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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 55:M434-M440 (2000)
© 2000 The Gerontological Society of America

Change in Muscle Mass and Muscle Strength After a Hip Fracture

Relationship to Mobility Recovery

Marjolein Vissera,b, Tamara B. Harrisa, Kathleen M. Foxc, William Hawkesd, J. Richard Hebeld, Janet YuYahirod, Roger Michaeld, Sheryl Itkin Zimmermand and Jay Magazinerd

a Epidemiology, Demography and Biometry Program, National Institute on Aging, Bethesda, Maryland
b Institute for Research in Extramural Medicine, Faculty of Medicine, Vrije University, Amsterdam, The Netherlands
c ManagedEDGE, Euro RSCG, New York, New York
d Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, Baltimore

Marjolein Visser, Institute for Research in Extramural Medicine, Faculty of Medicine, Vrije University, Van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands E-mail: m.visser.emgo{at}med.vu.nl.

William B. Ershler, MD


    Abstract
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Background. Hip fracture in elderly persons has a serious impact on long-term physical function. This study determines the change in muscle strength and muscle mass after a hip fracture, and the associations between these changes and mobility recovery.

Methods. Ninety community-dwelling women aged 65 years and older who had recently experienced a fracture of the proximal femur were included in the study. At 2 to 10 days after hospital admission, the women's grip strength, ankle dorsiflexion strength, and regional muscle mass (by dual-energy x-ray absorptiometry) were measured, and the prefracture level of independence for five mobility function items was assessed. All measurements were repeated at 12 months.

Results. At follow-up, only 17.8% of the women had returned to their prefracture level of mobility function for all five items. Mobility function recovery was not related to change in skeletal muscle mass of the nonfractured leg or the arms. However, women who lost grip strength (mean loss of -28.7%, SD = 16.9%), or who lost ankle strength of the nonfractured leg (mean loss of -21.5%, SD = 14.7%), had a worse mobility recovery compared with those who gained strength ( p = .04 and p = .09, respectively). In addition, chronic disease ( p = .03), days hospitalized ( p = .04), and self-reported hip pain ( p = .07) were independent predictors of decline in mobility function.

Conclusions. The results suggest that loss of muscle strength, but not loss of muscle mass, is an independent predictor of poorer mobility recovery 12 months after a hip fracture. When confirmed by other studies, these findings may have implications for rehabilitation strategies after a hip fracture.

HIP fracture has a serious impact on long-term physical function in elderly men and women. Numerous studies report that 1 year after the fracture, between 30% and 83% of the patients return to their prefracture functional level, depending on the function evaluated and the population studied (1)(2)(3)(4)(5)(6). Therefore, knowledge about potential determinants of functional recovery is important.

Greater postfracture muscle strength of the legs (2)(7) and arms (8) and more physical therapy sessions (9) are associated with better functional recovery after a hip fracture, which suggests an important role of muscle strength. No studies, however, have investigated the prospective change in muscle strength after a hip fracture and the potential association of this change with functional recovery.

Two prospective studies have investigated change in body composition after a hip fracture (10)(11) and observed a mean 5%–6% loss of total body lean mass and a 4%–11% gain in fat mass at 1 year postfracture. Most of the loss in lean mass appeared to occur in the first 2 to 4 months after the fracture. This loss of lean body mass suggests a considerable loss of muscle mass. However, the change in regional skeletal muscle mass after a hip fracture and its contribution to functional recovery have not been studied.

The present study examined whether mobility recovery after hip fracture was related to change in appendicular skeletal muscle mass or to change in muscle strength. The study was conducted with 90 women aged 65 years and older who had experienced a new fracture of the proximal femur. These subjects were followed up during 1 year and were part of a larger project on postfracture changes in bone, muscle, and function.


    Methods
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Subjects
Between 1992 and 1995, community-dwelling white women aged 65 years and older who had been admitted within 48 hours to two Baltimore area hospitals with a new fracture of the proximal femur were invited to participate in a prospective study of hip fracture recovery. Of the 407 identified cases, 205 patients participated in a baseline assessment of body composition; out of these, 90 patients with complete data were included in the present analyses. Of these 90, 48 women (53.3%) had fractured the femoral neck, and 42 women (46.7%) had fractured the intertrochanteric region. Forty-seven women (52.2%) had fractured the right hip. Of the patients with intertrochanteric fractures, 95.9% had an internal fixation, and of the patients with a femoral neck fracture, 93.9% had an arthroplasty. Overall, 95.6% of the patients received physical therapy between discharge and the 12-month follow-up. The mean number of received therapy sessions was 29.2 (SD = 21.4). Two patients were still receiving physical therapy at 12 months. During the first 2 months after discharge, 67.5% of the patients received physical therapy in a private residence, 36.3% in a rehabilitation center, and 27.5% in a nursing home. During this period, 75.6% of the patients performed exercises on their own; less than 5% of these used weights or resistance.

