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Research Reports |
S Mathur, BSc(PT), PhD, is a post-doctoral fellow at the University of Florida, Gainesville, Fla. She was a doctoral student in Human Kinetics at the University of British Columbia, Vancouver, British Columbia, Canada, at the time of the study. Dr Mathur's institutional mailing address is: Muscle Biophysics Lab, Vancouver Coastal Health Research Institute, Room 500–828 W 10th Ave, Vancouver, British Columbia, Canada V5Z 1L8
KPR Takai, BSc(PT), MSc, is a clinical physical therapist. She was a graduate student in the School of Rehabilitation Sciences, University of British Columbia, at the time of the study
DL MacIntyre, BSc(PT), PhD, is Associate Professor, Department of Physical Therapy, University of British Columbia, and Investigator, Rehabilitation Research Lab, GF Strong Rehabilitation Centre
D Reid, BMR(PT), PhD, is Professor, Department of Physical Therapy, and Chair, Research Graduate Programs in Rehabilitation Sciences, University of British Columbia
Address all correspondence to Dr Mathur at: sunitamathur{at}phhp.ufl.edu
Submitted February 12, 2007;
Accepted September 17, 2007
 | Abstract |
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Subjects and Methods: Twenty older adults who were healthy and 20 people with chronic obstructive pulmonary disease (COPD), matched for age, sex, and body mass index, underwent MRI to obtain measurements of thigh muscle CSA and volume. Anthropometric measurements (skinfold thickness and thigh circumference) were used to estimate midthigh CSA.
Results: Muscle volumes were significantly lower in the people with COPD than in the older adults who were healthy. Moderate to high correlations were found between midthigh CSA and volume in both groups (r=.61–.94). Anthropometric measurements tended to overestimate midthigh CSA in both the people with COPD (estimated CSA=64.9±17.8; actual CSA=48.3±10.2 cm2) and the older adults who were healthy (estimated quadriceps femoris muscle CSA=65.0±14.0; actual CSA=56.8±13.5 cm2). Furthermore, the estimated quadriceps femoris muscle CSAs were not sensitive enough to detect a difference in muscle size between people with COPD and controls. Thigh circumference alone was not different between groups and showed only low to moderate correlations with muscle volume (r=.19–.47).
Discussion and Conclusion: Muscle CSA measured from a single slice provides a good indication of volume, but the most representative slice should be chosen on the basis of the muscle group of interest. Thigh circumference is not correlated with muscle volume and, therefore, should not be used as an indicator of muscle size. The development of population-specific reference equations for estimating muscle CSA from anthropometric measurements is warranted.
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As well as in aging, the loss of muscle mass is a common finding in chronic conditions such as cancer,6 HIV infection,7 chronic heart failure,8 and chronic obstructive pulmonary disease (COPD)9 and is related to exercise limitations, quality of life, and mortality.7,8,10 Because of the widespread prevalence of muscle atrophy and its impact on the health and independence of aging adults and people with chronic conditions, it is essential that physical therapists accurately assess and appropriately manage muscle atrophy.
There are several methods for quantifying muscle mass; these include dual x-ray absorptiometry, bioelectrical impedance, ultrasound, computed tomography (CT), and magnetic resonance imaging (MRI). Dual x-ray absorptiometry and bioelectrical impedance provide estimates of fat-free mass for the whole body or body segments,11,12 whereas ultrasound has been used to measure muscle thickness and examine muscle architecture.13 For examining the relationships between muscle mass and muscle strength or for determining the effectiveness of interventions in improving muscle mass, more specific measurements of muscle size, such as the cross-sectional area (CSA) and volume of individual muscles, are necessary.
