Sarcopenia: Beyond Muscle Atrophy and into the New Frontiers of Opportunistic Imaging, Precision Medicine, and Machine Learning

Abstract

As populations continue to age worldwide, the impact of sarcopenia on public health will continue to grow. The clinically relevant and increasingly common diagnosis of sarcopenia is at the confluence of three tectonic shifts in medicine: opportunistic imaging, precision medicine, and machine learning. This review focuses on the state-of-the-art imaging of sarcopenia and provides context for such imaging by discussing the epidemiology, pathophysiology, consequences, and future directions in the field of sarcopenia.

Keywords

sarcopenia - myosteatosis - osteoporosis - computed tomography - dual X-ray absorptiometry

• References

• 1 Cruz-Jentoft AJ, Baeyens JP, Bauer JM. , et al; European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010; 39 (04) 412-423
• 2 Boutin RD, Yao L, Canter RJ, Lenchik L. Sarcopenia: current concepts and imaging implications. AJR Am J Roentgenol 2015; 205 (03) W255-W266
• 3 Marty E, Liu Y, Samuel A, Or O, Lane J. A review of sarcopenia: enhancing awareness of an increasingly prevalent disease. Bone 2017; 105: 276-286
• 4 Ethgen O, Beaudart C, Buckinx F, Bruyère O, Reginster JY. The future prevalence of sarcopenia in Europe: a claim for public health action. Calcif Tissue Int 2017; 100 (03) 229-234
• 5 Pamoukdjian F, Bouillet T, Lévy V, Soussan M, Zelek L, Paillaud E. Prevalence and predictive value of pre-therapeutic sarcopenia in cancer patients: a systematic review. Clin Nutr 2017; S0261-5614(17)30249-2
• 6 Beaudart C, Zaaria M, Pasleau F, Reginster JY, Bruyère O. Health outcomes of sarcopenia: a systematic review and meta-analysis. PLoS One 2017; 12 (01) e0169548
• 7 Rier HN, Jager A, Sleijfer S, Maier AB, Levin MD. The prevalence and prognostic value of low muscle mass in cancer patients: a review of the literature. Oncologist 2016;theoncologist.2016-0066
• 8 Bruyère O, Beudart C, Locquet M. , et al. Sarcopenia as a public health problem. Eur Geriatr Med 2016; 7: 272-275
• 9 Dawson A, Dennison E. Measuring the musculoskeletal aging phenotype. Maturitas 2016; 93: 13-17
• 10 Giardino A, Gupta S, Olson E. , et al. Role of imaging in the era of precision medicine. Acad Radiol 2017; 24 (05) 639-649
• 11 Rosenkrantz AB, Mendiratta-Lala M, Bartholmai BJ. , et al. Clinical utility of quantitative imaging. Acad Radiol 2015; 22 (01) 33-49
• 12 Murray TÉ, Williams D, Lee MJ. Osteoporosis, obesity, and sarcopenia on abdominal CT: a review of epidemiology, diagnostic criteria, and management strategies for the reporting radiologist. Abdom Radiol (NY) 2017; 42 (09) 2376-2786
• 13 Baumgartner RN, Koehler KM, Gallagher D. , et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998; 147 (08) 755-763
• 14 Joglekar S, Nau PN, Mezhir JJ. The impact of sarcopenia on survival and complications in surgical oncology: a review of the current literature. J Surg Oncol 2015; 112 (05) 503-509
• 15 Kaplan SJ, Pham TN, Arbabi S. , et al. Association of radiologic indicators of frailty with 1-year mortality in older trauma patients: opportunistic screening for sarcopenia and osteopenia. JAMA Surg 2017; 152 (02) e164604
• 16 Praktiknjo M, Book M, Luetkens J. , et al. Fat-free muscle mass in magnetic resonance imaging predicts acute-on-chronic liver failure and survival in decompensated cirrhosis. Hepatology 2018; 67 (03) 1014-1026
• 17 Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle 2017; 8 (05) 702-712
• 18 Hsu B, Merom D, Blyth FM. , et al. Total physical activity, exercise intensity, and walking speed as predictors of all-cause and cause-specific mortality over 7 years in older men: the Concord Health and Aging in Men Project. J Am Med Dir Assoc 2018; 19 (03) 216-222
• 19 Fielding RA, Vellas B, Evans WJ. , et al; International Working Group on Sarcopenia. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. J Am Med Dir Assoc 2011; 12 (04) 249-256
