Original Article
Effects of Tamoxifen on Bone Mineral Density in Postmenopausal Women with Breast Cancer
N Engl J Med 1992; 326:852-856March 26, 1992
- Abstract
- Abstract
Background and Methods.
Tamoxifen, a synthetic antiestrogen, increases disease-free and overall survival when used as adjuvant therapy for primary breast cancer. Because it is given for long periods, it is important to know whether tamoxifen affects the skeleton, particularly since it is used extensively in postmenopausal women who are at risk for osteoporosis. Using photon absorptiometry, we studied the effects of tamoxifen on the bone mineral density of the lumbar spine and radius and on biochemical measures of bone metabolism in 140 postmenopausal women with axillary-node—negative breast cancer, in a two-year randomized, double-blind, placebo-controlled trial.
Results.
In the women given tamoxifen, the mean bone mineral density of the lumbar spine increased by 0.61 percent per year, whereas in those given placebo it decreased by 1.00 percent per year (P<0.001). Radial bone mineral density decreased to the same extent in both groups. In a subgroup randomly selected from each group, serum osteocalcin and alkaline phosphatase concentrations decreased significantly in women given tamoxifen (P<0.001 for each variable), whereas serum parathyroid hormone and 1,25-dihydroxyvitamin D concentrations did not change significantly in either group.
Conclusions.
In postmenopausal women, treatment with tamoxifen is associated with preservation of the bone mineral density of the lumbar spine. Whether this favorable effect on bone mineral density is accompanied by a decrease in the risk of fractures remains to be determined. (N Engl J Med 1992;326:852–6.)
Media in This Article
Figure 1
Change in Mean (±SE) Lumbar-Spine Bone Mineral Density (BMD) in Women with Breast Cancer Given Tamoxifen or Placebo for Two Years.Figure 2
Change in Mean (±SE) Radial Bone Mineral Density (BMD) in Women with Breast Cancer Given Tamoxifen or Placebo for Two Years.Article Activity
- Article
TAMOXIFEN is a synthetic antiestrogen that, since its introduction for the treatment of patients with breast cancer in the early 1970s, has come to have a major role in the management of all stages of the disease.1 More recently, tamoxifen has been proved to have a favorable effect on disease-free and overall survival when given as adjuvant therapy after primary treatment for invasive breast cancer.2 Although the optimal duration of therapy is not known, long courses — 5 to 10 years — are favored. 3 4 5 Tamoxifen is not a pure antiestrogen; it has some estrogen-agonist properties, such as the ability to decrease the serum concentrations of cholesterol and increase those of sex-hormone—binding globulin.6 Because many women treated with tamoxifen survive for long periods, it is important to know whether the drug has effects on other organ systems. In particular, does tamoxifen have antiestrogenic effects on the skeleton and thus accelerate the bone loss that occurs in postmenopausal women generally,7 or does it have estrogenic effects and thus minimize bone loss?
Studies in vitro and in animals have shown that the effects of tamoxifen on bone resemble those of estrogen. It reduces bone resorption and turnover, stimulates bone formation, and prevents bone loss after oophorectomy.8 9 10 11 12 13 14 15 Its effects in humans are less clear; data from longitudinal and cross-sectional studies of small groups of both premenopausal and postmenopausal women have shown no evidence of accelerated bone loss and some evidence of preservation of or increases in bone density.16 17 18 19 20 21 We report the results of a prospective trial specifically designed to address these uncertainties.
Methods
We conducted a two-year, randomized, double-blind trial of tamoxifen in 140 postmenopausal women with breast cancer, who received either 10 mg of the drug by mouth twice daily or placebo. The study was approved by the University of Wisconsin Committee for the Protection of Human Subjects, and all the women gave written informed consent. Both the drug and the placebo were provided by the ICI Pharma Division of ICI Americas (Wilmington, Del.). The women were stratified according to the time since menopause (<4 vs. ≥4 years) and the size of the primary tumor (<3 vs. ≥3 cm on pathological examination).
Subjects
The recruitment of patients, eligibility criteria, and details of the design of the study have been reported previously.6 In brief, through their personal physicians we recruited 140 postmenopausal women with a history of axillary-node—negative breast cancer during the previous 10 years. When the breast cancer was diagnosed, some of these women were premenopausal — i.e., they had menstruated within the previous 12 months. To be eligible for the study, the women had to be clinically free of breast cancer according to the history, physical examination, and laboratory and radiologic studies and could not be taking any hormonal or bone-preserving drugs. Their serum lipid concentrations had to be normal, and their values for the density of the radius (on single-photon absorptiometry) and the density of the lumbar spine (on dual-photon absorptiometry) had to be more than 80 percent of the values in age-matched normal women. The radius contains predominantly cortical bone, and the lumbar spine predominantly trabecular bone. Of 175 women evaluated for entry into the study, 7 were ineligible because their bone mineral density was low and 28 because they had hyperlipidemia or evidence of metastatic disease.
