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Bone density in white Brazilian women: Rapid loss at the time around the menopause

Bone density in white Brazilian women: Rapid loss at the time around the menopause
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  Calcif Tissue Int (1995) 56:186-191 SLIP aJ 9 1995 Springer-Verlag New York Inc. Bone Density in White Brazilian Women: Rapid Loss at the Time Around the Menopause V. L. Szejnfeld, 1 E. Atra, 1 E. C. Baracat, 1 J. M. Aldrighi, 2 R. Civitelli 3 IDivision of Rheumatology, Escola Paulista de Medicina, Rua Botucatu, 140, Silo Panlo, SP, Brazil 2Division of Gynecology, Departments of Medicine and Obstetrics and Gynecology, Escola Paulista de Medicina, Silo Paulo, Brazil 3Division of Bone and Mineral Diseases, Washington University School of Medicine at the Jewish Hospital, 216 S. Kingshighway Blvd., St. Louis, Missouri, 63110 USA Received: 29 April 1994 / Accepted: 4 October 1994 Abstract. Dual energy x-ray absorptiometry (DXA) was used to measure bone mineral density (BMD) of the lumbar spine and proximal femur (neck, Ward's triangle, and tro- chanter) in 417 normal women (aged 20-79) living in S~o Paulo, Brazil. Bone density decreased with age at all sites. At the spine, the greatest decrease occurred during the sixth decade, with an average 11.4% bone loss compared with the previous decade. Stratifying the subjects according to meno- pausal status revealed that the fastest bone loss occurred at the time around the menopause (ages 45-60) when the rate of bone loss (-0.66%/year) was almost twice as rapid as in postmenopausal women (-0.39%/year). Although signifi- cant linear rates of bone loss were detected in all proximal femur sites before the menopause, a menopause-dependent pattern was less evident than at the spine. Lifetime rates of bone loss at the appendicular skeleton were -0.43, -0.62, and -0.35%/year at the femoral neck, Ward's triangle, and trochanteric area, respectively. After the menopause, BMD declined with menopausal age at all sites, although the rate of bone loss was faster at the femoral neck (-0.62%/year) and Ward's triangle (-0.84%/year) than at the spine (-0.49%/year). The results are consistent with the notion that in women, the fastest bone loss occurs at the time around the menopause, most likely consequent to ovarian failure; and that faster rates of bone loss are detected at the proximal femur than at the lumbar spine in late postmeno- pausal women. Key words: Bone mineral density -- Dual energy X-ray ab- sorptiometry -- Osteoporosis -- Menopause. than other ethnic groups [7, 10]. In addition to the genetic potential, environmental factors also play a significant role in determining bone density in single individuals and in peo- ple living in specific geographical areas. For example, sib- lings of Japanese immigrants born in the United States were found to have higher bone densities than Japan-born immi- grants [11]. Therefore, the diagnostic value of bone mass measurements in a determined population living in a certain geographical location is heavily dependent on the knowledge of historical data obtained in healthy subjects living under the same environmental conditions and with similar ethnic characteristics. Deviations from normative values can thus be used to assess the risk of fractures, and to establish the need of therapeutic interventions. Although bone density of white populations of diverse ethnic srcin can be reasonably compared [12, 13], data on age-related distributions of bone density in predominantly Latin-American populations are still scanty. Normative data for Argentinean women have been reported [14], and only one study has compared bone mineral density (BMD) of the spine and proximal femur between healthy young women and postmenopausal osteoporotic patients in subjects living in Brazil [15]. However, that study did not provide numeri- cal data that could be used as normative reference values of bone density according to age groups in Brazilian female populations. This study was aimed at establishing normal reference values for vertebral and proximal femur bone density, and at defining patterns of age-related bone loss in Caucasian women living in an area of southern Brazil using dual energy x-ray absorptiometry (DXA). Bone mass is the most important factor for the skeleton to support the load