1 Department of Health Studies and The Alfred P. Sloan Working Families Center on Parents, Children, and Work, University of Chicago, Chicago, IL.
2 Department of Medicine, Section of Cardiology, Rush University Medical Center, Chicago, IL.
3 Department of Preventive Medicine, Rush University Medical Center, Chicago, IL.
4 Institute for Healthy Aging, Rush University Medical Center, Chicago, IL.
5 Department of Pediatrics, David Geffen School of Medicine at the University of California Los Angeles, Los Angeles, CA.
6 Department of Pediatrics, University of Chicago, Chicago, IL.
7 Department of Internal Medicine, University of Chicago, Chicago, IL.
8 Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI.
9 Department of Health Sciences, University of York, York, United Kingdom.
Received for publication October 13, 2003; accepted for publication March 24, 2004.
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ABSTRACT |
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African Americans; aging; European continental ancestry group; exercise; hand strength; hormone replacement therapy; menopause; womens health
Abbreviations: Abbreviations: CI, confidence interval; HRT; hormone replacement therapy; SWAN, Study of Womens Health Across the Nation.
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INTRODUCTION |
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Evidence is emerging that women of different races experience the menopausal transition differently (1114). For example, while Caucasian women report psychosomatic symptoms more frequently, African-American women more often report vasomotor symptoms (11, 12). Furthermore, estradiol and dihydroepiandrosterone sulfate levels decrease more rapidly during the late stages of the menopausal transition in African-American women than in Caucasian women (14). If changes in physical function are mediated by declines in estrogen, then African-American women might experience a more rapid decline in physical function over the menopausal period than Caucasian women do. To our knowledge, no published longitudinal studies have explicitly considered whether race modifies the relation between menopause and physical function.
The primary goal of this longitudinal study was to assess the impact of the menopausal transition on grip and pinch strength in a population sample of middle-aged African-American and Caucasian women. The secondary goal was to determine whether changes in grip or pinch strength varied by use of HRT.
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MATERIALS AND METHODS |
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Procedures
The institutional review boards of Rush University Medical Center and the University of Chicago approved this study. Beginning in January 1996, trained interviewers screened women with telephone interviews and home visits. Eligible women who agreed to participate underwent a baseline interview83 percent within the next month. Interviews took 34 hours and consisted of questions about medical history, reproductive and menstrual history, lifestyle, psychosocial factors, and physical symptoms as well as brief physical and cognitive tests (16). Follow-up assessments were conducted annually. At baseline, participation rates were 72 percent for both African-American and Caucasian women. At the three successive follow-up visits, retention rates among surviving participants who completed the baseline interview were 77, 74, and 77 percent for African-American women and 83, 84, and 85 percent for Caucasian women.
Outcome variables
Beginning in August 1997, grip and pinch strength were measured at the Chicago site with a standard handgrip dynamometer and pinch gauge (Baseline Corp., Irvington, New York), respectively. Participants were seated, with the elbow against the side of the body and the lower arm at a right angle to the body. For grip strength, the hand was parallel to the body and the wrist was bent slightly backward. Participants performed three grip tests with each hand. For pinch strength, the hand was parallel to the floor, and measures were taken in three positions: 1) the thumb tip to the tip of the index finger, 2) the thumb tip to the side of the middle portion of the index finger, and 3) the thumb tip to the tips of both the index and middle fingers. Three pinch tests were performed in each position with each hand. For both grip and pinch strength, measurements were recorded in kilograms and were rounded up to the nearest kilogram, with values averaged across hands. The averaged grip and pinch strength measures were analyzed as continuous variables. Annual quality control procedures assessed interviewer drift.
Main predictor variables
Race was self-reported as African American or non-Hispanic Caucasian (the referent category), following the convention used in the 2000 US Census (17). Menopausal status, assessed annually, was defined by bleeding criteria, as follows, and was modeled categorically: premenopausal (having menstruated within the last 3 months without irregularity (the referent category in analyses)), early perimenopausal (experiencing menstrual irregularities but having menstruated within the last 3 months), late perimenopausal (having menstruated within the last 12 months but not within the last 3 months), and postmenopausal (having had no menstrual period within the last 12 months). To be eligible for participation in the SWAN study, all women had to be either premenopausal or early perimenopausal at baseline. At follow-up visits, menopausal status was coded as undetermined for those women for whom menopausal status could not be clearly specified either because of nonconformity with bleeding criteria or because medication usage affected menstrual cycles. Use of HRT in the period since enrollment, including estrogen pills, patches, or oral contraceptives, was self-reported and was modeled as a binary variable.
Covariates
Covariates included time (i.e., study visit), age, household income, body mass index, smoking, and physical activity. Self-reported annual income was divided into five categories. Body mass index was calculated as weight divided by height squared (kg/m2). Standardized protocols were used to measure weight and height (15). Physical activity was measured by using a questionnaire adapted from Baecke et al. (18) that assessed frequency of activities in three domains: sports, household/child care, and nonsport leisure-time or daily routine. Domain-specific scores, ranging from 1 to 5, were assigned based on the average of individual items within each domain, with higher scores indicating more physical activity. A total physical activity score was calculated as the sum of the domain-specific scores, with a range of 3 to 15. The total score was used in the analyses. Smoking status was categorized as never, former, or current smoking.
Inclusion criteria
To be eligible for inclusion in the primary analyses for this paper, participants had to have pinch or grip strength measurements from at least two annual study visits. Of the initial 868 women included in the Chicago SWAN cohort, 563 met these criteria. Fourteen women who reported having had a stroke prior to or during the study or who had an unknown stroke history were excluded from analyses, and 25 women who experienced surgical menopause during the study period were included only until the time of surgery.
For secondary analyses of HRT use and changes in grip and pinch strength, eligible participants were required to have data on HRT use and grip or pinch strength measurements from at least two of the three follow-up visits. All women were non-HRT users at baseline, per SWAN eligibility criteria; therefore, analyses of HRT use excluded baseline data. Criteria for stroke history and surgical menopause were the same as those for the primary analyses. Data on a total of 550 women were included in the final analyses.
Statistical analysis
To examine whether menopausal status predicted changes in grip or pinch strength over 3 years and whether these changes varied by race, we included in the first model menopausal status at each visit as the main predictor and a term for time (i.e., study visit), with separate analyses for grip and pinch strength. Subsequently, we added a term representing race and then menopausal-status-by-race and time-by-race interaction terms. Adjusted analyses included age, body mass index, income, smoking status, and physical activity as covariates. Our analyses of the three hand positions for pinch strength yielded similar results. For ease of presentation, here we report the results for only the second pinch measurement and hereafter refer to it as pinch strength.
To assess whether HRT use influenced grip or pinch strength, we fit a model with HRT use at each follow-up visit as the main predictor and included the menopausal status categories and a term for time. Subsequently, a term for race was added to the model and then the HRT-use-by-race interaction term. Further statistical adjustments were made for age, body mass index, income, smoking status, and physical activity.
We used generalized estimating equations to account for the lack of independence among repeated measures within subjects. Because grip and pinch strength were continuous variables with normal distributions, we used linear regression. After examining the correlation matrices for pinch and grip strength within subjects, we selected an exchangeable correlation structure. Empirical standard error estimates were used because they are robust and do not depend on the correctness of the structure imposed on the working correlation matrix (19). When the normal errors structure assumption is met, there should be no difference between generalized estimating equations models and mixed models (20). Mixed models including random intercepts yielded essentially the same results as the generalized estimating equations models; for simplicity, here we present results from the generalized estimating equations analysis only. All analyses were conducted by using the GENMOD procedure in SAS, version 8 software (SAS Institute, Inc., Cary, North Carolina).
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RESULTS |
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No significant menopausal-status-by-race or time-by-race interactions were observed, without or with risk factor adjustments. Consequently, the adjusted models we report on include terms for the main effects for menopausal status and race but exclude the interaction terms.
After adjustment for all covariates, the association between late perimenopausal status and grip strength became marginally significant, although the size of the difference between late perimenopausal and premenopausal women was unchanged (table 3). In the adjusted analyses, the difference in grip strength between postmenopausal and premenopausal women increased slightly and was marginally significant (table 3). Race remained a significant predictor of grip strength; African Americans had greater strength than Caucasians did. Both body mass index and physical activity were positively and significantly associated with grip strength. Age was not significantly associated with grip strength.
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As with grip strength, no significant interactions between race and menopausal status or between race and time were observed with pinch strength as the outcome, with or without adjustment for risk factors. Thus, the risk-factor-adjusted models reported on here include only the main effects of race and menopausal status.
The associations between progression to postmenopausal or early perimenopausal status and decline in pinch strength were relatively unchanged after adjusting for all covariates (table 3). Race remained a highly significant covariate. Total physical activity and body mass index were positively and significantly associated with pinch strength. Age was not significantly associated with pinch strength.
HRT use and grip and pinch strength
By the third follow-up visit, approximately twice as many Caucasians as African Americans reported HRT use (14.2 vs. 7.3 percent, chi-square test = 5.6 (1 df); p = 0.02). In unadjusted analyses, women who became HRT users had marginally greater grip strength compared with non-HRT users (1.15 kg, 95 percent CI: 0.12, 2.41; p = 0.08). However, a significant race-by-HRT-use interaction term (ß = 2.02, 95 percent CI: 0.02, 4.03; p = 0.05) showed that African-American HRT users had significantly increased grip strength, whereas Caucasian HRT users did not. This interaction was unchanged after subsequent adjustment for covariates. In addition, with adjustment for these factors and HRT use, we observed significant declines in grip strength among postmenopausal women (1.39 kg, 95 percent CI: 2.80, 0.02; p = 0.05) and late perimenopausal women (0.93 kg, 95 percent CI: 2.02, 0.16; p = 0.10). Body mass index and physical activity were both highly significant covariates (p = 0.01 and p < 0.0001, respectively).
HRT use was not related to pinch strength, with or without covariate adjustment. Furthermore, we found no evidence of a race-by-HRT-use interaction for pinch strength.
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DISCUSSION |
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The results of our study are consistent with the hypothesis that changes in hormonal status from pre- to postmenopause contribute to declines in physical function. Studies have shown a greater decline in fine dexterity and hand strength with aging in women than in men (21); it is possible that this difference is attributable to changes in estrogen levels in aging women. For example, estrogen could influence the number of or force production of cross-bridges in the muscle (22, 23). While normative aging data consistently document a greater decline in pinch versus grip strength, our data revealed a greater decline in pinch versus grip strength in relation to menopausal status, possibly due to the impact of hormones on the sensory aspect of motor function. Pinch is a more precise movement than grip, requiring refined tactile afferent input to coordinate the movement and maximize force output (24). The peripheral and central nervous systems contain estradiol-sensitive cells that respond to the absence of ovarian steroids (25), and we hypothesize that sensory integration for pinch, compared with grip, may be impacted more substantially by hormone status. However, an explicit test of this hypothesis awaits data on the pattern of change in endogenous hormones in women transitioning through menopause.
Prior studies of the relation between menopausal status and physical function have been inconsistent. Several cross-sectional studies showed no differences among women in different menopausal stages regarding strength (handgrip or leg strength) (6) or cardiorespiratory fitness (4, 10). In contrast, Petrofsky et al. (2) showed that grip strength was significantly weaker in postmenopausal women than in premenopausal women, even after controlling for age. Phillips et al. (3) observed a dramatic decline in pinch strength around the time of menopause, although they did not formally test this observation. The association between menopausal transition and declining grip and pinch strength observed here is bolstered by the fact that we used a longitudinal design that included a population-based sample of African-American and Caucasian women. However, a relatively small proportion of our participants had become postmenopausal after 3 years of follow-up. In addition, the clinical significance of the declines in grip and pinch strength that we observed was not evaluated. Thus, more longitudinal studies are needed to confirm that the menopausal transition negatively influences overall physical function.
It is possible that the observed declines in grip and pinch strength are attributable to motivational deficits due to psychological changes associated with the menopausal transition. To test this hypothesis, we ran additional generalized estimating equations models using continuous depressive symptom scores as a time-dependent covariate in the fully adjusted models. Depressive symptoms were not significantly associated with grip or pinch strength, and the results for the main predictors and other covariates remained unchanged, indicating that the changes in grip and pinch strength observed were likely not due to psychological factors.
In our study, African-American women had greater grip and pinch strength than Caucasian women did, but we did not observe a significant race-by-menopausal-status interaction. Few prior studies of menopause and physical function have specified the race of the participants; in those that did, participants were primarily Caucasian (5, 8). In the cross-sectional screening survey for the SWAN study (1), Caucasian women were most likely to report "some" limitations, whereas African-American women were most likely to report "substantial" limitations. However, that report assessed self-reported global physical functioning and not a specific parameter of function.