Muscle volume and CSA can be obtained from CT and MRI scans and are commonly used in research settings. Muscle volume is the preferred measure of muscle size because it allows the entire muscle to be captured from multiple images and, therefore, takes into account the entire size of the muscle, regardless of its shape.14 However, to obtain measurements of muscle volume, multiple images along the length of a limb are required, resulting in increases in the time required for and the cost of scanning and analysis. In addition, with CT, longer scan times result in greater exposure to radiation, thereby increasing the risk to the patient.15 To reduce the time and cost of imaging and analysis, a single cross-sectional slice is commonly used as an indicator of total muscle size. For the lower limbs, the midthigh CSA is commonly used as an indicator of the muscle size of the thigh.4,10,16 However, it has not been clearly delineated whether the midthigh is the best representative level for all muscle groups of the thigh, such as the quadriceps femoris, hamstring, and adductor muscle groups, which show differences in anatomical distributions along the length of the thigh.17
Because of the cost of and the technical expertise required for the use of the instrumentation mentioned above, physical therapists working in typical clinical settings do not have access to these specific measurements of muscle CSA or volume. Anthropometric measurements (ie, limb circumference and skinfold thickness) often are used to estimate muscle mass with reference equations18; alternatively, limb circumference alone is used as an estimation of the size of the underlying muscle. However, there are many assumptions underlying the use of anthropometric measurements to estimate muscle mass. For example, it is assumed that the muscle has a circular shape and that subcutaneous tissue is uniformly distributed around the circumference of the limb and represents all of the adipose tissue in the section.19,20 These assumptions may not hold true, especially in older adults or people with chronic conditions who experience muscle atrophy, such as people with COPD.
The purpose of this study was to determine the relationships among muscle volume, muscle CSA, and thigh circumference measurements taken at different levels of the thigh. In addition, we examined whether a published reference equation for estimating midthigh muscle CSA provides a reasonable estimation of the muscle CSA obtained from MRI in older adults who are healthy and in people with COPD.
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None of the participants were currently smoking. Participants were asked to complete a health risk screening questionnaire prior to inclusion in the study.23 Those who indicated the presence of comorbid cardiovascular disease (eg, heart failure, previous myocardial infarction, or cardiovascular surgery), neurological conditions (eg, stroke or Parkinson disease), or lower-extremity musculoskeletal problems (knee or hip injury or arthritis) were excluded from the study. Each participant provided written informed consent prior to participation.
Height and weight were measured with shoes off and light clothing. Participants underwent spirometry according to the standards described by the American Thoracic Society24 to measure FEV1 and FVC to define the presence and severity of COPD.
MRI
Magnetic resonance imaging was used to determine the muscle CSA and muscle volume of the quadriceps femoris, hamstring, and adductor muscles. A 1.5-T MRI scanner* was used to acquire 5-mm axial contiguous slices from the anterior superior iliac spine to the femoral-tibial joint line on both thighs. The images were T1 weighted (echo time=8 milliseconds; repetition time=650 milliseconds), with a 40-cm2 field of view and a matrix of 512x384 pixels (in-plane spatial resolution=0.78x1.78 mm). The MRI scan resulted in approximately 100 slices for each participant.
For each participant, 2 landmarks were identified on the MRI scan: 2 cm below the anterior inferior iliac spine (proximal slice) and the superior aspect of the patella (distal slice). The distance between the proximal and distal slices was divided equally to select 17 slices from the MRI scan. The muscle CSA and volume of the quadriceps femoris, hamstring, and adductor muscles were determined from measurements taken on these 17 selected slices.
Muscle CSA and Volume
NIH Image, version 1.31,
was used to manually outline each of the quadriceps femoris (rectus femoris), vastus (vastus lateralis, vastus intermedius, and vastus medialis), hamstring (semitendinosus, semimembranosus, and biceps femoris long head and short head), and adductor (pectineus, adductor longus, adductor magnus, and adductor brevis) muscles on the 17 selected slices. Individual muscles are shown on 3 axial images in Figure 1.
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The CSAs measured for the quadriceps femoris, hamstring, and adductor muscles on 3 of the 17 slices, located at 30%, 50%, and 80% of the thigh length (Fig. 1), were used for further muscle volume comparisons. The 50% slice, or midthigh level, was chosen because it is commonly used in the literature to quantify thigh muscle CSA. The distal slice, closer to the knee (80% of the thigh length), was chosen for the hamstring muscles because this was the level at which the hamstring muscle CSAs were the largest in our subjects. The proximal slice (30% of the thigh length) was the slice at which the CSAs of the adductor muscle group tended to be the largest.
Thigh Circumference
Thigh circumference was measured by outlining the outside border of the thigh on the MR images at 5, 10, and 15 cm above the superior aspect of the patella by using NIH Image. To ensure the validity of circumference measurements obtained from MR images, a tape measure was used to compare these measurements with the measurements obtained in vivo from 10 of the subjects who were healthy. Measurements were obtained with the participant lying supine with the knee in slight flexion and supported by a rolled towel. Ink marks were made at 5 and 10 cm above the superior border of the patella, and a steel tape measure was placed with the lower border level with the mark. Three recordings were obtained at each distance, with the tape measure being removed each time, and an average was calculated. The tape measure was pulled taut so that no buckles occurred, but not so tight that it caused an indentation in the skin. The average percent errors between thigh circumference measurements obtained from MR images and those obtained with the tape measure were 3.2% at 5 cm and 4.2% at 10 cm.
