Phase Angle and Handgrip Strength as Predictors of Clinical Outcomes in Hospitalized COVID-19 Patients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Exclusion Criteria
2.3. Demographics, Comorbidities and Laboratory Values
2.4. Primary and Secondary Outcomes
2.5. Body Composition Measurements
2.5.1. Phase Angle
2.5.2. Handgrip Strength
2.6. Assessment of Severity of COVID-19
2.7. Statistical Analysis
3. Results
3.1. Patients Characteristics
3.2. Primary Outcomes
3.3. Secondary Outcomes
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Grant, W.B.; Lahore, H.; McDonnell, S.L.; Baggerly, C.A.; French, C.B.; Aliano, J.L.; Bhattoa, H.P. Evidence that Vitamin D Supplementation Could Reduce Risk of Influenza and COVID-19 Infections and Deaths. Nutrients 2020, 12, 988. [Google Scholar] [CrossRef] [PubMed]
- Velavan, T.P.; Meyer, C.G. The COVID-19 Epidemic. Trop. Med. Int. Health 2020, 25, 278–280. [Google Scholar] [CrossRef] [PubMed]
- Attaway, A.H.; Scheraga, R.G.; Bhimraj, A.; Biehl, M.; Hatipoğlu, U. Severe covid-19 pneumonia: Pathogenesis and clinical management. BMJ 2021, 372, n436. [Google Scholar] [CrossRef] [PubMed]
- Cronin, J.N.; Camporota, L.; Formenti, F. Mechanical ventilation in COVID-19: A physiological perspective. Exp. Physiol. 2021, 107, 683–693. [Google Scholar] [CrossRef]
- Lai, C.C.; Shih, T.P.; Ko, W.C.; Tang, H.J.; Hsueh, P.R. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) and Coronavirus Disease-2019 (COVID-19): The Epidemic and the Challenges. Int. J. Antimicrob. Agents 2020, 55, 105924. [Google Scholar] [CrossRef]
- Van der Sar-van der Brugge, S.; Talman, S.; Winter, L.B.-D.; de Mol, M.; Hoefman, E.; van Etten, R.W.; De Backer, I.C. Pulmonary function and health-related quality of life after COVID-19 pneumonia. Respir. Med. 2021, 176, 106272. [Google Scholar] [CrossRef]
- Baccolini, V.; Migliara, G.; Isonne, C.; Dorelli, B.; Barone, L.C.; Giannini, D.; Marotta, D.; Marte, M.; Mazzalai, E.; Alessandri, F.; et al. The impact of the COVID-19 pandemic on healthcare-associated infections in intensive care unit patients: A retrospective cohort study. Antimicrob. Resist. Infect. Control. 2021, 10, 87. [Google Scholar] [CrossRef]
- Brioni, M.; Meli, A.; Grasselli, G. Mechanical Ventilation for COVID-19 Patients. Semin. Respir. Crit. Care Med. 2022, 43, 405–416. [Google Scholar] [CrossRef]
- World Health Organization. Coronavirus Disease (COVID-19) Pandemic. Available online: https://www.who.int/europe/emergencies/situations/covid-19 (accessed on 13 November 2022).