Seventy women were assigned to receive placebo, and 70 to receive tamoxifen. The study design included evaluations at base line and after 3, 6, 12, 18, and 24 months of treatment. Before the women received any medication during these visits, we interviewed them in detail about their medications, symptoms, and behavior affecting health and performed physical examinations. Twelve-hour fasting blood samples were obtained, and bone mineral density was measured. Previous reports from this study have described the lipid and hormonal changes,6 the effects of cardiovascular risk factors,22 and the symptoms that occurred23 in these women.
Laboratory Measurements
Serum samples were coded and stored at —70°C for a maximum of three years. Serum osteocalcin was measured at base line in all 140 women and at 12 and 24 months in the first 70 women who entered the study. Serum parathyroid hormone and 1,25-dihydroxyvitamin D were measured in these 70 women at base line, at 12 months, and at 24 months; serum alkaline phosphatase was measured in all 140 at base line and at 12 months. The actual numbers of measurements were lower because samples were unavailable. Serum 1,25-dihydroxyvitamin D and intact parathyroid hormone were measured with commercial kits (from Incstar, Stillwater, Minn., and the Nichols Institute, San Juan Capistrano, Calif, respectively).24 Serum osteocalcin was measured by radioimmunoassay, with use of bovine osteocalcin as the standard and anti—bovine osteocalcin antibody; the details of this method have been reported elsewhere.24
We believe that osteocalcin, parathyroid hormone, and 1,25-dihydroxyvitamin D remain stable in serum for up to two years when stored as described above. All samples for individual women were assayed at the same time, without repeated freezing and thawing of samples. For the assays of osteocalcin, parathyroid hormone, and 1,25-dihydroxyvitamin D, the interassay coefficients of variation were 10, 4, and 9 percent, respectively, and the intraassay coefficients of variation were 2, 9, and 3 percent, respectively. Serum follicle-stimulating hormone and tamoxifen were measured as previously reported.22 , 25
Bone Densitometry
The bone mineral density of the lumbar spine (at L2 to L4) was measured by dual-photon absorptiometry (DP-3 densitometer, Lunar Corp., Madison, Wis.).26 This measurement is an area density that is obtained by dividing the mass of bone (in grams) by the total area of bone (in square centimeters) within the region measured. The bone density of the radius was measured at a site two thirds of the distance from the proximal to the distal end of the radius (SP-2 densitometer, Lunar Corp.).
Values for lumbar bone mineral density may be affected by the age and batch of the gadolinium-153 source. During the course of this study three gadolinium-153 sources were used. There were no detectable differences among these sources according to measurements on phantoms, including a phantom measured in an 18-cm water bath, nor were there changes in the standard provided by the manufacturer. All data were analyzed with version 8C software (Lunar Corp.), which corrected for the small effect of source activity on the results of the bone-density measurements. The women were enrolled in the study at different times in relation to the age of the source, and the measurements were performed at intervals that varied with respect to the age and batch of the source. Any effects of the use of different sources would thus be unlikely to affect the results systematically.
A single highly trained operator who was unaware of the subjects' study-group assignments analyzed the bone scans. The precision of the measurements of bone mineral density at both sites, as reflected by the variance around a regression line for individual subjects, was 2 percent. The actual intervals between the base-line and follow-up measurements were as follows: the mean (±SD) interval between the base-line and 12-month measurements was 11.9±0.5 months (range, 11.0 to 13.9) in the placebo group and 12.0±0.5 months (10.9 to 14.0) in the tamoxifen group, and the interval between the 12-month and 24-month measurements was 12.1±1.5 months (11.0 to 13.0) in the placebo group and 12.0±0.6 months (11.0 to 14.4) in the tamoxifen group. For each interval, the differences between the means of the two groups were not significant (P = 0.44 and P = 0.68, respectively, by t-test).
Statistical Analysis
Changes in bone density were evaluated in two ways. Net changes from base line were computed for each follow-up interval. In addition, the rate of bone loss per year, expressed as a percentage of the base-line measurement, was calculated by linear regression analysis for each woman.27 The averages of these rates in the two study groups were calculated and then compared by a two-sample t-test. They were also compared according to a more elaborate approach using methods proposed by Laird and Ware28; this approach also fits a linear model to the data for each subject but takes into account the correlations between and within individual subjects. The Statistical Analysis System was used for all the analyses except the Laird—Ware model. The analyses of bone mineral density included all women for whom three or more data points were available. With that exception, all major analyses were performed according to the intention-to-treat principle, regardless of compliance. Secondary efficacy analyses included all patients who complied with the regimen and completed the study.
Values for biochemical variables in the two groups and subgroups were analyzed by two-sample t-tests.