Estimation of Muscle CSA From Anthropometric Measurements
Measurements of thigh circumference and skinfold thickness were made on all participants with the protocol established by Housh et al.18 This protocol was chosen because it allows the prediction of quadriceps femoris and hamstring muscle CSAs individually rather than predicting the total thigh muscle CSA26 and because it was developed from muscle measurements obtained by MRI. In short, thigh circumference (tape measure) and skinfold thickness (Harpenden skinfold calipers
) were measured 3 times each at the point midway between the inguinal crease and the lateral femoral condyle. The average thigh circumference and the average skinfold thickness measurements were entered into the following regression equations developed by Housh et al18 to estimate the CSAs of the quadriceps femoris and hamstring muscles at 50% of the thigh length:
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Data Analysis
Data analysis was done with the Statistical Package for the Social Sciences, version 13.0.
Descriptive statistics (mean and standard deviation) were used to describe the sample characteristics and muscle volumes. Correlations were determined for BMI, muscle CSA, thigh circumference, and muscle volume as Pearson product moment correlation coefficients. The following descriptors were used to assess the strength of the correlations: low=.26–.49, moderate=.50–.69, high=.70–.89, and very high=.90–1.00.27 The Bland-Altman procedure was used to compare the anthropometric estimations of quadriceps femoris and hamstring muscle CSAs (ie, the alternative measurements) with the MRI measurements of the CSAs (ie, the criterion measurements). The Bland-Altman plot displayed the difference between the alternative and the criterion measurements on the y-axis against the average of the 2 measurements on the x-axis.28 The limits of agreement (ie, mean ± 2 standard deviations) were constructed around the mean difference between the 2 measurements. If the mean difference between the 2 measurements was different from 0, then there was either underestimation or overestimation of the criterion measurement.28
| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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The midthigh CSA was estimated from anthropometric measurements (thigh circumference and skinfold thickness) with a published equation.18 The mean quadriceps femoris and hamstring muscle CSAs estimated with the published equation were 64.9±17.8 and 23.3±5.6 cm2, respectively, for the people with COPD and 56.7±36.8 and 19.5± 16.9 cm2, respectively, for the older adults who were healthy. These values were not significantly different (Tab. 1), indicating that the equation was unable to detect a smaller muscle size in people with COPD than in the older adults who were healthy. Similarly, measurements of the thigh circumference at 5, 10, and 15 cm were not different between the groups (Tab. 1).
Relationships Among BMI, Muscle Volume, and Muscle CSA
Low to moderate correlations were found between BMI and specific measurements of muscle size. In people with COPD, significant correlations were found between BMI and the volume of the hamstring (r=.48, P=.03) and adductor (r=.49, P=.03) muscles (Tab. 2). Moderate correlations (r
.50) were found between BMI and the muscle CSA at various levels: quadriceps femoris muscle at 80% (r=.52, P=.02), hamstring muscle at 50% (r=.56, P=.01), hamstring muscle at 80% (r=.51, P=.02), and adductor muscle at 50% (r=.58, P=.008).
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Relationships Between Muscle CSA and Muscle Volume
The majority of the correlations between muscle CSA and muscle volume were moderate to very high, with the exception of the adductor muscles at 80% for both groups and the hamstring muscles at 30% only for the people with COPD (Tab. 3). When the entire sample of subjects was considered, the quadriceps femoris and hamstring muscles showed significant correlations between muscle volume and muscle CSA at all 3 levels (Tab. 3). The adductor muscle volume was significantly correlated with the adductor muscle CSA at 30% (close to the hip) and 50% (midthigh) but not at 80% (close to the knee). Representative scatterplots of the correlations between muscle volume and muscle CSA at 50% are shown in Figure 2.
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| Discussion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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The midthigh CSA often is used to represent the size of the thigh muscles29 or to calculate the specific torque (ie, torque/CSA) of a muscle group, such as the quadriceps femoris muscle group.30 However, the relationship between muscle CSA and muscle volume had not previously been examined in older adults or people with COPD. Muscle CSA and muscle volume were closely correlated; this result was expected because multiple CSAs were used to calculate the total muscle volume. Therefore, the correlation between volume and CSA is circular in nature because volume measurements are dependent on CSA measurements. For the quadriceps femoris and hamstring muscles, there were strong correlations between the CSAs at all 3 levels and muscle volume. However, the adductor muscle volume was most strongly correlated with the CSAs at the proximal slices (30% and 50%) and showed a low correlation at the distal slice, at which some people did not show the presence of any adductor muscles. Therefore, if one is interested in the size of a specific muscle group on a single image, it is necessary to choose the level at which the CSA is maximized for that particular muscle group.
