Journal of Clinical Endocrinology & Metabolism
, doi:10.1210/jc.2006-2695
The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 9 3453-3457
Copyright © 2007 by The Endocrine Society
Racial and Ethnic Differences in Bone Turnover Markers in Men
Benjamin Z. Leder,
Andre B. Araujo,
Thomas G. Travison and
John B. McKinlay
Endocrine Unit (B.Z.L.), Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts 02114; and New England Research Institutes (A.B.A., T.G.T., J.B.M.), Watertown, Massachusetts 02472
Address all correspondence and requests for reprints to: Benjamin Z. Leder, M.D., Endocrine Unit, Massachusetts General Hospital, Thier 1047, 50 Blossom Street, Boston, Massachusetts 02114. E-mail: bzleder{at}partners.org.
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Abstract
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Context: Whereas racial and ethnic differences in fracture risk and bone mineral density (BMD) in men have been well described, the influence of race and ethnicity on biochemical markers of bone turnover is less clear.
Methods: To examine the relationship between bone turnover, BMD, and race and ethnicity in men, we measured BMD, serum intact osteocalcin (OC), and serum C-terminal telopeptides of type 1 collagen (CTx) in 1029 men (aged 30–79 yr) enrolled in the Boston Area Community Health/Bone Survey, a population-based random sample of Black, Hispanic, and White. Men with diseases or on medications known to affect bone metabolism were excluded from the analysis. Mean serum levels of OC and CTx were adjusted for age, month and time of blood sample, and 25-hydroxyvitamin D.
Results: Compared with Black men, adjusted mean OC levels were 17.6 and 20.5% higher in Hispanic (P = 0.02) and White men (P < 0.01), respectively. There was no significant difference between White and Hispanic men. Adjusted mean CTx levels were 14.3% higher in White men, compared with Black men (P = 0.04), but no other differences were significant. OC declined by 0.4%/yr from age 30 to 65 yr and increased thereafter by 2.1%/yr. The age trend in CTx appeared to follow a pattern consistent with a quadratic function of age. Model-estimated annual percent changes within age decade were as follows: 30–39 yr, –2.5%; 40–49 yr, –1.4%; 50–59 yr, –0.3%; 60–69 yr, +0.9%; 70–79 yr, +1.7%. There was no variation in the shape of the age trend in OC or CTx by race or ethnic group. Correlations between bone turnover markers and BMD (adjusted for age, height, weight, serum 25-hydroxyvitamin D, and PTH and month and time of blood sample) were generally weak.
Conclusions: Bone turnover markers are lower in Black men, compared with White and Hispanic men. Age trends in bone turnover markers are not influenced by race or ethnicity. Future studies in this cohort and others are needed to explore further these reported differences in bone metabolism among Black, Hispanic, and White men.
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Introduction
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OSTEOPOROSIS IN MEN is increasingly recognized as a major public health issue, contributing significantly to morbidity and mortality in our aging population (1, 2). Numerous risk factors for osteoporotic fracture have been identified in men, many of which are common to those identified in women (3, 4, 5). Among these, race and ethnicity are known to be associated with fracture, with higher rates in White men and lower rates among Black, Hispanic, and Asian men (6, 7, 8, 9, 10, 11, 12, 13, 14). Bone mineral density (BMD), which is closely associated with hip, vertebral, and overall fracture rates in men (15), also differs by race and ethnicity (16, 17, 18, 19, 20, 21, 22, 23, 24). Yet while BMD is known to be a powerful predictor of fracture risk in men, differences in BMD alone cannot account for the diverse rates of fractures in varied populations (25, 26).
Recently, biochemical markers of bone turnover have become increasingly useful in assessing changes in the metabolic activity of the skeleton, measuring response to osteoporosis therapy, and helping to explain the mechanisms of action of various hormonal and therapeutic mediators of skeletal integrity (27). Furthermore, high bone turnover appears to be an independent risk factor for fracture in men (28). The relationship between race and ethnicity and bone turnover in men, however, has not been comprehensively examined. In the present study, we sought to characterize the influence of race and ethnicity on biochemical markers of bone turnover as well as the effect of race and ethnicity on age-related changes in bone turnover. To achieve this goal, we measured BMD, serum intact osteocalcin (OC), and serum C-terminal telopeptides of type 1 collagen (CTx) in a diverse population of men enrolled in the Boston Area Community Health/Bone (BACH/Bone) Survey.
