Obstetrics & Gynecology Email Alerts
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Obstetrics & Gynecology 1999;94:52-56
© 1999 by The American College of Obstetricians and Gynecologists
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by POLATTI, F.
Right arrow Articles by KLERSY, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by POLATTI, F.
Right arrow Articles by KLERSY, C.

ORIGINAL RESEARCH

Bone Mineral Changes During and After Lactation

FRANCO POLATTI, MD, EZIO CAPUZZO, MD, FRANCO VIAZZO, MD, ROSSELLA COLLEONI, MD and CATHERINE KLERSY, MD

From the Clinica Ostetrico-Ginecologica, Università di Pavia, and Biometry - Scientific Direction, IRCCS Policlinico San Matteo, Pavia, Italy.

Address reprint requests to: Franco Polatti, MD, Clinica Ostetrico-Ginecologica, IRCCS Policlinico San Matteo, Piazzale Golgi 2, 27100 Pavia, Italy, E-mail: amb.menopausa{at}smatteo.pv.it


   Abstract
Top
Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To investigate variations in bone mineral density during lactation and throughout the 12 months after scheduled cessation of lactation in relation to the resumption of ovarian function.

Methods: Three hundred eight mothers who decided to lactate were scheduled to fully breast-feed for 6 months, followed by a 1-month weaning period, and then suppress lactation with cabergoline. Their bone mineral density variations were compared with those of a control group of nonlactating mothers during the first 18 months postpartum. Half the lactating women were given daily oral calcium supplements of 1 g in an open design.

Results: There was a significant progressive decrease in bone mineral density in lactating women over the first 6 months, followed by recovery of bone mass up to levels that at 18 months were higher than baseline. In nonlactating women, bone mineral density increased progressively after delivery, and at 18 months postpartum had increased by 1.1–1.9% compared with baseline. Compared with lactating women who resumed menstruation within 5 months of delivery, breast-feeding mothers with longer amenorrhea initially lost more bone, but they also gained significantly more bone after resumption of menses, so there were no differences at 18 months postpartum. Oral calcium supplementation decreased bone loss, but had only a transient effect.

Conclusion: A scheduled lactation period of 6 months, followed by a 1-month weaning period, allowed bone mineral density to reach higher values compared with early postpartum, regardless of calcium supplementation and duration of postpartum amenorrhea.

In recent years, much attention has been focused on bone mass, with the aim of developing strategies to prevent bone loss. Marked changes in calcium metabolism were reported during lactation,1 related to amount of breast milk produced, diet, and duration of lactation. The decrease in bone mineral density averages 4–6% during the first 6 months of lactation.2,3 Previous reports of changes in bone mass postpartum were contradictory, with diminished,4,5 unchanged,6,7 or increased bone mineral density.8 Such discrepancies likely result from different timing of measurements and differences in techniques to measure bone mineral density and anatomic sites evaluated in regard to the ratio of cortical to trabecular bone, typical of sites investigated. During lactation, the women have a period of considerable hypoestrogenemia, which negatively affects calcium and phosphate metabolism, as seen in amenorrhea,9,10 and is widely documented after menopause.11,12 During lactation the return of ovarian function varies greatly, so that remarkable differences in bone mass might develop among individuals. Most previous studies were limited by wide ranges in duration of lactation and weaning. To control for those variations, we investigated bone mass variations at well-defined time points postpartum with a fixed length of lactation and weaning.

The aim of this study was to investigate variations of bone mineral density during lactation and throughout the 12 months after the scheduled cessation of lactation, in relation to resumption of ovarian function and calcium supplementation.


   Materials and Methods
Top
Abstract
 Materials and Methods
Results
 Discussion
 References
 
