Modifications of Chest CT Body Composition Parameters at Three and Six Months after Severe COVID-19 Pneumonia: A Retrospective Cohort Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Setting
2.2. Study Design and Ethics
2.3. Study Population
2.4. Data Collection
2.5. CT Retrospective Analysis
2.6. Outcomes
2.7. Putative Determinants
2.8. Data Analyses
3. Results
3.1. Study Population
3.2. Body Composition Changes
3.3. Impact of the Inflammatory Burden on Body Composition Changes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- WHO. World Health Statistics. Available online: https://www.who.int/data/gho/publications/world-health-statistics (accessed on 15 May 2022).
- Dennis, A.; Wamil, M.; Alberts, J.; Oben, J.; Cuthbertson, D.J.; Wootton, D.; Crooks, M.; Gabbay, M.; Brady, M.; Hishmeh, L.; et al. Multiorgan impairment in low-risk individuals with post-COVID-19 syndrome: A prospective, community-based study. BMJ Open 2021, 11, e048391. [Google Scholar] [PubMed]
- Ayoubkhani, D.; Khunti, K.; Nafilyan, V.; Maddox, T.; Humberstone, B.; Diamond, I.; Banerjee, A. Post-covid syndrome in individuals admitted to hospital with COVID-19: Retrospective cohort study. BMJ 2021, 372, n693. [Google Scholar] [CrossRef]
- Nalbandian, A.; Sehgal, K.; Gupta, A.; Madhavan, M.V.; McGroder, C.; Stevens, J.S.; Cook, J.R.; Nordvig, A.S.; Shalev, D.; Sehrawat, T.S.; et al. Post-acute COVID-19 syndrome. Nat. Med. 2021, 27, 601–615. [Google Scholar] [CrossRef]
- Soriano, J.B.; Murthy, S.; Marshall, J.C.; Relan, P.; Diaz, J.V. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect. Dis. 2021, 22, e102–e107. [Google Scholar] [CrossRef]
- Yang, Y.; Ding, L.; Zou, X.; Shen, Y.; Hu, D.; Hu, X.; Li, Z.; Kamel, I.R. Visceral Adiposity and High Intramuscular Fat Deposition Independently Predict Critical Illness in Patients with SARS-CoV-2. Obesity 2020, 28, 2040–2048. [Google Scholar] [CrossRef]
- Petersen, A.; Bressem, K.; Albrecht, J.; Thieß, H.-M.; Vahldiek, J.; Hamm, B.; Makowski, M.R.; Niehues, A.; Niehues, S.M.; Adams, L.C. The role of visceral adiposity in the severity of COVID-19: Highlights from a unicenter cross-sectional pilot study in Germany. Metabolism 2020, 110, 154317. [Google Scholar] [CrossRef]
- Watanabe, M.; Caruso, D.; Tuccinardi, D.; Risi, R.; Zerunian, M.; Polici, M.; Pucciarelli, F.; Tarallo, M.; Strigari, L.; Manfrini, S.; et al. Visceral fat shows the strongest association with the need of intensive care in patients with COVID-19. Metabolism 2020, 111, 154319. [Google Scholar] [CrossRef]
- Ufuk, F.; Demirci, M.; Sagtas, E.; Akbudak, I.H.; Ugurlu, E.; Sari, T. The prognostic value of pneumonia severity score and pectoralis muscle Area on chest CT in adult COVID-19 patients. Eur. J. Radiol. 2020, 131, 109271. [Google Scholar] [CrossRef]
- Favre, G.; Legueult, K.; Pradier, C.; Raffaelli, C.; Ichai, C.; Iannelli, A.; Redheuil, A.; Lucidarme, O.; Esnault, V. Visceral fat is associated to the severity of COVID-19. Metabolism 2020, 115, 154440. [Google Scholar] [CrossRef]
- Iacobellis, G.; Malavazos, A.E.; Ferreira, T. COVID-19 Rise in Younger Adults with Obesity: Visceral Adiposity Can Predict the Risk. Obesity 2020, 28, 1795. [Google Scholar] [CrossRef]
