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Endocrine Unit (J.S.F., R.M.N.), Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts 02114; Department of Epidemiology (M.S.), University of Michigan, Ann Arbor, Michigan 48109; Channing Laboratory (M.-L.T.L.), Brigham & Women’s Hospital, Boston, Massachusetts 02115; Division of Research (B.E.), Kaiser Permanente Medical Care Program, Oakland, California 94611; Department of Epidemiology (J.A.C.), Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania 15213; and Division of Geriatrics (G.A.G.), University of California Los Angeles School of Medicine, Los Angeles, California 90095
Address all correspondence and requests for reprints to: Joel S. Finkelstein, M.D., Endocrine Unit, Bulfinch 327, Massachusetts General Hospital, 55 Fruit Street, Boston, Massachusetts 02114. E-mail: . jfinkelstein{at}partners.org
Abstract
Bone mineral density (BMD) and fracture rates vary among women of differing ethnicities. Little is known, however, about ethnic variation in bone turnover. We measured serum osteocalcin (OC) and urinary N-telopeptide of type I collagen (NTX) levels in 2313 pre- or early perimenopausal women who were Caucasian (n = 1140), African-American (n = 651), Chinese (n = 247), or Japanese (n = 275) and were participating in the Study of Women’s Health Across the Nation. Serum OC and urinary NTX levels were compared before and after adjustment for a series of lifestyle and anthropometric variables that can affect bone turnover. Unadjusted serum OC levels were highest in Caucasian women (P < 0.001 vs. all other groups), higher in African-American than Chinese women (P = 0.006), and similar in Chinese and Japanese women (P = 0.203) and African-American and Japanese women (P = 0.187). Unadjusted serum OC levels were 11–24% higher in Caucasians than in the other groups. Adjustment for covariates did not alter the ethnic pattern of serum OC levels. Unadjusted urinary NTX levels were statistically significantly higher in Caucasian and African-American women than in Chinese women (P < 0.001) for both comparisons). Unadjusted urinary NTX levels were higher in Caucasian than in Japanese women (P = 0.071) and higher in Japanese than in Chinese women (P = 0.055), but these differences were of borderline statistical significance. Unadjusted urinary NTX levels were 9–18% higher in African-Americans and Caucasians than in the other groups. Among Caucasians, there were significant geographic regional variations in both serum OC and urinary NTX levels, with higher levels in women from the Northeast and the Midwest than in women from California. These data demonstrate significant ethnic differences in bone turnover in pre- and early perimenopausal women. Although these differences in adult bone turnover may explain some of the known ethnic variation in BMD, ethnic patterns of adult bone turnover do not parallel patterns of BMD. Other factors, such as differences in bone accretion, are likely responsible for much of the ethnic variation in adult BMD.
BONE MINERAL DENSITY (BMD) and fracture incidence vary widely across racial and ethnic groups (1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11). We recently reported that unadjusted lumbar spine and femoral neck BMDs are highest in pre- and early perimenopausal African-American women, next highest in Caucasian women, and lowest in Chinese and Japanese women (12). When BMD is adjusted for ethnic differences in anthropometric and lifestyle factors that affect BMD, with careful adjustment for body weight, lumbar spine BMD is similar in African-American, Chinese, and Japanese women, all of whom have higher spine BMD than Caucasian women (12). At the femoral neck, adjustment for these same factors, most importantly body weight, reduces the BMD advantage of African-American women, compared with the other groups, and eliminates differences among Chinese, Japanese, and Caucasian women (12). Lifestyle and anthropometric factors account for some of the ethnic variation in BMD, though additional ethnic variation in BMD remains unexplained.
Biochemical markers of bone turnover are important tools for understanding the pathophysiologic basis of variations in BMD in many clinical and research settings (13). Measurements of proteins made by osteoblasts, such as osteocalcin (OC), are used frequently to assess osteoblast activity; whereas measurements of degradation fragments of type I collagen, such as type I collagen N-telopeptide (NTX), are used frequently to assess osteoclast activity. It is likely, if not axiomatic, that differences in bone formation and/or bone resorption rates during skeletal development and adult skeletal remodeling are responsible for the observed ethnic differences in BMD. Little is known, however, about ethnic variation in bone turnover and factors that may underlie such ethnic variation.
