Mineral metabolism and COVID-19: is there a connection?
- Authors: Maganeva I.S.1, Gorbacheva A.M.1, Bibik E.E.1, Aboisheva E.A.1, Eremkina A.K.1, Mokrysheva N.G.1
-
Affiliations:
- Endocrinology Research Centre
- Issue: Vol 93, No 10 (2021)
- Pages: 1227-1233
- Section: Reviews
- URL: https://journals.rcsi.science/0040-3660/article/view/86970
- DOI: https://doi.org/10.26442/00403660.2021.10.201114
- ID: 86970
Cite item
Full Text
Abstract
Due to global spread of COVID-19, the search for new factors that could influence its clinical course becomes highly important. This review summarize the relevant publications on the association between immune system and the main regulators of mineral homeostasis including. In addition, we have highlighted the various aspects of phosphorus-calcium metabolism related to the acute respiratory diseases and in particular to COVID-19. The data about the calcium-phosphorus metabolism in SARS-CoV-2 infection is required to understand the possible clinical implications and to develop new therapeutic and preventive interventions.
Full Text
##article.viewOnOriginalSite##About the authors
Irina S. Maganeva
Endocrinology Research Centre
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0002-0067-3622
врач-эндокринолог отд-ния патологии околощитовидных желез
Russian Federation, MoscowAnna M. Gorbacheva
Endocrinology Research Centre
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0003-2669-9457
науч. сотр. отд-ния патологии околощитовидных желез
Russian Federation, MoscowEkaterina E. Bibik
Endocrinology Research Centre
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0001-5952-5846
науч. сотр. отд-ния патологии околощитовидных желез
Russian Federation, MoscowElizaveta A. Aboisheva
Endocrinology Research Centre
Author for correspondence.
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0002-0306-6588
врач-эндокринолог отд-ния патологии околощитовидных желез
Russian Federation, MoscowAnna K. Eremkina
Endocrinology Research Centre
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0001-6667-062X
канд. мед. наук, зав. отд-нием патологии околощитовидных желез
Russian Federation, MoscowNatalia G. Mokrysheva
Endocrinology Research Centre
Email: lizaveta.aboisheva@gmail.com
ORCID iD: 0000-0002-9717-9742
проф. РАН, д-р мед. наук, дир. центра
Russian Federation, MoscowReferences
- Geara AS, Castellanos MR, Bassil C, et al. Effects of parathyroid hormone on immune function. Clin Dev Immunol. 2010;2010:418695. doi: 10.1155/2010/418695
- Yu M, D’Amelio P, Tyagi AM, et al. Regulatory T cells are expanded by Teriparatide treatment in humans and mediate intermittent PTH-induced bone anabolism in mice. EMBO Rep. 2018;19(1):156-71. doi: 10.15252/embr.201744421
- Martens P-J, Gysemans C, Verstuyf A, Mathieu AC. Vitamin D’s Effect on Immune Function. Nutrients. 2020;12(5):1248. doi: 10.3390/nu12051248
- Hsu Y-H, Chen HI. Acute respiratory distress syndrome associated with hypercalcemia without parathyroid disorders. Chin J Physiol. 2008;51(6):414-8.
- Grant WB, Lahore H, McDonnell SL, et al. Evidence that Vitamin D Supplementation Could Reduce Risk of Influenza and COVID-19 Infections and Deaths. Nutrients. 2020;12(4):988. doi: 10.3390/nu12040988
- Chen P, Trummel C, Horton J, et al. Production of osteoclast-activating factor by normal human peripheral blood rosetting and nonrosetting lymphocytes. Eur J Immunol. 1976;6(10):732-6. doi: 10.1002/eji.1830061014
- Milhaud G, Labat ML. Thymus and osteopetrosis. Clin Orthop Relat Res. 1978;135:260-71.
