{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T22:31:51Z","timestamp":1790721111399,"version":"4.1.0"},"reference-count":33,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,6,29]],"date-time":"2021-06-29T00:00:00Z","timestamp":1624924800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Novel ultrasound (US) methods are required to assess qualitative changes in the quadriceps rectus femoris (QRF) muscle when evaluating mechanically ventilated, long-stay ICU patients with suspected neuromuscular acquired weakness (ICUAW). Our aim was to analyze novel US muscle assessment methods in these patients versus healthy controls by carrying out a prospective observational study. Shear wave elastography (SWE) showed, with a receiver operating characteristic (ROC) curve of 0.972 (95% confidence interval (CI) = 0.916\u20131.000), that patients increased muscle stiffness associated with muscle fibrosis when diagnosed with ICUAW. We also performed, for the first time, superb microvascular imaging (SMI), which is an innovative US technique designed for imaging microvascularization unseen with color Doppler US, and observed that 53.8% of cases had significantly lower QRF muscle microvascular angiogenic activity than controls (p &lt; 0.001). Finally, we used contrast-enhanced ultrasound (CEUS) to analyze maximum and minimum QRF muscle perfusion and obtained a ROC curve of 0.8, but when used as markers for SMI, their diagnostic capacity increased to 0.988 (CI = 0.965\u20131) and 0.932 (CI = 0.858\u20131), respectively. These findings show, for the first time, that these novel sonographic muscle methods should be used for their diagnostic capacity when assessing sarcopenic processes associated with this group of critically ill patients.<\/jats:p>","DOI":"10.3390\/nu13072224","type":"journal-article","created":{"date-parts":[[2021,6,29]],"date-time":"2021-06-29T04:31:07Z","timestamp":1624941067000},"page":"2224","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Novel High-Quality Sonographic Methods to Diagnose Muscle Wasting in Long-Stay Critically Ill Patients: Shear Wave Elastography, Superb Microvascular Imaging and Contrast-Enhanced Ultrasound"],"prefix":"10.3390","volume":"13","author":[{"given":"Carmen Rosa","family":"Hern\u00e1ndez-Socorro","sequence":"first","affiliation":[{"name":"Department of Radiology, Hospital Universitario de Gran Canaria Dr. Negr\u00edn, Universidad de Las Palmas de Gran Canaria, Barranco de la Ballena s\/n, 35010 Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pedro","family":"Saavedra","sequence":"additional","affiliation":[{"name":"Department of Mathematics, Universidad de Las Palmas de Gran Canaria, 35010 Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan Carlos","family":"L\u00f3pez-Fern\u00e1ndez","sequence":"additional","affiliation":[{"name":"Department of Neurology, Hospital Universitario de Gran Canaria Dr. Negr\u00edn, Universidad de Las Palmas de Gran Canaria, Barranco de la Ballena s\/n, 35010 Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federico","family":"L\u00fcbbe-Vazquez","sequence":"additional","affiliation":[{"name":"Department of Intensive Care, Hospital Universitario de Gran Canaria Dr. Negr\u00edn, Barranco de la Ballena s\/n, 35010 Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3927-3236","authenticated-orcid":false,"given":"Sergio","family":"Ruiz-Santana","sequence":"additional","affiliation":[{"name":"Department of Intensive Care, Hospital Universitario de Gran Canaria Dr. Negr\u00edn, Universidad de Las Palmas de Gran Canaria, Barranco de la Ballena s\/n, 35010 Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Viana, M.V., Pantet, O., Bagnoud, G., Martinez, A., Favre, E., Charri\u00e8re, M., Favre, D., Eckert, P., and Berger, M.M. (2019). Metabolic and nutritional characteristics of long-stay critically ill patients. J. Clin. Med., 8.","DOI":"10.3390\/jcm8070985"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.4187\/respcare.05485","article-title":"Variation in definition of prolonged mechanical ventilation","volume":"62","author":"Rose","year":"2017","journal-title":"Respir. Care"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1097\/CCM.0000000000000710","article-title":"ProVent study group investigators. The epidemiology of chronic critical illness in the United States","volume":"43","author":"Kahn","year":"2015","journal-title":"Crit. Care Med."