The Study of Women’s Health Across the Nation (SWAN) is a large, multiethnic, community-based study investigating a wide range of characteristics as women pass through the menopause (14). At the time of enrollment, all women were either pre- or early perimenopausal. In SWAN, biochemical markers of bone turnover have been measured in over 2000 women of either African-American, Caucasian, Chinese, or Japanese descent. Thus, the baseline data from the SWAN cohort provide a good opportunity to examine ethnic variation in bone turnover and factors that are related to those differences.
Materials and Methods
Study population
SWAN is a multisite, longitudinal cohort study being conducted in community-based groups of women. At baseline, 3,302 women who belonged to one of 5 ethnic/racial groups were recruited: Caucasian (n = 1550), African American (n = 935), Japanese (n = 281), Chinese (n = 250), and Hispanic (n = 286). Eligibility criteria for entry into the SWAN longitudinal cohort were: age 42–52 yr; intact uterus and at least 1 ovary; no current use of estrogens or other medications known to affect ovarian function; at least 1 menstrual period in the 3 months before screening; and self-identification as a member of 1 of the 5 eligible ethnic groups. Cohort recruitment and enrollment have been described in detail (14). In brief, participants were enrolled at 7 clinical sites in the following geographic areas: Boston, Massachusetts; Chicago, Illinois; Detroit area, Michigan; Los Angeles, California; Hudson County, New Jersey; Oakland, California; and Pittsburgh, Pennsylvania. Recruitment techniques were designed to generate a representative sample of women at each of the 7 sites. All 7 sites enrolled Caucasians, and each site also enrolled women belonging to 1 prespecified minority ethnic group. African-American women were enrolled in Boston, Chicago, Detroit area, and Pittsburgh; whereas Japanese, Chinese, and Hispanic women were enrolled in Los Angeles, Oakland, and Hudson County, respectively. The Chicago and Hudson County sites did not measure bone density or bone turnover markers, leaving a potential maximum of 2413 participants belonging to 4 ethnic groups for these analyses. Of these women, 19 did not have a baseline blood sample, and 22 women did not have a baseline urine sample, leaving 2394 and 2391 women with potentially usable blood and urine bone turnover measurements, respectively.
We excluded women who reported using tamoxifen (n = 4), warfarin (n = 8), anticonvulsants (n = 38), or oral glucocorticoids (n = 33) in the month before blood and urine collection because these drugs are known to affect bone turnover measurements. No women reported use of oral estrogens, oral or parenteral bisphosphonates, calcitonin, or raloxifene within the month before blood and urine collection or a fracture within the 12 months before blood or urine collection. In total, 2313 women had usable serum measurements, and 2312 had usable urine measurements (note: some women had more than 1 exclusion criterion).
Study protocol
We attempted to collect venous blood before 1000 h and a nonfirst voided urine sample before 0900 h, between d 2 and 5 of the menstrual cycle. Seventy-nine percent of the blood samples were collected between cycle d 2 and 5, and 86% were collected between cycle d 2 and 7. Ninety-five percent of the blood samples were collected before 1000 h, and 83% were collected between 0800 and 1000 h. Ninety-four percent of the urine samples were collected before 0900 h, and 99% were collected before 1000 h. Ninety-eight percent of serum aliquots were frozen within 3 h of collection, and 99% of urine aliquots were frozen within 10 h of collection. Samples were then stored at -20 C or -80 C, at the local sites, for 1–60 d, and then at -80 C until analysis at a centralized laboratory (Medical Research Laboratories, Highland Heights, KY).
Standardized interviewer-administered or self-administered questionnaires were used to assess the following parameters: age (years), cigarette smoking (number of pack-years), alcohol intake (g/d) (15), total calcium intake (mg/d) (15), physical activity (a summary score of home, recreational, and active living physical activity estimated by the modified Baecke instrument) (16, 17), age at menarche (years), number of prior pregnancies, menopausal status (premenopausal or early perimenopausal), thiazide diuretic use, inhaled glucocorticoid use, lithium use, history of chronic liver disease, history of hypercalcemia, history of anorexia nervosa, self-reported history of diabetes mellitus, and season when samples were collected. Women were classified as premenopausal if they reported monthly menstrual bleeding during each of the 3 months preceding study entry and were classified as perimenopausal if they experienced menstrual bleeding during at least 1 of the 3 months preceding study entry and had some change in the regularity of their menstrual cycle. Weight was measured, without shoes, in light indoor clothing, using a calibrated digital or balance beam scale. Height was measured using a calibrated stadiometer. The protocol was approved by the Institutional Review Board at each center, and all women provided written informed consent.
