Sonoelastography to Assess Muscular Stiffness Among Older Adults and its Use for the Diagnosis of Sarcopenia: A Systematic Review

Abstract

Changes in muscle stiffness have been reported with sarcopenia. Sonoelastography is an accessible and non-radiating imaging technique allowing quantification of elastic properties of tissue. We performed a systematic review of the literature to investigate whether sonoelastography can be a reliable method to assess sarcopenia in older patients. We searched Medline, Google Scholar, Scopus, SpringerLink and Science direct from January 1, 1990 to April 1, 2020. Three independent review authors assessed trial eligibility, extracted the data, and assessed risk of bias. We intended to learn which types of elastography have been tested, if such measures are repeatable, and if they have been compared to the currently accepted diagnostic method. Ten studies met the inclusion criteria. Most followed a cross-sectional design with young and older adult subgroups. The gastrocnemius, rectus femoris, and vastus intermedius appeared most frequently. Nine of the included studies used shear wave elastography and one-strain elastography. The passive elastic constant was significantly greater in sarcopenic versus healthy subjects after passive stretching (124.98 ± 60.82 vs. 46.35 ± 15.85, P = 0.004). However, even in non-sarcopenic patients, the age of the patient was responsible for about 45.5 % of the variance in SWV. Among ten included articles, four reported higher stiffness in the muscles of older adults, two reported lower stiffness, and four found no significant difference. Due to the substantial heterogenicity of actual data, we could not make any conclusions about the potential usefulness of elastography to assess sarcopenia. Further studies are needed, including a larger sample of older patients and using a standardized and reproducible protocol.

Zusammenfassung

Bei Sarkopenie wurden Veränderungen der Muskelsteifheit berichtet. Die Sonoelastografie ist eine einfach zugängliche und strahlungsfreie Bildgebungstechnik, die die Quantifizierung der elastischen Eigenschaften des Gewebes ermöglicht. Wir führten eine systematische Überprüfung der Literatur durch, um zu untersuchen, ob die Sonoelastografie eine zuverlässige Methode zur Beurteilung der Sarkopenie bei älteren Patienten sein kann. Wir haben MEDLINE, Google Scholar, Scopus, SpringerLink und ScienceDirect vom 1. Januar 1990 bis zum 1. April 2020 durchsucht. Drei unabhängige Review-Autoren bewerteten die Eignung der Studien, extrahierten die Daten und schätzten das Bias-Risiko ein. Wir wollten herausfinden, welche elastografischen Methoden eingesetzt wurden, ob entsprechende Messungen wiederholbar sind und ob sie mit der derzeit anerkannten Diagnostik verglichen wurden. Zehn Studien erfüllten die Einschlusskriterien. Die meisten folgten einem Querschnittsdesign mit Untergruppen von jungen und älteren Erwachsenen. Am häufigsten wurden M. gastrocnemius, M. rectus femoris und M. vastus intermedius untersucht. Neun der eingeschlossenen Studien verwendeten Scherwellen-Elastografie und eine Strain-Elastografie. Die passive Elastizitätskonstante war bei sarkopenischen gegenüber gesunden Probanden nach passiver Dehnung signifikant höher (124,98 ± 60,82 vs. 46,35 ± 15,85; p = 0,004). Selbst bei nichtsarkopenischen Patienten war das Alter des Patienten für etwa 45,5 % der Varianz der SWV verantwortlich. Von den 10 eingeschlossenen Arbeiten berichteten 4 über eine höhere Steifheit in den Muskeln älterer Erwachsener, 2 über eine geringere Steifheit und 4 fanden keinen signifikanten Unterschied. Aufgrund der erheblichen Heterogenität der derzeitigen Daten konnten wir den potenziellen Nutzen der Elastografie zur Bewertung der Sarkopenie nicht abschließend beurteilen. Es sind weitere Studien erforderlich, einschließlich einer größeren Stichprobe älterer Patienten und dem Einsatz eines standardisierten und reproduzierbaren Protokolls.

Key words

older adults - sarcopenia - elastography - sonoelastography - elasticity imaging techniques