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Hern\u00e1ndez-Socorro, C.R., Saavedra, P., Lopez-Fernandez, J.C., and Ruiz-Santana, S. (2018). Assessment of muscle wasting in long-stay ICU patients using a new ultrasound protocol. Nutrients, 10.","DOI":"10.3390\/nu10121849"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1148\/radiol.2015142212","article-title":"Skeletal muscle in healthy subjects versus those with GNE-related myopathy: Evaluation with shear wave US\u2014A pilot study","volume":"277","author":"Carpenter","year":"2015","journal-title":"Radiology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1495","DOI":"10.1513\/AnnalsATS.201612-967PS","article-title":"Skeletal muscle ultrasound in critical care: A tool in need of translation","volume":"14","author":"Mourtzakis","year":"2017","journal-title":"Ann. Am. Thorac. Soc"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1055\/a-0838-9937","article-title":"The EFSUMB guidelines and recommendations for the clinical practice of elastography in non-hepatic applications: Update 2018","volume":"40","author":"Gilja","year":"2019","journal-title":"Ultraschall. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1906","DOI":"10.1109\/TUFFC.2016.2591963","article-title":"Shear wave measurements for evaluation of tendon diseases","volume":"63","author":"Yeh","year":"2016","journal-title":"IEEE Trans. Ultrason. Ferroelectr. Freq. Control"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1097\/MD.0000000000001502","article-title":"The diagnostic value of superb microvascular imaging (SMI) in detecting blood flow signals of breast lesions. A preliminary study comparing SMI to color doppler flow imaging","volume":"94","author":"Ma","year":"2015","journal-title":"Medicine"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3025","DOI":"10.1002\/jum.15010","article-title":"Differentiation between malignant and benign lymph nodes: Role of superb microvascular imaging in the evaluation of cervical lymph nodes","volume":"38","author":"Sim","year":"2019","journal-title":"J. Ultrasound Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1186\/s40644-019-0277-6","article-title":"Superb microvascular imaging technique in depicting vascularity in focal liver lesions: More hypervascular supply patterns were depicted in hepatocellular carcinoma","volume":"30","author":"Yang","year":"2019","journal-title":"Cancer Imaging"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e00119","DOI":"10.1002\/phy2.119","article-title":"Development of a new Sonovue TM contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding","volume":"1","author":"Mitchell","year":"2013","journal-title":"Physiol. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1186\/s13054-015-0993-7","article-title":"Clinical review: Intensive care unit acquired weakness","volume":"19","author":"Hermans","year":"2015","journal-title":"Crit. Care"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1097\/MCO.0000000000000150","article-title":"Muscle weakness and nutrition therapy in ICU","volume":"18","author":"Casaer","year":"2015","journal-title":"Curr. Opin. Nutr. Metab. Care"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1016\/j.chest.2016.06.006","article-title":"ICU-acquired weakness: A rehabilitation perspective of diagnosis, treatment, and functional management","volume":"150","author":"Zorowitz","year":"2016","journal-title":"Chest"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/s13613-017-0263-8","article-title":"Diagnostic accuracy of quantitative neuromuscular ultrasound for the diagnosis of intensive care unit-acquired weakness: A cross-sectional observational study","volume":"7","author":"Witteveen","year":"2017","journal-title":"Ann. Intensive Care"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/cc10005","article-title":"Manual muscle strength testing of critically ill patients: Feasibility and interobserver agreement","volume":"15","author":"Hough","year":"2011","journal-title":"Crit. Care"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.pmr.2011.11.009","article-title":"Neuromuscular ultrasonography: Quantifying muscle and nerve measurements","volume":"23","author":"Mayans","year":"2012","journal-title":"Phys. Med. Rehabil. Clin."