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Subjects and Methods
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Study sample
BACH/Bone is a cross-sectional observational study of 1219 (of 1877 eligible, 65% response rate) randomly selected Black, Hispanic, and White male residents of Boston, Massachusetts, aged 30–79 yr (16). Persons of other racial or ethnic backgrounds were not enrolled. The BACH/Bone study was powered according to its primary aim of detecting race and ethnic differences in BMD. A priori power calculations indicated that a sample size of 300 subjects per race and ethnic subsample would yield greater than 80% power to detect a difference of 0.039 g/cm2 in mean BMD between any two racial and ethnic subpopulations. Enrollment for the study exceeded this minimum goal (367 Black, 401 Hispanic, 451 White subjects enrolled). This protocol was approved by institutional review boards at New England Research Institutes and Boston University School of Medicine (BUSM). All participants gave written informed consent.
Data collection
Data collection was performed by trained staff in a research clinic at BUSM. Race and ethnicity were determined according to the federal standard (29), with respondents self-identifying themselves as Black, Hispanic, or White via two questions on Hispanic ethnicity and racial status.
Bone turnover marker measurements
Serum measurements were performed at The Core Laboratory, BUSM. Blood samples were nonfasting, and collection times ranged from 0745 to 2000 h. Serum intact OC, a marker of bone formation, was measured in duplicate with the Nichols Advantage System (Nichols Institute Diagnostics, San Clemente, CA). Serum CTx, a marker of bone resorption, was measured with Serum CrossLaps ELISA (Nordic Bioscience Diagnostics, Herlev, Denmark). Intraassay coefficients of variation for OC and CTx are 5.3 and 5.0%, respectively. Interassay coefficients of variation for OC and CTx are less than 10 and 8.1%, respectively. Serum 25-hydroxyvitamin D [25(OH)D] was measured by a competitive binding protein assay (30) and serum biointact PTH with the Nichols Advantage System (Nichols Institute Diagnostics).
BMD measurements
BMD (grams per square centimeter) at the hip, anteroposterior lumbar spine (L1-L4), and forearm was measured by dual-energy x-ray absorptiometry using a QDR 4500 W densitometer (Hologic, Inc., Waltham, MA) located at the BUSM. The scanner was calibrated daily with an anthropometric (vertebral) phantom.
Statistical analysis
Visual displays showed substantial skew in OC and CTx. We transformed OC (square root) and CTx (log) to enhance their compliance with the assumptions of regression models (e.g. to enhance linearity and equality of variance in outcomes over the age range and to reduce skew). We judged the adequacy of the transformations by visual inspection. Transformed values were used in all analyses, with values back-transformed to their original units for presentation. We examined race and ethnic differences in descriptive characteristics by means of ANOVA, with Wald tests used for hypothesis testing. Based on previous work (31), it was anticipated that turnover markers may have nonlinear trends in age. Visual displays (with locally weighted linear regression) (32) and exploratory analyses supported this. We relied on Wald tests to judge the significance of terms in making modeling decisions. We also tested for race and ethnic differences in the shape of age trends in OC and CTx. These statistical models contained an age spline (OC) or age2 (CTx) term, and comparisons were made by assessing interaction through the use of race/ethnicity (represented by two indicator variables) and their product with both the age and age spline (OC) or age2 (CTx) terms. The significance of these effects was assessed via an F-statistic on four degrees of freedom. Percentage age changes, within appropriate age segments, in OC and CTx were obtained by dividing the model-estimated per-year change in (square root) OC and (log) CTx by the adjusted mean (square root) OC and (log) CTx for a typical 50-yr-old subject. Partial correlation coefficients (rp) were used to estimate the association between bone turnover markers and BMD adjusting for covariates [age, height, weight, serum 25(OH)D, and PTH and month and time of blood sample].
