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Muscle Size, Strength, and Bone Geometry in the Upper Limbs of Young and Old Men

^a Canadian Centre for Activity and Aging, Lawson Health Research Institute
^b Division of Imaging, Lawson Health Research Institute
^c School of Kinesiology, Faculty of Health Sciences, and Departments of
^d Anatomy and Cell Biology, Faculty of Medicine and Dentistry, The University of Western Ontario, London, Canada
^e Medical Biophysics, Faculty of Medicine and Dentistry, The University of Western Ontario, London, Canada

C.L. Rice, Canadian Centre for Activity and Aging, St. Joseph's Health Centre Annex, 1490 Richmond St., London, Ontario, N6G 2M3 Canada E-mail: crice{at}uwo.ca.

	Abstract

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Background. Bone loss in old men is associated with a decrease in muscle mass and strength. However, the influence of muscle size and strength on age-related changes in bone geometry has not been comprehensively described.

Methods. Men in their third (group I, 23 ± 3 y, n = 20), eighth (group II, 77 ± 1 y, n = 10), and ninth (group III, 86 ± 4 y, n = 13) decades of age were studied. The cross-sectional area (CSA) of the elbow flexors, elbow extensors, and forearm muscles, the total area (TA), cortical area (CA), and medullary area (MA) of the midhumerus, and distal third of the radius and ulna (n = 7 group II; n = 6 group III) were measured with magnetic resonance imaging. The maximal isometric strength (MVC) of the elbow flexors and elbow extensors was also determined.

Results. The CSA and MVC of the arm muscles (elbow flexors plus elbow extensors) were less in group II (-17% and -22%) and III (-32% and -39%), respectively, compared to group I. However, forearm CSA was less (-21%) in group III only. The TA and MA of all bones were greater in the older groups. The CA of the humerus (-14%) and ulna (-10%), but not the radius, was less in group III compared to group I, whereas CA was unchanged in group II. Stepwise multiple linear regression determined that arm muscle CSA (r = 0.52, p < .01) and forearm muscle CSA (r = 0.41, p < .05) provided the best prediction of CA in the humerus and forearm, respectively.

Conclusions. Muscle size and strength are important determinants of CA in the humerus and forearm. The lower CA in the ninth decade may be explained, in part, by reduced bone strains due to a smaller muscle mass.

BONE is remodeled throughout life, and by old age, bone density is reduced and substantial changes occur in bone geometry ⁽¹⁾. In general, total bone and medullary cavity cross-sectional area increase throughout adulthood because of continual periosteal apposition and endosteal resorption ⁽²⁾. Eventually, resorption outpaces apposition in old age, resulting in a reduction in cortical area and bone strength ^(2)(3)(4). The age-related reduction in cortical area, like bone density, is more pronounced in women than it is in men, as is the incidence of osteoporosis ⁽¹⁾⁽⁵⁾. However, bone loss in men is now recognized as a significant public health problem, because one third of fractures occur in men, and the morbidity and mortality of hip fractures is three times higher in men than women ⁽⁶⁾.

The mechanisms underlying age-related changes in bone density and bone geometry are not understood completely, but a decrease in physical activity and circulating androgen and estrogen levels have been proposed as significant factors ⁽⁷⁾⁽⁸⁾. It has also been suggested that the age-related loss of muscle mass and strength contributes to the changes in bone because smaller muscles would generate less bone strain ^(9)(10). A number of reports have demonstrated an association between bone density or bone mineral content and muscle mass or strength in young and elderly people ^{(11)(12)(13)(14)}. However, there is little information on whether the reduction of muscle mass and strength contributes directly to the changes in bone geometry ^(15)(16). Moreover, much of the information on age-related changes in bone geometry was obtained from direct measures on cadavers or from radiographs in vivo to estimate cross-sectional area ^(2)(3)(4)(5). However, the accuracy of estimating cross-sectional parameters from one-dimensional radiographs has been questioned ⁽¹⁷⁾. A recent report demonstrated a positive correlation between cortical area of the tibia and muscle cross-sectional area (CSA) in children using magnetic resonance imaging (MRI) ⁽¹⁸⁾. No investigators have used MRI, which is the preferred method for two- and three-dimensional imaging ⁽¹⁹⁾, to determine and relate changes in both muscle size and bone geometry in an elderly population.

The purpose of this study was to determine the relationships among muscle size, muscle strength, and bone geometry in the upper limbs of young and old men. It was hypothesized that a reduction in cortical bone area with age would be associated with a decrease in muscle cross-sectional area and strength.

	Methods

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Subjects
A total of 43 men volunteered to participate in the study, and they were divided into young (group I, mean age 23 ± 3 y, n = 20), older (group II, 77 ± 1.3 y, n = 10), and oldest groups (group III, 86 ± 4 y, n = 13). The data of 33 of these 43 men were collected as part of our earlier study ⁽²⁰⁾. Ten older men (two in group II, and eight in group III) were added to the data set in the present study. Some measures (i.e., forearm data) were not obtained on these 10 men and are noted in the results. All subjects were ambulatory and were living independently in the community. They were free of chronic conditions that affect muscle performance or bone metabolism. Three to four men in each group participated in seasonal activities such as golf, bicycling, and walking, but were otherwise sedentary. The local ethics review committee approved all procedures, and informed written consent was obtained from each subject.

