Assessing skeletal muscle mass: Historical overview and state of the art

Journal of Cachexia, Sarcopenia and Muscle

Volumn 5, Issue 1, 2014, Pages 9-18

  Heymsfield, Steven B ^a   Adamek, Michael ^a   Gonzalez, M Cristina ^b   Jia, Guang ^a,c   Thomas, Diana M ^d  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b CATHOLIC UNIVERSITY OF PELOTAS   (Brazil)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d MONTCLAIR STATE UNIVERSITY   (United States)

Author keywords

Body composition; Cachexia; Nutritional assessment; Sarcopenia

Indexed keywords

CREATINE;

ABSORPTIOMETRY; BODY COMPOSITION; BODY SIZE; CACHEXIA; COMPUTER ASSISTED TOMOGRAPHY; CONNECTIVE TISSUE; DIFFUSION TENSOR IMAGING; ELASTOGRAPHY; HUMAN; MEAT; MUSCLE FUNCTION; MUSCLE MASS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PATIENT MONITORING; PHOTON ABSORPTIOMETRY; PRIORITY JOURNAL; REVIEW; SARCOPENIA; SKELETAL MUSCLE; ULTRASOUND; URINE; WHOLE BODY COUNTING; X RAY;

EID: 84896405128     PISSN: 21905991     EISSN: 21906009     Source Type: Journal    
DOI: 10.1007/s13539-014-0130-5     Document Type: Review

References (101)