Compared with the 317 patients who were not included, the 90 participating women were younger (mean age 79.4 years vs 82.4 years, p = .0013) and had less comorbidity ( p = .06). There were no differences in type of fracture ( p = .3) or type of surgery ( p = .8). For 74 out of the 90 women included in the analyses, information on body composition and mobility function was also available for the 6-month follow-up.

Body Composition
Body composition was measured using dual-energy x-ray absorptiometry (DXA) (models QDR-1000W and QDR-1500, Hologic, Inc., Waltham, MA). Patients were always measured on the same DXA machine. Baseline body composition was obtained approximately 3 days after hospital admission. If DXA was not feasible at day 3, the information collected at approximately day 10 after admission was used as the baseline value. After completion of the scan, the body composition results for the whole body were given by the system's software (version V5.47P). The muscle mass of the leg was calculated: leg muscle = total leg mass - leg fat mass - (1.82*leg bone mineral content) (12). The muscle mass of the arms was calculated similarly. Complete information on the arms, that is, with no part of the arm outside the DXA scanning field, was obtained for 77 women.

To detect possible drift over time, quality control of the DXA machines was performed every day prior to scanning patients by using an anthropomorphic spine phantom. The coefficient of variation of these measurements over a 7-month period was 0.31%.

Only the results for leg muscle mass of the nonfractured leg were used in the analyses to eliminate bias that might occur with the swelling of soft tissue around the fracture site. At baseline, the mean difference in total leg mass between the fractured leg and the nonfractured leg was 1.3 kg (SD = 0.1 kg), suggesting that the leg and hip regions were swollen as a result of the fracture and the surgery. The excess of fluid and blood likely to cause the swelling is measured as lean soft tissue mass by DXA and would cause an overestimation of muscle mass in the affected leg at baseline, which would lead to an overestimation of muscle loss at follow-up when the swelling decreased.

Muscle Strength
Grip strength and ankle dorsiflexion strength were used as indicators of muscle strength and were measured at baseline and at 12-month follow-up. Grip strength was measured using a hand-held dynamometer (Jamar, Clifton, NJ). The correlation coefficients of grip strength with knee extension strength and quadriceps strength in elderly women are reported to be higher than 0.5 (13)(14). The maximum strength results (in kilograms) of the two grip strength trials (right arm with patients seated) were used. Ankle dorsiflexion strength was measured three times using a Spark hand-held dynamometer (Model 160, Spark Instruments and Academics, Inc., Iowa City, IA). The maximum strength result (in kilograms) of the two trials of the nonfractured leg was used. Data on grip strength and ankle dorsiflexion were available for 71 and 69 women, respectively.

Mobility Function
Within 1 week after hospital admission, the women's prefracture mobility function was assessed using a structured interview with the patient or the patient's proxy. The correspondence between hip fracture patient and proxy has been demonstrated to be good for information on functional status, especially for lower extremity activities (15)(16). At the 12-month follow-up, current mobility function was assessed. Five physical activities of daily living were included in the analyses: getting in and out of bed, rising from an armless chair, walking 10 feet or across a room, walking one block on a level sidewalk, and climbing five stairs. These items have been used in elderly hip fracture patients and have been shown to be sensitive to change (3)(4)(17).

For each item, ability was rated on a 3-point scale: 0 = complete independence; 1 = needing some assistance (human or equipment); and 2 = complete inability to perform the activity. The five individual items were summed to create an overall mobility function score ranging from 0 (independent on all five mobility items) to 10 (unable to perform all of the five mobility items). Change in mobility function was calculated as the mobility score at 12 months after the fracture minus the mobility score before the fracture.

An overall recovery score also was created. When the follow-up score on the 3-point scale was the same or less than the prefracture score for each individual mobility item, recovery was coded 1 for that item. When the follow-up score was greater, recovery was coded 0 for that item. Overall recovery was calculated as the sum of recovery on the five separate items, with the overall recovery score ranging from 0 (no recovery on all five items) to 5 (recovered on all five mobility items).

Potential Confounders
Based on previous studies, several factors that are predictive of functional recovery after a hip fracture and/or are associated with body composition or muscle strength were identified and included in the analyses (2)(3)(4)(5)(6)(8)(18).