Assays
Serum OC, urine NTX, and urine creatinine (Cr) measurements were performed at the Medical Research Laboratories. Each assay included three quality control samples supplied either by the measuring laboratory or by the assay kit manufacturer. Serum OC was measured in duplicate using an immunoradiometric assay (ELSA-OSTEO; CIS-Bio International, Bagnols/Ceze, France) that measures both the 1–49 amino acid intact human OC molecule and the 25–37 amino acid fragment. The lower limit of detection of the assay is 0.4 ng/ml, and the intra- and interassay coefficients of variation are both less than 6%. The manufacturer’s mean values for women of age 41–50 and 51–60 yr are 15.7 and 24.4 ng/ml, respectively. Urinary NTX was measured in duplicate using a competitive inhibition enzyme immunoassay (Osteomark; Ostex International, Inc., Seattle, WA). NTX is expressed as nanomoles of bone collagen equivalents per liter per millimole Cr per liter (nM BCE/mM Cr). The lower limit of detection is 20 nM BCE, and the intra- and interassay coefficients of variation are less than 8% and less than 12%, respectively. The manufacturer’s mean value for premenopausal women is 35 nM BCE/mM Cr. Samples were reanalyzed whenever the coefficient of variation of the replicates exceeded 10% and whenever the study-coordinating center identified the initial results as outliers.
Serum FSH and TSH measurements were performed by the SWAN core laboratory (RSP Laboratories, University of Michigan) using an ACS-180 automated analyzer (Bayer Corp., Tarrytown, NY). Serum FSH concentrations were measured with a two-site chemiluminescent immunoassay that uses constant amounts of two monoclonal antibodies (provided by Bayer Corp.). Each antibody is directed to different regions on the ß-subunit. One antibody is a solid-phase anti-IgG covalently coupled to paramagnetic particles, and the other is labeled with dimethylacridinium ester. Inter- and intraassay coefficients of variation are 12% and 6%, respectively, and the lower limit of detection is 1.05 mIU/ml. Serum TSH concentrations were measured using a two-site sandwich chemiluminescent assay using a dimethylacridinium ester-labeled monoclonal mouse antibody and a polyclonal sheep antibody covalently coupled to paramagnetic particles. Inter- and intraassay coefficients of variation are 8.9% and 5.5%, respectively.
Data analysis
Spearman correlation coefficients of serum OC and urinary NTX and each potential covariate were computed separately. Quantitative variables with significant (P < 0.05) univariate associations with OC or NTX, and categorical variables whose mean OC or NTX values were significantly (P < 0.05) different from the values in women without the variable of interest, were included in the multivariable models. Using these criteria, variables selected for inclusion were height, weight, age at menarche, physical activity, number of prior pregnancies, season, diabetes, thiazide use, inhaled glucocorticoid use, alcohol intake, serum TSH levels, and serum FSH levels. In addition, cigarette smoking, daily calcium intake, menopausal status, and age were included in the multivariable models because prior studies have reported that they are related to bone turnover (18). Finally, SWAN site was included in the multivariable models.
Because values for serum OC and NTX were not normally distributed, the values were log transformed before analyses were performed. After log transformation, the distributions of serum OC and urinary NTX were nearly normal. Values for serum OC and urinary NTX were first compared among the four ethnic groups, by ANOVA, without adjustment for covariates. To determine whether observed ethnic differences in bone turnover were attributable to ethnic variation in other factors that may affect bone turnover, serum OC and urinary NTX levels were recompared, after adjustment for the covariates listed above, using multivariable regression analyses (PROC GLM procedure in SAS). The Tukey-Welsch adjustments (option REGWQ in the MEANS statement) were used for multiple comparisons among ethnic groups. Adjusted group means (least-square means) were calculated after adjusting for the above covariates. Finally, to determine whether there were geographic differences in bone turnover, similar analyses were performed on the Caucasian women at each of the five SWAN clinical sites. This analysis was restricted to Caucasian women because women of other ethnic groups were not studied at all five SWAN clinical sites. All data are expressed as the mean ± SD, unless otherwise specified. P values less than 0.05 are considered statistically significant.
