Factors associated with osteopenia and osteoporosis in women undergoing bone mineral density test

Abstracts

O objetivo deste estudo foi determinar a prevalência de osteopenia e osteoporose em uma população de mulheres que fizeram exames de densitometria em uma clínica especializada no sul do Brasil. Nós conduzimos um estudo transversal, incluindo 1.871 mulheres que se submeteram à densitometria óssea entre janeiro e dezembro de 2012. Foi feita uma análise de regressão logística com todas as variáveis independentes e os desfechos (osteopenia, osteoporose e risco de fraturas). A densitometria óssea foi diagnosticada como normal em 36,5% das mulheres, 49,8% com osteopenia e 13,7% com osteoporose. Estar na menopausa e ter mais de 50 anos foram fatores de risco para osteopenia e osteoporose, enquanto ter feito histerectomia e apresentar índice de massa corporal (IMC) maior do que 25 foram fatores de proteção. Para o desfecho fratura em qualquer sítio, os fatores associados foram idade acima de 50 anos e osteopenia ou osteoporose, (OR = 2,09, intervalo de confiança [IC]: 1,28-3, 95%, 40) e (OR = 2,49, 95% CI: 1,65-3, 74), respectivamente.

Osteoporose; Densitometria; Epidemiologia; Doenças ósseas metabólicas


The aim of this study was to determine the prevalence of osteopenia and osteoporosis in a female population, that had bone mineral density (BMD) measured by dual-energy X-ray absorptiometry (DXA) in a specialized clinic in the south of Brazil. We conducted a cross-sectional study including 1871 women that performed scans between January and December 2012. We conducted a logistic regression analysis with all independent variables and outcomes (osteopenia, osteoporosis and fracture risk). According to DXA results, 36.5% of women had normal BMD, 49.8% were diagnosed with osteopenia and 13.7% with osteoporosis. Menopause and age over 50 years old were risk factors for osteopenia and osteoporosis while prior hysterectomy and BMI greater than 25 were protective factors. For the outcome of fracture at any site the risk factors were age over 50 years old, osteopenia and osteoporosis (OR = 2.09, 95% CI: 1.28–3.40) and (OR = 2.49, 95% CI: 1.65–3.74), respectively.

Osteoporosis; Dual-energy X-ray absorptiometry; Epidemiology; Metabolic bone diseases


Introduction

Osteoporosis is a systemic skeletal disease characterized by low bone mass and micro architectural deterioration of the bone tissue, resulting in increased risk of fracture due to bone fragility.1NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001). JAMA. 2001;285:785–95. It was recently acknowledged as one of the main public health issues of developed countries.2World Health Organization Burden of disease in DALYs by cause, sex, and mortality stratum in WHO regions, estimates for 2002. The World Health Report changing history. Geneva: World Health Organization; 2004. p. 126–31.

Osteoporosis is diagnosed by measuring the bone mineral density (BMD); a bone density that is 2.5 standard deviations (SD) or more below the young adult mean value (t -score <−2.5) indicates osteoporosis. Patients with bone density between 1 and 2.5 SD below average (t -score −1 to −2.5) are said to have osteopenia.3World Health Organization. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva: World Health Organization; 1994. p. 1–129. Technical Report Series n◦. 843.

In women, BMD decreases with age, presenting sharp drop during menopause. It is estimated that one in every two women in the UK from the age of 50 will suffer some kind of fracture during the remainder of her life.4Van Staa TP, Dennison EM, Leufkens HG, Cooper C. Epidemiology of fractures in England and Wales. Bone. 2001;29:517–22.

With increasing life expectancy and an aging population, it is anticipated that the impact of osteoporosis in the coming years will have a significant increase.5Lane NE. Epidemiology, etiology, and diagnosis ofosteoporosis. Am J Obstet Gynecol. 2006;194:S3–11. We should expect an economic burden for current and future public health system due to the high prevalence of osteoporosis and resulting fractures.6Hopkins RB, Tarride JE, Leslie WD, Metge C, Lix LM, Morin S, et al. Estimating the excess costs for patients with incident fractures, prevalent fractures, and nonfracture osteoporosis. Osteoporos Int. 2012 [Epub ahead of print].

