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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 61:1194-1200 (2006)
© 2006 The Gerontological Society of America

Correlates of Decline in Lower Extremity Performance in Older Women: A 10-Year Follow-Up Study

Kimberly Y. Z. Forrest, Joseph M. Zmuda and Jane A. Cauley

1 Department of Health and Safety, Slippery Rock University of Pennsylvania.
2 Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pennsylvania.

Address correspondence to Kimberly Y. Z. Forrest, PhD, Department of Health and Safety, Slippery Rock University of Pennsylvania, Slippery Rock, PA 16057. E-mail: kimberly.forrest{at}sru.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. Decline in lower extremity performance increases the risk of functional disability. This study examined the correlates of decline in lower extremity performance in older women.

Methods. A total of 5178 women aged 65–91 years were recruited from population-based listings from four centers in the United States. Clinical examinations were performed and lifestyle information was obtained at baseline and 10 years later. Lower extremity performance was measured by walking speed (meters/second) and time (seconds) to complete five chair-stands. Changes were calculated by subtracting baseline values from follow-up values.

Results. During the 10-year follow-up period, walking speed declined 17% and time to complete five chair-stands increased 22% (p <.0001). The decline in performance during the follow-up increased with baseline age: women aged 65–69 years experienced an 11% decline in walking speed and a 16% increase in the time to complete five chair-stands, while women aged 80 years or older experienced a 37% decline in walking speed and a 38% increase in chair-stand time. After adjusting for age, baseline physical performance, greater weight, greater height loss, smoking, history of arthritis and diabetes, and use of thyroid and estrogen medications were independently related to greater declines in lower extremity performance.

Conclusions. Lower extremity performance decreased dramatically with advancing age in older women. Effective management of common diseases, such as arthritis and diabetes, and a healthy lifestyle, including avoidance of smoking and weight control, could help older women maintain their lower extremity physical functions.

LOWER extremity function, as indicated by timed gait over a measured course and ability and time to complete five repeated chair-stands, gives insight on the health status and disability risk of individuals and populations (1–5). Evaluation of both the extent and rate of change in these parameters and identification of correlated factors that may impact on these changes can provide useful information for projecting or estimating functional dependency as the population ages. The present study prospectively examined the decline in lower extremity performance, measured by walking speed and time to complete five chair-stands across age groups and risk factors for this decline, in a large community-based population of older women followed longitudinally over 10 years.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Study Population
The women involved in the current analysis were enrolled in the Study of Osteoporotic Fractures (SOF), a longitudinal study of risk factors for fractures (6). The inclusion criteria included community residents (noninstitutionalized) and the ability to walk without the assistance of another person. Women with bilateral hip replacement were excluded; black women and men were also initially excluded because of their low incidence of hip fracture. During the period 1986–1988, 9704 women were recruited from population-based listings of women aged 65 years or older in four clinical centers of Portland, Oregon; Minneapolis, Minnesota; Monongahela Valley near Pittsburgh, Pennsylvania; and Baltimore, Maryland. After a baseline evaluation, the SOF participants were examined biennially. Institutional Review Boards of all four centers gave approval for this study, and all participants signed written informed consent forms.

The data used for the current analysis represent data from the baseline and tenth-year clinic visits of the SOF study. Due to the small number of women of other races (n = 33), the current study focused on 9671 Caucasian women. We excluded women from the analysis if they did not have measures of walking or chair-stand test at baseline (n = 25) or from the Year 10 clinic visit (n = 4468), of whom 2696 died and 320 were lost to follow-up. The remaining women might have been institutionalized or too sick to complete the test. Compared to the women included in the current analysis (n = 5178, 78% of survivors), women who were excluded from the current analysis (n = 4493) were older, had a lower physical activity level, were more likely to be currently smoking but less likely to use alcohol, had a higher prevalence of medical conditions, were more likely to use medications, had a slower walking speed, and required more time to complete five chair-stands at baseline (all p values <.01) (Table 1). The percentage of women without a follow-up visit increased with baseline age: 33%, 46%, 61%, and 80% for women aged 65–69, 70–74, 75–79, and 80+ years, respectively. The main reasons for not returning to the clinic were death and institutionalization.


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  		Table 1. Comparison of Baseline Characteristics between Participants Included and Not Included in the Current Analysis.