of the body, and to withstand the stress of everyday life [1, 2]. Although bone density can be measured with good precision, the wide interracial variability in bone mass precludes the use of single normative data. People of African srcin have higher bone density [3-6] and fewer os- teoporotic fractures [7, 8] than age- and weight-matched whites. Furthermore, blacks attain a higher peak bone mass compared with Caucasians, probably because of a greater bone density growth at puberty [91. Likewise, people of Asian srcin are thought to be at increased risk for fractures Correspondence to V. L. Szejnfeld Materials and Methods Experimental Subjects Normal Brazilian women, all residents of Sgo Paulo city (southwest- ern Brazil), served as subjects for this study. The sample was com- prised of Caucasian females, all born in Brazil, in good health from 20 to 79 years of age. Most of the subjects were recruited from three different outpatient clinics in the area. These subjects were healthy women undergoing routine gynecological examinations and/or phys- ical examinations. The youngest subjects (20-29 years) were volun- teers recruited among medical students attending the Escola Paulista de Medicina. Each subject underwent a medical interview to verify inclusion/exclusion criteria before undergoing a complete physical examination and bone density measurement.  V. L. Szejnfeld et al.: 187 one Density in Brazilian Women Table 1. Clinical and demographic characteristics of 417 normal Brazilian women living in the Silo Paul, area Age Weight Height BMI YSM (years) n (kg) (m) (g/m z) (years) 20-29 27 54.8 -+ 5.9 1.61 ---- 0.1 20.9 +-_1.7 0 30-39 47 58.0 -+ 6.3 1.60 -+ 0.1 22.6 _+ 2.1 0 40--49 126 63.2 -+ 8.5 1.60 -+ 0.1 24.5 -- 3.1 0.3 +- 1.1 50-59 138 64.0 +-- 8.1 1.58 -+ 0.1 25.5 -+ 3.1 4.5 -+ 4.3 60-69 61 63.4 -+ 8.1 1.55 -+ 0.1 26.4 -- 3.5 14.4 -+ 5.8 70-79 18 64.1 -+ 7.7 1.54 -+ 0.1 27.0 - 3.1 22.9 -+ 5.7 BMI = body mass index; YSM = years since menopause Data represent the mean -+ SD Table 2. Spine and proximal femur bone mineral density of 418 normal Brazilian women strat- ified by decade Spine Neck Ward Trochanter Age (years) n (g/cm 2) 20-29 27 1.18 -+ 0.14 0.95 --. 0.12 0.90 -+ 0.15 0.79 --- 0.14 30-39 47 1.17 -+ 0.11 0.89 -+ 0.08 0.82 --- 0.10 0.75 -+ 0.08 40--49 126 1.14 -+ 0.12 0.89 -+ 0.09 0.79 +- 0.12 0.73 -4- 0.09 50-59 138 1.01 -+ 0.14 0.83 --- 0.10 0.70 +- 0.13 0.69 --- 0.10 60-69 61 0.94 -+ 0.14 0.77 --+- 0.11 0.64 +- 0.13 0.66 - 0.12 70-79 18 0.95 -+ 0.16 0.75 -+ 0.10 0.60 +- 0.12 0.65 -+ 0.10 Data represent the mean -+ SD 1.5 E o r "EL 03 I >, 0~ 1.0 o a3 0.5 o o o o 9 9 o o o o o o o 9 o o o o o,~e o a a o o o 0 9 ea a I= ooo o OOo~,:,ff_g~Oo=~%.o . o o o 9 a . ~1 O~o ... o_~ ~o~_~,~.g . = ~ ~ o o og o~,~i~.;-=..*=~..:_~~ =~~ .~ ~ o -=~ 9 *0 =~b'+'B-.d~.. = a * = a o o8o ~ o e_.===e=lt~i. i....~... ~ o aaa aaa -a ....... |g.=g~. Ba ~ . -. 9 - H a I1=1~ a o 9 aa a* a aaaa ga a o a at ~ a a. a a o a a* * = I I I I. I I I 20 30 40 50 60 70 80 Age (years) Fig. 1. BMD of the lumbar spine against age in 418 normal white Brazilian women. Separate regression lines are illustrated for pre- menopausal (9 perimenopausal (O), and postmenopausal ([]) sub- jects. In order to only recruit normal subjects, the following exclusion criteria were applied: evidence of radiologically determined osteo- porotic fractures; radiologically evident osteopenia; history of pathological conditions known to interfere with bone metabolism; history or evidence of malignancy; intake of medications known to affect bone mineral metabolism (corticosteroids, diuretics, anticon- vulsants, heparin, vitamin D metabolites, calcium supplements, alu- minum containing antacids); use of oral contraceptives at any time in life; use of estrogen at any time after the menopause; body weight over 90 kg or body mass index (BMI)--defined as weight (kg) di- vided by the square of the height (,2)---above 30, which was con- sidered the upper limit of normal [16]; excessive consumption of tobacco (more than 10 cigarettes/day) and/or alcohol (more than two drinks/day); premature menopause (before 40 years of age); history of oophorectomy. Although athletes were excluded, the level of physical activity was not controlled for. Similarly, the nutritional intake of calcium and vitamin D and the average daily sunlight ir- radiation were not used as selection