Coronavirus disease and dyslipidemia — is there an association?
DOI: 10.32364/2587-6821-2023-7-1-36-40
v. A. Akhmedov
omsk state medical university, omsk, russian federation
dyslipidemia is one of the most common comorbidities in patients infected with the sars-cov-2 coronavirus. In this review based on the up-to-date publications the authors assess the potential impact of dyslipidemia on the clinical course and prognosis in covid-19 infected patients, as well as the viral infection effects on the lipid profile in patients with dyslipidemia. The covid-19 driven inflammatory response leads to an increase in high-density lipoprotein (hdl) levels, modulation of apolipoproteins, increase in serum amyloid protein a concentration, and a decrease in apolipoprotein a-i, m and e levels, thus affecting the antioxidant, anti-inflammatory and immunomodulatory properties of hdl. The use of statins in patients with covid-19 may mitigate the risk of lipid disorders. By inhibiting endogenous cholesterol synthesis, statins reduce its amount in lipid rafts and therefore may limit the entry of the sars-cov-2 virus into host cells. Moreover, statins, by reducing the overexpression of proinflammatory cytokines, can counteract covid-19-associated cytokine storm.
keywords: covid-19, dyslipidemia, obesity, treatment, lipoproteins, statins, fibrates.
for citation: Akhmedov V. A. Coronavirus disease and dyslipidemia - is there an association? Russian medical inquiry. 2023;7(1):36-40 (in russ. ). Doi: 10.32364/2587-6821-2023-7-1-36-40.
About the author:
Vadim A. Akhmedov — Dr. Sc. (Med.), Professor, Head of the Department of Medical Rehabilitation of Additional Professional Education, Omsk State Medical University; 12, Lenin str., Omsk, 644099, Russian Federation; ORCID iD 0000-0002-7603-8481.
Contact information: Vadim A. Akhmedov, e-mail: v_akhmedov@mail.ru.
Financial Disclosure: the author has no a financial or property interest in any material or method mentioned.
There is no conflict of interests.
Received 06.12.2022.
Revised 29.12.2022.
Accepted 30.01.2023.
References
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11. Wei X., Zeng W., Su J. et al. Hypolipidemia is associated with the severity of COVID-19. J Clin Lipidol. 2020;14:297–304. DOI: 10.1016/j.jacl.2020.04.008.
12. Farid A.S., Horii Y. Modulation of paraoxonases during infectious diseases and its potential impact on atherosclerosis. Lipids Health Dis. 2012;11:92. DOI: 10.1186/1476-511X-11-92.
13. Ryoo S., Bhunia A., Chang F. et al. OxLDL-dependent activation of arginase II is dependent on the LOX-1 receptor and downstream RhoA signaling. Atherosclerosis. 2011;214:279–287. DOI: 10.1016/j.atherosclerosis.2010.10.044.
14. Stancel N., Chen C.C., Ke L.Y. et al. Interplay between CRP, Atherogenic LDL, and LOX-1 and its potential role in the pathogenesis of atherosclerosis. Clin Chem. 2016;62:320–327. DOI: 10.1373/clinchem.2015.243923.
15. Erol A. Role of oxidized LDL-induced "trained macrophages" in the pathogenesis of COVID-19 and benefits of pioglitazone: a hypothesis. Diabetes Metab Syndr Clin Res Rev. 2020;14:713–714. DOI: 10.1016/j.dsx.2020.05.007.
16. Masana L., Correig E., Ibarretxe D. et al. Low HDL and high triglycerides predict COVID-19 severity. Sci Rep. 2021;11(1):7217. DOI: 10.1038/s41598-021-86747-5.
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19. Rossi R., Talarico M., Coppi F., Boriani G. Protective role of statins in COVID 19 patients: importance of pharmacokinetic characteristics rather than intensity of action. Intern Emerg Med. 2020;15(8):1573–1576. DOI: 10.1007/s11739-020-02504-y.
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21. Iqbal Z., Ho J.H., Adam S. et al. Managing hyperlipidaemia in patients with COVID-19 and during its pandemic: an expert panel position statement from HEART UK. Atherosclerosis. 2020;313:126–136. DOI: 10.1016/j.atherosclerosis.2020.09.008.
22. Sterne J.A., Egger M., Smith G.D. Systematic reviews in health care: investigating and dealing with publication and other biases in metaanalysis. BMJ. 2001;323(7304):101–105. DOI: 10.1136/bmj.323.7304.101.
23. Tandaju J.R., Ii W., Barati-Boldaji R., Raeisi-Dehkordi H. Meta-analysis of statin and outcomes of coronavirus disease 2019 (COVID-19): reconsideration is needed. Nutr Metab Cardiovasc Dis. 2021;31(9):2737–2739. DOI: 10.1016/j.numecd.2021.06.009.