- Hergens, M.-P.; Bell, M.; Haglund, P.; Sundström, J.; Lampa, E.; Nederby-Öhd, J.; Östlund, M.R.; Cars, T. Risk factors for COVID-19-related death, hospitalization and intensive care: A population-wide study of all inhabitants in Stockholm. Eur. J. Epidemiol. 2022, 37, 157–165. [Google Scholar] [CrossRef]
- Alves, E.A.S.; Salazar, T.C.D.N.; Silvino, V.O.; Cardoso, G.A.; dos Santos, M.A.P. Association between phase angle and adverse clinical outcomes in hospitalized patients with COVID-19: A systematic review. Nutr. Clin. Pr. 2022, 37, 1105–1116. [Google Scholar] [CrossRef]
- Bunnell, K.M.; Thaweethai, T.; Buckless, C.; Shinnick, D.J.; Torriani, M.; Foulkes, A.S.; Bredella, M.A. Body composition predictors of outcome in patients with COVID-19. Int. J. Obes. 2021, 45, 2238–2243. [Google Scholar] [CrossRef]
- Bhaskaran, K.; Rentsch, C.T.; Hickman, G.; Hulme, W.J.; Schultze, A.; Curtis, H.J.; Wing, K.; Warren-Gash, C.; Tomlinson, L.; Bates, C.J.; et al. Overall and cause-specific hospitalisation and death after COVID-19 hospitalisation in England: A cohort study using linked primary care, secondary care, and death registration data in the OpenSAFELY platform. PLoS Med. 2022, 19, e1003871. [Google Scholar] [CrossRef]
- Barazzoni, R.; Bischoff, S.C.; Breda, J.; Wickramasinghe, K.; Krznaric, Z.; Nitzan, D.; Pirlich, M.; Singer, P. ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection. Clin. Nutr. 2020, 39, 1631–1638. [Google Scholar] [CrossRef]
- Mesquita, R.D.R.; Junior, L.C.F.S.; Santana, F.M.S.; de Oliveira, T.F.; Alcântara, R.C.; Arnozo, G.M.; Filho, E.R.D.S.; dos Santos, A.G.G.; da Cunha, E.J.O.; de Aquino, S.H.S.; et al. Clinical manifestations of COVID-19 in the general population: Systematic review. Wien. Klin. Wochenschr. 2020, 133, 377–382. [Google Scholar] [CrossRef]
- Wierdsma, N.J.; Kruizenga, H.M.; Konings, L.A.; Krebbers, D.; Jorissen, J.R.; Joosten, M.-H.I.; van Aken, L.H.; Tan, F.M.; van Bodegraven, A.A.; Soeters, M.R.; et al. Poor nutritional status, risk of sarcopenia and nutrition related complaints are prevalent in COVID-19 patients during and after hospital admission. Clin. Nutr. ESPEN 2021, 43, 369–376. [Google Scholar] [CrossRef]
- Norman, K.; Pichard, C.; Lochs, H.; Pirlich, M. Prognostic impact of disease-related malnutrition. Clin. Nutr. 2008, 27, 5–15. [Google Scholar] [CrossRef]
- Evans, W.J. Skeletal muscle loss: Cachexia, sarcopenia, and inactivity. Am. J. Clin. Nutr. 2010, 91, S1123–S1127. [Google Scholar] [CrossRef]
- Esakandari, H.; Nabi-Afjadi, M.; Fakkari-Afjadi, J.; Farahmandian, N.; Miresmaeili, S.M.; Bahreini, E. A Comprehen-sive Review of COVID-19 Characteristics. Biol. Proced. Online 2020, 22, 19. [Google Scholar] [CrossRef]
- Li, Y.; Zhu, C.; Zhang, B.; Liu, L.; Ji, F.; Zhao, Y.; Cheng, J.; Shao, H.; Guan, X.; Ming, F.; et al. Nutritional status is closely related to the severity of COVID-19: A multi-center retrospective study. J. Infect. Dev. Ctries. 2021, 15, 490–500. [Google Scholar] [CrossRef]
- Osuna-Padilla, I.A.; Rodríguez-Moguel, N.C.; Rodríguez-Llamazares, S.; Aguilar-Vargas, A.; Casas-Aparicio, G.A.; Ríos-Ayala, M.A.; Hernández-Cardenas, C.M. Low phase angle is associated with 60-day mortality in critically ill patients with COVID-19. J. Parenter. Enter. Nutr. 2021, 46, 828–835. [Google Scholar] [CrossRef]
