Abstract
Purpose
Measurement of muscle mass is paramount in the screening and diagnosis of sarcopenia. Besides muscle quantity however, also quality assessment is important. Ultrasonography (US) has the advantage over dual-energy X-ray absorptiometry (DEXA) and bio-impedance analysis (BIA) to give both quantitative and qualitative information on muscle. However, before its use in clinical practice, several methodological aspects still need to be addressed. Both standardization in measurement techniques and the availability of reference values are currently lacking. This review aims to provide an evidence-based standardization of assessing appendicular muscle with the use of US.
Methods
A systematic review was performed for ultrasonography to assess muscle in older people. Pubmed, SCOPUS and Web of Sciences were searched. All articles regarding the use of US in assessing appendicular muscle were used. Description of US-specific parameters and localization of the measurement were retrieved.
Results
Through this process, five items of muscle assessment were identified in the evaluated articles: thickness, cross-sectional area, echogenicity, fascicle length and pennation angle. Different techniques for measurement and location of measurement used were noted, as also the different muscles in which this was evaluated. Then, a translation for a clinical setting in a standardized way was proposed.
Conclusions
The results of this review provide thus an evidence base for an ultrasound protocol in the assessment of skeletal muscle. This standardization of measurements is the first step in creating conditions to further test the applicability of US for use on a large scale as a routine assessment and follow-up tool for appendicular muscle.
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References
Beaudart C et al (2014) Sarcopenia: burden and challenges for public health. Arch Public Health 72(1):45
Beaudart C et al (2017) Health outcomes of sarcopenia: a systematic review and meta-analysis. PLoS ONE 12(1):e0169548
Cruz-Jentoft AJ 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):412–423
Muscaritoli M et al (2010) Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 29(2):154–159
Fielding RA 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):249–256
Morley JE et al (2011) Sarcopenia with limited mobility: an international consensus. J Am Med Dir Assoc 12(6):403–409
Dam TT et al (2014) An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci 69(5):584–590
Chen LK et al (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 15(2):95–101
Beaudart C et al (2015) Estimation of sarcopenia prevalence using various assessment tools. Exp Gerontol 61:31–37
Baumgartner RN et al (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763
Delmonico MJ et al (2007) Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J Am Geriatr Soc 55(5):769–774
Newman AB et al (2003) Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 51(11):1602–1609
Chien MY, Huang TY, Wu YT (2008) Prevalence of sarcopenia estimated using a bioelectrical impedance analysis prediction equation in community-dwelling elderly people in Taiwan. J Am Geriatr Soc 56(9):1710–1715
Janssen I et al (2004) Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol 159(4):413–421
Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50(5):889–896
Barbat-Artigas S et al (2012) How to assess functional status: a new muscle quality index. J Nutr Health Aging 16(1):67–77
Newman AB et al (2003) Strength and muscle quality in a well-functioning cohort of older adults: the Health, Aging and Body Composition Study. J Am Geriatr Soc 51(3):323–330
Goodpaster BH et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61(10):1059–1064
Perkisas S et al (2016) Physiological and architectural changes in the ageing muscle and their relation to strength and function in sarcopenia. Eur Geriatr Med 7(3):201–206. https://doi.org/10.1016/j.eurger.2015.12.016
Perkisas S, De Cock AM, Verhoeven V, Vandewoude M (2017) Intramuscular adipose tissue and the functional components of sarcopenia in hospitalized geriatric patients. Geriatrics 2(1):11. https://doi.org/10.3390/geriatrics2010011
Reinders I et al (2016) Muscle quality and myosteatosis: novel associations with mortality risk: the Age, Gene/Environment Susceptibility (AGES)-Reykjavik Study. Am J Epidemiol 183(1):53–60
Buckinx F et al (2018) Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle 9(2):269–278
