QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hopkinson, J. M. Articles by Smith, E. O達. Search for Related Content PubMed PubMed Citation Articles by Hopkinson, J. M. Articles by Smith, E. O達.

---

Article

Lactation Delays Postpartum Bone Mineral Accretion and Temporarily Alters Its Regional Distribution in Women ^{1 ,2 ,3}

U.S. Department of Agriculture/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX

⁴To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The objective of this work was to compare long-term changes in bone mineral in lactating (L) and nonlactating (NL) women for 2 y postpartum. The 40 L women (mean duration of breastfeeding 345 ± 177 d) and 36 NL women were enrolled during late pregnancy. Subjects were healthy and nonsmoking with a mean age of 28.8 ± 4.1 y. Bone mineral content (BMC) was measured at 0.5, 3, 6, 12, 18 and 24 mo by dual-energy X-ray absorptiometry set for total body scan with regional analysis. BMC adjusted for bone area, weight and height (adj-BMC) decreased in L women at the lumbar spine (-3.1%, P < 0.001) and pelvis (-0.9%, P = 0.03) by 3 mo, and at the total body (-0.9%, P = 0.05) by 6 mo. Losses were recovered following onset of menses. Adj-BMC at the lumbar spine, pelvis, thoracic spine and total body increased over baseline by 24 mo in L women. In NL women, adj-BMC increased over baseline within 3 mo and continued to increase thereafter. Net total-body gains were greater in the 27 NL women who completed the final measurement than in their 26 L counterparts (+2.3% vs. +0.6%, P = 0.001). Net regional gains differed at the head, legs, and ribs, but not at the lumber spine, pelvis or thoracic spine. Duration of breastfeeding, parity, onset of menses and maternal age affected bone changes in L women. These results indicate that lactation delays bone mineral accretion and temporarily alters its regional distribution in postpartum women.

KEY WORDS: • lactation • bone • parity • age • postpartum • women

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Because lower bone mass increases the risk of osteoporosis, the decline in bone density associated with lactation has received considerable attention. Decreases of 4–6% in lumbar spine bone mineral density (BMD)⁵ have been reported during the first 6 mo of lactation (Affinito et al. 1996 , Cross et al. 1995 , Hayslip et al. 1989 , Kalkwarf and Specker 1995 , Kolthoff et al. 1998 , Krebs et al. 1997 , Laskey et al. 1998 , Polatti et al. 1999 , Ritchie et al. 1998 , Sowers et al. 1993 ). Similar BMD losses have been reported at the hip, ultradistal radius, femoral neck, pelvis and thoracic spine (Drinkwater and Chestnut 1991 , Kent et al. 1990 , Kolthoff et al. 1998 , Lamke et al. 1977 , Laskey et al. 1998 , Polatti et al. 1999 , Sowers et al. 1993 ). These losses have been attributed to the hypoestrogenic state of lactational amenorrhea, combined with calcium losses in breast milk of ~210 mg/d. While some studies have not detected bone loss, these discrepancies are likely resulting from variations in the bone sites examined, the timing of the measurements during lactation and the method of measurement. Recovery of BMD to baseline has been reported at the lumbar spine, hip and radius within 6 mo of weaning (Kalkwarf and Specker 1995 , Kolthoff et al. 1998 , Krebs et al. 1997 , Polatti et al. 1999 , Ritchie et al. 1998 , Sowers et al. 1993 ).

Recently, net gains have been observed in lactating (L) women 12 mo after weaning at the lumbar spine and radius (Polatti et al. 1999 ). Nonlactating (NL) postpartum women also gain BMD at the lumbar spine, according to some reports (Caird et al. 1994 , Kalkwarf and Specker 1995 , Polatti et al. 1999 ). Pollati et al. (1999) recently reported that net gains in BMD of the lumbar spine and radius do not differ between L and NL women who did not conceive a second child within 18 mo postpartum, suggesting no residual effect of lactation on BMD at these sites. Total body bone mineral content (BMC) also declines during lactation, and subsequent recovery to baseline was not observed within 12–18 mo of delivery or at 6–8 mo postweaning (Kalkwarf and Specker 1995 , Kolthoff et al. 1998 , Ritchie et al. 1998 ). The possibility of prolonged lactation-related bone loss at other skeletal sites has not been explored. Longitudinal comparisons of changes in total BMC in L and NL women beyond 18 mo postpartum are lacking. Hence, little data are available for examining the long-term effect of lactation on primarily cortical bone sites.