The aim of this study was to determine the prevalence and factors associated with osteopenia and osteoporosis in women who have undergone bone mineral density test in a specialized service.

Methods

A cross-sectional study was made with 1871 women undergoing bone mineral density test in a specialized clinic from January 2012 to December 2012. The project was approved by the Research Ethics Committee of Universidade Extremo Sul Catarinense under Protocol No. 829 392 012.

Osteopenia and osteoporosis were diagnosed by Dual-energy X-ray absorptiometry (DXA), allowing the BMD to be measured with the GE Lunar Prodigy Primo equipment with software Encore version 13.20. The Lunar Prodigy series showed clinical accuracy even 40% higher compared to other systems. A study suggests that BMD measurement error is between 5% and 8%.7Kuiper JW, Van Kuijk C, Grashuis JL, Ederveen AG, Schutte HE. Accuracy and the influence of marrow fat on quantitative CT and dual-energy X-ray absorptiometry measurements of the femoral neck in vitro. Osteoporos Int. 1966;6:25–30.

DXA is considered the gold standard for measuring BMD and diagnosing osteopenia/osteoporosis. DXA results are presented by (1) absolute BMD values (g/cm2): absolute values are important because they are used to monitor changes in BMD over time; (2) t-score, calculated in SD, taking as reference the mean BMD of peak bone mass in young adults. The diagnostic criteria proposed by the World Health Organization (WHO) in 1994, based on the following data: up to −1.0 SD, normal, from −1.1 to −2.49 SD, osteopenia, and below −2.5 SD, osteoporosis8Kanis JA, WHO Study Group. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Synopsis of a WHO Report Osteoporos Int. 1994;4:368–81.; (3) Z -score, calculated on SD, taking as reference the mean BMD expected for individuals of same age, ethnicity and gender.

It is important to recognize that the DXA results described here are only valid when strict criteria for the exam, quality control and analysis of the images are observed. The professionals responsible for the acquisition of images, as well as for analyzing and interpreting them must act in accordance with recognized professional qualification programs in the country. The incorrect application of the method limits its use, as in all imaging tests.

General data were taken from the densitometry report and included measurement of weight and height, age, BMI, previous fractures, calcium intake, thyroid medication, menopause, hormone replacement therapy, symptoms of menopause, hysterectomy and oophorectomy. Age was categorized into percentiles: (1) 25th percentile: aged 51 years or less, (2) between 25th and 50th percentile: aged 52–57 years, (3) between 50th and 75th percentile: aged 58–65 years and (4) above the 75th percentile: aged 66 years or older. Other qualitative variables were dichotomized.

BMI was calculated using the formula weight (kg)/height2 (m). The DXA data collected included BMD values (g/cm2) of the femur neck, preferably the right one, the total femur and the mean value of the lumbar vertebrae (L1-L4).

Descriptive analysis of all variables was performed. A bivariate analysis was performed using the Pearson's chi-square test.

In the model building process, we observed the importance of each component through the likelihood ratio test. The −2log likelihood (deviance) value, which is a measure to determine how well the model fits the data, was used. Estimates per interval were calculated using 95% confidence level. All variables with p < 0.25 (univariate analysis) were candidates to enter the model, according to the method of Hosmer and Lemeshow. Only p < 0.05 variables remained in the model. In case any biologically important change was observed in the coefficient of estimated risk factor, comparing models with and without the risk factor, it was considered that the covariate would be a confounding factor, and if so, should remain in the model, even if its own coefficient was not significant. The method used to build the multivariable logistic regression model was the backward method, in which all the variables selected by the researchers enter the model, and selection is made by removing the least significant variable, one at a time, in an automatic sequence mode, based on statistical criteria. The estimates per interval were calculated using 95% confidence level. Interactions between variables were tested, and they were all nonsignificant at a 5% level of significance.

Statistical analysis was performed using the Statistical Package for Social Sciences (SPSS) version 18.0.

