Korean J Radiol.  2019 Feb;20(2):205-217. 10.3348/kjr.2018.0479.

Recent Issues on Body Composition Imaging for Sarcopenia Evaluation

Affiliations
  • 1Department of Radiology, Asan Image Metrics, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
  • 2Department of Radiology, Ajou University School of Medicine & Graduate School of Medicine, Ajou University Medical Center, Suwon, Korea. jimihuh.rad@gmail.com
  • 3Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
  • 4Department of Radiology, Wonkwang University College of Medicine, Wonkwang University Hospital, Iksan, Korea.

Abstract

Recently, sarcopenia has garnered renewed interest. Sarcopenia is a disease characterized by decreased skeletal muscle mass and strength/function, which can impair the quality of life and increase physical disability, adverse metabolic effects, and mortality. Imaging tools for evaluating and diagnosing sarcopenia have developed rapidly. Radiologists should be aware of sarcopenia and its clinical implications. We review current knowledge about sarcopenia, its pathophysiological impact, and advantages and disadvantages of methods for evaluation of sarcopenia focusing on body composition imaging modalities such as whole-body dual-energy X-ray absorptiometry, CT, and MRI. Controversial issues are discussed, including the lack of consensus and standardization of the disease definition, imaging modality, measurement methods, and diagnostic cutoff points.

Keyword

Body composition; Computed tomography; Magnetic resonance imaging; Dual-energy X-ray absorptiometry; Sarcopenia

MeSH Terms

Absorptiometry, Photon
Body Composition*
Consensus
Magnetic Resonance Imaging
Mortality
Muscle, Skeletal
Quality of Life
Sarcopenia*

Figure

  • Fig. 1 Muscle as secretory organ.Various myokines released through muscle contraction affecting anatomically distant organs, which could explain association between sedentary behavior and many chronic diseases. ANGPTL4 = angiopoietin-like 4, BAIBA = β-aminoisobutyric acid, BDNF = brain-derived neurotrophic factor, CSTB = cathepsin B, FAM5C = family with sequence similarity 5, FGF2 = fibroblast growth factor 2, FGF21 = fibroblast growth factor 21, FSTL1 = follistatin-related protein 1, IGF1 = insulin-like growth factor 1, SPARC = secreted protein acidic and rich in cysteine, IL-6 = interleukin-6, IL-7 = interleukin-7, IL-10 = interleukin-10, IL-15 = interleukin-15

  • Fig. 2 Sarcopenia cascade.Various cause of sarcopenia entering vicious cycle, resulting in physical disability, falling, fracture, hospitalization, depression, poor quality of life, increased health care costs, adverse metabolic effects, and notably increased mortality.

  • Fig. 3 Dual-energy x-ray absorptiometry results for body composition in healthy 47-year-old male.ASM is sum of lean muscle mass of both arms and legs. ASM is adjusted using height squared (ASM/ht2), weight (ASM/wt), or BMI (ASM/BMI). ASM = appendicular skeletal muscle, BMC = bone mineral content, BMI = body-mass index

  • Fig. 4 Body composition evaluation CT image with artificial intelligence segmentation technique.In clinically acquired axial CT images at L3 vertebral body level TAMA, visceral fat area, subcutaneous fat area are segmented in 43-year-old male (A), and 55-year-old obese male (B). TAMA = total abdominal muscle area

  • Fig. 5 Sarcopenia evaluation with MRI.In clinically acquired whole-body MRI of 55-year-old male patient (A), TAMA is segmented at L3 vertebral body level (B) and thigh muscle area is segmented at mid-thigh level (C).

  • Fig. 6 US images of thigh muscle.In clinically acquired axial view US image of 30-year-old female patient (A), and sagittal panoramic view (B) provides both qualitative and quantitative information of thigh muscle. US = ultrasonography