Yamada Y et al (2017) Electrical properties assessed by bioelectrical impedance spectroscopy as biomarkers of age-related loss of skeletal muscle quantity and quality. J Gerontol A Biol Sci Med Sci 72(9):1180–1186
Bartels EM, Sorensen ER, Harrison AP (2015) Multi-frequency bioimpedance in human muscle assessment. Physiol Rep 3(4):e12354
Beaudart C et al (2016) Sarcopenia in daily practice: assessment and management. BMC Geriatr 16(1):170
Goodpaster BH et al (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol (1985) 89(1):104–110
Heymsfield SB et al (2014) Assessing skeletal muscle mass: historical overview and state of the art. J Cachexia Sarcopenia Muscle 5(1):9–18
Fischer MA et al (2014) Dixon-based MRI for assessment of muscle-fat content in phantoms, healthy volunteers and patients with achillodynia: comparison to visual assessment of calf muscle quality. Eur Radiol 24(6):1366–1375
Pfirrmann CW et al (2004) Assessment of fat content in supraspinatus muscle with proton MR spectroscopy in asymptomatic volunteers and patients with supraspinatus tendon lesions. Radiology 232(3):709–715
Prompers JJ et al (2006) Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed 19(7):927–953
Valkovic L, Chmelik M, Krssak M (2017) In-vivo(31)P-MRS of skeletal muscle and liver: a way for non-invasive assessment of their metabolism. Anal Biochem 529:193–215
Mourtzakis M et al (2008) A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 33(5):997–1006
Shen W et al (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (1985) 97(6):2333–2338
Janssen I et al (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol (1985) 89(1):81–88
Pillen S, van Alfen N (2011) Skeletal muscle ultrasound. Neurol Res 33(10):1016–1024
Passmore E, Lai A, Sangeux M et al (2017) Application of ultrasound imaging to subject-specific modelling of the human musculoskeletal system. Meccanica 52:665. https://doi.org/10.1007/s11012-016-0478-z
Abe T et al (2016) Ultrasound-derived forearm muscle thickness is a powerful predictor for estimating DXA-derived appendicular lean mass in Japanese older adults. Ultrasound Med Biol 42(9):2341–2344
Takai Y et al (2014) Applicability of ultrasound muscle thickness measurements for predicting fat-free mass in elderly population. J Nutr Health Aging 18(6):579–585
Takai Y et al (2013) Validity of ultrasound muscle thickness measurements for predicting leg skeletal muscle mass in healthy Japanese middle-aged and older individuals. J Physiol Anthropol 32:12
Abe T et al (2015) Validity of ultrasound prediction equations for total and regional muscularity in middle-aged and older men and women. Ultrasound Med Biol 41(2):557–564
Thomaes T et al (2012) Reliability and validity of the ultrasound technique to measure the rectus femoris muscle diameter in older CAD-patients. BMC Med Imaging 12:7
Sanada K et al (2006) Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults. Eur J Appl Physiol 96(1):24–31
Tandon P et al (2016) A model to identify sarcopenia in patients with cirrhosis. Clin Gastroenterol Hepatol 14(10):1473–1480 e3
Reeves ND, Maganaris CN, Narici MV (2004) Ultrasonographic assessment of human skeletal muscle size. Eur J Appl Physiol 91:116–118
Nijholt W et al (2017) The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle 8(5):702–712
Mourtzakis M, Wischmeyer P (2014) Bedside ultrasound measurement of skeletal muscle. Curr Opin Clin Nutr Metab Care 17(5):389–395
Haberfehlner H et al (2016) Freehand three-dimensional ultrasound to assess semitendinosus muscle morphology. J Anat 229:591–599
Martin DC et al (2001) Comparing human skeletal muscle architectural parameters of cadavers with in vivo ultrasonographic measurements. J Anat 199:429–434
Tosovic D et al (2016) Anatomy of the long head of biceps femoris: an ultrasound study. Clin Anat 29(6):738–745
Kellis E et al (2009) Validity of architectural properties of the hamstring muscles: correlation of ultrasound findings with cadaveric dissection. J Biomech 42(15):2549–2554
Infantolino BW, Challis JH (2016) Evaluation of a simple method for determining muscle volume in vivo. J Biomech 49(9):1973–1975
Tillquist M et al (2014) Bedside ultrasound is a practical and reliable measurement tool for assessing quadriceps muscle layer thickness. J Parenter Enter Nutr 38(7):886–890
