Since the sentinel article by Baumgartner et al. in 1998, there has been an increased interest in the importance of muscle mass loss (sarcopenia) as a cause of multiple health-related problems in older persons. Loss of skeletal muscle is associated with weakness, falls, fractures, fear of falling, fatigue, depression, cognitive impairment, frailty, disability, and death . Despite this observation there has been increasing recognition that muscle mass is weakly related to muscle strength and function [3,4]. This has led to a shift in recent sarcopenia definitions with a greater emphasis on muscle strength and muscle function rather than on muscle mass [5–11]. Recently the GLIM (Global Leadership Initiative on Malnutrition) criteria included reduced muscle mass as a phenotypic criterion for the diagnosis of malnutrition, a condition with the highest prevalence rates in older patients . These two examples may illustrate the growing interest in body composition measurements in the older population.
Numerous methods for the assessment of muscle mass have been developed. Calf circumference was the original surrogate marker for calf muscle and it was reasonably correlated with calf muscle mass as measured by magnetic resonance imaging . Calf circumference corrected for sex, age, and ethnicity was also highly correlated with Dual-energy X-ray absorptiometry (DEXA) measurements of appendicular skeletal mass . The SARC-F is a highly specific rapid screen for sarcopenia  whose sensitivity is greatly improved by adding calf circumference .
Bioelectrical impedance analysis (BIA) is used to estimate muscle mass on the basis of the measurement of tissue conductivity and algorithms that are developed with the help of a reference method. BIA is therefore considered as a doubly indirect method. A recent overview concluded that there is still a lack of standardization of BIA for the assessment of muscle mass which may have contributed to the wide range of prevalence rates in different studies . BIA may overestimate muscle mass by approximately 2 kg . Both fluid overload and dehydration alter the accuracy of the measurements. Recently measuring phase angle has become popular but it is dependent on age, sex, BMI, and fat mass. The agreement between computed tomography and BIA does not show precise agreement  and it showed poor correlations with sarcopenia in active older women .
Dual-energy X-ray absorptiometry (DXA) has been considered the gold standard for measuring muscle mass . It has been validated against post mortem measurement of muscle, skin, and viscera, but it can be inaccurate on the basis of hydration status and thickness of lean tissue . In addition, different DEXA machines can lead to different results. It measures lean mass rather than muscle mass.
Both computed tomography and magnetic resonance imaging represent trusted methods to measure muscle mass, but their cost makes their use prohibitive for regular clinical use .
Ultrasound is a portable relatively simple method to measure quadriceps mass [23–25]. It is somewhat dependent on operator skill and among other details related to the applied probe pressure. It can also provide the angle of pennation which provides information on the ability of the muscle to generate force. At present, it has been underused to measure muscle mass. But with the increasing availability of affordable but reliable ultrasound devices, it may become a valuable tool in the clinic and in physician offices as well, especially if international standardization of its application will be achieved in the near future.
Most recently, it has been suggested that D3-creatine dilution may be the most accurate measure of muscle mass . More than 95% of body creatine is present in muscle. Creatine is converted to creatinine and is not synthesized in muscle. For this reason, orally ingested creatine which is labeled by deuterium will lead to excretion of D3-creatinine in the urine providing an estimate of muscle mass. In a preliminary study, Clark et al. found that orally administered D3-creatine produced a steady state of D3-creatinine in the urine after 30 h allowing an estimate of muscle mass . This estimate correlated with magnet resonance imaging (MRI) measurements of muscle mass and was more accurate than DXA measurements. In a second study, muscle mass measured by the D3-creatine dilution technique correlated with bioelectrical impedance . The D3-creatine dilution method for muscle mass was related to fall injuries, slow gait speed, SPPB, and mobility limitation . In a recent study, the D3-creatine dilution method was superior to DEXA with regard to the detection of age-associated changes of muscle mass over a follow-up interval of 1.6 years . In addition, the D3-creatine results correlated with the observed change of handgrip strength and walking speed.
This editorial has briefly reviewed the methods available to measure muscle and lean body mass. The advantages and disadvantages of each technique are outlined in Table 1. It would appear that in the future the D3-creatine dilution technique may become the best method to measure metabolically active muscle. However, at the moment additional studies are warranted that would allow to draw this conclusion on a sound basis.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
1. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998; 147:755–763. 15.
2. McKee A, Morley JE, Matsumoto AM, Vinik A. Sarcopenia: an endocrine disorder? Endocr Pract 2017; 23:1140–1149.
3. Clark BC, Manini TM. Sarcopenia =/= dynapenia. J Gerontol A Biol Sci Med Sci 2008; 63:829–834.
4. Chiles Shaffer N, Fabbri E, Ferrucci L, et al. Muscle quality, strength, and lower extremity physical performance in the Baltimore Longitudinal Study of Aging. J Frailty Aging 2017; 6:183–187.
5. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010; 39:412–423.
6. Chen LK, Liu LK, Woo J, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 2014; 15:95–101.
7. Fielding RA, Vellas B, Evans WJ, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: Prevalence, etiology, ad consequences. International working group on sarcopenia. J Am Med Dir Assoc 2011; 12:249–256.