We measured total body and regional BMC between 0.5 mo and 24 mo postpartum in 40 L and 36 NL women. Our objectives were: i) to compare changes in BMC in L and NL women over 24 mo postpartum and ii) to determine whether net changes in BMC at 2 y postpartum are associated with duration of lactation, amenorrhea, maternal demographic variables, voluntary exercise and/or changes in body weight.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Subjects.

Healthy, normotensive, nonsmoking, nondiabetic women from the Houston area were recruited in their third trimester of pregnancy. Infant feeding intentions were noted. Women who planned to breastfeed exclusively for a minimum of 4 mo were enrolled in the L group. Women who planned to formula-feed from birth were enrolled in the NL group. Participants were enrolled throughout the calendar year, and there were no differences between groups in the season of delivery of the infants; 40 L and 36 NL women were enrolled. A total of 19 women discontinued the study before completion of the 24-mo measurement due to pregnancy and 4 due to relocation; 26 L and 27 NL women completed the 24 mo. Because the 18-mo measurement was added after the study was underway, only 43 subjects were measured at both 18 and 24 mo while 53 subjects completed the 24-mo measurement. The study was approved by the Baylor Affiliates Review Boards for Human Subject Research, and informed written consent was obtained from each subject.

Experimental Design.

We set out to measure BMC by dual-energy X-ray absorptiometry (DXA) at 0.5, 3, 6, 12 and 24 mo postpartum. An 18-mo postpartum measurement was added to the design after several women became pregnant before the final 24-mo measurement. Breastfeeding frequency, use of complementary infant foods, voluntary exercise, maternal illness and use of hormonal contraceptives and medications were determined by questionnaire during pregnancy and at 3, 6, 9, 12, 18 and 24 mo postpartum.

Standard anthropometric measurements were conducted at each time point. Body weight and height were measured using an electronic balance (Healthometer, Bridgeview, IL) and stadiometer (Holtain Limited, Crymych, United Kingdom), respectively. Instrument calibrations were checked on a weekly basis.

Bone mineral measurements.

DXA was performed at each postpartum visit using a Hologic QDR-2000 (Hologic, Waltham, MA) in pencil beam mode (software version 5.56). The whole body was scanned, and regional partitioning for the head, arms, ribs, thoracic spine, lumbar spine, pelvis and legs was obtained according to the manufacturer’s instructions. Although site-specific scans of the hip and lumbar spine regions afford greater accuracy, we chose this method to reduce the radiation exposure and to evaluate relative changes in various parts of the skeleton on a group basis only. Using this methodology, the rib region includes the scapulae and the majority of the clavicles, the thoracic spine region includes a small portion of the clavicles and sternum and the femoral neck is bisected by the line dividing the pelvic region from the legs. The lumbar spine region includes the area from the first lumbar vertebra to a horizontal line just above the top of the iliac crest. Subjects were provided with gowns and removed all articles of clothing or jewelry containing metal whenever possible. The precision for BMC using a spine phantom was 0.5%, during the 5.5-y period of this study. Drift in the calibration during this period was negligible (<0.01%).

Voluntary exercise.

Activity levels were determined using a Physical Activity Questionnaire at each time point (Blair 1984 ). The individual was asked whether she routinely participated in voluntary exercise during the previous month, and if so, the type, frequency and duration of each activity. Frequency and duration of "moderate," "hard" and "very hard" activities were tabulated separately and expressed as average hours per day.

Onset of menses and hormonal contraceptive use.

At each visit, participants were asked to recall the date of their last menses, and the date on which menses resumed following delivery if not previously recorded. Contraceptive use and medications were recorded by type at each measurement interval. Hormonal contraceptive methods were later grouped together and their use coded as a binary (yes/no) variable at each visit.

Statistical analysis.