24. Hariyanto T.I., Kurniawan A. Authors' response: meta-analysis of statin and outcomes of coronavirus disease 2019 (COVID-19). Nutr Metab Cardiovasc Dis. 2021;31(9):2740–2742. DOI: 10.1016/j.numecd.2021.06.008.
25. Lu Y., Liu D.X., Tam J.P. Lipid rafts are involved in SARS-CoV entry into vero E6 cells. Biochem. Biophys. Res Commun. 2008;369:344–349. DOI: 10.1016/j.bbrc.2008.02.023.
26. Radenkovic D., Chawla S., Pirro M. et al. Cholesterol in relation to COVID-19: should we care about it? J Clin Med. 2020;9(6):1909. DOI: 10.3390/jcm9061909.
27. Reiner Ž., Hatamipour M., Banach M. et al. Statins and the COVID-19 main protease: in silico evidence on direct interaction. Arch Med Sci. 2020;16(3):490–496. DOI: 10.5114/aoms.2020.94655.
28. Baby K., Maity S., Mehta C.H. et al. Targeting SARS-CoV-2 RNA-dependent RNA polymerase: an in silico drug repurposing for COVID-19. F1000Res. 2020;9:1166. DOI: 10.12688/f1000research.26359.1.
29. Coomes E.A., Haghbayan H. Interleukin-6 in Covid-19: a systematic review and meta-analysis. Rev Med Virol. 2020;30(6):1–9. DOI: 10.1002/rmv.2141.
30. Henderson L.A., Cron R.Q. Macrophage activation syndrome and secondary Hemophagocytic Lymphohistiocytosis in childhood inflammatory disorders: diagnosis and management. Pediatr Drugs. 2020;22(1):29–44. DOI: 10.1007/s40272-019-00367-1.
31. Bonsu K.O., Reidpath D.D., Kadirvelu A. Effects of statin treatment on inflammation and cardiac function in heart failure: an adjusted indirect comparison Meta-analysis of randomized trials. Cardiovasc Ther. 2015;33(6):338–346. DOI: 10.1111/1755-5922.12150.
32. Pawlos A., Niedzielski M., Gorzelak-Pabiś P. et al. COVID-19: direct and indirect mechanisms of statins. Int J Mol Sci. 2021;22(8):4177. DOI: 10.3390/ijms22084177.
33. Chansrichavala P., Chantharaksri U., Sritara P., Chaiyaroj S.C. Atorvastatin attenuates TLR4-mediated NF-κB activation in a MyD88-dependent pathway. Asian Pac J Allergy Immunol. 2009;27:49–57.
34. Wang S., Xie X., Lei T. et al. Statins attenuate activation of the NLRP3 Inflammasome by oxidized LDL or TNF α in vascular endothelial cells through a PXR-dependent mechanism. Mol Pharmacol. 2017;92(3):256–264. DOI: 10.1124/mol.116.108100.
35. Oikonomou E., Siasos G., Zaromitidou M. et al. Atorvastatin treatment improves endothelial function through endothelial progenitor cells mobilization in ischemic heart failure patients. Atherosclerosis. 2015;238(2):159–164. DOI: 10.1016/j.atherosclerosis.2014.12.014.
36. Al-Samkari H., Karp Leaf R.S., Dzik W.H. et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020;136(4):489–500. DOI: 10.1182/blood.2020006520.
37. Biere-Rafi S., Hutten B.A., Squizzato A. et al. Statin treatment and the risk of recurrent pulmonary embolism. Eur Heart J. 2013;34(24):1800–1806. DOI: 10.1093/eurheartj/eht046.
38. Sahebkar A., Catena C., Ray K.K. et al. Impact of statin therapy on plasma levels of plasminogen activator inhibitor-1. A systematic review and meta-analysis of randomised controlled trials. Thromb Haemost. 2016;116(1):162–171. DOI: 10.1160/TH15-10-0770.
39. Sahebkar A., Serban C., Ursoniu S. et al. The impact of statin therapy on plasma levels of von Willebrand factor antigen: systematic review and meta-analysis of randomised placebo-controlled trials. Thromb Haemost. 2016;115(03):520–532. DOI: 10.1160/th15-08-0620.
40. Li G., Du L., Cao X. et al. Follow-up study on serum cholesterol profiles and potential sequelae in recovered COVID-19 patients. BMC Infect Dis. 2021;21(1):299. DOI: 10.1186/s12879-021-05984-1.
41. Yildirim M., Kayalar O., Atahan E., Oztay F. Anti-fibrotic effect of atorvastatin on the lung fibroblasts and myofibroblasts. Eur Resp J. 2018;52:PA991. DOI: 10.1183/13993003.congress-2018.PA991.