English C, Fisher L, Thoirs K (2012) Reliability of real-time ultrasound for measuring skeletal muscle size in human limbs in vivo: a systematic review. Clin Rehabil 26(10):934–944
Miyatani M et al (2004) The accuracy of volume estimates using ultrasound muscle thickness measurements in different muscle groups. Eur J Appl Physiol 91(2):264–272
Nijholt W et al (2018) Response to: “The use of ultrasound for the estimation of muscle mass: one site fits most?”. J Cachexia Sarcopenia Muscle 9:627–628
Reimers CD, Harder T, Saxe H (1998) Age-related muscle atrophy does not affect all muscles and can partly be compensated by physical activity: an ultrasound study. J Neurol Sci 159(1):60–66
Arts IMP et al (2007) Rise and fall of skeletal muscle size over the entire life span. J Am Geriatr Soc 55:1150–1152
Arts IMP et al (2010) Normal values for quantitative muscle ultrasonography in adults. Muscle Nerve 41(1):32–41
Verhulst FV et al (2011) Quantitative ultrasound of lower leg and foot muscles: feasibility and reference values. Foot Ankle Surg Off J Eur Soc Foot Ankle Surg 17(3):145–149
Maurits NM et al (2002) Quantitative muscle ultrasound analysis in healthy adults: weight- and age-related normal values. Neuromuscular Disord 12(7):776
Ticinesi A et al (2017) Muscle ultrasound and sarcopenia in older individuals: a clinical perspective. J Am Med Dir Assoc 18(4):290–300
Welch C et al (2018) Acute sarcopenia secondary to hospitalisation—an emerging condition affecting older adults. Aging Dis 9(1):151–164
van de Glind EM et al (2012) Search filters to identify geriatric medicine in Medline. J Am Med Inform Assoc 19(3):468–472
Ouzzani M et al (2016) Rayyan—a web and mobile app for systematic reviews. Syst Rev 5(1):210
Ema R et al (2013) In vivo measurement of human rectus femoris architecture by ultrasonography: validity and applicability. Clin Physiol Funct Imaging 33:267–273
de Bruin PF et al (1997) Size and strength of the respiratory and quadriceps muscles in patients with chronic asthma. Eur Respir J 10:59–64
Correa CS et al (2016) Effects of strength training, detraining and retraining in muscle strength, hypertrophy and functional tasks in older female adults. Clin Physiol Funct Imaging 36(4):306–310
Harris-Love MO et al (2016) Ultrasound estimates of muscle quality in older adults: reliability and comparison of Photoshop and ImageJ for the grayscale analysis of muscle echogenicity. PeerJ 4:e1721
Narici MV et al (2003) Effect of aging on human muscle architecture. J Appl Physiol (Bethesda, Md.: 1985) 95(6):2229–2234
Kaya A et al (2013) Ultrasonographic evaluation of the muscle architecture in patients with systemic lupus erythematosus. Clin Rheumatol 32(8):1155–1160
Kleinberg CR et al (2016) Influence of lower extremity muscle size and quality on stair-climb performance in career firefighters. J Strength Cond Res 30(6):1613–1618
da Silva RP et al (2017) Effect of strength training on sleep apnea severity in the elderly: study protocol for a randomized controlled trial. Trials 18(1):489
Akima H et al (2017) Relationship between quadriceps echo intensity and functional and morphological characteristics in older men and women. Arch Gerontol Geriatr 70:105–111
Bemben DA, Langdon DB (2002) Relationship between estrogen use and musculoskeletal function in postmenopausal women. Maturitas 42:119–127
Baroni BM et al (2013) Time course of neuromuscular adaptations to knee extensor eccentric training. Int J Sports Med 34(10):904–911
Gerovasili V et al (2009) Electrical muscle stimulation preserves the muscle mass of critically ill patients: a randomized study. Crit Care 13:R161
Guerreiro AC et al (2017) Bedside ultrasound of quadriceps to predict rehospitalization and functional decline in hospitalized elders. Front Med 4:122
Ikezoe T et al (2011) Age-related muscle atrophy in the lower extremities and daily physical activity in elderly women. Arch Gerontol Geriatr 53(2):e153–e157
Ikezoe T et al (2012) Associations of muscle stiffness and thickness with muscle strength and muscle power in elderly women. Geriatr Gerontol Int 12:86–92
Kara M et al (2015) Does vitamin D affect muscle strength and architecture? An isokinetic and ultrasonographic study. Asia Pac J Clin Nutr 26(1):85–88
Seymour JM et al (2009) Ultrasound measurement of rectus femoris cross-sectional area and the relationship with quadriceps strength in COPD. Thorax 64:418–423
Minetto MA et al (2016) Ultrasound-based detection of low muscle mass for diagnosis of sarcopenia in older adults. PM&R J Inj Funct Rehabil 8(5):453–462
