Advertisement

Aging Clinical and Experimental Research

, Volume 30, Issue 12, pp 1437–1443 | Cite as

Assessing sarcopenia with vastus lateralis muscle ultrasound: an operative protocol

  • Andrea Ticinesi
  • Marco V. Narici
  • Fulvio Lauretani
  • Antonio Nouvenne
  • Elena Colizzi
  • Marco Mantovani
  • Andrea Corsonello
  • Francesco Landi
  • Tiziana Meschi
  • Marcello Maggio
Original Article

Abstract

Background

Muscle ultrasound (MUS) has so far not been implemented for sarcopenia assessment in clinical geriatric practice due to allegedly low reproducibility of results in the absence of standardization of procedures. However, rigorous and standardized application of this technique yields highly reproducible results. Its application, especially if integrated with clinical evaluation and comprehensive geriatric assessment, proofs very useful for rapidly obtaining information on muscle mass and architecture.

Objective

Here, we present a standardized protocol for performing right vastus lateralis (RVL) MUS and measuring parameters of muscle size and architecture.

Methods

RVL muscle thickness (MT), fascicle length (FL), pennation angle (PA), echo-intensity (EI) and cross-sectional area (CSA) can be assessed with this protocol. A portable instrument equipped with a 5-cm long 3–11 mHz linear probe should be used with both B-mode real-time and extended-field-of-view (EFOV) techniques. Longitudinal B-mode and transverse EFOV images should be acquired during each exam, and analyzed with NIH-ImageJ software.

Conclusions

This operative protocol represents a good compromise between the feasibility of MUS in clinical settings and the need of obtaining precise measurements of muscle parameters. Future studies should verify the reproducibility of the proposed technique, and its correlation with appendicular lean mass and parameters of muscle function.

Keywords

Ultrasonography Skeletal muscle mass Sarcopenia Physical frailty Myopenia 

Notes

Acknowledgements

The ultrasonographic images of right vastus lateralis muscle were obtained using a portable ultrasound (MyLab Gamma™) by Esaote (Genova, Italy) equipped with an extended-field-of-view software (VPAN™). The operative protocol detailed in this paper has been elaborated in the context of an advanced training course on muscle ultrasound that Professor Marco V. Narici held at the University of Parma in November 2016 and January 2017. The authors wish to thank all the participants to the course and their tutors: Lara Bianchi, Prof. Stefano Volpato (University of Ferrara); Cesare Caliari, Stefano Gattazzo, Prof. Andrea Rossi (University of Verona); Anna Maria Dalise, Prof. Giuseppe Paolisso (University of Campania “Luigi Vanvitelli”, Naples); Christian Ferro, Prof. Francesco Corica (University of Messina); Alessandra Pratesi, Prof. Mauro Di Bari (University of Florence); Aurelio Lo Buglio, Lucia Barbera, Prof. Gaetano Serviddio, Prof Gianluigi Vendemmiale (University of Foggia); Costantino Caroselli, Prof. Antonio Cherubini, Prof. Fabrizia Lattanzio (Italian National Research Center on Aging, Ancona); Anna Maria Martone (Catholic University of the Sacred Heart, Rome); Giulia Mori, Nicoletta Cerundolo, Giacomo Bussolati, Erika Ciarrocchi, Chiara Guareschi, Alberto Fisichella, Prof. Gian Paolo Ceda (University of Parma). The authors also wish to thank Dr. Chiara Sidoli for assistance in literature review.

Funding

This study has been supported by a grant from the Cariparma Foundation (http://www.fondazionecrp.it) for implementation of muscle ultrasound techniques in the Geriatric-Rehabilitation Department of Parma University-Hospital.

Compliance with ethical standards

Conflict of interest

All the authors have no conflict of interest to declare.

Ethical approval

This paper does not contain data from human subjects, so Ethics Committee approval is not necessary.

Informed consent

For this kind of study, formal consent is not required.