8. Studenski SA, Peters KW, Alley DE, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 2014; 69:547–558.
9. Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16–31.
10. Dent E, Morley JE, Cruz-Jentoft AJ, et al. International Clinical Practice guidelines for sarcopenia (ICFSR): screening, diagnosis and management. J Nutr Health Aging 2018; 22:1148–1161.
11. Bauer J, Morley JE, Schols AM, et al. Sarcopenia: a time for action: an SCWD position paper. J Cachexia Sarcopenia Muscle 2019; 10:956–961.
12. Cederholm T, Jensen GL, Correia MI, et al. GLIM criteria for the diagnosis of malnutrition: a consensus report from the global clinical nutrition community. Clin Nutr 2019; 38:1–9.
13. Asai C, Akao K, Adachi T, et al. Maximal calf circumference reflects calf muscle mass measured using magnetic resonance imaging. Arch Gerontol Geriatr 2019; 83:175–178.
14. Santos LP, Gonzalez MC, Orlandi SP, et al. New prediction equations to estimate appendicular skeletal muscle mass using calf circumference: Results From NHANES 1999-2006. JPEN J Parenter Enteral Nutr. 2019. doi: 10.1002/jpen.1605.
15. Tanaka S, Kamiya K, Hamazaki N, et al. Utility of SARC-F for assessing physical function in elderly patients with cardiovascular disease. J Am Med Dir Assoc 2017; 18:176–181.
16. Yang M, Hu X, Xie L, et al. Screening sarcopenia in community-dwelling older adults: SARC-F vs SARC-F Combines with Calf Circumference (SARC-CalF). J Am Med Dir Assoc 2018; 19:277.e1–277.e8.
17. Gonzalez MC, Barbosa-Silva TG, Heymsfield SB. Bioelectrical impedance analysis in the assessment of sarcopenia. Curr Opin Clin Nutr Metab Care 2018; 21:366–374.
18. Lee SY, Ahn S, Kim YJ, et al. Comparison between dual-energy x-ray absorptiometry and bioelectrical impedance analyses for accuracy in measuring whole body muscle mass and appendicular skeletal muscle mass. Nutrients 2018; 10:
19. Looijaard WG, Stapel SN, Dekker IM, et al. Identifying critically ill patients with low muscle mass: agreement between bioelectrical impedance analysis and computed tomography. Clin Nutr 2019; DOI: 10.1016/j.clnu.2019.07.020 [Epub ahead of print].
20. Pessoa DF, de Branco FM, Dos Reis AS, et al. Association of phase angle with sarcopenia and its components in physically active older women. Aging Clin Exp Res 2019; DOI: 10. 1007/s40520-019-01325-0 [Epub ahead of print].
21. Scafoglieeeri A, Clarys JP. Dual energy x-ray absorptiometry: gold standard for muscle mass? J Cachexia Sarcopenia Muscle 2018; 9:786–787.
22. Heymsfield SB, Gonzalez MC, Lu J, et al. Conference on ‘nutrition and age-related muscle loss, sarcopenia and cachexia.’ Symposium 1: sarcopenia and cachexia: scale of the problem, importance, epidemiology and measurement: skeletal muscle mass and quality: evolution of modern measurement concepts in the context of sarcopenia. Proc Nutr Soc 2015; 74:355–366.
23. Ticinesi A, Meschi T, Narici MV, et al. Muscle ultrasound and sarcopenia in older individuals: a clinical perspective. J Am Med Dir Assoc 2017; 18:290–300.
24. Zhu S, Lin W, Chen S, et al. The correlation of muscle thickness and pennation angle assessed by ultrasound with sarcopenia in elderly Chinese community dwellers. Clin Interv Aging 2019; 28:987–996.
25. Chiaramonte R, Bonfiglio M, Castorina EG, Antoci SA. The primacy of ultrasound in the assessment of muscle architecture: precision, accuracy, reliability of ultrasonography: physiatrist, radiologist, general internist, and family practitioner's experiences. Rev Assoc Med Bras (1992) 2019; 65:165–170.
26. Evans WJ, Hellerstein M, Orwoll E, et al. D3
-creatine dilution and the importance of accuracy in the assessment of skeletal muscle mass. J Cachexia Sarcopenia Muscle 2019; 10:14–21.
27. Clark RV, Walker AC, O’Connor-Semmes RL, et al. Total body skeletal muscle mass; estimation by creatine (methyl-D3
) dilution in humans. J Appl Physiol (1985) 2014; 116:1605–1613.
28. Shankaran M, Czerwieniec G, Fessler C, et al. Dilution of oral D3
-creatine to measure creatine pool size and estimate skeletal muscle mass: development of a correction algorithm. J Cachexia Sarcopenia Muscle 2018; 9:540–546.
29. Cawthon PM, Orwoll ES, Peters KE, et al. Strong relation between muscle mass determined by D3
-creatine dilution, physical performance, and incidence of falls and mobility limitations in a prospective cohort of older men. J Gerontol A Biol Sci Med Sci 2019; 74:844–852.
30. Duchowny KA, Peters KE, Cummings SR, et al. Association of change in muscle mass assessed by D(3)-creatine dilution with changes in grip strength and walking speed. J Cachexia Sarcopenia Muscle 2019.