Mota JA, Stock MS (2017) Rectus femoris echo intensity correlates with muscle strength, but not endurance, in younger and older men. Ultrasound Med Biol 43(8):1651–1657
Rech A et al (2014) Echo intensity is negatively associated with functional capacity in older women. Age 36:9708
Rieder F et al (2015) Alpine Skiing With total knee ArthroPlasty (ASWAP): muscular adaptations. Scand J Med Sci Sports 25:26–32
Ticinesi A, Narici MV, Lauretani F et al (2018) Assessing sarcopenia with vastus lateralis muscle ultrasound: an operative protocol. Aging Clin Exp Res. https://doi.org/10.1007/s40520-018-0958-1
Scanlon, T.C., et al., Muscle architecture and strength: adaptations to short-term resistance training in older adults. Vol. 49. 2014. 584-92
Mangine GT et al (2014) Bilateral differences in muscle architecture and increased rate of injury in national basketball association players. J Athl Train 49(6):794–799
Marin PJ et al (2013) Effects of whole-body vibration on muscle architecture, muscle strength, and balance in stroke patients a randomized controlled trial. Am J Phys Med Rehabil 92(10):881–888
Cruz-Montecinos C et al (2016) Sonographic measurement of the quadriceps muscle in patients with chronic obstructive pulmonary disease: functional and clinical implications. J Ultrasound Med 35(11):2405–2412
Hammond K et al (2014) Validity and reliability of rectus femoris ultrasound measurements: comparison of curved-array and linear-array transducers. J Rehabil Res Dev 51:1155–1164
Mueller N et al (2016) Can sarcopenia quantified by ultrasound of the rectus femoris muscle predict adverse outcome of surgical intensive care unit patients as well as frailty? A prospective, observational cohort study. Ann Surg 264:1116–1124
Berger J et al (2015) Rectus femoris (RF) ultrasound for the assessment of muscle mass in older people. Arch Gerontol Geriatr 61:33–38
Fukumoto Y et al (2012) Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol 112(4):1519–1525
Shimizu S et al (2006) The relationship between cardiac muscle, skeletal muscle mass, and vessel structure in elderly women. Jpn J Phys Fit Sports Med 55:213–216
Nakatani M et al (2016) Validity of muscle thickness-based prediction equation for quadriceps femoris volume in middle-aged and older men and women. Eur J Appl Physiol 116(11):2125–2133
de Boer MD et al (2008) Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur J Appl Physiol 104(2):401–407
Lixandrão ME et al (2016) Time course of resistance training-induced muscle hypertrophy in the elderly. J Strength Cond Res 30:159–163
Alegre LM et al (2006) Effects of dynamic resistance training on fascicle length and isometric strength. J Sports Sci 24(5):501–508
Malas FÜ et al (2013) Effects of different strength training on muscle architecture: clinical and ultrasonographic evaluation in knee osteoarthritis. PM&R 5:655–662
de Oliveira Melo M et al (2015) Effects of neuromuscular electrical stimulation and low-level laser therapy on the muscle architecture and functional capacity in elderly patients with knee osteoarthritis: a randomized controlled trial. Clin Rehabil 29:570–580
Karamanidis K, Arampatzis A (2005) Mechanical and morphological properties of different muscle-tendon units in the lower extremity and running mechanics: effect of aging and physical activity. J Exp Biol 208:3907–3923
Fukutani A, Kurihara T (2015) Comparison of the muscle fascicle length between resistance-trained and untrained individuals: cross-sectional observation. Springerplus 4:341
Engelina S et al (2014) Ultrasound investigation of vastus medialis oblique muscle architecture: an in vivo study. Clin Anat (New York, NY) 27(7):1076–1084
Akazawa N et al (2017) Relationships between intramuscular fat, muscle strength and gait independence in older women: a cross-sectional study. Geriatr Gerontol Int 17(10):1683–1688
Selva Raj I, Bird SR, Shield AJ (2017) Ultrasound measurements of skeletal muscle architecture are associated with strength and functional capacity in older adults. Ultrasound Med Biol 43:586–594
Erskine RM et al (2017) The individual and combined effects of obesity- and ageing-induced systemic inflammation on human skeletal muscle properties. Int J Obes (2005) 41(1):102–111
Gerstner GR et al (2017) Neural and muscular contributions to the age-related reductions in rapid strength. Med Sci Sports Exerc 49(7):1331–1339
