The Association between Vitamin D and Zinc Status and the Progression of Clinical Symptoms among Outpatients Infected with SARS-CoV-2 and Potentially Non-Infected Participants: A Cross-Sectional Study
Sahar Golabi, Maryam Adelipour, Sara Mobarak, Maghsud Piri, Maryam Seyedtabib, Reza Bagheri, Katsuhiko Suzuki, Damoon Ashtary-Larky, Fatemeh Maghsoudi, Mahshid Naghashpour
Nutrients, doi:10.3390/nu13103368
Vitamin D and zinc are important components of nutritional immunity. This study compared the serum concentrations of 25-hydroxyvitamin D (25(OH)D) and zinc in COVID-19 outpatients with those of potentially non-infected participants. The association of clinical symptoms with vitamin D and zinc status was also examined. A checklist and laboratory examination were applied to collect data in a cross-sectional study conducted on 53 infected outpatients with COVID-19 and 53 potentially non-infected participants. Serum concentration of 25(OH)D were not significantly lower in patients with moderate illness (19 ± 12 ng/mL) than patients with asymptomatic or mild illness (29 ± 18 ng/mL), with a trend noted for a lower serum concentration of 25(OH)D in moderate than asymptomatic or mild illness patients (p = 0.054). Infected patients (101 ± 18 µg/dL) showed a lower serum concentration of zinc than potentially non-infected participants (114 ± 13 µg/dL) (p = 0.01). Patients with normal (odds ratio (OR), 0.19; p ≤ 0.001) and insufficient (OR, 0.3; p = 0.007) vitamin D status at the second to seventh days of disease had decreased OR of general symptoms compared to patients with vitamin D deficiency. This study revealed the importance of 25(OH)D measurement to predict the progression of general and pulmonary symptoms and showed that infected patients had significantly lower zinc concentrations than potentially non-infected participants.
Informed Consent Statement: Informed consent was obtained from all participants involved in the study.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
Aftanas, Eyu, Varenik, Grabeklis, Kiselev et al., Element status of population of Central Federal Region
Aggarwal, Sentz, Miller, Role of Zinc Administration in Prevention of Childhood Diarrhea and Respiratory Illnesses: A Meta-analysis, Pediatrics,
doi:10.1542/peds.2006-3481
Akbar, Wibowo, Pranata, Setiabudiawan, Low Serum 25-hydroxyvitamin D (Vitamin D) Level Is Associated with Susceptibility to COVID-19, Severity, and Mortality: A Systematic Review and Meta-Analysis, Front. Nutr,
doi:10.3389/fnut.2021.660420
Alexander, Tinkov, Strand, Alehagen, Skalny et al., Early Nutritional Interventions with Zinc, Selenium and Vitamin D for Raising Anti-Viral Resistance Against Progressive COVID-19, Nutrients,
doi:10.3390/nu12082358
Anuk, Polat, Akdas, Erol, Tanacan et al., The Relation Between Trace Element Status (Zinc, Copper, Magnesium) and Clinical Outcomes in COVID-19 Infection During Pregnancy, Biol. Trace Element Res,
doi:10.1007/s12011-020-02496-y
Ashtary-Larky, Kheirollah, Bagheri, Ghaffari, Mard et al., A single injection of vitamin D3 improves insulin sensitivity and β-cell function but not muscle damage or the inflammatory and cardiovascular responses to an acute bout of resistance exercise in vitamin D-deficient resistance-trained males, Br. J. Nutr
Asl, Nikfarjam, Majidi Zolbanin, Nassiri, Jafari, Immunopharmacological perspective on zinc in SARS-CoV-2 infection, Int. Immunopharmacol,
doi:10.1016/j.intimp.2021.107630
Cakman, Kirchner, Rink, Zinc Supplementation Reconstitutes the Production of Interferon-α by Leukocytes from Elderly Persons, J. Interf. Cytokine Res,
doi:10.1089/jir.1997.17.469
Campbell, Spector, Toll-like receptor 8 ligands activate a vitamin D mediated autophagic response that inhibits human immunodeficiency virus type 1, PLoS Pathog,
doi:10.1371/journal.ppat.1003017
Carlucci, Ahuja, Petrilli, Rajagopalan, Jones et al., Zinc sulfate in combination with a zinc ionophore may improve outcomes in hospitalized COVID-19 patients, J. Med. Microbiol,
doi:10.1099/jmm.0.001250