1. Evans WJ. Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr. 2010;91: 1123S-7S. doi: 10. 3945/ajcn. 2010. 28608A.
2. Wang ZM, Pierson Jr RN, Heymsfield SB. The five-level model: a new approach to organizing body-composition research. Am J Clin Nutr. 1992;56: 19-28.
3. Chevreul E. Sur la composition chimique du bouillon de viandes (On the chemical composition of meatbroth). J Pharm Sci Access. 1835;21: 231-42.
4. Folin O. Laws governing the chemical composition of urine. Am J Insanity. 1904;60: 709-10.
5. Bürger M. Beiträge zum Kreatininstoffwechsel. Z f d g Exp Med. 1919;9: 361-99. doi: 10. 1007/bf03002912.
6. Hahn A, Meyer G. On the mutual transformation of creatine and creatinine. Z Biol. 1928;78: 111-5.
7. Talbot NB, Broughton F. Measurement of obesity by the creatinine coefficient. Am J Dis Child. 1938;55: 42-50. doi: 10. 1001/archpedi. 1938. 01980070051004.
8. Graystone J. Creatinine excretion during growth, in human growth. Philadelphia: Lea & Febiger; 1968.
9. Graystone JE, Cheek DB. The effects of reduced caloric intake and increased insulin-induced caloric intake on the cell growth of muscle, liver, and cerebrum and on skeletal collagen in the postweanling rat. Pediatr Res. 1969;3: 66-76.
10. Kreisberg R, Bowdoin B, Meador CK. Measurement of muscle mass in humans by isotopic dilution of creatine-14C. J Appl Physiol. 1970;28: 264-7.
11. Picou D, Reeds PJ, Jackson A, Poulter N. The measurement of muscle mass in children using [15N] creatine. Pediatr Res. 1976;10: 184-8. doi: 10. 1203/00006450-197603000-00008.
12. Wang ZM, Sun YG, Heymsfield SB. Urinary creatinine-skeletal muscle mass method: a prediction equation based on computerized axial tomography. Biomed Environ Sci. 1996;9: 185-90.
13. Stimpson SA, Turner SM, Clifton LG, Poole JC, Mohammed HA, Shearer TW, et al. Total-body creatine pool size and skeletal muscle mass determination by creatine-(methyl-D3) dilution in rats. J Appl Physiol. 1985;112: 1940-8. doi: 10. 1152/japplphysiol. 00122. 2012. 2012.
14. Brozek J, Prokopec M. Historical note: early history of the anthropometry of body composition. Am J Hum Biol. 2001;13: 157-8. doi: 10. 1002/1520-6300(200102/03)13: 2<157:: AID-AJHB1023>3. 0. CO;2-L.
15. Matiegka J. The testing of physical efficiency. Am J Phys Anthropol. 1921;4: 223-30. doi: 10. 1002/ajpa. 1330040302.
16. Clarys JP, Martin AD, Drinkwater DT. Gross tissue weights in the human body by cadaver dissection. Hum Biol. 1984;56: 459-73.
17. Lee RC, Wang Z, Heo M, Ross R, Janssen I, Heymsfield SB. Total-body skeletal muscle mass: development and cross-validation of anthropometric prediction models. Am J Clin Nutr. 2000;72: 796-803.
18. Heymsfield SB, Arteaga C, McManus C, Smith J, Moffitt S. Measurement of muscle mass in humans: validity of the 24-h urinary creatinine method. Am J Clin Nutr. 1983;37: 478-94.
19. Heymsfield SB, Wang Z, Baumgartner RN, Ross R. Human body composition: advances in models and methods. Annu Rev Nutr. 1997;17: 527-58. doi: 10. 1146/annurev. nutr. 17. 1. 527.
20. Burkinshaw L, Hill GL, Morgan DB. Assessment of the distribution of protein in the human body by in vivo neutron activation analysis. In International Symposium on Nuclear Activation Techniques in the Life Sciences. IAEA: Vienna; 1978. p. 787-796.
21. Cohn SH, Vartsky D, Yasumura S, Sawitsky A, Zanzi I, Vaswani A, et al. Compartmental body composition based on total-body nitrogen, potassium, and calcium. Am J Physiol. 1980;239: E524-30.
22. Cohn SH, Gartenhaus W, Sawitsky A, Rai K, Zanzi I, Vaswani A, et al. Compartmental body composition of cancer patients by measurement of total body nitrogen, potassium, and water. Metabolism. 1981;30: 222-9.
23. Burkinshaw L. Some aspects of body composition in cancer. Infusionstherapie. 1990;17 Suppl 3: 57-8.
24. Lukaski HC, Mendez J, Buskirk ER, Cohn SH. Relationship between endogenous 3-methylhistidine excretion and body composition. Am J Physiol. 1981;240: E302-7.
25. Chinn KS. Prediction of muscle and remaining tissue protein in man. J Appl Physiol. 1967;23: 713-5.
26. Nitske WR. The life of Wilhelm Conrad Röntgen, discoverer of the X-ray. Tucson: University of Arizona Press; 1971.