Results

The sample consisted of 1871 women who underwent DXA scan in a specialized private clinic in south of Santa Catarina. The average age was 59.2 ± 10.5 years, mean weight of 68.7 ± 12.8 and height of 1.57 ± 0.06. The mean BMI was 27.7 ± 5.0, 65.1% had a BMI > 25. The prevalence of fractures at any site was of 5.5%; the forearm and ribs being the most prevalent (Table 1). It was found that 31.9% of women were taking calcium, and 22.1% were on thyroid medication, 24.9% had previously had a hysterectomy, and 18.1%, an oophorectomy (Table 1).

Table 1
Characteristics of the women that performed DXA scans from January to December, 2012, presented as frequency (%) or average (± SD).

According to the bone mineral density test diagnosis, 36.5% of women were normal, 49.8% had osteopenia and 13.7% had osteoporosis (Table 1).

Table 2 shows the prevalence of bone mass density in different subgroups, as well as the analysis of statistical significance using the chi-square test. The linear increase in osteopenia and osteoporosis was observed with advancing age (p < 0.001). The BMI, however, was inversely associated with reduced BMD ( p < 0.001), i.e., women with higher BMI had less osteopenia or osteoporosis.

Table 2
Prevalence of bone mineral mass density in patients subgroups.

The correlations between the BMD measured at the spine, femur and femoral neck and the BMI were ( r = −0.133, p < 0.001, r = 0.590 p < 0.001 and r = 0.258, p < 0.001), respectively.

The BMD at all sites had negative correlation with age (femoral neck r = −0.220, r = −0.337 total femur and lumbar spine r = −0.015, p < 0.001).

The multivariate regression had the following outcomes: osteoporosis, osteopenia and any fracture.

Table 3 shows the final logistic regression model for the first two outcomes, including the variables mean dichotomized age, menopause, BMI and hysterectomy. One can observe increased risk of osteoporosis for the variables age and menopause. Protection was found with an increased BMI and hysterectomy.

Table 3
Logistic regression model, considering the outcome variable – osteopenia vs. normal and osteoporosis vs. normal.

Table 4 shows the final fracture model, in which being older than 50 years old and presenting osteopenia/osteoporosis increase the chances of fractures at any site in 2.09 and 2.49, respectively, when compared to women aged 49 years or less and women with normal BMD.

Table 4
Final logistic regression model, considering the outcome variable – any fracture.

Discussion

Our study used data from a clinic specialized in the diagnosis of osteoporosis, so the prevalence of osteopenia and osteoporosis cannot be extended to the general population, being restricted to a group of women referred for a DXA scan. In this case, the prevalence of osteoporosis should be overrated in relation to other population groups.

According to the DXA results, 36.5% of women had normal BMD, 49.8% were diagnosed with osteopenia and 13.7% with osteoporosis. The prevalence of osteopenia and osteoporosis found in our study showed a linear increase with age in the four age percentiles of the population studied.

The prevalence found in this study was lower than that found in the literature on similar studies conducted before the year 2000. In a study that assessed the prevalence of osteoporosis in Brazilian women, above the age of 50, and referred for bone density test, this prevalence was of 40%.9Torres R, Marcelino C, Vieira L, Bandeira F. Prevalência de osteoporose em 1441 mulheres encaminhadas paradeterminação da densidade óssea. Arquivos Brasileiros de Endocrinol Metabol. 1998;42:S182. In the United States, a study with 600 patients at Wayne State University in Detroit, found a prevalence of 52%.1010 Nelson D, Molloy R, Kleerekoper M. Prevalence of osteoporosis in women referred for bone density testing: utility of multiples keletal sites. J Clinical Densit. 1998;1:5–12.

The NHANES III study conducted between 1988 and 1994 by the Centers for Disease Control and Prevention gathered 3311 postmenopausal women above the age of 50 for proximal femur BMD examinations. The prevalence of osteoporosis and osteopenia verified was 18% and 50%, respectively.1111 Looker AC, Orwoll ES, Johnston CC, Lindsay R, Wahner H, Dunn W. Prevalence of low femoral bone in older U.S. adults from NHANES III. J Bone Miner Res. 1997;12:1761–8. In Sao Paulo state, a cross-sectional study with 4332 women over the age of 40, in a primary care service, found the prevalence of osteoporosis to be 33% and osteoporotic fractures of 11.5%( p < 0.05),1212 Pinheiro MM, dos Reis Neto ET, Machado FS, Omura F, Yang JHK, Szejnfeld J, et al. Fatores de risco para fratura por osteoporose e baixa densidade óssea em mulheres na pré e pós-menopausa. Rev Saúde Pública. 2010;44:479–85. while another study with 627 women over the age of 50 showed prevalence of osteoporosis in the lumbar spine and in femoral neck of 28.8% and 18.8%, respectively.1313 Pinheiro MM, Reis N, Machado ET, Felipe FS, Yang O, Szejnfeld JH, et al. Risk factors for osteoporotic fractures and low bone density in pre and postmenopausal women. Rev Sau Pub. 2010;44:479–85.

