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The Journal of Clinical Endocrinology & Metabolism Vol. 82, No. 2 429-434
Copyright © 1997 by The Endocrine Society

Clinical Studies

Racial Differences in Bone Density between Young Adult Black and White Subjects Persist after Adjustment for Anthropometric, Lifestyle, and Biochemical Differences1,2

Bruce Ettinger, Stephen Sidney, Steven R. Cummings, Cesar Libanati, Daniel D. Bikle, Irene S. Tekawa, Kimberly Tolan and Peter Steiger

Division of Research (B.E., S.S., I.S.T., K.T.), Kaiser Permanente Medical Care Program, Oakland 94611; Department of Medicine (S.R.C.), University of California, San Francisco 94143; Division of Endocrinology (C.L.), Department of Medicine, Veterans Administration Medical Center, Loma Linda 92357; Mineral Metabolism Unit (D.D.B.), Veterans Administration Medical Center, San Francisco, California 94121; Hologic, Inc. (P.S.), Waltham, Massachusetts 02154

Address correspondence and reprint requests to Bruce Ettinger, MD, Division of Research, Kaiser Permanente Medical Care Program, 3505 Broadway, Oakland, California 94611-5714.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
This study tested whether racial differences in bone density can be explained by differences in bone metabolism and lifestyle. A cohort of 402 black and white men and women, ages 25–36 yr, was studied at the Kaiser Permanente Medical Care Program in Northern California, a prepaid health plan. Body composition (fat, lean, and bone mineral density) was measured using a Hologic-2000 dual-energy x-ray densitometer. Muscle strength, blood and urine chemistry values related to calcium metabolism, bone turnover, growth factors, and level of sex and adrenal hormones were also measured. Medical history, physical activity, and lifestyle were assessed. Statistical analyses using t- and chi-square tests and multiple regression were done to determine whether racial difference in bone density remained after adjustment for covariates. Bone density at all skeletal sites was statistically significantly greater in black than in white subjects; on average, adjustment for covariates reduced the percentage density differences by 42% for men and 34% for women. Adjusted bone density at various skeletal sites was 4.5–16.1% higher for black than for white men and was 1.2–7.3% higher for black than for white women. We concluded that racial differences in bone mineral density are not accounted for by clinical or biochemical variables measured in early adulthood.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
THE LOWER lifetime risk of hip fracture among black persons (1) results at least partly because American black women (2, 3, 4, 5) and men (5, 6) achieve 5%-15% greater peak bone mass than white persons.

The greater bone density among black persons may be caused by their higher obesity rate (7), greater frame size (7), and greater muscle mass (8). However, Luckey and coworkers (3) found that premenopausal black women had statistically significantly greater spinal and radial bone density than white women, even after adjusting for height, weight, and body mass index.

Many have hypothesized that genetically determined differences in skeletal metabolism account for racial differences in bone density; this hypothesis is supported by studies that show racial differences in calciotropic hormones (9, 10) and bone turnover markers (11). Compared with white persons, black persons have lower urinary calcium excretion, higher 1,25-dihydroxyvitamin D (1, 25D) level, and lower 25-hydroxyvitamin D (25D) and osteocalcin level (9). Moreover, bone biopsies in black persons have shown lower bone turnover (12).

Peak bone density can be influenced by lifestyle factors such as dietary calcium intake (13), physical activity (13), smoking, (14) and alcohol intake (14, 15). Menstrual and reproductive factors, including age of menarche (16), pregnancy early in life (15), breast-feeding (17), and oral contraceptive use (13), have also been found by some to influence peak bone density.

Gonadal steroids may account for gender differences (18) and for racial differences in bone density. Regardless of cause, it is generally agreed that lower estrogen level results in lower peak bone mass. Positive associations between bone density and serum estrogen (19) and androgen (20) level have been reported in young women. A positive association between androgen level and bone density exists in young men also (21). Black persons may differ from white persons in sex hormone level. Two studies have demonstrated statistically significantly higher serum testosterone level in young adult black men (22) and women (23).

Our study tested whether racial differences in bone density could be explained by differences in bone metabolism and lifestyle (24). Accordingly, we measured most of the clinical and biochemical variables believed to be related to skeletal health in young adult black and white men and women.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects

Eight hundred fifty volunteer subjects took part in this study, all age 25–36 yr and all simultaneously participants in the Cardiovascular Risk Development in Young Adults (CARDIA) study, a study initiated by the National Heart, Lung, and Blood Institute (NHLBI) in 1983 to determine risk factors for coronary heart disease among black and white men and women and to identify lifestyle characteristics associated with these risk factors (25). The Kaiser Permanente Medical Care Program (KPMCP), a prepaid health plan that serves about one quarter of the local population in Oakland, California, was one of four sites selected for recruitment of participants in the CARDIA study. The study protocol was approved by the KPMCP Northern California Region Institutional Review Board.

