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Ultrasound Measurements of the Calcaneus
Journal of Clinical Densitometry, vol. 2, no. 1, 31–36, Winter 1998 © Copyright 1999 by Humana Press Inc. All rights of any nature whatsoever reserved. 0169-4194/99/2:31–36/$11.50
Original Article
Ultrasound Measurements of the Calcaneus Effects of Ethnicity*
Frances A. Tylavsky, DR PH,1 Laura D. Carbone, MD,2 Sulin Cheng, PHD,3 and Jim Y. Wan, PHD1 1Department
of Preventive Medicine, 2Department of Medicine, University of Tennessee, Memphis, TN, 3Department of Radiology, University of California, San Francisco, CA
Abstract This study investigated whether there were differences in quantitative ultrasound (QUS) of the calcaneus between African-American and Caucasian females. QUS-1XTM, an ultrasonometer by Metra Biosystems Inc., was used to determine broadband ultrasound attenuation (UBI-4) using Burg Spectral Estimation in decibels/megahertz. The average transit time through the heel (TTH) in microseconds was used to estimate bone size. A multiple factor index taking into account bone size, UBI-4T, was calculated by dividing UBI-4 by TTH in decibels/(Megahertz·microseconds). Results showed that premenopausal Caucasian females (n = 37) have approx 6–8% lower values (p < 0.05) of QUS indices than their African-American (n = 54) counterparts. However, after adjusting for bone size, the differences in attenuation disappeared. Pilot data for males (Caucasian: n = 16, African-American: n = 18) suggest that the differences in QUS appear to be related to bone size. The limited scope of our study supports the fact that there are differences in QUS between premenopausal Caucasian and African-American females, but not with the same magnitude as evidenced by dual X-ray absorptiometry. We recommend that more data be collected on ethnic differences across all age ranges, to help understand how QUS may be used to assess bone mass and determine its value either as a screening tool to diagnose low bone mass or as a tool to predict osteoporotic fracture within various ethnic groups. Key Words: Ultrasound; ethnicity; calcaneus; premenopausal women; young males.
tinuing through the ninth decade (1–4). Bone mass measurements using dual X-ray absorptiometry (DXA) suggest that on average African-Americans have between 12 and 18% higher bone mineral density (BMD) (3). Quantitative computed tomography (QCT) of the spine suggests a 40% difference in volumetric density between African-American and Caucasian females (5), with ethnic differences becoming evident during late puberty (6). Studies utilizing histomorphometry and QCT suggest that these ethnic differences are because of thicker trabeculae and a thicker cortical shell in African-Americans (5–7).
Introduction Cross-sectional studies consistently report higher bone mass measurements in African-Americans compared with Caucasians beginning at age 1 yr and conReceived 08/12/98; Revised 11/09/98; Accepted 11/13/98. * Presented in part at the Annual Meeting of the American Society of Bone and Mineral Research, Seattle, Washington, September 1996. Address correspondence to Dr. Frances A. Tylavsky, Department of Preventive Medicine, 66 N. Pauline, Suite 633, Memphis, TN 38163. [email protected]
31
32 Quantitative ultrasound (QUS) is a technique that has been utilized to provide estimates of mechanical and architectural properties in bone (8–12). QUS values have been shown to correlate with bone structure, strength, and architecture in vitro (13–16). Whether these same properties are measured in vivo remains to be determined. In theory, QUS measurements should reflect differences in the quantity and arrangement of trabecular and cortical tissue. The aim of this study was to evaluate whether there were differences in QUS of the calcaneus between African-American and Caucasian females.
Tylavsky et al. of reported onset of menses. A self-report of high blood pressure, osteoarthritis, or noninsulin-dependent diabetes mellitus was considered to be a comorbid condition.
Smoking History Current and past use of cigarettes was assessed using a questionnaire. The age of initiation of tobacco smoking, number of packs per week, and duration of cigarette use in years was ascertained. Pack years were calculated to represent smoking behavior.
Calcium Intake
Materials and Methods Subjects One hundred twenty-five individuals between the age of 18 and 50 yr were recruited from the Metropolitan Statistical Area surrounding Memphis, Tennessee, to participate in a study assessing normal levels of bone mass at the calcaneus using an ultrasonometer. Individuals were excluded on the basis of self-report of any condition or medication known to affect calcium metabolism including long-term immobilization, surgical menopause, chronic renal failure, chronic liver impairment, malabsorptive disorders, and the use of anticonvulsants or corticosteroids. Subjects were also excluded if they reported any atraumatic fractures. The complete data set on all variables for the 125 individuals (37 Caucasian females, 54 African-American females, 16 Caucasian males, and 18 African-American males) was used for statistical analyses in this report. Written consent for participation in the study was obtained from all subjects prior to performing ultrasound measurements. The study was approved by the Institutional Review Board of the University of Tennessee.
