Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
Critical Care
Published in: Critical Care 1/2020

Open Access 01-12-2020 | Ultrasound | Research

Real-time shear wave ultrasound elastography: a new tool for the evaluation of diaphragm and limb muscle stiffness in critically ill patients

Authors: Aurelien Flatres, Yassir Aarab, Stephanie Nougaret, Fanny Garnier, Romaric Larcher, Mathieu Amalric, Kada Klouche, Pascal Etienne, Gilles Subra, Samir Jaber, Nicolas Molinari, Stefan Matecki, Boris Jung

Published in: Critical Care | Issue 1/2020

Login to get access

Abstract

Background

Muscle weakness following critical illness is the consequence of loss of muscle mass and alteration of muscle quality. It is associated with long-term disability. Ultrasonography is a reliable tool to quantify muscle mass, but studies that evaluate muscle quality at the critically ill bedside are lacking. Shear wave ultrasound elastography (SWE) provides spatial representation of soft tissue stiffness and measures of muscle quality. The reliability and reproducibility of SWE in critically ill patients has never been evaluated.

Methods

Two operators tested in healthy controls and in critically ill patients the intra- and inter-operator reliability of the SWE using transversal and longitudinal views of the diaphragm and limb muscles. Reliability was calculated using the intra-class correlation coefficient and a bootstrap sampling method assessed their consistency.

Results

We collected 560 images. Longitudinal views of the diaphragm (ICC 0.83 [0.50–0.94]), the biceps brachii (ICC 0.88 [0.67–0.96]) and the rectus femoris (ICC 0.76 [0.34–0.91]) were the most reliable views in a training set of healthy controls. Intra-class correlation coefficient for inter-operator reproducibility and intra-operator reliability was above 0.9 for all muscles in a validation set of healthy controls. In critically ill patients, inter-operator reproducibility and intra-operator 1 and 2 reliability ICCs were respectively 0.92 [0.71–0.98], 0.93 [0.82–0.98] and 0.92 [0.81–0.98] for the diaphragm; 0.96 [0.86–0.99], 0.98 [0.94–0.99] and 0.99 [0.96–1] for the biceps brachii and 0.91 [0.51–0.98], 0.97 [0.93–0.99] and 0.99 [0.97–1] for the rectus femoris. The probability to reach intra-class correlation coefficient greater than 0.8 in a 10,000 bootstrap sampling for inter-operator reproducibility was respectively 81%, 84% and 78% for the diaphragm, the biceps brachii and the rectus femoris respectively.

Conclusions

SWE is a reliable technique to evaluate limb muscles and the diaphragm in both healthy controls and in critically ill patients.