After exclusions for certain laboratory abnormalities and pregnancy-related criteria, 799 subjects were used in the analysis: 197 black men, 263 black women, 157 white men, and 182 white women. Because of financial constraints, blood and urine chemistry studies, planned for only the first 100 in each sex-race subject group, were obtained for 402 of the study subjects (the core group): 109 black men, 95 black women, 114 white men, and 84 white women. We excluded women who were currently breast-feeding or who, within the previous year, had been pregnant or had less than 10 spontaneous menstrual cycles. We also excluded women from the core group if they reported current usage of oral contraceptive agents. We also excluded those with renal failure (serum creatinine >1.5 mg/dL), hypocalcemia (<8.5 mg/dL), or hypercalcemia (>10.3 mg/dL), a total of 4 subjects.

Bone and body composition measurement

Dual energy x-ray absorptiometry (DXA) of total body, hip, and lumbar spine was done by using a Hologic 2000 densitometer (Hologic, Inc, Waltham, MA) in the array scanning mode. In vivo precision for bone mineral density (BMD), based on repeated scans of 20 volunteers done 1–6 weeks apart and expressed as a coefficient of variation, was .9% for total body BMD, 1.4% for posteroanterior spine BMD, and 2.2% for femoral neck BMD. Hologic software calculates the estimated volume for L-3 vertebra from the product of the projected area of the lateral scan and the vertebral width. The latter is the quotient of the projected area of the PA scan divided by the vertebral height. L-3 volumetric density is the L-3 bone mineral content divided by L-3 estimated volume (26). Lean body mass, fat mass, and ratio of trunk to leg fat were also measured using DXA in the enhanced total body array scanning mode. In vivo precision for fat mass based on repeated scans in 18 volunteers was 5.9%.

Muscle strength

Average isokinetic muscle strength of the quadriceps and hamstring muscles was measured with a Cybex II dynamometer (Lumex, Ronkonkoma, NY). The best of five repetitions was used for both flexion and extension.

Biochemical tests

The following markers of bone and mineral metabolism were obtained from blood drawn when the subject was fasting: creatinine, calcium, phosphorus, bone-specific alkaline phosphatase, intact parathyroid hormone, 25D, 1,25D, and osteocalcin (Bikle D.D., unpublished material). The following growth factors were measured by immunoassay: insulin, insulin-like growth factor-I (IGF-I) (27), and IGF-binding protein 3 (IGFBP3) (28). Sex and adrenal hormone immunoassays were done at Endocrine Sciences Laboratory, Calabasas Hills, California; these included assays for testosterone (total, free, and bioavailable), sex-hormone-binding globulin, estradiol, and dehydroepiandrosterone sulfate. Estradiol was measured in women only, and this measurement was obtained between day 3 and day 11 of the menstrual cycle. The estradiol index was calculated by dividing the estradiol by the sex-hormone-binding globulin. Urine (collected during 24 h) was obtained for calcium, creatinine, and free total pyridinoline measurement. Free total pyridinoline cross-links were measured by enzyme-linked immunoassay (29) (Metra Biosystems Inc, Palo Alto, CA).

Medical history and habits

Usual diet was assessed by a diet history interview in which food models and measuring cups and spoons were used to estimate portion size (30). Daily nutrient intake, including intake of calcium and vitamin D, was estimated by translating the precoded CARDIA diet history from the database. Calcium and vitamin D intake estimates included supplemental sources.

Physical activity was assessed by an interviewer-administered questionnaire, which asked about level of participation during the last year in 13 specific activities (or groups of activities that have similar intensity). Because type and intensity of different activities were documented separately, we were able to separately analyze the effect of heavy-weight-bearing activity. We computed physical activity scores based on the sum of time spent in each activity weighted by an estimate of kilocalories expended for each activity (31). The reliability of this instrument was studied by comparing questionnaire results with results repeated 2 weeks later (n = 129). The test-retest correlation of the total score was .84 (32).

Medical histories and histories of tobacco use and alcohol use were obtained by a self-administered and interview-administered questionnaire.

