LITTLE, KATHLEEN D.; CLAPP, JAMES F. III
We have recently reviewed the interaction of regular exercise on bone mineralization and other health-related issues during various phases of a woman's reproductive life including puberty, the menstrual cycle, pregnancy, lactation, and the menopause (5). The magnitude of bone mineralization changes during lactation is striking, especially relative to the rather short-term duration of this period (i.e., 3-12 months), thus providing a short-term model for assessing the potential impact of various intervention strategies on bone density.
The profound detrimental effects of lactation on maternal bone mineral density are because of prolonged estrogen deficiency, compounded by the "calcium drain" of breastfeeding (200-400 mg excess calcium loss per day). Studies evaluating the effect of lactation on bone density have been numerous (7-9,12,14,24-26) and have consistently shown axial bone loss ranging in magnitude from 3 to 6%, with little or no change in appendicular or total body bone measures. Site-specific differences likely reflect the well documented higher metabolic activity of the trabecular bone of the axial skeleton. Several of these previous studies showed significant axial bone loss in excess of 3% in only 3 to 4 months (7,12,14,24), suggesting that bone remodeling is accelerated in response to the cumulative negative effects of estrogen deficiency and lactation calcium loss. Although it is encouraging that lactation-induced osteopenia seems to be reversible with cessation of lactation in healthy women (7,8,14,24,25), the prognosis for individuals with compromised skeletal integrity before lactation is unknown.
Contrary to lactation, exercise enhances skeletal mineralization due to mechanical forces exerted by gravity and muscle contraction. As reviewed previously (2,21,22), this effect has been well documented in animal studies, as well as in cross-sectional and prospective studies in humans. Unfortunately, the appropriate exercise prescription in terms of mode, frequency, intensity, and duration has not yet been elucidated. Because current theories of bone remodeling suggest that activities which impart high impact, site-specific skeletal stress should be most effective (2,10,21,22), the recent position stand on osteoporosis and exercise published by the American College of Sports Medicine recommends weight-bearing activities including those designed to increase muscle strength (2).
Although many women exercise regularly during lactation, the effect on bone density has only been previously addressed by Drinkwater and Chesnut (9) in a small sample of six women athletes. Of multiple skeletal sites measured over 6 months' lactation, the only significant change was a 3.1% decrease in femur neck density, which is similar to that previously reported in nonexercising lactating women (24). In contrast, however, to studies showing significant lumbar spine density loss in nonexercising lactating women (7,12,14,24), a 3.4% increase at this site was observed in this sample of women athletes. Although the latter change was not significant, the magnitude of the change would suggest that further research is warranted to determine if postpartum exercise can reduce lactation-induced bone loss at one or more axial sites.
A case-control study to evaluate the potential impact of regular, recreational exercise on lactation-induced bone density changes in women has not been previously conducted. In light of the pronounced magnitude and rate of lactation-induced bone loss, the potential effect of exercise may also be accelerated, suggesting that assessment over a relatively short duration may be warranted. This information may be relevant for exercise prescription during lactation as well as for the prevention of osteopenia.
Thus, the purpose was to compare lactation-induced bone changes in women who engaged in regular, self-selected, recreational exercise versus those who refrained from such during early postpartum. We hypothesized that lactation-induced bone loss would be significantly less in exercising women as compared to controls.
In this initial attempt to assess the impact of exercise on lactation-induced bone loss, we have used a case-control design to describe the skeletal response to self-selected, recreational exercise engaged in over a relatively short time period, as opposed to imposing a given exercise regime over a longer time period. Lactation-induced bone changes were compared in women who engaged in regular, self-selected, recreational exercise versus those who refrained from such during early postpartum. Early postpartum was defined as three months following parturition and was selected as the study duration because most of the women in our study population worked and planned to return to work about 3 months postpartum. Thus, all subjects planned to breastfeed for at least 3 months. Further, it was our opinion that the magnitude and rate of lactation-induced bone loss justified the evaluation of the potential effect of exercise over a relatively short time period. Accordingly, bone density and related variables of interest were measured within 2 wk of parturition (baseline) and repeated between 12 and 14 wk after parturition (3 months postpartum).