Cereda, Bogliolo, Lobascio, Barichella, Zecchinelli et al., Vitamin D supplementation and outcomes in coronavirus disease 2019 (COVID-19) patients from the outbreak area of Lombardy, Italy, Nutrition,
doi:10.1016/j.nut.2020.111055
Fabri, Realegeno, Jo, Modlin, Role of autophagy in the host response to microbial infection and potential for therapy, Curr. Opin. Immunol,
doi:10.1016/j.coi.2010.10.010
Finzi, Harrington, Zinc treatment of outpatient COVID-19: A retrospective review of 28 consecutive patients, J. Med. Virol,
doi:10.1002/jmv.26812
Galmés, Serra, Palou, Current State of Evidence: Influence of Nutritional and Nutrigenetic Factors on Immunity in the COVID-19 Pandemic Framework, Nutrients,
doi:10.3390/nu12092738
Gay, Grimes, Idiopathic hypoparathyroidism with impaired vitamin B12 absorption and neuropathy, Can. Med. Assoc. J
Giménez, Bergam, Tajer, Antonietti, Inserra et al., Association Between Vitamin D Deficiency and COVID-19 Incidence, Complications, and Mortality in 46 Countries: An Ecological Study, Health Secur,
doi:10.1089/hs.2020.0137
Ginde, Mansbach, Camargo, Association Between Serum 25-Hydroxyvitamin D Level and Upper Respiratory Tract Infection in the Third National Health and Nutrition Examination Survey, Arch. Intern. Med,
doi:10.1001/archinternmed.2008.560
Gombart, Borregaard, Koeffler, Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3, FASEB J,
doi:10.1096/fj.04-3284com
Gombart, Pierre, Maggini, A Review of Micronutrients and the Immune System-Working in Harmony to Reduce the Risk of Infection, Nutrients,
doi:10.3390/nu12010236
Guan, Liang, Zhao, Liang, Chen et al., Comorbidity and its impact on 1590 patients with COVID-19 in China: A nationwide analysis, Eur. Respir. J,
doi:10.1183/13993003.00547-2020
Hastie, Mackay, Ho, Celis-Morales, Katikireddi et al., Vitamin D concentrations and COVID-19 infection in UK Biobank, Diabetes. Metab. Syndr,
doi:10.1016/j.dsx.2020.04.050
Ilie, Stefanescu, Smith, The role of vitamin D in the prevention of coronavirus disease 2019 infection and mortality, Aging Clin. Exp. Res,
doi:10.1007/s40520-020-01570-8
Jothimani, Kailasam, Danielraj, Nallathambi, Ramachandran et al., COVID-19: Poor outcomes in patients with zinc deficiency, Int. J. Infect. Dis
Karakochuk, Barr, Boy, Bahizire, Tugirimana et al., The effect of inflammation on serum zinc concentrations and the prevalence estimates of population-level zinc status among Congolese children aged 6-59 months, Eur. J. Clin. Nutr,
doi:10.1038/ejcn.2017.127
Khera, Singh, Purohit, Sharma, Singh, Prevalence of Zinc deficiency and effect of Zinc supplementation on prevention of acute respiratory infections: A non-randomized open label study, Turk. Thorac. J,
doi:10.5152/TurkThoracJ.2019.19020
Komolmit, Charoensuk, Thanapirom, Suksawatamnuay, Thaimai et al., Correction of vitamin D deficiency facilitated suppression of IP-10 and DPP IV levels in patients with chronic hepatitis C: A randomised double-blinded, placebo-control trial, PLoS ONE,
doi:10.1371/journal.pone.0174608
Korant, Kauer, Butterworth, Zinc ions inhibit replication of rhinoviruses, Nature,
doi:10.1038/248588a0
Lang, Hansen, Roscioli, Jones, Murgia et al., Dietary zinc mediates inflammation and protects against wasting and metabolic derangement caused by sustained cigarette smoke exposure in mice, BioMetals,
doi:10.1007/s10534-010-9370-9
Liu, Stenger, Li, Wenzel, Tan et al., Toll-Like Receptor Triggering of a Vitamin D-Mediated Human Antimicrobial Response, Science,
doi:10.1126/science.1123933
Macdonell, Miller, Harper, Reid, Haszard et al., A comparison of methods for adjusting biomarkers of iron, zinc, and selenium status for the effect of inflammation in an older population: A case for interleukin 6, Am. J. Clin. Nutr,
doi:10.1093/ajcn/nqy052
Mccarty, Sunlight exposure assessment: Can we accurately assess vitamin D exposure from sunlight questionnaires?, Am. J. Clin. Nutr,
doi:10.1093/ajcn/87.4.1097S
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
Oyagbemi, Ajibade, Aboua, Gbadamosi, Adedapo et al., Potential health benefits of zinc supplementation for the management of COVID-19 pandemic, J. Food Biochem,
doi:10.1111/jfbc.13604