Subjects for this study were recruited from among 786 women who delivered vaginally at term (38–41 weeks’ gestation) during a 1-year period (January through December 1994). Eligible women had to be free of diseases known to interfere with calcium or phosphate metabolism. Smokers and those taking aluminum-containing antacids were excluded. At enrollment, only women who did not contemplate starting oral contraception until the end of the study at 18 months post-partum were recruited. Within 3 to 5 days of delivery, eligible mothers were asked whether they wanted to breast-feed their babies. Three hundred eight who declared intent to breast-feed their infants according to a proposed, standardized schedule made up the lactation cohort. Each gave written informed consent at enrollment. They agreed to fully breast-feed their infants for 6 months, followed by a 1-month period of weaning, and to take cabergoline administered at the end of the seventh postpartum month. Cabergoline, a long-acting dopamine agonist, is used routinely for lactation suppression at our institution. Diet was unrestricted, but lactating women were allocated either no dietary supplement or a daily calcium supplement of 1 g. Calcium supplementation was restricted to lactating mothers and was assigned using a computer-generated list of random numbers. One hundred seventy-four other women who declared no intent to breast-feed were given lactation suppression with cabergoline between postpartum days 2 and 3 and formed the nonlactating cohort. Of 308 women in the lactation cohort, 274 completed the 6-month follow-up. Among those who withdrew in the first 6 months, 24 started bottle feeding between 2 and 6 months postpartum, and ten others said they wanted to take oral contraceptives after the weaning month. Of 174 women in the nonlactating cohort, 153 completed the study; the other 21 requested oral contraception after 3–5 menstrual cycles and therefore were excluded from analysis.

The women were instructed to record the date they resumed menstruation, the following menstrual bleedings, and monthly measurements of body weight. In all women, we measured bone mineral density of the radius and spine (L2–L4) at baseline (postpartum days 5–10) and at 3, 6, and 12 or 18 months postpartum. Lactating mothers also had bone mineral density measurements at 7 months postpartum, at the end of the weaning period. All bone mineral density values were adjusted for weight and height of each woman.

Bone mineral density of the radius of the nondominant arm was measured using the Osteometer DTX 100 (Osteometer A/S, Roedovre, Denmark) where the distance between the ulna and radius is less than 8 mm (automatic scanning) and the trabecular and cortical components of the radius are similar to those of the lumbar spine. The coefficient of variation was 1.2%. To evaluate bone mineral density at the lumbar spine (vertebrae L2–L4), we used a dual energy x-ray absorptiometer (Norland XR 26; Norland Corp, Fort Atkinson, WI) with 1.1% coefficient of variation.

To assess the association between radius and spine bone mineral density at the start of observation, Spearman correlation coefficient was computed, and to verify the independence of treatment group, multiple regression was used. Nonparametric analysis of variance (Kruskall-Wallis test) was used, because of the presence of nonhomogeneous variances across groups. For post hoc comparisons, the Mann-Whitney U test was used. To overcome possible differences at baseline, the relative percentage change in density with respect to baseline was computed for all times and was considered the outcome of interest. A generalized linear model was used for the analysis of repeated measurements (percent change) for radium and spine mineral density, to compare the three study groups over time. To assess the additional and independent effect of early versus late resumption of menstruation (no more than 5 versus over 5 months postpartum) on bone mineral density in breast-feeding women, with or without calcium supplementation, a new model was fitted that included time, treatment group, and time to resumption of menstruation, with the interaction of the latter two. P < .05 was statistically significant. Stata 5.0 (StataCorp, College Station, TX) was used for computation.


   Results
Top
Abstract
 Materials and Methods
 Results
Discussion
 References
 
Demographic characteristics of women who completed the 6-month follow-up are shown in Table 1Go. At baseline, there were no differences among the three groups in age, height, body weight, parity, and body mass index (BMI), with all subjects aged between 27 and 36 years.


View this table:
[in this window]
[in a new window]
  		Table 1. Demographic Characteristics
 
Wanting to use oral contraception was the reason for most withdrawals in the lactation cohort. Between 12 and 18 months, 22 lactating women who were taking no calcium supplement withdrew from the study, of whom 18 decided to take oral contraceptives. The respective numbers of lactating women taking calcium were 18 and 16, leaving 113 women taking no calcium and 121 with calcium in the lactating cohort available for the final 18-month evaluation.