Body mass index is considered to be a general measure of body composition, incorporating both fat mass and lean mass in relation to a person's stature.31 In the present study, we found moderate correlations between BMI and some measurements of muscle volume and CSA; however, no difference in BMI was found between people with COPD and controls, despite the presence of muscle atrophy in people with COPD. It was previously shown that up to 11% of men and 24% of women who have COPD and who have a BMI within the normal range actually have a low lean body mass.9 In addition, BMI does not appear to be an adequate marker of changes in body composition in older adults because the decrease in lean muscle mass with age can be countered by an increase in fat mass, resulting in a stable BMI over time.31 Therefore, more specific measurements of muscle size are needed to determine the presence of muscle atrophy or sarcopenia in these populations.
Magnetic resonance imaging and CT are costly techniques that require specialized equipment, technical support, and software for analysis.15 In the clinical setting, it is important to have low-cost, efficient, and accurate measurements that can easily be applied during an assessment. Anthropometric measurements are ideal for this situation; however, they may not provide adequate estimates of muscle size in older adults or people with COPD. We chose to use a published equation that was developed from young men to attempt to estimate midthigh CSA18 because no reference equations have been developed for older adults or people with COPD. The equation developed by Housh et al18 was appealing because it allowed for individual estimates of quadriceps femoris and hamstring muscle midthigh CSAs rather than only a general estimate of thigh muscle CSA.
In our sample, the equation tended to overestimate the CSAs of both the quadriceps femoris and the hamstring muscles, to such an extent that it was unable to detect a difference in muscle size between adults who are healthy and people with COPD. This finding is similar to the findings of previous studies that compared estimates made from MRI or CT with anthropometric estimates in middle-age adults,19 people with various levels of adiposity,20 and people who had COPD and muscle atrophy.10 Prediction equations, such as that described by Housh et al,18 are typically developed in young men who are healthy and are based on several assumptions about the shape of the muscle and the distribution of adipose tissue that may not hold true as people age or under conditions in which muscle atrophy occurs, such as COPD. For example, in a young person, the majority of adipose tissue in the thigh lies within the subcutaneous tissue compartment, whereas in older adults and people who have atrophy, there is a greater distribution of intermuscular fat4 that is not captured in measurements of limb circumference or skinfold thickness. Furthermore, we have found that people with COPD have greater intramuscular fat infiltration, as seen on T1-weighted MRI, compared with matched controls who are healthy.32 This feature can lead to an overestimation of muscle CSA by the prediction equation because thigh circumference and skinfold thickness do not properly reflect the amount or location of adipose tissue and the size of the underlying muscle. The development of population-specific reference equations for older adults who are healthy and people with COPD would benefit clinicians in assessing muscle CSA with a simple, but accurate, method.
Thigh circumference is another measurement that can be easily applied in the clinical setting and that is often used by clinicians to assess muscle atrophy or changes in muscle size with training. From the present study, however, it does not appear that thigh circumference provides a sensitive measure of muscle size because it was not able to distinguish muscle size in people with COPD from that in controls who are healthy. Similarly, Arangio et al33 found that in people who had undergone anterior cruciate ligament reconstruction and experienced thigh muscle atrophy, thigh circumference showed a difference of only 1.8% between the injured (atrophied) leg and the noninjured leg, whereas muscle CSA obtained by MRI showed a difference of 8.6%. Furthermore, we observed only a single significant correlation: between thigh circumference and muscle volume (ie, thigh circumference at 10 cm in the sample of people with COPD). Therefore, it appears that thigh circumference is not a good indicator of muscle size and should not be used alone as a clinical measure of muscle atrophy.
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| Footnotes |
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The Clinical Research Ethics Board of the University of British Columbia approved the study.
* General Electric, 2421 N Mayfair Rd, Milwaukee, WI 53266. 
National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892. Available at: http://rsb.info.nih.gov/nih-image/download.html.
Baty International, Victoria Rd, Burgess Hill, West Sussex RHI5 9LB, United Kingdom.
SPSS Inc, 233 S Wacker Drive, Chicago, IL 60606
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