 
Measurements of Lower Extremity Performance
Lower extremity performance was measured by a walking test and chair-stand test. During the walking test, study participants were asked to walk, from a standing start, at their usual pace over a 6-meter course. The number of seconds used to complete the course was recorded using a stopwatch. Two trials were performed, with the average walking speed (meters/second) used in the current analysis. In the chair-stand test, the participants were asked to sit and stand up from a standard chair consecutively five times without using their arms if possible, and the number of seconds used to complete the trials was recorded. Whether or not a participant used her arms to stand up during the test was recorded as well. Changes in lower extremity performance during follow-up were calculated by subtracting baseline values from follow-up values measured at the 10th clinical visit. To adjust for baseline values, percentage change was also calculated as ({follow-up measures – baseline measures}/baseline measures) * 100.

Other Measurements
SOF participants were interviewed and examined using standard protocols as previously described (16). Weight (kg) was measured with a balance beam scale, and height (cm) was measured with a wall-mounted stadiometer. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2). Waist girth and hip girth were measured, and the waist-to-hip ratio (WHR) was computed. Participants were asked if a doctor ever told them that they had osteoporosis, arthritis, diabetes, hyperthyroidism, back pain, or stroke. Information on coronary heart disease was obtained at visit 2 which was conducted 2 years after baseline visit. Blood pressure was measured using a standard protocol. Women were also asked to rate their overall health in comparison to others of similar age (excellent/good/fair vs poor/very poor).

Current smoking status (former/current/never) and smoking history were assessed. The number of packs of cigarettes smoked per day and the number of years smoked over a lifetime were recorded and summed as pack/years (this value is 0 if an individual never smoked). Information on alcohol use was obtained as number of drinks per week, and heavy alcohol use, defined as ≥9 drinks/week, was used in the analysis. The Paffenbarger questionnaire (7) was used to assess physical activity in the past year estimated as total energy expenditure. Leisure-time physical activities were attributed an intensity weighting of 5 kcal/min for low intensity, 7.5 kcal/min for medium intensity, or 10 kcal/min for high intensity; each city block walked was assigned 8 kcal/min, and each stair climbed was assigned 4 kcal/min. Used in the current analysis was the total physical activity index, expressed in kcal/wk, which was the sum of kilocalories expended in all activities mentioned above. Information on caffeine intake was also obtained, and lifetime caffeine intake amount (grams) was used in the current analysis.

Statistical Analyses
Descriptive statistics (independent t tests for continuous variables and chi-square tests for categorical variables) were used to compare baseline characteristics of the study participants to those who were excluded from the current analysis. To evaluate the relationship between changes in lower extremity performance during 10 years of follow-up and other variables, age-adjusted bivariate regression was used. Multiple regression models were utilized to identify independent predictors of change in walking speed over 10 years of follow-up. A total of 4858 women had no missing values for all related covariate measures and were included in the multiple regression analysis of change in walking speed.

Among the participants included in the current analysis, 253 women had no measures for the chair-stand test at the 10th year follow-up visit due to an inability to complete the test. We formed a group of study participants (n = 1731) with a decreased performance of chair-stand test defined as: 1) being in the top quartile of increased percent time to complete five chair-stands over follow-up; 2) those who were able to complete the chair-stand test at baseline but unable to complete the same test at the follow-up visit (with missing data for this measured at follow-up visit); and 3) those women who did not use their arms to complete five chair-stands at baseline but had to use their arms to complete the same test at the follow-up visit. This group of women was compared to the remaining women using multiple logistic regression to examine the independent risk factors for decreased chair-stand performance. A total of 4885 women had no missing values for all related covariate measures and were included in this multiple logistic regression analysis of decline in chair-stand ability.

All variables with a significant bivariate association (p <.05) with lower extremity performance measures were included in the multivariate models with a stepwise selection method. Variables with a skewed distribution were logarithm-transformed and included smoking (pack/years), alcohol use, and physical activity. Significant interactions between age and other covariates were evaluated. To avoid issues of collinearity, for highly correlated variables within a category of exposure (e.g., weight and WHR), we selected the variable that demonstrated the strongest univariate association with the outcome. The significance level for all analyses was 0.05. The criterion for a factor to be retained in the multivariate model was p value < 0.05. No outliers were excluded from the analyses. All analyses were performed using SAS (V8.2; SAS Institute Inc., Cary, NC).