Results
Clinical demographic characteristics
Table 1
shows baseline characteristics of the cohort as a whole and for each of the four ethnic groups. The mean age of the cohort was 46.3 ± 2.7 yr, and there were small differences in age among groups. Fifty-four percent of women were classified as premenopausal, and 46% were classified as early perimenopausal; Chinese and Japanese women were least likely to be perimenopausal. On average, African-American women were 10 kg heavier than Caucasian women and 27–29 kg heavier than Chinese and Japanese women, and African-American and Caucasian women were 6–7 cm taller than Chinese and Japanese women. Mean calcium intake was highest in Caucasian women. African-American women had the most prior pregnancies and were most likely to be current smokers. Chinese women had the latest age at menarche and were the least likely to smoke cigarettes or drink alcohol.
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Fig. 1 shows the mean serum OC levels of each of the four ethnic groups before and after adjustment for covariates. Before adjustment for covariates, serum OC levels were highest in Caucasian women (P < 0.001 vs. all other groups), higher in African-American than Chinese women (P = 0.006), and similar in Chinese and Japanese women (P = 0.203) and African-American and Japanese women (P = 0.187). Unadjusted serum OC levels were 11% higher in Caucasians than in African Americans and 21–24% higher in Caucasians than in Chinese and Japanese women.
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When the analysis was restricted to Caucasian women at each of the five sites, serum OC levels were significantly higher in Boston (P = 0.017) and Pittsburgh (P = 0.024) than in Oakland (Fig. 2).
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Fig. 3 shows the mean urinary NTX levels of each of the four ethnic groups before and after adjustment for covariates. Before adjustment for covariates, urinary NTX levels were significantly higher in Caucasian and African-American women than in Chinese women (P < 0.001 for both comparisons). Urinary NTX levels were higher in Japanese than in Chinese women (P = 0.055) and in Caucasian than in Japanese women (P = 0.071), though these differences were of borderline statistical significance. Unadjusted urinary NTX levels were 9–18% higher in African-Americans and Caucasians than in Japanese and Chinese women.
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When the analysis was restricted to Caucasian women at each of the five sites, urinary NTX levels were lower in Los Angeles and Oakland than in Pittsburgh (P = 0.007 and P = 0.010), Boston (P = 0.006 and P = 0.009), and Detroit (P = 0.057 and P = 0.073) (Fig. 2
).
Discussion
These data demonstrate that there are significant differences in biochemical markers of bone turnover among late pre- and early perimenopausal African-American, Caucasian, Chinese, and Japanese women. In unadjusted analyses, serum OC levels are highest in Caucasian women, next highest in African-American women, and lowest in Chinese and Japanese women. Unadjusted urinary NTX levels are highest in Caucasian and African-American women, next highest in Japanese women, and lowest in Chinese women, though only the comparisons of Caucasians and African-Americans with Chinese women were statistically significant. The patterns of ethnic differences in serum OC levels were not altered when the values were adjusted for a series of factors known to affect serum OC levels. Although adjustments for anthropometric and lifestyle factors altered some of the relationships between ethnic groups and urinary NTX, the adjusted multivariable model needs to be interpreted cautiously because the model explained very little of the total variability in urinary NTX.
Cross-sectional studies indicate that serum OC and urinary NTX levels are approximately 36% and 96% higher, respectively, in postmenopausal than in premenopausal women (19). Thus, the 21–24% difference that we observed in serum OC levels between Caucasians and Japanese and Chinese women is nearly as great as the difference in serum OC levels across the menopause transition. Although the maximal difference in urinary NTX levels between ethnic groups was only 18%, this difference is also notable, particularly in relationship to the differences in NTX that are observed across the menopause.