Subjects were recruited from a large, ongoing study on the interaction between exercise and pregnancy (6) to participate in a substudy of exercise and bone density during pregnancy and lactation. This paper will only address the lactation phase of the study.
Thirty women who read and signed an informed consent statement approved by the Institutional Review Board at MetroHealth Medical Center were initially enrolled before conception. Ten subjects were subsequently excluded due to one of the following: five had fertility problems, two moved out-of-state, one dropped out because of time constraints, one was prescribed estrogen during lactation for stress fractures, and one was unable to breastfeed for the 3-month duration of the study.
The remaining 20 subjects were healthy, nonsmoking Caucasians, aged 25 to 40 yr, who had generally active lifestyles and reported no complications during pregnancy or the early postpartum period. All subjects breastfed their infants for at least 3 months postpartum. Although a few subjects occasionally supplemented their infants with formula, in all cases the majority of the infant's calories came directly from the mother. None of the subjects were on oral contraceptives for the study duration.
Postpartum exercise volume was quantified in all subjects by use of Polar portable heart rate monitors and daily exercise logs. Subjects were then retrospectively categorized as exercisers or controls based on whether they had met the minimal criteria for regular exercise (i.e., ≥3 d·wk−1, ≥20 min·session−1, ≥50% maximal oxygen consumption) as described by the American College of Sports Medicine (1) over the 3-month postpartum period. Thus, the control group consisted of women who exercised occasionally, as well as those who exercised regularly before and/or during pregnancy, but refrained from or reduced their exercise volume below these minimal criteria during the postpartum period. Based on these criteria, 11 women were assigned to the exercise group and 9 women served as controls.
Subjects in the exercise group ranged from recreational exercisers to those who had competed in road races (i.e., 10 K, marathon) and triathalons before pregnancy. Accordingly, fitness level was variable with preconception maximal oxygen consumption (V˙O2max) ranging from 44 to 66 mL·min−1·kg−1 and percent fat at parturition ranging from 17 to 27%. In addition to quantification of exercise volume by use of Polar portable heart rate monitors and daily exercise logs, exercise intensity was also quantified by laboratory assessment of exercise V˙O2 at 3 months postpartum. Based on these measures, exercise volume during the early postpartum period ranged from 3-6 d·wk−1, 25-70 min·session−1, at 55-75% of preconception V˙O2max. Aerobic, weight-bearing exercise (i.e., walking, running, aerobics, step aerobics, stair machines) was the primary exercise mode for all subjects. However, many subjects engaged in other activities (i.e., biking, swimming, resistance training) as well. Postpartum exercise mode and volume were similar to that during pregnancy, although the range of values for frequency, intensity, and duration was wider during pregnancy owing to the longer duration and more variable physiological and biomechanical changes.
Aerobic capacity. V˙O2max was measured before conception using a constant speed, progressive grade, treadmill protocol to volitional exhaustion (4), with indirect calorimetry measures obtained using a Sensormedics 2900Z Metabolic Measurement Cart.
Body composition. Body composition measures included height, weight, and skinfold-assessed relative fat obtained within 2 wk postpartum and repeated at 3 months postpartum using standardized techniques (11). Relative fat was computed from five skinfold sites (i.e., triceps, subscapular, suprailiac, abdominal, and thigh) using equations derived by Jackson and Pollock (13).
Estradiol. At 3 months postpartum, a venous blood sample was drawn from the antecubital vein, and serum was analyzed in duplicate for 17β-estradiol by radioimmunoassay using a commercial kit (Diagnostic Products, Los Angeles, CA).
Dietary calcium intake. Average dietary calcium intake was determined from 3-d diet records obtained on one or more occasions during the early postpartum period. For those subjects who failed to complete three-day diet records, a 24-h dietary recall was obtained during a laboratory visit. We have obtained reasonable agreement between these diet assessment methods in our laboratory. Diet records were analyzed using Food Processor II software.
