Journal of Clinical Densitometry: Assessment & Management of Musculoskeletal Health, vol. -, no. -, 1e5, 2015 Ó Copyright 2015 by The International Society for Clinical Densitometry 1094-6950/-:1e5/$36.00 http://dx.doi.org/10.1016/j.jocd.2015.05.063
Review Article
Assessment of Lean Mass and Physical Performance in Sarcopenia Peggy M. Cawthon* Research Institute, California Pacific Medical Center, San Francisco, CA, USA
Abstract This review provides a description of the assessment of lean mass and physical performance with particular attention to how these measures are used in the context of sarcopenia, in both research and clinical settings. One of the most common methods to estimate muscle mass is whole-body dual-energy X-ray absorptiometry (DXA). DXA estimates the total amount of lean tissue but does not directly measure muscle mass. Appendicular lean mass (ALM), derived from DXA scans, is the sum of the lean tissue in the arms and legs. ALM alone, or scaled to height squared (ALM/height2) or body mass index (ALM/body mass index), is the most common metric used as an approximation of muscle mass in sarcopenia research. Other methods to assess muscle mass include central or peripheral quantitative computed tomography (to determine muscle cross-sectional area and muscle density, a marker of fat i nfiltration into the muscle); magnetic resonance (to assess muscle cross-sectional area and volume); and bioelectrical impedance analysis (to determine fat-free mass). Many approaches to objectively measuring physical performance have been used in sarcopenia research. Muscle strength is often measured: Grip strength is very inexpensive and straightforward to assess, whereas assessment of lower extremity strength is more difficult. However, lower extremity strength may be a more relevant measure than grip strength in the context of mobility outcomes. Dynamic physical performance is also widely measured in research settings and may be emerging as a routine assessment in clinical care. The most widely used measure of physical performance is walking speed over a short distance, usually 3e6 m. Other measures of objective physical performance include the Short Physical Performance Battery that includes gait speed, ability and time to rise from a chair 5 times, and static balance tests; and the Timed Up and Go test that measures the time to rise from a chair and walk a short distance. Finally, longer distance walking tests are also used. ‘‘Fast’’ versions of these tests measure either distance traveled in a set amount of time (as for the 6-minute walk test) or time to walk a set distance (such as the fast long distance corridor walk more than 400 m). The ‘‘usual pace’’ version of the longer distance walking test, the usual-pace 400 m walk, is an objective measure of disability and has been used as an outcome in clinical trials. In summary, there are many methods available to assess muscle mass and physical function, each with advantages and limitations. The choice of what test to use depends on the nature of the research question or the clinical environment and the availability of resources for evaluation. Key Words: Sarcopenia; physical performance; strength; walking speed; lean mass.
research and clinical settings. First, the article will begin with a discussion of the assessment of lean mass and will then describe the assessment of physical performance. The first definition of sarcopenia was proposed by Baumgartner (1) in 1988. This definition used lean mass in the arms and the legs (appendicular lean mass) from dualenergy X-ray absorptiometry (DXA) to define sarcopenia. Another definition of sarcopenia, proposed by Newman (2) in 2003, defined sarcopenia based on lean mass values adjusted for height and fat mass. More recently proposed
Introduction This article will describe the assessment of lean mass and physical performances with particular attention to how these measures are used in the context of sarcopenia in both Received 05/04/15; Accepted 05/04/15. *Address correspondence to: Peggy M. Cawthon, PhD, Research Institute, California Pacific Medical Center, 550 16th Street, 2nd Floor, Box 0560, San Francisco, CA 94158. E-mail: pcawthon@ psg.ucsf.edu
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definitions of sarcopenia are more integrative and include components of performance in addition to measures of lean mass. These definitions include those proposed by the International Working Group, (3) the European Working Group for Sarcopenia in Older Persons (4), and the Foundation for the NIH Sarcopenia Project (FNIH) (5).
connective or fibrotic tissue, water, and organ mass. Typically, total body lean mass and abdominal lean mass are not considered in the assessment of sarcopenia as lean mass from the abdomen in particular may not reflect actual muscle mass.
Other Imaging Methods Assessment of Muscle Mass and Muscle Characteristics The assessment of muscle mass is complex and numerous methods have been used to estimate muscle mass in the context of sarcopenia (Table 1).