Few studies have compared bone turnover between people of different ethnic groups, and most comparisons are between Caucasians and African-Americans. In a small study of young men and women, histomorphometric indices of bone formation were lower in African-Americans than in Caucasians, though static measurements of cortical and trabecular bone architecture were similar (20). Two studies have reported that serum OC levels are higher in postmenopausal Caucasian women than in African-American women (4, 5). In premenopausal women, prior studies have reported both that serum OC levels are higher in Caucasians than in African-Americans (21) and that OC levels are similar in Caucasians and African-Americans (4, 22). Although the reasons for these discrepant results are not apparent, our study population was much larger than those reported previously, thereby enabling us to detect differences that might not have been detected in smaller studies.
Levels of several biochemical markers of bone resorption have been compared between African-American and Caucasian women. Urinary hydroxyproline and calcium excretion (4, 5) and urinary pyridinium cross-link excretion (21) are higher in Caucasian than in African-American women. Similar differences in urinary calcium, hydroxyproline, and pyridinium excretion have been reported between African-American and Caucasian children (23). In contrast, several studies have reported that urinary NTX excretion is similar in Caucasian and African-American women (22, 24, 25), just as we found in our cohort.
Ethnic variations in bone turnover could be attributable to intrinsic or extrinsic factors that regulate bone turnover. The positive association between height and serum OC may be because taller people have more bone. The positive association between serum FSH levels and both serum OC and urinary NTX likely reflects an increase in bone turnover during the earliest phase of the menopausal transition. In contrast, the negative association between weight and serum OC may seem counterintuitive, because many prior studies suggest that mechanical loading stimulates bone formation. The negative association between alcohol use and both serum OC and urinary NTX is consistent with prior data that suggest that ethanol reduces bone turnover (18, 26). The negative association between cigarette use and serum OC, but not with urinary NTX, is also consistent with prior data (18, 26). Season variation in urinary NTX, with lower levels during the summer, is consistent with prior data that demonstrate that bone turnover markers are higher in winter than in summer (26). In contrast, it is surprising that we failed to detect a significant association between calcium intake and either serum OC or urinary NTX, because previous studies have reported that high calcium intake reduces bone turnover (18). Although Chinese and Japanese women were more likely to be premenopausal than African-American or Caucasian women, menopausal status was not a significant determinant of serum OC or urinary NTX levels in the multivariable models. Finally, ethnic differences in biochemical markers of bone turnover could be attributable to differences in partitioning of OC between bone and blood, differences in the proportion of the collagen cross-links that are released as peptides or free cross-links, or differences in the metabolism or clearance of the markers.
Significant geographic differences in bone turnover have been reported in postmenopausal women (27). Levels of serum OC, serum bone-specific alkaline phosphatase, and urinary C-telopeptide of type I collagen are highest in Americans and Canadians and lowest in German and Spanish women (27). To assess possible regional variation in bone turnover independent from ethnicity in our cohort, we compared serum OC and urinary NTX levels among the Caucasian women recruited at each of the five sites. Serum OC and urinary NTX levels were higher in women from the Northeastern United States or the Midwest than in women from California. Although it is possible that serum OC and urinary NTX values are lower in California because of more sun exposure and higher vitamin D levels, the actual basis for these regional variations in bone turnover is unknown. Because all of the Chinese and Japanese women in our study were from California, it is possible that regional variations in urinary NTX levels are responsible, at least in part, for our finding that urinary NTX levels were no longer higher in African-American than in Chinese women or in Caucasian than in Japanese women in a multivariable model that included the study site.
There are both striking similarities and notable differences in ethnic patterns of bone turnover and BMD in these women. In these same subjects, BMD was consistently highest in African-American women and lowest in Caucasian women after adjustment for a similar group of anthropometric and lifestyle covariates (12). Adjusted lumbar spine BMD of Chinese and Japanese women was similar to that of African-Americans, whereas adjusted femoral neck BMD of Chinese and Japanese women was similar to that of Caucasians (12). If the higher bone turnover of Caucasian women were related to their lower BMD, one would expect BMD of African-American women to be similar to that of Caucasians and lower than that of Chinese and Japanese women, a pattern that was not observed.