Data are summarized as means ± SD unless otherwise indicated. Descriptive statistics, correlation and multiple regression analysis were performed using Minitab (release 11; Minitab, State College, PA). Because of concerns that BMD affords incomplete adjustment among individuals of BMC for bone and body size, we adjusted BMC for bone area (BA), height and weight as covariates in the ANOVA and regression models. We refer to the outcomes as adjusted BMC (adj-BMC) after the manner of Prentice et al. (1994) and Laskey et al. (1998) . Repeated measures ANOVA with time-varying covariates was performed using BMDP (Statistical Software, Los Angeles, CA) to test the effects of lactation and time postpartum on BMC. Version BMDP-5V, which estimates missing data points, was used for analyses of multiple time points and BMDP-2V, which disallows incomplete data sets, was used for comparison of any two time points.

The basic model included BMC as the dependent variable, a grouping factor (L or NL), linear and quadratic functions of time, covariates (BA, weight, height) and interactions between group and time. Significant interactions were further examined by analyzing the effect of time within each group and making comparisons between L and NL women using one-way ANOVA. Covariates (age, parity, gravidity, prepregnancy weight, onset of menses, time postweaning, voluntary exercise, hormonal contraceptive use, month of measurement) were entered to test their effect on the changes in adj-BMC. In addition, the relative impact of significant covariates on the net change in adj-BMC over the 24 mo of the study was examined using multiple regression.

A wide variety of contraceptive hormones was used by both L and NL women during the course of the study, and no analysis could be made regarding individual preparations. Parity was examined as a continuous variable (1–4), and as a dichotomous variable (primaparous or multiparous) to avoid undue influence from the small number of women with parity >2. The ethnic makeup of the study participants provided insufficient power to examine the impact of race.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
There were no differences in baseline weight, height, age, gravidity, parity or ethnic distribution between L and NL women (Table 1 ). The mean duration of breastfeeding was 327 d (range 109–760). On average, L women resumed menses ~5 mo later than NL women (P < 0.001). By design, all L women breast-fed exclusively for at least 4 mo. At 6 mo, eight of these women had weaned their babies, four were still exclusively breastfeeding and 28 were partially breastfeeding. By 9 mo, all infants were receiving beikost. Use of hormonal contraceptives was sporadic. Several women changed hormonal preparations or switched between barrier and hormonal methods during the study. NL women were more likely to use hormonal contraceptives in the first 6 mo (P = 0.03).

There were no differences between total body BMC of L and NL women at the 0.5-mo baseline measurement. In addition to BA, maternal weight (r = 0.59, P < 0.01) and height (r = 0.56, P = 0.001) were positively correlated with total body BMC. Feeding mode, maternal age, gravidity and parity at baseline were not significantly related to total body BMC adjusted for weight, height and BA (adj-BMC). Regional adj-BMC did not differ between feeding groups at any skeletal region at 0.5 mo postpartum (Table 2 ).

By 6 mo postpartum, L women had lost 0.9% of total body adj-BMC (P = 0.05). Losses were recovered and followed by net gains over baseline (+0.6%, P = 0.03) within 24 mo postpartum. Conversely, NL women gained 0.8% of adj-BMC by 3 mo (P < 0.001) and continued to gain thereafter (Fig. 1 ). Between 0.5 and 24 mo, net gains in adj-BMC of NL women (+2.3%, P = 0.002) were greater than those in L women (P = 0.001). Change in BMC was correlated with change in body weight (r = 0.63, P = 0.001). Changes in adj-BMC differed between L and NL groups, as indicated by significant interactions between feeding group and both linear and quadratic functions of time in the repeated measures analyses (P < 0.001). The linear and quadratic terms were significant in each group separately (L and NL), indicating curvature in the models for changes in adj-BMC in all postpartum women.

View larger version (19K): [in this window] [in a new window]   Figure 1. Mean change from 0.5 mo baseline for total body bone mineral content (g) adjusted for weight, height and bone area are plotted against time postpartum for nonlactating (NL) women, short-term (9 mo) lactating women (SL) and long-term (>9 mo) lactating women (LL). Values are means ± SEM; n = 36, 16 and 24 in NL, SL and LL women at 0.5 mo decreasing to 27, 10 and 16, respectively by 24 mo. asignificantly different (P < 0.05) from NL women; bsignificantly different (P < 0.05) from SL women.