   RESULTS
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 Methods
 Results
Discussion
 References
 
The average age of the study population was 70.1 ± 4.2 years at baseline, with a range of 65–91 years. The mean weight of the women in this study was 67.5 ± 12.1 kg and mean height was 159.5 ± 5.9 cm. Approximately 5% of the women used alcohol heavily (>9 drinks/week), and the current smoking rate was 8.1%. The prevalence of some common health problems was 12.8% for osteoporosis, 61.9% for arthritis, 67.0% for back pain, 4.6% for diabetes, 6.3% for coronary heart disease, and 1.9% for stroke. Less than 1% of women rated themselves as having poor health status (Table 1).

At baseline, the average walking speed of the women included in the current study was 1.1 ± 0.2 m/s, and the mean time to complete five chair-stands was 11.6 ± 3.6 s (Table 1). Over the 10 years of follow-up, walking speed decreased 17 ± 24% and time to complete five chair-stands increased 22 ± 44% (both p values <.0001). With increasing age, lower extremity performance decreased (Figure 1). Walking speed declined 11% among women aged 65 to 69 years compared to 37% among women aged 80 years or older. The time to complete five chair-stands increased 16% among women aged 65 to 69 years compared to 38% among women aged 80 years or older.


Figure 01
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  		Figure 1. Change in lower extremity performance during 10 years of follow-up by age

 
Changes in walking speed and time to complete five chair-stands were negatively correlated with their baseline measures (p value <.0001). Although women who had better performance at baseline tended to perform better at the follow-up, women who were in the fastest walking speed tertile at baseline experienced a 21% decline in walking speed compared to 11% among women who were in the slowest walking speed tertile at baseline. The difference in loss of performance was even greater for the chair-stand test (36% vs 9%) between women in the top tertile (fastest) versus the lowest tertile (slowest).

Table 2 lists the coefficients from age-adjusted and multivariate regression models for change in walking speed during the 10 years of follow-up. Older age, greater weight, shorter height, greater height loss over follow-up, higher systolic blood pressure, greater lifetime smoking, greater baseline walking speed, history of arthritis and diabetes, and use of thyroid supplements and estrogen were independently associated with a greater decline in walking speed. These variables explained 31% of the model variance. Some variables, such as weight loss, were associated in age-adjusted models but not in multivariate models.


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  		Table 2. Age-Adjusted and Multivariate-Adjusted Regression Coefficients for Changes in Walking Speed During 10-Years of Follow-Up.

 
Similar correlates were observed for decline in chair-stand performance (Table 3). A 5-year increase in age was associated with a 63% increased odds of experiencing the greatest decline in chair-stand function that was independent of other factors, including poor health status. Other significant variables in the multivariate model included greater weight, greater height and height loss, lifetime smoking, history of arthritis, diabetes, and use of thyroid supplements and thiazide diuretics.


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  		Table 3. Selected Characteristics, Age-Adjusted OR and Multivariate-Adjusted OR for Greatest Decline{dagger} in Ability to Complete Five Chair-Stands Test During 10-Years of Follow-Up.

 

   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
The current study prospectively examined the pattern of decline in lower extremity performance, as measured by walking speed and time to complete five chair-stands, and factors associated with the decline in a large community-based population of older women followed over 10 years. Walking speed declined 17% and time to complete five chair-stands decreased by 22%. The decline in performance was greatest among women aged 80 years or older. In addition to age and baseline performance, greater weight, greater height loss, presence of arthritis and diabetes, and use of thyroid and estrogen medications were independently related to greater declines. Our results revealed several modifiable factors that could help older adults maintain their physical function into older age.

Although women who performed better at baseline tended to maintain their initial advantage, they experienced a greater decline during follow-up compared with women with weak performance at baseline. Rantanen and Heikkinen reported a similar result (8). Individuals with weak performance at baseline had less room for change than those with better performance. This phenomenon suggests that older adults who have adequate lower extremity function may experience more noticeable decline in performance with age.

Aging itself had a significant impact on the decline in lower extremity performance even after controlling for a variety of age-associated factors. The age association may reflect a number of factors including over production of proinflammatory cytokines (9,10), declines in sex steroid hormones (11,12), and declines in growth hormone and insulin-like growth factors (13).

Greater height was associated with slower declines in walking speed, consistent with findings from Buchner and colleagues (14). This may reflect a longer stride length in taller individuals and faster walking speeds. However, greater height was associated with greater declines in the time to complete five chair-stands. The reason for this is unknown but may reflect longer leg length and decreased ability to push off from the floor. Greater height loss over the follow-up contributed to greater loss of physical function measured by both walking speed and chair-stand tests in this study population. Height loss might act as an overall marker for frailty and possibly changes in body composition. For example, height loss could reflect vertebral fractures, which have been associated with functional limitations (15).