References

  1. 1.
    Ticinesi A, Meschi T, Narici MV et al (2017) Muscle ultrasound and sarcopenia in older individuals: a clinical perspective. J Am Med Dir Assoc 18:290–300CrossRefGoogle Scholar
  2. 2.
    Cruz-Jentoft A, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on sarcopenia in older people. Age Ageing 39:412–423CrossRefGoogle Scholar
  3. 3.
    McLean RR, Shardell MD, Alley DE et al (2014) 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 69:576–583CrossRefGoogle Scholar
  4. 4.
    Cesari M, Landi F, Calvani R et al (2017) Rationale for a preliminary operational definition of physical frailty and sarcopenia in the SPRINTT trial. Aging Clin Exp Res 29:81–88CrossRefGoogle Scholar
  5. 5.
    Tosato M, Marzetti E, Cesari M et al (2017) Measurement of muscle mass in sarcopenia: from imaging to biochemical markers. Aging Clin Exp Res 29:19–27CrossRefGoogle Scholar
  6. 6.
    Leone AF, Schumacher SM, Krotish DE et al (2012) Geriatricians’ interest to learn bedside portable ultrasound (GEBUS) for application in the clinical practice and education. J Am Med Dir Assoc 13:308.e7–308.e10CrossRefGoogle Scholar
  7. 7.
    Ticinesi A, Lauretani F, Nouvenne A et al (2016) Lung ultrasound and chest X-ray for detecting pneumonia in an acute geriatric ward. Medicine 95:e4153CrossRefGoogle Scholar
  8. 8.
    Strasser EM, Draskovits T, Praschak M et al (2013) Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age 35:2377–2388CrossRefGoogle Scholar
  9. 9.
    Narici MV, Binzoni T, Hiltbrand E et al (1996) In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 496:289–297CrossRefGoogle Scholar
  10. 10.
    Narici M (1999) Human skeletal muscle architecture studied in vivo by non-invasive imaging techniques: functional significance and applications. J Electromyogr Kinesiol 9:97–103CrossRefGoogle Scholar
  11. 11.
    Esformes JI, Narici MV, Maganaris CN (2002) Measurement of human muscle volume using ultrasonography. Eur J Appl Physiol 87:90–92CrossRefGoogle Scholar
  12. 12.
    Narici MV, Maganaris CN, Reeves ND et al (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234CrossRefGoogle Scholar
  13. 13.
    Reeves ND, Maganaris CN, Narici MV (2004) Ultrasonographic assessment of human skeletal muscle size. Eur J Appl Physiol 91:116–118CrossRefGoogle Scholar
  14. 14.
    Agyapong-Badu S, Warner M, Samuel D et al (2014) Anterior thigh composition measured using ultrasound imaging to quantify relative thickness of muscle and non-contractile tissue: a potential biomarker for musculoskeletal health. Physiol Meas 35:2165–2176CrossRefGoogle Scholar
  15. 15.
    Narici M, Cerretelli P (1998) Changes in human muscle architecture in disuse-atrophy evaluated by ultrasound imaging. J Gravit Physiol 5:P73–P74PubMedGoogle Scholar
  16. 16.
    de Boer MD, Maganaris CN, Seynnes OR et al (2007) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091CrossRefGoogle Scholar
  17. 17.
    de Boer MD, Seynnes OR, di Prampero PE 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 104:401–407CrossRefGoogle Scholar
  18. 18.
    Reeves ND, Narici MV, Maganaris CN (2004) In vivo human muscle structure and function: adaptations to resistance training in old age. Exp Physiol 89:675–689CrossRefGoogle Scholar
  19. 19.
    Reeves ND, Maganaris CN, Longo S et al (2009) Differential adaptations to eccentric versus conventional resistance training in older humans. Exp Physiol 94:825–833CrossRefGoogle Scholar
  20. 20.
    Narici MV, Flueck M, Koesters A et al (2011) Skeletal muscle remodeling in response to alpine skiing training in older individuals. Scand J Med Sci Sports 21:23–28CrossRefGoogle Scholar
