CT Scan-Derived Muscle, But Not Fat, Area Independently Predicts Mortality in COVID-19

Abstract

BackgroundCOVID-19 has demonstrated a highly variable disease course, from asymptomatic to severe illness and eventually death. Clinical parameters, as included in the 4C Mortality Score, can predict mortality accurately in COVID-19. Additionally, CT scan-derived low muscle and high adipose tissue cross-sectional areas (CSAs) have been associated with adverse outcomes in COVID-19.Research QuestionAre CT scan-derived muscle and adipose tissue CSAs associated with 30-day in-hospital mortality in COVID-19, independent of 4C Mortality Score?Study Design and MethodsThis was a retrospective cohort analysis of patients with COVID-19 seeking treatment at the ED of two participating hospitals during the first wave of the pandemic. Skeletal muscle and adipose tissue CSAs were collected from routine chest CT-scans at admission. Pectoralis muscle CSA was demarcated manually at the fourth thoracic vertebra, and skeletal muscle and adipose tissue CSA was demarcated at the first lumbar vertebra level. Outcome measures and 4C Mortality Score items were retrieved from medical records.ResultsData from 578 patients were analyzed (64.6% men; mean age, 67.7 ± 13.5 years; 18.2% 30-day in-hospital mortality). Patients who died within 30 days demonstrated lower pectoralis CSA (median, 32.6 [interquartile range (IQR), 24.3-38.8] vs 35.4 [IQR, 27.2-44.2]; P = .002) than survivors, whereas visceral adipose tissue CSA was higher (median, 151.1 [IQR, 93.6-219.7] vs 112.9 [IQR, 63.7-174.1]; P = .013). In multivariate analyses, low pectoralis muscle CSA remained associated with 30-day in-hospital mortality when adjusted for 4C Mortality Score (hazard ratio, 0.98; 95% CI, 0.96-1.00; P = .038).InterpretationCT scan-derived low pectoralis muscle CSA is associated significantly with higher 30-day in-hospital mortality in patients with COVID-19 independently of the 4C Mortality Score. COVID-19 has demonstrated a highly variable disease course, from asymptomatic to severe illness and eventually death. Clinical parameters, as included in the 4C Mortality Score, can predict mortality accurately in COVID-19. Additionally, CT scan-derived low muscle and high adipose tissue cross-sectional areas (CSAs) have been associated with adverse outcomes in COVID-19. Are CT scan-derived muscle and adipose tissue CSAs associated with 30-day in-hospital mortality in COVID-19, independent of 4C Mortality Score? This was a retrospective cohort analysis of patients with COVID-19 seeking treatment at the ED of two participating hospitals during the first wave of the pandemic. Skeletal muscle and adipose tissue CSAs were collected from routine chest CT-scans at admission. Pectoralis muscle CSA was demarcated manually at the fourth thoracic vertebra, and skeletal muscle and adipose tissue CSA was demarcated at the first lumbar vertebra level. Outcome measures and 4C Mortality Score items were retrieved from medical records. Data from 578 patients were analyzed (64.6% men; mean age, 67.7 ± 13.5 years; 18.2% 30-day in-hospital mortality). Patients who died within 30 days demonstrated lower pectoralis CSA (median, 32.6 [interquartile range (IQR), 24.3-38.8] vs 35.4 [IQR, 27.2-44.2]; P = .002) than survivors, whereas visceral adipose tissue CSA was higher (median, 151.1 [IQR, 93.6-219.7] vs 112.9 [IQR, 63.7-174.1]; P = .013). In multivariate analyses, low pectoralis muscle CSA remained associated with 30-day in-hospital mortality when adjusted for 4C Mortality Score (hazard ratio, 0.98; 95% CI, 0.96-1.00; P = .038). CT scan-derived low pectoralis muscle CSA is associated significantly with higher 30-day in-hospital mortality in patients with COVID-19 independently of the 4C Mortality Score. FOR EDITORIAL COMMENT, SEE PAGE 269Take-home PointsStudy Question: Are CT scan-derived muscle and adipose tissue cross-sectional areas (CSAs) associated with 30-day in-hospital mortality in patients with COVID-19, independent of 