• References

• 1 Cruz-Jentoft AJ, Bahat G, Bauer J. et al. Sarcopenia: revised European consensus on definition and diagnosis. Age and Ageing 2019; 48: 16-31
• 2 Sousa AS, Guerra RS, Fonseca I. et al. Financial impact of sarcopenia on hospitalization costs. Eur J Clin Nutr 2016; 70: 1046-1051
• 3 Landi F, Liperoti R, Russo A. et al. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr 2012; 31: 652-658
• 4 Di Monaco M, Vallero F, Di Monaco R. et al. Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr 2011; 52: 71-74
• 5 Guralnik JM, Ferrucci L, Simonsick EM. et al. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med 1995; 332: 556-561
• 6 Chang KV, Hsu TH, Wu WT. et al. Association Between Sarcopenia and Cognitive Impairment: A Systematic Review and Meta-Analysis. Journal of the American Medical Directors Association 2016; 17: 1164.e7-1164.e15
• 7 Brown JC, Harhay MO, Harhay MN. Sarcopenia and mortality among a population‐based sample of community‐dwelling older adults. J Cachexia Sarcopenia Muscle 2016; 7: 290-298
• 8 Goodpaster BH, Park SW, Harris TB. et al. 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 2006; 61: 1059-1064
• 9 Larsson L, Degens H, Li M. et al. Sarcopenia: Aging-Related Loss of Muscle Mass and Function. Physiol Rev 2019; 99: 427-511
• 10 Yamada Y. Muscle Mass, Quality, and Composition Changes During Atrophy and Sarcopenia. Adv Exp Med Biol 2018; 1088: 47-72
• 11 Komai S, Watanabe Y, Fujiwara Y. et al. Association between the nutritional status and the severity of sarcopenia among community-dwelling elderly Japanese people. Nihon Ronen Igakkai Zasshi 2016; 53: 387-395
• 12 Dalle S, Rossmeislova L, Koppo K. The Role of Inflammation in Age-Related Sarcopenia. Front Physiol 2017; 8: 1045
• 13 Ng TP, Lu Y, Choo RWM. et al Dysregulated homeostatic pathways in sarcopenia among frail older adults. Aging Cell 2018; 17: e12842 . Epub 2018 Oct 9
• 14 Bussolotto M, Ceccon A, Sergi G. et al. Assessment of body composition in elderly: accuracy of bioelectrical impedance analysis. Gerontology 1999; 45: 39-43
• 15 Kistorp CN, Svendsen OL. Body composition analysis by dual energy X-ray absorptiometry in female diabetics differ between manufacturers. European Journal of Clinical Nutrition 1997; 51: 449-454
• 16 Moher D, Liberati A, Tetzlaff J. et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of internal medicine 2009; 151: 264-269
• 17 Garra BS. Elastography: history, principles, and technique comparison. Abdom Imaging 2015; 40: 680-697
• 18 Ouzzani M, Hammady H, Fedorowicz Z. et al. Rayyan – a web and mobile app for systematic reviews. Systematic Reviews 2016; 5: 210
• 19 Whiting PF, Rutjes AWS, Westwood ME. et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011; 155: 529-536
• 20 Sun Y, Xiao Y, Li F. et al. Diagnosing Muscle Atrophy by Use of a Comprehensive Method of Assessing the Elastic Properties of Muscle During Passive Stretching. Am J Roentgenol 2020; 214: 862-870
• 21 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
• 22 Alfuraih AM, Tan AL, O’Connor P. et al. The effect of ageing on shear wave elastography muscle stiffness in adults. Aging Clin Exp Res 2019; 31: 1755-1763
• 23 Baumer TG, Dischler J, Davis L. et al. Effects of age and pathology on shear wave speed of the human rotator cuff. J Orthop Res 2018; 36: 282-288
• 24 Eby SF, Cloud BA, Brandenburg JE. et al. Shear Wave Elastography of Passive Skeletal Muscle Stiffness: Influences of Sex and Age throughout Adulthood. Clin Biomech (Bristol, Avon) 2015; 30: 22-27
• 25 Wang CZ, Li TJ, Zheng YP. Shear Modulus Estimation on Vastus Intermedius of Elderly and Young Females over the Entire Range of Isometric Contraction. PLoS One 2014; 9: e101769 . eCollection 2014
• 26 Wang CZ, Guo JY, Li TJ. et al Age and Sex Effects on the Active Stiffness of Vastus Intermedius under Isometric Contraction. Biomed Res Int 2017; 2017: 9469548 . Epub 2017 Apr 3
• 27 Akagi R, Yamashita Y, Ueyasu Y. Age-Related Differences in Muscle Shear Moduli in the Lower Extremity. Ultrasound Med Biol 2015; 41: 2906-2912
• 28 Saito A, Wakasa M, Kimoto M. et al. Age-related changes in muscle elasticity and thickness of the lower extremities are associated with physical functions among community-dwelling older women. Geriatr Gerontol Int 2019; 19: 61-65
• 29 Nakamura M, Ikezoe T, Nishishita S. et al. Acute effects of static stretching on the shear elastic moduli of the medial and lateral gastrocnemius muscles in young and elderly women. Musculoskelet Sci Pract 2017; 32: 98-103
• 30 Heizelmann A, Tasdemir S, Schmidberger J. et al. Measurements of the trapezius and erector spinae muscles using virtual touch imaging quantification ultrasound-Elastography: a cross section study. BMC Musculoskelet Disord 2017; 18: 370
• 31 Bortolotto C, Lungarotti L, Fiorina I. et al. Influence of subjects’ characteristics and technical variables on muscle stiffness measured by shear wave elastosonography. J Ultrasound 2017; 20: 139-146
• 32 Rominger MB, Kälin P, Mastalerz M. et al. Influencing Factors of 2D Shear Wave Elastography of the Muscle – An Ex Vivo Animal Study. Ultrasound Int Open 2018; 4: E54-E60
• 33 Wang X, Hu Y, Zhu J. et al. Effect of acquisition depth and precompression from probe and couplant on shear wave elastography in soft tissue: an in vitro and in vivo study. Quantitative Imaging in Medicine and Surgery 2020; 10: 754-765
• 34 Reimers CD, Harder T, Saxe H. Age-related muscle atrophy does not affect all muscles and can partly be compensated by physical activity: An ultrasound study1Presented in part at the 34^th German Congress of Sports Medicine in Saarbrücken/Germany, October 19–22, 1995 [8].1. Journal of the Neurological Sciences 1998; 159: 60-66
• 35 Bamber J, Cosgrove D, Dietrich CF. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in Med 2013; 34: 169-184