(Table 3 )

The effects of age, parity, gravidity and duration of amenorrhea on the net change in adj-BMC from 0.5 to 24 mo were examined in L and NL women using multiple regression. The effect of breastfeeding duration was added to the analysis when breastfeeding women were examined separately. Because of the high correlation between duration of amenorrhea and duration of breastfeeding (r = 0.78; P = 0.001) and between parity and gravidity (r = 0.76; P = 0.001), only one of each pair of interchangeable predictors was entered into the model. After controlling for feed type, net 24-mo change in adj-BMC was negatively related to duration of amenorrhea and maternal age (Table 4 ). There was a significant interaction between feed type and parity with respect to net change in adj-BMC. The interaction between parity and feed type was further explored by repeating the analysis on L and NL groups separately. Parity was positively related to the 24-mo net increase in adj-BMC of the total body for L women (P = 0.001) and was unrelated to the net change in NL women. None of the other covariates were significantly related to net changes.

Factors predicting changes in total body adj-BMC in L women.

Parity: By 24 mo, adj-BMC of primiparous L women returned to values not significantly different from the 0.5-mo baseline. Conversely, adj-BMC of multiparous L women exceeded baseline by 1.8% (P 0.003) at 24 mo. Between 0.5 and 6 mo, mean changes in BMC after adjusting for weight, height and bone area were -17 g and -0.74 g in primiparous and multiparous L women, respectively (P = 0.03 for difference between groups), largely accounting for the difference at 24 mo.

Primiparous and multiparous L women did not differ by age, weight, height, baseline BMC, voluntary physical activity, duration of amenorrhea or use of hormonal contraceptives at any time point in the study. The duration of breastfeeding (381 ± 190 vs. 287 ± 141 d; P = 0.08) tended to be longer, and net weight loss was somewhat greater in primiparous women (-4.11 ± 4.05 vs. -2.08 ± 4.83 kg; P = 0.26). Parity remained a significant predictor of net 24-mo gains in BMC of L women even after adjusting for age, duration of breastfeeding, change in weight, duration of amenorrhea and baseline BMC (P < 0.001).

Duration of breastfeeding/amenorrhea.

At 24 mo, the net gain in adj-BMC was inversely related to the duration of breastfeeding (P < 0.001). Between 12 and 24 mo postpartum, gains in adj-BMC were not related to breastfeeding duration (P = 0.13) or duration of amenorrhea (P = 0.87). For the purpose of illustration, we divided the L group into short-term ( 9 mo) and long-term (9 mo) categories. The results are presented graphically in (Fig. 1) . Changes in total body adj-BMC of women who breast-fed for 9 mo or less did not differ from NL at 24 mo postpartum.

Among L women, net change in adj-BMC over 24 mo was independently related to parity (or gravidity), age and duration of breastfeeding (or amenorrhea) (Table 3) . Inclusion of parity and duration of breastfeeding in the model explained more of the variability than inclusion of gravidity and duration of amenorrhea. To rule out the possibility that differences in hormonal contraceptive use biased the results, we repeated the analysis on L women who did not use hormonal contraceptives. Of the 26 lactating women who completed the study, 15 were nonhormone users, 8 were primiparous, and 7 were multiparous. Parity (P < 0.0005), age (P < 0.002) and duration of breastfeeding (P < 0.002) were independent predictors of net change in adj-BMC in the nonhormone-using L subgroup.

Regional changes in adjusted BMC.

Loss and recovery of adj-BMC were seen at all skeletal sites except the arms. Adj-BMC of the lumbar spine (-3.1%, P = 0.0001) and pelvis (- 0.9%, P = 0.03) decreased within 3 mo in L women. Changes over time were also significant at thoracic spine, legs and head in L women. At 3 mo, differences between L and NL groups at these sites apparently resulted from gains in NL women. Adj-BMC increased in NL women at the head (+1.5%, P = 0.001), ribs (+2.3%, P = 0.003) and pelvis (+1.7%, P = 0.004) within 3 mo, and in the legs (+0.5%, P = 0.05) and thoracic spine (3.4%, P = 0.01) within 6 mo. Changes over time differed between L and NL for the total body, lumbar spine, thoracic spine, pelvis, legs, head and ribs (P < 0.004).

For the 26 L and 27 NL women who completed the 24-mo measurement, net changes in adj-BMC differed by feed type at the head, ribs, legs and arms, but not at the thoracic spine, lumbar spine or pelvis. Comparison of changes in regional BMD between L and NL women produced results qualitatively similar to changes in adj-BMC.