4C Mortality Score?Results: In multivariate analyses, low pectoralis muscle CSA was associated with 30-day in-hospital mortality when adjusted for 4C Mortality Score.Interpretation: Low CT scan-derived pectoralis muscle CSA is associated significantly with higher 30-day in-hospital mortality in patients with COVID-19 independently of the 4C Mortality Score. FOR EDITORIAL COMMENT, SEE PAGE 269 Study Question: Are CT scan-derived muscle and adipose tissue cross-sectional areas (CSAs) associated with 30-day in-hospital mortality in patients with COVID-19, independent of 4C Mortality Score? Results: In multivariate analyses, low pectoralis muscle CSA was associated with 30-day in-hospital mortality when adjusted for 4C Mortality Score. Interpretation: Low CT scan-derived pectoralis muscle CSA is associated significantly with higher 30-day in-hospital mortality in patients with COVID-19 independently of the 4C Mortality Score. COVID-19 caused by the SARS-CoV-2 presents with a highly variable disease course varying from asymptomatic disease to severe illness requiring hospitalization, ICU admission, mechanical ventilation, and eventually death.1Chen S. Sun H. Heng M. et al.Factors predicting progression to severe COVID-19: a competing risk survival analysis of 1753 patients in community isolation in Wuhan, China.Engineering (Beijing). 2022; 13: 99-106PubMed Google Scholar,2Adjei S. Hong K. Molinari N.M. et al.Mortality risk among patients hospitalized primarily for COVID-19 during the omicron and delta variant pandemic periods—United States, April 2020-June 2022.MMWR Morb Mortal Wkly Rep. 2022; 71: 1182-1189Crossref PubMed Scopus (50) Google Scholar However, the high prevalence of SARS-CoV-2 infections resulted in very high absolute numbers of severely ill patients requiring hospitalization and high mortality rates of up to 20% to 25% in several European regions, putting a high burden on hospitals and health-care systems worldwide.3Nijman G. Wientjes M. 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Endorsed by the Society of Thoracic Radiology, the American College of Radiology, and RSNA—Secondary Publication.J Thorac Imaging. 2020; 35: 219-227Crossref PubMed Scopus (429) Google Scholar, 6Bai Y. Yao L. Wei T. et al.Presumed asymptomatic carrier transmission of COVID-19.JAMA. 2020; 323: 1406-1407Crossref PubMed Scopus (2950) Google Scholar, 7Prokop M. van Everdingen W. van Rees Vellinga T. et al.CO-RADS: a categorical CT assessment scheme for patients suspected of having COVID-19—definition and evaluation.Radiology. 2020; 296: E97-E104Crossref PubMed Scopus (528) Google Scholar, 8Schalekamp S. Bleeker-Rovers C.P. Beenen L.F.M. et al.Chest CT in the emergency department for diagnosis of COVID-19 pneumonia: Dutch experience.Radiology. 2021; 298: E98-E106Crossref PubMed Google Scholar Based on systematic classification of intrapulmonary abnormalities, these chest CT scans can provide a likelihood of COVID-19 with high diagnostic accuracy.7Prokop M. van Everdingen W. van Rees Vellinga T. et al.CO-RADS: a categorical CT assessment scheme for patients suspected of having COVID-19—definition and evaluation.Radiology. 2020; 296: E97-E104Crossref PubMed Scopus (528) Google Scholar, 8Schalekamp S. Bleeker-Rovers C.P. Beenen L.F.M. et al.Chest CT in the emergency department for diagnosis of COVID-19 pneumonia: Dutch experience.Radiology. 2021; 298: E98-E106Crossref PubMed Google Scholar, 9Liu G. Chen Y. Runa A. Liu J. Diagnostic performance of CO-RADS for COVID-19: a systematic review and meta-analysis.Eur Radiol. 2022; 32: 4414-4426Crossref PubMed Scopus (5) Google Scholar, 10Turcato G. Zaboli A. Panebianco L. et al.Clinical application of the COVID-19 Reporting and Data System (CO-RADS) in patients with suspected SARS-CoV-2 infection: observational study in an emergency department.Clin Radiol. 2021; 76: 74 e23-74 e29Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar Next to the pulmonary abnormalities, CT scans contain relevant information on muscle and adipose tissue mass and distribution.11Shen W. Punyanitya M. Wang Z. et al.Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image.J Appl Physiol (1985). 2004; 97: 2333-2338Crossref PubMed Scopus (1155) Google Scholar Quantification of muscle cross-sectional area (CSA) at the level of the third lumbar vertebra is considered the reference for estimating whole body muscle mass.11Shen W. Punyanitya M. Wang Z. et al.Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image.J Appl Physiol (1985). 2004; 97: 2333-2338Crossref PubMed Scopus (1155) Google Scholar,12Tolonen A. Pakarinen T. Sassi A. et al.Methodology, clinical applications, and future directions of body composition analysis using computed tomography (CT) images: a review.Eur J Radiol. 2021; 145109943Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar However, analyses at higher vertebral levels available on chest CT scan images, for example, at the level of the first lumbar vertebra or the pectoralis muscle, also recently were validated for assessment of clinically relevant muscle mass.12Tolonen A. Pakarinen T. Sassi A. et al.Methodology, clinical applications, and future directions of body composition analysis using computed tomography (CT) images: a review.Eur J Radiol. 2021; 145109943Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar,13Sanders K.J.C. Degens J. Dingemans A.C. Schols A. Cross-sectional and longitudinal assessment of muscle from regular chest computed tomography scans: L1 and pectoralis muscle compared to L3 as reference in non-small cell lung cancer.Int J Chron Obstruct Pulmon Dis. 2019; 14: 781-789Crossref PubMed Scopus (14) Google Scholar Additionally, the levels of first and third lumbar vertebrae appeared to be comparable for assessment of adipose tissue mass and distribution.12Tolonen A. Pakarinen T. Sassi A. et al.Methodology, clinical applications, and future directions of body composition analysis using computed tomography (CT) images: a review.Eur J Radiol. 2021; 145109943Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar Therefore, chest CT scans obtained for the diagnosis and assessment of severity of pulmonary involvement also can be used to gain insight into body composition of these patients. Multiple authors have investigated the possible prognostic value of CT scan-derived body composition parameters on COVID-19 outcomes.14Siahaan Y.M.T. Hartoyo V. Hariyanto T.I. Kurniawan A. Coronavirus disease 2019 (Covid-19) outcomes in patients with sarcopenia: a meta-analysis and meta-regression.Clin Nutr ESPEN. 2022; 48: 158-166Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar, 15Pranata R. Lim M.A. Huang I. et al.Visceral adiposity, subcutaneous adiposity, and severe coronavirus disease-2019 (COVID-19): systematic review and meta-analysis.Clin Nutr ESPEN. 2021; 43: 163-168Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar, 16Foldi M. Farkas N. Kiss S. et al.Visceral adiposity elevates the risk of critical condition in COVID-19: a systematic review and meta-analysis.Obesity (Silver Spring). 2021; 29: 521-528Crossref PubMed Scopus (46) Google Scholar Methodology and exact anatomic levels at which these parameters were quantified varied among studies. Still, meta-analyses showed that low skeletal muscle mass predicts short-term mortality and high visceral adipose tissue (VAT), but not subcutaneous adipose tissue (SAT), is associated with severe disease in patients with Y.M.T. Hartoyo V. Hariyanto T.I. Kurniawan A. Coronavirus disease 2019 (Covid-19) outcomes in patients with sarcopenia: a meta-analysis and meta-regression.Clin Nutr ESPEN. 2022; 48: 158-166Abstract Full Text Full Text PDF PubMed Scopus (16) Google R. Lim M.A. Huang I. et al.Visceral adiposity, subcutaneous adiposity, and severe coronavirus disease-2019 (COVID-19): systematic review and meta-analysis.Clin Nutr ESPEN. 