- Yoneda T, Mundy GR. Monocytes regulate osteoclast-activating factor production by releasing prostaglandins. J Exp Med. 1979;150(2):338-50. doi: 10.1084/jem.150.2.338
- Terauchi M, Li J-Y, Bedi B, et al. T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab. 2009;10(3):229-40. doi: 10.1016/j.cmet.2009.07.010
- Ohkura N, Kitagawa Y, Sakaguchi S. Development and maintenance of regulatory T cells. Immunity. 2013;38(3):414-23. doi: 10.1016/j.immuni.2013.03.002
- McCarthy TL, Centrella M, Canalis E. Parathyroid hormone enhances the transcript and polypeptide levels of insulin-like growth factor I in osteoblast-enriched cultures from fetal rat bone. Endocrinology. 1989;124(3):1247-53. doi: 10.1210/endo-124-3-1247
- Alexiewicz JM, Klinger M, Pitts TO, et al. Parathyroid hormone inhibits B cell proliferation: implications in chronic renal failure. J Am Soc Nephrol. 1990;1(3):236-44. doi: 10.1681/ASN.V13236
- Jiang Y, Yoshida A, Ishioka C, et al. Parathyroid hormone inhibits immunoglobulin production without affecting cell growth in human B cells. Clin Immunol Immunopathol. 1992;65(3):286-93. doi: 10.1016/0090-1229(92)90159-l
- Emam AA, Mousa SG, Ahmed KY, Al-Azab AA. Inflammatory biomarkers in patients with asymptomatic primary hyperparathyroidism. Med Princ Pract. 2012;21(3):249-53. doi: 10.1159/000334588
- Chertok-Shacham E, Ishay A, Lavi I, Luboshitzky R. Biomarkers of hypercoagulability and inflammation in primary hyperparathyroidism. Med Sci Monit Int Med J Exp Clin Res. 2008;14(12):CR628-32.
- Veldman CM, Cantorna MT, DeLuca HF. Expression of 1,25-dihydroxyvitamin D(3) receptor in the immune system. Arch Biochem Biophys. 2000;374(2):334-8. doi: 10.1006/abbi.1999.1605
- Booth DR, Ding N, Parnell GP, et al. Cistromic and genetic evidence that the vitamin D receptor mediates susceptibility to latitude-dependent autoimmune diseases. Genes Immun. 2016;17(4):213-9. doi: 10.1038/gene.2016.12
- Bilezikian JP, Bikle D, Hewison M, et al. MECHANISMS IN ENDOCRINOLOGY: Vitamin D and COVID-19. Eur J Endocrinol. 2020;183(5):R133-47. doi: 10.1530/eje-20-0665
- Wei R, Christakos S. Mechanisms Underlying the Regulation of Innate and Adaptive Immunity by Vitamin D. Nutrients. 2015;7(10):8251-60. DOI:10.3390%2Fnu7105392
- Christakos S, Hewison M, Gardner DG, et al. Vitamin D: beyond bone. Ann N Y Acad Sci. 2013;1287(1):45-58. DOI:10.1111%2Fnyas.12129
- Liu PT, Stenger S, Tang DH, Modlin RL. Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol. 2007;179(4):2060-3. doi: 10.4049/jimmunol.179.4.2060
- White JH. Vitamin D as an inducer of cathelicidin antimicrobial peptide expression: past, present and future. J Steroid Biochem Mol Biol. 2010;121(1-2):234-8. doi: 10.1016/j.jsbmb.2010.03.034
- Cantorna MT, Snyder L, Lin Y-D, Yang L. Vitamin D and 1,25(OH)2D regulation of T cells. Nutrients. 2015;7(4):3011-21. doi: 10.3390/nu7043011
- Amano Y, Komiyama K, Makishima M. Vitamin D and periodontal disease. J Oral Sci. 2009;51(1):11-20. doi: 10.2334/josnusd.51.11
- Chen S, Sims GP, Chen XX, et al. Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol. 2007;179(3):1634-47. doi: 10.4049/jimmunol.179.3.1634
- Rossaint J, Oehmichen J, Van Aken H, et al. FGF23 signaling impairs neutrophil recruitment and host defense during CKD. J Clin Invest. 2016;126(3):962-74. doi: 10.1172/jci83470
- Masuda Y, Ohta H, Morita Y, et al. Expression of Fgf23 in activated dendritic cells and macrophages in response to immunological stimuli in mice. Biol Pharm Bull. 2015;38(5):687-93. doi: 10.1248/bpb.b14-00276
- D’Elia JA, Weinrauch LA. Calcium Ion Channels: Roles in Infection and Sepsis Mechanisms of Calcium Channel Blocker Benefits in Immunocompromised Patients at Risk for Infection. Int J Mol Sci. 2018;19(9):2465. doi: 10.3390/ijms19092465
- Zheng L, Hunter K, Gaughan J, Poddar S. Preadmission Use of Calcium Channel Blockers and Outcomes After Hospitalization With Pneumonia: A Retrospective Propensity-Matched Cohort Study. Am J Ther. 2017;24(1):e30-8. doi: 10.1097/mjt.0000000000000312
- Lee C, Xu D-Z, Feketeova E, et al. Calcium entry inhibition during resuscitation from shock attenuates inflammatory lung injury. Shock. 2008;30(1):29-35. doi: 10.1097/shk.0b013e318145a589