Interestingly, after controlling for menopausal status and other covariates, we observed no significant effect of age on either grip or pinch strength. Many cross-sectional studies have shown decreases in strength or cardiorespiratory fitness with advancing age (24, 6, 26); however, most studied women over a wide range of ages, including some women in their second decade. The women in our study were between 42 and 52 years of age, and we followed them for just 3 years. It is possible that the women in the SWAN study are still too young to suffer age-related decrements in hand strength, that our follow-up period is still too short, or that we lacked the variation in age necessary to detect an effect.
We observed a positive association between total physical activity and both grip and pinch strength. This result is consistent with the findings of Cauley et al. (26), who showed that physical activity was positively associated with muscle strength in postmenopausal women. Physical activity may influence ones performance on grip and pinch testing through a variety of metabolic and neurologic mechanisms, both central and peripheral (27). However, the interplay of sex hormones in these various domains remains to be fully elucidated. Although we did not explicitly test this possibility, it is reasonable to expect that increasing physical activity could minimize losses in strength that accompany menopause.
HRT use was unrelated to pinch strength in our study. We did observe a significant race-by-HRT-use interaction for grip strength, however. African-American women who initiated HRT use during the study had increased grip strength, whereas Caucasian women did not. These results must be interpreted with caution, because relatively small numbers of women used HRT during the course of the study. Prior research on HRT and strength is inconsistent with some studies finding a protective effect of HRT use on muscle strength and exercise capacity (3, 9, 28, 29) and other clinical trials and cross-sectional studies reporting no effect (5, 8, 26, 30). When the SWAN study was initiated, it was even found that hormone use was significantly associated with substantial physical limitation, as measured with Short Form-36 from the Medical Outcomes Survey (1, 31). Now that significant risks of heart disease, stroke, and breast cancer have been linked to HRT (3234), its use has declined dramatically, and physicians are no longer recommending HRT for long-term health benefits. As HRT use declines, it is unlikely to impact menopause-related declines in strength or physical function.
To our knowledge, this is the first longitudinal study to document the effects of the natural menopausal transition on changes in physical function in a biracial, population-based sample. We observed declines in grip and pinch strength among women who became postmenopausal over the 3-year follow-up period relative to women who remained premenopausal. Early perimenopausal women also experienced significant declines in pinch strength relative to premenopausal women. It is possible that reduced levels of estrogen or changes in other reproductive hormones are responsible for the decline in strength observed. Continued data collection will further elucidate the effects of menopausal status and hormonal changes on physical function in women.
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ACKNOWLEDGMENTS |
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This study reports on data collected at the Chicago Clinical Center: Rush University Medical Center, Chicago, IllinoisDr. Lynda Powell, Principal Investigator (grant U01 AG12505). National Institutes of Health Project Office: National Institute on Aging, Bethesda, MarylandDrs. Sherry Sherman and Marcia Ory; National Institute of Nursing Research, Bethesda, MarylandDr. Carole Hudgings. Coordinating Center: New England Research Institutes, Watertown, MassachusettsDr. Sonja McKinlay, Principal Investigator (grant U01 AG12553) 19952001 and/or the University of Pittsburgh, Pittsburgh, PennsylvaniaDr. Kim Sutton-Tyrrell, Principal Investigator (grant U01 AG12546) 2001present. Steering Committee Chairs: Drs. Chris Gallagher (19951997), Jenny Kelsey (19972002), and Susan Johnson (2002present).
This paper originated as a student project in an advanced epidemiologic methods class taught by Dr. Kate E. Pickett at the University of Chicago. The project was developed by then-students Drs. Martha Gulati, Lianne M. Kurina, Paul J. Chung, Namratha Kandula, Renata Lukezic, and Nicole J. Cohen.
The authors thank Chicago SWAN Project Director Deidre Wesley and the study staff of the Chicago site. The authors also thank Drs. Diane S. Lauderdale, Peter Meyer, Paul Rathouz, and Ronald A. Thisted for their assistance with this manuscript.
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NOTES |
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Correspondence to Dr. Lianne M. Kurina, Department of Health Studies, University of Chicago, 5841 South Maryland Avenue, MC2007, Chicago, IL 60637-1470 (e-mail: lkurina{at}uchicago.edu).
Drs. Lianne M. Kurina and Martha Gulati made equal contributions to this work and share primary authorship.
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REFERENCES |
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