Results
The two study groups were similar at base line (Table 1Table 1
Characteristics of the Study Groups at Base Line.*). Specifically, they did not differ significantly in mean body mass, history of oophorectomy, reported number of hours of exercise or work per week, or number of current smokers. The two groups were balanced in terms of the number of women who had been postmenopausal for less than four years at base line by means of the stratified randomization procedure (Table 1). The mean base-line values for lumbar-spine and radial bone mineral density were not significantly different in the two groups (spine, P = 0.55; radius, P = 0.53). A total of 22 women (16 percent) did not complete the study (11 in the placebo group and 11 in the tamoxifen group): 7 women dropped out because of disease recurrence (5 in the placebo group and 2 in the tamoxifen group), 9 stopped taking their assigned tablets because of side effects23 (4 in the placebo group and 5 in the tamoxifen group), and 6 dropped out for other reasons (2 in the placebo group and 4 in the tamoxifen group). Two other women treated with tamoxifen became depressed and had hot flashes; all other side effects or toxic reactions were less severe. Both vasomotor symptoms (hot flashes or facial flushing) and gynecologic symptoms (vaginal discharge or vaginal dryness) were more frequent among the tamoxifen-treated women, as reported previously in detail.23 The numbers of women evaluated at each of the five follow-up visits were 70, 68, 67, 64, and 62 in the placebo group and 66, 66, 65, 64, and 64 in the tamoxifen group, respectively (1 woman in the placebo group did not undergo measurement of bone mineral density at the final visit). There were no significant differences between the two groups in compliance with appointments. Compliance with medication consumption, assessed by pill counts and measurements of tamoxifen in serum, was excellent.21 Tamoxifen was not detectable in serum samples from any woman in the placebo group at any time in the study, whereas it was detectable in all the women in the tamoxifen group at all times. The two groups did not differ significantly in their use of diuretic agents.
Changes in Bone Mineral Density
During the two-year study period, the density of the radius decreased 0.88 percent per year in the women given tamoxifen (P<0.001 for the comparison with the base-line value), but the density of the lumbar spine increased 0.61 percent per year (P = 0.04) (Table 2Table 2
Changes in Bone Mineral Density and Serum Biochemical Variables in the Study Groups during Two Years.* and Fig. 1Figure 1Change in Mean (±SE) Lumbar-Spine Bone Mineral Density (BMD) in Women with Breast Cancer Given Tamoxifen or Placebo for Two Years. and 2Figure 2Change in Mean (±SE) Radial Bone Mineral Density (BMD) in Women with Breast Cancer Given Tamoxifen or Placebo for Two Years.). Bone density at both sites decreased significantly in the women given placebo (radius: —1.29 percent per year, P<0.001 for the comparison with the base-line value; spine: —1.00 percent per year, P<0.001). The change in lumbar-spine bone density in the two groups was significantly different (P<0.001 by intention-to-treat analysis), whereas the change in radial bone density in the groups was similar (Table 2 and Fig. 2). The results were similar when the data were evaluated with the LairdWare model28 or with analysis of covariance that included as covariates smoking status, base-line bone mineral density, hours of exercise per week, menopausal status at diagnosis, and time since menopause. When the changes in bone mineral density were analyzed separately, according to menopausal status at the time of diagnosis of breast cancer, the lumbar-spine bone density was found to have increased 1.00 percent per year (P = 0.001) in the women given tamoxifen who were postmenopausal at diagnosis. In contrast, among the small number of women given tamoxifen who were premenopausal at the time of diagnosis, the lumbar bone density decreased at a rate of 1.12 percent per year (P = 0.18).The results reported above were derived from analyses that included only women with three or more measurements of bone mineral density. Although potentially biased because of differences in the reasons for noncompliance, the results of analyses that included women with complete measurements for the two-year study period were similar. In the women who received tamoxifen for the two years of the study, bone mineral density at the lumbar spine increased by 0.72 percent per year (P = 0.01); in contrast, in the women who received placebo for two years, lumbar bone density decreased by 0.76 percent per year (P = 0.01). The difference between the two groups in the rate of change was significant (P<0.001). Among all the women completing two years of study, radial bone mineral density decreased by 0.72 percent per year in those given tamoxifen (P = 0.001) and by 1.29 percent per year in those given placebo (P<0.001).
The results were similar when the analyses were performed without the data on the five women who were considered to be premenopausal on the basis of their base-line serum concentrations of follicle-stimulating hormone (≤30 IU per liter).