- Nieto-Torres JL, Verdiá-Báguena C, Jimenez-Guardeño JM, et al. Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology. 2015;485:330-9. doi: 10.1016/j.virol.2015.08.010
- Millet JK, Whittaker GR. Physiological and molecular triggers for SARS-CoV membrane fusion and entry into host cells. Virology. 2018;517:3-8. doi: 10.1016/j.virol.2017.12.015
- Straus MR, et al. Ca2+ ions promote fusion of Middle East respiratory syndrome coronavirus with host cells and increase infectivity. J Virol. 2020;94:e00426-20. doi: 10.1128/JVI.00426-20
- Hoffmann HH, Schneider WM, Blomen VA, et al. Diverse Viruses Require the Calcium Transporter SPCA1 for Maturation and Spread. Cell Host Microbe. 2017;22(4):460-70.e5. doi: 10.1016/j.chom.2017.09.002
- Pizzorno A, Terrier O, Nicolas de Lamballerie C, et al. Repurposing of Drugs as Novel Influenza Inhibitors From Clinical Gene Expression Infection Signatures. Front Immunol. 2019;10:60. doi: 10.3389/fimmu.2019.00060
- Fujioka Y, Nishide S, Ose T, et al. A Sialylated Voltage-Dependent Ca(2+) Channel Binds Hemagglutinin and Mediates Influenza A Virus Entry into Mammalian Cells. Cell Host Microbe. 2018;23(6):809-18.e5. doi: 10.1016/j.chom.2018.04.015
- Di Filippo L, Formenti AM, Rovere-Querini P, et al. Hypocalcemia is highly prevalent and predicts hospitalization in patients with COVID-19. Endocrine. 2020;68(3):475-8. doi: 10.1007/s12020-020-02383-5
- Liu J, Han P, Wu J, et al. Prevalence and predictive value of hypocalcemia in severe COVID-19 patients, J Infect and Public Health. 2020;13(9):1224-8. doi: 10.1016/j.jiph.2020.05.029
- Lippi G, South AM, Henry BM. Electrolyte imbalances in patients with severe coronavirus disease 2019 (COVID-19). Ann Clin Biochem. 2020;57(3):262-5. doi: 10.1177/0004563220922255
- Torres B, Alcubilla P, González-Cordón A, et al. Impact of low serum calcium at hospital admission on SARS-CoV-2 infection outcome. Int J Infect Dis. 2020;104:164-8. doi: 10.1016/j.ijid.2020.11.207
- Wu Y, Hou B, Liu J, et al. Risk Factors Associated With Long-Term Hospitalization in Patients With COVID-19: A Single-Centered, Retrospective Study. Front Med (Lausanne). 2020;7:315. doi: 10.3389/fmed.2020.00315
- Sun JK, Zhang WH, Zou L, et al. Serum calcium as a biomarker of clinical severity and prognosis in patients with coronavirus disease 2019. Aging (Albany NY). 2020;12(12):11287-95. doi: 10.18632/aging.103526
- Маганева И.С., Еремкина А.К., Бибик Е.Е., и др. Статус минерального обмена у пациентов с COVID-19 при поступлении в стационар. Профилактическая медицина. 2020;23(8):64-73 [Maganeva IS, Eremkina AK, Bibik EE, et al. Status of mineral metabolism in patients with COVID-19 on admission to the hospital. Profilakticheskaia meditsina. 2020;23(8):64-73 (in Russian)]. doi: 10.17116/profmed20202308164
- Nijjer S, Ghosh AK, Dubrey SW. Hypocalcaemia, long QT interval and atrial arrhythmias. BMJ Case Rep. 2010;2010:bcr0820092216. doi: 10.1136/bcr.08.2009.2216
- Zivin JR, Gooley T, Zager RA, Ryan MJ. Hypocalcemia: a pervasive metabolic abnormality in the critically ill. Am J kidney Dis. 2001;37(4):689-98. doi: 10.1016/s0272-6386(01)80116-5
- Di Filippo L, Formenti AM, Doga M, et al. Hypocalcemia is a distinctive biochemical feature of hospitalized COVID-19 patients. Endocrine. 2021;71:9-13. doi: 10.1007/s12020-020-02541-9
- Cappellini F, Brivio R, Casati M, et al. Low levels of total and ionized calcium in blood of COVID-19 patients. Clinical Chemistry and Laboratory Medicine (CCLM). 2020;58(9):171-3. doi: 10.1515/cclm-2020-0611
- Tao RJ, Luo X-L, Xu W, et al. Viral infection in community acquired pneumonia patients with fever: a prospective observational study. J Thorac Dis. 2018;10(7):4387-95. doi: 10.21037/jtd.2018.06.33
- Zhang J, Zhao Y, Chen Y. Laboratory findings in patients with avian-origin influenza A (H7N9) virus infections. J Med Virol. 2014;86(5):895-8. doi: 10.1002/jmv.23780
- Song S-Z, Liu H-Y, Shen H, et al. Comparison of serum biochemical features between SARS and other viral pneumonias. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue. 2004;16(11):664-6.