Muscle CSA, MVC, and Bone Geometry
The procedures for determining the maximal isometric strength (MVC) and muscle and bone morphology using MRI have been described previously ⁽²⁰⁾. Briefly, the MVC of the elbow flexors (EF) and elbow extensors (EE) were recorded on three occasions using a custom force dynamometer with the subjects in a supine position. Within 3 weeks of the MVC testing, a series of MR axial images (7-mm slice thickness) of the entire arm, or midarm at the largest girth, was recorded in all subjects. MR images of the entire forearm were taken in all young subjects and in seven and six subjects of groups II and III, respectively. The CSA of the biceps brachii, brachialis, triceps brachii, and forearm muscles (flexors + extensors), excluding fat and connective tissue, were determined in all images using a software program (Analyze 7.5, Mayo Clinic, Rochester, MN). Subcutaneous fat percentage (%) was determined at the level of the midhumerus as: subcutaneous fat CSA/whole arm CSA x 100. The bone measurements taken were length of the humerus and radius, total bone area (TA), and medullary area (MA). Cortical area (CA) was calculated as TA–MA. The values for TA, MA, and CA were means of 10 consecutive slices from the midhumerus (just distal to the deltoid tuberosity) and at 37% of the radius length from the styloid process (equivalent to the standard one third ulnar length site). Incorporating multiple slices was considered to be more representative of bone geometry than a single slice.

Statistical Analysis
Two-factor analyses of variance were used to determine the main effects of age (groups I, II, and III) and bone (humerus, radius, and ulna), and posthoc comparisons were completed using a Tukey test. Partial correlation coefficients were determined after adjusting for two or more of age, height, and weight. Stepwise multiple linear regression analysis was applied to determine which variables of age, height, weight, muscle CSA, and MVC provided the best prediction of CA. Differences were considered significant when p < .05, and all data are presented as means ± SD.

	Results

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Muscle CSA and MVC
There was no difference between groups I (76 ± 9 kg, 177 ± 7 cm), II (81 ± 12, 178 ± 5), and III (72 ± 8, 174 ± 6) in body weight and height (p > .05). Muscle CSA was less, and arm subcutaneous fat was greater with increased age (Table 1 ). The CSA of all muscles were lower in group III compared to group I and, except for the forearm and biceps brachii muscles, also were less than group II. The CSA of the biceps brachii, triceps brachii, and total arm muscles (EF + EE), but not the forearm muscles (p = .13), was less in group II compared to group I. The MVC was 333 ± 40 N and 292 ± 49 N for the EF and EE, respectively, in group I. The MVC of the EF and EE was reduced significantly in group II (-18% and -25%) and group III (-40% and -39%), respectively, compared to group I, with no significant difference between the muscle groups (Fig. 1).

View larger version (9K): [in this window] [in a new window]   Figure 1. Maximal isometric strength (MVC) of the elbow flexors and extensors in groups I, II, and III. *p < .05 compared to group I. p < .05 compared to group II.

View larger version (16K): [in this window] [in a new window]   Figure 2. Relationship between cross-sectional area (CSA) of the elbow flexors (EF) plus elbow extensors (EE) and cortical area (CA) of the midhumerus in all subjects. There was a significant correlation between the two measures (r = 0.52).

View larger version (14K): [in this window] [in a new window]   Figure 3. Relationship between cross-sectional area (CSA) of the forearm muscles and cortical area (CA) of the forearm (distal radius + ulna) in all subjects. There was a significant correlation between the two measures (r = 0.41).

	Discussion

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There were significant differences in bone geometry with increased age. The TA and MA, which reflect subperiosteal apposition (bone expansion) and endosteal resorption, respectively, were greater in the two older groups compared to group I. However, TA was similar between groups II and III, but MA was greater in the ninth decade in the ulna and humerus. Thus, bone expansion may not occur indefinitely, though endosteal resorption seems to be more prominent with increased age. The expansion of bone throughout adulthood has been described previously in both cross-sectional and longitudinal studies, but whether cessation occurs in men during the ninth decade is equivocal ^(5)(24)(25).

In our subjects, CA was significantly less in the humerus and ulna, but not the radius, in the ninth decade. Similar changes in CA were obtained in cadaver specimens, but in those studies, TA and MA of the humerus were not measured ^(4)(25). Also, Martin and colleagues ⁽⁴⁾ observed that the decline in CA of the second metacarpal began at age 60 years, some 20 years before CA was reduced in the humerus and femur ⁽⁴⁾. Moreover, the magnitude of the age-related differences in bone geometry was dependent on the bone site ⁽¹⁷⁾. That the magnitude and time course of differences in bone geometry with age are bone-site–dependent suggests that mechanical factors, such as strain induced by skeletal muscle, likely influence bone geometry.

