5
). Weaver et al. (2
) also reported a significant relationship between urinary calcium excretion and net calcium absorption in adults but not in adolescents, suggesting that adolescents retain more calcium at higher intakes (>1300 mg/d), whereas in adults, the excess calcium absorbed is excreted into the urine. This is consistent with the higher calcium demand during adolescence.
Pregnancy and lactation are also periods of high calcium demands for fetal skeletal growth and milk production met mainly by physiologic adjustments (6
). During pregnancy, the major physiologic adaptations to meet fetal needs include increased calcium intestinal absorption and increased rate of bone turnover (6
–8
). During lactation, there is a contribution of renal calcium conservation, but a temporary demineralization of the skeleton is the main mechanism to meet calcium requirements even when dietary calcium exceeds the recommended intake (6
,8
,9
). These adjustments have been investigated mainly in adult women and are similar in women with a wide range of calcium intakes (10
–13
). Less is known about calcium homeostasis in pregnancy and lactation of adolescent women, particularly those with habitually low calcium intakes.
The physiologic adaptation to pregnancy and lactation in adolescents may be different from that in adults, particularly at low calcium intake. Chan and collaborators (14
) found a substantial reduction (8–10%) of bone mineral content during lactation in adolescent mothers consuming 900 mg Ca/d but no significant reduction in bone mineral in lactating adolescents consuming >1600 mg Ca/d (15
). This suggests that pregnancy and lactation in adolescent women may increase susceptibility to bone mineral loss, especially when dietary calcium is low.
The purpose of this study was to compare biochemical markers of calcium and bone metabolism between adolescent and adult women with customary low calcium intakes in three different physiologic states, i.e., control, pregnancy and lactation.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Pregnant (n = 66) and lactating (n = 45) women, recruited from a public prenatal clinic in Rio de Janeiro (Maternidade Escola/UFRJ), participated in the study after giving informed consent. Nonpregnant nonlactating (n = 37; NPNL) women also participated in the study as a control group and were recruited among students at UFRJ. The experimental protocol of the study was approved by the Ethical Committee of Maternidade Escola/UFRJ.
All women were apparently healthy, nonsmokers and had no history of bone or renal disorders affecting calcium metabolism. Pregnant women were at 28–39 wk of gestation; lactating women were at 6–20 wk postpartum, were exclusively breast-feeding, and gave birth to healthy infants. All NPNL women were nulliparous; pregnant and lactating women were primiparous and had no complications during pregnancy and/or lactation.
The NPNL women studied included 25 adults and 12 adolescents; the pregnant women, 36 adults and 30 adolescents; and the lactating women, 26 adults and 19 adolescents. Adults were 21–35 y of age and adolescents, 14–19 y of age. Within each adolescent group, results were similar between women 14–17 y old (NPNL, n = 6; pregnant, n = 19; lactating, n = 12) compared with 18–19 y old (NPNL, n = 6; pregnant, n = 11; lactating, n = 7) (data not shown). Therefore, results in adolescents are presented as a combined age group.
Habitual calcium intake of the women was assessed by three 24-h dietary recall questionnaires. Dietary nutrient analysis was done using the program "The Food Processor" (ESHA Research, Salem, OR) with the database adapted to Brazilian foods based on published information (16
).
Morning blood (10 mL) and urine (50 mL) samples were collected from fasting woman between 0800 and 1000 h. Immediately after being drawn, 3 mL of whole blood was transferred into tubes with heparin for separation of plasma; the remaining blood was used for separation of serum. Aliquots of serum, plasma and urine, both acidified with HCl (final concentration 0.01 mol/L) and nonacidified, were stored at - 20°C until analyzed.
Laboratory analysis.
All materials used for sample collection, storage and analysis were either disposable or previously soaked overnight in dilute nitric acid (1:4) and carefully rinsed with deionized water.