In both male and female individuals, there is a balance between bone formation and resorption, but this becomes progressively negative with increasing age. Age-related bone loss begins immediately after the peak bone mass, but most of the bone loss occurs after the age of 65. Men, however, are less likely to develop osteoporosis than women, for two reasons: first, they gain more bone mass during puberty and, second, they lose less bone mass during aging, because, unlike women, men do not experience a sudden loss of estrogen. Elderly living at retirement homes are at greater risk. Eighty-five percent of women living in nursing homes over age 80 have osteoporosis.1414 Bandeira FC, Freese E. Prevalência de osteoporose e fraturas vertebrais em mulheres na pós-menopausa atendidas em serviços de referência. Rev Brasil Epidemiol. 2007;10:86–98.

Our results showed a linear increase of osteopenia and osteoporosis with advancing age. In addition to the effects on bone mass, the aging also increases the risk of fractures, regardless of the bone mass, and an increase of 20 years of age means a fourfold risk of fractures.1515 Vu MQ, Weintraub N, Rubenstein LZ. Falls in the nursinghome: are they preventable? J Am Med Dir Assoc. 2006;7:S53.

Oxidative stress (OS) is a common mechanism of pathogenesis of various degenerative diseases associated with aging, including osteoporosis.1616 Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass aspredictors of fracture in a prospective study. J Clin Invest. 1988;81:1804.,1717 Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants,and aging. Cell. 2005;120:483. An increase in reactive oxygen species (ROS) was implicated in decreased bone formation associated with advancing age, as well as increased resorption associated with estrogen deficiency.1616 Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass aspredictors of fracture in a prospective study. J Clin Invest. 1988;81:1804. In line with this evidence, increased ROS production in osteoblasts stimulates apoptosis and decreased bone formation. As of the fourth decade, the bone formation is lower than the resorption.1818 Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev. 2010;31:266. Serum levels of the insulin-like growth hormone that modulates the effect of the GH in the bone also decrease with age.1919 Lips P, Courpron P, Meunier PJ. Mean wall thicknessof trabecular bone packets in human liac crest: changeswith age. Calciforme Tissue Research. 1978;26:13–7.

Our study showed a higher prevalence of forearm, rib, hip and spine fractures, respectively. According to the literature, the vertebral fracture is the most common clinical manifestation of osteoporosis. Most of these fractures (about two thirds) are asymptomatic, diagnosed as an incidental finding on X-ray.2020 Rudman D, Kutner MH, Rogers CM, Lubin MF, Fleming GA, Bain RP. Implaired growth hormone secretion in the adult population: relation to age and adiposity. Journal of Clinical Investigation. 1981;67:1361–9. Hip fractures are relatively common in osteoporosis and affects 15% of women and 5% of men at the age of 80. Subchondral insufficiency fractures of the femoral head, resulting in osteopenia, can lead to rapid loss of cartilage and space-destructive osteoarthritis.2121 Lindsay R, Silverman SL, Cooper C, Hanley DA, Barton I, Broy SB, et al. Risk of new vertebral fracture in the year following a fracture. JAMA. 2001;285:320–3. In addition to that, fractures of the distal radius (Colles’ fractures) may also occur and are more common in women after menopause, while the risk of hip fracture increases exponentially with age.