2021; 43: 163-168Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar clinical decision-making in the of patients with COVID-19 is on parameters and analyses that are available and in the these parameters, a of predicting adverse outcomes in COVID-19 have been Based on a systematic the 4C Mortality Score was and validated by et A. R. et al.Risk of patients to with using the Clinical and of the 4C Mortality 2020; PubMed Scopus Google Scholar in and of and and has been as the validated and to predict in-hospital mortality in COVID-19 30 A. R. et al.Risk of patients to with using the Clinical and of the 4C Mortality 2020; PubMed Scopus Google Scholar, L. et for diagnosis and of systematic review and critical 2020; PubMed Scopus Google Scholar, to systematic review on for diagnosis and of 2021; Google Scholar 4C Mortality Score is a risk on the highly clinical age, of and level. information on the clinical of the and and the condition of the and of the CT scan-derived body composition parameters are associated with clinical parameters used to can be CT scan-derived body composition is associated with mortality independent of the 4C Mortality Score. Therefore, this study to the of CT scan-derived body composition parameters independent of a validated of clinical parameters on 30-day in-hospital mortality in patients with COVID-19. This was a cohort analysis of patients with COVID-19 from the and the in the province of of patients who treatment at the ED of the with a clinical of COVID-19 during the first wave of the pandemic and chest CT scan imaging at of COVID-19 were by or a high clinical likelihood in with a COVID-19 Reporting and Data System (CO-RADS) of a high likelihood on CT scan and M. van Everdingen W. van Rees Vellinga T. et al.CO-RADS: a categorical CT assessment scheme for patients suspected of having COVID-19—definition and evaluation.Radiology. 2020; 296: E97-E104Crossref PubMed Scopus (528) Google Scholar cohort of hospitalized patients and patients who at the but were not whereas the cohort of hospitalized patients. Mortality within 30 days was for of hospitalization of the retrospective of the the medical of for this study and was Additionally, on from the patients were the possible of for In patients to were from the Skeletal muscle and adipose tissue parameters were retrieved from obtained chest CT scans at ED or admission. CT scans were obtained the application of cross-sectional area (CSA) of the pectoralis and was at the level of the fourth thoracic Additionally, CSA of skeletal muscle, and was demarcated at the level of the first lumbar vertebra analyzed at the L1 level included the and and a single at the with vertebral was used A. Pakarinen T. Sassi A. et al.Methodology, clinical applications, and future directions of body composition analysis using computed tomography (CT) images: a review.Eur J Radiol. 2021; 145109943Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar,13Sanders K.J.C. Degens J. Dingemans A.C. Schols A. Cross-sectional and longitudinal assessment of muscle from regular chest computed tomography scans: L1 and pectoralis muscle compared to L3 as reference in non-small cell lung cancer.Int J Chron Obstruct Pulmon Dis. 2019; 14: 781-789Crossref PubMed Scopus (14) Google Scholar the was of or not tissue of the or tissue was considered as a value and was not CSA of these were quantified by to clinical on muscle, to to and to A. and computed tomography imaging to (Silver Spring). PubMed Scopus Google M. T. and to of body composition in patients using computed tomography during routine Physiol Nutr PubMed Scopus Google Scholar were manually when analyses were with body and clinical of on and parameters and and information on disease course or admission, mechanical were collected from the medical in parameters of the 4C Mortality Score were and in a 4C Mortality Score from to A. R. et al.Risk of patients to with using the Clinical and of the 4C Mortality 2020; PubMed Scopus Google Scholar Additionally, of at the of CT scan of and of also were retrieved from the medical records. clinical of who died in within 30 days and of were compared using the for categorical and the for