Prasad, Discovery of Zinc for Human Health and Biomarkers of Zinc deficiency
Raoofi, Takian, Sari, Olyaeemanesh, Haghighi et al., COVID-19 Pandemic and Comparative Health Policy Learning in Iran, Arch. Iran. Med,
doi:10.34172/aim.2020.02
Ross, Taylor, Yaktine, Del Valle, Institute of Medicine (US) Committee to Review Dietary Reference Intakes for Vitamin D and Calcium Dietary Reference Intakes for Calcium and Vitamin D
Shakeri, Azimian, Ghasemzadeh-Moghaddam, Safdari, Haresabadi et al., Evaluation of the relationship between serum levels of zinc, vitamin B12, vitamin D, and clinical outcomes in patients with COVID-19, J. Med. Virol,
doi:10.1002/jmv.27277
Sharifi, Vahedi, Nedjat, Rafiei, Hosseinzadeh-Attar, Effect of single-dose injection of vitamin D on immune cytokines in ulcerative colitis patients: A randomized placebo-controlled trial, APMIS,
doi:10.1111/apm.12982
Skalny, Rink, Ajsuvakova, Aschner, Gritsenko et al., Zinc and respiratory tract infections: Perspectives for COVID-19, Int. J. Mol. Med,
doi:10.3892/ijmm.2020.4575
Sulli, Gotelli, Casabella, Paolino, Pizzorni et al., Vitamin D and Lung Outcomes in Elderly COVID-19 Patients, Nutrients,
doi:10.3390/nu13030717
Tabrizi, Moosazadeh, Akbari, Dabbaghmanesh, Mohamadkhani et al., High Prevalence of Vitamin D Deficiency among Iranian Population: A Systematic Review and Meta-Analysis, Iran. J. Med. Sci
Takeuti, Guimaraes, Guimaraes, Applications of vitamin D in sepsis prevention, Discov. Med
Ugbolue, Duclos, Urzeala, Berthon, Kulik et al., An Assessment of the Novel COVISTRESS Questionnaire: COVID-19 Impact on Physical Activity, Sedentary Action and Psychological Emotion, J. Clin. Med,
doi:10.3390/jcm9103352
Vankadari, Wilce, Emerging WuHan (COVID-19) coronavirus: Glycan shield and structure prediction of spike glycoprotein and its interaction with human CD26, Emerg. Microbes Infect,
doi:10.1080/22221751.2020.1739565
Velthuis, Worm, Sims, Snijder, Van Hemert, Zn2+ Inhibits Coronavirus and Arterivirus RNA Polymerase Activity In Vitro and Zinc Ionophores Block the Replication of These Viruses in Cell Culture, PLoS Pathog,
doi:10.1371/journal.ppat.1001176
Wang, Nestel, Bourdeau, Nagai, Wang et al., Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression, J. Immunol,
doi:10.4049/jimmunol.173.5.2909
Wessels, Haase, Engelhardt, Rink, Uciechowski, Zinc deficiency induces production of the proinflammatory cytokines IL-1β and TNFα in promyeloid cells via epigenetic and redox-dependent mechanisms, J. Nutr. Biochem,
doi:10.1016/j.jnutbio.2012.06.007
Wessels, Rolles, Slusarenko, Zinc deficiency as a possible risk factor for increased susceptibility and severe progression of Corona Virus Disease 19, Br. J. Nutr,
doi:10.1017/S0007114521000738
Xu, Tong, Wu, Zhao, Lin, Targeted oxidation strategy (TOS) for potential inhibition of coronaviruses by disulfiram-A 70-year old anti-alcoholism drug, ChemRxiv,
doi:10.26434/chemrxiv.11936292.v1
Zabetakis, Lordan, Norton, Tsoupras, COVID-19: The Inflammation Link and the Role of Nutrition in Potential Mitigation, Nutrients,
doi:10.3390/nu12051466
Zhang, Liu, Potential interventions for novel coronavirus in China: A systematic review, J. Med. Virol
Zhang, Penninger, Li, Zhong, Slutsky, Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: Molecular mechanisms and potential therapeutic target, Intensive Care. Med,
doi:10.1007/s00134-020-05985-9
Zhao, Ran, Jiang, Hu, Yu et al., Vitamin D Alleviates Rotavirus Infection through a Microrna-155-5p Mediated Regulation of the TBK1/IRF3 Signaling Pathway In Vivo and In Vitro, Int. J. Mol. Sci,
doi:10.3390/ijms20143562
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'series-title': 'Molecular, Genetic, and Nutritional Aspects of Major and Trace Minerals',
'first-page': '241',
'article-title': 'Discovery of Zinc for Human Health and Biomarkers of Zinc deficiency',
'author': 'Prasad',
'year': '2017'},
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{'key': 'ref18', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/S0140-6736(13)60222-6'},
{ 'key': 'ref19',
'series-title': 'Element Status of Population of Russia. Part II.',