Our results show an inverse correlation between the BMI and the risk of osteopenia and osteoporosis. Published studies show that low body weight (less than 58 kg) is associated with an increased risk of osteoporosis and fractures. Weight losses after the age of 50 in women increases the risk of hip fracture, while weight gains decreases this risk.2222 Yamamoto T, Bullough PG. The role of subchondral insufficiency fracture in rapid destruction of the hip joint: a preliminary report. Arthritis Rheum. 2000;43:2423.,2323 Green AD, Colón-Emeric CS, Bastian L, Drake MT, Lyles KW. Does this woman have osteoporosis? JAMA. 2004;292:2890–900.

Menopause was also a risk factor with statistical significance in our study. The rate of bone loss in women with postmenopausal hypoestrogenism is probably around 0.5% and 1.5% per year, with a small percentage of women who are “fast bone losers” and can lose 3%–5% of bone mass per year. The rate of bone loss is highly dependent on hormonal factors, environmental and genetic factors. In a longitudinal study with 272 healthy pre- and perimenopausal women, there was no bone loss in women beyond the menopause, while an accelerated bone loss was observed in the 2–3 years prior to the cessation of menstruation, with significant correlation between the rate of bone lost and the elevation of follicle-stimulating hormone (FSH) and markers of bone metabolism.2424 Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, et al. Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med. 2006;166:2502–10.2626 Park HA, Lee JS, Kuller LH, Cauley JA. Effects of weight controlduring the menopausal transition on bone mineral density. J Clin Endocrinol Metab. 2007;92:3809.

We also found that hysterectomy would be a protective factor for osteopenia and could not find a plausible explanation for this protection, since it goes against the literature, which reports a decrease in bone mass after hysterectomy.2727 Warming L, Hassager C, Christiansen C. Changes in bone mineral density with age in men and women: a longitudinal study. Osteoporos Int. 2002;13:105–12.2929 Watson NR, Studd JW, Garnett T, Savvas M, Milligan P. Bone loss after hysterectomy with ovarian conservation. Obstet Gynecol. 1995;86:72–7. This variable is independent of the oophorectomy, which was analyzed apart and showed no statistical significance. This analysis may be biased, since confounding factors, such as the lifestyle and the reproductive history of the patients, were not controlled.

Conclusion

Our study showed that the prevalence of osteopenia is greater than that of osteoporosis and that old age and menopause are risk factors for both outcomes, while BMI above 25 and prior hysterectomy were protective factors. For the fracture outcome, the statistically significant risks were age above 50 years old and osteopenia or osteoporosis.

  • Institution: Universidade do Extremo Sul Catarinense – UNESC, Laboratory of Epidemiology.

