Association between Vitamin D Status and Risk of Developing Severe COVID-19 Infection: A Meta-Analysis of Observational Studies

Mohamed Ben-Eltriki; Robert Hopefl; James M. Wright; Subrata Deb

Mohamed Ben-Eltriki, Robert Hopefl, James M Wright, Subrata Deb

Journal of the American Nutrition Association, doi:10.1080/07315724.2021.1951891

Objective: The relationship between 25-hydroxyvitamin D3 (25(OH)D), the surrogate marker for vitamin D 3 , serum concentration and COVID-19 has come to the forefront as a potential pathway to improve COVID-19 outcomes. The current evidence remains unclear on the impact of vitamin D status on the severity and outcomes of COVID-19 infection. To explore possible association between low 25(OH)D levels and risk of developing severe COVID-19 (i.e. need for invasive mechanical ventilation, the length of hospital stay, total deaths). We also aimed to understand the relationship between vitamin D insufficiency and elevated inflammatory and cardiac biomarkers. Methods: We conducted a comprehensive electronic literature search for any original research study published up to March 30, 2021. For the purpose of this review, low vitamin D status was defined as a range of serum total 25(OH)D levels of <10 to <30 ng/ml. Two independent investigators assessed study eligibility, synthesized evidence, analyzed, critically examined, and interpreted herein. Results: Twenty-four observational studies containing 3637 participants were included in the meta-analysis. The mean age of the patients was 61.1 years old; 56% were male. Low vitamin D status was statistically associated with higher risk of death (RR, 1.60 (95% CI, 1.10-2.32), higher risk of developing severe COVID-19 pneumonia (RR: 1.50; 95% CI, 1.10-2.05). COVID-19 patients with low vitamin D levels had a greater prevalence of hypertension and cardiovascular diseases, abnormally high serum troponin and peak D-dimer levels, as well as elevated interleukin-6 and C-reactive protein than those with serum 25(OH)D levels ≥30 ng/ml. Conclusions: In this meta-analysis, we found a potential increased risk of developing severe COVID-19 infection among patients with low vitamin D levels. There are plausible biological mechanisms supporting the role of vitamin D in COVID-19 severity. Randomized controlled trials are needed to test for potential beneficial effects of vitamin D in COVID-19 outcomes.

Disclosure statement The authors declare that they have no conflicts of interest.

References

Abrishami, Dalili, Torbati, Asgari, Arab-Ahmadi et al., Possible association of vitamin D status with lung involvement and outcome in patients with COVID-19: a retrospective study, Eur J Nutr, doi:10.1007/s00394-020-02411-0

Adami, Giollo, Fassio, Benini, Bertoldo et al., Vitamin D and disease severity in coronavirus disease 19 (COVID-19), Reumatismo, doi:10.4081/reumatismo.2020.1333

Angelidi, Belanger, Lorinsky, Karamanis, Chamorro-Pareja et al., Vitamin D status is associated with in-hospital mortality and mechanical ventilation: a cohort of COVID-19 hospitalized patients, Mayo Clin Proc, doi:10.1016/j.mayocp.2021.01.001

Anjum, Examine the association between severe Vitamin D deficiency and mortality in patients with Covid-19, Pak J Med Health Sci

Baeke, Takiishi, Korf, Gysemans, Mathieu, Vitamin D: modulator of the immune system, Curr Opin Pharmacol, doi:10.1016/j.coph.2010.04.001

Bagri, Dahri, Legal, Hospital pharmacists' perceptions and decision-making related to drug-drug interactions, Can J Hosp Pharm

Baktash, Hosack, Patel, Shah, Kandiah et al., Vitamin D status and outcomes for hospitalised older patients with COVID-19, Postgrad Med J

Bassatne, Basbous, Chakhtoura, El Zein, Rahme et al., The link between COVID-19 and vitamin D (VIVID): a systematic review and meta-analysis, Metabolism, doi:10.1016/j.metabol.2021.154753