Dual-Energy X-ray Absorptiometry Perhaps the most commonly used method for the assessment of lean mass in research settings is whole-body DXA. Regional DXA scans (such as scans of the proximal femur) are commonly used to determine bone mineral density at the hip or spine for the diagnosis of osteoporosis. Modern densitometry machines are also capable of whole-body DXA scans to measure fat mass, bone mineral content, and lean mass. The lean mass in the arms and legs (appendicular lean mass) is used as an approximation of muscle mass in sarcopenia research. ALM alone, or scaled to height2 (ALM/height2) or BMI (ALM/BMI), is the most common metric used. Clinicians and researchers should be aware that DXA does not measure muscle mass directly. Some of the mass identified as lean is not muscle, and likely includes
There are numerous other imaging modalities that can assess the quantity of muscle in a specific region of the body, including computed tomography (CT) and magnetic resonance imaging. Both central CT scans, such as abdominal CT or thigh CT, as well as peripheral CT (usually of the calf), have been used to assess muscle cross-sectional area (CSA). One advantage of CT is that muscle density can be calculated. Muscle density is a marker of fat infiltration into the muscle. It is determined by the attenuation of muscle tissue and expressed in Hounsfield units. Thigh muscle density has been shown to increase the risk of mobility limitations in older adults, independent of muscle CSA and strength (6). Magnetic resonance imaging can be used to assess muscle CSA and volume, but muscle density cannot be measured on MR images. There is no radiation exposure in MR image acquisition. However, patients must be free of implanted metal, which limits the number of individuals in whom these measures could be completed. Whole-body MR is perhaps the most accurate assessment of total body muscle mass, but whole-body scans take a long time to complete. Relatively limited availability of CT and MR machines (especially outside the United States)
Table 1 Advantages and Disadvantages of Common Methods to Assess Muscle Mass Method
Most common metric(s)
Advantages
Whole-body DXA Appendicular lean mass Densitometers commonly available (at least in the United States); common research tool CT (central and Muscle cross-sectional Precise measures of crossperipheral) area, muscle density sectional area; muscle density provides estimate of ‘‘muscle quality’’ MRI Muscle cross-sectional Precise measures of muscle area and volume cross-sectional area and volume; no radiation exposure
BIA and BIS
Fat-free mass and lean mass
Disadvantages Radiation exposure; measures lean mass which is an indirect assessment of muscle
Radiation exposure; high cost; intermachine differences; only provide regional estimates of muscle size
High cost; intermachine differences, only provides regional estimate of muscle size unless whole-body scan is completed; cannot estimate muscle density; implanted metal precludes use (which is relatively common in older adults) Widely available and low cost Not a direct measure of lean mass; hydration status and electrolyte balance can bias measures
Abbr: BIA, bioelectrical impedance analysis; BIS, bioimpedance spectroscopy; CT, computed tomography; DXA, dual-energy X-ray absorptiometry; MRI, magnetic resonance imaging. Journal of Clinical Densitometry: Assessment & Management of Musculoskeletal Health
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and substantial expense with these methodologies are other disadvantages of these methods.
Bioelectrical Impedance Analysis Other methods to estimate muscle mass include bioelectrical impedance analysis and bioimpedance spectroscopy. These noninvasive measures take advantage of the fact that various tissues of the body have different resistivity to currents, or impedance. With both of these technologies, a weak electrical current is directed through the body. This impedance is measured and used to extrapolate body composition parameters, such as total body water and lean mass. These measures are widely available and devices are relatively of low cost. Impedance technologies have several limitations, however. Impedance measurements are most accurate for healthy individuals. Measurements are influenced by physiological factors such as hydration status and electrolyte balance, problems that may be more common in older adults.
Assessment of Physical Function Physical function can be assessed in 2 ways: It can be assessed objectively, using standard protocols, often with minimal equipment, or subjectively, by asking individuals about their ability to complete specific tasks. Generally, measures of subjective function, such as activities of daily living (e.g., feeding, dressing, toileting, transferring) and instrumental activities of daily living (e.g., managing finances
and medications, shopping, preparing meals), are not included in definitions of sarcopenia and are therefore omitted from this review. Objective measures of strength and physical function are common in research settings but are much less common in clinical practice (Table 2).