- Földi, M.; Farkas, N.; Kiss, S.; Dembrovszky, F.; Szakács, Z.; Balaskó, M.; Erőss, B.; Hegyi, P.; Szentesi, A. Visceral Adiposity Elevates the Risk of Critical Condition in COVID-19: A Systematic Review and Meta-Analysis. Obesity 2020, 29, 521–528. [Google Scholar] [CrossRef] [PubMed]
- Besutti, G.; Pellegrini, M.; Ottone, M.; Cantini, M.; Milic, J.; Bonelli, E.; Dolci, G.; Cassone, G.; Ligabue, G.; Spaggiari, L.; et al. The impact of chest CT body composition parameters on clinical outcomes in COVID-19 patients. PLoS ONE 2021, 16, e0251768. [Google Scholar] [CrossRef] [PubMed]
- Joskova, V.; Patkova, A.; Havel, E.; Najpaverova, S.; Uramova, D.; Kovarik, M.; Zadak, Z.; Hronek, M. Critical evaluation of muscle mass loss as a prognostic marker of morbidity in critically ill patients and methods for its determination. J. Rehabilitation Med. 2018, 50, 696–704. [Google Scholar] [CrossRef] [PubMed]
- Lambell, K.J.; Goh, G.S.; Tierney, A.C.; Forsyth, A.; Nanjayya, V.; Nyulasi, I.; King, S.J. Marked losses of computed tomography–derived skeletal muscle area and density over the first month of a critical illness are not associated with energy and protein delivery. Nutrition 2020, 82, 111061. [Google Scholar] [CrossRef]
- Piotrowicz, K.; Gąsowski, J.; Michel, J.-P.; Veronese, N. Post-COVID-19 acute sarcopenia: Physiopathology and management. Aging Clin. Exp. Res. 2021, 33, 2887–2898. [Google Scholar] [CrossRef]
- Thackeray, M.; Kotowicz, M.A.; Pasco, J.A.; Mohebbi, M.; Orford, N. Changes in body composition in the year following critical illness: A case-control study. J. Crit. Care 2022, 71, 154043. [Google Scholar] [CrossRef]
- Chan, K.S.; Mourtzakis, M.; Friedman, L.A.; Dinglas, V.D.; Hough, C.L.; Ely, E.W.; Morris, P.E.; Hopkins, R.O.; Needham, D.M. Evaluating Muscle Mass in Survivors of Acute Respiratory Distress Syndrome: A 1-Year Multicenter Longitudinal Study. Crit. Care Med. 2018, 46, 1238–1246. [Google Scholar] [CrossRef]
- Thompson, E.J.; Williams, D.M.; Walker, A.J.; Mitchell, R.E.; Niedzwiedz, C.L.; Yang, T.C.; Huggins, C.F.; Kwong, A.S.F.; Silverwood, R.J.; Di Gessa, G.; et al. Risk factors for long COVID: Analyses of 10 longitudinal studies and electronic health records in the UK. medRxiv 2021. [Google Scholar] [CrossRef]
- Aminian, A.; Bena, J.; Pantalone, K.M.; Burguera, B. Association of obesity with postacute sequelae of COVID-19. Diabetes Obes. Metab. 2021, 23, 2183–2188. [Google Scholar] [CrossRef]
- van den Borst, B.; Peters, J.B.; Brink, M.; Schoon, Y.; Bleeker-Rovers, C.P.; Schers, H.; van Hees, H.W.H.; van Helvoort, H.; van den Boogaard, M.; van der Hoeven, H.; et al. Comprehensive Health Assessment 3 Months After Recovery from Acute Coronavirus Disease 2019 (COVID-19). Clin. Infect. Dis. 2020, 73, e1089–e1098. [Google Scholar] [CrossRef]
- Gualtieri, P.; Falcone, C.; Romano, L.; Macheda, S.; Correale, P.; Arciello, P.; Polimeni, N.; De Lorenzo, A. Body Composition Findings by Computed Tomography in SARS-CoV-2 Patients: Increased Risk of Muscle Wasting in Obesity. Int. J. Mol. Sci. 2020, 21, 4670. [Google Scholar] [CrossRef] [PubMed]
- Gobbi, M.; Brunani, A.; Arreghini, M.; Baccalaro, G.; Dellepiane, D.; La Vela, V.; Lucchetti, E.; Barbaglia, M.; Cova, A.; Fornara, E.; et al. Nutritional status in post SARS-Cov2 rehabilitation patients. Clin. Nutr. 2021, in press. [CrossRef] [PubMed]