Beard, Bearden, Striker, Vitamin D and the anti-viral state, J Clin Virol, doi:10.1016/j.jcv.2010.12.006

Bhowmik, Tirtha, Iraganaboina, Eluru, A comprehensive analysis of COVID-19 transmission and mortality rates at the county level in the United States considering socio-demographics, health indicators, mobility trends and health care infrastructure attributes, PLoS One, doi:10.1371/journal.pone.0249133

Carpagnano, Lecce, Quaranta, Zito, Buonamico et al., Vitamin D deficiency as a predictor of poor prognosis in patients with acute respiratory failure due to COVID-19, J Endocrinol Invest, doi:10.1007/s40618-020-01370-x

Castillo, Costa, Barrios, Díaz, Miranda et al., Effect of calcifediol treatment and best available therapy versus best available therapy on intensive care unit admission and mortality among patients hospitalized for COVID-19: A pilot randomized clinical study, J Steroid Biochem Mol Biol, doi:10.1016/j.jsbmb.2020.105751

Cereda, Bogliolo, Klersy, Lobascio, Masi et al., Vitamin D 25OH deficiency in COVID-19 patients admitted to a tertiary referral hospital, Clin Nutr, doi:10.1016/j.clnu.2020.10.055

Charoenngam, Shirvani, Reddy, Vodopivec, Apovian et al., Association of vitamin D status with hospital morbidity and mortality in adult hospitalized patients with COVID-19, Endocr Pract

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, doi:10.1016/S0140-6736(20)30211-7

Cheng, Levine, Bell, Mangelsdorf, Russell, Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase, Proc Natl Acad Sci, doi:10.1073/pnas.0402490101

De Las Heras, Gimenez, Ferder, Manucha, Lahera, Implications of oxidative stress and potential role of mitochondrial dysfunction in COVID-19: therapeutic effects of vitamin D, Antioxidants, doi:10.3390/antiox9090897

De Lucena, Da, Santos, De Lima, De et al., Mechanism of inflammatory response in associated comorbidities in COVID-19, Diabetes Metab Syndr, doi:10.1016/j.dsx.2020.05.025

Demir, Demir, Aygun, Vitamin D deficiency is associated with COVID-19 positivity and severity of the disease, J Med Virol, doi:10.1002/jmv.26832

Dong, Mo, Hu, Qi, Jiang et al., Epidemiology of COVID-19 among children in China, Pediatrics, doi:10.1542/peds.2020-0702

Drincic, Fuller, Heaney, Armas, 25-Hydroxyvitamin D response to graded vitamin D 3 supplementation among obese adults, J Clin Endocrinol Metab, doi:10.1210/jc.2012-4103

Ejaz, Alsrhani, Zafar, Javed, Junaid et al., COVID-19 and comorbidities: deleterious impact on infected patients, J Infect Public Health, doi:10.1016/j.jiph.2020.07.014

Garg, Kalra, Mahalle, Defining vitamin D deficiency, using surrogate markers, Indian J Endocrinol Metab, doi:10.4103/2230-8210.117189

Gavioli, Miyashita, Hassaneen, Siau, An evaluation of serum 25-hydroxy vitamin D Levels in patients with COVID-19 in New York City, J Am Coll Nutr

Giustina, Bouillon, Binkley, Sempos, Adler et al., Controversies in vitamin D: a statement from the third international conference, JBMR Plus, doi:10.1002/jbm4.10417

Griffin, Hewison, Hopkin, Kenny, Quinton et al., Preventing vitamin D deficiency during the COVID-19 pandemic: UK definitions of vitamin D sufficiency and recommended supplement dose are set too low, Clin Med (Lond)), doi:10.7861/clinmed.2020-0858

Griffin, Xing, Kumar, Vitamin D and its analogs as regulators of immune activation and antigen presentation, Annu Rev Nutr, doi:10.1146/annurev.nutr.23.011702.073114

Hernandez, Nan, Fernandez-Ayala, Garcia-Unzueta, Hernandez-Hernandez et al., Vitamin D status in hospitalized patients with SARS-CoV-2 infection, J Clin Endocrinol Metab, doi:10.1210/clinem/dgaa733