The strength of an intact bone is defined by its material properties such as porosity (or density) and geometry (or structure) ⁽²⁶⁾. For example, the resistance of bone to compressive (axial) loads primarily depends on CA, whereas resistance to bending and torsion depends on the distribution of cortical mass about the bone center ⁽²⁶⁾. Because CA was lower in group III, but not group II, the strength of the humerus during compression may not decrease significantly until the ninth decade. However, because the cortical mass is redistributed further from the bone center, bending and torsional strength may actually increase with age, particularly if the loss of material strength is negligible ^(3)(26). The redistribution of cortical mass increases the bone's polar and area moments of inertia, measures that combine the distribution and area of cortical bone as an index of bending and torsional strength ^(4)(26). Although we did not directly measure the polar moment of inertia, it is likely greater in group II compared to group I by virtue of the subjects' larger MA and TA, but similar CA. In support of this idea, Martin and colleagues ⁽⁴⁾ reported that the polar moment of inertia of the humerus was progressively larger between 40 years and 80 years and then was less in the ninth decade. Also, others reported that the polar moment of inertia of the radius, tibia, and femur was greater with age in men, but whether a subsequent decline occurred after age 80 was not clear from their linear regression analysis ^(5)(25). It seems that the redistribution of cortical mass compensates, at least somewhat, for the loss in material strength in men and thereby helps to preserve bone strength to at least 80 years of age.

Muscle contraction, as opposed to body weight, generates the largest strain on bone ⁽⁹⁾. Consequently, age-related bone loss and differences in bone geometry may stem, in part, from reduced bone strains secondary to a loss of muscle mass with age. Our findings suggest that muscle CSA and MVC explained as much as 35% of the variation in CA of the arm and forearm, and were more powerful predictors of CA than age, height, and weight. In addition, the partial correlations between muscle CSA or MVC and CA were greater in the forearm (r =0.47–0.59) than the humerus (r = 0.18–0.36). The radius, in particular, may be more malleable or experience superior loading from the attached musculature during daily activities than the ulna and humerus. Palmer and Werner ⁽²⁷⁾ reported that 82% and 18% of an axial load on the forearm is transmitted across the radiocarpal and ulnacarpal joints, respectively. There are no previous reports on the association of muscle CSA (MVC) and CA in the aged population using MRI ⁽¹⁶⁾, but these measures were significantly related in children and young adults ^(18)(28). Other investigators, however, reported that the age-related decline in muscle mass or strength explained up to 50% of the variation in bone density or estimated bone strength ^{(11)(12)(13)(14)(15)(29)}, although in some cases no association was observed ⁽³⁰⁾.

Although muscle CSA and MVC were better determinants of CA in the present study, arm muscle CSA and MVC were 20% less, whereas CA was not different (i.e., a lower CSA/CA ratio) in group II compared to group I. However, muscle CSA and CA were both lower in group III compared to group II. Although muscle CSA was smaller, but CA was not different, in group II compared to group I, this does not necessarily negate the hypothesis that muscle mass influences bone mass and geometry during the aging process ^(9)(10). Indeed, changes in CA may lag behind the gradual loss of muscle mass and strength by several years because bone remodeling is relatively slow compared to the adaptation of muscle mass and strength ⁽⁹⁾. Moreover, it seems that the greater porosity of cortical bone with age is more closely related in time to the loss of muscle mass (strength). For example, porosity of the humerus and femur are progressively greater after age 40 or 50 ^(4)(31)(32), the age at which lower (i.e., 10%) muscle mass and strength become evident ^(21)(22)(23). Thus, any muscle-induced effect on cortical bone may first become apparent as increased porosity, followed years later by a decline in CA. Clearly, numerous other factors such as genetics, hormone levels, diet, and physical activity may influence the changes in bone with age ⁽¹⁾⁽⁷⁾. As well, these factors likely contributed to the intersubject variability in the present study and thereby reduced the correlative power between muscle CSA and CA. A longitudinal study would help to illustrate more clearly the magnitude of the association between the changes in muscle and bone in the aged population.

In summary, CA was unchanged in the eighth decade, but was less in the ninth decade in the humerus and ulna. Muscle CSA and MVC were more strongly associated with CA, particularly in the forearm, than age, height, and weight. The results suggest that the decrease in muscle size and strength with age contributes significantly to the decline in CA.

	Acknowledgments

 
We thank Mr. Jean Theberge for excellent technical support in the acquisition of the MR images. We are grateful to all the subjects who participated in this study. We acknowledge the support of the Natural Sciences and Engineering Research Council of Canada, St. Joseph's Health Centre, and the Academic Development Fund of the University of Western Ontario. C.S. Klein was a recipient of an Ontario Graduate Scholarship in Science and Technology during the course of this study.

Received January 17, 2002

Accepted February 15, 2002

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