References

  • 1
    NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001). JAMA. 2001;285:785–95.
  • 2
    World Health Organization Burden of disease in DALYs by cause, sex, and mortality stratum in WHO regions, estimates for 2002. The World Health Report changing history. Geneva: World Health Organization; 2004. p. 126–31.
  • 3
    World Health Organization. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva: World Health Organization; 1994. p. 1–129. Technical Report Series n◦. 843.
  • 4
    Van Staa TP, Dennison EM, Leufkens HG, Cooper C. Epidemiology of fractures in England and Wales. Bone. 2001;29:517–22.
  • 5
    Lane NE. Epidemiology, etiology, and diagnosis ofosteoporosis. Am J Obstet Gynecol. 2006;194:S3–11.
  • 6
    Hopkins RB, Tarride JE, Leslie WD, Metge C, Lix LM, Morin S, et al. Estimating the excess costs for patients with incident fractures, prevalent fractures, and nonfracture osteoporosis. Osteoporos Int. 2012 [Epub ahead of print].
  • 7
    Kuiper JW, Van Kuijk C, Grashuis JL, Ederveen AG, Schutte HE. Accuracy and the influence of marrow fat on quantitative CT and dual-energy X-ray absorptiometry measurements of the femoral neck in vitro. Osteoporos Int. 1966;6:25–30.
  • 8
    Kanis JA, WHO Study Group. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Synopsis of a WHO Report Osteoporos Int. 1994;4:368–81.
  • 9
    Torres R, Marcelino C, Vieira L, Bandeira F. Prevalência de osteoporose em 1441 mulheres encaminhadas paradeterminação da densidade óssea. Arquivos Brasileiros de Endocrinol Metabol. 1998;42:S182.
  • 10
    Nelson D, Molloy R, Kleerekoper M. Prevalence of osteoporosis in women referred for bone density testing: utility of multiples keletal sites. J Clinical Densit. 1998;1:5–12.
  • 11
    Looker AC, Orwoll ES, Johnston CC, Lindsay R, Wahner H, Dunn W. Prevalence of low femoral bone in older U.S. adults from NHANES III. J Bone Miner Res. 1997;12:1761–8.
  • 12
    Pinheiro MM, dos Reis Neto ET, Machado FS, Omura F, Yang JHK, Szejnfeld J, et al. Fatores de risco para fratura por osteoporose e baixa densidade óssea em mulheres na pré e pós-menopausa. Rev Saúde Pública. 2010;44:479–85.
  • 13
    Pinheiro MM, Reis N, Machado ET, Felipe FS, Yang O, Szejnfeld JH, et al. Risk factors for osteoporotic fractures and low bone density in pre and postmenopausal women. Rev Sau Pub. 2010;44:479–85.
  • 14
    Bandeira FC, Freese E. Prevalência de osteoporose e fraturas vertebrais em mulheres na pós-menopausa atendidas em serviços de referência. Rev Brasil Epidemiol. 2007;10:86–98.
  • 15
    Vu MQ, Weintraub N, Rubenstein LZ. Falls in the nursinghome: are they preventable? J Am Med Dir Assoc. 2006;7:S53.
  • 16
    Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass aspredictors of fracture in a prospective study. J Clin Invest. 1988;81:1804.
  • 17
    Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants,and aging. Cell. 2005;120:483.
  • 18
    Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev. 2010;31:266.
  • 19
    Lips P, Courpron P, Meunier PJ. Mean wall thicknessof trabecular bone packets in human liac crest: changeswith age. Calciforme Tissue Research. 1978;26:13–7.
  • 20
    Rudman D, Kutner MH, Rogers CM, Lubin MF, Fleming GA, Bain RP. Implaired growth hormone secretion in the adult population: relation to age and adiposity. Journal of Clinical Investigation. 1981;67:1361–9.
  • 21
    Lindsay R, Silverman SL, Cooper C, Hanley DA, Barton I, Broy SB, et al. Risk of new vertebral fracture in the year following a fracture. JAMA. 2001;285:320–3.
  • 22
    Yamamoto T, Bullough PG. The role of subchondral insufficiency fracture in rapid destruction of the hip joint: a preliminary report. Arthritis Rheum. 2000;43:2423.
  • 23
    Green AD, Colón-Emeric CS, Bastian L, Drake MT, Lyles KW. Does this woman have osteoporosis? JAMA. 2004;292:2890–900.
  • 24
    Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, et al. Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med. 2006;166:2502–10.
  • 25
    Chapurlat RD, Garnero P, Sornay-Rendu E, Arlot ME, Claustrat B, Delmas PD. Longitudinal study of bone loss in pre- and perimenopausal women: evidence for bone loss in perimenopausal women. Osteoporos Int. 2000;11:493–8.
  • 26
    Park HA, Lee JS, Kuller LH, Cauley JA. Effects of weight controlduring the menopausal transition on bone mineral density. J Clin Endocrinol Metab. 2007;92:3809.
  • 27
    Warming L, Hassager C, Christiansen C. Changes in bone mineral density with age in men and women: a longitudinal study. Osteoporos Int. 2002;13:105–12.
  • 28
    Hreshchyshyn MM, Hopkins A, Zylstra S, Anbar M. Effects of natural menopause, hysterectomy and o ophorectomyon lumbar spine and femoral neck bone densities. Obstet Gynecol. 1988;72:631–8.
  • 29
    Watson NR, Studd JW, Garnett T, Savvas M, Milligan P. Bone loss after hysterectomy with ovarian conservation. Obstet Gynecol. 1995;86:72–7.

Publication Dates

  • Publication in this collection
    May-Jun 2015

History

  • Received
    10 Feb 2014
  • Accepted
    17 Aug 2014
Sociedade Brasileira de Reumatologia Av Brigadeiro Luiz Antonio, 2466 - Cj 93., 01402-000 São Paulo - SP, Tel./Fax: 55 11 3289 7165 - São Paulo - SP - Brazil
E-mail: sbre@terra.com.br