- Cornejo-Pareja, I.; Vegas-Aguilar, I.M.; García-Almeida, J.M.; Bellido-Guerrero, D.; Talluri, A.; Lukaski, H.; Tinahones, F.J. Phase angle and standardized phase angle from bioelectrical impedance measurements as a prognostic factor for mortality at 90 days in patients with COVID-19: A longitudinal cohort study. Clin. Nutr. 2021, 41, 3106–3114. [Google Scholar] [CrossRef] [PubMed]
- Di Vincenzo, O.; Marra, M.; Di Gregorio, A.; Pasanisi, F.; Scalfi, L. Bioelectrical impedance analysis (BIA)-derived phase angle in sarcopenia: A systematic review. Clin. Nutr. 2020, 40, 3052–3061. [Google Scholar] [CrossRef] [PubMed]
- Moonen, H.P.F.X.; van Zanten, F.J.L.; Driessen, L.; de Smet, V.; Slingerland-Boot, R.; Mensink, M.; van Zanten, A.R.H. Association of bioelectric impedance analysis body composition and disease severity in COVID-19 hospital ward and ICU patients: The BIAC-19 study. Clin. Nutr. 2020, 40, 2328–2336. [Google Scholar] [CrossRef] [PubMed]
- Ali, A.M.; Kunugi, H. Skeletal Muscle Damage in COVID-19: A Call for Action. Medicina 2021, 57, 372. [Google Scholar] [CrossRef]
- Pucci, G.; D’Abbondanza, M.; Curcio, R.; Alcidi, R.; Campanella, T.; Chiatti, L.; Gandolfo, V.; Veca, V.; Casarola, G.; Leone, M.C.; et al. Handgrip strength is associated with adverse outcomes in patients hospitalized for COVID-19-associated pneumonia. Intern. Emerg. Med. 2022, 17, 1997–2004. [Google Scholar] [CrossRef]
- Cheval, B.; Sieber, S.; Maltagliati, S.; Millet, G.P.; Formánek, T.; Chalabaev, A.; Cullati, S.; Boisgontier, M.P. Muscle strength is associated with COVID-19 hospitalization in adults 50 years of age or older. J. Cachex Sarcopenia Muscle 2021, 12, 1136–1143. [Google Scholar] [CrossRef]
- World Medical Association. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013, 310, 2191–2194. [Google Scholar] [CrossRef]
- Jansen, A.K.; Gattermann, T.; Fink, J.D.S.; Saldanha, M.F.; Rocha, C.D.N.; Moreira, T.H.D.S.; Silva, F.M. Low standardized phase angle predicts prolonged hospitalization in critically ill patients. Clin. Nutr. ESPEN 2019, 34, 68–72. [Google Scholar] [CrossRef]
- Moonen, H.P.; Bos, A.E.; Hermans, A.J.; Stikkelman, E.; van Zanten, F.J.; van Zanten, A.R. Bioelectric impedance body composition and phase angle in relation to 90-day adverse outcome in hospitalized COVID-19 ward and ICU patients: The prospective BIAC-19 study. Clin. Nutr. ESPEN 2021, 46, 185–192. [Google Scholar] [CrossRef]
- Reyes-Torres, C.A.; Flores-López, A.; Osuna-Padilla, I.A.; Hernández-Cárdenas, C.M.; Serralde-Zúñiga, A.E. Phase angle and overhydration are associated with post-extubating dysphagia in patients with COVID-19 discharged from the ICU. Nutr. Clin. Pract. 2021, 37, 110–116. [Google Scholar] [CrossRef]
- Lee, S.Y. Handgrip Strength: An Irreplaceable Indicator of Muscle Function. Ann. Rehabil. Med. 2021, 45, 167–169. [Google Scholar] [CrossRef]
- Lee, S.H.; Gong, H.S. Measurement and Interpretation of Handgrip Strength for Research on Sarcopenia and Osteoporosis. J. Bone Metab. 2020, 27, 85–96. [Google Scholar] [CrossRef]