Strong correlation between spine and radius measurements was found at the start, with a Spearman correlation coefficient of 0.7197 (P < .01); this association was independent of study group. Percent variations of bone mineral density of the spine and radius in the three groups are shown in Table 2Go. There was a significant progressive decline in bone mineral density in the lactation cohort during the first 6 months post-partum. A significant recovery of bone mass was found thereafter, levels that at 18 months were higher than baseline levels. In the nonlactating cohort, bone mineral density of the spine increased progressively and at 18 months postpartum was 1.9% higher than baseline levels. A similar pattern was found for bone mineral density of the radius, with an increase up to 1.1% by 18 months postpartum. When groups were compared over time, we found a significant decrease in bone loss in between lactating women receiving no calcium and lactating women with calcium, and between those and controls, for radius and spine mineral density, as well as a significant decrease over time. However, calcium supplementation did not allow us to separate breast-feeding mothers for the spine measurement. No interaction was observed between time and group. Twelve months after breast-feeding cessation, no significant differences in bone mineral density of radius or spine were found between groups.


View this table:
[in this window]
[in a new window]
  		Table 2. Bone Mineral Density Percent Changes in the Spine* and Radius{dagger}
 
To assess the impact of the return of menstruation on bone mineral density, lactating women were further subclassified according to whether menses resumed within 5 months postpartum or later. Results are shown in Table 3Go. Among lactating women taking no calcium, 77 of 135 had menstrual flow within 5 months, compared with 80 of 139 taking calcium. There were significant differences in bone mineral density at the levels of radius and spine in both groups between women who had menstruated early and those who had not. Such differences were evident at 6–7 months postpartum, but did not persist at 18 months. All nonlactating controls resumed menses within 35–55 days postpartum, thus they were not categorized by timing of menstruation.


View this table:
[in this window]
[in a new window]
  		Table 3. Bone Mineral Density Percent Changes in Lactating Women According to Return of Menstruation
 
Among breast-feeding women, calcium supplementation and amenorrhea duration independently predicted changes in radius mineral density over time, but no interaction was observed between them. To better illustrate the phenomenon, all pairwise comparisons among the four subgroups of subjects, which were significant at 1% level, were done. A decreasing loss of radius mineral density was observed from the no-calcium, late-menstruation subgroup to the with-calcium, late-menstruation subgroup, then to the no-calcium, early menstruation subgroup and with-calcium, early menstruation subgroup, in that order. In spine measurements for the same subgroups, amenorrhea duration was the only independent predictor of percentage changes in spine mineral density over time. A significant qualitative interaction was present between calcium supplementation and time to menses resumption. Pairwise comparisons of all subgroups showed significant differences at 1% level for all of them, except between the no-calcium, early menstruation subgroup and the with-calcium, early-menstruation subgroup, where no differences were found. As with the radius, decreasing bone loss was observed across subgroups.

A more rapid weight loss was seen in controls compared with lactating women at 6 months (mean weight change, -4.3 ± 2.8 kg compared with -2.8 ± 2.5 kg, respectively, P < .01). At 18 months postpartum, mean values were comparable among all groups.


   Discussion
Top
Abstract
 Materials and Methods
 Results
 Discussion
References
 
Finding decreased radius and spine bone mineral density during the 6 months of lactation might prompt us to consider the risk for osteoporosis, which might lead to fractures in lactating women.13,14 However, bone mineral density values at 18 months were higher than those in early postpartum in our study, whereas others found recovery of bone mineral density even in women who become pregnant during lactation.15 Our results regarding changes in bone density of the lumbar spine over the first 12 months postpartum agree with those of other authors.2–5

Oral calcium supplements yielded significant variations in comparison with women who did not take calcium; however, the bone mineral density data at 18 months postpartum suggested that calcium supplementation might have only a transient effect on postpartum bone mineral changes, resulting in a negligible effect on bone strength. Similar findings were reported by Prentice15 and Kalkwarf et al.16 Our study was limited by our not taking into account dietary calcium intake. Additional bias might have been introduced by our providing supplemental calcium openly.

We found that bone mineral density variations of the radius were related to those of the spine, a relationship also reported by Wardlaw and Pike,13 but negated by others.2,3,7 Our finding might be explained by the fact that measurements are done automatically by the scanning system where the trabecular component in the radius was comparable to that of the spine.10 Mineral loss during lactation was found mostly at the level of trabecular bone.

In nonlactating women, the relative increment of bone mineral density over the 18-month period might be accounted for by the early return of ovarian function. Differing patterns of bone loss were found among lactating women according to whether they resumed menstruation within 3–6 months postpartum, in accordance with findings reported by Sowers et al14 and Kalkwarf and Specker.3 Without regular ovarian function, the amount of bone loss almost doubles that found in women with regular menses. After the first 6 months postpartum, women who lost more bone mass showed a more pronounced increase in bone mineral density compared with those who lost less. At 18 months postpartum, bone mineral density values were comparable between those with early and late return of menstruation. Serum estradiol or prolactin were not measured in our study, so we could not characterize the relationship between hormonal patterns and bone mass.