Biochemical Measures of Bone Turnover
The mean serum osteocalcin concentration decreased by more than 50 percent in the 35 women in the tamoxifen group who underwent measurements at base line and at 24 months, but it did not change in the women given placebo (Table 2). The differences between the two groups in the changes observed at 12 and 24 months were significant (P<0.001) (Fig. 3Figure 3
Mean (±SE) Serum Osteocalcin Concentrations in Women with Breast Cancer Given Tamoxifen or Placebo for Two Years.). The mean serum parathyroid hormone and 1,25-dihydroxyvitamin D concentrations were similar and did not change significantly during the study (Table 2).Serum alkaline phosphatase concentrations, measured in all women, had fallen by 21 percent in the tamoxifen group after 12 months (P<0.001 for the comparison with the base-line concentration and for the comparison with the concentration in the placebo group).
To assess changes in bone density and bone turnover, the women were grouped according to whether they had high or low bone turnover on the basis of their initial serum osteocalcin concentration (<2069 vs. ≥2069 pmol per liter [i.e., >1 SD above the mean in premenopausal women]), and the rates of change were examined within these two groups. In both groups, tamoxifen had appreciable protective effects on lumbar-spine bone density, but in neither group did it affect radial bone density.
The changes in bone mineral density in the women who had repeated serum osteocalcin measurements (at 12 and 24 months) were similar to those in all the women in the study.
Discussion
We found strong evidence that tamoxifen tends to preserve bone mineral density in the lumbar spine. There were no obvious differences in confounding variables that might negate this conclusion, and the excellent compliance evident in the consumption of assigned medication and the low dropout rates suggest that bias is an unlikely explanation for this finding.
The women who were studied had base-line values for spinal and radial bone mineral density that were only slightly lower than those of age-matched normal women.29 Younger populations of women with breast cancer have lower bone mineral density than normal women,30 and women who are less than 50 years of age at diagnosis have a higher risk of hip fracture than women who are more than 50 years old at diagnosis.31
Studies in animals suggest that tamoxifen is an anti-resorptive agent, like estrogen, and preserves trabecular bone and, perhaps to a lesser extent, cortical bone.8 9 10 11 12 13 14 15 The results reported here are consistent with the findings of those studies and previous studies in humans.16 17 18 19 20 21 We found that the women given tamoxifen had a significant loss of bone density in the radius, a site composed mainly of cortical bone. The decline in bone mass associated with the cessation of ovarian estrogen production involves mainly the more metabolically active trabecular bone found in the spine and to a lesser degree in the hips. In humans, the agents used to treat osteoporosis have greater effects on spinal bone mineral density than on radial bone mineral density.32 33 34 Unfortunately, we did not measure bone density in the femur. The 3 percent difference in lumbar-spine bone mineral density between the tamoxifen and placebo groups at the end of two years is identical to the difference induced in women given etidronate for osteoporosis34 but is lower than the difference of 5 to 10 percent induced during the same period in women given calcitonin or estrogen for that disorder.32 , 33 Estrogen also has a stabilizing effect on radial bone, an effect not found in our short-term study. If further data can be collected on the effects of tamoxifen on the radius and femur, this agent could be considered an alternative treatment for stabilizing bone mass, particularly in women in whom estrogens or bisphosphonates are contraindicated. The mechanisms of action of estrogen and tamoxifen in preserving trabecular bone are not well understood. In this study, the reduction in serum concentrations of osteocalcin and alkaline phosphatase associated with tamoxifen administration presumably reflects decreased bone turnover or bone remodeling.
The estrogen-agonist effect of tamoxifen on bone demonstrated in this study adds to the growing list of other estrogen-like effects of this antiestrogen. Estrogen-like increases in serum levels of sex-hormone—binding globulin and changes in lipid concentrations6 also occur during tamoxifen treatment. Whether the effects of long-term tamoxifen treatment in preserving bone mineral density and changing lipid levels will lead to a reduction in fracture rates and in mortality and morbidity due to cardiovascular disease is not yet known. Preliminary data suggest that the cardiovascular effects may indeed be favorable.35 For the many postmenopausal women with breast cancer for whom tamoxifen is prescribed (and estrogen proscribed), the results reported here are reassuring.
Supported by grants (PDT302A and PDT302B) from the American Cancer Society, by grants from the ICI Pharma Division of ICI Americas, and by a Public Health Service grant (CA-50243) from the National Cancer Institute.
Presented in part at the Breast Cancer Symposium, Nottingham, United Kingdom, September 26–28, 1990 (Br J Cancer 1990;62:Suppl 12:3. abstract 2), and the 15th San Antonio Breast Cancer Symposium, San Antonio, Tex., November 2 and 3, 1990 (Breast Cancer Res Treat 1990;76:145. abstract 3).
Source Information
From the Departments of Human Oncology (R.R.L., P.A.N., V.C.J., P.P.C., D.L.D.) and Medical Physics (R.B.M., H.S.B.), University of Wisconsin-Madison, and the Department of Medicine, Albert Einstein Medical Center, Philadelphia (S.E.). Address reprint requests to Dr. Love at 7C Medical Sciences Ctr., 1300 University Ave., Madison, WI 53706.
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