Journal of Gerontology: MEDICAL SCIENCES 1990. Vol. 45. No. 3. M82-88
In the Public Domain
The Role of Muscle Loss in the Age-Related Decline of Grip Strength: Cross-sectional and Longitudinal Perspectives Douglas A. Kallman, Chris C. Plato, and Jordan D. Tobin Gerontology Research Center, National Institute on Aging.
cross-sectional studies have shown a loss of grip MANY strength with increasing age (1-13). These studies, because of their cross-sectional design, are limited to describing changes at the population level, and cannot determine how a specific individual's grip strength changes with age. They are also not suitable for examining whether the decline of grip strength with age is due to confounding secular or cohort effects. The cause of the age-related decline of strength also remains unresolved. It has been attributed to several factors including declining muscle mass (13-18), increasing muscular fibrous tissue (3), alterations in muscle fiber type (16,1824), and motoneuron abnormalities (16,24-26), in older people. Other age changes, such as chronic diseases, osteoarthritis (OA), or decreasing physical activity may also be contributing factors. The purposes of this longitudinal study are: (a) to determine whether the results of the longitudinal and crosssectional analyses of grip strength agree, (b) to examine the distribution of individual rates of change of grip strength with age, and (c) to ascertain whether declines in grip strength can be explained by the decreasing muscle mass that often occurs with aging.
METHODS
Subjects. —Grip strength measurements, anthropometric assessments, and creatinine excretion determinations were made at one- to two-year intervals on apparently healthy, community-dwelling male participants in the Baltimore Longitudinal Study of Aging (BLSA) who have previously been described (27). For this analysis, data collected from 1961 through 1974 M82
from 864 subjects (2650 total visits) were selected because the method of measuring grip strength remained the same. Seventeen BLSA subjects with disorders which might specifically influence grip strength were excluded: peripheral nerve injury (n = 4), stroke and other central nervous system disease (n = 3), polio (n = 2), rheumatoid arthritis (n = 2), tendon injury (n = 2), Dupuytren's contracture (n = 2), carpal tunnel syndrome (n = 1), and recent wrist fracture (// = 1). Data from visits on which the grip measurements were more than 25c/c different from both the visit before and after it were excluded as erroneous. These outlying points were more than 4 standard deviations from an individual's mean value. Erroneous data points (36 visits from 30 subjects excluded, 3 subjects had multiple visits excluded) represented 1.4% of the entire data base. After exclusions, the last visit of 847 subjects, age 20 to 100 years, who had bilateral grip strength measurements was selected for cross-sectional analysis. From the crosssectional population, a subsample of subjects followed 5 or more years and with at least three bilateral grip strength measurements was selected for longitudinal analysis. The longitudinal subsample consisted of 342 subjects followed 5 to 13 years with an average of 9 years. Grip strength, creatinine excretion, and forearm circumference measurements were not always performed on each subject at every visit. Thus, there were differing numbers of subjects available for study of the relationship between grip strength and muscle mass: (a) 382 subjects with all three measurements; (b) 608 subjects with grip strength and forearm circumference measurements; (c) 784 subjects with grip strength and creatinine excretion determinations, and (d) 293 subjects available for longitudinal analysis with at least three grip strength and three creatinine excretion measurements each performed over at least a 5-year period.
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
The decline of strength with age has often been attributed to declining muscle mass in older subjects. To investigate factors which might influence changes in strength across the life span, grip strength and muscle mass (as estimated by creatinine excretion and forearm circumference) were measured in 847 healthy volunteers, aged 20—100 years, from the Baltimore Longitudinal Study of Aging. Cross-sectional and longitudinal results concur that grip strength increases into the thirties and declines at an accelerating rate after age 40. However, the grip strength of 48% of subjects less than 40 years old, 29% of individuals 40-59 years old, and 15% of subjects older than 60 did not decline during the average 9-year follow-up. Grip strength is strongly correlated with muscle mass (r = .60, p < .0001). However, using multiple regression analysis, grip strength is more strongly correlated with age (partial r2 = .38) than muscle mass (partial r2 = .16). Additionally, a residuals analysis demonstrates that younger subjects are stronger and older subjects are weaker than one would predict based on their muscular size. Thus, while strength losses are partially explained by declining muscle mass, there remain other yet undetermined factors beyond declining muscle mass to explain some of the loss of strength seen with aging.