- Cuerda, C.; López, I.S.; Gil Martínez, C.; Viveros, M.M.; Velasco, C.; Peñafiel, V.C.; Jiménez, M.M.; Gonzalo, I.; González-Sánchez, V.; Carrasco, A.R.; et al. Impact of COVID-19 in nutritional and functional status of survivors admitted in intensive care units during the first outbreak. Preliminary results of the NUTRICOVID study. Clin. Nutr. 2021, in press. [CrossRef] [PubMed]
- Di Filippo, L.; De Lorenzo, R.; D’Amico, M.; Sofia, V.; Roveri, L.; Mele, R.; Saibene, A.; Rovere-Querini, P.; Conte, C. COVID-19 is associated with clinically significant weight loss and risk of malnutrition, independent of hospitalisation: A post-hoc analysis of a prospective cohort study. Clin. Nutr. 2020, 40, 2420–2426. [Google Scholar] [CrossRef]
- Di Filippo, L.; De Lorenzo, R.; Cinel, E.; Falbo, E.; Ferrante, M.; Cilla, M.; Martinenghi, S.; Vitali, G.; Bosi, E.; Giustina, A.; et al. Weight trajectories and abdominal adiposity in COVID-19 survivors with overweight/obesity. Int. J. Obes. 2021, 45, 1986–1994. [Google Scholar] [CrossRef]
- Joris, M.; Minguet, P.; Colson, C.; Joris, J.; Fadeur, M.; Minguet, G.; Guiot, J.; Misset, B.; Rousseau, A.-F. Cardiopulmonary Exercise Testing in Critically Ill Coronavirus Disease 2019 Survivors: Evidence of a Sustained Exercise Intolerance and Hypermetabolism. Crit. Care Explor. 2021, 3, e0491. [Google Scholar] [CrossRef] [PubMed]
- Rossi, P.G.; Broccoli, S.; Angelini, P. Case fatality rate in patients with COVID-19 infection and its relationship with length of follow up. J. Clin. Virol. 2020, 128, 104415. [Google Scholar] [CrossRef]
- Rossi, P.G.; Marino, M.; Formisano, D.; Venturelli, F.; Vicentini, M.; Grilli, R.; the Reggio Emilia COVID-19 Working Group. Characteristics and outcomes of a cohort of COVID-19 patients in the Province of Reggio Emilia, Italy. PLoS ONE 2020, 15, e0238281. [Google Scholar] [CrossRef]
- Besutti, G.; Rossi, P.G.; Ottone, M.; Spaggiari, L.; Canovi, S.; Monelli, F.; Bonelli, E.; Fasano, T.; Sverzellati, N.; Caruso, A.; et al. Inflammatory burden and persistent CT lung abnormalities in COVID-19 patients. Sci. Rep. 2022, 12, 4270. [Google Scholar] [CrossRef]
- Besutti, G.; Rossi, P.G.; Iotti, V.; Spaggiari, L.; Bonacini, R.; Nitrosi, A.; Ottone, M.; Bonelli, E.; Fasano, T.; Canovi, S.; et al. Accuracy of CT in a cohort of symptomatic patients with suspected COVID-19 pneumonia during the outbreak peak in Italy. Eur. Radiol. 2020, 30, 6818–6827. [Google Scholar] [CrossRef]
- Looijaard, W.G.P.M.; Dekker, I.M.; Stapel, S.N.; Girbes, A.R.J.; Twisk, J.W.R.; Straaten, H.M.O.-V.; Weijs, P.J.M. Skeletal muscle quality as assessed by CT-derived skeletal muscle density is associated with 6-month mortality in mechanically ventilated critically ill patients. Crit. Care 2016, 20, 386. [Google Scholar] [CrossRef]
- Tong, Y.; Udupa, J.K.; Torigian, D.A.; Odhner, D.; Wu, C.; Pednekar, G.; Palmer, S.; Rozenshtein, A.; Shirk, M.A.; Newell, J.D.; et al. Chest Fat Quantification via CT Based on Standardized Anatomy Space in Adult Lung Transplant Candidates. PLoS ONE 2017, 12, e0168932. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.S.; Park, S.H.; Lee, S.S.; Kim, D.Y.; Shin, Y.M.; Lee, W.; Lee, S.-G.; Yu, E.S. Biopsy-proven Nonsteatotic Liver in Adults: Estimation of Reference Range for Difference in Attenuation between the Liver and the Spleen at Nonenhanced CT. Radiology 2011, 258, 760–766. [Google Scholar] [CrossRef] [PubMed]