27. Stuart HCDP. The growth of bone, muscle, and overlying tissues in children 6 to 10 years of age as revealed by studies of roentgenograms of the leg area. Monogr Soc Res Child Dev. 1942;13: 195.
28. Hounsfield GN. Computerized transverse axial scanning (tomography). 1. Description of system. Br J Radiol. 1973;46: 1016-22.
29. Cormack AM. Nobel award address. Early two-dimensional reconstruction and recent topics stemming from it. Med Phys. 1980;7: 277-82.
30. Heymsfield SB, Noel R, Lynn M, Kutner M. Accuracy of the soft tissue density predicted by CT. J Comput Assist Tomogr. 1979;8: 859.
31. Bulcke JA, Termote JL, Palmers Y, Crolla D. Computed tomography of the human skeletal muscular system. Neuroradiology. 1979;17: 127-36.
32. Haggmark T, Jansson E, Svane B. Cross-sectional area of the thigh muscle in man measured by computed tomography. Scand J Clin Lab Invest. 1978;38: 355-60.
33. Heymsfield SB, Olafson RP, Kutner MH, Nixon DW. A radiographic method of quantifying protein-calorie undernutrition. Am J Clin Nutr. 1979;32: 693-702.
34. Tokunaga K, Matsuzawa Y, Ishikawa K, Tarui S. A novel technique for the determination of body fat by computed tomography. Int J Obes. 1983;7: 437-45.
35. Sjöström S. Chefer och människor. 1. uppl. ed. Solna: SIPU; 1984.
36. Heymsfield SB, Noel R. Radiographic analysis of body composition by computerized axial tomography. Nutr Cancer. 1981;17: 161-72.
37. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes. 1997;46: 1579-85.
38. Rabi II, Millman S, Kusch P, Zacharias JR. The molecular beam resonance method for measuring nuclear magnetic moments. The magnetic moments of Li63, Li73, and F199. Phys Rev. 1939;55: 526-35.
39. Bloch F. The principle of nuclear induction. Science. 1953;118: 425-30. doi: 10. 1126/science. 118. 3068. 425.
40. Purcell. Research in nuclear magnetism in Nobel lectures, physics: 1942-1962. Amsterdam: Elsevier; 1962. p. 232.
41. Lauterbur. Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature. 1973;242: 190-1.
42. Garroway A. Solid state NMR, MRI, and Sir Peter Mansfield: (1) from broad lines to narrow and back again; and (2) a highly tenuous link to landmine detection. MAGMA. 1999;9: 103-8. doi: 10. 1007/bf02594604.
43. Damadian R. Tumor detection by nuclear magnetic resonance. Science. 1971;171: 1151-3.
44. Foster MA, Hutchison JM, Mallard JR, Fuller M. Nuclear magnetic resonance pulse sequence and discrimination of high- and low-fat tissues. Magn Reson Imaging. 1984;2: 187-92.
45. Ross R, Leger L, Guardo R, De Guise J, Pike BG. Adipose tissue volume measured by magnetic resonance imaging and computerized tomography in rats. J Appl Physiol. 1985;70: 2164-72. 1991.
46. Ross R, Rissanen J, Pedwell H, Clifford J, Shragge P. Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. J Appl Physiol. 1985;81: 2445-55. 1996.
47. Ross R, Pedwell H, Rissanen J. Effects of energy restriction and exercise on skeletal muscle and adipose tissue in women as measured by magnetic resonance imaging. Am J Clin Nutr. 1995;61: 1179-85.
48. Selberg O, Burchert W, Graubner G, Wenner C, Ehrenheim C, Muller MJ. Determination of anatomical skeletal muscle mass by whole body nuclear magnetic resonance. Basic Life Sci. 1993;60: 95-7.
49. Wüthrich K, Wider G, Wagner G, Braun W. Sequential resonance assignments as a basis for determination of spatial protein structures by high resolution proton nuclear magnetic resonance. J Mol Biol. 1982;155: 311-319.
50. Kumar A, Ernst R, Wuthrich K. A two-dimensional nuclear overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun. 1980;95: 1-6. doi: 10. 1016/0006-291x(80)90695-6.
51. Cameron JR, Sorenson J. Measurement of bone mineral in vivo: an improved method. Science. 1963;142: 230-2.
52. Mazess RB, Cameron JR, Sorenson JA. Determining body composition by radiation absorption spectrometry. Nature. 1970;228: 771-2.
53. Pietrobelli A, Formica C, Wang Z, Heymsfield SB. Dual-energy X-ray absorptiometry body composition model: review of physical concepts. Am J Physiol. 1996;271: E941-51.
54. Heymsfield SB. Anthropometric measurements: application in hospitalized patients. Infusionstherapie. 1990;17 Suppl 3: 48-51.