• 20 McLean RR, Shardell MD, Alley DE. , et al. Criteria for clinically relevant weakness and low lean mass and their longitudinal association with incident mobility impairment and mortality: the foundation for the National Institutes of Health (FNIH) sarcopenia project. J Gerontol A Biol Sci Med Sci 2014; 69 (05) 576-583
• 21 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 (05) 547-558
• 22 Dam TT, Peters KW, Fragala M. , et al. An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci 2014; 69 (05) 584-590
• 23 Shachar SS, Williams GR, Muss HB, Nishijima TF. Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur J Cancer 2016; 57: 58-67
• 24 Bodine SC, Stitt TN, Gonzalez M. , et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 2001; 3 (11) 1014-1019
• 25 Brioche T, Pagano AF, Py G, Chopard A. Muscle wasting and aging: experimental models, fatty infiltrations, and prevention. Mol Aspects Med 2016; 50: 56-87
• 26 Ali S, Garcia JM. Sarcopenia, cachexia and aging: diagnosis, mechanisms and therapeutic options—a mini-review. Gerontology 2014; 60 (04) 294-305
• 27 Sandri M. Protein breakdown in cancer cachexia. Semin Cell Dev Biol 2016; 54: 11-19
• 28 Johns N, Stephens NA, Fearon KC. Muscle wasting in cancer. Int J Biochem Cell Biol 2013; 45 (10) 2215-2229
• 29 Hirschfeld HP, Kinsella R, Duque G. Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int 2017; 28 (10) 2781-2790
• 30 Kalinkovich A, Livshits G. Sarcopenic obesity or obese sarcopenia: a cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res Rev 2017; 35: 200-221
• 31 Cauley JA. An overview of sarcopenic obesity. J Clin Densitom 2015; 18 (04) 499-505
• 32 Ormsbee MJ, Prado CM, Ilich JZ. , et al. Osteosarcopenic obesity: the role of bone, muscle, and fat on health. J Cachexia Sarcopenia Muscle 2014; 5 (03) 183-192
• 33 Fried LP, Tangen CM, Walston J. , et al; Cardiovascular Health Study Collaborative Research Group. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 2001; 56 (03) M146-M156
• 34 Fearon KC. Cancer cachexia and fat-muscle physiology. N Engl J Med 2011; 365 (06) 565-567
• 35 Evans WJ, Morley JE, Argilés J. , et al. Cachexia: a new definition. Clin Nutr 2008; 27 (06) 793-799
• 36 Binkley N, Krueger D, Buehring B. What's in a name revisited: should osteoporosis and sarcopenia be considered components of “dysmobility syndrome?”. Osteoporos Int 2013; 24 (12) 2955-2959
• 37 Lee WJ, Liu LK, Hwang AC, Peng LN, Lin MH, Chen LK. Dysmobility syndrome and risk of mortality for community-dwelling middle-aged and older adults: the nexus of aging and body composition. Sci Rep 2017; 7 (01) 8785
• 38 Androga L, Sharma D, Amodu A, Abramowitz MK. Sarcopenia, obesity, and mortality in US adults with and without chronic kidney disease. Kidney Int Rep 2017; 2 (02) 201-211
• 39 Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B. Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: a systematic review and meta-analysis. Maturitas 2017; 103: 16-22
• 40 Shaw SC, Dennison EM, Cooper C. Epidemiology of sarcopenia: determinants throughout the lifecourse. Calcif Tissue Int 2017; 101 (03) 229-247
• 41 Batsis JA, Mackenzie TA, Jones JD, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity and inflammation: results from the 1999–2004 National Health and Nutrition Examination Survey. Clin Nutr 2016; 35 (06) 1472-1483
• 42 Batsis JA, Mackenzie TA, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity, and functional impairments in older adults: National Health and Nutrition Examination Surveys 1999–2004. Nutr Res 2015; 35 (12) 1031-1039
• 43 Rizzoli R, Reginster JY, Arnal JF. , et al. Quality of life in sarcopenia and frailty. Calcif Tissue Int 2013; 93 (02) 101-120
• 44 Paknikar R, Friedman J, Cron D. , et al. Psoas muscle size as a frailty measure for open and transcatheter aortic valve replacement. J Thorac Cardiovasc Surg 2016; 151 (03) 745-751