We also examined the impact of duration of lactation on regional changes in adj-BMC by comparing short-term (<9 mo) (SL) and long-term (>9 mo) L women (LL) with NL women (Fig. 2 ). Differences between SL women and LL women were significant at the head at 12, 18 and 24 mo; at the legs at 3, 6, 12, 18 and 24 mo; at the thoracic spine at 6 and 12 mo; at the lumbar spine at 3,6,12 and 24 mo; and at the pelvis at 6 and 12 mo. At the 24-mo measurement, net gains of LL women were lower than NL women at all body regions; those of SL women did not differ from NL at any region, with the possible exception of the head (P = 0.06) (Table 5 ).

View larger version (25K): [in this window] [in a new window]   Figure 2. Mean change in regional bone mineral content (g) adjusted for weight, height and bone area plotted against time postpartum (months) for nonlactating women (NL), short-term (9 mo) lactating women (SL) and long-term (>9 mo) lactating women (LL). (A) head, (B) ribs - including scapulae and clavicles, (C) legs, (D) thoracic spine, (E) lumbar spine, (F) pelvis. n = 36, 16 and 24 for NL, SL and LL women at 0.5 mo decreasing to 27, 10 and 16, respectively by 24 mo. asignificantly different (P < 0.05) from NL women; bsignificantly different (P < 0.05) from SL women.

View this table: [in this window] [in a new window]   Table 5. Two-year changes in regional adjusted bone mineral content of women who lactated for <9 mo (SL), 9 mo (LL) and nonlactating (NL) women1

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Our findings agree with previous reports of initial losses in BMD at the lumbar spine in L women. Typically, a loss of 4–6% of BMD at the lumbar spine has been reported during the first 3 - 6 mo of lactation (Affinito et al. 1996 , Cross et al. 1995 , Hayslip et al. 1989 , Kalkwarf and Specker 1995 , Kolthoff et al. 1998 , Krebs et al. 1997 , Laskey et al. 1998 , Polatti et al. 1999 , Ritchie et al. 1998 , Sowers et al. 1993 ). Our L women averaged a loss of 4.2% of baseline lumbar spine adj-BMC (or 4.4% expressed as BMD) in the first 6 mo of lactation. We chose to express our data as adj-BMC in order to normalize for variations in body size and to adjust for changes in body weight (Laskey et al. 1998 , Prentice at al. 1994 ).

In agreement with most investigators (Sowers et al. 1993 ) but not others (Polatti et al. 1999 ), we found that adj-BMC (or BMD) of the lumbar spine region of NL women did not change significantly during the first 6 mo postpartum. However, it did increase over baseline by 12 mo and continued to increase thereafter. The few studies which have measured long-term changes in the lumbar spine of NL women also report increases during the second half of the first postpartum year (Kalkwarf et al. 1997 , Polatti et al. 1999 ). In our cohort, total body adj-BMC of NL women was increased significantly within 3 mo of delivery (+.8%, P < 0.001). We are aware of only one other study which included longitudinal observations of total body BMC in NL postpartum women. Kalkwarf et al. (1997) reported net losses (<1%) for NL women during the first 6 mo postpartum, and significant gains between 6 and 12 mo after delivery.

Among our L women, total body BMC decreased in the first 6 mo, in agreement with some investigators (Kalkwarf and Specker 1995 , Kolthoff et al. 1998 , Laskey et al. 1998 ), but not all (Cross et al. 1995 , Ritchie et al. 1998 ). These losses were followed by recovery and net gain in mean adj-BMC of the L women. Van Loan has suggested that weight loss may alter detection of pixels containing bone by DXA, which causes an apparent or artificial decrease in the measured BMD (Van Loan et al. 1998 ). Others have suggested that decreases in BMD with weight loss are physiologic (Jensen et al. 1994 ). Our L women were losing weight during the observation period, but, as we have reported previously (Butte et al. 1997 ), neither weight loss nor fat loss differed between L women who were losing bone, and NL women who were gaining bone during the same time period. Therefore, it is not likely that the observed changes in total body BMC and the adj-BMC were an artifact or a physiological consequence of weight loss per se.

