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ORIGINAL RESEARCH |
From MRC Human Nutrition Research (formerly The Dunn Nutritional Laboratory), Cambridge, United Kingdom.
Address reprint requests to: M. Ann Laskey, Dphil MRC Human Nutrition Research Downhams Lane Milton Road Cambridge CB4 1XJ United Kingdom E-mail: ann.laskey{at}mrc-hnr.cam.ac.uk
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Abstract |
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Methods: Fifty-nine breast-feeding women, 11 formula-feeding women, and 22 nonpregnant, nonlactating women had dual-energy x-ray absorptiometry measurements of the whole body, spine, hip, and forearm at 0.5 (baseline), 3, 6, and 12 months postpartum, with an additional measurement at 3 months after lactation for women who had breast-fed for more than 9 months.
Results: Lactation was associated with decreases in bone mineral at the whole body, spine, femoral neck, total hip, and radial wrist, which reversed as lactation declined and menstruation resumed. These changes were not seen in formula-feeding women. The magnitude and duration of the response were greater for women who breast-fed for a longer time. After lactation had stopped for at least 3 months, bone mineral, adjusted for bone area, had increased significantly above baseline at the whole body (+1.44%; 95% confidence interval [CI] +0.97%, +1.91%; P < .001), spine (+2.66%; 95% CI +1.60%, +3.72%; P < .001), and greater trochanter (+3.55%; 95% CI +2.53%, +4.57%; P < .001), was not different at the total hip and radial shaft, but was lower at the femoral neck (-2.07%; 95% CI -3.21%, -0.93%; P < .001) and radial wrist (-1.23%; 95% CI -1.99%, -0.47%; P < .01). Changes after lactation were largely independent of the duration of lactation or amenorrhea, and similar effects were observed in formula-feeding women.
Conclusion: Lactation was associated with temporary decreases in bone mineral. After lactation, there were significant residual effects on bone mineral that were unrelated to the duration of lactation and may be related to having been pregnant. The long-term effect of lactation on the femoral neck requires further investigation.
During lactation, calcium is required for breast milk production, and the extra demand might mobilize bone mineral from the maternal skeleton, potentially influencing women’s osteoporosis risk in later life. Epidemiologic studies of the effects of lactation on bone mineral and later fracture risk are contradictory; some studies found a benefit,1 others a detriment,2 and still others found no effect.3,4 The conflicting results of these studies probably relate to recall bias. Recent longitudinal studies have shown consistently that lactation is associated with a reversible decrease in bone mineral.5–11 There is disagreement about which skeletal regions are most affected and whether changes are still evident after breast-feeding has stopped.
The aim of the present study was to investigate the influence of lactation and weaning on bone mineral. Women who chose not to breast-feed were included to differentiate between the effects of lactation and recent pregnancy. Measurements of women who had not been pregnant recently were included to investigate any variations in bone mineral unrelated to lactation and recent pregnancy and to monitor the long-term reproducibility of bone mineral measurements. This report extends a previous analysis that focused on changes in bone mineral by 3 months.12 That study found that lactation was associated with significant decreases in bone mineral at the spine, hip, and whole body and that a major predictor of the decrease at the spine was the volume of breast milk consumed by infants. This report describes the pattern of bone mineral changes during and after lactation by women who breast-fed for different lengths of time and the possible determinants of differences in response among individuals, including duration of amenorrhea, weight changes, and calcium intake.
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Materials and Methods |
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Women visited the Dunn Clinical Nutrition Centre as soon as possible after discharge from the hospital (0.5 months postpartum, baseline) and again at 3, 6, and 12 months postpartum. An additional visit was made 3 months after cessation of lactation if women breast-fed for more than 9 months. Measurements of breast-feeding women were done on the following days after delivery, expressed as mean (standard deviation [SD], range): baseline, 17 (5, 10–42) days; 3 months, 90 (5, 79–104) days; 6 months, 181 (11, 157–217) days; 12 months, 358 (17, 290–396) days; and postlactation, 485 (83, 401–709) days. The corresponding values for formula-feeding women were: baseline, 19 (7, 10–29) days; 3 months, 90 (13, 67–120) days; 6 months, 186 (15, 166–218) days; and 12 months, 366 (11, 349–384) days. Measurements of nonpregnant, nonlactating women were done after baseline measurements at 3 months, 85 (20, 46–124) days; 6 months, 164 (32, 102–244) days; and 12 months, 336 (73, 152–415) days.