Lactation calcium loss. Average daily calcium loss from lactation was measured at 3 months postpartum during a 24-h admission of the subject to the General Clinical Research Center. Milk volume was determined by weighing the infant before and after each feeding on an infant research electronic balance to the nearest gram (3). Thus, total infant weight change in 24 h was equal to total daily lactation milk volume loss. To control for potential diurnal variation in breast milk calcium concentration, aliquots obtained at each feeding were pooled. Samples were then diluted (threefold) and analyzed using an Ektachem chemistry analyzer (Clinical Diagnostic Systems, Inc., Rochester, NY). Average daily calcium loss from lactation was then computed from 24-h breast milk volume and calcium concentration.
Bone density. Total body, lumbar spine (L2-4), and femur neck bone density were measured by dual-energy x-ray absorptiometry using either a Lunar DPX (Lunar Radiation Corp., Madison, WI) or a Hologic QDR 2000 (Hologic, Inc., Waltham, MA) bone densitometer. These instruments utilize an x-ray tube photon source to emit photons through the bone. An x-ray detector and photomultiplier tube are used for photon counting and bone mineral content, and density is calculated by integrated software.
In vivo precision in our laboratory was similar for the two machines with the average coefficient of variation and test/retest reliability documented at 0.5% and 0.99 for total body, 1.2% and 0.93 for lumbar spine, and 1.6% and 0.99 for femur neck, respectively.
The study was initiated offsite on a Lunar machine, but halfway through the project's duration a Hologic machine was acquired on site. For practical considerations and subject convenience, all subjects enrolled from that time on were tested on the Hologic machine. As the primary focus of this study was change in bone density over time, all serial measures for a given subject were obtained on the same machine. Subject breakdown for each machine was as follows: Lunar, 10 subjects (6 exercisers, 4 controls); Hologic, 10 subjects (5 exercisers, 5 controls).
Although bone density values differ between machines due to methodological differences, equations supplied by Hologic, Inc. (Waltham, MA) allow for conversion of data obtained on a Lunar machine to a Hologic equivalent. We (17) and others (27) have recently evaluated the use of these equations in women and men, respectively. To combine the data on all 20 subjects for statistical analysis, data for the 10 subjects tested on the Lunar machine were converted to the Hologic equivalent using the conversion equations supplied by Hologic, Inc.
Data analysis. Sample size estimation was based on previous studies (12,24) of early postpartum lactation-induced bone loss in which respective effect sizes of 1.5 and 2.4 were computed based on repeated measures obtained with good precision (r > 0.9). Based on these data, power calculations estimated a sample size of less than eight subjects per group at an alpha of 0.05 and a power of 0.80. Repeated measures ANOVA was used to test for significant group, time, and interaction effects. t-tests for independent samples were used to test for significant initial group differences. Product moment correlation was used to test for significant relationships between bone density measures and selected, relevant variables. All statistical analyses were conducted using the Statistical Analysis System (SAS Institute, Cary, NC) with 0.05 used as the level of significance for all tests.
Subject characteristics. Subject characteristics for the total sample (N = 20), control (N = 9), and exercise (N = 11) groups are shown in Table 1. The majority of these measures were obtained within 2 wk postpartum. Exceptions include V˙O2max, which was obtained preconception, and serum estradiol and lactation calcium loss, which were both obtained at 3 months postpartum.
The only significant initial group difference was preconception V˙O2max, which, as expected, was significantly higher in the exercisers compared with the controls. Although weight and percent fat were less in the exercisers than the controls, these differences were not significant owing to the wide range of values within each group. As expected, weight significantly decreased over the postpartum period by 2.1, 2.7, and 1.8 kg for the total sample, controls, and exercisers, respectively. However, in agreement with our previous findings (16), no significant group by time interaction was observed.
There were no significant group differences in mean serum estradiol with values at the low end of the early follicular phase range for nonpregnant, nonlactating women but higher than expected for lactating, estrogen-deficient women. This is likely because of two outliers (one in each group) who had high values of 155 and 177 pg·mL−1, even though both confirmed they were not taking oral contraceptives. Excluding these two subjects, the mean for the total sample was 32 pg·mL−1 (range = 13-63 pg·mL−1), which is more representative of the lactating, hypoestrogenic state.