Calcium in serum and urine was determined by complexing with methyl thymol blue; phosphorus in serum and urine by the method of Fiske-Subbarow; serum albumin with bromocresol green, and urinary creatinine by the Jaffe reaction, as previously described (17
). Serum intact parathyroid hormone (iPTH) was measured by a two-site immunoradiometric assay (DSL, Webster, TX). Plasma activity of bone-specific alkaline phosphatase (BAP) was measured according to Farley et al. (18
). Deoxypyridinoline (D-Pyr) crosslinks were determined in nonacidified urine by a competitive immunoassay (Metra Biosystems, Mountain View, CA). Urinary indices were expressed as creatinine ratios. Urinary creatinine excretion is similar in adults and adolescents 
14 y old (19
).
Statistical analysis.
Data were analyzed using ANOVA followed by Tukey’s test for normally distributed variables, and using Kruskal-Wallis test followed by Dunn’s test for nonnormally distributed variables (iPTH, urinary calcium, urinary D-Pyr, and BAP). Interactions between physiologic state (NPNL, pregnant and lactating) and age group (adolescent and adult) were evaluated by two-way ANOVA using log-transformed values for nonnormally distributed variables. Differences with P < 0.05 were considered significant. The statistical analyses were performed using Statgraphics Version 7 for DOS (Manugistics, Cambridge, MA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. The NPNL, pregnant and lactating women did not differ in age for either adults or adolescents. Adult and adolescent women had similar calcium intakes corresponding, on average, to 49 and 36% of recommended intakes in the U.S. and Canada for adults and adolescents, respectively (20
).
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, P < 0.001). Serum phosphorus was higher (P < 0.05) in lactating women than in the other groups. Serum iPTH was lower in pregnant compared with lactating women (P < 0.001). Urinary calcium was lower in lactating than in NPNL and pregnant women (P < 0.001). Urinary phosphorus was lower in lactating than in pregnant women (P < 0.05). Pregnant and lactating women had higher (P < 0.001) urinary D-Pyr (133 and 125%, respectively) and higher (P < 0.001) plasma BAP (59 and 65%, respectively) compared with NPNL women.
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Biochemical indices were compared between adolescent and adult women within each physiologic state. In NPNL women, serum iPTH, urinary D-Pyr, and BAP were higher (P < 0.001) in adolescent than in adult women (75, 71 and 91%, respectively), whereas urinary calcium was 43% lower (P < 0.001). In the pregnant women, serum calcium, urinary calcium, urinary phosphorus and urinary D-Pyr were lower (P < 0.01) in adolescents compared with adults (6, 22, 27 and 24%, respectively), whereas serum iPTH was 110% higher (P < 0.001). In the lactating women, serum iPTH and BAP were higher (P < 0.001) in adolescents than in adults (63 and 39%, respectively), whereas urinary calcium was 57% lower (P < 0.001).
Significant interactions between physiologic state (NPNL, pregnant and lactating) and age group (adult and adolescent) were observed for serum calcium (P < 0.001), urinary D-Pyr (P = 0.013), and plasma BAP (P < 0.001). The decrease in serum calcium associated with pregnancy (physiologic state as main effect, P < 0.001) occurred mainly in adolescents. The increase in urinary D-Pyr with pregnancy and lactation (P < 0.001) was very pronounced in adults (130%) but less in adolescents (<25%). BAP increased with pregnancy and lactation (60%) in adults but decreased with pregnancy (13%) and did not change with lactation in adolescents.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and may be less sensitive to further increase in bone turnover because of pregnancy and lactation. However a low calcium intake in adolescent women may limit the maximal rates of bone turnover, possibly affecting its response to pregnancy and lactation. Our study is the first to compare biochemical markers of calcium and bone metabolism between adolescent and adult women with similar low calcium intakes, in pregnancy and lactation, compared with nonpregnant nonlactating controls. Mean calcium intake in the women of our study, 400–500 mg/d, appears to be common in Brazil (4
,21
). Comparisons between NPNL adolescent and adult women.