the CT scan-derived with Data are as numbers and for categorical and and for of of the 4C Mortality Score were using were in 20% of patients. In than two of the 4C Mortality Score were was analysis was to the area the of the 4C Mortality Score. were to the of independent CT scan-derived skeletal muscle mass and adipose tissue CSA with 30-day in-hospital parameters with a P value of were considered for in a multivariate adjusted for the 4C Mortality Score, with a likelihood analyses were to the of the CT scan-derived parameters adjusted for the 4C mortality with 30-day in-hospital of the are as with 95% the 4C Mortality Score was validated for hospitalized analyses were the CT scan-derived parameters and 30-day in-hospital mortality in hospitalized patients as as the with 30-day mortality in patients. 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Additionally, in a multivariate pectoralis muscle CSA was associated significantly with in-hospital 30-day independent of the 4C Mortality Score. findings are in with have demonstrated that low CT scan-derived muscle at anatomic significantly predict mortality and clinical in patients with Y.M.T. Hartoyo V. Hariyanto T.I. Kurniawan A. Coronavirus disease 2019 (Covid-19) outcomes in patients with sarcopenia: a meta-analysis and meta-regression.Clin Nutr ESPEN. 2022; 48: 158-166Abstract Full Text Full Text PDF PubMed Scopus (16) Google S. G. et of muscle mass and on and during in COVID-19 2022; Full Text Full Text PDF PubMed Scopus Google Scholar, S. D. A. et chest muscle for in patients with 2021; PubMed Scopus Google Scholar, S. of pectoralis muscle and with severity of COVID-19 in Radiol. 2021; Full Text Full Text PDF PubMed Scopus Google Scholar, A. H. G. et of the pectoralis in patients with COVID-19. Radiol. Full Text Full Text PDF PubMed Scopus Google Scholar, Z. H. W. et of muscle on chest computed tomography with clinical outcomes in patients with severe coronavirus disease 2021; 76: PubMed Scopus Google Scholar also demonstrated a of high with 30-day in-hospital with an of the clinical of this be Additionally, when adjusted for the 4C Mortality Score, was not associated significantly with This is in with meta-analyses a as as and COVID-19 but not R. Lim M.A. Huang I. et al.Visceral adiposity, subcutaneous adiposity, and severe coronavirus disease-2019 (COVID-19): systematic review and meta-analysis.Clin Nutr ESPEN. 2021; 43: 163-168Abstract Full Text Full Text PDF PubMed Scopus (30) Google S. W. of with COVID-19 severity and a meta-analysis of 2022; Scholar of the 4C Mortality Score demonstrated that an age, and having the risk of mortality in patients with COVID-19. that low pectoralis CSA significantly associated with in-hospital 30-day mortality when for the 4C Mortality Score is an in this Pectoralis muscle CSA has been to be associated with third lumbar vertebra muscle which is related to muscle mass W. Punyanitya M. Wang Z. et al.Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image.J Appl Physiol (1985). 2004; 97: 2333-2338Crossref PubMed Scopus (1155) Google Scholar,13Sanders K.J.C. Degens J. Dingemans A.C. Schols A. Cross-sectional and longitudinal assessment of muscle from regular chest computed tomography scans: L1 and pectoralis muscle compared to L3 as reference in non-small cell lung cancer.Int J Chron Obstruct Pulmon Dis. 2019; 14: 781-789Crossref PubMed Scopus (14) Google Scholar Low muscle mass is for and is to be associated with M. outcomes of sarcopenia: a systematic review and One. PubMed Scopus Google Scholar, Chen D. Y. as a of mortality among the ill in an a systematic review and 2021; PubMed Scopus (30) Google Scholar, associated with an risk of mortality and PubMed Scopus Google Scholar with are to and as have a higher risk for Y. in the 2019; PubMed Google Scholar the exact for this are not can be that a higher muscle mass an which during of as a COVID-19 can the of CT scan-derived muscle and adipose tissue CSA with disease severity and mortality in COVID-19 was