M83
MUSCLE LOSS, GRIP STRENGTH, AND AGING
Table 1. Cross-sectional and Longitudinal Analysis of Grip Strength* Longitudinal Results
Cross-sectional Results Age Group
/vt
Mean Age (yr)
20-29 30-39 40-49 50-59 60-69 70-79 80-89
55 115 130 187 158 155 42
27.2 34.7 45.8 55.0 64.4 74.6 83.2
Mean Grip Strength (kg)
/vt
Mean+ Age
Mean Grip§ Strength (kg)
Mean Follow-up (yr)
Mean Slope (kg/yr)
100.2 104.3 101.0 95.2 88.0 75.4 66.0
5 24 90 105 71 40 5
— 36.8 45.6 54.8 64.6 74.5 —
103.9 100.7 97.1 88.2 77.9
— ± ± ± ± ± —
— 8.5 8.7 9.3 9.2 8.8 —
— 0.33 ± 0.23 -0.31 ±0.12 - 0 . 6 5 ±0.11 - 0 . 7 8 ±0.15 - 1 . 2 7 ±0.21 —
± ± ± ± ± ± ±
.97 .56 .28 .03 .00 .04 .56
2.70 1.36 1.17 1.58 1.43
Grip strength measurement. — Grip strength was measured with an adjustable Smedley hand dynamometer (C.H. Stoelting Co., Wood Dale, IL) that was calibrated using known weights. After adjusting the dynamometer for hand comfort, subjects were instructed to use the stationary arm position they found most comfortable. The highest grip strength of three maximal efforts, done after rest intervals selected by the subject, was recorded for each hand at each visit. There was a 6% coefficient of variation for repeated grip tests. Left- and righthand grip measurements were summed for this analysis to remove consideration of hand dominance. Creatinine excretion and forearm circumference determination. — Creatinine is thought to be produced exclusively by skeletal muscle and is excreted by the kidneys in direct proportion to muscle mass (28). Accordingly, 24-hour urinary creatinine excretion provides an excellent index of total body muscle mass (28-30). In this study, creatinine excretion was determined from aliquots of supervised 24-hour urine collections. True creatinine concentrations were measured using standard laboratory methods (31). The forearm circumference of each arm was measured in centimeters at its widest point with the arm relaxed and the hand open. Statistical analysis. — Statistical analysis was performed using SAS software. The critical level for statistical significance was/? < .05. For longitudinal analysis, linear regressions were used to calculate the slope for each subject's grip strength change over time. Multiple regression analysis was used to examine whether the initial level of grip strength or muscle mass influenced the rate of decline of grip strength. Because the starting level of each of these variables was agerelated, age was included in the regression analyses in order to determine if there was a relationship between initial levels and rate of change of grip strength beyond an age effect. RESULTS
Grip strength and aging cross-sectional analysis. — The sum of bilateral grip strength (summed grip) had the highest
170 D) 160 * 150
J. 140 § 130 w 120 fc 110 Q. 100 QC 90 O 80 Q LJJ
summed grip= go.e+.SAtageJ-.OUfage2) r -.64
% • •«
•
70
i 60 \ i 50 1 40 I I i 30 10 20 30 40 50 60 70 80 90 100110 AGE Figure I. Regression of individual grip strengths on age (N = 847).
value in 30-39-year-olds, although it is not significantly different from the adjacent age groups. Decade means (mean value for each 10-year age group) of grip strength decline in 40-49-year-olds and become progressively lower at an accelerating rate, showing 80-89-year-olds with 37% less grip strength than 30-39-year-olds (Table 1). The accelerating decline of strength across the age-span is best described by the curvilinear regression equation: Summed Grip = 90.6 + .84 (Age)-.014 (Age2) ( r = .64, p < .0001) (Figure 1).