  21. 21.
    Franchi MV, Atherton PJ, Reeves ND et al (2014) Architectural, functional and molecular responses to concentric and eccentric loading in human skeletal muscle. Acta Physiol 210:642–654CrossRefGoogle Scholar
  22. 22.
    Franchi MV, Wilkinson DJ, Quinlan JI et al (2015) Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle. Physiol Rep 3:e12593CrossRefGoogle Scholar
  23. 23.
    Atkinson RA, Srinivas-Shankar U, Roberts SA et al (2011) Effects of testosterone on skeletal muscle architecture in intermediate-frail and frail elderly men. J Gerontol A Biol Sci Med Sci 65:1215–1219Google Scholar
  24. 24.
    Thom JM, Morse CI, Birch KM et al (2007) Influence of muscle architecture on the torque and power-velocity characteristics of young and elderly men. Eur J Appl Physiol 100:613–619CrossRefGoogle Scholar
  25. 25.
    Nijholt W, Scafoglieri A, Jager-Wittenaar H et al (2017) The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle 8:702–712CrossRefGoogle Scholar
  26. 26.
    Franchi MV, Longo S, Mallinson J et al (2018) Muscle thickness correlates to muscle cross-sectional area in the assessment of strength training-induced hypertrophy. Scand J Med Sci Sports 28:846–853CrossRefGoogle Scholar
  27. 27.
    Nielsen PK, Jensen BR, Darvann T et al (2006) Quantitative ultrasound tissue characterization in shoulder and thigh muscles—a new approach. BMC Musculoskelet Disord 7:2CrossRefGoogle Scholar
  28. 28.
    Barbat-Artigas S, Rolland Y, Vellas B et al (2013) Muscle quantity is not synonymous with muscle quality. J Am Med Dir Assoc 14:852.e1–852.e7CrossRefGoogle Scholar
  29. 29.
    Narici M, Franchi M, Maganaris C (2016) Muscle structural assembly and functional consequences. J Exp Biol 219:276–284CrossRefGoogle Scholar
  30. 30.
    Harris-Love MO, Monfaredi R, Ismail C et al (2014) Quantitative ultrasound: measurement considerations for the assessment of muscular dystrophy and sarcopenia. Front Aging Neurosci 6:172CrossRefGoogle Scholar
  31. 31.
    Narici MV, Maffulli N (2010) Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 95:139–159CrossRefGoogle Scholar
  32. 32.
    Minetto MA, Caresio C, Menapace T et al (2016) Ultrasound-based detection of low muscle mass for diagnosis of sarcopenia in older adults. PM R 8:453–462CrossRefGoogle Scholar
  33. 33.
    Noorkoiv M, Stavnsbo A, Aagaard P et al (2010) In vivo assessment of muscle fascicle length by extended field-of-view ultrasonography. J Appl Physiol 109:1974–1979CrossRefGoogle Scholar
  34. 34.
    Noorkoiv M, Nosaka K, Blazevich AJ (2010) Assessment of quadriceps muscle cross-sectional area by ultrasound extended-field-of-view imaging. Eur J Appl Physiol 109:631–639CrossRefGoogle Scholar
  35. 35.
    Education and Practical Standards Committee, European Federation of Societies for Ultrasound in Medicine and Biology (2006) Minimum training recommendations for the practice of medical ultrasound. Ultraschall Med 27:709–715Google Scholar
  36. 36.
    https://imagej.nih.gov/ij/. Accessed 8 Apr 2017
  37. 37.
    Janssen I, Heymsfield SB, Wang Z et al (2008) Skeletal muscle mass and distribution in 468 men and women aged 18–88 years. J Appl Physiol 89:81–88CrossRefGoogle Scholar
  38. 38.
    Abe T, Kawakami Y, Kondo M et al (2011) Comparison of ultrasound-measured age-related site-specific muscle loss between healthy Japanese and German men. Clin Physiol Funct Imaging 31:320–325CrossRefGoogle Scholar
  39. 39.
    Abe T, Sakamaki M, Yasuda T et al (2011) Age-related site-specific muscle loss in 1507 Japanese men and women aged 20 to 95 years. J Sports Sci Med 10:145–150PubMedPubMedCentralGoogle Scholar
  40. 40.