- Singh VP, Khatua B, El-Kurdi B. Hypocalcemia and hypoalbuminemia during COVID-19 infection: Opportunities for therapeutic intervention. J Infect Public Health. 2020;13(12):1887. doi: 10.1016/j.jiph.2020.09.019
- Singh VP, Khatua B, El-Kurdi B, et al. Mechanistic basis and therapeutic relevance of hypocalcemia during severe COVID-19 infection. Endocrine. 2020;70:461-2. doi: 10.1007/s12020-020-02530-y
- di Filippo L, Formenti AM, Giustina A. Hypocalcemia: the quest for the cause of a major biochemical feature of COVID-19. Endocrine. 2020;70(3):463-4. doi: 10.1007/s12020-020-02525-9
- El-Kurdi B, Khatua B, Rood C, et al. Mortality From Coronavirus Disease 2019 Increases With Unsaturated Fat and May Be Reduced by Early Calcium and Albumin Supplementation. Gastroenterology. 2020;159(3):1015-8.e4. doi: 10.1053/j.gastro.2020.05.057
- Thomas T, Stefanoni D, Reisz JA, et al. COVID-19 infection alters kynurenine and fatty acid metabolism, correlating with IL-6 levels and renal status. JCI Insight. 2020;5(14):e140327. doi: 10.1172/jci.insight.140327
- Khatua B, Yaron JR, El-Kurdi B, et al. Ringer's Lactate Prevents Early Organ Failure by Providing Extracellular Calcium. J Clin Med. 2020;9(1):263. doi: 10.3390/jcm9010263
- Navina S, Acharya C, DeLany JP, et al. Lipotoxicity causes multisystem organ failure and exacerbates acute pancreatitis in obesity. Sci Transl Med. 2011;3(107):107ra110. doi: 10.1126/scitranslmed.3002573
- Мокрышева Н.Г. Околощитовидные железы. Первичный гиперпаратиреоз. М.: Медицинское информационное агентство, 2019 [Mokrysheva NG. Okoloshchitovidnye zhelezy. Pervichnyi giperparatireoz. Moscow: Meditsinskoe informatsionnoe agentstvo, 2019 (in Russian)].
- Hope-Simpson RE. The role of season in the epidemiology of influenza. J Hyg (Lond). 1981;86(1):35-47. doi: 10.1017/s0022172400068728
- Cannell JJ, Zasloff M, Garland CF, et al. On the epidemiology of influenza. Virol J. 2008;5:29. doi: 10.1186/1743-422X-5-29
- Cannell JJ, Vieth R, Umhau JC, et al. Epidemic influenza and vitamin D. Epidemiol Infect; 2006;134(6):1129-40. doi: 10.1017/s0950268806007175
- Grant WB, Giovannucci E. The possible roles of solar ultraviolet-B radiation and vitamin D in reducing case-fatality rates from the 1918–1919 influenza pandemic in the United States. Dermatoendocrinol. 2009;1(4):215-9. doi: 10.4161/derm.1.4.9063
- Berry DJ, Hesketh K, Power C, Hyppönen E. Vitamin D status has a linear association with seasonal infections and lung function in British adults. Br J Nutr. 2011;106(9):1433-40. doi: 10.1017/s0007114511001991
- Dancer RC, Parekh D, Lax S, et al. Vitamin D deficiency contributes directly to the acute respiratory distress syndrome (ARDS). Thorax. 2015;70(7):617-24. doi: 10.1136/thoraxjnl-2014-206680
- Esposito S, Lelii M. Vitamin D and respiratory tract infections in childhood. BMC Infect Dis. 2015;15:487. doi: 10.1186/s12879-015-1196-1
- Loeb M, Dang AD, Thiem VD, et al. Effect of Vitamin D supplementation to reduce respiratory infections in children and adolescents in Vietnam: A randomized controlled trial. Influenza Other Respi Viruses. 2019;13(2):176-83. doi: 10.1111/irv.12615