(1)
Grip strength and aging longitudinal analysis. — The decade mean of the slope of summed grip strength versus age is positive in 30-39-year-olds, and then becomes progressively more negative with increasing age (Table 1, Figure 2). The acceleration of the decline in grip strength with age is also reflected in the distributions of individual slopes for each age group (Figure 3). The older the subject, the more
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
*Summed grip strength (left- + righthand grip). iData are not reported when n = 5 or less. Cross-sectional data are not shown for one 19-year-old subject. 3 subjects in their 90s. and one 100-year-old subject. Data for all 847 cross-sectional subjects are shown in Figure 1. £ Decade means of each subject's average age during the period he was followed. SDecade means of each subject's average grip strength during the period he was followed. Mean values ± standard error of the mean.
KALLMAN ET AL.
M84
120
MIDDLE AGED 29%NoD«c*n»
O)
10
20 30 40 PERCENT
50
10
20 30 40 PERCENT
50
10
20 30 40 PERCENT
50
3000 creatinine excretion--1223+52.3(summed forearm) r-.56
20
30
40
50 60 AGE
70
80
90
Figure 2. Comparison of cross-sectional age differences and longitudinal age changes in grip strength. The dots represent the mean values for each decade obtained from cross-sectional data. Line segments represent the longitudinal results, and indicate the decade means of the rate of change of grip strength for each individual as determined by regression analysis. Lines are drawn with the midpoints at the mean grip strength for each age decade, and with their lengths, along the abscissa, representing the mean time span over which the longitudinal data were collected for each age group (see Table 1).
2500 2000
LU DC O X Ul LU
z z
< LU
1500 1000 500
DC O
0 35
40
45
50
55
60
65
70
SUMMED FOREARM CIRCUMFERENCE (cm) Figure 4. Regression of individual creatinine excretion on summed forearm circumference (A' = 382).
170 D) 160 : 150 z 140 o 130 LU 120 110 S 100 Q. 90 CC O 80 Q 70 LU | 60
summed grip- 72.3+3.04(summed forearm) r-.6O
i i i
likely he is to lose grip strength. However, not all subjects lose grip strength as they age; 48% of subjects less than 40 years old, 29% of individuals 40-59 years old, and 15% of subjects older than 60 had no decline in grip strength during the study period. The lack of decline in strength in these subjects is not biased by differing lengths of follow-up; the slope of grip strength is not dependent on the length of time a subject is followed. In each age group, the difference between high and low slope values is similar, suggesting that there is no age effect on the variability of grip strength slopes (Figure 3). The slope and starting level of grip strength are associated (partial r1 = .12, p < .0001) beyond the effect of age, indicating that the stronger a subject is at the start of the study, the more likely he is to have a fast rate of loss of grip strength.
CVI O>
i i i i i
Grip strength and muscle mass. — Cross-sectional analysis demonstrates that both indices of muscle mass, creatinine excretion and summed forearm circumference decline with age and are highly associated, as best described by the regression equation:
:'": j ; ! ' : . :
i
Creatinine Excretion = -1222 + 52.3 (Summed Forearm Circumference) (r = .58, p < .0001) (Figure 4). (2) In the 382 subjects with grip, creatinine excretion, and forearm circumference data, summed grip strength is strongly related to both creatinine excretion (r = .58, p < .0001) and summed forearm circumference (r = .60, p < .0001) (Figure 5). Stepwise multiple regression analysis
•
i 50 m
40 30 40
i
1
I
i
i
1
45
50
55
60
65
70
75
SUMMED FOREARM CIRCUMFERENCE (cm) Figure 5. Regression of individual grip strength on forearm circumference (N = 382).