Duration of breastfeeding was inversely related to the extent of recovery/net gain of BMC at 24 mo. Duration of amenorrhea had a similar effect. However, duration of breastfeeding seemed to explain more of the variability in this cohort. Among women who breast-fed longer than 9 mo, mean adj-BMC increased over baseline only at the thoracic spine and pelvic regions. Conversely, among SL women (9 mo), gains in adj-BMC occurred at all skeletal regions examined and did not differ significantly from those of NL women at any site, with the possible exception of the head. Trabecular bone is the first to exhibit detectable bone mineral loss in lactation. The more rapid recovery of sites higher in trabecular bone compared to the total body suggests that it may also be the first to recover from lactational losses. This is further supported by the pattern of change in adj-BMC at individual skeletal regions (Fig. 2) . Working with cynomolgus macaques, Lees and Jerome (1998) reached a similar conclusion regarding recovery of lactation-related bone loss.

It seems probable that LL women would eventually exhibit increases over baseline at the remaining skeletal sites. Nonetheless, our observations raise questions about the impact of closely spaced pregnancies, multiple births and advanced maternal age on bone mass in women who lactate for long periods of time.

The relationship between parity and change in adj-BMC was unexpected. For the total body, parity and gravidity significantly predicted net gains in adj-BMC only in L women. This association remained significant after controlling for duration of breastfeeding. While differences in BMC between primiparous and multiparous women approached significance at baseline (P = 0.1), parity nevertheless remained a strong predictor (P < 0.001) of net gain in adj-BMC, after controlling for baseline BMC. The association between parity and changes in BMC is consistent with a previous observation by Berning et al. (1993) in which a positive association between parity and cortical thickness of the lumbar spine was demonstrated.

Between 18 and 24 mo postpartum, both L and NL women continued to gain BMC at similar rates, and no evidence of a plateau was seen in either group. While it is widely held that females achieve peak bone mass shortly after puberty, it is controversial whether gains continue in adult women (Anderson and Rondano 1996 ). A few reports have indicated secular gains of ~1.2% per year in total body BMC (Anderson and Rondano 1996 , Recker et al. 1992 ) in women during the third and possibly fourth decade of life. Bennell et al. (1997) found that total body BMC increased by 0.4 and 2.2% per year in younger (17–26 y) sedentary and athletic women, respectively. Increases in BMD have also been reported in women during the third and fourth decades of life (Sowers et al. 1998 , Xu et al. 1997 ). Rates of gain in BMC of our NL women over the entire 24-mo period were comparable to previous reports of secular gains in nonreproductive adult women (Bennell et al. 1997 , Recker et al. 1992 , Sowers et al. 1998 ). When our data are expressed as BMD, our NL cohort showed a gain of 2.8% per year at the lumbar spine. This gain is comparable to previous reports in NL postpartum women (Caird et al. 1994 , Kalkwarf and Specker 1995 , Polatti et al. 1999 ) as well as that reported in younger (17–26 y) power athletes (Bennell et al. 1997 ). In contrast, changes of 0 to + 1.1% per year have been reported in women of similar age but unspecified reproductive status (Alekel et al. 1996 , Barr et al. 1998 , Recker et al. 1992 , Sowers et al. 1998 ,). Whether pregnancy contributed to or modified the gains observed in the present study cannot be determined in the absence of a nonpregnant, NL control group of similar ages.

In conclusion, our data suggest that BMC at trabecular-predominate bone sites prone to osteoporotic fracture are the first to recover from lactation-associated losses. Residual effects of long-term breastfeeding on BMC may be more apparent at stronger, predominately cortical skeletal regions. However, it remains to be seen how long accretion of bone mineral continues following pregnancy and lactation, and whether long-term breastfeeding women ultimately increase BMC at all skeletal regions to the same extent as other postpartum women.

	ACKNOWLEDGMENTS

 
The authors acknowledge the contributions of time and effort from the women who participated in this study, and from the study coordinator, Carolyn Heinz. We also extend thanks to Marilyn Navarrete for subject recruitment; Sopar Seributra, Alice Ponce and Sandra Kattner for nursing and dietary support; Maurice Puyau, JoAnn Pratt, Roman Shypaillo and Judy Joo for technical assistance; Anne Adolph and Laura Ferlic for data management; J. Kennard Fraley for statistical assistance; Leslie Loddeke for editorial review; and Judith Croom for manuscript preparation.