Holick, Binkley, Bischoff-Ferrari, Gordon, Hanley et al., Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline, J Clin Endocrinol Metab, doi:10.1210/jc.2011-0385

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, Sci Rep, doi:10.1038/s41598-020-77093-z

Jevalikar, Mithal, Singh, Sharma, Farooqui et al., Lack of association of baseline 25-hydroxyvitamin D levels with disease severity and mortality in Indian patients hospitalized for COVID-19, Sci Rep, doi:10.1038/s41598-021-85809-y

Ji, Zhu, Zhong, Li, Pang et al., Association of elevated inflammatory markers and severe COVID-19: a meta-analysis, Medicine, doi:10.1097/MD.0000000000023315

Karahan, Katkat, Impact of serum 25(OH) vitamin D level on mortality in patients with COVID-19 in Turkey, J Nutr Health Aging, doi:10.1007/s12603-020-1479-0

Kerget, Kerget, Kızıltunç, Koçak, Araz et al., Evaluation of the relationship of serum vitamin D levels in COVID-19 patients with clinical course and prognosis, Tuberk Toraks, doi:10.5578/tt.70027

Levin, Hanage, Owusu-Boaitey, Cochran, Walsh et al., Assessing the age specificity of infection fatality rates for COVID-19: systematic review, meta-analysis, and public policy implications, Eur J Epidemiol, doi:10.1007/s10654-020-00698-1

Liberati, Altman, Tetzlaff, Mulrow, Gøtzsche et al., The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration, BMJ, doi:10.1136/bmj.b2700

Lui, Yip, Wong, Chow, Ho et al., Significantly lower case-fatality ratio of coronavirus disease 2019 (COVID-19) than Severe Acute Respiratory Syndrome (SARS) in Hong Kong-a territory-wide cohort study, Clin Infect Dis, doi:10.1093/cid/ciaa1187

Luo, Liao, Shen, Li, Cheng, Vitamin D deficiency is inversely associated with COVID-19 incidence and disease severity in Chinese people, J Nutr, doi:10.1093/jn/nxaa332

Maghbooli, Sahraian, Ebrahimi, Pazoki, Kafan et al., Vitamin D sufficiency, a serum 25-hydroxyvitamin D at least 30 ng/mL reduced risk for adverse clinical outcomes in patients with COVID-19 infection, PLoS One, doi:10.1371/journal.pone.0239799

Medrano, Carrillo-Cruz, Montero, Perez-Simon, Vitamin D: effect on haematopoiesis and immune system and clinical applications, Int J Mol Sci, doi:10.3390/ijms19092663

Mercola, Grant, Wagner, Evidence regarding vitamin D and risk of COVID-19 and its severity, Nutrients, doi:10.3390/nu12113361

Moher, Liberati, Tetzlaff, Altman, Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement, BMJ, doi:10.1136/bmj.b2535

Munshi, Hussein, Toraih, Elshazli, Jardak et al., Vitamin D insufficiency as a potential culprit in critical COVID-19 patients, J Med Virol, doi:10.1002/jmv.26360

Naserghandi, Allameh, Saffarpour, All about COVID-19 in brief, New Microbes New Infect, doi:10.1016/j.nmni.2020.100678

Onder, Rezza, Brusaferro, Case-fatality rate and characteristics of patients dying in relation to COVID-19 in Italy, JAMA, doi:10.1001/jama.2020.4683

Orchard, Baldry, Nasim-Mohi, Monck, Saeed et al., Vitamin D levels and intensive care unit outcomes of a cohort of critically ill COVID-19 patients, Clin Chem Lab Med, doi:10.1515/cclm-2020-1567

Pereira, Vitamin D deficiency aggravates COVID-19: systematic review and meta-analysis, Crit Rev Food Sci Nutr, doi:10.1080/10408398.2020.1841090