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Reference

1. Beaudart C, Zaaria M, Pasleau F, Reginster JY, Bruyère O. Health outcomes of sarcopenia: a systematic review and meta-analysis. PLoS One. 2017; 12:e0169548. PMID: 28095426.
Article
2. Bazzocchi A, Diano D, Ponti F, Salizzoni E, Albisinni U, Marchesini G, et al. A 360-degree overview of body composition in healthy people: relationships among anthropometry, ultrasonography, and dual-energy x-ray absorptiometry. Nutrition. 2014; 30:696–701. PMID: 24800668.
Article
3. Boutin RD, Yao L, Canter RJ, Lenchik L. Sarcopenia: current concepts and imaging implications. AJR Am J Roentgenol. 2015; 205:W255–W266. PMID: 26102307.
Article
4. Santilli V, Bernetti A, Mangone M, Paoloni M. Clinical definition of sarcopenia. Clin Cases Miner Bone Metab. 2014; 11:177–180. PMID: 25568649.
Article
5. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, 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. PMID: 20392703.
Article
6. Xue QL. The frailty syndrome: definition and natural history. Clin Geriatr Med. 2011; 27:1–15. PMID: 21093718.
Article
7. Chen X, Mao G, Leng SX. Frailty syndrome: an overview. Clin Interv Aging. 2014; 9:433–441. PMID: 24672230.
8. Cederholm T. Overlaps between Frailty and sarcopenia definitions. Nestle Nutr Inst Workshop Ser. 2015; 83:65–69. PMID: 26484770.
Article
9. Anandavadivelan P, Lagergren P. Cachexia in patients with oesophageal cancer. Nat Rev Clin Oncol. 2016; 13:185–198. PMID: 26573424.
Article
10. Cruz-Jentoft AJ, Landi F, Schneider SM, Zúñiga C, Arai H, Boirie Y, et al. Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing. 2014; 43:748–759. PMID: 25241753.
Article
11. Wang C, Bai L. Sarcopenia in the elderly: basic and clinical issues. Geriatr Gerontol Int. 2012; 12:388–396. PMID: 22530761.
Article
12. Kaji H. Effects of myokines on bone. Bonekey Rep. 2016; 5:826. PMID: 27579164.
Article
13. Laske C, Stransky E, Leyhe T, Eschweiler GW, Wittorf A, Richartz E, et al. Stage-dependent BDNF serum concentrations in Alzheimer's disease. J Neural Transm (Vienna). 2006; 113:1217–1224. PMID: 16362629.
Article
14. Pratesi A, Tarantini F, Di Bari M. Skeletal muscle: an endocrine organ. Clin Cases Miner Bone Metab. 2013; 10:11–14. PMID: 23858303.
Article
15. Kim KM, Jang HC, Lim S. Differences among skeletal muscle mass indices derived from height-, weight-, and body mass index-adjusted models in assessing sarcopenia. Korean J Intern Med. 2016; 31:643–650. PMID: 27334763.
Article
16. Chin SO, Rhee SY, Chon S, Hwang YC, Jeong IK, Oh S, et al. Sarcopenia is independently associated with cardiovascular disease in older Korean adults: the Korea National Health and Nutrition Examination Survey (KNHANES) from 2009. PLoS One. 2013; 8:e60119. PMID: 23533671.
Article
17. Sanada K, Miyachi M, Tanimoto M, Yamamoto K, Murakami H, Okumura S, et al. A cross-sectional study of sarcopenia in Japanese men and women: reference values and association with cardiovascular risk factors. Eur J Appl Physiol. 2010; 110:57–65. PMID: 20390291.
Article
18. Levolger S, van Vugt JL, de Bruin RW, IJzermans JN. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015; 102:1448–1458. PMID: 26375617.
Article
19. Oakland K, Nadler R, Cresswell L, Jackson D, Coughlin PA. Systematic review and meta-analysis of the association between frailty and outcome in surgical patients. Ann R Coll Surg Engl. 2016; 98:80–85. PMID: 26741674.
Article
20. Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, Harbaugh C, et al. Sarcopenia and mortality after liver transplantation. J Am Coll Surg. 2010; 211:271–278. PMID: 20670867.
Article
21. Ganapathi AM, Englum BR, Hanna JM, Schechter MA, Gaca JG, Hurwitz LM, et al. Frailty and risk in proximal aortic surgery. J Thorac Cardiovasc Surg. 2014; 147:186–191.e1. PMID: 24183336.
Article