'first-page': '430',
'article-title': 'Element status of population of Central Federal Region',
'author': 'Aftanas',
'year': '2011'},
{'key': 'ref20', 'doi-asserted-by': 'publisher', 'DOI': '10.1002/jmv.25707'},
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'first-page': '54',
'article-title': 'Idiopathic hypoparathyroidism with impaired vitamin B12 absorption and '
'neuropathy',
'volume': '107',
'author': 'Gay',
'year': '1972',
'journal-title': 'Can. Med. Assoc. J.'},
{'key': 'ref24'},
{ 'key': 'ref25',
'unstructured': 'COVID-19: Clinical '
'Featureshttps://www.uptodate.com/contents/covid-19-clinical-features#H2858229650'},
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'for Vitamin D and Calcium Dietary Reference Intakes for Calcium and '
'Vitamin D',
'author': 'Ross',
'year': '2011'},
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'first-page': '291',
'article-title': 'Applications of vitamin D in sepsis prevention',
'volume': '25',
'author': 'Takeuti',
'year': '2018',
'journal-title': 'Discov. Med.'},
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{'key': 'ref40', 'doi-asserted-by': 'publisher', 'DOI': '10.3390/ijms20143562'},
{'key': 'ref41', 'doi-asserted-by': 'publisher', 'DOI': '10.1111/apm.12982'},
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{'key': 'ref43', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/j.nut.2020.111055'},
{'key': 'ref44', 'doi-asserted-by': 'publisher', 'DOI': '10.1080/22221751.2020.1739565'},
{'key': 'ref45', 'doi-asserted-by': 'publisher', 'DOI': '10.1371/journal.pone.0174608'},
{'key': 'ref46', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/j.coi.2010.10.010'},
{'key': 'ref47', 'doi-asserted-by': 'publisher', 'DOI': '10.1371/journal.ppat.1003017'},
{'key': 'ref48', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/j.ijid.2020.09.014'},
{'key': 'ref49', 'doi-asserted-by': 'publisher', 'DOI': '10.1007/s12011-020-02496-y'},
{'key': 'ref50', 'doi-asserted-by': 'publisher', 'DOI': '10.1002/jmv.27277'},
{'key': 'ref51', 'doi-asserted-by': 'publisher', 'DOI': '10.1371/journal.pntd.0008895'},
{'key': 'ref52', 'doi-asserted-by': 'publisher', 'DOI': '10.1093/advances/nmz013'},
{'key': 'ref53', 'doi-asserted-by': 'publisher', 'DOI': '10.1542/peds.2006-3481'},
{'key': 'ref54', 'doi-asserted-by': 'publisher', 'DOI': '10.1002/jmv.26812'},
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{'key': 'ref56', 'doi-asserted-by': 'publisher', 'DOI': '10.3892/ijmm.2020.4575'},
{'key': 'ref57', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/j.intimp.2021.107630'},
{'key': 'ref58', 'doi-asserted-by': 'publisher', 'DOI': '10.1371/journal.ppat.1001176'},
{'key': 'ref59', 'doi-asserted-by': 'publisher', 'DOI': '10.1099/jmm.0.001250'},
{'key': 'ref60', 'doi-asserted-by': 'publisher', 'DOI': '10.2105/AJPH.2009.187773'},
{'key': 'ref61', 'doi-asserted-by': 'publisher', 'DOI': '10.26434/chemrxiv.11936292.v1'},
{'key': 'ref62', 'doi-asserted-by': 'publisher', 'DOI': '10.1038/248588a0'},
{'key': 'ref63', 'doi-asserted-by': 'publisher', 'DOI': '10.1089/jir.1997.17.469'},
{'key': 'ref64', 'doi-asserted-by': 'publisher', 'DOI': '10.1111/jfbc.13604'},
{'key': 'ref65', 'doi-asserted-by': 'publisher', 'DOI': '10.1007/s10534-010-9370-9'},
{'key': 'ref66', 'doi-asserted-by': 'publisher', 'DOI': '10.1016/j.jnutbio.2012.06.007'},
{'key': 'ref67', 'doi-asserted-by': 'publisher', 'DOI': '10.5152/TurkThoracJ.2019.19020'},
{'key': 'ref68', 'doi-asserted-by': 'publisher', 'DOI': '10.3390/nu12051466'},
{'key': 'ref69', 'doi-asserted-by': 'publisher', 'DOI': '10.1038/ejcn.2017.127'},
{'key': 'ref70', 'doi-asserted-by': 'publisher', 'DOI': '10.1093/ajcn/nqy052'}],
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'references-count': 70,
'journal-issue': {'issue': '10', 'published-online': {'date-parts': [[2021, 10]]}},
'alternative-id': ['nu13103368'],
'URL': 'http://dx.doi.org/10.3390/nu13103368',
'relation': {},
'ISSN': ['2072-6643'],
'subject': ['Food Science', 'Nutrition and Dietetics'],
'container-title-short': 'Nutrients',
'published': {'date-parts': [[2021, 9, 25]]}}