Height and weight were measured at each visit. Calcium intake of volunteers was determined at each time point using the Calquest food frequency questionnaire (Calquest; Department of Food and Nutritional Sciences, King’s College, London, UK), and at 2 months postpartum a prospective 7-day diary was completed. Calcium intake from supplements and medication was included in the totals. Details of these measurements have been published.12
The bone mineral content (g) and bone area (cm2) of the whole body, lumbar spine (L1–L4), left hip, and nondominant forearm were measured by dual-energy x-ray absorptiometry (Hologic QDR-1000/W with system software V.6.10C; Hologic Inc., Waltham, MA). The performance mode was used for the spine and hip (femoral neck, greater trochanter, and total hip) measurements, and Hologic software V4.47P was used for analysis. Two regions of the radius were examined, the ultradistal (wrist) and the distal third (shaft) (Hologic analysis software V5.61Q). The enhanced whole-body analysis was used (Hologic analysis software V5.61). Repeat scans for each subject were analyzed using the compare mode. Quality assurance and long-term instrument stability were assessed daily using the Hologic spine phantom. Over the 4 years of the study, coefficients of variation of phantom measurements of bone mineral content and bone area were less than 0.4%, and there was no indication of a significant drift with time. Values for the longitudinal precision (coefficient of variation) of bone mineral content adjusted for bone area for in vivo measurements, determined from two sets of scans approximately 3 months apart from the 22 control subjects, were whole body 0.5%, spine 0.9%, total hip 1.2%, femoral neck 2.3%, greater trochanter 2.2%, radial wrist 1.4%, and radial shaft 1.2%. Bone mineral densities of the three groups, at all skeletal sites investigated, were similar to each other and close to the mean values of the manufacturer’s reference data appropriate for their ages.
Statistical analysis was done using Linear Model Software DataDesk 4.1 (Data Description Inc., Ithaca, NY), which combines elements of analysis of variance, analysis of covariance, and multiple regression analysis in integrated models. Scheffé post hoc tests were used for significance of differences between pairs of discrete variables to minimize problems of multiple testing. Continuous variables were transformed to natural logarithms to ease interpretation of statistical models, an approach that permits examination of proportional (percentage) differences between discrete variables.13 Bone mineral content was adjusted for bone area using regression analysis, rather than calculating areal bone mineral density, to avoid incomplete bone area correction.14
Trends in bone mineral across time at each skeletal site were examined using two modeling approaches: repeat-measures analysis of covariance (hierarchical form) with bone mineral content as the dependent variable and bone area, subject, and time point as independent variables; and longitudinal quadratic modeling using bone mineral content as the dependent variable and bone area, days postpartum, square of days postpartum, and subject as independent variables. Fixed and mixed (fixed plus random) models gave similar results, and the analysis of covariance models were not altered by adjusting for days postpartum. The influence of potential predictors of change in bone mineral over time was examined by multiple regression analysis to identify predictors of change in bone mineral content between two time points15 and unified regression based on the longitudinal quadratic models. In both cases, variables were added separately in the first instance and together using a simultaneous (partial, type 3) modeling procedure, with backward elimination of nonsignificant variables.
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Results |
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. Breast-feeding, formula-feeding, and nonpregnant, nonlactating control women were similar in OC usage and smoking habits. Breast-feeding and formula-feeding women lost similar amounts of weight during the study (mean ± SD, breast-feeding -5.4 ± 5.0%, formula-feeding -6.8 ± 6.4%; difference across time P < .001, difference between groups not significant). There was no significant change in weight among the controls. Breast-feeding women had a higher calcium intake at baseline than formula-feeding women and nonpregnant, nonlactating women (P < .001). Similar differences in calcium intake between the groups were noted at 2 months postpartum as measured by prospective 7-day diaries. Calcium intake of the breast-feeding women decreased over time and was not significantly different from that of the other two groups after 6 months (26.6 ± 7.2 mmol/day).
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. There was a close relation between length of lactation and duration of amenorrhea for breast-feeding women (correlation coefficient 0.70, P < .001); however, although there was some concordance, the distribution of women in each group was not identical. For those who breast-fed for less than 6 months, menstruation generally resumed close to or slightly after lactation had stopped. For women who lactated longer, menstruation generally returned before the end of lactation, often many months earlier. The period of amenorrhea was less than 3 months for all formula-feeding women. There were no significant differences at baseline between breast-feeding groups in terms of age, height, weight, calcium intake, or bone mineral density.