    Abe T, Thiebaud RS, Loenneke JP et al (2014) Prevalence of site-specific thigh sarcopenia in Japanese men and women. Age 36:417–426CrossRefGoogle Scholar
  41. 41.
    Abe T, Loenneke JP, Thiebaud RS et al (2014) Age-related site-specific muscle wasting of upper and lower extremities and trunk in Japanese men and women. Age 36:813–821CrossRefGoogle Scholar
  42. 42.
    Paris MT, Lafleur B, Dubin JA et al (2017) Development of a bedside viable ultrasound protocol to quantify appendicular lean mass. J Cachexia Sarcopenia Muscle 8:713–726CrossRefGoogle Scholar
  43. 43.
    Takai Y, Ohta M, Akagi R et al (2014) Applicability of ultrasound muscle thickness measurements for predicting fat-free mass in elderly population. J Nutr Health Aging 18:579–585CrossRefGoogle Scholar
  44. 44.
    Maddocks M, Nolan CM, Man WDC et al (2016) Neuromuscular electrical stimulation to improve exercise capacity in patients with severe COPD: a randomized double-blind, placebo-controlled trial. Lancet Respir Med 4:27–36CrossRefGoogle Scholar
  45. 45.
    Jenkins ND, Miller JM, Buckner SL et al (2015) Test-retest reliability of single transverse versus panoramic ultrasound imaging for muscle size and echo intensity of the biceps brachii. Ultrasound Med Biol 41:1584–1591CrossRefGoogle Scholar
  46. 46.
    Seymour JM, Ward K, Sidhu PS et al (2009) Ultrasound measurement of rectus femoris cross-sectional area and the relationship with quadriceps strength in COPD. Thorax 64:418–423CrossRefGoogle Scholar
  47. 47.
    Scott JM, Martin DS, Ploutz-Snyder R et al (2017) Panoramic ultrasound: a novel and valid tool for monitoring change in muscle mass. J Cachexia Sarcopenia Muscle 8:475–481CrossRefGoogle Scholar
  48. 48.
    Caresio C, Molinari F, Emanuel G et al (2015) Muscle echo intensity: reliability and conditioning factors. Clin Physiol Funct Imaging 35:493–503CrossRefGoogle Scholar
  49. 49.
    Pillen S, van Alfen N (2011) Skeletal muscle ultrasound. Neurol Res 33:1016–1024CrossRefGoogle Scholar
  50. 50.
    Rech A, Radaelli R, Goltz FR et al (2014) Echo intensity is negatively associated with functional capacity in older women. Age 36:9708CrossRefGoogle Scholar
  51. 51.
    Wilhelm EN, Rech A, Minozzo F et al (2014) Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity in older men. Age 36:9625CrossRefGoogle Scholar
  52. 52.
    Tillquist M, Kutsogiannis DJ, Wischmeyer PE et al (2014) Bedside ultrasound is a practical and reliable measurement tool for assessing quadriceps muscle layer thickness. JPEN 38:886–890CrossRefGoogle Scholar
  53. 53.
    Sabatino A, Regolisti G, Bozzoli L et al (2017) Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. Clin Nutr 36:1710–1715CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Andrea Ticinesi
    • 1
    • 2
  • Marco V. Narici
    • 3
  • Fulvio Lauretani
    • 1
    • 2
  • Antonio Nouvenne
    • 1
    • 2
  • Elena Colizzi
    • 1
  • Marco Mantovani
    • 1
  • Andrea Corsonello
    • 4
  • Francesco Landi
    • 5
  • Tiziana Meschi
    • 1
    • 2
  • Marcello Maggio
    • 1
    • 2
  1. 1.Department of Medicine and SurgeryUniversity of ParmaParmaItaly
  2. 2.Geriatric-Rehabilitation DepartmentParma University HospitalParmaItaly
  3. 3.Institute of Physiology, Department of Biomedical SciencesUniversity of PadovaPaduaItaly
  4. 4.Unit of Geriatric PharmacoepidemiologyItalian National Research Center on Aging (INRCA)CosenzaItaly
  5. 5.Department of Geriatrics, Neurosciences and Orthopedics, Center for Geriatric Medicine (CEMI), Institute of Internal Medicine and GeriatricsCatholic University of the Sacred HeartRomeItaly

Personalised recommendations