Menstrual, Reproductive, and Medical History Menstrual, reproductive, and medical histories were assessed by questionnaire. Report of an osteoporotic fracture or kyphosis for any family member was considered as a positive family history of osteoporosis. Chronologic age was calculated as the date of bone measurement minus the date of birth. For females the age of menarche was the age Journal of Clinical Densitometry
Usual calcium intake in milligrams/day was obtained using a 7-d food-frequency recall. This method has been shown to provide a moderate correlation with 24-h recalls, a reasonable calcium intake compared to 3-d food records, and a test-retest reliability of 0.80 (17).
Physical Activity Physical activity was assessed by self-report concerning leisure time and activities of daily living. An integrated scoring system was developed using intensity, duration, and frequency of reported activities. Subjects were considered to have low physical activity if they reported performing only those activities necessary for daily care. High physical activity was assigned to those subjects that reported engaging in leisure time activity daily, with the remaining subjects classified as having moderate levels of physical activity.
Bone Measurements QUS-1X TM, an ultrasonometer by Metra Biosystems Inc., Mountain View, CA, is a dry scanning ultrasound system. The QUS-1X used point source transducers with a frequency range of 200–800 kHz to determine attenuation (UBI-4) using Burg spectral estimation in decibels/megahertz. Burg spectral analyses estimated the parameters of an autoregressive process using maximal entropy ideas. The average transit time through the heel (TTH) is the average time interval from 600 ns after the start of capacitor discharge to the first peak of the signal in microseconds. Since the heel thickness can be calculated as a function of time, TTH can be used as an indicator for the estimation of heel Volume 2, 1999
Ethnicity and Ultrasound of the Calcaneus thickness, i.e., bone size. A multiple factor index taking into account bone size, UBI-4T, was calculated by dividing UBI-4 by TTH. The heel was placed in a foot holder between two transducers by keeping the ankle at a 90° angle. The midcalcaneus, which geometrically represents the most uniform part of the bone, was identified by taking two-thirds of the distance from the heel to the distal end of the lateral malleolus as the site of the scan. Optimal contact between the skin and transducer was ensured by a thin layer of water-based jelly. To minimize measurement error, two measurements were performed on each participant. If the differences in two measurements exceeded 10.0 dB/MHz, a third measurement was performed. The average of two measurements that were within 10.00 dB/MHz was used for reporting purposes. The coefficient of variation (CV) was determined by performing repeat measurement without repositioning. The CV of measurements was <3% from TTH and UBI-4. Similar CV’s have been reported elsewhere (14) on other QUS instruments.
Statistical Analyses All statistical analyses were performed using the Statistical Analysis System (18). Descriptive means and standard deviations (SDs) were obtained for all bone and continuous independent variables according to ethnicity and sex groupings. T-tests were used to evaluate differences in QUS parameters between the ethnic groups. No adjustment was made for the influences of comorbid disease conditions on QUS parameters between the ethnic groups owing to only one report of a comorbid disease. Fisher exact test was used to determine whether the frequency of distribution for the number of children, family history of osteoporosis, or oral contraceptive use was different between the ethnic groups.
Results Descriptive Statistics Table 1 presents means ± SD of age, height, weight, body mass index (BMI), dietary calcium intake, cigarette smoking history, and percentage positive for a family history of osteoporosis. Fisher exact test determined the observed frequency distribution of the number of biological children for Journal of Clinical Densitometry
33 Table 1 Description of Selected Characteristics for Females According to Race (Mean ± SD)a Variable
Caucasian
n 37 Age (yr) 30.1±9.4 Height (cm) 164.6±8.1 Weight (kg) 63.6±11.2 BMI (kg/cm2) 23.6 ± 4.4 Education (yr) 14.2±1.6 Smoking (pack yr) 13.1±7.9(11) Calcium intake (mg) 819±381 Family history of osteoporosis (%) 27.0a Exercise level(%) Low 43.2 Moderate 40.5 High 16.2 Biological children (%) 0 62.2 1–2 29.7 ≥3 8.1 Age of menarche (yr) 12.4±1.7 Oral contraceptive use (%) 64.9
African-American 54 26.7±8.0 163.8±7.4 71.7±16.8 26.8 ± 6.3 13.8±2.0 0.1±0.4 (2) 792±493 3.7b 54.7 39.6 5.7 44.4 44.4 11.1 12.3± 1.6 48.2
a
p<0.05 between ethnic group. Twenty percent of the Caucasian and 12% of the AfricanAmerican females reported uncertainty of the presence of a family history of osteoporosis. b
Caucasian and African-American females. A family history of osteoporosis was reported by 27% of Caucasian females, 6% of Caucasian males, and 3.7% of African-American females, and there were no reports of a positive family history of osteoporosis by males of African-American ethnicity (p < 0.001). Twenty percent of Caucasian females and 12% of African-American females reported uncertainty of the presence of a family history of osteoporosis. Only one person reported the presence of osteoarthritis as a comorbid condition. Table 2 presents the mean ± SD, minimum, and maximum values for UBI-4, TTH, and UBI-4T for Caucasian and African-American females. Caucasian females had different attenuation values for UBI-4 and TTH compared with AfricanAmerican females (p < 0.05). However, when adjusting for TTH, an indicator of bone size, the difVolume 2, 1999
34
Tylavsky et al. Table 2 QUS Parameters for the Female Study Population According to Ethnicity (Mean ± SD, Minimum and Maximum Values)
Variable n
UBI-4 (dB/MHz) Mean ± SD Minimum Maximum TTH (µs) Mean ± SD Minimum Maximum UBI-4T (dB/MHz/µs) Mean ± SD Minimum Maximum
Caucasian
African-American
37
54
96.3±11.7a 56.3 116.0
102.7±10.1a 72.3 122.0
28.9±3.0a 23.8 38.3
31.3 ± 3.2a 25.2 39.5
3.4±0.5 1.9 4.4
3.3±0.4 2.4 4.4
a Significant differences (p<0.05) between Caucasian and African-American females.