Pike, Christakos, Biology and mechanisms of action of the vitamin D hormone, Endocrinol Metab Clin North Am, doi:10.1016/j.ecl.2017.07.001

Piotrowska, Wierzbicka, Żmijewski, Vitamin D in the skin physiology and pathology, Acta Biochim Pol, doi:10.18388/abp.2015_1104

Radujkovic, Hippchen, Tiwari-Heckler, Dreher, Boxberger, Vitamin D deficiency and outcome of COVID-19 patients, Nutrients, doi:10.3390/nu12092757

Ricci, Pagliuca, ' Ascanio, Innammorato, Vitis et al., Circulating vitamin D levels status and clinical prognostic indices in COVID-19 patients, Respir Res, doi:10.1186/s12931-021-01666-3

Rosen, Abrams, Aloia, Brannon, Clinton et al., IOM committee members respond to Endocrine Society vitamin D guideline, J Clin Endocrinol Metab, doi:10.1210/jc.2011-2218

Shereen, Khan, Kazmi, Bashir, Siddique, COVID-19 infection: origin, transmission, and characteristics of human coronaviruses, J Adv Res, doi:10.1016/j.jare.2020.03.005

Smet, Smet, Herroelen, Gryspeerdt, Martens, Serum 25(OH)D level on hospital admission associated with COVID-19 stage and mortality, Am J Clin Pathol, doi:10.1093/ajcp/aqaa252

Sreedharan, Nair, Muttappallymyalil, Gopakumar, Eapen et al., Case fatality rates of COVID-19 across the globe: are the current draconian measures justified?, Z Gesundh Wiss, doi:10.1007/s10389-021-01491-4

Stroehlein, Wallqvist, Iannizzi, Mikolajewska, Metzendorf et al., Vitamin D supplementation for the treatment of COVID-19: a living systematic review, Cochrane Database Syst Rev, doi:10.1002/14651858.CD015043

Takeyama, Kitanaka, Sato, Kobori, Yanagisawa et al., 25-Hydroxyvitamin D3 1alpha-hydroxylase and vitamin D synthesis, Science, doi:10.1126/science.277.5333.1827

Tehrani, Khabiri, Moradi, Mosavat, Khabiri, Evaluation of vitamin D levels in COVID-19 patients referred to Labafinejad hospital in Tehran and its relationship with disease severity and mortality, Clin Nutr Espen, doi:10.1016/j.clnesp.2021.01.014

Vassiliou, Jahaj, Pratikaki, Orfanos, Dimopoulou et al., Low 25-hydroxyvitamin D levels on admission to the intensive care unit may predispose COVID-19 pneumonia patients to a higher 28-day mortality risk: a pilot study on a Greek ICU Cohort, Nutrients, doi:10.3390/nu12123773

Volkert, Beck, Cederholm, Goisser, Hooper et al., ESPEN guideline on clinical nutrition and hydration in geriatrics, Clin Nutr, doi:10.1016/j.clnu.2018.05.024

Walker, Deb, Ling, Wang, Assessing the elevation of cardiac biomarkers and the severity of COVID-19 infection: a meta-analysis, J Pharm Pharm Sci, doi:10.18433/jpps31501

White, Vitamin D signaling, infectious diseases, and regulation of innate immunity, Infect Immun, doi:10.1128/IAI.00353-08

Xu, Soruri, Gieseler, Peters, 1,25-Dihydroxyvitamin D3 exerts opposing effects to IL-4 on MHC class-II antigen expression, accessory activity, and phagocytosis of human monoc y t e s . S c a n d J Im mu n, doi:10.1111/j.1365-3083.1993.tb03237.x

Xu, Yang, Chen, Luo, Zhang et al., Vitamin D alleviates lipopolysaccharide-induced acute lung injury via regulation of the renin-angiotensin system, Mol Med Rep, doi:10.3892/mmr.2017.7546

Ye, Tang, Liao, Shaw, Deng et al., Does serum vitamin D level affect COVID-19 infection and its severity?-A case-control study, J Am Coll Nutr

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