- Kühn J, Trotz P, Stangl GI. Prevalence of vitamin D insufficiency and evidence for disease prevention in the older population. Z Gerontol Geriatr. 2018;51(5):567-72. doi: 10.1007/s00391-018-1390-z
- Gois PHF, Ferreira D, Olenski S, Seguro AC. Vitamin D and Infectious Diseases: Simple Bystander or Contributing Factor? Nutrients. 2017;9(7):651. doi: 10.3390/nu9070651
- Zdrenghea MT, Makrinioti H, Bagacean C, et al. Vitamin D modulation of innate immune responses to respiratory viral infections. Rev Med Virol. 2017;27(1). doi: 10.1002/rmv.1909
- Urashima M, Mezawa H, Noya M, Camargo CA. Effects of vitamin D supplements on influenza A illness during the 2009 H1N1 pandemic: A randomized controlled trial. Food Funct. 2014;5(9):2365-70. doi: 10.1039/c4fo00371c
- Urashima M, Segawa T, Okazaki M, et al. Randomized trial of vitamin D supplementation to prevent seasonal influenza A in schoolchildren. Am J Clin Nutr. 2010;91(5):1255-60. doi: 10.3945/ajcn.2009.29094
- Zhou J, Du J, Huang L, et al. Preventive effects of Vitamin D on seasonal influenza a in infants: A multicenter, randomized, open, controlled clinical trial. Pediatr Infect Dis J. 2018;37(8):749-54. doi: 10.1097/inf.0000000000001890
- Arihiro S, Nakashima A, Matsuoka M, et al. Randomized Trial of Vitamin D Supplementation to Prevent Seasonal Influenza and Upper Respiratory Infection in Patients With Inflammatory Bowel Disease. Inflamm Bowel Dis. 2019;4;25(6):1088-95. doi: 10.1093/ibd/izy346
- Martineau AR, Jolliffe DA, Hooper RL, et al. Vitamin D supplementation to prevent acute respiratory tract infections: Systematic review and meta-analysis of individual participant data. BMJ. 2017;356;i6583. doi: 10.1136/bmj.i6583
- Pereira M, Dantas Damascena A, Galvão Azevedo LM, et al. Vitamin D deficiency aggravates COVID-19: systematic review and meta-analysis. Crit Rev Food Sci Nutr. 2020:1-9. doi: 10.1080/10408398.2020.1841090
- Hastie CE, Mackay DF, Ho F, et al. Vitamin D concentrations and COVID-19 infection in UK Biobank. Diabetes Metab Syndr. 2020;14(4):561-5. doi: 10.1016/j.dsx.2020.04.050
- Jakovac H. COVID-19 and vitamin D-Is there a link and an opportunity for intervention? Am J Physiol Endocrinol Metab. 2020;318(5):E589. doi: 10.1152/ajpendo.00138.2020
- McCartney DM, Byrne DG. Optimisation of Vitamin D Status for Enhanced Immuno-protection Against COVID-19. Ir Med J. 2020;113(4):58.
- Panarese A, Shahini E. Letter: COVID-19, and vitamin D. Aliment Pharmacol Ther. 2020;51(10):993-5. doi: 10.1111/apt.15752
- Rhodes JM, Subramanian S, Laird E, Kenny RA. Letter: low population mortality from COVID-19 in countries south of latitude 35° North supports vitamin D as a factor determining severity. Authors' reply. Aliment Pharmacol Ther. 2020;52(2):412-3. doi: 10.1111/apt.15823
- Marik PE, Kory P, Varon J. Does vitamin D status impact mortality from SARS-CoV-2 infection?. Med Drug Discov. 2020;6:100041. doi: 10.1016/j.medidd.2020.100041
- Garg M, Al-Ani A, Mitchell H, Hendy P, Christensen B. Editorial: low population mortality from COVID-19 in countries south of latitude 35 degrees North-supports vitamin D as a factor determining severity. Authors' reply. Aliment Pharmacol Ther. 2020;51(12):1438-9. doi: 10.1111/apt.15796