Cognition.-- Cognition was measured with the Mini-Mental State Examination at baseline, a 30-point test of cognitive status in which lower scores indicate greater degrees of impairment (19).

Prefracture health status.-- A measure of comorbidity was created using history of chronic conditions reported in the medical chart as present at the time of fracture, including joint disease (arthritis, rheumatism, or degenerative joint disease), heart disease (angina, arrhythmias, chronic heart failure, or other heart problems), diabetes mellitus, cancer (cancer, leukemia, or malignancy), and stroke. Values ranged from 0 to 5.

Body fatness.-- This measurement was obtained from DXA at baseline and was calculated as total body fat mass divided by total body mass.

Number of days in hospital.-- The number of days in the hospital at the time of the index fracture was obtained from discharge summaries.

Hip pain.-- Self-reported pain in the affected hip 2 months after the fracture was coded as yes/no.

Statistical Methods
Data were analyzed using SAS software (SAS Institute, Inc., Cary, NC). Results are presented as mean ± SD or mean ± SE. A p value of less than .05 was considered statistically significant. Student's t test for paired samples was used to compare mean values of muscle mass, muscle strength, and mobility function score at baseline and after 12 months. Participants were categorized by tertile of nonfractured leg muscle mass change from baseline to month 12 (cutoff points <-3.3%, -3.3% to +5.5%, >+5.5%); by tertile of arm muscle mass change (cutoff points <-11.6%, -11.6% to 0, >0); by tertile of change in grip strength (cutoff points <-9.2%, -9.2% to +8.3%, >8.3%); and by tertile of change in ankle dorsiflexion strength of the nonfractured leg (cutoff points <0, 0 to +23.0%, >+23.0%). Analysis of variance was used to test the association of tertile of muscle mass change or tertile of muscle strength change, with selected continuous variables. The Mantel-Haenzel chi-square statistic was used to test the association of categorical variables with these tertiles. Analysis of covariance was used to assess the association between tertiles of muscle mass change, or tertiles of muscle strength change, and the mobility function outcomes, adjusting for potential confounders. Analyses were also performed using the change in muscle mass or muscle strength as a continuous variable. The analyses were repeated, including only those women who were mobility independent or who had used a device before the fracture (n = 57), thereby excluding patients who were unable to perform the activity at baseline. Among the 74 women who had additional measurements of body composition and mobility function at the 6-month follow-up, the association between short-term change in muscle mass and muscle strength with short-term change in mobility function was investigated.


    Results
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
The changes in skeletal muscle mass and muscle strength from baseline to 12 months after a hip fracture are shown in Table 1 . The overall change in skeletal muscle mass was +1.1% (SD = 11.8%) for the nonaffected leg and -4.7% (SD = 13.7%) for the arms. The overall change in grip strength was -1.5% (SD = 32.7%), and the change in ankle dorsiflexion strength was +13.2 (SD = 33.4%). The change in arm muscle mass and ankle dorsiflexion strength were statistically significant ( p < .01). Although the overall change in leg muscle mass and grip strength from baseline to 12-month follow-up was not significant, the variability in the change was high, which indicates the presence of different patient subgroups. Hence, the total study cohort was divided into tertiles based on muscle mass change and muscle strength change.


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Table 1. Skeletal Muscle Mass Assessed by Dual-Energy X-ray Absorptiometry and Muscle Strength in Elderly Women at Baseline and 12 Months After a Hip Fracture

 
Mean weight change at the 12-month follow-up was -2.9% (SD = 8.0%, p < .01). Weight change was positively associated with change in muscle mass ( p = .0001); it explained 23% of the variance in leg muscle mass change and 18% of the variance in arm muscle mass change. Change in body weight was not associated with change in muscle strength ( p > .24).

Patient characteristics according to tertile of muscle mass change are shown in Table 2 . Women with the greatest decline in muscle mass (tertile I) had a lower cognitive status score, the highest muscle mass at baseline, and lost the most weight compared with the other tertiles. The association between selected variables and tertile of muscle strength change is shown in Table 3 . Women who lost strength (tertile I) were stronger at baseline compared with women in tertile III.