Lifetime smoking exposure had a significant influence on the loss of physical function. Women who reported a greater number of packs of cigarettes smoked per year were more likely to experience greater decline in walking speed and increased time to complete five chair-stands. This association is not surprising given the multiple chronic conditions associated with smoking, although we adjusted for several of these in our model. The observation is consistent with our cross-sectional observation of the association between poor neuromuscular function and smoking (16).

Physical activity has been consistently shown to help maintain or improve muscle strength and physical function in older adults (17–20). However, physical activity was not associated with decline in lower extremity performance in this study population. This may reflect the difficulty in measurement of physical activity. Alternatively, low physical activity could be a marker for chronic illness. When specific medical conditions were entered into the model, the relationship between physical activity and performance became trivial (data are not shown).

Increased weight was found to be associated with a greater decline in lower extremity performance. Knee osteoarthritis, which is common among overweight people (21), might contribute to decreased lower extremity performance. We adjusted for self-report of arthritis, but this may be a marker of the overall osteoarthritis burden and could include hand osteoarthritis, which is unlikely to influence lower extremity performance. Studies have demonstrated that inflammatory cytokines, including interleukin-6 and tumor necrosis factor-alpha, are secreted by adipose tissue explants from obese and normal weight individuals (22,23). This evidence has lead to the hypothesis that obesity may represent a low-grade chronic inflammatory state (24,25). Thus, the association between increased weight and greater decline in lower extremity performance may also reflect proinflammatory cytokines.

Use of thyroid supplement hormones was related to a decreased lower extremity performance measured by both the walking speed and chair-stand test. Both hypothyroidism and hyperthyroidism may cause signs and symptoms of neuromuscular dysfunction (26). Use of the thyroid hormones may reflect a history of hypothyroidism, but could also reflect exogenous overuse of thyroid hormone, both of which could lead to decreased muscle strength and performance. The association may reflect impaired muscle energy metabolism (27), which leads to weakness and decreased ability to complete these performance tests. Future studies should include biochemical evidence of thyroid disease by specifically measuring thyroid-stimulating hormone and relating this to longitudinal changes in physical performance.

Estrogen use was independently related to a faster decline in walking speed. Although it was not significant in the multivariate model, estrogen use also accounted for a 23% increase of odds for experiencing declined chair-stand performance. The association between hormone use and neuromuscular function is mixed. Previously in SOF, we reported no cross-sectional association between estrogen use and neuromuscular function or falls (28). We also found that postmenopausal estrogen use was associated with an increased likelihood of back pain in impaired back function (29), both of which could influence lower extremity performance. However, a number of studies, both cross-sectional and experimental, have found positive associations between hormone therapy and muscle performance (30–32). As part of the Health, Aging and Body Composition Study, current use of hormone therapy was associated with greater quadriceps muscle area and greater grip strength, although the magnitude of the effects was modest and did not translate into improved physical function (33). An association between hormone use and muscle function is biologically plausible since skeletal muscle does have estrogen receptors (34). However, selection factors for estrogen use are well established (35) and these observations may reflect residual confounding. Results from randomized trials such as the Women's Health Initiative are needed to delineate the role of postmenopausal hormone therapy on maintenance of physical function.

Arthritis, back pain, diabetes, and high blood pressure are common health problems in older adults, and all of these conditions were independently associated with greater declines in lower extremity performance. Diabetes has been associated with an increased incidence of functional disability (36) and weaker muscle strength (37). It is not known if this is a causal association or reflects complications related to the diabetes. Nevertheless, the results may suggest that prevention of diabetes and control of diabetes could improve functional performance in older individuals. Osteoarthritis is the most common joint disease and is one of the most frequent causes of loss of functional disability in older adults (38). Public health efforts are needed to identify means of preventing arthritis and to prevent the impact on physical function. The association with back pain may reflect vertebral fractures, which, as noted earlier, have been associated with increases in disability (39). Taken together, these results suggest that treatment of these common conditions could possibly help to preserve physical function with advancing age.

Strengths of the current study include the large community-based population of older women who were followed over a 10-year period. We evaluated a large number of risk factors that could be related to lower extremity performance. Standard assessments of lower extremity performance were used. There are, however, several limitations including missing information from participants who were unable to attend the tenth-year follow-up visit. These censored participants were older and frailer at the study entry. Therefore, the observed percent decline in walking speed and increase in chair-stand time likely underestimates the true rate of functional decline in the general population.