ferences in attenuation disappeared. Pilot data for males suggest that Caucasians have similar UBI-4 values but lower TTH values than African-American males (105.6 ± 9.8 vs 104.9 ± 6.4 and 30.6 ± 2.2 vs 34.5 ± 4.5, respectively).
Discussion Increased levels of BMD (3) and a geometrical difference in hip axis length are considered to be responsible, in part, for a lower risk of fracture for African-American females (19) but have not been clearly demonstrated for males (20). Our study shows that premenopausal Caucasian females have approx 6 to 7% lower values (p < 0.05) of UBI-4 and TTH than their African-American counterparts. For males, the differences in QUS indices appear to vary from 0 to 8% between ethnic groups depending on the bone parameter assessed. This is in contrast to reports of differences in BMD of the total femur by DXA, which range from 7 to 14% for young adults in the third and fourth decade (3). Only recently have ethnic differences been reported for broadband ultrasound attenuation (BUA) as assessed by QUS. A study by Cauley et al. (21) of postmenopausal females found that the difJournal of Clinical Densitometry
ferences between ethnic groups for BUA ranged from 7.5% (unadjusted) to no difference when adjusted for age, weight, height, and/or calcaneal BMD. These results imply that differences in QUS measurements are due to differences in anthropometric measurements and BMD. Although BMD estimates by DXA were not obtained in the current study, we have found that adjusting for BMD of the femoral neck had little or no impact on differences in QUS measurements performed in our other studies (22). Since there is little standardization in the ultrasonic industry, the disparity between our study and others could be owing to differences in the ultrasonometers used in the respective studies. Other factors most often cited to account for ethnic differences in bone mass are considered to be genetically expressed through skeletal size (23,24), muscle mass (5,24), bone turnover (25), and skeletal metabolism (26–28). Our study agrees with the premise that the larger skeletal size is a primary difference between African-Americans and Caucasians. TTH, an indicator of bone size, was the major difference observed between sex-matched ethnic groups. Furthermore, once bone size was taken into account the differences disappeared. In theory, this parameter can be affected by differences in microarchitecture, geometry of the bone, and the soft tissue. Some histomorphometric measurements of the iliac crest suggest that the primary differences between African-American and Caucasian females are owing to a thicker cortical shell and thicker trabeculae (7). Cross-sectional analysis of data by Han et al. (7) suggests that the number of trabeculae, the cortical porosity, and the rate of loss with age are similar across the ethnic groups. QCT of the spine provided similar results (5). Since the calcaneus is composed of 95% trabecular bone tissue with the remaining 5% representing the cortical shell, differences in QUS observed in this study could be interpreted as representing differences in trabecular tissue between the two ethnic groups. Weight-bearing loads are considered to have significant effects on the quantity of bone mass at different skeletal sites. Body height and weight produce the most consistent load-bearing effects on the calcaneus. In our sample, height, weight, or BMI was similar among the sex and ethnic groupings. Other researchers have shown that for a given weight
Volume 2, 1999