Analysis sample
Of the 1219 men, 1138 had serum available for analysis. The following exclusions were made: missing OC or CTx (n = 4); missing BMD (n = 10); exclusionary medication use (current), which included all anticoagulants, testosterone, glucocorticoids, selected anticonvulsants (phenytoin, carbamazepine, and Depakote, Phenobarbital), suppressive doses of T4 in men with thyroid cancer, and lithium (n = 65); self-reported osteoporosis (n = 11); serum calcium greater than 10.1 mg/dl and serum PTH greater than 50 pg/ml (n = 5); and outlying data values (>4 SD from mean) (n = 14). This left 1029 men for analysis, none of whom reported a fracture in the past 6 months (also an exclusion).
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Results
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Of the 1029 men in the analysis sample, 307 (29.8%) were Black, 332 (32.3%) were Hispanic, and 390 (37.9%) were White. There were race and ethnic group differences on all variables considered with the exception of BMI and PTH (Table 1
). Race and ethnic group-specific medians and 2.5 and 97.5 percentiles for OC and CTx are displayed in Table 1
. Median OC was clearly higher in White as compared with Black and Hispanic subjects, and the upper limit of normal, defined as the 97.5 percentile, was higher in Hispanic and White subjects, compared with Black subjects. There were no appreciable differences in CTx medians or percentiles among the groups.
Mean serum OC and CTx adjusted for age, month and time of blood sample, and 25(OH)D level is shown in Fig. 1
, A and B, respectively. Compared with Black men, adjusted mean OC was 17.6 and 20.5% higher in Hispanic (P = 0.02) and White men (P < 0.01), respectively. There was no significant difference between White and Hispanic men. Adjusted mean CTx was 14.3% higher in White compared with Black men (P = 0.04), and whereas mean CTx was 11.1% higher in White compared with Hispanic men (P = 0.08). Note that adjustment for 25(OH)D level was made due to the large differences in vitamin D levels between racial and ethnic groups. When serum 25(OH)D levels are removed from the model, the Black/Hispanic and Black/White differences in OC are slightly reduced (16.2 and 18.5%, respectively), and the Black/White difference in CTx is no longer significant (P = 0.16). Figure 1
, C and D, shows age trends in OC and CTx. The age trend in OC appeared to follow a pattern that was consistent with a two-slope linear model with a single knot at age 65 yr. OC declined by approximately 0.4%/yr between the ages of 30 and 65 yr and increased by approximately 2.1%/yr after age 65 yr. The age trend in CTx appeared to follow a pattern consistent with a quadratic function of age. Model-estimated yearly percent changes within age decade were as follows: 30–39 yr, – 2.5%; 40–49 yr, – 1.4%; 50–59 yr, – 0.3%; 60–69 yr, +0.9%; and 70–79 yr, +1.7%. We found no evidence of variation in the shape of the age trend in OC (P = 0.29) or CTx (P = 0.76) by race and ethnic group.

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FIG. 1. A and B, Mean (95% confidence interval) OC (A) and CTx (B) by race and ethnic group, adjusted for age, serum 25(OH)D, and month and time of blood sample. Adjusted means were obtained from linear regression models using square root OC and log CTx as outcomes, which were then back-transformed to their original units for presentation. C and D, Age trends in OC (C) and CTx (D). Fitted lines are generated using locally weighted linear regression (smoothing parameter = 0.5), n = 1029, BACH/Bone 2002–2005.
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We examined partial correlations (rp), adjusted for age, height, weight, 25(OH)D, PTH, and month and time of blood sample, between bone turnover markers and BMD. There were weak but significant negative correlations between serum OC and BMD at the proximal femur (femoral neck rp = –0.10; total hip rp = –0.12) as well as between CTx and total hip (rp = –0.08) and ultradistal radius (rp = –0.09) BMD.