Our study has limitations. First, we measured only one marker of osteoblast activity and one marker of bone resorption. Different markers of either osteoblast activity or bone resorption can give qualitatively different results (28, 29, 30). Although there is no consensus regarding the optimal biochemical markers of bone turnover, serum OC and urinary NTX are among the most widely used assays. Moreover, serum OC and urinary NTX are more responsive to changes in estrogen status than other commonly used markers such as bone-specific alkaline phosphatase and urinary free deoxypyridinoline (29, 30). Second, we measured bone turnover markers at a single point in time. Because of the large day-to-day variation in biochemical markers of bone turnover (31), multiple measurements allow a more accurate estimate of each woman’s mean values. Third, not all ethnic groups are represented. Nonetheless, this study is the most comprehensive assessment of ethnic variation in bone turnover to date. Finally, our analysis does not include all factors that may affect bone turnover, such as vitamin D, PTH, gonadal steroids, or IGF-1. We feel that this approach is reasonable, however, because our goal was to determine whether there are differences in bone turnover among pre- and early perimenopausal women of various racial and ethnic groups and to assess the extent to which lifestyle and anthropometric variables contribute to these differences.
In summary, there is significant ethnic variation in bone turnover in pre- and early perimenopausal women. Therefore, ethnicity should be considered when interpreting results of these tests. Locale and season should also be considered when establishing reference ranges for bone turnover markers. Ethnic patterns of adult bone turnover do not parallel ethnic patterns of BMD. Thus, other factors, such as differences in bone accretion, are likely responsible for much of the ethnic variation in BMD. While it is not known whether these ethnic differences in bone turnover persist or are accentuated across the menopause transition, further study of the relationships between turnover and postmenopausal bone loss are warranted.
Acknowledgments
We acknowledge Dr. Christopher Gallagher for his leadership in the development of the study, Dr. Gordon Fitzgerald and Ms. Beth Willis for helping with data management and data analysis, Dr. Sybil Crawford for her advice on data analysis, the project directors and research assistants at the participating centers for their dedicated work on the protocol, and all of the SWAN participants for the generous donation of their time. The manuscript was reviewed by the Publications and Presentations Committee of SWAN and has its endorsement.
Footnotes
SWAN was funded by the National Institute on Aging, the National Institute of Nursing Research and the Office of Research on Women’s Health of the National Institutes of Health. Supplemental funding from National Institute of Mental Health, the National Institute on Child Health and Human Development, the National Center on Complementary and Alternative Medicine, the Office of Minority Health, and the Office of AIDS Research is also gratefully acknowledged.
Clinical centers and grant support: University of Michigan (U01 NR04061, to M.S.); Massachusetts General Hospital (UO1 AG12531: to R.M.N., 1995–1999; to J.S.F., 1999 to present); University of California/Kaiser, Davis, CA (U01 AG12554; to Ellen Gold, P.I.); University of California, Los Angeles, CA (U01 AG12539, to G.A.G.); and the University of Pittsburgh (U01 AG12546; to Karen Matthews, P.I.). This work was also supported by Department of Defense Grant DAMD17-96-6118, NIH Grant K24-DK02759 (to J.S.F.), the Iris Cantor—UCLA Women’s Health Center, a UCLA Center of Excellence in Women’s Health Grant (to G.A.G., RFP 282-97-0025), and NIH Grant RR-1066 (to Massachusetts General Hospital).
Laboratory support: University of Michigan (U01 AG12495: to Rees Midgley, P.I., 1995–1999; to Daniel McConnell, P.I., 1999 to present) and Medical Research Laboratories (subcontract of U01 AG12553; to Evan Stein, Director). Coordinating center: New England Research Institutes, Watertown, MA (U01 AG12553; to Sonja McKinlay, P.I.). Project Officers: Sherry Sherman, Taylor Harden, Carole Hudgings, Marcia Ory. Steering Committee Chair: Jennifer L. Kelsey.
Abbreviations: BCE, Bone collagen equivalents; BMD, bone mineral density; Cr, creatinine; NTX, N-telopeptide of type I collagen; OC, osteocalcin; SWAN, Study of Women’s Health Across the Nation.
Received December 12, 2001.
Accepted February 7, 2002.
References
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