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gives the mean (± standard error of the mean) percentage changes from baseline in bone area–adjusted bone mineral for the whole body, spine, and two forearm regions for breast-feeding women grouped by duration of lactation and amenorrhea. The corresponding data for the three hip sites are shown in Figure 2. The data for formula-feeding women and controls are given in Figures 3 and 4. Lactation was associated with significant changes in bone mineral over time at all sites except the radial shaft, generally causing a decrease followed by an increase. The pattern over time for all breast-feeding women together was best described at each site in terms of a quadratic equation, with a positive, squared term plus a negative, linear term. However, there were marked differences in the magnitude and duration of response to lactation among different regions of the skeleton and different women, depending on the duration of lactation (Figures 1 and 2). There were significant differences between lactation groups in the pattern of change over time at all skeletal sites (P < .001). Duration of lactation was a significant predictor of bone mineral content in the longitudinal quadratic models and interacted with change across time such that, in general, the longer the lactation, the more accentuated the pattern. We found similar effects in women grouped by duration of amenorrhea, and the influence of duration of amenorrhea in longitudinal models was indistinguishable from that of length of lactation.
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). At the femoral neck, bone mineral decreased in the first months postpartum and increased in later months toward baseline only for women who breast-fed for more than 6 months. At the greater trochanter, a decrease in bone mineral was evident only for women who breast-fed for more than 9 months. When lactation declined, bone mineral increased rapidly, resulting in bone mineral values above baseline. At the total hip, responses were intermediate between those at the femoral neck and greater trochanter. No decrease in bone mineral was observed in formula-feeding women or controls at any skeletal site at any time (Figures 3 and 4). Results were similar when analyses were restricted to controls who had never been pregnant. In the formula-feeding group, there was a steady increase in bone mineral above baseline at the whole body (Figure 3) and greater trochanter (Figure 4). These linear trends were significant (P < .01).
Table 3 shows the changes in bone mineral, adjusted for bone area, from baseline to final measurement at each skeletal site for all breast-feeding women combined and for formula-feeding women. At the final measurement, bone mineral values of breast-feeding women at the whole body, spine, and trochanter were significantly above initial baseline values, whereas those at the femoral neck and radial wrist were significantly below. There were significant increases of similar magnitude for formula-feeding women at the whole body and trochanter (Table 3). Analysis of covariance showed significant differences in the change in bone mineral over time between breast-feeding women and controls at the whole body (P < .05), spine (P < .05), femoral neck (P < .05), and trochanter (P < .01). There were no significant differences between breast-feeding women and formula-feeding women at any skeletal site.
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Discussion |
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There was no evidence that the duration of lactation had a major effect on bone mineral by the time breast-feeding had stopped for at least 3 months. The increases at the spine and trochanter and the decreases at the femoral neck and radial wrist were independent of the duration of lactation, and there was no difference between women who had breast-fed for less than 3 months and those who had breast-fed for many months. At the whole body and total hip, there was an indication of a differential between women depending on the duration of lactation, suggesting that bone mineral might still have been increasing at these sites at 3–6 months after lactation.
By the final measurements, women who chose to formula-feed their infants had increases in bone mineral at the whole body and greater trochanter similar to those who had lactated, and there were no statistically significant differences in the changes in bone mineral between baseline and final measurements in these two groups at any skeletal site. Although these results need verification, especially at the femoral neck, using larger numbers of formula-feeding women, it is possible that any long-term effect of childbearing on bone mineral might relate more to having been pregnant than to the mode of infant feeding, despite considerable skeletal changes that accompany lactation. An alternative is that bone mineral values measured shortly after delivery show temporary effects of pregnancy on the skeleton, and changes in bone mineral from baseline to final measurement show a return to prepregnancy values. Information about bone mineral changes during pregnancy is limited and inconsistent. Several studies reported decreases at the spine16 with minimal changes at the hip.16,17 Bone mineral has been shown to increase at the spine, femoral neck, and whole body during pregnancy if a woman conceives during lactation, when the decrease in bone mineral is still evident.18
A striking finding was the apparent redistribution of bone mineral in the hip associated with lactation, so that by the final measurements, bone mineral decreased in the femoral neck and increased at the greater trochanter (Figure 2). Bone mineral at the total hip, a composite of the femoral neck, greater trochanter, and intertrochanteric regions, was similar to baseline. During pregnancy, the weight increase of the mother causes static adjustment of the pelvis, and the femoral neck assumes a different position that slowly returns to normal after delivery. There might be postpartum changes in the precision and comparability of hip measurements, or there might be redistribution of bone mineral in the hip region. The International Committee for Standards in Bone Measurements (
Hanson J. Standardization of proximal femur BMD measurements [letter]. International Committee for Standardization in Bone Measurements. Osteoporos Int 1997;7:500–1[Medline]) stated that the total hip region should be used as the region of interest for all femur evaluations because it has equal diagnostic value to the femoral neck region and can be measured with greater precision. Our study shows that reliance on total-hip measurements could mask changes in the hip in certain situations, such as during lactation.