- Moriconi, D.; Masi, S.; Rebelos, E.; Virdis, A.; Manca, M.L.; De Marco, S.; Taddei, S.; Nannipieri, M. Obesity prolongs the hospital stay in patients affected by COVID-19, and may impact on SARS-COV-2 shedding. Obes. Res. Clin. Pract. 2020, 14, 205–209. [Google Scholar] [CrossRef]
- Kalyon, S.; Gültop, F.; Şimşek, F.; Adaş, M. Relationships of the neutrophil–lymphocyte and CRP–albumin ratios with the duration of hospitalization and fatality in geriatric patients with COVID-19. J. Int. Med Res. 2021, 49, 03000605211046112. [Google Scholar] [CrossRef]
- Goodpaster, B.H.; Kelley, D.E.; Thaete, F.L.; He, J.; Ross, R. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J. Appl. Physiol. 2000, 89, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Larson-Meyer, D.E.; Smith, S.R.; Heilbronn, L.K.; Kelley, D.E.; Ravussin, E.; Newcomer, B.R. Look AHEAD Adipose Research Group Muscle-associated Triglyceride Measured by Computed Tomography and Magnetic Resonance Spectroscopy. Obesity 2006, 14, 73–87. [Google Scholar] [CrossRef]
- Miljkovic, I.; Kuipers, A.L.; Kammerer, C.M.; Wang, X.; Bunker, C.H.; Patrick, A.L.; Wheeler, V.W.; Kuller, L.H.; Evans, R.W.; Zmuda, J.M. Markers of Inflammation Are Heritable and Associated with Subcutaneous and Ectopic Skeletal Muscle Adiposity in African Ancestry Families. Metab. Syndr. Relat. Disord. 2011, 9, 319–326. [Google Scholar] [CrossRef]
- Bakaloudi, D.R.; Barazzoni, R.; Bischoff, S.C.; Breda, J.; Wickramasinghe, K.; Chourdakis, M. Impact of the first COVID-19 lockdown on body weight: A combined systematic review and a meta-analysis. Clin. Nutr. 2021, in press. [CrossRef]
- Di Santo, S.G.; Franchini, F.; Filiputti, B.; Martone, A.; Sannino, S. The Effects of COVID-19 and Quarantine Measures on the Lifestyles and Mental Health of People Over 60 at Increased Risk of Dementia. Front. Psychiatry 2020, 11, 578628. [Google Scholar] [CrossRef]
- Acedo, C.; Roncero-Martín, R.; Sánchez-Fernández, A.; Mendoza-Holgado, C.; Pedrera-Canal, M.; López-Espuela, F.; Rey-Sánchez, P.; Pedrera-Zamorano, J.D.; Puerto-Parejo, L.M.; Moran, J.M.; et al. Body Composition and Nutrients Dietary Intake Changes during COVID-19 Lockdown in Spanish Healthy Postmenopausal Women. Eur. J. Investig. Health Psychol. Educ. 2022, 12, 631–638. [Google Scholar] [CrossRef] [PubMed]
- Mason, S.E.; Moreta-Martinez, R.; Labaki, W.W.; Strand, M.J.; Regan, E.A.; Bon, J.; Estepar, R.S.J.; Casaburi, R.; McDonald, M.-L.; Rossiter, H.B.; et al. Longitudinal Association Between Muscle Loss and Mortality in Ever Smokers. Chest 2021, 161, 960–970. [Google Scholar] [CrossRef] [PubMed]
- Rhéaume, C.; Arsenault, B.J.; Dumas, M.-P.; Perusse, L.; Tremblay, A.; Bouchard, C.; Poirier, P.; Després, J.-P. Contributions of Cardiorespiratory Fitness and Visceral Adiposity to Six-Year Changes in Cardiometabolic Risk Markers in Apparently Healthy Men and Women. J. Clin. Endocrinol. Metab. 2011, 96, 1462–1468. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.S.; Kim, E.Y.; Kang, S.M.; Ahn, H.K.; Kim, H.S. Single cross-sectional area of pectoralis muscle by computed tomography-correlation with bioelectrical impedance based skeletal muscle mass in healthy subjects. Clin. Physiol. Funct. Imaging 2015, 37, 507–511. [Google Scholar] [CrossRef]