Atkinson RA et al (2010) Effects of testosterone on skeletal muscle architecture in intermediate-frail and frail elderly men. J Gerontol Ser A Biomed Sci Med Sci 65:1215–1219
Morse CI et al (2005) In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J Appl Physiol (1985) 99(3):1050–1055
Rosenberg JG et al (2014) Reliability of panoramic ultrasound imaging to simultaneously examine muscle size and quality of the medial gastrocnemius. Muscle Nerve 49(5):736–740
Fujiwara K et al (2010) Regular heel-raise training focused on the soleus for the elderly: evaluation of muscle thickness by ultrasound. J Physiol Anthropol 29(1):23–28
Ohata K et al (2006) Measurement of muscle thickness as quantitative muscle evaluation for adults with severe cerebral palsy. Phys Ther 86(9):1231–1239
Kawakami Y, Abe T, Fukunaga T (1993) Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 74:2740–2744
Kubo K et al (2003) Muscle architectural characteristics in women aged 20–79 years. Med Sci Sports Exerc 35:39–44
Ojanen T, Rauhala T, Häkkinen K (2007) Strength and power profiles of the lower and upper extremities in master throwers at different ages. J Strength Cond Res 21(1):216–222
Stock MS et al (2016) Evidence of muscular adaptations within four weeks of barbell training in women. Human Mov Sci 45:7–22
Nijboer-Oosterveld J, Van Alfen N, Pillen S (2011) New normal values for quantitative muscle ultrasound: obesity increases muscle echo intensity. Muscle Nerve 43:142–143
Fragala MS et al (2014) Biomarkers of muscle quality: N-terminal propeptide of type III procollagen and C-terminal agrin fragment responses to resistance exercise training in older adults. J Cachexia Sarcopenia Muscle 5(2):139–148
Taniguchi M et al (2017) Increase in echo intensity and extracellular-to-intracellular water ratio is independently associated with muscle weakness in elderly women. Eur J Appl Physiol 117(10):2001–2007
Yamada M et al (2017) Differential characteristics of skeletal muscle in community-dwelling older adults. J Am Med Dir Assoc 18(9):807.e9–807.e16
Ye X, Wang MJ, Xiao H (2017) Echo intensity of the rectus femoris in stable COPD patients. Int J Chronic Obstr Pulm Dis 12:3007–3015
Wilhelm EN et al (2014) Concurrent strength and endurance training exercise sequence does not affect neuromuscular adaptations in older men. Exp Gerontol 60:207–214
Fukumoto Y et al (2015) Age-related ultrasound changes in muscle quantity and quality in women. Ultrasound Med Biol 41(11):3013–3017
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675
Aagaard P et al (2001) A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol 534(Pt. 2):613–623
Greening NJ et al (2015) Bedside assessment of quadriceps muscle by ultrasound after admission for acute exacerbations of chronic respiratory disease. Am J Respir Crit Care Med 192:810–816
Lieber RL, Friden J (2002) Morphologic and mechanical basis of delayed-onset muscle soreness. J Am Acad Orthop Surg 10(1):67–73
Austin N, Nilwik R, Herzog W (2010) In vivo operational fascicle lengths of vastus lateralis during sub-maximal and maximal cycling. J Biomech 43(12):2394–2399
Erskine RM et al (2009) In vivo specific tension of the human quadriceps femoris muscle. Eur J Appl Physiol 106(6):827–838
Korhonen MT et al (2009) Biomechanical and skeletal muscle determinants of maximum running speed with aging. Med Sci Sports Exerc 41:844–856
Cadore EL et al (2012) Echo intensity is associated with skeletal muscle power and cardiovascular performance in elderly men. Exp Gerontol 47:473–478
Wu R et al (2016) Effects of age and sex on neuromuscular-mechanical determinants of muscle strength. Age 38:57
Muraki S, Fukumoto K, Fukuda O (2013) Prediction of the muscle strength by the muscle thickness and hardness using ultrasound muscle hardness meter. Springerplus 2:457
Varanoske AN et al (2017) Scanning plane comparison of ultrasound-derived morphological characteristics of the vastus lateralis. Clin Anat 30(4):533–542
Wilhelm EN et al (2014) Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity of older men. Age 36:9625
Tang ZW et al (2015) Size of quadriceps femoris may contribute to thyrotoxic periodic paralysis. Med Hypotheses 85(6):749–753
Watson EL et al (2015) Progressive resistance exercise training in CKD: a feasibility study. Am J Kidney Dis 66(2):249–257