• 45 Leeper CM, Lin E, Hoffman M. , et al. Computed tomography abbreviated assessment of sarcopenia following trauma: the CAAST measurement predicts 6-month mortality in older adult trauma patients. J Trauma Acute Care Surg 2016; 80 (05) 805-811
• 46 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 (02) 80-85
• 47 Moisey LL, Mourtzakis M, Cotton BA. , et al; Nutrition and Rehabilitation Investigators Consortium (NUTRIC). Skeletal muscle predicts ventilator-free days, ICU-free days, and mortality in elderly ICU patients. Crit Care 2013; 17 (05) R206
• 48 Yoo T, Lo WD, Evans DC. Computed tomography measured psoas density predicts outcomes in trauma. Surgery 2017; 162 (02) 377-384
• 49 Jones K, Gordon-Weeks A, Coleman C, Silva M. Radiologically determined sarcopenia predicts morbidity and mortality following abdominal surgery: a systematic review and meta-analysis. World J Surg 2017; 41 (09) 2266-2279
• 50 Deren ME, Babu J, Cohen EM, Machan J, Born CT, Hayda R. Increased mortality in elderly patients with sarcopenia and acetabular fractures. J Bone Joint Surg Am 2017; 99 (03) 200-206
• 51 Dirks RC, Edwards BL, Tong E. , et al. Sarcopenia in emergency abdominal surgery. J Surg Res 2017; 207: 13-21
• 52 Matsubara Y, Matsumoto T, Inoue K. , et al. Sarcopenia is a risk factor for cardiovascular events experienced by patients with critical limb ischemia. J Vasc Surg 2017; 65 (05) 1390-1397
• 53 Uchiyama H. Sarcopenia in liver transplant recipients: its relevance to peritransplant morbidity and mortality. Hepatobiliary Surg Nutr 2017; 6 (03) 196-199
• 54 Shibahashi K, Sugiyama K, Kashiura M, Hamabe Y. Decreasing skeletal muscle as a risk factor for mortality in elderly patients with sepsis: a retrospective cohort study. J Intensive Care 2017; 5: 8
• 55 van Vugt JL, Levolger S, de Bruin RW, van Rosmalen J, Metselaar HJ, IJzermans JN. Systematic review and meta-analysis of the impact of computed tomography-assessed skeletal muscle mass on outcome in patients awaiting or undergoing liver transplantation. Am J Transplant 2016; 16 (08) 2277-2292
• 56 Hale AL, Twomey K, Ewing JA, Langan III EM, Cull DL, Gray BH. Impact of sarcopenia on long-term mortality following endovascular aneurysm repair. Vasc Med 2016; 21 (03) 217-222
• 57 Boutin RD, Bamrungchart S, Bateni CP. , et al. CT of patients with hip fracture: muscle size and attenuation help predict mortality. AJR Am J Roentgenol 2017; 208 (06) W208-W215
• 58 Pavasini R, Guralnik J, Brown JC. , et al. Short Physical Performance Battery and all-cause mortality: systematic review and meta-analysis. BMC Med 2016; 14 (01) 215
• 59 Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 1994; 843: 1-129
• 60 ACR–SPR–SSR practice parameter for the performance of quantitative computed tomography (QCT) bone densitometry. Available at: https://www.acr.org/-/media/ACR/Files/Practice-Parameters/qct.pdf?la=en . Accessed April 3, 2018
• 61 Graffy PM, Lee SJ, Ziemlewicz TJ, Pickhardt PJ. Prevalence of vertebral compression fractures on routine CT scans according to L1 trabecular attenuation: determining relevant thresholds for opportunistic osteoporosis screening. AJR Am J Roentgenol 2017; 209 (03) 491-496
• 62 Loenneke JP, Loprinzi PD, Abe T. The prevalence of sarcopenia before and after correction for DXA-derived fat-free adipose tissue. Eur J Clin Nutr 2016; 70 (12) 1458-1460
• 63 Abe T, Patterson KM, Stover CD, Young KC. Influence of adipose tissue mass on DXA-derived lean soft tissue mass in middle-aged and older women. Age (Dordr) 2015; 37 (01) 9741
• 64 Therkelsen KE, Pedley A, Hoffmann U, Fox CS, Murabito JM. Intramuscular fat and physical performance at the Framingham Heart Study. Age (Dordr) 2016; 38 (02) 31
• 65 Sheu Y, Marshall LM, Holton KF. , et al. Abdominal body composition measured by quantitative computed tomography and risk of non-spine fractures: the Osteoporotic Fractures in Men (MrOS) study. Osteoporos Int 2013; 24 (08) 2231-2241