criteria. Menopausal status was defined as follows: premenopausal, sub- jects with regular menstrual cycles; postmenopausal, subjects with- out menses for 1 year or more; perimenopausal, women with oligo- menhorrea, or amenorrhea for less than 1 year. A total of 1146 women were screened. Of these, 68 were ex- cluded because of premature menopause (before age 40), 124 be- cause of surgical menopause. Thirty-one had a previous history of malignancy, and 506 had a history positive for one of the other exclusion criteria. Therefore, the final population consisted of 417 women. Measurement of Bone Mass Bone mineral density (g/cm z) of the lumbar spine (vertebral bodies of L2-L4) and of the proximal femur (neck, Ward's triangle, and trochanteric area) was measured using the DXA unit, Lunar DPX (Lunar Radiation Corporation, Madison, WI). The published preci- sion for spine and femur BMD measurements in vivo is 1% [17]. In our institution, the coefficient of variation is 1.82 for the spine, 3.0% for the femoral neck, 3.5% for the Ward's triangle, and 3.1% for the trochanteric area [18]. All measurements were performed by only one investigator (VLS) to minimize the effect of interoperator vari- ability. Statistical Analysis Linear and higher-order regression models were applied to study the patterns of age-related bone loss. The role of menopause was inves- tigated by calculating separate regression lines for the three groups of subjects, stratified by menopausal status. Patterns of cross- sectional postmenopausal bone loss were determined for each group and for the entire population by regressing bone density against age or years since menopause (YSM). In each subset, yearly percent changes in bone density were calculated by normalizing the slopes of the regression lines to the estimated average BMD corresponding to the age of the youngest subject. The effect of body mass on  188 V. L. Szejnfeld et al.: Bone Density in Brazilian Women Table 3. Linear regression models for menopause-related bone loss in Brazilian women: lum- bar spine n Model SEE r % Loss/year Premenopaasai 176 1.2115--0,0015 age 0.1260 -0.11 0.12 Perimenopaasal 42 1.6495-0.0108 age 0.1335 -0.32 ~ 0.66 Postmenopausal 199 1,2290-0.0043 x age 0.1411 -0.21 ~ 0.39 Overall 417 1.3937-0.0064 age 0.1403 -0.50 a 0,46 SEE: standard error of estimate a Slope different than 0 at 95% confidence limit age-related bone density was estimated by partial correlation anal- yses. Regression models were considered significant at the 95% con- fidence level. Data were analyzed using a statistical package (Stat- graphics, vers. 5.0, Manugistics, Inc., Rockville, MD). Results The clinical and demographic characteristics of the study population are shown in Table 1. With age, there was an increase of BMI consequent to the decreasing height and increasing weight of the population. As expected, as the population aged, bone density de- creased at all sites (Table 2). At the lumbar spine, BMD did not change during the two decades between ages 20 and 39, and a minor decrease occurred within ages 40 and 49. The greatest decrease in BMD was observed during the sixth decade (age 50--59), with an average 11.4% bone loss com- pared with the fifth decade (age 40-49), whereas the average spinal BMD in the seventh decade (age 60-69) was 6.9% less than the average in the sixth decade. No further decline in bone mass was observed in the eighth decade. This pattern of bone loss was less evident at the proximal femur, although in the Ward's area, which is mainly composed of trabecular bone, the largest decrement of bone mass also occurred be- tween ages 40 and 49 and 50 and 59 (11.4%). At the neck and trochanteric areas, bone density appeared to decrease lin- early with age. Age-dependent changes of BMD were then analyzed by regression analyses. Cross-sectional plots of bone density by age at the four different sites are illustrated in Figures 1 to 4. As pointed out above, since the fastest bone loss appeared to occur between ages 45 and 60---the time around the meno- pause-different regression lines were calculated for three groups, according to the menopausal status. In the spine, a steeper slope was obtained for the perimenopausal group compared with the postmenopausal subjects, whereas an in- significant negative correlation was observed in the pre- menopausal period (Table 3). Accordingly, the