Kawai H et al (2018) Morphological and qualitative characteristics of the quadriceps muscle of community-dwelling older adults based on ultrasound imaging: classification using latent class analysis. Aging Clin Exp Res 30(4):283–291
Caresio C et al (2017) Fully automated muscle ultrasound analysis (MUSA): robust and accurate muscle thickness measurement. Ultrasound Med Biol 43(1):195–205
Welch D et al. (2018) Thigh muscle and subcutaneous tissue thickness measured using ultrasound imaging in older females living in extended care: a preliminary study. Aging Clin Exp Res 30(5):463–469
Shim DG, Kwon TY, Lee KB (2017) Rectus femoris muscle atrophy and recovery caused by preoperative pretibial traction in femoral shaft fractures-comparison between traction period. Orthop Traumatol Surg Res 103(5):691–695
Bemben MG (2002) Use of diagnostic ultrasound for assessing muscle size. J Strength Cond Res 16:103–108
Tok F et al (2011) Effects of botulinum toxin-A on the muscle architecture of stroke patients: an ultrasonographic study. J Rehabil Med 43(11):1016–1019
Tomlinson DJ et al (2014) The impact of obesity on skeletal muscle architecture in untrained young vs. old women. J Anat 225(6):675–684
Padhiar N et al (2008) Pennation angle of the soleus in patients with unilateral Achilles tendinopathy. Disabil Rehabil 30(20):1640–1645
Nagano Y, Higashihara A, Edama M (2015) Change in muscle thickness under contracting conditions following return to sports after a hamstring muscle strain injury—a pilot study. Asia Pac J Sports Med Arthrosc Rehabil Technol 2(2):63–67
Sjogaard G, Saltin B (1982) Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. Am J Physiol 243(3):R271–R280
Thoirs K, English C (2009) Ultrasound measures of muscle thickness: intra-examiner reliability and influence of body position. Clin Physiol Funct Imaging 29(6):440–446
Berg HE, Tedner B, Tesch PA (1993) Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol Scand 148(4):379–385
Cerniglia LM et al (2007) Effects of acute supine rest on mid-thigh cross-sectional area as measured by computed tomography. Clin Physiol Funct Imaging 27(4):249–253
Wagle JP et al (2017) Comparison of the relationship between lying and standing ultrasonography measures of muscle morphology with isometric and dynamic force production capabilities. Sports 5(4):88
Koda H et al (2018) Relationship between muscle strength asymmetry and body sway in older adults. J Aging Phys Act 26(3):457–461
Heckmatt JZ, Pier N, Dubowitz V (1988) Assessment of quadriceps femoris muscle atrophy and hypertrophy in neuromuscular disease in children. J Clin Ultrasound 16(3):177–181
Dupont AC et al (2001) Real-time sonography to estimate muscle thickness: comparison with MRI and CT. J Clin Ultrasound 29(4):230–236
Backhaus M et al (2001) Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis 60(7):641–649
Narici MV et al (1989) Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol Occup Physiol 59(4):310–319
Kubo K et al (2003) Muscle architectural characteristics in young and elderly men and women. Int J Sports Med 24(2):125–130
Reeves ND, Narici MV, Maganaris CN (2004) In vivo human muscle structure and function: adaptations to resistance training in old age. Exp Physiol 89:675–689
Miljkovic I et al (2015) Greater skeletal muscle fat infiltration is associated with higher all-cause and cardiovascular mortality in older men. J Gerontol A Biol Sci Med Sci 70(9):1133–1140
Rollins KE et al (2016) The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin Nutr 35(5):1103–1109
Montano-Loza AJ et al (2016) Sarcopenic obesity and myosteatosis are associated with higher mortality in patients with cirrhosis. J Cachexia Sarcopenia Muscle 7(2):126–135
Reimers K et al (1993) Skeletal muscle sonography: a correlative study of echogenicity and morphology. J Ultrasound Med 12(2):73–77
Ismail C et al (2015) Diagnostic ultrasound estimates of muscle mass and muscle quality discriminate between women with and without sarcopenia. Front Physiol 6:302
Pillen S et al (2009) Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 35(3):443–446
Moher D et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012
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Perkisas, S., Baudry, S., Bauer, J. et al. Application of ultrasound for muscle assessment in sarcopenia: towards standardized measurements. Eur Geriatr Med 9, 739–757 (2018). https://doi.org/10.1007/s41999-018-0104-9
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DOI: https://doi.org/10.1007/s41999-018-0104-9