• 66 Santanasto AJ, Goodpaster BH, Kritchevsky SB. , et al. Body composition remodeling and mortality: the Health Aging and Body Composition Study. J Gerontol A Biol Sci Med Sci 2017; 72 (04) 513-519
• 67 Kim EY, Kim YS, Park I. , et al. Evaluation of sarcopenia in small-cell lung cancer patients by routine chest CT. Support Care Cancer 2016; 24 (11) 4721-4726
• 68 Nemec U, Heidinger B, Sokas C, Chu L, Eisenberg RL. Diagnosing sarcopenia on thoracic computed tomography: quantitative assessment of skeletal muscle mass in patients undergoing transcatheter aortic valve replacement. Acad Radiol 2017; 24 (09) 1154-1161
• 69 Hyun SJ, Bae CW, Lee SH, Rhim SC. Fatty degeneration of the paraspinal muscle in patients with degenerative lumbar kyphosis: a new evaluation method of Quantitative digital analysis using MRI and CT scan. Clin Spine Surg 2016; 29 (10) 441-447
• 70 Swartz JE, Pothen AJ, Wegner I. , et al. Feasibility of using head and neck CT imaging to assess skeletal muscle mass in head and neck cancer patients. Oral Oncol 2016; 62: 28-33
• 71 Boutin RD, Kaptuch JM, Bateni CP, Chalfant JS, Yao L. Influence of IV contrast administration on CT measures of muscle and bone attenuation: implications for sarcopenia and osteoporosis evaluation. AJR Am J Roentgenol 2016; 207 (05) 1046-1054
• 72 Lang T, Koyama A, Li C. , et al. Pelvic body composition measurements by quantitative computed tomography: association with recent hip fracture. Bone 2008; 42 (04) 798-805
• 73 Prado CM, Lieffers JR, McCargar LJ. , 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 (07) 629-635
• 74 Cruz-Jentoft AJ, Kiesswetter E, Drey M, Sieber CC. Nutrition, frailty, and sarcopenia. Aging Clin Exp Res 2017; 29 (01) 43-48
• 75 Marzetti E, Calvani R, Tosato M. , et al; SPRINTT Consortium. Physical activity and exercise as countermeasures to physical frailty and sarcopenia. Aging Clin Exp Res 2017; 29 (01) 35-42
• 76 Kitajima Y, Takahashi H, Akiyama T. , et al. Supplementation with branched-chain amino acids ameliorates hypoalbuminemia, prevents sarcopenia, and reduces fat accumulation in the skeletal muscles of patients with liver cirrhosis. J Gastroenterol 2018; 53 (03) 427-437
• 77 Mochamat, Cuhls H, Marinova M. , et al. A systematic review on the role of vitamins, minerals, proteins, and other supplements for the treatment of cachexia in cancer: a European Palliative Care Research Centre cachexia project. J Cachexia Sarcopenia Muscle 2017; 8 (01) 25-39
• 78 Segal R, Zwaal C, Green E, Tomasone JR, Loblaw A, Petrella T. ; Exercise for People with Cancer Guideline Development Group. Exercise for people with cancer: a systematic review. Curr Oncol 2017; 24 (04) e290-e315
• 79 Arends J, Bachmann P, Baracos V. , et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr 2017; 36 (01) 11-48
• 80 Dawson-Hughes B, Bischoff-Ferrari H. Considerations concerning the definition of sarcopenia. Osteoporos Int 2016; 27 (11) 3139-3144
• 81 Sun G, French CR, Martin GR. , et al. Comparison of multifrequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for assessment of percentage body fat in a large, healthy population. Am J Clin Nutr 2005; 81 (01) 74-78
• 82 Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology 2016; 278 (02) 563-577
• 83 Morley JE, Anker SD. Myopenia and precision (P4) medicine. J Cachexia Sarcopenia Muscle 2017; 8 (06) 857-863
• 84 Polan DF, Brady SL, Kaufman RA. Tissue segmentation of computed tomography images using a Random Forest algorithm: a feasibility study. Phys Med Biol 2016; 61 (17) 6553-6569
• 85 Kullberg J, Hedström A, Brandberg J. , et al. Automated analysis of liver fat, muscle and adipose tissue distribution from CT suitable for large-scale studies. Sci Rep 2017; 7 (01) 10425
• 86 Shah RV, Yeri AS, Murthy VL. , et al. Association of multiorgan computed tomographic phenomap with adverse cardiovascular health outcomes: the Framingham Heart Study. JAMA Cardiol 2017; 2 (11) 1236-1246