rate of bone loss per year in the perimenopausal group was almost twice as high as that of the postmenopausal women, whereas yearly changes in the premenopausal group were close to zero. A significant correlation between age and bone density was obtained by analyzing the entire population, thus indi- cating that a simple linear function may be adequate to de- scribe age-induced bone loss in cross-sectional studies. Rates of bone loss detected in all the proximal femur sites before the menopause were mostly not statistically signifi- cant (Tables 4--6), and a clear menopause-dependent pattern did not emerge as it did for the spine (Figs. 2-4). Yearly bone loss showed the same behavior in the perimenopausal and postmenopausal groups at both the femoral neck (Table 4), and the Ward's area (Table 5). The calculated slopes for the E < v I r Y_ o 1.0 0.5 o o n a o%~ .oo" "o o ~ oOo gw ~o. ~o0 ~ O cl B o o,~.,,., o 0 aaellg aam~ a O0 9 O0 u| n 9 a ~---~o-~=_~o~o,,,~ o ~ %0 o ao ~ g*'~ ~ u 81a= ...... =pa = O v = n = o a -... o oe .o~ ~ 0o ..... ?.. o a aau== = = [] - = = l~176 8 9 o = a a aa a a o oo a a a o o a [ 20 30 40 50 60 70 80 Age years) Fig. 2. BMD of the femoral neck against age in 418 normal white Brazilian women. Separate regression lines are illustrated for pre- menopausal (C)), perimenopausal (O), and postmenopausal ([3) sub- jects. three groups were not significant at the trochanter site, al- though the regression on the total population yielded a sig- nificant correlation (Table 6), underlining the lesser preci- sion of DXA in this area. To further study the pattern of bone loss after the meno- pause, correlation analyses were applied to the postmeno- pausal subset according to the time elapsed since the meno- pause (Table 7). At each site, both an exponential and a linear model gave significant correlations. Results of the lin- ear regression analysis at each site are shown in Table 7, along with the estimated percent yearly bone loss. Interest- ingly, the rate of bone loss in the Ward's triangle was almost twice as high as that calculated for the lumbar spine. Also, the postmenopausal demineralization process was faster in the femoral neck than in the spine. The slope of the linear model in the trochanteric area barely reached significance, in analogy to the poor correlation found at this site between bone density and age (see above). Discussion Availability of normative data for bone density at different sites provides a precise tool for comparison with values ob- tained in patients, thus making the diagnosis of osteopenia possible based on densitometric values. The data reported in this study establish normative bone densitometric values for Caucasian women born and living in the S~o Paulo area of southwestern Brazil.  V. L. Szejnfeld et al.: Bone Density in Brazilian Women o o E ~ o ~ . ~ o~ o oo oo o o o OOo oo ~ o a o e6 9 o o~ o ~ ~ ~ o 08 : ~ * 00 :; .... .o_ _~o--.~ oo 0=,,0 oo0 O --~ ~,bLgO 8 gO am o a g 0o o o0 s~elil;.o~.,'~ ,~ o o o e-o~,.~e~ ~. e . = 0~ >- o '-02? 8t._o~ a. . [] o o o o o o 9 o-n~ 9 B -'-- [] .~ o o o o 0 ~ l~.~176 ~0~ *=~* 0- = 0~ c o~176 o 176 ~ -~..p c~ : 9 no n:= ,~0~ ....... ? o a o~o:: Bo moo -,. 9 = a r 8 a [] o~ oo [] o -- m a a o o a [] o I I I I I I I r~ 20 30 40 50 60 70 80 Age (years) Fig. 3. BMD of the proximal femur (Ward's triangle) against age in 418 normal white Brazilian women. Separate regression lines are illustrated for premenopausal (9 perimenopausal (0), and post- menopausal (~) subjects. E o v 1.0 ~z ~t I m c~ c 0.5 o c13 a a o o o a a o ~ o e 9 D o~oo 8 ,00o.~ ~ .%..oo o ~% o~oo; ~o ~ oe o ~176 ~ ~oO-- ~--.o o o% ~_ ~oeoetloo.oo o o _ --o__ ~o2o~-ooa ~ o 8 = o o o o o o~ ~ -~o-o~ ~o. o..Eo- o o o o o o~. go ~ ~oB~ o ~r~ = -""d,;n ~---sa .... o _ o ~o-~176176176176176 8 o o u o o ~ o o o Btal~ mob B o~ o o= o o o . o on o= ~ B n g = aao 9 o o oo o o o 9 o r o = I I I [ I I I 20 30 40 50 60 70 80 Age (years) Fig. 4. BMD of the proximal femur (trochanteric area) against age in 418 normal white Brazilian women. Separate regression lines are illustrated for premenopausal ((3), perimenopausal (O), and post- menopausal (E3) subjects. Brazil is a large country, with a large and cosmopolitan population, including people of European, African, Oriental, and Indian descent. As the present study was limited to a specific ethnic group and geographical