The association between serum levels of micronutrients and the severity of disease in patients with COVID-19
Mohammad Taghi Beigmohammadi, M.D Sama Bitarafan, Alireza Abdollahi, Laya Amoozadeh, Faeze Salahshour, Maedeh Mahmoodi Ali Abadi, Danesh Soltani, Zoya Asl Motallebnejad
Nutrition, doi:10.1016/j.nut.2021.111400
This study aimed to compare the serum level of micronutrients with normal amounts, and assess their association with the severity of disease and inflammatory cytokines in patients with coronavirus disease 2019 (COVID-19). Methods: The present cross-sectional study included 60 patients admitted to the intensive care unit with COVID-19. We recorded data on demographic characteristics, anthropometric information, and medical history. Serum levels of inflammatory markers (erythrocyte sedimentation rate, C-reactive protein, interferongamma, tumor necrosis factor-alpha, interleukin-6), vitamins (A, B 9 , B 12 , C, D, E), and minerals (magnesium, zinc, iron) were measured. A radiologist assessed the severity of lung involvement according to patient computed tomography scans. The severity of illness was evaluated with the Acute Physiologic Assessment and Chronic Health Evaluation (APACHE) score, oxygen saturation, and body temperature. Independent associations among the serum levels of micronutrients with the severity of COVID-19 were measured. Results: Median patient age was 53.50 years (interquartile range, 12.75 years). Except for vitamin A and zinc, serum levels of other micronutrients were lower than the minimum normal. Patients with APACHE score 25 had a higher body mass index (P = 0.044), body temperature (P = 0.003), erythrocyte sedimentation rate (P = 0.008), C-reactive protein (P = 0.003), and lower oxygen saturation (P = 0.005), serum levels of vitamin D (P = < 0.001), and zinc (P = < 0.001) compared with patients with APACHE score <25. We found that lower serum levels of vitamin D, magnesium, and zinc were significantly and independently associated with higher APACHE scores (P = 0.001, 0.028, and < 0.001, respectively) and higher lung involvement (P = 0.002, 0.045, and < 0.001, respectively). Conclusions: Lower serum levels of vitamin D, zinc, and magnesium were involved in severe COVID-19.
Conclusions Low serum levels of some micronutrients, such as B9, B12, vitamins C and D, magnesium, and iron, were observed in patients with COVID-19. Furthermore, lower levels of vitamin D, zinc, and magnesium were correlated with more severe disease. We recommend identifying and addressing the deficiency of micronutrients that could be involved in immune system responses to prevent severe COVID-19 disease.
CRediT author statement Mohammad Taghi Beigmohammadi: Methodology, Investigation, Data Curation, Writing -Review & Editing; Sama Bitarafan: Conceptualization, Methodology, Visualization, Supervision, Project administration, Funding acquisition, Writing -Review & Editing; Alireza Abdollahi: Investigation, Resources; Laya Amoozadeh: Investigation, Data Curation, Visualization; Faeze Salahshour: Investigation, Resources, Data Curation; Maedeh Mahmoodi ali abadi: Investigation, Resources; Danesh Soltani: Formal analysis, Software, Writing -Review & Editing;Zoya Asl Motalebnegad: Formal analysis, Writing -Original Draft.
Conflict of interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
References
Abobaker, Alzwi, Alraied, Overview of the possible role of vitamin C in management of COVID-19, Pharmacol Rep
Alipio, Vitamin D supplementation could possibly improve clinical outcomes of patients infected with coronavirus
Annweiler, Corvaisier, Gautier, Dub Ee, Legrand et al., Vitamin D supplementation associated to better survival in hospitalized frail elderly COVID-19 patients: The GERIA-COVID quasi-experimental study, Nutrients
Arvinte, Singh, Marik, Serum levels of vitamin C and vitamin D in a cohort of critically ill COVID-19 patients of a North American community hospital intensive care unit in May 2020: A pilot study, Med Drug Discovery
Bernheim, Mei, Huang, Yang, Fayad et al., Chest CT findings in coronavirus disease-19 (COVID-19): Relationship to duration of infection, Radiology
Bouch, Thompson, Severity scoring systems in the critically ill, Cont Educ Anaesth Crit Care Pain
Calder, Carr, Gombart, Eggersdorfer, Optimal nutritional status for a well-functioning immune system is an important factor to protect against viral infections, Nutrients
Chen, Zhou, Dong, Qu, Gong et al., Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study, Lancet
Dai, Zeng, Cui, Wang, Feng et al., Prediction of COVID-19 patients at high risk of progression to severe disease, Front Public Health
Elm, Altman, Egger, Pocock, Gøtzsche et al., The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies, Ann Int Med
Fairfield, Fletcher, Vitamins for chronic disease prevention in adults: Scientific review, JAMA
Fletcher, Fairfield, Vitamins for chronic disease prevention in adults: Clinical applications, JAMA
Gombart, Pierre, Maggini, A review of micronutrients and the immune systemÀWorking in harmony to reduce the risk of infection, Nutrients
Gonçalves, Gonçalves, Guarnieri, Risegato, Guimarães et al., Association between low zinc levels and severity of acute respiratory distress syndrome by new coronavirus SARS-CoV-2, Nutr Clin Pract
Hu, Zhan, Chen, Ai, Xia, Chest CT findings related to mortality of patients with COVID-19: A retrospective case-series study, PLoS One