Muscle Strength and Power Many research studies have assessed muscle strength in many tens of thousands of participants. The most straightforward measure of strength to obtain is grip strength. Grip strength is typically measured with a relatively inexpensive hand-held dynamometer. The protocol to measure 2e3 trials in each hand can be completed in several minutes with few exclusion criteria, although individuals with hand and wrist pain due to arthritis and other conditions may find the test uncomfortable. Weak grip strength is predictive of poor health outcomes; for example, Rantanen et al (7) found that poor grip strength measured in mid-life (45e68 years) was associated with increased likelihood of disability 25 years later. The major disadvantage of grip strength is that it is a measure of upper extremity strength; when clinicians and researchers are interested in mobility, measures of lower extremity strength may be more relevant. Additional advantage of grip strength is that dynamometers are highly portable, allowing grip strength to be measured in many settings. However, direct measures of lower extremity strength are more difficult to obtain. Lower extremity strength measures can be obtained using inexpensive equipment (such as dynamometers tied to a chair), but these
Table 2 Advantages and Disadvantages of Objective Physical Performance Measures Method Grip strength, lower extremity strength, power
Most common metric(s)
Advantages
Disadvantages
Maximum or average For grip strength, cheap strength; peak power equipment, quick protocol, few exclusions, widely used in research
Lower extremity strength or power may be a better measures for assessing mobility performance, but such measures are difficult, expensive and results may differ between machines Gait speed (short distance) Walking speed in Inexpensive and simple Many factors contribute to walking meters per second protocol; few exclusions speed, thus this measure is nonspecific for identifying particular deficits Short Physical Summary score Inexpensive and simple Potential ceiling effects as it is difficult Performance Battery from 0 to 12 protocol; few exclusions to discern good versus excellent performance Timed Up and Go Time to complete Specifically evaluated for fall Integrative measure does not allow for risk; inexpensive and simple separate evaluation of gait and chair protocol, few exclusions rise components Long distance walking 400-m walk: time to Relatively inexpensive Some exclusions and safety tests (400 m walk, complete protocol. considerations especially for ‘‘fast’’ 6-minute walking test) 6MWT: distance versions. Requires long corridor or walked in 6 minutes other space to complete assessment
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4 methods tend to be highly variable. Large, nonportable machines measure lower extremity strength in a highly reproducible manner. However, these devices are costly (often $10,000 or more). In addition, many different types of machines have been used in research settings. It is difficult to compare measures of lower extremity strength across machines owing to differences in the positioning and the specific muscles targeted. Thus, given the cost and complexity of assessing lower extremity strength, and the lack of overlapping data, integrative definitions of sarcopenia tend to include grip strength as the measure of muscle strength, rather than a lower extremity strength measure. Power, which measures both force and the speed of the force generation, is also assessed in research settings. Assessment of power often requires specialized equipment and complex protocols; therefore, it is not commonly used in clinical practice.
Performance Dynamic measures of physical performance have been widely assessed in research settings and may be emerging as routine assessments in clinical settings. The most widely used measure of objective performance in research in older adults is gait speed over a short distance, usually 3e6 m. Generally, the time to walk 2 or more trials is assessed, and the maximum or average gait speed over this time is calculated and expressed as meters walked per second, or m/s. Gait speed is strongly and independently predictive of mortality, even after accounting for comorbid factors and physiological deficits that may affect walking ability (8). Various cut points to define ‘‘slow’’ walking speed have been proposed. Integrative definitions of sarcopenia include cut points for slow walking speed of !1.0 m/s or !0.8 m/s. Cummings et al recently proposed a definition for the condition ‘‘dismobility,’’ defined as gait speed 0.6 m/s (9). Gait speed slows dramatically with age, reflected in increasing prevalence of dismobility. In data from the National Health and Nutrition Examination Survey, only 1.2% of men aged 50e54 years walked 0.6 m/s or slower, whereas 31% of men aged 85 years or older walked this slowly. Many other objective measures of performance that have been included in research settings. The Short Physical Performance Battery (SPPB) (http://www.grc.nia.nih.gov/ branches/leps/sppb/) incorporates performance on 3 tests: gait speed over a short distance, ability and time to rise from a chair 5 times, and balance tests. Performance on each of the components is given a score of 1e4; those unable to complete a component receive a score of 0 for that component. The scores are then summed, and the summary score then ranges from 0 to 12. Generally, for older adults, high performance on the SPPB is a score of 9e10 or greater. However, there may be ceiling effects in the SPPB, as it can be difficult to distinguish differences among those with good