Ethnicity and Ultrasound of the Calcaneus African-Americans have higher levels of lean body mass (4,29,30). In our study, we were not able to estimate whether or not levels of lean body mass influenced our results. Physical activity with high-impact loading on the calcaneus could be a differentiating factor. Although we used a physical activity questionnaire that included duration, frequency, and intensity of loadbearing activity, we were unable to see any ethnic differences in activity patterns that could contribute to differences in bone parameters. Other factors known to affect the risk of osteoporosis and impact on bone density include longterm dietary calcium (31), cigarette smoking, and reproductive history. Our study did not obtain longterm dietary calcium intake and found no differences in reported current intake. A higher percentage of Caucasian females reported smoking cigarettes and had a higher quantity of pack years. However, the differences were minimal and unlikely to impact bone mass. Both ethnic groups of females reported a similar age of menarche, which has been shown to affect BMD levels of females in the third decade (32). Both groups reported using oral contraceptives with similar frequency, and had a similar number of children. Therefore, we were unable to estimate differences because of these factors. Family history of osteoporosis, a risk factor for osteoporosis, and lower BMD was reported more frequently by Caucasians than African-Americans (p<0.001), with 9% of the African-American and 16% of the Caucasian females uncertain of its presence. This reported difference in family history of osteoporosis may be because of a genetic tendency for osteoporosis in Caucasians. Alternatively, it could reflect a lack of true awareness of the presence of osteoporosis in our research subjects. A previous report demonstrated that Caucasian females between the age of 18 and 22 yr were unable to provide information on family history of osteoporosis (31). The limited scope of our study shows that there are differences in UBI-4 and TTH when measured with the QUS IX between premenopausal Caucasian and African-American females, but not with the same magnitude as evidenced by DXA. For males, our pilot data suggest that differences between African-American and Caucasian males were smaller than those obtained by DXA. A better under-
Journal of Clinical Densitometry
35 standing of the differences in bone properties between African-Americans and Caucasians is important, and may ultimately lead to better strategies to prevent fractures. We recommend that more data be collected on ethnic differences across all age ranges, to help understand how QUS may be used to assess bone mass and to determine its value either as a screening tool or as a tool to predict osteoporotic fracture within various ethnic groups.
Acknowledgments The authors would like to acknowledge the support of Metra Biosystems, Inc. in performing this study.
References 1. Li JY, Specker BL, Ho ML, Tsang RC. 1989 Bone mineral content in black and white children 1 to 6 years of age: early appearance of race and sex differences. Am J Dis Child 143:1346–1349. 2. Pollitzer W, Anderson J. 1989 Ethnic and genetic differences in bone mass: a review with a hereditary versus environmental perspective. Am J Clin Nutr 50:244–259. 3. Looker AC, Wahner HW, Dunn WL, Calvo MS, et al. 1995 Proximal femur bone mineral levels of US adults. Osteoporos Int 5:389–409. 4. Nelson D, Simpson P, Johnson C, Barondess D, Kleerekoper M. 1997 The accumulation of whole body skeletal mass in third and fourth grade children: effects of age, gender, ethnicity, and body composition. Bone 20:73–78. 5. Kleerekoper M, Nelson DA, Peterson EL, et al. 1994 Reference data for bone mass, calcitropic hormones, and biochemical markers of bone remodeling in older (55–75) postmenopausal white and black women. J Bone Miner Res 9:1267–1276. 6. Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG. 1991 Changes in vertebral bone density in black girls and white girls during childhood and puberty. N Engl J Med 325:1597–600. 7. Han ZH, Palnitkar S, Sudhaker Roa D, Nelson D, Parfitt AM. 1996 Effect of ethnicity and age or menopause on the structure and geometry of iliac bone. J bone Miner Res 11:1967–1975. 8. Langton C, Evans G, Hodgskinson R, Riggs C. 1990 Ultrasonic, elastic and structural properties of cancellous bone. In: Current Research in Osteoporosis and Bone Mineral Measurements. British Institute of Radiology 10–11. 9. Evans J, Tavakoli M. 1990 Ultrasonic attenuation and velocity in bone. Phys Med Biol 35:1387–1396. 10. Tavakoli M, Evans J. 1991 Dependence of the velocity and attenuation of ultrasound in bone on the mineral content. Phys Med Biol 36:1529–1537.
