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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 58:M436-M440 (2003)
© 2003 The Gerontological Society of America

Prevalence of Sarcopenia and Predictors of Skeletal Muscle Mass in Nonobese Women Who Are Long-Term Users of Estrogen-Replacement Therapy

Anne M. Kenny1, Latesha Dawson1, Alison Kleppinger1, Michele Iannuzzi-Sucich1 and James O. Judge2

1 Center on Aging, University of Connecticut Health Center, Farmington, Connecticut.
2 Masonic Healthcare Center, Wallingford, Connecticut.


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 Conclusion
 References
 
Background. Sarcopenia refers to the loss of skeletal muscle mass with age. We have found a prevalence of sarcopenia of 22.6% in older postmenopausal women not receiving estrogen. The objective of this study was to determine the prevalence of sarcopenia in a population of older, nonobese, community-dwelling women who had been long-term users of estrogen replacement therapy (ERT).

Methods. We measured appendicular skeletal muscle mass by dual x-ray absorptiometry (DXA) in 189 women aged 59 to 78 years old who had been using ERT for at least 2 years (mean ± SD duration, 12.7 ± 8.2 years). We defined sarcopenia as an adjusted appendicular skeletal muscle mass (ASM) (mass divided by height squared) more than 2 SDs below the mean for a young healthy reference population. Health and menopause history were obtained. Body mass index (BMI) was calculated, and physical activity and performance were measured using the Physical Activity Scale in the Elderly, the chair rise time, the 6-minute walk, and measures of lower extremity strength and power. Serum estrone, estradiol, testosterone, and sex hormone binding globulin were measured.

Results. The prevalence of sarcopenia in nonobese, community-dwelling women who were long-term ERT users was 23.8%. Skeletal muscle mass correlated significantly with BMI, age at the time of starting ERT, hand grip strength, lower extremity strength and power, and testosterone level, but not with estradiol level. In linear regression analysis, BMI, leg press strength, and testosterone level contributed to adjusted ASM, accounting for 48.7% of the variance (p <.001).

Conclusions. Sarcopenia is as common in nonobese women who are long-term ERT users as in community-dwelling women not using ERT, suggesting that ERT does not protect against the muscle loss of aging. BMI, strength, and testosterone level contributed to appendicular skeletal mass in women. These data suggest that interventions to target nutrition, strength training, and testosterone replacement should be further investigated for their role in preventing muscle loss with age.

SARCOPENIA is the loss of muscle mass and strength associated with aging (1). Sarcopenia, defined in two different ways, is associated with disability (2,3). Although the causes of sarcopenia are not completely understood, it has been postulated that menopausal transition and loss of estrogen may play a role in muscle loss (4–7). Women lose fat-free mass and gain fat mass with the onset of menopause (6–10). The role of estrogen at menopause in the associated changes in body composition needs clarification. Current studies regarding the effects of estrogen on skeletal muscle mass have had conflicting results. One study found an association between the loss of estrogen at menopause and the loss of lean muscle mass (7), and another study found that muscle strength declined around menopause (11). However, most studies do not support these findings (10,12–16). Studies have found that use of hormone replacement therapy (HRT) does not prevent the menopausal changes in body composition (10) or improve appendicular skeletal mass (15). Increased strength has been associated with higher estrogen levels or estrogen replacement therapy (ERT) in cross-sectional studies (17,18), but this too is an inconsistent finding (14,19). There are no large studies of appendicular skeletal mass in older women who are long-term users of HRT. In this study, we determined the prevalence of sarcopenia in 189 community-dwelling older women who had been using ERT for at least 2 years. In addition, we evaluated the predictors of appendicular skeletal mass in this group.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 Conclusion
 References
 
We performed a cross-sectional analysis of baseline information obtained from women originally recruited to participate in a study of the effects of exercise in women using estrogen. Volunteers included 189 women older than age 59 who had been using ERT for at least 2 years. Exclusion criteria were current smoking, use of medications known to affect bone mineral density (calcitonin, bisphosphonates, prednisone >=5 mg/d, testosterone, phenytoin), prior hip fracture, body mass index (BMI) of greater than 30 kg/m2 (based on self-report of height and weight), history of cancer in the last 5 years (excluding skin cancer), or regular heavy resistance exercise. Baseline data collection included determination of body composition measured by dual x-ray absorptiometry (DXA), as well as height, weight, and dietary calcium and vitamin D intakes. We estimated physical activity using the Physical Activity Scale in the Elderly (PASE) (20). PASE includes questions about minutes of walking per day. Weekly walking was calculated by multiplying minutes of walking per day by the number of days walked each week.

Body Composition
Total and regional lean-tissue masses of volunteers were determined from a whole-body DXA scan using a DPX-IQ scanner (GE Medical Systems Lunar, Madison, WI); all scans were obtained by the same certified technician. The whole-body scan provided total lean body mass in kilograms, total fat mass in kilograms, and total body bone mineral content in kilograms. Appendicular skeletal muscle mass (ASM) was determined by combining the lean tissue mass of the regions of the arms and legs, excluding all other regions from analysis (21). We adjusted ASM for height by dividing each mass by the square of height (in meters squared). We used the definition of sarcopenia proposed by Baumgartner and colleagues (2), defined as an adjusted ASM greater than 2 SDs below the sex-specific mean from a young healthy reference population (5.45 kg/m2). Normative levels for adjusted ASM are taken from a previous study (2).