55. Fuller NJ, Laskey MA, Elia M. Assessment of the composition of major body regions by dual-energy X-ray absorptiometry (DEXA), with special reference to limb muscle mass. Clin Physiol. 1992;12: 253-66.
56. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D. Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr. 2002;76: 378-83.
57. Quetelet A. Sur l'homme et le développement de ses facultés, essai d'une physique sociale. Paris: Bachelie;1835.
58. VanItallie TB, Yang MU, Heymsfield SB, Funk RC, Boileau RA. Height-normalized indices of the body's fat-free mass and fat mass: potentially useful indicators of nutritional status. Am J Clin Nutr. 1990;52: 953-9.
59. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147: 755-63.
60. Heymsfield SB, Gallagher D, Mayer L, Beetsch J, Pietrobelli A. Scaling of human body composition to stature: new insights into body mass index. Am J Clin Nutr. 2007;86: 82-91.
61. Heymsfield SB, Heo M, Thomas D, Pietrobelli A. Scaling of body composition to height: relevance to height-normalized indexes. Am J Clin Nutr. 2011;93: 736-40. doi: 10. 3945/ajcn. 110. 007161.
62. Webster JD, Hesp R, Garrow JS. The composition of excess weight in obese women estimated by body density, total body water, and total body potassium. Hum Nutr Clin Nutr. 1984;38: 299-306.
63. Forbes GB. Human body composition: growth, aging, nutrition, and activity. New York: Springer-Verlag; 1987. p. 28-49.
64. Nyboer J. Workable volume and flow concepts of bio-segments by electrical impedance plethysmography. TIT J Life Sci. 1972;2: 1-13.
65. Thomasset A. Bioelectrical properties of tissue impedance measurements. Lyon Med. 1962;208: 107-18.
66. Hoffer EC, Meador CK, Simpson DC. Correlation of whole-body impedance with total body water volume. J Appl Physiol. 1969;27: 531-4.
67. Organ LW, Bradham GB, Gore DT, Lozier SL. Segmental bioelectrical impedance analysis: theory and application of a new technique. J Appl Physiol. 1985;77: 98-112. 1994.
68. Tan YX, Nunez C, Sun Y, Zhang K, Wang Z, Heymsfield SB. New electrode system for rapid whole-body and segmental bioimpedance assessment. Med Sci Sports Exerc. 1997;29: 1269-73.
69. Paiva SI, Borges LR, Halpern-Silveira D, Assuncao MC, Barros AJ, Gonzalez MC. Standardized phase angle from bioelectrical impedance analysis as prognostic factor for survival in patients with cancer. Support Care Cancer. 2010;19: 187-92. doi: 10. 1007/s00520-009-0798-9.
70. Dussik KT. The ultrasonic field as a medical tool. Am J Phys Med. 1954;33: 5-20.
71. Ludwig GD, Bolt RH, Heuter TF, Ballantine Jr HT. Factors influencing the use of ultrasound as a diagnostic aid. Trans Am Neurol Assoc. 1950;51: 225-8.
72. Bullen BA, Quaade F, Olessen E, Lund SA. Ultrasonic reflections used for measuring subcutaneous fat in humans. Hum Biol. 1965;37: 375-84.
73. Booth RA, Goddard BA, Paton A. Measurement of fat thickness in man: a comparison of ultrasound, Harpenden calipers and electrical conductivity. Br J Nutr. 1966;20: 719-25.
74. Ikai M, Fukunaga T. Calculation of muscle strength per unit cross-sectional area of human muscle by means of ultrasonic measurement. Int Z Angew Physiol. 1968;26: 26-32.
75. Sarvazyan AP, Urban MW, Greenleaf JF. Acoustic waves in medical imaging and diagnostics. Ultrasound Med Biol. 2013;39: 1133-46. doi: 10. 1016/j. ultrasmedbio. 2013. 02. 006.
76. Heymsfield SB, Stevens V, Noel R, McManus C, Smith J, Nixon D. Biochemical composition of muscle in normal and semistarved human subjects: relevance to anthropometric measurements. Am J Clin Nutr. 1982;36: 131-42.
77. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;246: 623-7. doi: 10. 1097/BOR. 0b013e328358d59b.
78. Gallagher D, Kuznia P, Heshka S, Albu J, Heymsfield SB, Goodpaster B, et al. Adipose tissue in muscle: a novel depot similar in size to visceral adipose tissue. Am J Clin Nutr. 2005;81: 903-10.
79. Bley TA, Wieben O, Francois CJ, Brittain JH, Reeder SB. Fat and water magnetic resonance imaging. J Magn Reson Imaging. 2010;31: 4-18. doi: 10. 1002/jmri. 21895.
80. Dixon WT. Simple proton spectroscopic imaging. Radiology. 1984;153: 189-94. doi: 10. 1148/radiology. 153. 1. 6089263.