Similar levels of serum calcium and serum PTH have been observed in adolescent and adult women with calcium intakes >1000 mg/d (2
). In the present study, serum calcium was similar, but serum iPTH was higher in adolescent compared with adult women, possibly as a response to their low calcium intake. In fact, serum PTH has been found to be negatively related with dietary calcium in adolescents (22
). A low calcium intake ( 400 mg/d) appeared to induce a compensatory hypersecretion of PTH in adolescent women (22
) and a similar response may be occurring in our study.
Studies have shown that adolescent women with adequate calcium intake excrete approximately half the amount of calcium in urine as excreted by adult women (2
,3
). A similar reduction was observed in our study in women with low calcium intakes. Fasting urinary calcium in adolescents was approximately half that in adults. In fact, urinary calcium excretion in adolescence represents obligatory renal calcium losses, independent of calcium intake, whereas in adults, this excretion reflects dietary calcium intake (23
).
Markers of bone formation and resorption were found to be two- to fivefold higher in adolescent compared with adult women with adequate calcium intakes (5
), whereas in our study of women with low calcium intakes, differences in these markers between adolescent and adult women were less pronounced (less than twofold). Therefore, the typical increase of bone turnover in adolescence appears to be limited when calcium intake is low.
Comparisons between pregnant adolescent and adult women.
Serum calcium and serum iPTH decreased with pregnancy in adolescents but not in adults. Similar to NPNL women, adolescents had higher levels of serum iPTH than adults during pregnancy, but also lower serum calcium. PTH levels do not usually change with pregnancy (24
) as observed in the adult women in our study, or are slightly decreased (24
) as observed in the adolescent women. Pregnancy is typically associated with a fall in serum total calcium as a result of decreased serum albumin concentration because of hemodilution (24
). In our study, this fall was more evident in adolescents. Although we did not measure serum ionized calcium, it is possible that adolescent pregnant women have reduced serum ionized calcium levels compared with adult pregnant women because no difference in albumin levels was found between adults and adolescents. This may reflect a more intense calcium tissue uptake, both for fetal growth and maternal bone accretion in adolescent pregnant women.
Pregnancy is usually associated with an increase in urinary calcium excretion (10
) due primarily to increased glomerular filtration rate and increased intestinal calcium absorption (7
,8
). In the present study, an increase in fasting urinary calcium associated with pregnancy occurred only in the adolescent women. However, pregnant adolescents had lower fasting urinary calcium than pregnant adults although the difference was less pronounced in pregnant than in NPNL women (22 vs. 43%). Our results suggest that, at least when calcium intake is low, the physiologic mechanism operating in adolescence that efficiently conserves renal calcium for bone accumulation remains active during pregnancy although to a lesser extent.
Pregnancy has been found to substantially increase bone turnover in adult women both with adequate (10
,13
) and low (17
) calcium intakes, as seen in the adult women in the present study. In the adolescents, however, pregnancy seemed to increase bone resorption to a lesser extent than in adults and to decrease bone formation unlike in adults. Moreover, bone formation, as indicated by BAP, did not differ between adolescent and adult pregnant women. Therefore, the expected higher bone formation rate in adolescents than in adults was not observed during pregnancy. These results suggest that skeletal growth of adolescents may be suppressed during pregnancy. In contrast to NPNL women, bone resorption in pregnant women, as indicated by urinary D-Pyr, was lower (and not higher) in adolescents than in adults. This may be a protective adaptation in pregnant adolescents, at least when calcium intake is low, that decreases the risk of bone loss associated with increased bone turnover during pregnancy.
Comparisons between lactating adolescent and adult women.
Serum calcium, albumin, and iPTH did not differ between lactating and NPNL women either in adults or adolescents, as expected in normal lactation (24
). However, serum iPTH was higher in lactating adolescents than in lactating adults, as observed in the NPNL and pregnant groups, probably as an adaptive response to low calcium intake associated with the high calcium demand in adolescence.