Huang, Wang, Li, Ren, Zhao et al., Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China, Lancet
Jain, Chaurasia, Sengar, Singh, Mahor et al., Analysis of vitamin D level among asymptomatic and critically ill COVID-19 patients and its correlation with inflammatory markers, Scientific Rep
Ji, Zhang, Xu, Chen, Yang et al., Prediction for progression risk in patients with COVID-19 pneumonia: The CALL Score, Clin Infect Dis
Jothimani, Kailasam, Danielraj, Nallathambi, Ramachandran et al., COVID-19: Poor outcomes in patients with zinc deficiency, Int J Infect Dis
Li, Sun, Han, Ying, Wang, A study on the predictors of disease severity of COVID-19, Med Sci Monit
Long, Montoya, Hertzmark, Santos, Rosado, A double-blind, randomized, clinical trial of the effect of vitamin A and zinc supplementation on diarrheal disease and respiratory tract infections in children in Mexico City, Mexico, Am J Clin Nutr
Manzanares, Dhaliwal, Jiang, Murch, Heyland, Antioxidant micronutrients in the critically ill: A systematic review and meta-analysis, Crit Care
Ong, Impact of nutritional epigenomics on disease risk and prevention: Introduction, J Nutrigenet Nutrigenomics
Pecora, Persico, Argentiero, Neglia, Esposito, The role of micronutrients in support of the immune response against viral infections, Nutrients
Pereira, Damascena, Azevedo, De Almeida Oliveira, Da et al., Vitamin D deficiency aggravates COVID-19: Systematic review and meta-analysis, Crit Rev Food Sci Nutr
Preiser, Ichai, Orban, Groeneveld, Metabolic response to the stress of critical illness, Br J Anaesth
Prelack, Sheridan, Micronutrient supplementation in the critically ill patient: Strategies for clinical practice, J Trauma
Shakoor, Feehan, Dhaheri, Ali, Platat et al., Immuneboosting role of vitamins D, C, E, zinc, selenium and omega-3 fatty acids: Could they help against COVID-19?, Maturitas
Singh, Can vitamins, as epigenetic modifiers, enhance immunity in COVID-19 patients with non-communicable disease?, Curr Nutr Rep
Skalny, Rink, Ajsuvakova, Aschner, Gritsenko et al., Zinc and respiratory tract infections: Perspectives for COVID-19, Int J Mol Med
Wong, Lam, Wu, Ip, Lee et al., Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome, Clin Exp Immunol
Wu, Mcgoogan, Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: Summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention, JAMA
Xu, Yang, Yang, Zou, Wang et al., Clinical course and predictors of 60-day mortality in 239 critically ill patients with COVID-19: A multicenter retrospective study from Wuhan. China, Crit Care
Yang, Yu, Xu, Shu, Liu et al., Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: A singlecentered, retrospective, observational study, Lancet Respir Med
Zabetakis, Lordan, Norton, Tsoupras, COVID-19: The inflammation link and the role of nutrition in potential mitigation, Nutrients
Zaim, Chong, Sankaranarayanan, Harky, COVID-19 and multi-organ response, Curr Probl Cardiol
Zhang, Zhou, Qiu, Feng, Feng et al., Clinical characteristics of 82 death cases with COVID-19, PLoS One
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"volume": "147",
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"DOI": "10.1093/bjaceaccp/mkn033",
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"doi-asserted-by": "crossref",
"journal-title": "PLoS One",
"key": "10.1016/j.nut.2021.111400_bib0016",
"volume": "15",
"year": "2020"
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"DOI": "10.1093/bja/aeu187",
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"author": "Preiser",
"doi-asserted-by": "crossref",
"first-page": "945",
"journal-title": "Br J Anaesth",
"key": "10.1016/j.nut.2021.111400_bib0017",
"volume": "113",
"year": "2014"
},
{
"DOI": "10.1186/cc11316",
"article-title": "Antioxidant micronutrients in the critically ill: A systematic review and meta-analysis",
"author": "Manzanares",
"doi-asserted-by": "crossref",
"first-page": "R66",
"journal-title": "Crit Care",
"key": "10.1016/j.nut.2021.111400_bib0018",
"volume": "16",
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},
{
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"author": "Prelack",
"first-page": "601",
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"volume": "51",
"year": "2001"
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"article-title": "Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: A single-centered, retrospective, observational study",
"author": "Yang",
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"key": "10.1016/j.nut.2021.111400_bib0020",
"volume": "8",
"year": "2020"
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"DOI": "10.3389/fpubh.2020.574915",
"article-title": "Prediction of COVID-19 patients at high risk of progression to severe disease",
"author": "Dai",
"doi-asserted-by": "crossref",
"first-page": "1",
"journal-title": "Front Public Health",
"key": "10.1016/j.nut.2021.111400_bib0021",
"volume": "8",
"year": "2020"
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"DOI": "10.1093/cid/ciaa414",
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"author": "Ji",
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"first-page": "1393",
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"key": "10.1016/j.nut.2021.111400_bib0022",
"volume": "71",
"year": "2020"
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"key": "10.1016/j.nut.2021.111400_bib0023",
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"author": "Pereira",
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