Although there were no significant group differences, mean dietary calcium intake for the total sample was below the RDA (i.e., 1200 mg·d−1) for lactating women. However, as many of the women continued to take their prenatal vitamins (typical calcium content = 200-300 mg/supplement) during the postpartum period, total calcium intake was adequate for a majority of the subjects. Of those subjects whose total calcium intake was below the RDA, seven were in the exercise group and one in the control group, thus accounting for the nonsignificant group deficiency observed in the exercisers. Lactation calcium loss did not differ significantly between groups and was at the low end of the reported range (200-400 mg·d−1) for lactating women.
Bone density. Changes in total body, lumbar spine, and femur neck bone density for the total sample (N = 20), control (N = 9), and exercise (N = 11) groups are shown in Table 2. Changes in the control and exercise groups paralleled those of the total sample in both direction and magnitude, and no significant group by time interaction was observed. No significant relationships were observed between the various bone density measures and selected variables including weight, serum estradiol, dietary calcium intake, and lactation calcium loss. Further, none of the correlation coefficients exceeded 0.38. However, when the latter variables were evaluated relative to percent change in bone density, a significant relationship was found between lactation calcium loss and percent change at the femur neck site (r = −0.49, P < 0.05). Surprisingly, weight change did not significantly correlate with percent change in bone density at any site, with the highest correlation coefficient of −0.40 observed with total body bone density.
In this initial attempt to assess the impact of exercise on lactation-induced bone loss, we evaluated bone density changes in women who engaged in regular, self-selected, recreational exercise for the first 3 months postpartum. As such, the results will be discussed within the limitations of this design.
Contrary to our hypothesis, lactation-induced bone loss was not significantly reduced in the exercisers as compared with the controls. Similar to previous studies (7,8,12,14,24-26), total body bone density was unchanged, whereas significant loss was observed at the femur neck and lumbar spine for both exercisers and controls. As shown in Table 2, the magnitude of change for the exercisers and controls was almost identical for the total body (±0.4%) and femur neck (−2.7, −2.8%). Although the magnitude of lumbar spine bone loss was higher in the controls (−5.4%) than the exercisers (−4.1%), the group by time interaction effect failed to reach statistical significance (P = 0.26). We observed a similar and significant femur neck bone loss in our exercising women as that exhibited by the athletes evaluated by Drinkwater and Chesnut (9). However, in contrast to their results, our exercisers also showed significant lumbar spine bone loss.
There are several potential reasons to explain why the results of this study did not support our hypothesis. First, the study design was limited to a description of the skeletal response to self-selected, recreational exercise. Although some of the exercisers in this study engaged in resistance training in addition to weight-bearing, aerobic exercise, the latter was the primary mode for all subjects. Further, within this context, exercise was highly variable among subjects in terms of mode, intensity, frequency, and duration.
Although the appropriate exercise prescription for maintenance and improvement of skeletal integrity has not yet been elucidated, weight-bearing activity is considered essential (2). However, current theories of bone remodeling suggest that high impact, site-specific activities will more effectively load the skeleton (2,10,21,22). Subsequent to the initiation of this study, Frost's "mechanostat" theory was published (10), proposing the critical interaction of mechanical stress and estrogen in mediating the set point for bone remodeling. According to this model, mechanical stress will decrease, whereas estrogen deficiency will increase, the remodeling set point. Thus, a greater mechanical stress is required during estrogen deficiency to maintain or improve bone mass. In preliminary support of this theory, several cross-sectional studies in athletes with oligo- or amenorrhea who engage in activities such as rowing (23), figure skating (20), and gymnastics (19) have observed bone density values in these estrogen-deficient women that are significantly higher than eumenorrheic controls and amenorrheic athletes engaged in aerobic, weight-bearing exercise. Thus, the exercise mode engaged in by the subjects in this study may have imparted an insufficient skeletal stimulus, especially within the context of their hypoestrogenic state.