Statistics

The purpose of these analyses was to determine how much racial differences in bone density would remain after adjustment for covariates. The analysis was done separately for men and women in 3 phases. First, by using subjects from the entire cohort (n = 799), variables that showed possible racial differences (P < .1) using t- and chi-square tests were identified as possible predictor variables. These variables were assigned to 1 of 10 categories: 6 clinical categories: body size, muscle, fat, physical activity, lifestyle, and reproductive history (women only); and 4 biochemical categories: calcium metabolism, bone turnover, growth factors, and sex and adrenal hormones.

All later analytic phases were completed for subjects in the core cohort (n = 402) who had data on both clinical and biochemical variables. Next, forward, stepwise regression models were used to identify predictor variables which showed a relation (P < .1) with bone density, when considered simultaneously. Relations were examined for posteroanterior spine, lateral L3 spine, volumetric L3 spine, total femur, femoral neck, femoral trochanter, Ward’s triangle, and total body bone density. Regression analyses were first done within each of the 10 categories. Variables that were significant within a category were then tested simultaneously in a regression model that included variables from all categories. Because variables in the fat category were highly correlated, we separated them into 2 groups, those that measured overall fat (total fat by DXA, weight, BMI, and sum of skinfolds) and those that measured fat distribution (ratio of trunk:leg fat by DXA and ratio of waist:hip circumference). BMI, as a measure of overall fat, and waist:hip ratio, as a measure of fat distribution, were the most consistent and strong predictors of BMD. In the third phase, variables that still had a statistically significant relation (P < .05) with bone density were used in a final regression model that included race as a covariate. The difference in adjusted means by race in the final model is a measure of remaining racial differences in BMD. As a measure of relative magnitude of difference in bone density, we calculated percentage difference for each skeletal site; this was defined as the mean for black persons minus mean for white persons divided by mean for white persons. Absolute differences in BMD with 95% confidence intervals were calculated on the basis of unadjusted means and adjusted means from the regression models.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Demographic, anthropometric, and lifestyle characteristics of the core group are shown in Table 1Go. Differences were noted in a number of these variables; statistically significant racial differences in the full cohort for clinical and laboratory variables are summarized in Table 2Go. Among men, physical activity scores were higher among black participants; among women, white participants had higher scores. Calcium and vitamin D intake were higher in white women than in black women, but no statistically significant differences were seen among men. Black participants were heavier than white participants, had higher caloric intake, and reported more hours of sun exposure per week. The proportion of current smokers among black participants was about twice as high, while the amount of caffeine consumption was about half. Black women were more likely to have earlier menarche, to have more children, and to give birth before age 21 yr. In contrast, breast feeding was more common among white women than black women. Both black men and black women had lower 25D as well as higher 1,25D levels and markedly lower urinary calcium excretion. We plan to report the details of calciotropic hormone analyses elsewhere (Bikle D.D., unpublished material). Inconsistent racial differences were observed in markers of bone turnover and growth factors.


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  		Table 1. Characteristics of the core group of 402 subjects age 25–36 yr, by gender and race

 

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  		Table 2. Summary significance for clinical and biochemical variables that differed between races when tested in the entire cohort

 
Mean hip and spine size, determined by DXA, was smaller in black than in white women; among men, there were no statistically significant racial differences in these sites. Because of their larger appendicular bone area, black men had 3% greater total skeletal area than their white counterparts; similar trends were observed between women subjects (Table 3Go). Lean body mass was greater in black persons than in white persons; differences observed were 6.6% for men and 2.6% for women. Black women had greater mean body fat and other mean fat indexes than white women, but black men were leaner than white men. Measures of fat distribution showed higher ratio of abdominal to lower extremity fat in men compared with women; however, white men showed greater abdominal fat than black men, whereas black women showed greater abdominal fat than white women.


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  		Table 3. Body composition variables for the core group by gender and race

 
Black men and women tended to have higher mean total, free, and bioavailable testosterone levels but lower dehydroepiandrosterone sulfate levels than their white counterparts. Among women, no statistically significant racial differences were found in mean estradiol or estradiol index (Table 4Go).


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  		Table 4. Sex and adrenal hormones in the core group by gender and race

 
Bone density at all skeletal sites was statistically significantly greater in black persons than in white persons (Table 5Go); the racial differences were about 1.5–2 times as great in men as in women. The greatest racial differences were noted in Ward’s triangle. In the relatively narrow age range of our subjects, no consistent age-related change in BMD was found for BMD measurements (data not shown). The BMD of white women and men in our cohort agreed closely with the age-expected values provided in the Hologic reference database; for women, posteroanterior spine density was within +0.2%, total hip density was within 1.6%, and whole body BMD was within -0.4%; for men, posteroanterior spine density was -5.8%, and total hip density was -3.7%.