- Wiśniowska-Szurlej, A.; Ćwirlej-Sozańska, A.; Kilian, J.; Wołoszyn, N.; Sozański, B.; Wilmowska-Pietruszyńska, A. Reference values and factors associated with hand grip strength among older adults living in southeastern Poland. Sci. Rep. 2021, 11, 9950. [Google Scholar] [CrossRef]
- Del Giorno, R.; Quarenghi, M.; Stefanelli, K.; Rigamonti, A.; Stanglini, C.; De Vecchi, V.; Gabutti, L. Phase angle is associated with length of hospital stay, readmissions, mortality, and falls in patients hospitalized in internal-medicine wards: A retrospective cohort study. Nutrition 2020, 85, 111068. [Google Scholar] [CrossRef]
- Rosas-Carrasco, O.; Núñez-Fritsche, G.; López-Teros, M.T.; Acosta-Méndez, P.; Cruz-Oñate, J.C.; Navarrete-Cendejas, A.Y.; Delgado-Moreno, G. Low muscle strength and low phase angle predicts greater risk to mortality than severity scales (APACHE, SOFA, and CURB-65) in adults hospitalized for SARS-CoV-2 pneumonia. Front. Nutr. 2022, 9, 965356. [Google Scholar] [CrossRef]
- Kellnar, A.; Hoppe, J.M.; Brunner, S.; Stremmel, C. Hospitalization for COVID-19 is associated with significant changes in body composition. Clin. Nutr. ESPEN 2021, 45, 499–502. [Google Scholar] [CrossRef]
- Bedock, D.; Lassen, P.B.; Mathian, A.; Moreau, P.; Couffignal, J.; Ciangura, C.; Poitou-Bernert, C.; Jeannin, A.-C.; Mosbah, H.; Fadlallah, J.; et al. Prevalence and severity of malnutrition in hospitalized COVID-19 patients. Clin. Nutr. ESPEN 2020, 40, 214–219. [Google Scholar] [CrossRef]
- Rabbani, G.; Ahn, S.N. Review: Roles of human serum albumin in prediction, diagnoses and treatment of COVID-19. Int. J. Biol. Macromol. 2021, 193, 948–955. [Google Scholar] [CrossRef]
- Paliogiannis, P.; Mangoni, A.A.; Cangemi, M.; Fois, A.G.; Carru, C.; Zinellu, A. Serum albumin concentrations are associated with disease severity and outcomes in coronavirus 19 disease (COVID-19): A systematic review and meta-analysis. Clin. Exp. Med. 2021, 21, 343–354. [Google Scholar] [CrossRef]
- Zerbato, V.; Sanson, G.; De Luca, M.; Di Bella, S.; di Masi, A.; Caironi, P.; Marini, B.; Ippodrino, R.; Luzzati, R. The Impact of Serum Albumin Levels on COVID-19 Mortality. Infect. Dis. Rep. 2022, 14, 278–286. [Google Scholar] [CrossRef]
- Mey, R.; Calatayud, J.; Casaña, J.; Torres-Castro, R.; Cuenca-Martínez, F.; Suso-Martí, L.; Andersen, L.; López-Bueno, R. Handgrip strength and respiratory disease mortality: Longitudinal analyses from SHARE. Pulmonology 2022. [Google Scholar] [CrossRef] [PubMed]
- Kara, Ö.; Kara, M.; Akın, M.E.; Özçakar, L. Grip strength as a predictor of disease severity in hospitalized COVID-19 patients. Hear. Lung 2021, 50, 743–747. [Google Scholar] [CrossRef] [PubMed]
- Nicolau, J.; Ayala, L.; Sanchís, P.; Olivares, J.; Dotres, K.; Soler, A.-G.; Rodríguez, I.; Gómez, L.A.; Masmiquel, L. Influence of nutritional status on clinical outcomes among hospitalized patients with COVID-19. Clin. Nutr. ESPEN 2021, 43, 223–229. [Google Scholar] [CrossRef] [PubMed]