demonstrated in these body composition parameters in an clinical is not in Clinical parameters as included in the highly 4C Mortality Score are of assessment in and are However, of these clinical parameters also are associated with CT scan-derived muscle and adipose tissue I. Wang R. Skeletal muscle mass and in and Appl Physiol (1985). PubMed Scopus Google Scholar Therefore, investigated CT scan-derived muscle and adipose tissue CSA are associated with mortality when adjusted for a validated of clinical parameters, the 4C Mortality Score. Based on can that pectoralis muscle CSA associated with 30-day in-hospital mortality when adjusted for the 4C Mortality Score. analyses demonstrated in this when using hospitalized patients compared with the which showed an of pectoralis muscle CSA the of the highly 4C Mortality Score and as to be to the 4C Mortality Score was not the of this However, an adjusted 4C Mortality Score low pectoralis In analyses, of the pectoralis muscle to the 4C Mortality Score demonstrated a to an very This findings the of pectoralis muscle is associated significantly with 30-day in-hospital this a as as a of comparable as the and cohort of the 4C Mortality Score is A. R. et al.Risk of patients to with using the Clinical and of the 4C Mortality 2020; PubMed Scopus Google Scholar pectoralis muscle CSA to the 4C Mortality Score, to patients with high or low muscle CSA are In with demonstrated a muscle CSA and and W. Punyanitya M. Wang Z. et al.Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image.J Appl Physiol (1985). 2004; 97: 2333-2338Crossref PubMed Scopus (1155) Google I. Wang R. Skeletal muscle mass and in and Appl Physiol (1985). PubMed Scopus Google Scholar However, and for pectoralis muscle CSA are Therefore, future in large on and for muscle analyses were on chest CT scans that were obtained with the of intrapulmonary in an clinical This is an that to be have caused from the tissue at the L1 level in of on that chest CT scans the L1 level in the future for of the prognostic value of pectoralis and L1 muscle the of analysis of CT scan-derived muscle and adipose tissue CSA for retrospective analysis of CT scans at admission. This for longitudinal of patients with COVID-19 using the CT scans that are of regular in muscle mass during and from COVID-19 have been in J. L. et outcomes and with performance in coronavirus disease 2019 at a cohort 2021; PubMed Scopus Google A. N. D. et skeletal muscle in SARS-CoV-2 to clinical outcomes in COVID-19 2022; 13: PubMed Scopus Google Scholar However, the and is very This application in the clinical and prognostic Therefore, and analysis of CT scan-derived body composition has et A. et al.Visceral adiposity and severe COVID-19 application of an to clinical risk Dis. 2021; PubMed Scopus (14) Google Scholar and et R. S. et by body composition analysis from chest CT with SARS-CoV-2 Rep. 2022; Scopus Google Scholar demonstrated the of in COVID-19 by using an to the of CT scan-derived muscle and adipose tissue parameters on disease severity and Additionally, in the of a to CT scan-derived muscle and adipose tissue recently was L. L. et al.Clinical of for body composition analysis on abdominal L3 CT in 2022; Full Text Full Text PDF PubMed Scopus Google L. L. L. et for muscle and adipose tissue from abdominal computed tomography in 2021; PubMed Scopus (14) Google Scholar of this the to these analyses from to clinical in areas of and body composition assessment as a prognostic in from to clinical J 2022; Scholar Low CT scan-derived pectoralis muscle, high and low muscle CSA at L1 are significantly associated with higher 30-day in-hospital mortality in patients with COVID-19. Additionally, CT scan-derived pectoralis muscle CSA associated with 30-day in-hospital mortality in patients with COVID-19 independent of the clinical 4C Mortality Score. to R. J. H. G. by the European Society of Clinical and and a from to H. A. G. and A. M. W. J. S. this

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