area, our database is obviously not representative of the entire Brazilian female population. Therefore, these normative values should be ap- plied only to Caucasian women living in comparable envi- ronmental and social conditions, and sharing similar genetic characteristics and habits. An additional factor to be consid- ered concerning bone density in Brazilian populations is the interracial mixing, an aspect perhaps less frequently seen in other countries, which limits the applicability of normative data to large populations. Thus, in order to construct an integral "normal Brazilian database," population-based studies should be extended to all racial groups living in this country. Besides the natural heterogeneity of populations included in cross-sectional studies, the vertebral BMD values we measured in our subjects were lower than those observed in 189 other white populations in whom BMD was assessed by dual photon absorptiometry [19]. Normal BMD values published as reference for spine bone density of white North American and European women are 3.4-6.5% higher than those re- ported here for subjects between ages 30 and 69 [19]. The apparent discrepancies between Brazilian and North Amer- ican women of European ancestry are more evident in the proximal femur than at the spine, with values 5-8% lower in the South American population at the various femoral sites. In theory, this discrepancy could be simply explained by the different techniques employed. Conversely, if this difference is real, genetic characteristics, exposure to different envi- ronmental factors, and a different socioeconomic status may be invoked as possible confounders [12]. The last hypothesis seems less plausible considering that our subjects derived almost exclusively from middle-high social classes in Brazil. Furthermore, bone density levels of Argentinean women of similar socioeconomic level [14] are closer to the published North American data [20] than to our population. Although our data were obtained using the same instrument model also employed in the North American and European studies, and its reported precision is consistently below 1%, methodolog- ical issues may still be critical factors for the observed lower density levels in our subjects. Our cross-sectional analysis also indicates that bone mass remains relatively stable between 30 and 50 years of age, that is, as long as estrogen function is maintained. On the other hand, the total bone loss in a lifetime (between 20 and 79 years of age) calculated in this cohort is approxi- mately 23% at the spine, with almost half (11.4%) of the loss occurring during the transition between the pre- and post- menopausal periods. Although the cross-sectional nature of our study does not allow us to rule out a cohort effect (i.e., women with different birthdates may have differed for diet or other lifestyle habits in the past), similar rapid decreases of BMD immediately following the menopause have been reported by others [21-23]. Interestingly, in a cross-sectional study similar to ours, which included 280 white females be- tween 19 and 87 years of age, Hui et at. [23] found that the loss of trabecular bone was accelerated at the time around the onset of the menopause, whereas slower rates of bone loss were found in later years. The accumulated data on bone density as a function of age and menopausal status obtained in population-based studies indicate that, although linear models of bone loss can generally be applied to nor- mative data [24, 25], an acceleration of bone loss occurs at around the menopause [23, 26, 27]. Our study also appears to suggest that the menopausal status has lesser influence on the appendicular than on the axial skeleton, as a menopause- dependent bone loss was not so evident at the proximal fe- mur as it was at the spine. The notion that absorptiometric measurements of bone density are less sensitive to artifacts due to osteoarthritic processes and vascular calcifications when used at nonvertebral locations, i.e., the proximal fe- mur [28-30], may explain, at least in part, the faster post- menopausal bone loss we observed in the proximal femur sites compared with the loss at the vertebral site. These historical trends underscore the clinical value of bone den- sity measurements for the identification of subjects at risk for fast bone loss, and the implementation of preventive measures. In summary, we have established normative bone density data for white Brazilian women, and confirmed that the age- related decline of bone mass is faster at the time around the menopause. Though at this time bone loss is more rapid in the axial skeleton, postmenopausal rates of bone loss appear to be greater at appendicular skeletal sites.  