Summary
Lower extremity performance, as measured by walking speed and time to complete five chair-stands, decreased dramatically with advancing age in older women. Treatment of common diseases, such as arthritis and diabetes, and a healthy lifestyle, including avoidance of smoking and weight control, could help older adults maintain their lower extremity physical functions.


   Acknowledgments
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 Methods
 Results
 Discussion
 References
 
Investigators in the Study of Osteoporotic Fractures Research Group

University of California, San Francisco (Coordinating Center): S. R. Cummings (Principal Investigator), M. C. Nevitt (Co-Investigator), D. M. Black (Study Statistician), H. K. Genant (Director, Central Radiology Laboratory), C. Arnaud, D. Bauer, W. Browner, L. Christianson, M. Dockrell, C. Fox, R. Gore, S. Harvey, M. Jaime-Chavez, L. Laidlaw, R. Lipschutz, L. Lui, G. Milani, L. Palermo, R. San Valentin, K. Stone, H. Tabor, D. Tanaka, and C. Yeung.

University of Maryland: J. C. Scott (Principal Investigator), R. Sherwin (Co-Investigator), M. C. Hochberg (Co-Investigator), J. Lewis (Project Director), E. Peddicord (Clinic Coordinator), A. Bauer, C. Boehm, G. Cullum, L. Finazzo, M. E. Flaks, T. Ford, D. Harris, B. Hohman, E. Oliner, T. Page, J. Schlossberg, C. Shaffer, A. Trimble, and S. Trusty.

University of Minnesota: K. Ensrud (Principal Investigator), P. Schreiner (Co-Investigator), C. Bell (Project Director), E. Mitson (Clinic Coordinator), C. Bird, D. Blanks, S. Estill, S. Fillhouer, S. Fincham, J. Griffith, J. Hansen, F. Imker-Witte, K. Jacobson, K. Kiel, K. Knauth, N. Nelson, E. Penland-Miller, and M. Riley-Alves.

University of Pittsburgh: J. A. Cauley (Principal Investigator), L. H. Kuller (Co-Principal Investigator), M. Vogt (Co-Investigator), L. Harper (Project Director), L. Buck (Clinic Coordinator), C. Bashada, D. Cusick, G. Engleka, A. Githens, M. Gorecki, K. McCune, D. Medve, M. Nasim, C. Newman, S. Rudovsky, and N. Watson.

The Kaiser Permanente Center for Health Research, Portland, Oregon: E. Harris (Principal Investigator and Project Director), W. M. Vollmer (Co-Investigator), E. Orwoll (Co-Investigator), H. Nelson (Co-Investigator), K. Crannell (Project Administrator and Clinic Coordinator), J. Bender, A. Doherty, K. Easter, M. Erwin, F. Heinith, J. Kann, K. Redden, C. Romero, K. Snider, and C. Souvanlasy.

Grant Support: In part by Public Health Service Grants 1-R01-AR35582, 1-R01-AR35583, 1-R01-AM35584, 1-R01-AG05395, 1-R01-AG05407, P30 AG024827 (NIA), and the Pittsburgh Claude D. Pepper Older Americans Independence Center.


   Footnotes
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Decision Editor: Luigi Ferrucci, MD, PhD

Received October 26, 2005

Accepted July 13, 2006


   References
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 Results
 Discussion
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S. Volpato, M. Cavalieri, G. Guerra, F. Sioulis, M. Ranzini, C. Maraldi, R. Fellin, and J. M. Guralnik
Performance-Based Functional Assessment in Older Hospitalized Patients: Feasibility and Clinical Correlates
J. Gerontol. A Biol. Sci. Med. Sci., December 1, 2008; 63(12): 1393 - 1398.
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M. L. Callisaya, L. Blizzard, M. D. Schmidt, J. L. McGinley, and V. K. Srikanth
Sex Modifies the Relationship Between Age and Gait: A Population-Based Study of Older Adults
J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2008; 63(2): 165 - 170.
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C. A Clay, S. Perera, J. M Wagner, M. E Miller, J. B Nelson, and S. L Greenspan
Physical Function in Men With Prostate Cancer on Androgen Deprivation Therapy
Physical Therapy, October 1, 2007; 87(10): 1325 - 1333.
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