Although there were subtle differences, grouping breast-feeding women by duration of lactation or amenorrhea gave similar results, and the two effects could not be distinguished. The skeletal response to lactation varied widely among individuals, but there was no evidence that these differences were related to dietary calcium in the decrease by 3 months of lactation,12 the subsequent increase, or the overall change between delivery and the postlactation period. These findings support recent evidence that the skeletal response to lactation might be independent of current calcium intake.7,19 Further research is required to determine whether pregnancy and lactation are associated with long-term effects on bone mineral status, particularly at the femoral neck, and to determine why women differ in their skeletal response to lactation.
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Footnotes |
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Received October 1, 1998. Received in revised form March 30, 1999. Accepted April 8, 1999.
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References |
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2. Lissner L, Bengtsson C, Hansson T. Bone mineral content in relation to lactation history in pre- and postmenopausal women. Calcif Tissue Int 1991;48:319–25.[Medline]
3. Sinigaglia L, Varenna M, Binelli L, Gallazzi M, Calori G, Ranza R. Effect of lactation on postmenopausal bone mineral density of the lumbar spine. J Reprod Med 1996;41:439–43.[Medline]
4. Kritz-Silverstein D, Barrett-Connor E, Hollenbach KA. Pregnancy and lactation as determinants of bone mineral density in postmenopausal women. Am J Epidemiol 1992;136:1052–9.
5. Sowers M, Corton G, Shapiro B, Jannausch ML, Crutchfield M, Smith ML, et al. Changes in bone density with lactation. JAMA 1993;269:3130–5.[Abstract]
6. Lopez JM, Gonzalez G, Reyes V, Campino C, Diaz S. Bone turnover and density in healthy women during breastfeeding and after weaning. Osteoporos Int 1996;6:153–9.[Medline]
7. 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.
8. Affinito P, Tommaselli GA, Carlo CD, 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;81:2314–8.[Abstract]
9. Kolthoff N, Eiken P, Kristensen B, Nielsen SP. Bone mineral changes during pregnancy and lactation: A longitudinal cohort study. Clin Sci (Colch) 1998;94:405–12.[Medline]
10. Krebs NF, Reidinger CJ, Robertson AD, Brenner M. Bone mineral density changes during lactation: Maternal, dietary, and biochemical correlates. Am J Clin Nutr 1997;65:1738–46.
11. Caird LE, Reid-Thomas V, Hannan WJ, Gow S, Glasier AF. Oral progestogen-only contraception may protect against loss of bone mass in breast-feeding women. Clin Endocrinol (Oxf) 1994;41:739–45.[Medline]
12. Laskey MA, Prentice A, Hanratty LA, Jarjou MA, Dibba B, Beavan SR, et al. Bone changes after 3 months of lactation: Influence of calcium intake, breast-milk output and vitamin-D receptor genotype. Am J Clin Nutr 1998;67:685–92.[Abstract]
13. Prentice A, Laskey MA, Shaw J, Cole TJ, Fraser DR. Bone mineral content of Gambian and British children aged 0–36 months. Bone Miner 1990;10:211–24.[Medline]
14. Prentice A, Parsons TJ, Cole TJ. 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;60:837–42.
15. Parsons TJ, Prentice A, Smith EA, Cole TJ, Compston JE. Bone mineral mass consolidation in young British adults. J Bone Miner Res 1996;11:264–74.[Medline]
16. Black AJ, Topping J, Durham B, Farquharson FG, Fraser WD. Assessment of biochemical markers of bone turnover in pregnant women. In: Ring EFL, Elvins DM, eds. Current research in osteoporosis and bone mineral measurement IV. London: British Institute of Radiology, 1996:21.
17. Sowers M, Crutchfield M, Jannausch MJ, Updike S, Corton G. A prospective evaluation of bone mineral change in pregnancy. Obstet Gynecol 1991;77:841–5.
18. Laskey MA, Prentice A. Effect of pregnancy on recovery of lactational bone loss. Lancet 1997;349:1518–9.[Medline]
19. Prentice A, Jarjou LMA, Cole TJ, Stirling DM, Dibba B, Fairweather-Tait S. 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 1995;62:58–67.
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