190 V. L. Szejnfeld et al.: Bone Density in Brazilian Women Table 4. Linear regression models for menopause-related bone loss in Brazilian women: fem- oral neck n Model SEE r % Loss/year Premenopausal 176 0.9928-0.0022 x age 0.0950 -0.20 0.22 PerimenopansaI 42 1.1723-0.0059 • age 0.1015 -0.24 0.50 Postmenopausal 199 1.0802-0.0048 • age 0.1150 - 0.29 ~ 0.45 Overall 417 1.0827-0.0046 • age 0.1067 - 0.45 ~ 0.43 a Slope different than 0 at 95% confidence limit Table 5. Linear regression models for menopause-related bone loss in Brazilian women: Ward's area n Model SEE r % Loss/year Premenopausal 176 1.0152-0.0050 x age 0.1168 -0.36 a 0.47 Perimenopausal 42 1.1650-0.0080 x age 0.1172 - 0.28" 0.69 Postmenopansal 199 0.9963-0.0056 • age 0.1406 -0.28 ~ 0.56 Overall 417 1.0755-0.0067 x age 0.1292 -0.53 ~ 0.62 Slope different than 0 at 95% confidence limit Table 6. Linear regression models for menopause-related bone loss in Brazilian women: tro- chanteric area n Model SEE r % Loss/year Premenopausal 176 0.8472-0.0027 x age 0.0952 -0.24 0.32 Perimenopausal 42 0.9601-0.0046 x age 0.0985 - 0.19 0.48 Postmenopausal 199 0.7598-0.0015 x age 0.1127 -0.09 0.20 Overall 417 0.8583-0.0030 • age 0.1046 -0.33 ~ 0.35 Slope different than 0 at 95% confidence limit Table 7. Bone mineral density according to years since menopause in 199 postmenopausal Brazilian women % Loss/ Skeletal site Model SEE r year Lumbar spine 1.0234-0.0050 x YSM 0.1431 -0.26 a 0.49 Femoral neck 0.8517-0.0053 x YSM 0.1134 -0.33 a 0.62 Ward's area 0.7275-0.0061 x YSM 0.1390 -0.32 ~ 0.84 Trochanteric area 0.6981-0.0025 x YSM 0.116 -0.17 b 0.36 YSM: years since menopause Slope different than 0 at 99%; b 95% confidence limit Acknowledgments. The authors wish to thank Mrs. Judy Hirstein for secretarial help. Part of this work has been presented at the 13th annual meeting of the American Society for Bone and Mineral Re- search, San Diego, CA, August 24-28, 1991; Abstract #165. References 1. Einhorn TA (1992) Bone strength: the bottom line [Editorial]. Calcif Tissue Int 51:333-339 2. Horsman A, Currey JD (1983) Estimation of mechanical prop- erties of the distal radius from bone mineral content and cortical width. Clin Orthop Rel Res 176:298 3. Cohn SH, Yasumura AS, Aloia JF, Zanzi I, Ellis KJ (1977) Comparative skeletal mass radial bone mineral content in black and white women. Metabolism 26:171-178 4. Trotter M, Broman GE, Peterson RR (1960) Densities of bones of white and Negro skeletons. J Bone Joint Surg 42-A:50--58 5. Liel Y, Edwards J, Shary J, Spicer KM, Gordon L, Bell NH (1988) The effect of race and body habitus on bone mineral density of the radius, hip and spine in premenopansal women. J Clin Endocrinol Metab 66:1247-1250 6. Luckey MM, Meier DE, Mandeli JP, DaCosta MC, Hubbard ML, Goldsmith SJ (1989) Radial and vertebral bone density in white and black women: evidence for racial differences in pre- menopausal bone homeostasis. J Clin Endocrinol Metab 69: 762-770 7. Melton LJ III, Riggs BL (1993) Epidemiology of age-related fractures. In: Avioli LV (ed) The osteoporotic syndrome: de- tection, prevention and treatment. Wiley-Liss, Inc. New York, pp 17-38 8. Farmer ME, White LR, Brody JA (1984) Race and sex differ- ences in hip fracture incidence. Am J Public Health 44:1374- 1380 9. 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 Eng[ J Med 325:1597-1600 10. Ross PD, Orimo H, Wasnich RD, Vogel JM, McLean C J, Davis JW, Nomura A (1989) Methodological issues in comparing ge- netic and environmental influences on bone mass. Bone Miner 7:67-77 11. Yano K, Wasnich RD, Vogel JM, Heilbrun LK (1984) Bone mineral measurements among middle-aged and elderly Japa- nes residents in Hawaii. Am J Epidemiol 119:751-764 12. Del Rio Barquero L, Banres MR, Segura JP, Quinquer JS, Ma- jem LS, Ruiz PG (1992) Bone mineral density in two different socio-economic population groups. Bone Miner 18:159-168 13. Pocock NA, Eisman JA, Mazess RB, Sambrook PN, Yeates
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