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
Figure 3. Comparison of the distribution of grip strength slopes by age group (young
In the Public Domain
The Role of Muscle Loss in the Age-Related Decline of Grip Strength: Cross-sectional and Longitudinal Perspectives Douglas A. Kallman, Chris C. Plato, and Jordan D. Tobin Gerontology Research Center, National Institute on Aging.
cross-sectional studies have shown a loss of grip MANY strength with increasing age (1-13). These studies, because of their cross-sectional design, are limited to describing changes at the population level, and cannot determine how a specific individual's grip strength changes with age. They are also not suitable for examining whether the decline of grip strength with age is due to confounding secular or cohort effects. The cause of the age-related decline of strength also remains unresolved. It has been attributed to several factors including declining muscle mass (13-18), increasing muscular fibrous tissue (3), alterations in muscle fiber type (16,1824), and motoneuron abnormalities (16,24-26), in older people. Other age changes, such as chronic diseases, osteoarthritis (OA), or decreasing physical activity may also be contributing factors. The purposes of this longitudinal study are: (a) to determine whether the results of the longitudinal and crosssectional analyses of grip strength agree, (b) to examine the distribution of individual rates of change of grip strength with age, and (c) to ascertain whether declines in grip strength can be explained by the decreasing muscle mass that often occurs with aging.
METHODS
Subjects. —Grip strength measurements, anthropometric assessments, and creatinine excretion determinations were made at one- to two-year intervals on apparently healthy, community-dwelling male participants in the Baltimore Longitudinal Study of Aging (BLSA) who have previously been described (27). For this analysis, data collected from 1961 through 1974 M82
from 864 subjects (2650 total visits) were selected because the method of measuring grip strength remained the same. Seventeen BLSA subjects with disorders which might specifically influence grip strength were excluded: peripheral nerve injury (n = 4), stroke and other central nervous system disease (n = 3), polio (n = 2), rheumatoid arthritis (n = 2), tendon injury (n = 2), Dupuytren's contracture (n = 2), carpal tunnel syndrome (n = 1), and recent wrist fracture (// = 1). Data from visits on which the grip measurements were more than 25c/c different from both the visit before and after it were excluded as erroneous. These outlying points were more than 4 standard deviations from an individual's mean value. Erroneous data points (36 visits from 30 subjects excluded, 3 subjects had multiple visits excluded) represented 1.4% of the entire data base. After exclusions, the last visit of 847 subjects, age 20 to 100 years, who had bilateral grip strength measurements was selected for cross-sectional analysis. From the crosssectional population, a subsample of subjects followed 5 or more years and with at least three bilateral grip strength measurements was selected for longitudinal analysis. The longitudinal subsample consisted of 342 subjects followed 5 to 13 years with an average of 9 years. Grip strength, creatinine excretion, and forearm circumference measurements were not always performed on each subject at every visit. Thus, there were differing numbers of subjects available for study of the relationship between grip strength and muscle mass: (a) 382 subjects with all three measurements; (b) 608 subjects with grip strength and forearm circumference measurements; (c) 784 subjects with grip strength and creatinine excretion determinations, and (d) 293 subjects available for longitudinal analysis with at least three grip strength and three creatinine excretion measurements each performed over at least a 5-year period.
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
The decline of strength with age has often been attributed to declining muscle mass in older subjects. To investigate factors which might influence changes in strength across the life span, grip strength and muscle mass (as estimated by creatinine excretion and forearm circumference) were measured in 847 healthy volunteers, aged 20—100 years, from the Baltimore Longitudinal Study of Aging. Cross-sectional and longitudinal results concur that grip strength increases into the thirties and declines at an accelerating rate after age 40. However, the grip strength of 48% of subjects less than 40 years old, 29% of individuals 40-59 years old, and 15% of subjects older than 60 did not decline during the average 9-year follow-up. Grip strength is strongly correlated with muscle mass (r = .60, p < .0001). However, using multiple regression analysis, grip strength is more strongly correlated with age (partial r2 = .38) than muscle mass (partial r2 = .16). Additionally, a residuals analysis demonstrates that younger subjects are stronger and older subjects are weaker than one would predict based on their muscular size. Thus, while strength losses are partially explained by declining muscle mass, there remain other yet undetermined factors beyond declining muscle mass to explain some of the loss of strength seen with aging.