- García-Hermoso, A.; Cavero-Redondo, I.; Ramírez-Vélez, R.; Ruiz, J.R.; Ortega, F.B.; Lee, D.-C.; Martínez-Vizcaíno, V. Muscular Strength as a Predictor of All-Cause Mortality in an Apparently Healthy Population: A Systematic Review and Meta-Analysis of Data From Approximately 2 Million Men and Women. Arch. Phys. Med. Rehabilit. 2018, 99, 2100–2113. [Google Scholar] [CrossRef] [PubMed]
- Gil, S.; Filho, W.J.; Shinjo, S.K.; Ferriolli, E.; Busse, A.L.; Avelino-Silva, T.J.; Longobardi, I.; de Oliveira Júnior, G.N.; Swinton, P.; Gualano, B.; et al. Muscle strength and muscle mass as predictors of hospital length of stay in patients with moderate to severe COVID-19: A prospective observational study. J. Cachexia Sarcopenia Muscle 2021, 12, 1871–1878. [Google Scholar] [CrossRef]
- de Sevilla, G.G.P.; Sánchez-Pinto, B. Associations between muscle strength, dyspnea and quality of life in post-COVID-19 patients. Rev. Da Assoc. Médica Bras. 2022, 68, 1753–1758. [Google Scholar] [CrossRef]
- Silverio, R.; Gonçalves, D.C.; Andrade, M.F.; Seelaender, M. Coronavirus Disease 2019 (COVID-19) and Nutritional Status: The Missing Link? Adv. Nutr. 2021, 12, 682–692. [Google Scholar] [CrossRef]
- Soeroto, A.Y.; Soetedjo, N.N.; Purwiga, A.; Santoso, P.; Kulsum, I.D.; Suryadinata, H.; Ferdian, F. Effect of increased BMI and obesity on the outcome of COVID-19 adult patients: A systematic review and meta-analysis. Diabetes Metab. Syndr. Clin. Res. Rev. 2020, 14, 1897–1904. [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, 41, 3046–3054. [Google Scholar] [CrossRef]
- Palaiodimos, L.; Kokkinidis, D.G.; Li, W.; Karamanis, D.; Ognibene, J.; Arora, S.; Southern, W.N.; Mantzoros, C.S. Severe obesity, increasing age and male sex are independently associated with worse in-hospital outcomes, and higher in-hospital mortality, in a cohort of patients with COVID-19 in the Bronx, New York. Metabolism 2020, 108, 154262. [Google Scholar] [CrossRef]
- Longmore, D.K.; Miller, J.E.; Bekkering, S.; Saner, C.; Mifsud, E.; Zhu, Y.; Saffery, R.; Nichol, A.; Colditz, G.; Short, K.R.; et al. Diabetes and Overweight/Obesity Are Independent, Nonadditive Risk Factors for In-Hospital Severity of COVID-19: An International, Multicenter Retrospective Meta-analysis. Diabetes Care 2021, 44, 1281–1290. [Google Scholar] [CrossRef]
- Da Porto, A.; Tascini, C.; Peghin, M.; Sozio, E.; Colussi, G.; Casarsa, V.; Bulfone, L.; Graziano, E.; De Carlo, C.; Catena, C.; et al. Prognostic Role of Malnutrition Diagnosed by Bioelectrical Impedance Vector Analysis in Older Adults Hospitalized with COVID-19 Pneumonia: A Prospective Study. Nutrients 2021, 13, 4085. [Google Scholar] [CrossRef]
- Rinaldi, S.; Gilliland, J.; O’Connor, C.; Chesworth, B.; Madill, J. Is phase angle an appropriate indicator of malnutrition in different disease states? A systematic review. Clin. Nutr. ESPEN 2018, 29, 1–14. [Google Scholar] [CrossRef]
- Fernández-Jiménez, R.; Dalla-Rovere, L.; García-Olivares, M.; Abuín-Fernández, J.; Sánchez-Torralvo, F.J.; Doulatram-Gamgaram, V.K.; Hernández-Sanchez, A.M.; García-Almeida, J.M. Phase Angle and Handgrip Strength as a Predictor of Disease-Related Malnutrition in Admitted Patients: 12-Month Mortality. Nutrients 2022, 14, 1851. [Google Scholar] [CrossRef]
N (%) | ||
---|---|---|
Age (years) | 59 (47.5–67) * | |