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Discussion
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In this study we report that adjusted serum OC is lower in Black men, compared with White and Hispanic men. CTx is also lower in Black men compared with White men, but not different from Hispanic men. In previous studies performed in women, most, but not all, have similarly reported that bone formation markers are lower in Black compared with White subjects (9, 33, 34, 35, 36) whereas differences in markers of bone resorption were inconsistently found (9, 33, 34, 35, 36, 37, 38). In men, the Third National Health and Nutrition Examination Survey study reported lower serum OC among Black subjects but reported no between-group differences in another biochemical marker of bone formation, bone-specific alkaline phosphatase (31). Data on racial differences in bone resorption are less robust, although the present study generally confirms the results of previous small studies (9, 39).
The mechanisms underlying the lower serum levels of OC and CTx in Black men are unclear. It has been suggested that these differences could be due to racial differences in the skeletal sensitivity to PTH. That hypothesis is supported by a study in women that demonstrated a greater increase in bone resorption markers in White vs. Black women undergoing PTH infusion (40). The PTH-induced response in bone formation markers in this study, however, showed no racial differences, making this mechanistic explanation less pertinent to our finding of decreased bone formation in Black men. Alternatively, because 1,25-dihydroxyvitamin D directly stimulates OC gene transcription and synthesis (41), the lower serum 25(OH)D in Black men could be contributing to the observed lower serum OC. Similarly, because 1,25-dihydroxyvitamin D directly stimulates osteoblast/stromal cell expression of receptor activator of nuclear factor-
B ligand, down-regulates osteoblast/stromal cell expression of osteoprotegerin, and stimulates osteoclastic receptor activator of nuclear factor-
B expression (42), the lower 25(OH)D in Black men may also help explain differences in CTx. These latter hypotheses are consistent with our findings that removing serum 25(OH)D from the linear regression narrowed between group differences in OC and CTx (42). Clearly, however, the influence of serum 25(OH)D is modest, pointing to more complex mechanisms including potential racial/ethnic differences in vitamin D receptor polymorphisms or other genetic factors (43, 44, 45, 46).
In this study we also describe the age-related changes in OC and CTx in men. The increase in OC we observed in the later decades was also reported in the National Health and Nutrition Examination Survey cohort and in some, but not all, smaller studies (31, 47, 48). The observed age-related changes in CTx we report also generally agree with previous reports of smaller numbers of patients (48, 49). We then further attempted to explore the relationship between bone turnover and BMD in Black, Hispanic, and White men. Whereas associations between bone turnover and BMD were found, they were inconsistent, relatively weak, and not influenced by race and ethnicity. Taken together, these results suggest that neither differences in overall bone turnover nor differences in the effect of age on bone turnover are likely to explain the observed differences in BMD between racial/ethnic groups.
The interpretation of our study is limited by the fact that a single measurement of a single bone resorption and formation marker may not consistently represent that subjects steady-state level of bone turnover. Additionally, the fact that the markers were not consistently measured in the fasting state likely added to their variability (particularly CTx). Nonetheless, the strengths of this study, including the large racially diverse population-based cohort, provide important information regarding the influence of race and ethnicity on bone turnover in men. The conclusion we have drawn, namely that bone turnover markers are generally lower in Black men compared with other ethnic groups, and that the relationship between bone turnover and bone density is generally weak and not influenced by race and ethnicity should help inform ongoing research in this area.
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Footnotes
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The BACH/Bone Survey was supported by Grant AG 20727 from the National Institute on Aging. The parent study (BACH) was supported by Grant DK 56842 from the National Institute of Diabetes and Digestive and Kidney Diseases. B.Z.L. was supported by National Institutes of Health Grant K23-RR16310.
None of the authors has a conflict of interest.
First Published Online June 19, 2007
Abbreviations: BACH/Bone, Boston Area Community Health/Bone Survey; BMD, bone mineral density; BUSM, Boston University School of Medicine; CTx, C-terminal telopeptides of type 1 collagen; OC, osteocalcin; 25(OH)D, 25-hydroxyvitamin D; rp, partial correlation coefficient.
Received December 6, 2006.
Accepted June 8, 2007.
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