All Patients | ||
---|---|---|
n (%) | ||
N = 208 | ||
Age (years), median (IQR) | 65 (58–74) | |
Female sex | 65 (31.3) | |
Smoking habit | Never | 178 (85.6) |
Previous | 27 (13.0) | |
Current | 3 (1.4) | |
COPD | 8 (3.9) | |
Asthma | 9 (4.3) | |
Cardiovascular diseases | 52 (25.0) | |
Cancer | 23 (11.1) | |
Diabetes | 48 (23.1) | |
Hypertension | 102 (49) | |
Chronic kidney failure | 3 (1.4) | |
Cerebrovascular disease | 16 (7.7) | |
Liver diseases | 6 (2.9) | |
Baseline BMI (kg/m2) * | 29.1 (26.1–33.1) | |
Days from symptom onset, median (IQR) | 6 (4–9) | |
Baseline CT disease extension | ||
0 | 1 (0.5) | |
<20 | 12 (5.8) | |
20–40 | 51 (24.5) | |
40–60 | 107 (51.4) | |
≥60 | 37 (17.8) | |
CRP interval, median (IQR) | 168 (96–253) | |
Tocilizumab administration ** | 56 (53.3) | |
Steroid therapy | 61 (29.3) | |
Non-invasive mechanical ventilation | 86 (41.3) | |
Invasive mechanical ventilation | 26 (24.1) | |
Mechanical ventilation | 100 (48.1) | |
Lowest PaO2/FiO2 (mmHg), median (IQR) *** | 120 (81–219) | |
D-dimer peak (ng/mL), median (IQR) **** | 1816 (926–4236) | |
Length of hospital stay (days), median (IQR) | 18 (12–29) |
Mean (SD) | Mean Difference (95%CI) | |||||
---|---|---|---|---|---|---|
T0 | T1 | T2 | ∆T1-T0 | ∆T2-T1 | ∆T2-T0 | |
Pectoral Muscle Area (n = 202) | 18.01 (6.69) | 17.23 (6.81) | 16.90 (6.48) | −0.78 (−1.39;−0.17) | −0.33 (−0.84;0.18) | −1.11 (−1.72;−0.51) |
Pectoral Muscle Density (n = 203) | 33.97 (9.94) | 33.82 (9.61) | 36.89 (9.76) | −0.15 (−1.09;0.79) | 3.07 (2.08;4.06) | 2.92 (1.79;4.05) |
Liver-to-spleen Ratio (n = 184) | 0.98 (0.26) | 1.10 (0.24) | 1.14 (0.21) | 0.13 (0.09;0.16) | 0.04 (0.01;0.07) | 0.17 (0.13;0.20) |
IMAT (n = 204) | 32.3 (16.7) | 31.6 (15.9) | 31.1 (16.7) | −0.75 (−1.72;0.23) | −0.47 (−1.45;0.52) | −1.21 (−2.23;−0.19) |
VAT (n = 205) | 41.4 (19.6) | 39.2 (18.5) | 37.8 (18.8) | −2.21 (−3.35;−1.08) | −1.34 (−2.67;−0.01) | −3.55 (−4.94;−2.17) |
TAT (n = 203) | 274.8 (133.2) | 273.1 (142.9) | 271.7 (148.2) | −1.67 (−7.89;4.55) | −1.46 (−7.18;4.26) | −3.13 (−10.79;4.52) |
SAT (n = 203) | 201.1 (116.7) | 202.4 (126.9) | 202.5 (130.7) | 1.33 (−4.77;7.43) | 0.09 (−5.23;5.41) | 1.42 (−5.57;8.41) |
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Besutti, G.; Pellegrini, M.; Ottone, M.; Bonelli, E.; Monelli, F.; Farì, R.; Milic, J.; Dolci, G.; Fasano, T.; Canovi, S.; et al. Modifications of Chest CT Body Composition Parameters at Three and Six Months after Severe COVID-19 Pneumonia: A Retrospective Cohort Study. Nutrients 2022, 14, 3764. https://doi.org/10.3390/nu14183764
Besutti G, Pellegrini M, Ottone M, Bonelli E, Monelli F, Farì R, Milic J, Dolci G, Fasano T, Canovi S, et al. Modifications of Chest CT Body Composition Parameters at Three and Six Months after Severe COVID-19 Pneumonia: A Retrospective Cohort Study. Nutrients. 2022; 14(18):3764. https://doi.org/10.3390/nu14183764
Chicago/Turabian StyleBesutti, Giulia, Massimo Pellegrini, Marta Ottone, Efrem Bonelli, Filippo Monelli, Roberto Farì, Jovana Milic, Giovanni Dolci, Tommaso Fasano, Simone Canovi, and et al. 2022. "Modifications of Chest CT Body Composition Parameters at Three and Six Months after Severe COVID-19 Pneumonia: A Retrospective Cohort Study" Nutrients 14, no. 18: 3764. https://doi.org/10.3390/nu14183764