BMI (kg/m2) | 29 (25–32.5) | |
Sex | Male 61 (59.8%) # | Female 41 (40.2%) |
Yes | No | |
Smokers | 17 (16.7%) | 85 (83.3%) |
Hypertension | 31 (30.4%) | 71 (69.6%) |
Diabetes | 16 (15.7%) | 86 (84.3%) |
Cardiovascular Disease | 9 (8.8%) | 93 (91.2%) |
Dyslipidemia | 26 (25.5%) | 76 (74.5%) |
Obesity | 16 (15.7%) | 86 (84.3%) |
Cancer | 8 (7.8%) | 94 (92.2%) |
Autoimmune Disease | 9 (8.8%) | 93 (91.2%) |
Pulmonary Disease | 5 (4.9%) | 97 (95.1%) |
Day 1 | Day 7 | ||
---|---|---|---|
Phase Angle (°) | Total | 6.1 (5.2–8.3) | 5.95 (4.8–9.8) |
Male | 6.5 (5.4–8.6) | 6.25 (4.9–10.7) | |
Female | 5.8 (4.9–8.2) | 5.4 (4.9–9.7) | |
Lean Body Mass (kg) | 57.3 (13.4) | 57.5 (14.0) | |
Dry Lean Body Mass (kg) | 14.5 (5.7) | 14.5 (5.5) | |
Fat Mass (kg) | 39.4 (18.8) | 38.6 (17.6) | |
Handgrip Strength (kg) | Total | 34.1 (14.1) | 34.9 (14.5) |
Male | 39.9 (11.8) | 40.9 (12.2) | |
Female | 22 (6.2) | 23.1 (5) | |
Arm circumference (cm) | 36.4 (5.2) | 35.5 (5.2) | |
CRP (mg/dL) | 7.6 (5.6) | 1.3 (1.6) | |
Albumin (g/dL) | 3.6 (0.4) | - | |
IL-6 (pm/mL) | 32.5 (17.8–63.1) | - | |
NET/LYMA (k/μL) | 3.5 (2.3–5.6) | 3.6 (2.4–5.8) | |
Ferritin (ng/mL) | 577 (246–986) | - | |
Uric acid (mg/dL) | 4.5 (3.4–5.9) | - | |
Phosphorus (mg/dL) | 3.9 (0.7) | - | |
D-dimers (ng/mL) | 227 (145–387) | 243 (161–353) | |
Oxygen requirements N (%) | |||
Without support | 23 (22.5%) | 51 (50.0%) | |
≤4 L O2 | 34 (33.3%) | 15 (14.7%) | |
>4 L | 27 (26.5%) | 12 (11.8%) | |
High flow | 18 (17.6%) | 11 (10.8%) | |
Intubation | - | 11 (10.8%) |
28-Day Outcome | |
---|---|
PhA (Day 1) | p = 0.769 |
PhA (Day 7) | p = 0.807 |
HGS (Day 1) | p = 0.008 |
HGS (Day 7) | p = 0.476 |
LOS | Ferritin (ng/dL) | CRP (mg/dL) | Albumin (mg/dL) | |||||
---|---|---|---|---|---|---|---|---|
rs | p | rs | p | rs | p | rs | p | |
PhA (Day 1) | −0.081 | 0.422 | 0.092 | 0.370 | −0.043 | 0.680 | 0.286 | 0.006 |
HGS (Day 1) | 0.137 | 0.177 | - | - | - | - | - | - |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Papaemmanouil, A.; Bakaloudi, D.R.; Gkantali, K.; Kalopitas, G.; Metallidis, S.; Germanidis, G.; Chourdakis, M. Phase Angle and Handgrip Strength as Predictors of Clinical Outcomes in Hospitalized COVID-19 Patients. Nutrients 2023, 15, 1409. https://doi.org/10.3390/nu15061409
Papaemmanouil A, Bakaloudi DR, Gkantali K, Kalopitas G, Metallidis S, Germanidis G, Chourdakis M. Phase Angle and Handgrip Strength as Predictors of Clinical Outcomes in Hospitalized COVID-19 Patients. Nutrients. 2023; 15(6):1409. https://doi.org/10.3390/nu15061409
Chicago/Turabian StylePapaemmanouil, Androniki, Dimitra Rafailia Bakaloudi, Konstantina Gkantali, Georgios Kalopitas, Simeon Metallidis, Georgios Germanidis, and Michael Chourdakis. 2023. "Phase Angle and Handgrip Strength as Predictors of Clinical Outcomes in Hospitalized COVID-19 Patients" Nutrients 15, no. 6: 1409. https://doi.org/10.3390/nu15061409
APA StylePapaemmanouil, A., Bakaloudi, D. R., Gkantali, K., Kalopitas, G., Metallidis, S., Germanidis, G., & Chourdakis, M. (2023). Phase Angle and Handgrip Strength as Predictors of Clinical Outcomes in Hospitalized COVID-19 Patients. Nutrients, 15(6), 1409. https://doi.org/10.3390/nu15061409