M83
MUSCLE LOSS, GRIP STRENGTH, AND AGING
Table 1. Cross-sectional and Longitudinal Analysis of Grip Strength* Longitudinal Results
Cross-sectional Results Age Group
/vt
Mean Age (yr)
20-29 30-39 40-49 50-59 60-69 70-79 80-89
55 115 130 187 158 155 42
27.2 34.7 45.8 55.0 64.4 74.6 83.2
Mean Grip Strength (kg)
/vt
Mean+ Age
Mean Grip§ Strength (kg)
Mean Follow-up (yr)
Mean Slope (kg/yr)
100.2 104.3 101.0 95.2 88.0 75.4 66.0
5 24 90 105 71 40 5
— 36.8 45.6 54.8 64.6 74.5 —
103.9 100.7 97.1 88.2 77.9
— ± ± ± ± ± —
— 8.5 8.7 9.3 9.2 8.8 —
— 0.33 ± 0.23 -0.31 ±0.12 - 0 . 6 5 ±0.11 - 0 . 7 8 ±0.15 - 1 . 2 7 ±0.21 —
± ± ± ± ± ± ±
.97 .56 .28 .03 .00 .04 .56
2.70 1.36 1.17 1.58 1.43
Grip strength measurement. — Grip strength was measured with an adjustable Smedley hand dynamometer (C.H. Stoelting Co., Wood Dale, IL) that was calibrated using known weights. After adjusting the dynamometer for hand comfort, subjects were instructed to use the stationary arm position they found most comfortable. The highest grip strength of three maximal efforts, done after rest intervals selected by the subject, was recorded for each hand at each visit. There was a 6% coefficient of variation for repeated grip tests. Left- and righthand grip measurements were summed for this analysis to remove consideration of hand dominance. Creatinine excretion and forearm circumference determination. — Creatinine is thought to be produced exclusively by skeletal muscle and is excreted by the kidneys in direct proportion to muscle mass (28). Accordingly, 24-hour urinary creatinine excretion provides an excellent index of total body muscle mass (28-30). In this study, creatinine excretion was determined from aliquots of supervised 24-hour urine collections. True creatinine concentrations were measured using standard laboratory methods (31). The forearm circumference of each arm was measured in centimeters at its widest point with the arm relaxed and the hand open. Statistical analysis. — Statistical analysis was performed using SAS software. The critical level for statistical significance was/? < .05. For longitudinal analysis, linear regressions were used to calculate the slope for each subject's grip strength change over time. Multiple regression analysis was used to examine whether the initial level of grip strength or muscle mass influenced the rate of decline of grip strength. Because the starting level of each of these variables was agerelated, age was included in the regression analyses in order to determine if there was a relationship between initial levels and rate of change of grip strength beyond an age effect. RESULTS
Grip strength and aging cross-sectional analysis. — The sum of bilateral grip strength (summed grip) had the highest
170 D) 160 * 150
J. 140 § 130 w 120 fc 110 Q. 100 QC 90 O 80 Q LJJ
summed grip= go.e+.SAtageJ-.OUfage2) r -.64
% • •«
•
70
i 60 \ i 50 1 40 I I i 30 10 20 30 40 50 60 70 80 90 100110 AGE Figure I. Regression of individual grip strengths on age (N = 847).
value in 30-39-year-olds, although it is not significantly different from the adjacent age groups. Decade means (mean value for each 10-year age group) of grip strength decline in 40-49-year-olds and become progressively lower at an accelerating rate, showing 80-89-year-olds with 37% less grip strength than 30-39-year-olds (Table 1). The accelerating decline of strength across the age-span is best described by the curvilinear regression equation: Summed Grip = 90.6 + .84 (Age)-.014 (Age2) ( r = .64, p < .0001) (Figure 1).