Urinary calcium excretion is typically reduced in adult lactating women with both high (13
) and low (25
,26
) calcium intakes. In the present study, fasting urinary calcium was lower in the lactating than in NPNL and pregnant women, both in adults and adolescents. However, urinary calcium was substantially lower in lactating adolescents compared with lactating adults, as observed in the NPNL women. The typical renal calcium conservation in lactation appears to be very efficient in lactating adolescents with low calcium intakes.
Biochemical markers of bone resorption and formation are substantially elevated during lactation irrespective of calcium intake (6
), as seen in the adult women in the present study. However, in the adolescents, urinary D-Pyr was only slightly higher in lactating compared with NPNL women and BAP did not differ between these groups. Although small differences in bone biomarkers should be interpreted with caution, our results suggest that the already high bone turnover in adolescents is little affected by lactation. Similar to NPNL women, BAP in the lactating women was higher in adolescents compared with adults, although the increase was less pronounced. This suggests that during lactation, bone formation is gradually reestablished in adolescents.
Pregnancy and lactation appeared to affect markers of bone turnover in adolescent and adult women with low calcium intakes differently. The increased bone resorption associated with pregnancy and lactation was less pronounced in the adolescents, possibly as a protective mechanism against excessive bone loss. Pregnancy, but not lactation, seemed to impair bone formation in the adolescents. During lactation, adolescents may be partially catching up on skeletal growth that ceased or slowed down during pregnancy.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in part by CNPq, FUJB, FAPERJ, and CAPES (Brazil). F.F.B. is a Doctoral Student Fellow and C.M.D. is a Research Fellow of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil.
4 Abbreviations used: BAP, bone alkaline phosphatase; D-Pyr, deoxypyridinoline; iPTH, intact parathyroid hormone; NPNL, nonpregnant, nonlactating women.
Manuscript received 26 February 2002. Initial review completed 1 April 2002. Revision accepted 6 May 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Matkovic, V., Fontana, D., Tominac, C., Goel, P. & Chestnut, C.H., III (1990) Factors that influence peak bone mass formation: a study of calcium balance and the inheritance of bone mass in adolescent females. Am. J. Clin. Nutr. 52:878-888.
2. Weaver, C. M., Peacock, M., Martin, B. R., Plawecki, K. L. & McCabe, G. P. (1996) Calcium retention estimated from indicators of skeletal status in adolescent girls and young women. Am. J. Clin. Nutr. 64:67-70.
3. Wastney, M. E., Ng, J., Smith, D., Martin, B. R., Peacock, M. & Weaver, C. M. (1996) Differences in calcium kinetics between adolescent girls and young women. Am. J. Physiol. 271:R208-R216.
4. Sichieri, R. (1999) Consumo alimentar no município do Rio de Janeiro. Saúde En Foco 8:40-43.
5. Weaver, C. M., Martin, B. R., Plaweki, K. L., Peacock, M., Wood, O. B., Smith, D. L. & Wastney, M. E. (1995) Differences in calcium metabolism between adolescent and adult females. Am. J. Clin. Nutr. 61:577-581.[Abstract]
6. Prentice, A. (2000) Calcium in pregnancy and lactation. Annu. Rev. Nutr. 20:249-272.[Medline]
7. King, C. J., Halloran, B. P., Huq, N., Diamond, T. & Buckendahl, P. E. (1992) Calcium metabolism during pregnancy and lactation. Picciano, M. F. Lonnerdal, B. eds. Mechanisms Regulating Lactation and Infant Nutrient Utilization 1992:129-146 Wiley-Liss New York, NY. .
8. Kovacs, C. S. & Kronenberg, H. M. (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr. Rev. 18:832-872.
9. Kalkwarf, H. J. (1999) Hormonal and dietary regulation of changes in bone density during lactation and after weaning in women. J. Mammary Gland Biol. Neoplasia 4:319-329.[Medline]
10. Cross, N. A., Hillman, L. S., Allen, S. H., Krause, G. F. & Vieira, N. E. (1995) Calcium homeostasis and bone metabolism during pregnancy, lactation, and postweaning: a longitudinal study. Am. J. Clin. Nutr. 61:514-523.