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36 11. Tavakoli M, Evans J. 1992 The effect of bone structure on ultrasonic attenuation and velocity. Ultrasonics 30:389–395. 12. Gluer C, Vahlensieck M, Faulkner K, Engelke K, Black D, Genant H. 1992 Site-matched calcaneal measurements of broad-band ultrasound attenuation and single X-ray absorptiometry: do they measure different skeletal properties? J Bone Miner Res 7:1071–1079. 13. Gluer C, Wu C, Jergas M, Goldstein S, Genant H. 1994 Three quantitative ultrasound parameters reflect bone structure. Calcif Tissue Int 55:46–52. 14. Hans D, Arlot M, Scjptt A, Roux J, Kotzki P, Meunier P. 1995 Do ultrasound measurements on the os calcis reflect more the microarchitecture of bone than the bone mass? A two-dimensional histomorphometrics study. Bone 15:295–300. 15. Bouxsein ML CA, Hayes WC. 1995 Ultrasound and densitometry of the calcaneus correlate with the failure loads of cadaveric femurs. Calcif Tissue Int 56:99–103. 16. Langton C, Njeh C, Hodskinson R, Currey J. 1996 Prediction of mechanical properties of the human calcaneus by broadband ultrasonic attenuation. Bone 18:495–503. 17. Hertzler A, Frary RB. 1994 A dietary calcium rapid assessment method. Top Clin Nutr 9:76–85. 18. SAS Institute I. 1990 SAS/STAT user’s guide, version 6, 4th ed. Cary, North Carolina: SAS Institute. 19. Cummings S, Cauley J, Palermo L, et al. 1994 Racial differences in hip axis lengths might explain racial differences in rates of hip fracture. Osteoporos Int 4:226–229. 20. Nelson D, Jacobsen G, Barondess D, Parfitt A. 1995 Ethnic differences in regional bone density, hip axis length, and lifestyle variables among healthy black and white men. J Bone Miner Res 10:782–787. 21. Cauley J, Danielson M, Gregg E, Vogt M, Zmuda J, Bauer D. 1997 Calcaneal ultrasound attenuation in older AfricanAmerican and Caucasian-American women. Osteoporos Int 7:100–104. 22. Cheng S, Tylavsky F, Orwoll ES, Rho J, Carbone L. 1999 The role of collagen abnormalities in ultrasound and densitometry assessment in vivo evidence. Calcif Tissue Int, in press. 23. Perry HM, Horowitz M, Morely JE, et al. Aging and bone metabolism in African-American and Caucasian women. 1996 J Clin Endocrinol Metab 81:1108.
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Tylavsky et al. 24. Ettinger B, Sidney S, Cummings S, et al. 1997 Racial differences in bone density between young adult black and white subjects persist after adjustment for anthropometric, lifestyle, and biochemical differences. J Clin Endocrinol Metab 82:429–434. 25. Slemenda C, Peacock M, Hui S, Zhou L, Johnston C. 1997 Reduced rates of skeletal remodeling are associated with increased bone mineral density during the development of peak skeletal mass. J Bone Miner Res 12:676–682. 26. Bell NH, Yergery AL, Vieiri NE, Oexmann MJ, Shary JR. 1993 Demonstration of a difference in urinary calcium, not calcium absorption, in black and white adolescents. J Bone Miner Res 8:1111–11115. 27. Meier D, Luckey M, Wallenstein S, Clemens T, Orwoll E, Waslien C. 1991 Calcium, vitamin D, and parathyroid hormone status in young white and black women: association with racial differences in bone mass. J Clin Endocrinol Metab 72:703–710. 28. Luckey M, Meier D, Mandeli J, DaCosta M, Hubbard M, Goldsmith S. 1989 Radial and vertebral bone density in white and black women: evidence for racial differences in premenopausal bone homeostasis. J Clin Endocrinol Metab 69:762–770. 29. Cohn S, Abesamis C, Yasumura S, Aloia J, Zanzi I, Ellis K. 1977 Comparative skeletal mass and radial bone mineral content in black and white women. Metabolism 26:171–178. 30. Oritz O, Russell M, Daley R, et al. 1992 Differences in skeletal muscle and bone mineral mass between black and white females and their relevance to estimates of body composition. Am J Clin Nutr 55:8–13. 31. Tylavsky F, Anderson J, Talmage R, Taft T. 1992 Are calcium intakes and physical activity patterns during adolescence related to radial bone mass of white college-aged females? Osteoporos Int 2:232–240. 32. Tylavsky FA, Bortz AD, Hancock RL Anderson JJB. 1989 Familial resemblance of radial bone mass between premenopausal mothers and their college-age daughters. Calcif Tissue Int 45:265–272.
Volume 2, 1999
Original Article
Ultrasound Measurements of the Calcaneus Effects of Ethnicity*
Frances A. Tylavsky, DR PH,1 Laura D. Carbone, MD,2 Sulin Cheng, PHD,3 and Jim Y. Wan, PHD1 1Department
of Preventive Medicine, 2Department of Medicine, University of Tennessee, Memphis, TN, 3Department of Radiology, University of California, San Francisco, CA
Abstract This study investigated whether there were differences in quantitative ultrasound (QUS) of the calcaneus between African-American and Caucasian females. QUS-1XTM, an ultrasonometer by Metra Biosystems Inc., was used to determine broadband ultrasound attenuation (UBI-4) using Burg Spectral Estimation in decibels/megahertz. The average transit time through the heel (TTH) in microseconds was used to estimate bone size. A multiple factor index taking into account bone size, UBI-4T, was calculated by dividing UBI-4 by TTH in decibels/(Megahertz·microseconds). Results showed that premenopausal Caucasian females (n = 37) have approx 6–8% lower values (p < 0.05) of QUS indices than their African-American (n = 54) counterparts. However, after adjusting for bone size, the differences in attenuation disappeared. Pilot data for males (Caucasian: n = 16, African-American: n = 18) suggest that the differences in QUS appear to be related to bone size. The limited scope of our study supports the fact that there are differences in QUS between premenopausal Caucasian and African-American females, but not with the same magnitude as evidenced by dual X-ray absorptiometry. We recommend that more data be collected on ethnic differences across all age ranges, to help understand how QUS may be used to assess bone mass and determine its value either as a screening tool to diagnose low bone mass or as a tool to predict osteoporotic fracture within various ethnic groups. Key Words: Ultrasound; ethnicity; calcaneus; premenopausal women; young males.
tinuing through the ninth decade (1–4). Bone mass measurements using dual X-ray absorptiometry (DXA) suggest that on average African-Americans have between 12 and 18% higher bone mineral density (BMD) (3). Quantitative computed tomography (QCT) of the spine suggests a 40% difference in volumetric density between African-American and Caucasian females (5), with ethnic differences becoming evident during late puberty (6). Studies utilizing histomorphometry and QCT suggest that these ethnic differences are because of thicker trabeculae and a thicker cortical shell in African-Americans (5–7).
Introduction Cross-sectional studies consistently report higher bone mass measurements in African-Americans compared with Caucasians beginning at age 1 yr and conReceived 08/12/98; Revised 11/09/98; Accepted 11/13/98. * Presented in part at the Annual Meeting of the American Society of Bone and Mineral Research, Seattle, Washington, September 1996. Address correspondence to Dr. Frances A. Tylavsky, Department of Preventive Medicine, 66 N. Pauline, Suite 633, Memphis, TN 38163. [email protected]
31
32 Quantitative ultrasound (QUS) is a technique that has been utilized to provide estimates of mechanical and architectural properties in bone (8–12). QUS values have been shown to correlate with bone structure, strength, and architecture in vitro (13–16). Whether these same properties are measured in vivo remains to be determined. In theory, QUS measurements should reflect differences in the quantity and arrangement of trabecular and cortical tissue. The aim of this study was to evaluate whether there were differences in QUS of the calcaneus between African-American and Caucasian females.
Tylavsky et al. of reported onset of menses. A self-report of high blood pressure, osteoarthritis, or noninsulin-dependent diabetes mellitus was considered to be a comorbid condition.
Smoking History Current and past use of cigarettes was assessed using a questionnaire. The age of initiation of tobacco smoking, number of packs per week, and duration of cigarette use in years was ascertained. Pack years were calculated to represent smoking behavior.
Calcium Intake
Materials and Methods Subjects One hundred twenty-five individuals between the age of 18 and 50 yr were recruited from the Metropolitan Statistical Area surrounding Memphis, Tennessee, to participate in a study assessing normal levels of bone mass at the calcaneus using an ultrasonometer. Individuals were excluded on the basis of self-report of any condition or medication known to affect calcium metabolism including long-term immobilization, surgical menopause, chronic renal failure, chronic liver impairment, malabsorptive disorders, and the use of anticonvulsants or corticosteroids. Subjects were also excluded if they reported any atraumatic fractures. The complete data set on all variables for the 125 individuals (37 Caucasian females, 54 African-American females, 16 Caucasian males, and 18 African-American males) was used for statistical analyses in this report. Written consent for participation in the study was obtained from all subjects prior to performing ultrasound measurements. The study was approved by the Institutional Review Board of the University of Tennessee.
Menstrual, Reproductive, and Medical History Menstrual, reproductive, and medical histories were assessed by questionnaire. Report of an osteoporotic fracture or kyphosis for any family member was considered as a positive family history of osteoporosis. Chronologic age was calculated as the date of bone measurement minus the date of birth. For females the age of menarche was the age Journal of Clinical Densitometry
Usual calcium intake in milligrams/day was obtained using a 7-d food-frequency recall. This method has been shown to provide a moderate correlation with 24-h recalls, a reasonable calcium intake compared to 3-d food records, and a test-retest reliability of 0.80 (17).
Physical Activity Physical activity was assessed by self-report concerning leisure time and activities of daily living. An integrated scoring system was developed using intensity, duration, and frequency of reported activities. Subjects were considered to have low physical activity if they reported performing only those activities necessary for daily care. High physical activity was assigned to those subjects that reported engaging in leisure time activity daily, with the remaining subjects classified as having moderate levels of physical activity.
Bone Measurements QUS-1X TM, an ultrasonometer by Metra Biosystems Inc., Mountain View, CA, is a dry scanning ultrasound system. The QUS-1X used point source transducers with a frequency range of 200–800 kHz to determine attenuation (UBI-4) using Burg spectral estimation in decibels/megahertz. Burg spectral analyses estimated the parameters of an autoregressive process using maximal entropy ideas. The average transit time through the heel (TTH) is the average time interval from 600 ns after the start of capacitor discharge to the first peak of the signal in microseconds. Since the heel thickness can be calculated as a function of time, TTH can be used as an indicator for the estimation of heel Volume 2, 1999
Ethnicity and Ultrasound of the Calcaneus thickness, i.e., bone size. A multiple factor index taking into account bone size, UBI-4T, was calculated by dividing UBI-4 by TTH. The heel was placed in a foot holder between two transducers by keeping the ankle at a 90° angle. The midcalcaneus, which geometrically represents the most uniform part of the bone, was identified by taking two-thirds of the distance from the heel to the distal end of the lateral malleolus as the site of the scan. Optimal contact between the skin and transducer was ensured by a thin layer of water-based jelly. To minimize measurement error, two measurements were performed on each participant. If the differences in two measurements exceeded 10.0 dB/MHz, a third measurement was performed. The average of two measurements that were within 10.00 dB/MHz was used for reporting purposes. The coefficient of variation (CV) was determined by performing repeat measurement without repositioning. The CV of measurements was <3% from TTH and UBI-4. Similar CV’s have been reported elsewhere (14) on other QUS instruments.
Statistical Analyses All statistical analyses were performed using the Statistical Analysis System (18). Descriptive means and standard deviations (SDs) were obtained for all bone and continuous independent variables according to ethnicity and sex groupings. T-tests were used to evaluate differences in QUS parameters between the ethnic groups. No adjustment was made for the influences of comorbid disease conditions on QUS parameters between the ethnic groups owing to only one report of a comorbid disease. Fisher exact test was used to determine whether the frequency of distribution for the number of children, family history of osteoporosis, or oral contraceptive use was different between the ethnic groups.
Results Descriptive Statistics Table 1 presents means ± SD of age, height, weight, body mass index (BMI), dietary calcium intake, cigarette smoking history, and percentage positive for a family history of osteoporosis. Fisher exact test determined the observed frequency distribution of the number of biological children for Journal of Clinical Densitometry
33 Table 1 Description of Selected Characteristics for Females According to Race (Mean ± SD)a Variable
Caucasian
n 37 Age (yr) 30.1±9.4 Height (cm) 164.6±8.1 Weight (kg) 63.6±11.2 BMI (kg/cm2) 23.6 ± 4.4 Education (yr) 14.2±1.6 Smoking (pack yr) 13.1±7.9(11) Calcium intake (mg) 819±381 Family history of osteoporosis (%) 27.0a Exercise level(%) Low 43.2 Moderate 40.5 High 16.2 Biological children (%) 0 62.2 1–2 29.7 ≥3 8.1 Age of menarche (yr) 12.4±1.7 Oral contraceptive use (%) 64.9
African-American 54 26.7±8.0 163.8±7.4 71.7±16.8 26.8 ± 6.3 13.8±2.0 0.1±0.4 (2) 792±493 3.7b 54.7 39.6 5.7 44.4 44.4 11.1 12.3± 1.6 48.2
a
p<0.05 between ethnic group. Twenty percent of the Caucasian and 12% of the AfricanAmerican females reported uncertainty of the presence of a family history of osteoporosis. b
Caucasian and African-American females. A family history of osteoporosis was reported by 27% of Caucasian females, 6% of Caucasian males, and 3.7% of African-American females, and there were no reports of a positive family history of osteoporosis by males of African-American ethnicity (p < 0.001). Twenty percent of Caucasian females and 12% of African-American females reported uncertainty of the presence of a family history of osteoporosis. Only one person reported the presence of osteoarthritis as a comorbid condition. Table 2 presents the mean ± SD, minimum, and maximum values for UBI-4, TTH, and UBI-4T for Caucasian and African-American females. Caucasian females had different attenuation values for UBI-4 and TTH compared with AfricanAmerican females (p < 0.05). However, when adjusting for TTH, an indicator of bone size, the difVolume 2, 1999
34
Tylavsky et al. Table 2 QUS Parameters for the Female Study Population According to Ethnicity (Mean ± SD, Minimum and Maximum Values)
Variable n
UBI-4 (dB/MHz) Mean ± SD Minimum Maximum TTH (µs) Mean ± SD Minimum Maximum UBI-4T (dB/MHz/µs) Mean ± SD Minimum Maximum
Caucasian
African-American
37
54
96.3±11.7a 56.3 116.0
102.7±10.1a 72.3 122.0
28.9±3.0a 23.8 38.3
31.3 ± 3.2a 25.2 39.5
3.4±0.5 1.9 4.4
3.3±0.4 2.4 4.4
a Significant differences (p<0.05) between Caucasian and African-American females.
ferences in attenuation disappeared. Pilot data for males suggest that Caucasians have similar UBI-4 values but lower TTH values than African-American males (105.6 ± 9.8 vs 104.9 ± 6.4 and 30.6 ± 2.2 vs 34.5 ± 4.5, respectively).