	FOOTNOTES

 
¹ This work is a publication of the U.S. Department of Agriculture (USDA) Agricultural Research Service (ARS) Children’s Nutrition Research Center (CNRC), Department of Pediatrics, Baylor College of Medicine (BCM) and Texas Children’s Hospital (TCH), Houston, Texas.

² This project was funded in part with federal funds from the USDA/ARS under Cooperative Agreement 58–6240-6001.

³ The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

⁵ Abbreviations used: Adj-BMC, bone mineral content adjusted for bone area, weight and height; BA, bone area; BMC, bone mineral content; BMD, bone mineral density; DXA, dual energy X-ray absorptiometry; L, lactating; LL, long-term lactating/lactation; NL, nonlactating; SL, short-term lactating/lactation.

Manuscript received September 23, 1999. Initial review completed November 2, 1999. Revision accepted December 16, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Affinito P., Tommaselli G. A., DiCarlo C., Guida F., Nappi C. Changes in bone mineral density and calcium metabolism in breastfeeding women: a one year follow-up study. J. Clin. Endocrinol. Metab. 1996;81:2314-2318[Abstract]

2. Alekel L., Clasey J. L., Fehling P. C., Weigel R. M., Boileau R. A., Erdman J. W., Stillman R. Contributions of exercise, body composition and age to bone mineral density in premenopausal women. Med. Sci. Sports Exerc. 1996;28:1477-1485

3. Anderson J. J. B., Rondano P. A. Peak bone mass development of females: can young adult women improve their peak bone mass?. J. Am. Coll. Nutr. 1996;15:570-574[Abstract]

4. Barr S. I., Prior J. C., Janelle K. C., Lentle B. C. Spinal bone mineral density in premenopausal vegetarian and nonvegetarian women: Cross-sectional and prospective comparisons. J. Am. Diet. Assoc. 1998;98:760-765[Medline]

5. Bennell K. L., Malcolm S. A., Khan K. M., Thomas S. A., Reid S. J., Brukner P. D., Ebeling P. R., Wark J. D. Bone mass and bone turnover in power athletes, endurance athletes and controls: A 12-month longitudinal study. Bone 1997;20:477-484[Medline]

6. Berning B., Kuijk C., Schutte H. E., Kuiper J. W., Drogendijk A. C., Fauser B. C. Determinants of lumbar bone mineral density in normal weight, non-smoking women soon after menopause. A study using clinical data and quantitative computed tomography. Bone and Mineral. 1993;21:129-139

7. Blair S. How to assess exercise habits and physical fitness. Matarazzo J. V. Weiss M. Herd J. S. eds. Behavioral Health 1984:424-447 John-Wiley New York.

8. Butte N. F., Hopkinson J. M., Ellis K. J., Wong W. W., Smith E. O. Changes in fat-free mass and fat mass in postpartum women: a comparison of body composition models. Int. J. Obes. 1997;21:876-879

9. Caird L. E., Reid-Thomas V., Hannan W. J., Gow S., Glasier A. F. Oral progestogen-only contraception may protect against loss of bone mass in breast-feeding women. Clin. Endocrinology 1994;41:739-745[Medline]

10. Cross N. A., Hillman L. S., Allen S. H., Krebs N. F. Changes in bone mineral density and markers of bone remodeling during lactation and postweaning in women consuming high amounts of calcium. J. Bone Miner. Res. 1995;10:1312-1320[Medline]

11. Drinkwater B. L., Chesnut C. H. Bone density changes during pregnancy and lactation in active women: a longitudinal study. Bone and Mineral 1991;14:153-160[Medline]

12. Hayslip C., Klein T. A., Wray H. L., Duncan W. E. Effects of lactation on bone mineral content in healthy postpartum women. Obstet. Gynecol. 1989;73:588-592[Medline]

13. Jensen L. B., Quaade F., Sorensen O. H. Bone loss accompanying voluntary weight loss in obese humans. J. Bone Miner. Res. 1994;9:459-463[Medline]

14. Kalkwarf H. J., Specker B. L. Bone mineral loss during lactation and recovery after weaning. Obstet. Gynecol. 1995;86:26-32[Medline]

15. Kalkwarf H. J., Specker B. L., Bianchi D. C., Ranz J., Ho M. The effect of calcium supplementation on bone density during lactation and after weaning. N. Engl. J. Med. 1997;337:532-538