Unlike most studies of lactation, our protocol provided all women with the fixed time limits of 6 months for lactation and 1 month for weaning. Cabergoline administration at 7 months postpartum to women who breast-fed decreased prolactin levels and restored the function of the pituitary-ovarian axis more rapidly. In theory, that might have been beneficial to bone mass recovery.


   Footnotes
 
PII S0029-7844(99)00236-7

Received August 31, 1998. Received in revised form November 30, 1998. Accepted December 30, 1998.


   References
Top
Abstract
 Materials and Methods
 Results
 Discussion
 References
 
1. Specker BL, Tsang RC, Ho ML. Changes in calcium homeostasis over the first year postpartum: Effect of lactation and weaning. Obstet Gynecol 1991;78:56–62.[Abstract/Free Full Text]

2. Hayslip CC, Klein TA, Wray HL, Duncan WE. The effect of lactation on bone mineral content in healthy postpartum women. Obstet Gynecol 1989;73:588–92.[Abstract/Free Full Text]

3. Kalkwarf HJ, Specker BL. Bone mineral loss during lactation and recovery after weaning. Obstet Gynecol 1995;86:26–32.[Abstract]

4. Atkinson PJ, West RR. Loss of skeletal calcium in lactating women. J Obstet Gynaecol Br Comm 1970;77:555–60.[Medline]

5. Lamke B, Brundin J, Moberg P. Changes of bone mineral content during pregnancy and lactation. Acta Obstet Gynecol Scand 1977; 56:217–9.[Medline]

6. Chan GM, Slater P, Ronald M, Roberts CC, Thomas HR, Folland D, et al. Bone mineral status of lactating mothers of different ages. Am J Obstet Gynecol 1982;144:438–41.[Medline]

7. Frisancho AR, Garn SM, Ascoli W. Unaltered cortical area of pregnant and lactating women. Studies of the second metacarpal bone in North and Central American populations. Invest Radiol 1971;6:119–21.[Medline]

8. Cann CE, Martin MC, Genant HK, Jaffe RB. Decreased spinal mineral content in amenorrheic women. JAMA 1984;251:626–9.[Abstract]

9. Johansen JS, Riis BJ, Hassager C, Moen M, Jacobson J, Christiansen C. The effect of a gonadotropin-releasing hormone agonist analog (nafarelin) on bone metabolism. J Clin Endocrinol Metab 1988;67: 701–6.[Abstract]

10. Schlenker RA. Percentages of cortical and trabecular bone mineral mass in the radius and ulna. Am J Roentgenol 1976;126:1309–12.[Medline]

11. Cumming RG, Klineberg RJ. Breastfeeding and other reproductive factors and the risk of hip fractures in elderly women. Int J Epidemiol 1993;22:684–91.[Abstract/Free Full Text]

12. Aloia JF, Cohn SH, Vaswani A, Yeh JK, Yuen K, Ellis K. Risk factors for postmenopausal osteoporosis. Am J Med 1985;78:95–100.[Medline]

13. Wardlaw GM, Pike AM. The effect of lactation on peak adult shaft on ultradistal forearm bone mass in women. Am J Clin Nutr 1986;44:283–6.[Abstract/Free Full Text]

14. Sowers MF, Hollis BW, Shapiro B, Randolph J, Janney CA, Zhang D, et al. Elevated parathyroid hormone-related peptide associated with lactation and bone density loss. JAMA 1996;276:549–54.[Abstract]

15. Prentice A. Calcium supplementation during breast-feeding. N Engl J Med 1997;337:558–9.[Free Full Text]

16. Kalkwarf HJ, Specker BL, Bianchi DC, Ranz J, Ho M. The effect of calcium supplementation on bone density during lactation and after weaning. N Engl J Med 1997;337:523–8.[Abstract/Free Full Text]




This article has been cited by other articles:


Home page
 IBMS BoneKEyHome page
J. J. Wysolmerski
Conversations Between Breast and Bone: Physiological Bone Loss During Lactation as Evolutionary Template for Osteolysis in Breast Cancer and Pathological Bone Loss After Menopause
IBMS BoneKEy, August 1, 2007; 4(8): 209 - 225.
[Abstract] [Full Text] [PDF]

Home page
 EndocrinologyHome page
L. Ardeshirpour, P. Dann, D. J. Adams, T. Nelson, J. VanHouten, M. C. Horowitz, and J. J. Wysolmerski
Weaning Triggers a Decrease in Receptor Activator of Nuclear Factor-{kappa}B Ligand Expression, Widespread Osteoclast Apoptosis, and Rapid Recovery of Bone Mass after Lactation in Mice
Endocrinology, August 1, 2007; 148(8): 3875 - 3886.
[Abstract] [Full Text] [PDF]

Home page
 Reproductive SciencesHome page
M. Shaarawy, S. Zaki, A.-M. Ramzi, M. E. Salem, and A. M. El-Minawi
Feto-maternal Bone Remodeling in Normal Pregnancy and Preeclampsia
Reproductive Sciences, July 1, 2005; 12(5): 343 - 348.
[Abstract] [PDF]

Home page
 Am. J. Clin. Nutr.Home page
B. Specker
Vitamin D requirements during pregnancy
Am. J. Clinical Nutrition, December 1, 2004; 80(6): 1740S - 1747S.
[Abstract] [Full Text] [PDF]

Home page
 Arch Pediatr Adolesc MedHome page
C. J. Chantry, P. Auinger, and R. S. Byrd
Lactation Among Adolescent Mothers and Subsequent Bone Mineral Density
Arch Pediatr Adolesc Med, July 1, 2004; 158(7): 650 - 656.
[Abstract] [Full Text]

Home page
 Hum ReprodHome page
H. Matsushita, T. Kurabayashi, M. Tomita, and K. Tanaka
Effects of vitamin D and estrogen receptor gene polymorphisms on the changes in lumbar bone mineral density with multiple pregnancies in Japanese women
Hum. Reprod., January 1, 2004; 19(1): 59 - 64.
[Abstract] [Full Text] [PDF]

Home page
 EndocrinologyHome page
J. N. VanHouten and J. J. Wysolmerski
Low Estrogen and High Parathyroid Hormone-Related Peptide Levels Contribute to Accelerated Bone Resorption and Bone Loss in Lactating Mice
Endocrinology, December 1, 2003; 144(12): 5521 - 5529.
[Abstract] [Full Text] [PDF]

Home page
 J. Nutr.Home page
A. Prentice
Micronutrients and the Bone Mineral Content of the Mother, Fetus and Newborn
J. Nutr., May 1, 2003; 133(5): 1693S - 1699.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Clin. Nutr.Home page
L. M Paton, J. L Alexander, C. A Nowson, C. Margerison, M. G Frame, B. Kaymakci, and J. D Wark
Pregnancy and lactation have no long-term deleterious effect on measures of bone mineral in healthy women: a twin study
Am. J. Clinical Nutrition, March 1, 2003; 77(3): 707 - 714.
[Abstract] [Full Text] [PDF]

Home page
 J. Nutr.Home page
P. B. Moser-Veillon, A. R. Mangels, N. E. Vieira, A. L. Yergey, K. Y. Patterson, A. D. Hill, and C. Veillon
Calcium Fractional Absorption and Metabolism Assessed Using Stable Isotopes Differ between Postpartum and Never Pregnant Women
J. Nutr., September 1, 2001; 131(9): 2295 - 2299.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
C. S. Kovacs
Calcium and Bone Metabolism in Pregnancy and Lactation
J. Clin. Endocrinol. Metab., June 1, 2001; 86(6): 2344 - 2348.
[Full Text] [PDF]

Home page
 J. Nutr.Home page
J. M. Hopkinson, N. F. Butte, K. Ellis, and E. O’B. Smith
Lactation Delays Postpartum Bone Mineral Accretion and Temporarily Alters Its Regional Distribution in Women
J. Nutr., April 1, 2000; 130(4): 777 - 783.
[Abstract] [Full Text]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by POLATTI, F.
Right arrow Articles by KLERSY, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by POLATTI, F.
Right arrow Articles by KLERSY, C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS