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Smoking as a Risk Factor for Bone Mineral Density in the Heel of Japanese Men*
Journal of Clinical Densitometry, vol. 2, no. 3, 219–222, Fall 1999 © Copyright 1999 by Humana Press Inc. All rights of any nature whatsoever reserved. 0169-4194/99/2:219–222/$11.00
Original Article
Smoking as a Risk Factor for Bone Mineral Density in the Heel of Japanese Men* Satoshi Hagiwara, MD, PHD,1 and Kei Tsumura, MD, PHD.2 1Matsushita
Health Care Center, Moriguchii, Japan; 2Second Internal Medicine, Osaka City University Medical School, Osaka, Japan
Abstract Bone mineral density (BMD) of the calcaneus was measured in 1736 male Japanese office workers (age 20–64 yr) using a DX-2000 (Matsushita Industrial Equipment, Toyonaka, Japan). The scanning time was 10 s, with an in vitro precision error of 0.85% and an in vivo precision error of 1.54%. A significant gradual loss of BMD was detected between 20 and 60 yr of age, with an age difference of 0.27% per year. Significant determinants for heel BMD were body mass index, age, and smoking. A nonsignificant factor was alcohol consumption. The coefficient of determination was 30.7%. These results suggest that smoking is a risk factor for osteoporosis in middle-aged Japanese men. Key Words: Calcaneus; smoking; dual X-ray absorptiometry; bone mineral density.
preferred anatomical sites to measure bone mass using quantitative ultrasound (15–18). Few studies have described dual X-ray absorptiometry (DXA) measurements of the calcaneus (18–20). Measurement of BMD in the calcaneus using DXA can be used to predict the risk of spinal fracture (19). However, these studies were performed in women with osteoporosis, and limited data are available for BMD of the heel in men. It usually takes more than 3 min to perform a series of measurements using the existing DXA machines. A new, fast DXA machine is now available to measure the BMD in the heel. The objectives of this cross-sectional study were to evaluate the precision of the new DXA machine, and to assess the determinants of BMD of the heel in male Japanese office workers.
Introduction Osteoporosis is a serious condition in the elderly. The incidence of osteoporosis in men is approximately one-half that in women, which is much more common than previously considered (1,2). The incidence of hip fracture in men is almost one-third that in women (3). The main causes of fracture in men include alcohol abuse, steroid excess, and hypogonadism, as well as primary osteoporosis (4). Although smoking is a risk factor for osteoporosis in women, this factor remains controversial in men (5–7). Bone mineral density (BMD) is useful to assess fracture risk (8). A variety of methods are currently available to measure BMD at various anatomical sites (9–14). The calcaneus is one of the
Materials and Methods
Received 10/15/98; Revised 02/03/99; Accepted 02/25/99. Address correspondence to Dr. Satoshi Hagiwara, Chief, Health Service Station, Corporate Production Engineering Division, Matsushita Electric Industrial Co. Ltd., 2–7 Matsubacho, Kadoma 571–8502 Japan. E-mail: [email protected]
There were 1812 adult male subjects in this study. All were office workers between 20 and 64 yr of age. Table 1 presents the demographic data. Subjects with
219
220
Hagiwara and Tsumura
Table 1 Demographic Dataa
Number Age (yr) Height (cm) Weight (kg) a
All subjects
Number tested
1812 39.4 ± 10.6 169.5 ± 6.0 66.9 ± 9.6
1736 39.1 ± 10.4 169.7 ± 5.9 66.6 ± 9.5
Data are expressed as mean ± SD.
Table 2 Significance of Differences Between the Highest and Lowest Quintilesa
BMD Age (yr) BMI Smokingb Alcoholc
Highest
Lowest
p valued
1.058 ± 0.046 36.6 ± 9.9 24.9 ± 3.0 10.2 ± 15.2 25.4 ± 16.0
0.793 ± 0.058 42.0 ± 10.9 21.0 ± 2.4 13.8 ± 16.6 24.6 ± 18.2
<0.001 <0.001 <0.001 <0.001 NS
Data are expressed as mean ± SD. Pack-years. c Alcohol consumed per week (in ethanol). d NS, not significant. a b
Fig. 1. Age-related bone loss. BMD of the heel shows a significant age difference. The difference was found to be 0.27% less per year. Data are expressed as mean ± 2 SDs.
metabolic bone disease, those receiving medication that influenced calcium metabolism, or those who did not give informed consent to participate in the examination were excluded. The BMD of the right heel was measured in 1736 men using a Heelscan DX-2000 (Matsushita Industrial Equipment, Toyonaka, Japan). According to the instructions in the manufacturer’s manual, the subject placed his right foot encased in a sock on the machine. Ten seconds were required to obtain the measurement and 50 s to cool off the machine. Precision was evaluated in vitro and in vivo by obtaining measurements six times after repositioning. The manufacturer provided a phantom for in vitro measurement. In vivo precision error was Journal of Clinical Densitometry
assessed in five volunteers by obtaining measurements six times after repositioning. Height and weight of the subjects were measured on the same day. Information concerning smoking habits (number of packs of cigarettes smoked per day per year times the number of years or pack-years) and alcohol consumption (type, volume, and frequency per week) was obtained during an interview by a physician at the time of examination. Alcohol consumption per week in ethanol was calculated using a standard conversion table. Current smokers constituted 48.8% of all subjects, ex-smokers 15.7%, and nonsmokers 35.5%.
Statistical Analysis Linear regression analysis was used to evaluate age-related changes. Differences among group means were compared with the Student t-test. Multiple regression analysis was used to assess the determinants of BMD. p < 0.05 was considered significant.
Results In vitro short-term precision error was 0.85%, and in vitro day-to-day coefficient of variation (CV) was 0.94%. In vivo CV was 1.54 ± 0.28%. The cross-sectional data indicated that the BMD of the calcaneus was lower in old adults (Fig. 1). A significant difference of 0.27% less per year was detected. Table 2 gives the difference between the highest and lowest BMD quintiles. Men in the highest BMD quintile were significantly younger, had a higher body mass index (BMI) and lower mean pack-years history than Volume 2, 1999
Smoking and BMD in the Heel of Japanese Men
Table 3 Factors Contributing to BMD of the Heela
BMI Age (yr) Smokingb Alcoholc
β
p valued
0.468 –0.251 –0.079 0.024
<0.001 <0.001 <0.05 NS
a
Coefficient of determination is 30.7%. Pack-years. c Alcohol consumed per week (in ethanol). d NS, not significant. b
men in the lowest quintile. BMI, age, and smoking (pack-years) were significant determinants for heel BMD. A nonsignificant factor was alcohol consumption (Table 3). The coefficient of determination was 30.7%.
Discussion The new heel DXA machine showed a low precision error, which was similar to that previously reported (18). According to the Japanese health insurance system, one such measurement costs 1800 JPY ($13.3 U.S.$). This cost is half that of measuring lumbar spine BMD with DXA (3600 JPY or $26.7 U.S.$). Another advantage is the rapid scanning time. One minute is sufficient to complete the entire measurement, which is faster than other instruments used for this purpose. In terms of recent concept (21,22), this DXA machine can be used to screen for osteoporosis. Since the health-screening system including BMD measurement is quite popular in Japan, the fast scanning time is a significant benefit. The difference of 0.27% less per year determined in this cross-sectional study is similar to rates previously reported (23,24), although the sites of measurement and/or the methods differ. Since this study was cross-sectional, various factors such as year of birth, nutritional practices, and economic conditions influenced the results. The age trend may have been affected by the cohort effect. Longitudinal studies are needed to confirm age-related bone loss. The highest quintile in BMD showed a younger age, larger BMI, and lower smoking score (packyears) compared with the lowest quintile. Alcohol consumption was not significantly related to BMD. Journal of Clinical Densitometry
221 Significant risk factors for heel BMD were BMI, age, and smoking. However, the influence of smoking on heel BMD was less than that of BMI and age. Lower weight has been shown to contribute to the low bone mass in women who smoked (25). However, we observed no significant difference in body weight or BMI between smokers and nonsmokers. No difference in BMD was found between subjects who stopped smoking and those who continued to smoke (data not shown). Of course, numerous factors such as exercise, dietary calcium intake, and other lifestyle variables are potential covariates that may affect the bone. Further study is necessary to evaluate the influence of these factors. Previously, the diagnosis of osteoporosis was made based on the presence of spinal fracture(s). According to the recent criteria issued by the World Health Organization, osteoporosis can be defined by BMD measurement of the spine (3). Although no criteria of osteoporosis have been established for calcaneus BMD, the presence of fracture(s) was not always necessary for the diagnosis of osteoporosis. Other studies have shown that alcohol abuse is a frequent cause of osteoporosis in men (26,27). One reason that our study did not show a significant influence was the small number of subjects who consumed large amounts of alcohol. Moreover, we examined the biochemical findings in a subset of subjects; however, no significant liver dysfunction was detected (data not shown). The results from other studies were compatible with our findings. Interestingly, Holbrook and Barrett-Connor (28) indicated that a modest alcohol intake may increase bone density. In summary, our study results indicate that smoking is a risk factor for osteoporosis in men as well as BMI and age. The new DXA machine for the calcaneus can be used as a screening method for osteoporosis that shows low precision error and allows rapid scanning time.
Acknowledgments We acknowledge Professor Harry K. Genant, M.D., Department of Radiology, University of California San Francisco, for his helpful comments. We also thank Yomiko Tanabe, R.N. and Kyoko Nitta, R.N. for their technical assistance. Volume 2, 1999
222
References 1. Cooper C, Atkinson EJ, O’Fallon WM, Melton LJ III. 1992 Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985–1989. J Bone Miner Res 7:221–227. 2. Johansson C, Mellstroem D, Rosengren K, Rundgren A. 1994 A community-based population study of vertebral fractures in 85-year-old men and women. Age Ageing 23:388–392. 3. Kanis JA, Melton LJ III, Christiansen C, Johnston CC, Khaltaev N. 1994 The diagnosis of osteoporosis. J Bone Miner Res 9:1137–1141. 4. Orwell ES, Klein RF. 1995 Osteoporosis in men. Endocr Rev 16:298–327 5. Cummings RG, Klineberg RJ. 1994 Case-control study of risk factors for hip fractures in the elderly. Am J Epidemiol 139:493–503 6. Resch A, Scheinder B, Bernecker P, Battmann A, Wergedal J, Willvonseder R, Resch H. 1995 Risk of vertebral fractures in men: relationship to mineral density of vertebral body. AJR 164:1447–1450 7. Mann T, Oviatt SK, Wilson D, Nelson D, Orwoll ES. 1992 Vertebral deformity in men. J Bone Miner Res 7:1259–1265 8. Cummings SR, Kelsey JL, Nevitt MC, O’Dowd KJ. 1985 Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev 7:178–208 9. Cosman F, Herrington B, Himmelstein S, Lindsay R. 1991 Radiographic absorptiometry: a simple method for determination of bone mass. Osteoporos Int 2:34–38 10. Cameron JR, Sorenson J. 1963 Measurement of bone mineral in vivo: an improved method. Science 142:230–232. 11. Peppler WW, Mazess RB. 1981 Total body bone mineral and lean body mass by dual photon absorptiometry, I: theory and measurement procedure. Calcif Tissue Int 33:353–359. 12. Kelly TL, Slovick DM, Schoenfield DA, Neer RM. 1987 Quantitative digital radiography versus dual photon absorptiometry of the lumbar spine. J Clin Endocrinol Metab 67:839–844. 13. Cann CE, Genant HK. 1983 Single versus dual-energy CT for vertebral mineral quantification. J Comput Assist Tomogr 7:551, 552. 14. Langton CM, Palmer SB, Porter RW. 1984 The measurement of broadband ultrasonic attenuation in calcaneus bone. N Engl J Med 13:89–91.
Journal of Clinical Densitometry
Hagiwara and Tsumura 15. Bouxsein ML, Radloff SE. 1997 Quantitative ultrasound of the calcaneus reflects the mechanical properties of calcaneal trabecular bone. J Bone Miner Res 12:839–846. 16. Glüer CC. For the International Quantitative Ultrasound Consensus Group. 1997 Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. J Bone Miner Res 12:1280–1288. 17. Njeh CF, Boivin CM, Langton CM. 1997 The role of ultrasound in the assessment of osteoporosis: a review. Osteoporos Int 7:7–22. 18. Greenspan SL, Bouxsein ML, Melton ME, Kolodny AH, Clair JH, Pelucca PT, et al. 1997 Precision and discriminatory ability of calcaneal bone assessment technologies. J Bone Miner Res 12:1303–1313. 19. Yamada M, Ito M, Hayashi K, Ohki M, Nakamura T. 1994 Dual energy x-ray absorptiometry of the calcaneus: comparison with other techniques to assess bone density and value in predicting risk of spine fracture. AJR 163:1435–1440. 20. Brooke-Wavell K, Jones PR, Pye DW. 1995 Ultrasound and dual x-ray absorptiometry measurement of the calcaneus: influence of region of interest location. Calcif Tissue Int 57:20–24. 21. Grampp S, Genant HK, Mathur A, Lang P, Jergas M, Takada M, et al. 1997 Comparisons of noninvasive bone mineral measurements in assessing age-related loss, fracture discrimination, and diagnostic classification. J Bone Miner Res 12:697–711. 22. Kleerekoper M, Nelson DA. 1997 Which bone density measurement? J Bone Miner Res 12:712–714. 23. Hagiwara S, Miki T, Nishizawa Y, Ochi H, Onoyama Y, Morii H. 1989 Quantification of bone mineral content using dual-photon absorptiometry in a normal Japanese population. J Bone Miner Res 4:217–222. 24. Mazess RB, Barden HS, Drinka PH, Bauwens SF, Orwoll ES, Bell NH. 1990 Influence of age and body weight on spine and femur bone mineral density in US white men. J Bone Miner Res 5:645–652. 25. Krall EA, Dawson-Hughes B. 1991 Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338. 26. Peris P, Guanabens N, Monegal A, et al. 1995 Aetiology and presenting symptoms in male osteoporosis. Br J Rheumatol 34:936–941. 27. Khosla S, Lufkin EG, Hodgson SF, Fitzpatrick LA, Melton LJ III. 1994 Epidemiology and clinical features of osteoporosis in young individuals. Bone 15:551–555. 28. Holbrook TL, Barrett-Connor E. 1993 A prospective study of alcohol consumption and bone mineral density. Br Med J 306:1506–1509.
Volume 2, 1999
Original Article
Smoking as a Risk Factor for Bone Mineral Density in the Heel of Japanese Men* Satoshi Hagiwara, MD, PHD,1 and Kei Tsumura, MD, PHD.2 1Matsushita
Health Care Center, Moriguchii, Japan; 2Second Internal Medicine, Osaka City University Medical School, Osaka, Japan
Abstract Bone mineral density (BMD) of the calcaneus was measured in 1736 male Japanese office workers (age 20–64 yr) using a DX-2000 (Matsushita Industrial Equipment, Toyonaka, Japan). The scanning time was 10 s, with an in vitro precision error of 0.85% and an in vivo precision error of 1.54%. A significant gradual loss of BMD was detected between 20 and 60 yr of age, with an age difference of 0.27% per year. Significant determinants for heel BMD were body mass index, age, and smoking. A nonsignificant factor was alcohol consumption. The coefficient of determination was 30.7%. These results suggest that smoking is a risk factor for osteoporosis in middle-aged Japanese men. Key Words: Calcaneus; smoking; dual X-ray absorptiometry; bone mineral density.
preferred anatomical sites to measure bone mass using quantitative ultrasound (15–18). Few studies have described dual X-ray absorptiometry (DXA) measurements of the calcaneus (18–20). Measurement of BMD in the calcaneus using DXA can be used to predict the risk of spinal fracture (19). However, these studies were performed in women with osteoporosis, and limited data are available for BMD of the heel in men. It usually takes more than 3 min to perform a series of measurements using the existing DXA machines. A new, fast DXA machine is now available to measure the BMD in the heel. The objectives of this cross-sectional study were to evaluate the precision of the new DXA machine, and to assess the determinants of BMD of the heel in male Japanese office workers.
Introduction Osteoporosis is a serious condition in the elderly. The incidence of osteoporosis in men is approximately one-half that in women, which is much more common than previously considered (1,2). The incidence of hip fracture in men is almost one-third that in women (3). The main causes of fracture in men include alcohol abuse, steroid excess, and hypogonadism, as well as primary osteoporosis (4). Although smoking is a risk factor for osteoporosis in women, this factor remains controversial in men (5–7). Bone mineral density (BMD) is useful to assess fracture risk (8). A variety of methods are currently available to measure BMD at various anatomical sites (9–14). The calcaneus is one of the
Materials and Methods
Received 10/15/98; Revised 02/03/99; Accepted 02/25/99. Address correspondence to Dr. Satoshi Hagiwara, Chief, Health Service Station, Corporate Production Engineering Division, Matsushita Electric Industrial Co. Ltd., 2–7 Matsubacho, Kadoma 571–8502 Japan. E-mail: [email protected]
There were 1812 adult male subjects in this study. All were office workers between 20 and 64 yr of age. Table 1 presents the demographic data. Subjects with
219
220
Hagiwara and Tsumura
Table 1 Demographic Dataa
Number Age (yr) Height (cm) Weight (kg) a
All subjects
Number tested
1812 39.4 ± 10.6 169.5 ± 6.0 66.9 ± 9.6
1736 39.1 ± 10.4 169.7 ± 5.9 66.6 ± 9.5
Data are expressed as mean ± SD.
Table 2 Significance of Differences Between the Highest and Lowest Quintilesa
BMD Age (yr) BMI Smokingb Alcoholc
Highest
Lowest
p valued
1.058 ± 0.046 36.6 ± 9.9 24.9 ± 3.0 10.2 ± 15.2 25.4 ± 16.0
0.793 ± 0.058 42.0 ± 10.9 21.0 ± 2.4 13.8 ± 16.6 24.6 ± 18.2
<0.001 <0.001 <0.001 <0.001 NS
Data are expressed as mean ± SD. Pack-years. c Alcohol consumed per week (in ethanol). d NS, not significant. a b
Fig. 1. Age-related bone loss. BMD of the heel shows a significant age difference. The difference was found to be 0.27% less per year. Data are expressed as mean ± 2 SDs.
metabolic bone disease, those receiving medication that influenced calcium metabolism, or those who did not give informed consent to participate in the examination were excluded. The BMD of the right heel was measured in 1736 men using a Heelscan DX-2000 (Matsushita Industrial Equipment, Toyonaka, Japan). According to the instructions in the manufacturer’s manual, the subject placed his right foot encased in a sock on the machine. Ten seconds were required to obtain the measurement and 50 s to cool off the machine. Precision was evaluated in vitro and in vivo by obtaining measurements six times after repositioning. The manufacturer provided a phantom for in vitro measurement. In vivo precision error was Journal of Clinical Densitometry
assessed in five volunteers by obtaining measurements six times after repositioning. Height and weight of the subjects were measured on the same day. Information concerning smoking habits (number of packs of cigarettes smoked per day per year times the number of years or pack-years) and alcohol consumption (type, volume, and frequency per week) was obtained during an interview by a physician at the time of examination. Alcohol consumption per week in ethanol was calculated using a standard conversion table. Current smokers constituted 48.8% of all subjects, ex-smokers 15.7%, and nonsmokers 35.5%.
Statistical Analysis Linear regression analysis was used to evaluate age-related changes. Differences among group means were compared with the Student t-test. Multiple regression analysis was used to assess the determinants of BMD. p < 0.05 was considered significant.
Results In vitro short-term precision error was 0.85%, and in vitro day-to-day coefficient of variation (CV) was 0.94%. In vivo CV was 1.54 ± 0.28%. The cross-sectional data indicated that the BMD of the calcaneus was lower in old adults (Fig. 1). A significant difference of 0.27% less per year was detected. Table 2 gives the difference between the highest and lowest BMD quintiles. Men in the highest BMD quintile were significantly younger, had a higher body mass index (BMI) and lower mean pack-years history than Volume 2, 1999
Smoking and BMD in the Heel of Japanese Men
Table 3 Factors Contributing to BMD of the Heela
BMI Age (yr) Smokingb Alcoholc
β
p valued
0.468 –0.251 –0.079 0.024
<0.001 <0.001 <0.05 NS
a
Coefficient of determination is 30.7%. Pack-years. c Alcohol consumed per week (in ethanol). d NS, not significant. b
men in the lowest quintile. BMI, age, and smoking (pack-years) were significant determinants for heel BMD. A nonsignificant factor was alcohol consumption (Table 3). The coefficient of determination was 30.7%.
Discussion The new heel DXA machine showed a low precision error, which was similar to that previously reported (18). According to the Japanese health insurance system, one such measurement costs 1800 JPY ($13.3 U.S.$). This cost is half that of measuring lumbar spine BMD with DXA (3600 JPY or $26.7 U.S.$). Another advantage is the rapid scanning time. One minute is sufficient to complete the entire measurement, which is faster than other instruments used for this purpose. In terms of recent concept (21,22), this DXA machine can be used to screen for osteoporosis. Since the health-screening system including BMD measurement is quite popular in Japan, the fast scanning time is a significant benefit. The difference of 0.27% less per year determined in this cross-sectional study is similar to rates previously reported (23,24), although the sites of measurement and/or the methods differ. Since this study was cross-sectional, various factors such as year of birth, nutritional practices, and economic conditions influenced the results. The age trend may have been affected by the cohort effect. Longitudinal studies are needed to confirm age-related bone loss. The highest quintile in BMD showed a younger age, larger BMI, and lower smoking score (packyears) compared with the lowest quintile. Alcohol consumption was not significantly related to BMD. Journal of Clinical Densitometry
221 Significant risk factors for heel BMD were BMI, age, and smoking. However, the influence of smoking on heel BMD was less than that of BMI and age. Lower weight has been shown to contribute to the low bone mass in women who smoked (25). However, we observed no significant difference in body weight or BMI between smokers and nonsmokers. No difference in BMD was found between subjects who stopped smoking and those who continued to smoke (data not shown). Of course, numerous factors such as exercise, dietary calcium intake, and other lifestyle variables are potential covariates that may affect the bone. Further study is necessary to evaluate the influence of these factors. Previously, the diagnosis of osteoporosis was made based on the presence of spinal fracture(s). According to the recent criteria issued by the World Health Organization, osteoporosis can be defined by BMD measurement of the spine (3). Although no criteria of osteoporosis have been established for calcaneus BMD, the presence of fracture(s) was not always necessary for the diagnosis of osteoporosis. Other studies have shown that alcohol abuse is a frequent cause of osteoporosis in men (26,27). One reason that our study did not show a significant influence was the small number of subjects who consumed large amounts of alcohol. Moreover, we examined the biochemical findings in a subset of subjects; however, no significant liver dysfunction was detected (data not shown). The results from other studies were compatible with our findings. Interestingly, Holbrook and Barrett-Connor (28) indicated that a modest alcohol intake may increase bone density. In summary, our study results indicate that smoking is a risk factor for osteoporosis in men as well as BMI and age. The new DXA machine for the calcaneus can be used as a screening method for osteoporosis that shows low precision error and allows rapid scanning time.
Acknowledgments We acknowledge Professor Harry K. Genant, M.D., Department of Radiology, University of California San Francisco, for his helpful comments. We also thank Yomiko Tanabe, R.N. and Kyoko Nitta, R.N. for their technical assistance. Volume 2, 1999
222
References 1. Cooper C, Atkinson EJ, O’Fallon WM, Melton LJ III. 1992 Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985–1989. J Bone Miner Res 7:221–227. 2. Johansson C, Mellstroem D, Rosengren K, Rundgren A. 1994 A community-based population study of vertebral fractures in 85-year-old men and women. Age Ageing 23:388–392. 3. Kanis JA, Melton LJ III, Christiansen C, Johnston CC, Khaltaev N. 1994 The diagnosis of osteoporosis. J Bone Miner Res 9:1137–1141. 4. Orwell ES, Klein RF. 1995 Osteoporosis in men. Endocr Rev 16:298–327 5. Cummings RG, Klineberg RJ. 1994 Case-control study of risk factors for hip fractures in the elderly. Am J Epidemiol 139:493–503 6. Resch A, Scheinder B, Bernecker P, Battmann A, Wergedal J, Willvonseder R, Resch H. 1995 Risk of vertebral fractures in men: relationship to mineral density of vertebral body. AJR 164:1447–1450 7. Mann T, Oviatt SK, Wilson D, Nelson D, Orwoll ES. 1992 Vertebral deformity in men. J Bone Miner Res 7:1259–1265 8. Cummings SR, Kelsey JL, Nevitt MC, O’Dowd KJ. 1985 Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev 7:178–208 9. Cosman F, Herrington B, Himmelstein S, Lindsay R. 1991 Radiographic absorptiometry: a simple method for determination of bone mass. Osteoporos Int 2:34–38 10. Cameron JR, Sorenson J. 1963 Measurement of bone mineral in vivo: an improved method. Science 142:230–232. 11. Peppler WW, Mazess RB. 1981 Total body bone mineral and lean body mass by dual photon absorptiometry, I: theory and measurement procedure. Calcif Tissue Int 33:353–359. 12. Kelly TL, Slovick DM, Schoenfield DA, Neer RM. 1987 Quantitative digital radiography versus dual photon absorptiometry of the lumbar spine. J Clin Endocrinol Metab 67:839–844. 13. Cann CE, Genant HK. 1983 Single versus dual-energy CT for vertebral mineral quantification. J Comput Assist Tomogr 7:551, 552. 14. Langton CM, Palmer SB, Porter RW. 1984 The measurement of broadband ultrasonic attenuation in calcaneus bone. N Engl J Med 13:89–91.
Journal of Clinical Densitometry
Hagiwara and Tsumura 15. Bouxsein ML, Radloff SE. 1997 Quantitative ultrasound of the calcaneus reflects the mechanical properties of calcaneal trabecular bone. J Bone Miner Res 12:839–846. 16. Glüer CC. For the International Quantitative Ultrasound Consensus Group. 1997 Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. J Bone Miner Res 12:1280–1288. 17. Njeh CF, Boivin CM, Langton CM. 1997 The role of ultrasound in the assessment of osteoporosis: a review. Osteoporos Int 7:7–22. 18. Greenspan SL, Bouxsein ML, Melton ME, Kolodny AH, Clair JH, Pelucca PT, et al. 1997 Precision and discriminatory ability of calcaneal bone assessment technologies. J Bone Miner Res 12:1303–1313. 19. Yamada M, Ito M, Hayashi K, Ohki M, Nakamura T. 1994 Dual energy x-ray absorptiometry of the calcaneus: comparison with other techniques to assess bone density and value in predicting risk of spine fracture. AJR 163:1435–1440. 20. Brooke-Wavell K, Jones PR, Pye DW. 1995 Ultrasound and dual x-ray absorptiometry measurement of the calcaneus: influence of region of interest location. Calcif Tissue Int 57:20–24. 21. Grampp S, Genant HK, Mathur A, Lang P, Jergas M, Takada M, et al. 1997 Comparisons of noninvasive bone mineral measurements in assessing age-related loss, fracture discrimination, and diagnostic classification. J Bone Miner Res 12:697–711. 22. Kleerekoper M, Nelson DA. 1997 Which bone density measurement? J Bone Miner Res 12:712–714. 23. Hagiwara S, Miki T, Nishizawa Y, Ochi H, Onoyama Y, Morii H. 1989 Quantification of bone mineral content using dual-photon absorptiometry in a normal Japanese population. J Bone Miner Res 4:217–222. 24. Mazess RB, Barden HS, Drinka PH, Bauwens SF, Orwoll ES, Bell NH. 1990 Influence of age and body weight on spine and femur bone mineral density in US white men. J Bone Miner Res 5:645–652. 25. Krall EA, Dawson-Hughes B. 1991 Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338. 26. Peris P, Guanabens N, Monegal A, et al. 1995 Aetiology and presenting symptoms in male osteoporosis. Br J Rheumatol 34:936–941. 27. Khosla S, Lufkin EG, Hodgson SF, Fitzpatrick LA, Melton LJ III. 1994 Epidemiology and clinical features of osteoporosis in young individuals. Bone 15:551–555. 28. Holbrook TL, Barrett-Connor E. 1993 A prospective study of alcohol consumption and bone mineral density. Br Med J 306:1506–1509.
Volume 2, 1999