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  		Table 5. Bone mineral density (BMD) in the core group by gender and race

 
Of 37 variables that differed between races, less than half were significantly (P < .05) associated with bone density in any of the final regression models. Anthropometric variables appeared in all the final models; most frequently included for men was lean mass, and for women, body mass index. At least one lifestyle variable appeared in most of the final models, with caloric intake most consistent. Biochemical tests did not show a consistent pattern of inclusion in these models. Multivariate models that did not include race as a covariate explained from 22–45% of the variance in 8 BMD measurements in men and from 10–34% of this variance in women (Table 6Go). Adjustment for covariates reduced racial differences in the 8 BMD measurements, on average, 42% for men (range 35–55%) and 34% for women (range 0–81%). After these adjustments, similar racial differences in total body BMD in both genders remained, but larger racial differences were found between spine and hip densities in men than in women.


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  		Table 6. Difference in various BMD measurements between black and white subjects, adjusted (and unadjusted)

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
By using DXA area measurements, we confirmed that young, adult, black men and women have substantially greater BMD than white persons (2, 3, 4, 5, 6); this finding is true at all skeletal sites, and we have extended these observations to volumetric estimates of spinal BMD. Despite an extensive search for clinical and biochemical explanations, we were unable to account for most of the racial differences in BMD.

The racial differences we observed in BMD do not appear to be artifacts of the DXA method. Although the greater area bone density observed after measurement with DXA could be caused by larger bone size and therefore may not represent a true increase in volumetric density, our measurement of area and volume of both spine and hip show that black persons do not have larger vertebrae or upper femurs than white persons. Further, the magnitude of the BMD differences in spinal volumetric density are similar to those for spinal area density.

Our large, population-based study had sufficient power to detect racial differences in clinical and biochemical variables on the order of 0.5 standard deviations. Clinical and biochemical assessment was extensive and enabled us to study a comprehensive list of variables that others have considered relevant to bone mass. After multiple adjustments for these variables, about half the racial differences in BMD still remained. This finding suggests that other factors than those controlling muscle mass and body size must act specifically on the skeleton.

We conclude that racial differences in BMD are established early in childhood (33) and are not explained by clinical and biochemical variables measured in young adulthood. Studies of adolescents might find differences in metabolic or lifestyle factors that account for a larger share of the racial differences in bone mass than those that we observed. By midadolescence, black boys and girls have 10–15% greater bone density than their white counterparts (33). However, most of the difference would be expected to remain evident 10–20 yr later. Thus, the appearance of such a large racial difference in young adults cannot be attributed to persistent differences in metabolic or lifestyle factors and supports the view that bone density differences result from influences operating during childhood and adolescence.


   Footnotes
 
1 This study was supported by the National Institute of Health & Human Services through Control N01-HC-48050 from the National Heart, Lung, and Blood Institute, National Institute of Health, and through Grant 5 R01-AR40430-03 from the National Institute of Arthritis and Musculoskeletal and Skin Diseases. Back

2 The Medical Editing Department, Kaiser Foundation Research Institute, provided editorial assistance. Back

Received May 2, 1996.

Revised September 24, 1996.

Accepted September 30, 1996.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  12. Weinstein RS, Bell NH. 1988 Diminished rates of bone formation in normal black adults. N Engl J Med. 319:1698–1701.[Abstract]
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  20. Buchanan JR, Myers C, Lloyd T, Leuenberger P, Demers LM. 1988 Determinants of peak trabecular bone density in women: the role of androgens, estrogen, and exercise. J Bone Miner Res3 :673–80.
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  23. Henderson BE, Bernstein L, Ross RK, Depue RH, Judd HL. 1988 The early in utero oestrogen and testosterone environment of blacks and whites: potential effects on male offspring. Br J Cancer 57:216–218.
  24. Kelly PJ, Eisman JA, Sambrook PN. 1990 Interaction of genetic and environmental influences on peak bone density. Osteoporos Int 1:56–60.
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  27. Mohan S, Bautista CM, Herring SJ, Linkhart TA, Baylink DJ. 1990 Development of valid methods to measure insulin-like growth factors-I and -II in bone cell-conditioned medium. Endocrinology126 :2534–42.
  28. Blum WF, Ranke MB, Kietzmann K, Gauggel E, Zeisel HJ, Bierich JR. 1990 A specific radioimmunoassay for the growth hormone (GH)-dependent somatomedin-binding protein: its use for diagnosis of GH deficiency. J Clin Endocrinol Metab. 70:1292–1298.[Abstract]
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