Trial registration

The study was registered (ClinicalTrial NCT03550222).
Literature
1.
Herridge MS, Chu LM, Matte A, Tomlinson G, Chan L, Thomas C, et al. The RECOVER program: disability risk groups and 1-year outcome after 7 or more days of mechanical ventilation. Am J Respir Crit Care Med. 2016;194:831–44.PubMed
2.
Iwashyna TJ, Ely EW, Smith DM, Langa KM. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA. 2010;304:1787–94.PubMedPubMedCentral
3.
Hodgson CL, Haines KJ, Bailey M, Barrett J, Bellomo R, Bucknall T, et al. Predictors of return to work in survivors of critical illness. J Crit Care. 2018;48:21–5.PubMed
4.
Jung B, Moury PH, Mahul M, de Jong A, Galia F, Prades A, et al. Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med. 2016;42:853–61.PubMed
5.
Jaber S, Petrof BJ, Jung B, Chanques G, Berthet J-P, Rabuel C, et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med. 2011;183:364–71.PubMed
6.
Matecki S, Dridi H, Jung B, Saint N, Reiken SR, Scheuermann V, et al. Leaky ryanodine receptors contribute to diaphragmatic weakness during mechanical ventilation. Proc Natl Acad Sci U S A. 2016;113:9069–74.PubMedPubMedCentral
7.
Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310:1591–600.PubMed
8.
Herridge MS, Tansey CM, Matté A, Tomlinson G, Diaz-Granados N, Cooper A, et al. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med. 2011;364:1293–304.PubMed
9.
Hermans G, Van Mechelen H, Clerckx B, Vanhullebusch T, Mesotten D, Wilmer A, et al. Acute outcomes and 1-year mortality of intensive care unit–acquired weakness. A cohort study and propensity-matched analysis. Am J Respir Crit Care Med. 2014;190:410–20.PubMed
10.
TEAM Study Investigators, Hodgson C, Bellomo R, Berney S, Bailey M, Buhr H, et al. Early mobilization and recovery in mechanically ventilated patients in the ICU: a bi-national, multi-centre, prospective cohort study. Crit Care. 2015;19:81.
11.
Dres M, Jung B, Molinari N, Manna F, Dubé B-P, Chanques G, et al. Respective contribution of intensive care unit-acquired limb muscle and severe diaphragm weakness on weaning outcome and mortality: a post hoc analysis of two cohorts. Crit Care. 2019;23:370.PubMedPubMedCentral
12.
Demoule A, Jung B, Prodanovic H, Molinari N, Chanques G, Coirault C, et al. Diaphragm dysfunction on admission to the intensive care unit. Prevalence, risk factors, and prognostic impact-a prospective study. Am J Respir Crit Care Med. 2013;188:213–9.PubMed
13.
14.
Dres M, Demoule A. Diaphragm dysfunction during weaning from mechanical ventilation: an underestimated phenomenon with clinical implications. Crit Care Lond Engl. 2018;22:73.
15.
Dos Santos C, Hussain SNA, Mathur S, Picard M, Herridge M, Correa J, et al. Mechanisms of chronic muscle wasting and dysfunction after an intensive care unit stay. A pilot study. Am J Respir Crit Care Med. 2016;194:821–30.PubMed
16.
Souweine J-S, Kuster N, Chenine L, Rodriguez A, Patrier L, Morena M, et al. Physical inactivity and protein energy wasting play independent roles in muscle weakness in maintenance haemodialysis patients. PLoS One. 2018;13:e0200061.PubMedPubMedCentral
17.
Bunnell A, Ney J, Gellhorn A, Hough CL. Quantitative neuromuscular ultrasound in intensive care unit-acquired weakness: a systematic review. Muscle Nerve. 2015;52:701–8.PubMedPubMedCentral
18.
Pillen S, Van Alfen N. Muscle ultrasound from diagnostic tool to outcome measure--quantification is the challenge. Muscle Nerve. 2015;52:319–20.PubMed
19.
O’brien TG, Cazares Gonzalez ML, Ghosh PS, Mandrekar J, Boon AJ. Reliability of a novel ultrasound system for gray-scale analysis of muscle. Muscle Nerve. 2017;56:408–12.PubMed
20.
Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control. 2004;51:396–409.PubMed
21.
Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas J-M, Gilja OH, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med Stuttg Ger 1980. 2013;34:238–53.
22.
Carpenter EL, Lau HA, Kolodny EH, Adler RS. Skeletal muscle in healthy subjects versus those with GNE-related myopathy: evaluation with shear-wave US--a pilot study. Radiology. 2015;277:546–54.PubMed
23.
Bachasson D, Dres M, Niérat M-C, Gennisson J-L, Hogrel J-Y, Doorduin J, et al. Diaphragm shear modulus reflects transdiaphragmatic pressure during isovolumetric inspiratory efforts and ventilation against inspiratory loading. J Appl Physiol 1985. 2019;126:699–707.PubMed
24.
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370:1453–7.PubMed
25.
Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça A, Bruining H, et al. The SOFA (sepsis-related organ failure assessment) score to describe organ dysfunction/failure. On behalf of the working group on sepsis-related problems of the European Society of Intensive Care Medicine. Intensive Care Med. 1996;22:707–10.PubMed
26.
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;8:702–12.PubMedPubMedCentral
27.
Taljanovic MS, Gimber LH, Becker GW, Latt LD, Klauser AS, Melville DM, et al. Shear-wave elastography: basic physics and musculoskeletal applications. Radiogr Rev Publ Radiol Soc N Am Inc. 2017;37:855–70.