Discussion Increased levels of BMD (3) and a geometrical difference in hip axis length are considered to be responsible, in part, for a lower risk of fracture for African-American females (19) but have not been clearly demonstrated for males (20). Our study shows that premenopausal Caucasian females have approx 6 to 7% lower values (p < 0.05) of UBI-4 and TTH than their African-American counterparts. For males, the differences in QUS indices appear to vary from 0 to 8% between ethnic groups depending on the bone parameter assessed. This is in contrast to reports of differences in BMD of the total femur by DXA, which range from 7 to 14% for young adults in the third and fourth decade (3). Only recently have ethnic differences been reported for broadband ultrasound attenuation (BUA) as assessed by QUS. A study by Cauley et al. (21) of postmenopausal females found that the difJournal of Clinical Densitometry
ferences between ethnic groups for BUA ranged from 7.5% (unadjusted) to no difference when adjusted for age, weight, height, and/or calcaneal BMD. These results imply that differences in QUS measurements are due to differences in anthropometric measurements and BMD. Although BMD estimates by DXA were not obtained in the current study, we have found that adjusting for BMD of the femoral neck had little or no impact on differences in QUS measurements performed in our other studies (22). Since there is little standardization in the ultrasonic industry, the disparity between our study and others could be owing to differences in the ultrasonometers used in the respective studies. Other factors most often cited to account for ethnic differences in bone mass are considered to be genetically expressed through skeletal size (23,24), muscle mass (5,24), bone turnover (25), and skeletal metabolism (26–28). Our study agrees with the premise that the larger skeletal size is a primary difference between African-Americans and Caucasians. TTH, an indicator of bone size, was the major difference observed between sex-matched ethnic groups. Furthermore, once bone size was taken into account the differences disappeared. In theory, this parameter can be affected by differences in microarchitecture, geometry of the bone, and the soft tissue. Some histomorphometric measurements of the iliac crest suggest that the primary differences between African-American and Caucasian females are owing to a thicker cortical shell and thicker trabeculae (7). Cross-sectional analysis of data by Han et al. (7) suggests that the number of trabeculae, the cortical porosity, and the rate of loss with age are similar across the ethnic groups. QCT of the spine provided similar results (5). Since the calcaneus is composed of 95% trabecular bone tissue with the remaining 5% representing the cortical shell, differences in QUS observed in this study could be interpreted as representing differences in trabecular tissue between the two ethnic groups. Weight-bearing loads are considered to have significant effects on the quantity of bone mass at different skeletal sites. Body height and weight produce the most consistent load-bearing effects on the calcaneus. In our sample, height, weight, or BMI was similar among the sex and ethnic groupings. Other researchers have shown that for a given weight
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Ethnicity and Ultrasound of the Calcaneus African-Americans have higher levels of lean body mass (4,29,30). In our study, we were not able to estimate whether or not levels of lean body mass influenced our results. Physical activity with high-impact loading on the calcaneus could be a differentiating factor. Although we used a physical activity questionnaire that included duration, frequency, and intensity of loadbearing activity, we were unable to see any ethnic differences in activity patterns that could contribute to differences in bone parameters. Other factors known to affect the risk of osteoporosis and impact on bone density include longterm dietary calcium (31), cigarette smoking, and reproductive history. Our study did not obtain longterm dietary calcium intake and found no differences in reported current intake. A higher percentage of Caucasian females reported smoking cigarettes and had a higher quantity of pack years. However, the differences were minimal and unlikely to impact bone mass. Both ethnic groups of females reported a similar age of menarche, which has been shown to affect BMD levels of females in the third decade (32). Both groups reported using oral contraceptives with similar frequency, and had a similar number of children. Therefore, we were unable to estimate differences because of these factors. Family history of osteoporosis, a risk factor for osteoporosis, and lower BMD was reported more frequently by Caucasians than African-Americans (p<0.001), with 9% of the African-American and 16% of the Caucasian females uncertain of its presence. This reported difference in family history of osteoporosis may be because of a genetic tendency for osteoporosis in Caucasians. Alternatively, it could reflect a lack of true awareness of the presence of osteoporosis in our research subjects. A previous report demonstrated that Caucasian females between the age of 18 and 22 yr were unable to provide information on family history of osteoporosis (31). The limited scope of our study shows that there are differences in UBI-4 and TTH when measured with the QUS IX between premenopausal Caucasian and African-American females, but not with the same magnitude as evidenced by DXA. For males, our pilot data suggest that differences between African-American and Caucasian males were smaller than those obtained by DXA. A better under-
Journal of Clinical Densitometry
35 standing of the differences in bone properties between African-Americans and Caucasians is important, and may ultimately lead to better strategies to prevent fractures. We recommend that more data be collected on ethnic differences across all age ranges, to help understand how QUS may be used to assess bone mass and to determine its value either as a screening tool or as a tool to predict osteoporotic fracture within various ethnic groups.
Acknowledgments The authors would like to acknowledge the support of Metra Biosystems, Inc. in performing this study.
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