22. Lee JS, He K, Harbaugh CM, Schaubel DE, Sonnenday CJ, Wang SC, et al. Michigan Analytic Morphomics Group (MAMG). Frailty, core muscle size, and mortality in patients undergoing open abdominal aortic aneurysm repair. J Vasc Surg. 2011; 53:912–917. PMID: 21215580.
Article
23. Peng P, Hyder O, Firoozmand A, Kneuertz P, Schulick RD, Huang D, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012; 16:1478–1486. PMID: 22692586.
Article
24. de Hoogt PA, Reisinger KW, Tegels JJW, Bosmans JWAM, Tijssen F, Stoot JHMB. Functional Compromise Cohort Study (FCCS): sarcopenia is a strong predictor of mortality in the intensive care unit. World J Surg. 2018; 42:1733–1741. PMID: 29285609.
Article
25. Du Y, Karvellas CJ, Baracos V, Williams DC, Khadaroo RG. Acute Care and Emergency Surgery (ACES) Group. Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery. Surgery. 2014; 156:521–527. PMID: 24929435.
Article
26. Miljkovic I, Zmuda JM. Epidemiology of myosteatosis. Curr Opin Clin Nutr Metab Care. 2010; 13:260–264. PMID: 20179586.
Article
27. Reinders I, Murphy RA, Koster A, Brouwer IA, Visser M, Garcia ME, et al. Muscle quality and muscle fat infiltration in relation to incident mobility disability and gait speed decline: the age, gene/environment susceptibility-Reykjavik Study. J Gerontol A Biol Sci Med Sci. 2015; 70:1030–1036. PMID: 25748031.
Article
28. Buford TW, Lott DJ, Marzetti E, Wohlgemuth SE, Vandenborne K, Pahor M, et al. Age-related differences in lower extremity tissue compartments and associations with physical function in older adults. Exp Gerontol. 2012; 47:38–44. PMID: 22015325.
Article
29. Lorbergs AL, Noseworthy MD, Adachi JD, Stratford PW, MacIntyre NJ. Fat infiltration in the leg is associated with bone geometry and physical function in healthy older women. Calcif Tissue Int. 2015; 97:353–363. PMID: 26071112.
Article
30. Hamrick MW, McGee-Lawrence ME, Frechette DM. Fatty infiltration of skeletal muscle: mechanisms and comparisons with bone marrow adiposity. Front Endocrinol (Lausanne). 2016; 7:69. PMID: 27379021.
Article
31. Montano-Loza AJ, Angulo P, Meza-Junco J, Prado CM, Sawyer MB, Beaumont C, et al. Sarcopenic obesity and myosteatosis are associated with higher mortality in patients with cirrhosis. J Cachexia Sarcopenia Muscle. 2016; 7:126–135. PMID: 27493866.
Article
32. Rollins KE, Tewari N, Ackner A, Awwad A, Madhusudan S, Macdonald IA, et al. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin Nutr. 2016; 35:1103–1109. PMID: 26411749.
Article
33. Reinders I, Murphy RA, Brouwer IA, Visser M, Launer L, Siggeirsdottir K, et al. Muscle quality and myosteatosis: novel associations with mortality risk: the age, gene/environment susceptibility (AGES)-Reykjavik Study. Am J Epidemiol. 2016; 183:53–60. PMID: 26643983.
34. Shepherd J. Evaluation of sarcopenia by DXA. Clin Rev Bone Miner Metab. 2016; 14:45–49.
Article
35. Morrell GR, Ikizler TA, Chen X, Heilbrun ME, Wei G, Boucher R, et al. Psoas muscle cross-sectional area as a measure of whole-body lean muscle mass in maintenance hemodialysis patients. J Ren Nutr. 2016; 26:258–264. PMID: 26994780.
36. Noumura Y, Kamishima T, Sutherland K, Nishimura H. Visceral adipose tissue area measurement at a single level: can it represent visceral adipose tissue volume? Br J Radiol. 2017; 90:20170253. PMID: 28707539.
Article
37. Guerri S, Mercatelli D, Aparisi Gómez MP, Napoli A, Battista G, Guglielmi G, et al. Quantitative imaging techniques for the assessment of osteoporosis and sarcopenia. Quant Imaging Med Surg. 2018; 8:60–85. PMID: 29541624.
Article
38. 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; 147:755–763. PMID: 9554417.
Article
39. Fuggle N, Shaw S, Dennison E, Cooper C. Sarcopenia. Best Pract Res Clin Rheumatol. 2017; 31:218–242. PMID: 29224698.
Article
40. Kim H, Hirano H, Edahiro A, Ohara Y, Watanabe Y, Kojima N, et al. Sarcopenia: prevalence and associated factors based on different suggested definitions in community-dwelling older adults. Geriatr Gerontol Int. 2016; 16(Suppl 1):110–122. PMID: 27018289.