Cawthon to excellent performance. Poor SPPB performance predicts disability and other adverse health outcomes in older persons (10). One component of the SPPB, ability and time to complete repeat chair stands, is a measure of dynamic power and balance and is also often assessed in research studies. The ability to rise from a chair once without the use of the arms is predictive of poor outcomes. In community dwelling older adults, relatively few are unable to complete this task. However, the single chair stand test is attractive as a potential clinical measure owing to its ease of implementation. Another test that has been used to assess mobility is the Timed Up and Go Test (http://www.cdc. gov/homeandrecreationalsafety/pdf/steadi/timed_up_and_go_ test.pdf). In this test, individuals are asked to stand from a chair, walk 3 m, turn around, return to the chair, and sit down. Those who take longer than 12 seconds to perform this task have been shown to have a high risk of falling. Finally, the last type of physical performance test that is routinely used in research studies is observed performance on longer distance walks. There are generally 2 approaches to long-distance walks. One version asks participants to walk as quickly as possible over a longer distance (such as 400 m) (11) or asks participants to walk as far as possible in a given time (such as the 6-minute walk test) (12). These ‘‘fast’’ walk tests are considered to be measures of aerobic capacity and have been used as outcomes in clinical trials. In the second version of these tests, usually completed only for the 400 m distance walk, participants are asked to walk at their usual pace, and time to complete the walk is recorded. Participants unable to complete the walk, or those who cannot complete the walk in 15 minutes, are considered to have mobility disability. This objective outcome of disability has recently been used as the primary outcome in the LIFE study that demonstrated a reduction in mobility disability among those who completed a physical activity program. In conclusion, this review has summarized methods for assessing muscle mass (including DXA, MR, CT, and bioelectrical impedance analysis) and objective physical performance (including strength, walking performance, power, and the SPPB) in the context of sarcopenia. There are many methods available to assess each domain, each with advantages and limitations. The choice of what test to use depends on the nature of the research question or the clinical environment and the availability of resources for evaluation.
Acknowledgments The author thanks Augusta Broughton for her administrative assistance with the manuscript. Peggy M. Cawthon reports consultancy with Amgen and Eli Lilly, and grants to her institution from IMS Health, GlaxoSmithKline, Merck, and Amgen for work outside this manuscript.
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Key Points Sarcopenia definitions include measurement of lean mass and physical performance. There are many methods available to assess muscle mass and physical function; each has advantages and limitations Dual-energy X-ray absorptiometry is commonly used to estimate muscle mass but does not directly measure muscle mass. Rather, it estimates the total amount of lean tissue. Appendicular lean mass (ALM), derived from DXA scans, is the sum of the lean tissue in the arms and legs. ALM alone, scaled to height2 (ALM/ht2) or to BMI (ALM/BMI), is the most common metric used as an approximation of muscle mass in sarcopenia research and consensus definitions. Physical performance is generally measured in sarcopenia research. Lower extremity strength may be a more relevant measure than grip strength in the context of mobility outcomes, but lower extremity strength is more difficult to measure in clinical and research settings than grip strength. The most widely used measure of physical performance is walking speed over a short distance, usually 3e6 m.
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5 2. Newman AB, Kupelian V, Visser M, et al. 2003 Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 51(11):1602e1609. 3. Fielding RA, Vellas B, Evans WJ, et al. 2011 Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. J Am Med Dir Assoc 12(4): 249e256. 4. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. 2010 Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39(4):412e423. 5. Studenski SA, Peters KW, Alley DE, et al. 2014 The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol Ser A Biol Sci Med Sci 69(5):547e558. 6. Visser M, Goodpaster BH, Kritchevsky SB, et al. 2005 Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol Ser A Biol Sci Med Sci 60(3): 324e333. 7. Rantanen T, Guralnik JM, Foley D, et al. 1999 Midlife hand grip strength as a predictor of old age disability. JAMA 281(6): 558e560. 8. Studenski S, Perera S, Patel K, et al. 2011 Gait speed and survival in older adults. JAMA : J Am Med Assoc 305(1): 50e58. 9. Cummings SR, Studenski S, Ferrucci L. 2014 A diagnosis of dismobilitydgiving mobility clinical visibility: a Mobility Working Group recommendation. JAMA 311(20): 2061e2062. 10. Guralnik JM, Ferrucci L, Simonsick EM, et al. 1995 Lowerextremity function in persons over the age of 70 years as a predictor of subsequent disability [see comments]. N Engl J Med 332:556e561. 11. Newman AB, Simonsick EM, Naydeck BL, et al. 2006 Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability. JAMA 295(17):2018e2026. 12. ATS statement: guidelines for the six-minute walk test. 2002 Am J Respir Crit Care Med 166(1):111e117.
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