A second explanation for the failure to observe an exercise effect on lactation-induced bone loss may have been the study duration. We selected 3 months as the evaluation period to assure all subjects would breastfeed for the project's duration. Further, it was our opinion that the magnitude and rate of lactation-induced bone loss justified the evaluation of the potential effect of exercise over a relatively short time period. Although 3 months is extremely short relative to the normal bone remodeling cycle (i.e., 4-8 months), the magnitude of lactation-induced bone loss documented (7,12,14,24) within 3 to 4 months suggests that bone remodeling is accelerated in response to the cumulative negative effects of estrogen deficiency and lactation calcium loss. Our results support this as all 20 subjects exhibited bone loss at the lumbar spine (range = −2 to −9%), with 17 of these also showing loss at the femur neck (range = −0.4 to −6.2%). However, the potential protective effect of a much less potent skeletal stressor, such as exercise, regardless of the specific prescription, likely necessitates a longer intervention period encompassing one or more bone remodeling cycles.
Finally, it is possible that our results would have been the same even if an exercise regime consisting of high impact, site-specific stress had been employed over a longer time period. It may be that exercise, regardless of the specific prescription, cannot counterbalance the cumulative negative effects of estrogen deficiency and lactation calcium loss on bone density. As reviewed previously (21), bone loss in exercising, nonlactating, estrogen-deficient women, such as the amenorrheic athlete, has been well documented. Several cross-sectional studies have shown that athletes with oligoor amenorrhea who engage in high impact, site-specific activities such as rowing (23), figure skating (20), and gymnastics (19) exhibit significantly higher bone density than eumenorrheic controls and amenorrheic athletes engaged in aerobic, weight-bearing exercise. Although it would be premature to speculate as to the potential protective effect of such activity on lactation-induced bone loss where estrogen deficiency is further compounded by lactation calcium loss, this may provide a good model for further evaluating Frost's theory (10).
The synergistic role of estrogen in eliciting a skeletal response to exercise training has been demonstrated in two longitudinal studies in postmenopausal women. Notelovitz et al. (18) found that women on estrogen therapy exhibited a significant and marked (8.3%) increase in spine bone density after a year of resistance training, whereas nonestrogen-treated women enrolled in a similar resistance training program (unpublished results) showed a nonsignificant decrease. Although Kohrt et al. (15) found significant independent effects of weight-bearing exercise and estrogen therapy on bone density at several skeletal sites, the combined effect of these two interventions was the most pronounced.
The critical role of estrogen in bone maintenance is further supported by studies indicating that lactation-induced bone loss is reversible with cessation of lactation and resumption of normal estrogen status in healthy women (7,8,14,24,25). However, the prognosis for individuals with compromised skeletal integrity, such as the amenorrheic athlete, is unknown. We observed such a scenario in one of our subjects who was subsequently excluded from the data analysis. The subject was a 34-yr-old heavy exerciser who had been amenorrheic for a number of years. Her preconception bone density was 80% of that of a young adult female for both lumbar spine and femur neck sites. Her physician prescribed clomiphene citrate (dienestrol, a synthetic estrogen compound) to facilitate conception. Although her pregnancy was otherwise normal, she was diagnosed with pelvic stress fractures during late pregnancy. As a result, her physician subsequently prescribed low-dose estrogen therapy at 4 wk postpartum to prevent further bone loss during lactation. The subject chose to discontinue estrogen therapy at 8 wk postpartum because of a perceived reduction in breast milk production. Even 4 wk of estrogen therapy may have been beneficial, however, as her femur neck bone density at 3 months postpartum had increased 2.7%. Unfortunately, no therapeutic effect was observed at the lumbar spine, where bone density decreased 4.3%.
In conclusion, within the limitations of the research design, the results of this study suggest that regular, self-selected, recreational exercise has no impact on early postpartum lactation-induced bone loss. The effect of this type of exercise during prolonged lactation encompassing one or more bone remodeling cycles is unknown, as is the effect of high impact, site-specific exercise during short- or long-term lactation. Additional research is warranted in light of the implications for exercise prescription during lactation, as well as for the prevention of osteopenia. Further, in individuals with compromised skeletal integrity, such as the amenorrheic athlete, low dose estrogen therapy may be indicated during lactation to prevent additional, and possibly irreversible, bone loss.
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Key Words: CALCIUM; DUAL ENERGY X-RAY ABSORPTIOMETRY; ESTRADIOL; FEMUR NECK; LUMBAR SPINE
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