16. Kalkwarf H. J., Specker B. L., Ho M. Effects of calcium supplementation on calcium homeostasis and bone turnover in lactating women. J. Clin. Endocrin. Metab. 1999;84:464-470[Abstract/Free Full Text]

17. Kent G. N., Price R. I., Gutteridge D. H., Smith M., Allen J. R., Bhagat C. I., Barnes M. P., Hickling C. J., Retallack R. W., Wilson S. G., Devlin R. D., Davies C., St. John A. Human lactation: forearm trabecular bone loss, increased bone turnover, and renal conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J. Bone Miner. Res. 1990;5:361-369[Medline]

18. Kolthoff N., Eiken P., Kristensen B., Nielsen S. P. Bone mineral changes during pregnancy and lactation: a longitudinal cohort study. Clin. Sci. 1998;94:405-412[Medline]

19. Krebs N. F., Reidinger C. J., Robertson A. D., Brenner M. Bone mineral density changes during lactation: maternal, dietary, and biochemical correlates. Am. J. Clin. Nutr. 1997;65:1738-1746[Abstract/Free Full Text]

20. Lamke B., Brundin J., Moberg P. Changes of bone mineral content during pregnancy and lactation. Acta Obstet. Gynecol. Scand. 1977;56:217-219[Medline]

21. Laskey M. A., Prentice A., Hanratty L. A., Jarjou L. M. A., Dibba B., Beavan S. R., Cole T. J. Bone changes after 3 mo of lactation: influence of calcium intake, breast-milk output, and vitamin D-receptor genotype. Am. J. Clin. Nutr. 1998;67:685-692[Abstract]

22. Lees C. J., Jerome C. P. Effects of pregnancy and lactation on bone in cynomolgus macaques: histomorphometric analysis of iliac biopsies. Bone 1999;22:545-549

23. Polatti F., Capuzzo E., Viazzo F., Colleoni R., Klersy C. Bone mineral changes during and after lactation. Obstet. Gynecol. 1999;94:52-56[Medline]

24. Prentice A., Parsons T. J., Cole T. J. Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants. Am. J. Clin. Nutr. 1994;60:837-842[Abstract/Free Full Text]

25. Recker R. R., Davies K. M., Hinders S. M., Heaney R. P., Stegman M. R., Kimmel D. B. Bone gain in young adult women. JAMA 1992;268:2403-2408[Abstract/Free Full Text]

26. Ritchie L. D., Fung E. B., Halloran B. P., Turnlund J. R., Van Loan M. D., Cann C. E., King J. C. A longitudinal study of calcium homeostasis during human pregnancy and lactation and after resumption of menses. Am. J. Clin. Nutr. 1998;67:693-701[Abstract]

27. Sowers M., Corton G., Shapiro B., Jannausch M., Crutchfield M., Smith M. L., Randolph J. F., Hollis B. Changes in bone density with lactation. JAMA 1993;269:3130-3135[Abstract/Free Full Text]

28. Sowers M., Crutchfield M., Bandekar R., Randolph J. F., Shapiro B., Schork M. A., Jannausch M. Bone mineral density and its change in pre- and perimenopausal white women: The Michigan Bone Health Study. J. Bone Miner. Res. 1998;13:1134-1140[Medline]

29. Van Loan M. D., Johnson H. L., Barbieri T. F. Effect of weight loss on bone mineral content and bone mineral density in obese women. Am. J. Clin. Nutr. 1998;67:734-738[Abstract]

30. Xu S. Z., Huang W. M., Ren J. Y. The new model of age-dependent changes in bone mineral density. Growth Dev. Aging. 1997;61:19-26[Medline]

This article has been cited by other articles:

				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]

				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]

				S. DeSantiago, L. Alonso, A. Halhali, F. Larrea, F. Isoard, and H. Bourges Negative calcium balance during lactation in rural Mexican women Am. J. Clinical Nutrition, October 1, 2002; 76(4): 845 - 851. [Abstract] [Full Text] [PDF]

				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]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hopkinson, J. M. Articles by Smith, E. O達. Search for Related Content PubMed PubMed Citation Articles by Hopkinson, J. M. Articles by Smith, E. O達.