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Table 2. Characteristics of Elderly Women Before and 12 Months After Hip Fracture by Tertile of Muscle Mass Change from Baseline to 12 Months (mean ± SD)

 

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Table 3. Characteristics of Elderly Women Before and 12 Months After Hip Fracture by Tertile of Muscle Strength Change from Baseline to 12 Months (mean ± SD)

 
In comparing mobility function before the fracture and 12 months after the fracture, an overall decline in mobility function was observed (Fig. 1). For each mobility item, the percentage of women who were able to perform the item independently decreased after the fracture, and the percentage of women who were unable to perform the item increased after the fracture. Thirteen (14.4%) women were fully independent on all five mobility items before the fracture, whereas only two (2.2%) women were fully independent 12 months after the fracture. The overall mobility score increased from 2.31 ± 1.86 prefracture to 4.08 ± 2.35 12 months after the fracture ( p = .0001).



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Figure 1. Percentage of women who reported themselves as independent (black rectangles), needing any assistance (gray rectangles), or unable (white rectangles) to perform a mobility item before a hip fracture (Pre) and 12 months after the fracture (Post).

 
The overall mobility score was calculated for each tertile of muscle mass change and muscle strength change (Table 4 ). The decline in mobility function after a hip fracture was not different between tertiles of leg muscle mass change or arm muscle mass change. Adjustment for potential confounders or restricting the analyses to those women who also had valid measurements of grip strength (n = 71) or ankle dorsiflexion strength (n = 69) did not substantially change these results. In contrast to the results for muscle mass change, the decline in mobility function was associated with the change in muscle strength. Women who lost the most grip strength (tertile I) had the greatest decline in mobility function. After adjustment for potential confounders, women in tertile I had a greater decline in mobility function (2.45, SE = 0.35) compared with women in tertile III (1.13, SE = 0.36, p = .012) and tended to have a greater decline compared with women in tertile II (1.45, SE = 0.35, p = .052). A similar pattern was observed for ankle dorsiflexion strength, but the association was not statistically significant. In this analysis, the change in mobility function score was also associated with chronic disease (women with more chronic illnesses at baseline were less likely to decline in mobility function; p = .03), the number of days in the hospital (women who stayed in the hospital longer were more likely to decline in mobility function; p = .04), and hip pain (those with hip pain tended to have a greater decline in mobility function; p = .07). No interaction between change in muscle strength and any of the potential confounders was observed. Among the subgroup of women (n = 74) who were also measured at a 6-month follow-up, there was no significant association between the short-term change (from baseline to 6-month follow-up) in muscle mass or muscle strength and the short-term change in mobility function ( p > .2).


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Table 4. Change in Overall Mobility Function Score 12 Months After Hip Fracture in Elderly Women by Tertile of Muscle Mass Change and by Tertile of Muscle Strength Change from Baseline to 12 Months

 
Overall mobility recovery was calculated as the sum of the individual recovery scores of the five mobility items. After 12 months, only 16 women (17.8%) recovered on all five mobility items. The association between overall mobility recovery and tertiles of muscle mass and muscle strength change is shown in Table 5 . There were no differences in mobility recovery by level of muscle mass change after hip fracture, even after adjustment for baseline characteristics and hip pain. In contrast, women who lost muscle strength during the 12 months after the fracture (tertile I) tended to have a poorer mobility recovery than those who gained muscle strength (tertile III). After adjustment for potential confounders, the difference for grip strength became statistically significant ( p = .04) and tended to be significant ( p = .09) for ankle dorsiflexion strength. In this analysis, the recovery score was also associated with chronic disease (those with more chronic illnesses were less likely to recover; p = .04) and with self-reported hip pain (women with hip pain had a poorer mobility recovery; p = .03).


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Table 5. Overall Mobility Recovery Score 12 Months After Hip Fracture in Elderly Women by Tertile of Muscle Mass Change and by Tertile of Muscle Strength Change from Baseline to 12 Months (mean ± SE)

 
Restricting the analyses to those women who were mobility independent or used an assistive device (walker or cane) before the fracture showed similar results. The same pattern of association was observed using changes in muscle mass and muscle strength as continuous variables in the analyses.


    Discussion
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
The present study is, to our knowledge, the first to investigate the change in muscle mass and muscle strength after hip fracture and to relate these changes to mobility recovery at 12 months after the fracture. The results show that elderly women who lose muscle mass have a similar recovery of mobility function after the fracture compared with women who did not change or who gained muscle mass. In contrast, loss of strength, measured by loss of grip strength (13)(14) or ankle dorsiflexion strength, was associated with a greater decline in mobility function and poorer recovery of function after the fracture, even when adjustments were made for potential confounders, including hip pain and morbidity, at the time of the fracture.