Performance Measures
Leg extension strength and power were measured on the Keiser sitting leg press; for 1 repetition maximum (22), intratester and intertester variability was less than 10%. Function was assessed using the chair rise time (23) and the 6-minute walk (23).

Biochemical Measurements
Blood and urine samples were collected between 0700 and 0900 hours after a 10- to 12-hour fast. Urine and serum were divided into 0.5-ml aliquots and stored at -70°C. Levels of estrone, estradiol, testosterone, and sex hormone binding globulin (SHBG) were determined in the General Clinical Research Center core laboratory by radioimmunoassay (Diagnostic Systems Lab, Inc., Webster, TX), with an intra-assay variability of less than 10%. The detection limit of the estradiol assay is 2 pg/ml. Testosterone levels were measured by enzyme-linked immunosorbent assay, with an intra-assay variability of less than 5.6% (Diagnostic Systems Labs, Inc.). The detection limit of the testosterone assay is 0.04 ng/dl. SHBG was measured by IRMA, with an intra-assay variability of less than 4% (Diagnostic Products Co., Los Angeles, CA).

Statistical Analysis
We used Pearson correlation coefficients to determine the association between adjusted ASM and years of ERT use, time since menopause, sex hormone levels, PASE, physical performance measures, power, strength, and health perception. We used multiple linear regression to evaluate the contributors to adjusted ASM and included years of ERT use, years since menopause, sex hormone levels, strength, power, physical activity, and performance. The SPSS statistical software package (version 10.0; SPSS, Inc., Chicago, IL) was used for all analyses.


   Results
Top
 Abstract
 Methods
 Results
Discussion
 Conclusion
 References
 
A total of 189 postmenopausal women with a mean ± SD age of age 67.4 ± 4.8 years (range, 59–78 years) participated in the study. Almost all of the women (99%) were white. The mean BMI was 24.4 ± 3 kg/m2, and 60% of the women had a BMI of less than 25 kg/m2. Descriptive characteristics and baseline physical performance scores are outlined in Table 1. The prevalence of sarcopenia was 23.8%, based on the definition of sarcopenia proposed by Baumgartner and colleagues (2). The variables that correlated with adjusted ASM are outlined in Table 2. BMI, strength measures, testosterone level, and age at the start of ERT correlated with adjusted ASM. Women who had a hysterectomy started ERT at earlier ages. There were no significant correlations between estradiol level, physical performance (chair rise time, 6-minute walk), physical activity (minutes walked per month or PASE score), or calcium and vitamin D intakes and adjusted ASM.


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  		Table 1. Descriptive Characteristics of Healthy Postmenopausal Women Using ERT (N = 189).

 

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  		Table 2. Correlation Between ASM Adjusted for Height and Measured Parameters in Healthy Postmenopausal Women Using ERT (N = 189).

 
Multiple linear regression analysis, with adjusted ASM as the dependent variable, revealed that BMI, leg press strength, and testosterone level contributed to adjusted ASM and accounted for 48.7% of the variance (B = 2.674, p <.001). Examining each variable independently, BMI accounted for 23.0%, leg press strength accounted for 22.7%, and testosterone level accounted for 3.0% of the variance in adjusted ASM (all p <.05).


   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
Conclusion
 References
 
We found that the prevalence of sarcopenia, as defined by an appendicular skeletal mass more than 2 SDs below a young adult norm established by Baumgartner and colleagues (2) was similar to that in postmenopausal women not receiving HRT (22.6%) (24). Using this definition, the prevalence rate in our cohort was over 20%. This suggests that sarcopenia is common in older women, and the use of ERT does not protect against the skeletal loss associated with aging.

In other studies that have reported the prevalence of sarcopenia, the use of HRT by women is not defined or is absent. Further, the prevalences of sarcopenia in these studies (2,3,12,25–27) have not differed markedly from those that we have found. The small differences may be explained by differences in the definition of sarcopenia used in the populations being studied or in the reference populations. There is no consensus definition of sarcopenia. Many methods have been used to measure skeletal muscle mass, including direct measurement by magnetic resonance imaging, computed tomography, or DXA scan, and indirect measurement by bioelectrical impedance, 24-hour urinary creatinine excretion, total body potassium determination, and estimation of total body protein using underwater weighing and total body water measurement (28–30). From these measurements, various definitions of sarcopenia have been proposed. Studies that have used DXA-derived estimates of sarcopenia (corrected for height) have found prevalences of sarcopenia similar to those we have found, but a lower prevalence of sarcopenia (11%) was found in a large epidemiologic study in which lean tissue mass (measured by bioelectrical impedance) was corrected for body weight (2). The two definitions of sarcopenia will, most likely, yield disparate results and identify different individuals as sarcopenic. This disparity in results from the two definitions of sarcopenia can be predicted from the strong associations between physical characteristics such as height and weight, and skeletal muscle mass. Each definition has predicted disability (2,3), but further work will be required to obtain the best definition of sarcopenia and its ability to predict health outcomes.