Article
41. Cawthon PM, Peters KW, Shardell MD, McLean RR, Dam TT, Kenny AM, et al. Cutpoints for low appendicular lean mass that identify older adults with clinically significant weakness. J Gerontol A Biol Sci Med Sci. 2014; 69:567–575. PMID: 24737559.
Article
42. Seabolt LA, Welch EB, Silver HJ. Imaging methods for analyzing body composition in human obesity and cardiometabolic disease. Ann N Y Acad Sci. 2015; 1353:41–59. PMID: 26250623.
Article
43. Sergi G, Trevisan C, Veronese N, Lucato P, Manzato E. Imaging of sarcopenia. Eur J Radiol. 2016; 85:1519–1524. PMID: 27117135.
Article
44. Yoon DY, Moon JH, Kim HK, Choi CS, Chang SK, Yun EJ, et al. Comparison of low-dose CT and MR for measurement of intra-abdominal adipose tissue: a phantom and human study. Acad Radiol. 2008; 15:62–70. PMID: 18078908.
45. Lustgarten MS, Fielding RA. Assessment of analytical methods used to measure changes in body composition in the elderly and recommendations for their use in phase II clinical trials. J Nutr Health Aging. 2011; 15:368–375. PMID: 21528163.
Article
46. Dalakas MC. Inflammatory muscle diseases. N Engl J Med. 2015; 372:1734–1747. PMID: 25923553.
Article
47. Erlandson MC, Lorbergs AL, Mathur S, Cheung AM. Muscle analysis using pQCT, DXA and MRI. Eur J Radiol. 2016; 85:1505–1511. PMID: 27005009.
Article
48. Gloor M, Fasler S, Fischmann A, Haas T, Bieri O, Heinimann K, et al. Quantification of fat infiltration in oculopharyngeal muscular dystrophy: comparison of three MR imaging methods. J Magn Reson Imaging. 2011; 33:203–210. PMID: 21182140.
Article
49. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008; 9:629–635. PMID: 18539529.
Article
50. Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013; 31:1539–1547. PMID: 23530101.
Article
51. Schweitzer L, Geisler C, Pourhassan M, Braun W, Glüer CC, Bosy-Westphal A, et al. What is the best reference site for a single MRI slice to assess whole-body skeletal muscle and adipose tissue volumes in healthy adults? Am J Clin Nutr. 2015; 102:58–65. PMID: 26016860.
52. Yip C, Dinkel C, Mahajan A, Siddique M, Cook GJ, Goh V. Imaging body composition in cancer patients: visceral obesity, sarcopenia and sarcopenic obesity may impact on clinical outcome. Insights Imaging. 2015; 6:489–497. PMID: 26070723.
Article
53. Cheng X, Zhang Y, Wang C, Deng W, Wang L, Duanmu Y, et al. The optimal anatomic site for a single slice to estimate the total volume of visceral adipose tissue by using the quantitative computed tomography (QCT) in Chinese population. Eur J Clin Nutr. 2018; 3. 20. [Epub ahead of print]. DOI: 10.1038/s41430-018-0122-1.
Article
54. Schweitzer L, Geisler C, Pourhassan M, Braun W, Glüer CC, Bosy-Westphal A, et al. Estimation of skeletal muscle mass and visceral adipose tissue volume by a single magnetic resonance imaging slice in healthy elderly adults. J Nutr. 2016; 146:2143–2148. PMID: 27581576.
Article
55. Tosato M, Marzetti E, Cesari M, Savera G, Miller RR, Bernabei R, et al. Measurement of muscle mass in sarcopenia: from imaging to biochemical markers. Aging Clin Exp Res. 2017; 29:19–27. PMID: 28176249.
Article
56. Xu L, Duanmu Y, Blake GM, Zhang C, Zhang Y, Brown K, et al. Validation of goose liver fat measurement by QCT and CSE-MRI with biochemical extraction and pathology as reference. Eur Radiol. 2018; 28:2003–2012. PMID: 29238866.
Article
57. Ticinesi A, Meschi T, Narici MV, Lauretani F, Maggio M. Muscle ultrasound and sarcopenia in older individuals: a clinical perspective. J Am Med Dir Assoc. 2017; 18:290–300. PMID: 28202349.
Article
58. Glüer CC. Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. The International Quantitative Ultrasound Consensus Group. J Bone Miner Res. 1997; 12:1280–1288. PMID: 9258759.
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