11. Allen, L. H. (1998) Women’s dietary calcium requirements are not increased by pregnancy or lactation. Am. J. Clin. Nutr. 67:591-592.[Medline]
12. Prentice, A., Jarjou, L.M.A., Stirling, D. M., Buffenstein, R. & Fairweather-Tait, S. (1998) Biochemical markers of calcium and bone metabolism during 18 months of lactation in Gambian women accustomed to a low calcium intake and in those consuming a calcium supplement. J. Clin. Endocrinol. Metab. 83:1059-1066.
13. Ritchie, L. D., Fung, E. B. & Halloran, B. P. (1998) A longitudinal study of calcium homeostasis during pregnancy and lactation and after resumption of menses. Am. J. Clin. Nutr. 67:693-701.[Abstract]
14. Chan, G. M., Ronald, N., Slater, P., Hollis, J. & Thomas, M. R. (1982) Decreased bone mineral status in lactating adolescent mothers. J. Pediatr. 101:767-770.[Medline]
15. Chan, G. M., McMurry, M., Westover, K., Engelbert-Fenton, K. & Thomas, M. R. (1987) Effects of increased dietary calcium intake upon the calcium and bone mineral status of lactating adolescent and adult women. Am. J. Clin. Nutr. 46:319-323.
16. Ministério do Planejamento e Orçamento, Instituto Brasileiro de Geografia e Estatística (1996) Estudo Nacional da Despesa Familiar, Tabelas de Composição de Alimentos, 4a edição 1996 Rio de Janeiro, Brazil. .
17. Laboissière, F. P., Bezerra, F. F., Rodrigues, R. B., King, J. C. & Donangelo, C. M. (2000) Calcium homeostasis in primiparae and multiparae pregnant women with marginal calcium intakes and response to a 7-day calcium supplementation trial. Nutr. Res. 20:1229-1239.
18. Farley, J. R., Chestnut, C. H. & Baylink, D. J. (1981) Improved method for quantitative determination in serum of alkaline phosphatase of skeletal origin. Clin. Chem. 27:2002-2007.
19. Manz, F., Kehrt, R., Lausen, B. & Merkel, A. (1999) Urinary calcium excretion in healthy children and adolescents. Pediatr. Nephrol. 13:894-899.[Medline]
20. Food and Nutrition Board, Institute of Medicine (1997) Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D and Fluoride 1997 National Academy Press Washington, DC. .
21. Trugo, N.M.F. (1997) Micronutrient regulation in pregnant and lactating women from Rio de Janeiro. Arch. Latinoam. Nutr. 47(Suppl.):30S-34S.
22. Bonofiglio, D., Maggiolini, M., Catalano, S., Marsico, S., Aquila, S., Giorno, A. & Andò, S. (2000) Parathyroid hormone is elevated but bone markers and density are normal in young female subjects who consume inadequate dietary calcium. Br. J. Nutr. 84:111-116.[Medline]
23. Matkovic, V. (1991) Calcium metabolism and calcium requirements during skeletal modeling and consolidation of bone mass. Am. J. Clin. Nutr. 54(Suppl.):245S-260S.
24. Kovacs, C. S. (2001) Calcium and bone metabolism in pregnancy and lactation. J. Clin. Endocrinol. Metab. 86:2344-2348.
25. Prentice, A., Jarjou, L. M., Cole, T. J., Stirling, D. M., Dibba, B. & Fairweather-Tait, S. (1995) Calcium requirements of lactating Gambian mothers: effects of a calcium supplement on breast-milk calcium concentration, maternal bone mineral content, and urinary calcium excretion. Am. J. Clin. Nutr. 62:58-67.
26. Donangelo, C. M., Trugo, N. M., Melo, G. J., Gomes, D. D. & Henriques, C. (1996) Calcium homeostasis during pregnancy and lactation in primiparous and multiparous women with sub-adequate calcium intakes. Nutr. Res. 16:1631-1640.
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