The small differences in prevalences between other studies using DXA to measure skeletal muscle mass can be explained by differences in the populations studied or sample size. Baumgartner and colleagues (2) reported a prevalence rate of 33.9% in a population-based sample, whereas we studied women volunteering for an exercise research program, a group more likely to be healthy and with the potential for healthier lifestyle and probable selection bias. In addition, Baumgartner and colleagues measured muscle mass in a subgroup and estimated skeletal muscle mass for the entire cohort, potentially introducing error. Tankó and colleagues (25) used the same definition as Baumgartner and colleagues but used a different reference population. They found the prevalence of sarcopenia to be 12.3%; their population seems the most similar to the population that we studied, although differences do exist. Differences in prevalences between our groups may be explained by the different reference population, the smaller sample size in the study of Tankó and colleagues, or differences in the exclusion criteria. We excluded women who performed regular heavy resistance exercise, whereas Tankó and colleagues had no such exclusionary criterion, although we do not believe that this contributed to the difference in prevalence. More importantly, we excluded women who were obese and who had a normal bone mineral density, criteria that may have introduced differences given the strong correlation between BMI and appendicular skeletal muscle mass.

Long-term prospective studies are required to evaluate the appropriate definition of sarcopenia and its impact on health-related outcomes such as quality of life, disability, and mortality. Baumgartner and colleagues (2) and Janssen and colleagues (3) have reported increased disability rates in a older adults with sarcopenia, and several investigators have reported association of poor outcomes such as hospitalization (31), disability (32), or mortality (32,33) with performance measures that rely on muscle mass.

Predictors of skeletal muscle mass in this cohort included BMI, strength, and testosterone level, but not ERT use. Cross-sectional studies have reported that menopause leads to changes in body composition, including a decrease in fat-free muscle mass and an increase in fat mass (6–10). Women using ERT are stronger (17,18), but this may be the result of selection bias and not the effects of estrogen. Women using ERT may be healthier, more active, or more physically fit, or they may have better nutritional intake, which may result in greater muscle mass and strength (34). Our results are consistent with those of Aloia and colleagues (10), which indicated that women using HRT did not differ in lean body mass through the menopausal transition from those not using HRT. Further, in a study of postmenopausal women, no differences in appendicular muscle mass were found after 6 months of HRT use (15). In fact, Gower and Nyman (13) speculate that HRT use may decrease bioavailable testosterone levels and thereby increase loss of skeletal muscle mass.

BMI has been a consistent predictor of skeletal mass in several studies (12,24–27). This finding points to the need for further studies of the impact of nutritional factors or the inflammatory process on cachexia to understand the components of sarcopenia. Decreased protein intake, vitamin D insufficiency, and increased catabolic cytokine levels have been associated with decreased strength or physical performance (35–38). Strength, similarly, has been found to be associated with muscle mass in studies of men (39,40), but strength measurements have not been a frequent part of ASM assessments in women (24,25) or have not been found to be associated with adjusted ASM (12). Regardless, studies of strength training in older adults demonstrate significant gains in strength and lean tissue mass (22,41). Testosterone levels explain a small portion of the variance in skeletal muscle mass. Testosterone has known anabolic properties in muscle and has been found to be associated with ASM in men (12,24) but not in women (12). Interestingly, there is a direct correlation between the age at the start of ERT use and ASM that is lost when women experiencing menopause before age 45 are excluded, suggesting that hysterectomy with oophorectomy (resulting in testosterone withdrawal) is the factor behind this correlation. Previous studies have found that total lean mass correlates with bioavailable testosterone levels in postmenopausal women (13), and lower body strength increases in women treated with an estrogen and androgen preparation (42). No studies have assessed the effects of testosterone replacement on sarcopenia or function in older women.


   Conclusion
Top
 Abstract
 Methods
 Results
 Discussion
 Conclusion
References
 
Our study demonstrates that sarcopenia, defined as ASM corrected for height measured by DXA, is present in 23% of healthy independent older women who are long-term ERT users. This prevalence does not differ from that of another large group of healthy older women not using estrogen. Although the definition and importance of sarcopenia needs clinical clarification, ERT does not appear play a protective role. ASM was associated with body mass index, strength, and testosterone levels, suggesting areas to address with further research for the prevention of skeletal muscle loss and functional decline.


   Acknowledgments
 
This work was supported by General Clinical Research Center (MO1-RR06192) and by Claude Pepper OAIC (5P60-AG13631). Dr. Kenny was supported with fellowships from the Brookdale Foundation and the Paul Beeson Faculty Scholar Program.

Address correspondence to Anne Kenny, MD, Center on Aging, MC-5215, University of Connecticut Health Center, Farmington, CT 06030-5215. E-mail: kenny{at}nso1.uchc.edu

Received October 7, 2002

Accepted October 10, 2002


   References
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 Abstract
 Methods
 Results
 Discussion
 Conclusion
 References
 

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