28.
Parry SM, El-Ansary D, Cartwright MS, Sarwal A, Berney S, Koopman R, et al. Ultrasonography in the intensive care setting can be used to detect changes in the quality and quantity of muscle and is related to muscle strength and function. J Crit Care. 2015;30:1151.e9–14.
29.
Fischer A, Spiegl M, Altmann K, Winkler A, Salamon A, Themessl-Huber M, et al. Muscle mass, strength and functional outcomes in critically ill patients after cardiothoracic surgery: does neuromuscular electrical stimulation help? The Catastim 2 randomized controlled trial. Crit Care. 2016;20:30.PubMedPubMedCentral
30.
Goligher EC, Fan E, Herridge MS, Murray A, Vorona S, Brace D, et al. Evolution of diaphragm thickness during mechanical ventilation. Impact of inspiratory effort. Am J Respir Crit Care Med. 2015;192:1080–8.PubMed
31.
Zambon M, Beccaria P, Matsuno J, Gemma M, Frati E, Colombo S, et al. Mechanical ventilation and diaphragmatic atrophy in critically ill patients: an ultrasound study. Crit Care Med. 2016;44:1347–52.PubMed
32.
Schepens T, Verbrugghe W, Dams K, Corthouts B, Parizel PM, Jorens PG. The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care. 2015;19:422.PubMedPubMedCentral
33.
Mourtzakis M, Parry S, Connolly B, Puthucheary Z. Skeletal muscle ultrasound in critical care: a tool in need of translation. Ann Am Thorac Soc. 2017;14:1495–503.PubMedPubMedCentral
34.
Creze M, Nordez A, Soubeyrand M, Rocher L, Maître X, Bellin M-F. Shear wave sonoelastography of skeletal muscle: basic principles, biomechanical concepts, clinical applications, and future perspectives. Skelet Radiol. 2018;47:457–71.
35.
Lacourpaille L, Hug F, Guével A, Péréon Y, Magot A, Hogrel J-Y, et al. Non-invasive assessment of muscle stiffness in patients with Duchenne muscular dystrophy. Muscle Nerve. 2015;51:284–6.PubMed
36.
Taş S, Onur MR, Yılmaz S, Soylu AR, Korkusuz F. Shear wave elastography is a reliable and repeatable method for measuring the elastic modulus of the rectus femoris muscle and patellar tendon: shear wave elastography of the rectus femoris muscle and patellar tendon. J Ultrasound Med. 2017;36:565–70.PubMed
37.
Dorado Cortez C, Hermitte L, Ramain A, Mesmann C, Lefort T, Pialat JB. Ultrasound shear wave velocity in skeletal muscle: a reproducibility study. Diagn Interv Imaging. 2016;97:71–9.PubMed
38.
Du L-J, He W, Cheng L-G, Li S, Pan Y-S, Gao J. Ultrasound shear wave elastography in assessment of muscle stiffness in patients with Parkinson’s disease: a primary observation. Clin Imaging. 2016;40:1075–80.PubMed
39.
Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med. 2008;358:1327–35.PubMed
40.
Hooijman PE, Beishuizen A, Witt CC, de Waard MC, Girbes ARJ, Spoelstra-de Man AME, et al. Diaphragm muscle fiber weakness and ubiquitin–proteasome activation in critically ill patients. Am J Respir Crit Care Med. 2015;191:1126–38.PubMedPubMedCentral
41.
Dres M, Goligher EC, Heunks LMA, Brochard LJ. Critical illness-associated diaphragm weakness. Intensive Care Med. 2017;43:1441–52.PubMed
42.
Goligher EC, Brochard LJ, Reid WD, Fan E, Saarela O, Slutsky AS, et al. Diaphragmatic myotrauma: a mediator of prolonged ventilation and poor patient outcomes in acute respiratory failure. Lancet Respir Med. 2019;7:90–8.PubMed
43.
Chino K, Ohya T, Katayama K, Suzuki Y. Diaphragmatic shear modulus at various submaximal inspiratory mouth pressure levels. Respir Physiol Neurobiol. 2018;252–253:52–7.PubMed
44.
Alfuraih AM, O’Connor P, Hensor E, Tan AL, Emery P, Wakefield RJ. The effect of unit, depth, and probe load on the reliability of muscle shear wave elastography: variables affecting reliability of SWE. J Clin Ultrasound JCU. 2018;46:108–15.PubMed
Metadata
Title
Real-time shear wave ultrasound elastography: a new tool for the evaluation of diaphragm and limb muscle stiffness in critically ill patients
Authors
Aurelien Flatres
Yassir Aarab
Stephanie Nougaret
Fanny Garnier
Romaric Larcher
Mathieu Amalric
Kada Klouche
Pascal Etienne
Gilles Subra
Samir Jaber
Nicolas Molinari
Stefan Matecki
Boris Jung
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Critical Care / Issue 1/2020
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/s13054-020-2745-6

Other articles of this Issue 1/2020

Critical Care 1/2020 Go to the issue

Research Letter

Effect of favipiravir and an anti-inflammatory strategy for COVID-19

Viewpoint

Nutritional support in sepsis: when less may be more

Letter

Hemoadsorption of cytokines by CytoSorb filter: a simulation study without human factor—pilot is the difference

Letter

Medical Research Council-sumscore: a tool for evaluating muscle weakness in patients with post-intensive care syndrome

Review

Physiology of the Respiratory Drive in ICU Patients: Implications for Diagnosis and Treatment

Letter

New-onset atrial fibrillation can be falsely associated with increased length of stay in ICU due to immortal time bias