81. Sions JM, Tyrell CM, Knarr BA, Jancosko A, Binder-Macleod SA. Age- and stroke-related skeletal muscle changes: a review for the geriatric clinician. J Geriatr Phys Ther. 2012;35: 155-61. doi: 10. 1519/JPT. 0b013e318236db92.
82. Yamada Y, Schoeller DA, Nakamura E, Morimoto T, Kimura M, Oda S. Extracellular water may mask actual muscle atrophy during aging. J Gerontol A Biol Sci Med Sci. 2010;65: 510-6. doi: 10. 1093/gerona/glq001.
83. Young IR, Bydder GM. Magnetic resonance: new approaches to imaging of the musculoskeletal system. Physiol Meas. 2003;24: R1-R23.
84. Fontana M, White SK, Banypersad SM, Sado DM, Maestrini V, Flett AS, et al. Comparison of T1 mapping techniques for ECV quantification. Histological validation and reproducibility of ShMOLLI versus multibreath-hold T1 quantification equilibrium contrast CMR. J Cardiovasc Magn Reson. 2012;14: 88. doi: 10. 1186/1532-429X-14-88.
85. Miller CA, Naish JH, Bishop P, Coutts G, Clark D, Zhao S, et al. Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circ Cardiovasc Imaging. 2013;6: 373-83. doi: 10. 1161/CIRCIMAGING. 112. 000192.
86. Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, et al. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99: 932-7. doi: 10. 1136/heartjnl-2012-303052.
87. Mariappan YK, Glaser KJ, Ehman RL. Magnetic resonance elastography: a review. Clin Anat. 2010;23: 497-511. doi: 10. 1002/ca. 21006.
88. Glaser KJ, Manduca A, Ehman RL. Review of MR elastography applications and recent developments. J Magn Reson Imaging. 2012;36: 757-74. doi: 10. 1002/jmri. 23597.
89. Dresner MA, Rose GH, Rossman PJ, Muthupillai R, Manduca A, Ehman RL. Magnetic resonance elastography of skeletal muscle. J Magn Reson Imaging. 2001;13: 269-76.
90. Ringleb SI, Bensamoun SF, Chen Q, Manduca A, An KN, Ehman RL. Applications of magnetic resonance elastography to healthy and pathologic skeletal muscle. J Magn Reson Imaging. 2007;25: 301-9. doi: 10. 1002/jmri. 20817.
91. Basford JR, Jenkyn TR, An KN, Ehman RL, Heers G, Kaufman KR. Evaluation of healthy and diseased muscle with magnetic resonance elastography. Arch Phys Med Rehabil. 2002;83: 1530-6.
92. Du J, Carl M, Bydder M, Takahashi A, Chung CB, Bydder GM. Qualitative and quantitative ultrashort echo time (UTE) imaging of cortical bone. J Magn Reson. 2010;207: 304-11. doi: 10. 1016/j. jmr. 2010. 09. 013.
93. Du J, Hamilton G, Takahashi A, Bydder M, Chung CB. Ultrashort echo time spectroscopic imaging (UTESI) of cortical bone. Magn Reson Med. 2007;58: 1001-9. doi: 10. 1002/mrm. 21397.
94. Barker AR, Armstrong N. Insights into developmental muscle metabolism through the use of 31P-magnetic resonance spectroscopy: a review. Pediatr Exerc Sci. 2010;22: 350-68.
95. Lanza IR, Nair KS. Mitochondrial metabolic function assessed in vivo and in vitro. Curr Opin Clin Nutr Metab Care. 2010;13: 511-7. doi: 10. 1097/MCO. 0b013e32833cc93d.
96. Chang G, Wang L, Cardenas-Blanco A, Schweitzer ME, Recht MP, Regatte RR. Biochemical and physiological MR imaging of skeletal muscle at 7 T and above. Semin Musculoskelet Radiol. 2010;14: 269-78. doi: 10. 1055/s-0030-1253167.
97. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR Imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiol. 1986;161: 401-407.
98. Longwei X. Clinical application of diffusion tensor magnetic resonance imaging in skeletal muscle. Muscles Ligaments Tendons J. 2012;2: 19-24.
99. Scheel M, von Roth P, Winkler T, Arampatzis A, Prokscha T, Hamm B, et al. Fiber type characterization in skeletal muscle by diffusion tensor imaging. NMR Biomed. 2013;26: 1220-4. doi: 10. 1002/nbm. 2938.
100. Kogan F, Haris M, Singh A, Cai K, Debrosse C, Nanga RP, et al. Method for high-resolution imaging of creatine in vivo using chemical exchange saturation transfer. Magn Reson Med. 2014;71: 164-72. doi: 10. 1002/mrm. 24641.
101. Haris M, Nanga RP, Singh A, Cai K, Kogan F, Hariharan H, et al. Exchange rates of creatine kinase metabolites: feasibility of imaging creatine by chemical exchange saturation transfer MRI. NMR Biomed. 2012;25: 1305-9. doi: 10. 1002/nbm. 2792.