Loss of muscle mass has been hypothesized to be associated with impaired physical function because both loss of muscle and poorer physical function are age related (20)(21). However, currently no empirical evidence supports a direct causal relationship between muscle mass and disability, even though low muscle mass has been associated with lower bone mineral density (22)(23) and may be a predictor of falls. In fact, clinical trial data from growth hormone trials show increases in muscle mass but no improvement in functional ability (24). In contrast, increases in muscle strength after resistance training were associated with improved function (25)(26), and grip strength in mid-life predicts disability 25 years later (27). The results of these earlier studies and this study suggest that change in strength may have a greater effect on physical function than change in muscle mass.

The importance of strength may have clinical implications for rehabilitation after hip fracture. Our study suggests that specific strength training might increase the chance for full mobility recovery, in addition to usual modes of physical therapy. Future intervention studies should include strength measurements of different muscle groups to confirm our findings and to contribute to the development of optimal rehabilitation programs after a hip fracture.

Several factors should be considered that may explain the lack of association between change in muscle mass and mobility recovery. The observed net change in skeletal muscle mass was rather small. A threshold value for muscular strength has been reported below in which strength is critical to physical performance of the lower extremities (28). A similar threshold may exist for muscle mass, and the community-dwelling women included in our study might still be above that threshold after the fracture. Second, our measure of mobility function might not have been sensitive enough to detect a small change in mobility function. Although a relationship between change in muscle strength and change in mobility function was observed, the effect of a relatively small loss of muscle mass on functional decline might not have been detected.

The overall change we observed in appendicular skeletal muscle mass after a hip fracture was modest. However, an underestimation of muscle mass loss may have been caused by several factors. First, the change in leg muscle mass could only be studied in the nonfractured leg because of the swelling of the fractured leg. Loss of muscle mass in the nonfractured leg is less likely to occur because of its compensating for the fractured leg. Indeed, a greater loss of muscle mass was observed in the arms compared with the nonfractured leg. Second, the women who completed the study and were included in our statistical analyses were relatively younger and healthier. Elderly women have a poorer functional recovery after a hip fracture (1)(2)(4)(5)(6) and are expected to have a greater loss of muscle mass and muscle strength. Third, an earlier analysis by our group showed that loss of lean body mass mainly occurred in the first 2 months after the fracture and that some of this loss was regained in the next 10 months (11). Because skeletal muscle mass comprises the largest part of lean body mass, approximately 55% (29), the change in skeletal muscle mass is likely to follow the same pattern. Thus, instead of using peak muscle mass loss, we investigated the net change over 12 months. Finally, the validity of the DXA method for assessing change in soft tissue should be considered (30). The precision of the measurements of regional skeletal muscle mass by DXA is good, with reported coefficients of variation of 1%–2% for leg muscle mass and 2%–3% for arm muscle mass (31)(32). Moreover, several validation studies that used changes in total body water during dialysis to simulate changes in total body lean mass of only 2%–4% have shown good results (33)(34). These studies support the use of DXA for measuring small change in regional muscle mass over time.

In conclusion, the results of the study suggest that loss of muscle strength after a hip fracture might lead to poorer mobility recovery 12 months after the fracture. No association was observed between loss of muscle mass and mobility recovery. Because these findings may have implications for the rehabilitation of elderly hip fracture patients, future studies are needed to determine the independent role of loss of muscle strength and loss of muscle mass on functional recovery in elderly men and women.


    Acknowledgments
 
This research was supported by the National Institute on Aging (Grant R37 AG09901). The authors acknowledge the cooperation of medical and administrative personnel and the departments of orthopedic surgery at Union Memorial Hospital and Saint Joseph's Hospital; the commitment to measuring body composition by Bernadette Jenkins, Michele Gladfelter, and Sue Bright; assistance with patient recruitment from Penelope Smith; and the administrative oversight and expert consultation of Drs. Darrell McIndoe and Arthur Serpick.

Received September 24, 1998

Accepted November 1, 1999


    References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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D. R. Thomas
The Critical Link Between Health-Related Quality of Life and Age-Related Changes in Physical Activity and Nutrition
J. Gerontol. A Biol. Sci. Med. Sci., October 1, 2001; 56(10): M599 - 602.
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Am. J. Physiol. Endocrinol. Metab.Home page
S. Salinari, A. Bertuzzi, G. Mingrone, E. Capristo, A. Pietrobelli, P. Campioni, A. V. Greco, and S. B. Heymsfield
New bioimpedance model accurately predicts lower limb muscle volume: validation by magnetic resonance imaging
Am J Physiol Endocrinol Metab, April 1, 2002; 282(4): E960 - E966.
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