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1016\/j.cgh.2016.04.040","article-title":"A model to identify sarcopenia in patients with cirrhosis","volume":"14","author":"Tandon","year":"2016","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2377","DOI":"10.1007\/s11357-013-9517-z","article-title":"Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly","volume":"35","author":"Strasse","year":"2013","journal-title":"Age"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Yoo, M.H., Kim, H.J., Choi, I.H., Park, S., Kim, S.J., Park, H.K., Byun, D.W., and Suh, K. (2020). Shear wave elasticity by tracing total nodule showed high reproducibility and concordance with fibrosis in thyroid cancer. BMC Cancer, 20.","DOI":"10.1186\/s12885-019-6437-z"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1001\/jama.2013.278481","article-title":"Acute skeletal muscle wasting in critical illness","volume":"16","author":"Puthucheary","year":"2013","journal-title":"JAMA"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1164\/rccm.201604-0875LE","article-title":"Rectus femoris cross-sectional area and muscle layer thickness: Comparative markers of muscle wasting and weakness","volume":"195","author":"Puthucheary","year":"2017","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/cc13050","article-title":"Muscle ultrasound for early assessment of critical illness neuromyopathy in severe sepsis","volume":"17","author":"Grimm","year":"2013","journal-title":"Crit. Care"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1002\/ncp.10230","article-title":"Body composition technology: Implications for the ICU","volume":"34","author":"Mundi","year":"2019","journal-title":"Nutr. Clin. Pract."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1186\/s13054-016-1563-3","article-title":"Skeletal muscle quality as assessed by CT-derived skeletal muscle density is associated with 6-month mortality in mechanically ventilated critically ill patients","volume":"20","author":"Looijaard","year":"2016","journal-title":"Crit. Care"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1002\/jpen.1719","article-title":"Early detection of muscle weakness and functional limitations in the critically ill: A retrospective evaluation of bioimpedance spectroscopy","volume":"44","author":"Baldwin","year":"2020","journal-title":"J. Parenter. Enter. Nutr."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Wandrag, L., Brett, S.J., Frost, G.S., Bountziouka, V., and Hickson, M. (2019). Exploration of muscle loss and metabolic state during prolonged critical illness: Implications for intervention?. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0224565"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1186\/s13054-020-2745-6","article-title":"Real-time shear wave ultrasound elastography: A new tool for the evaluation of diaphragm and limb muscle stiffness in critically ill patients","volume":"24","author":"Flattres","year":"2020","journal-title":"Crit. Care"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1109\/TUFFC.2004.1295425","article-title":"Supersonic shear imaging: A new technique for soft tissue elasticity mapping","volume":"51","author":"Bercoff","year":"2004","journal-title":"IEEE Trans. Ultrason. Ferroelectr. Freq. Control"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1148\/radiol.10090385","article-title":"Breast lesions: Quantitative elastography with supersonic shear imaging\u2014Preliminary results","volume":"256","author":"Athanasiou","year":"2010","journal-title":"Radiology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1111\/jgh.14782","article-title":"Comparing point shear wave elastography (ElastPQ) and transient elastography for diagnosis of fibrosis stage in non-alcoholic fatty liver disease","volume":"35","author":"Leong","year":"2020","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4535","DOI":"10.12659\/MSM.915252","article-title":"Utility of contrast-enhanced ultrasound for the assessment of skeletal muscle perfusion in diabetes mellitus: A meta-analysis","volume":"25","author":"Chen","year":"2019","journal-title":"Med. Sci. Monit."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/7\/2224\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:26:22Z","timestamp":1760163982000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/7\/2224"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,29]]},"references-count":33,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["nu13072224"],"URL":"https:\/\/doi.org\/10.3390\/nu13072224","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,29]]}}}