(1)
Grip strength and aging longitudinal analysis. — The decade mean of the slope of summed grip strength versus age is positive in 30-39-year-olds, and then becomes progressively more negative with increasing age (Table 1, Figure 2). The acceleration of the decline in grip strength with age is also reflected in the distributions of individual slopes for each age group (Figure 3). The older the subject, the more
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
*Summed grip strength (left- + righthand grip). iData are not reported when n = 5 or less. Cross-sectional data are not shown for one 19-year-old subject. 3 subjects in their 90s. and one 100-year-old subject. Data for all 847 cross-sectional subjects are shown in Figure 1. £ Decade means of each subject's average age during the period he was followed. SDecade means of each subject's average grip strength during the period he was followed. Mean values ± standard error of the mean.
KALLMAN ET AL.
M84
120
MIDDLE AGED 29%NoD«c*n»
O)
10
20 30 40 PERCENT
50
10
20 30 40 PERCENT
50
10
20 30 40 PERCENT
50
3000 creatinine excretion--1223+52.3(summed forearm) r-.56
20
30
40
50 60 AGE
70
80
90
Figure 2. Comparison of cross-sectional age differences and longitudinal age changes in grip strength. The dots represent the mean values for each decade obtained from cross-sectional data. Line segments represent the longitudinal results, and indicate the decade means of the rate of change of grip strength for each individual as determined by regression analysis. Lines are drawn with the midpoints at the mean grip strength for each age decade, and with their lengths, along the abscissa, representing the mean time span over which the longitudinal data were collected for each age group (see Table 1).
2500 2000
LU DC O X Ul LU
z z
< LU
1500 1000 500
DC O
0 35
40
45
50
55
60
65
70
SUMMED FOREARM CIRCUMFERENCE (cm) Figure 4. Regression of individual creatinine excretion on summed forearm circumference (A' = 382).
170 D) 160 : 150 z 140 o 130 LU 120 110 S 100 Q. 90 CC O 80 Q 70 LU | 60
summed grip- 72.3+3.04(summed forearm) r-.6O
i i i
likely he is to lose grip strength. However, not all subjects lose grip strength as they age; 48% of subjects less than 40 years old, 29% of individuals 40-59 years old, and 15% of subjects older than 60 had no decline in grip strength during the study period. The lack of decline in strength in these subjects is not biased by differing lengths of follow-up; the slope of grip strength is not dependent on the length of time a subject is followed. In each age group, the difference between high and low slope values is similar, suggesting that there is no age effect on the variability of grip strength slopes (Figure 3). The slope and starting level of grip strength are associated (partial r1 = .12, p < .0001) beyond the effect of age, indicating that the stronger a subject is at the start of the study, the more likely he is to have a fast rate of loss of grip strength.
CVI O>
i i i i i
Grip strength and muscle mass. — Cross-sectional analysis demonstrates that both indices of muscle mass, creatinine excretion and summed forearm circumference decline with age and are highly associated, as best described by the regression equation:
:'": j ; ! ' : . :
i
Creatinine Excretion = -1222 + 52.3 (Summed Forearm Circumference) (r = .58, p < .0001) (Figure 4). (2) In the 382 subjects with grip, creatinine excretion, and forearm circumference data, summed grip strength is strongly related to both creatinine excretion (r = .58, p < .0001) and summed forearm circumference (r = .60, p < .0001) (Figure 5). Stepwise multiple regression analysis
•
i 50 m
40 30 40
i
1
I
i
i
1
45
50
55
60
65
70
75
SUMMED FOREARM CIRCUMFERENCE (cm) Figure 5. Regression of individual grip strength on forearm circumference (N = 382).
Downloaded from http://geronj.oxfordjournals.org/ at Cornell University Library on June 23, 2015
Figure 3. Comparison of the distribution of grip strength slopes by age group (young