42. Yang T., Chen M., Sun T. Simvastatin attenuates TGF-β1-induced epithelialmesenchymal transition in human alveolar epithelial cells. Cell Physiol Biochem. 2013;31(6):863–874. DOI: 10.1159/000350104.
43. Saewong S., Thammasitboon K., Wattanaroonwong N. Simvastatin induces apoptosis and disruption of the actin cytoskeleton in human dental pulp cells and periodontal ligament fibroblasts. Arch Oral Biol. 2013;58(8):964–974. DOI: 10.1016/j.archoralbio.2013.03.002.
44. Lee R.-P., Lin N.T., Chao Y.-F.C. et al. High-density lipoprotein prevents organ damage in endotoxemia. Res Nurs Health. 2007;30(3):250–260. DOI: 10.1002/nur.20187.
45. Feingold K.R., Grunfeld C. Lipids: a key player in the battle between the host and microorganisms. J Lipid Res. 2012;53(12):2487–2489. DOI: 10.1194/jlr.E033407.
46. Stasi A., Franzin R., Fiorentino M. Multifaced roles of HDL in sepsis and SARS-CoV-2 infection: renal implications. Int J Mol Sci. 2021;22(11):5980. DOI: 10.3390/ijms22115980.
47. Hoxha M. What about COVID-19 and arachidonic acid pathway? Eur J Clin Pharmacol. 2020;76(11):1501–1504. DOI: 10.1007/s00228-020-02941-w.
48. Risé P., Pazzucconi F., Sirtori C.R., Galli C. Statins enhance arachidonic acid synthesis in hypercholesterolemic patients. Nutr Metab Cardiovasc Dis. 2001;11(2):88–94.
49. Goc A., Niedzwiecki A., Rath M. Polyunsaturated ω-3 fatty acids inhibit ACE2-controlled SARS-CoV-2 binding and cellular entry. Sci Rep. 2021;11(1):5207. DOI: 10.1038/s41598-021-84850-1.
50. Fijen L.M., Grefhorst A., Levels J.H.M. et al. Severe acquired hypertriglyceridemia following COVID-19 BMJ Case Rep. 2021;14:e246698. DOI: 10.1136/bcr-2021-246698.
51. Bhaskar S., Sinha A., Banach M. et al. Cytokine storm in COVID-19-immunopathological mechanisms, clinical considerations, and therapeutic approaches: the REPROGRAM Consortium Position Paper. Front Immunol. 2020;11:1648. DOI: 10.3389/fimmu.2020.01648.
2. Choi G.J., Kim H.M., Kang H. The potential role of dyslipidemia in COVID-19 severity: an umbrella review of systematic reviews. J Lipid Atheroscler. 2020;9:435. DOI: 10.12997/jla.2020.9.3.435.
3. Pranata R., Lim M.A., Yonas E. et al. Body mass index and outcome in patients with COVID-19: a dose-response meta-analysis. Diabetes Metab. 2021;47(2):101178. DOI: 10.1016/j.diabet.2020.07.005.
4. Lim M.A., Huang I., Yonas E. et al. A wave of non-communicable diseases following the COVID-19 pandemic. Diabetes Metab Syndr Clin Res Rev. 2020;14:979–980. DOI: 10.1016/j.dsx.2020.06.050.
5. Foley J., Robinson M., Ryan J., Cronin J. Impact of a National Lockdown on Cycling Injuries. Ir Med J. 2021;114(7):412.
6. Huang I., Pranata R., Lim M.A. et al. C-reactive protein, procalcitonin, D-dimer, and ferritin in severe coronavirus disease-2019: a meta-analysis. Ther Adv Respir Dis. 2020;14:175346662093717. DOI: 10.1177/1753466620937175.
7. Sorokin A.V., Karathanasis S.K., Yang Z.-H. et al. COVID-19-Associated dyslipidemia: implications for mechanism of impaired resolution and novel therapeutic approaches. FASEB J. 2020;34:9843–9853. DOI: 10.1096/fj.202001451.
8. Barter P.J., Nicholls S., Rye K.A. et al. Antiinflammatory properties of HDL. Circ Res. 2004;95:764–772. DOI: 10.1161/01.RES.0000146094.59640.13.
9. Feingold K.R., Krauss R.M., Pang M. et al. The hypertriglyceridemia of acquired immunodeficiency syndrome is associated with an increased prevalence of low density lipoprotein subclass pattern B. J Clin Endocrinol Metab. 1993;76:1423–1427. DOI: 10.1210/jcem.76.6.8501146.
10. Van Lenten B.J., Wagner A.C., Nayak D.P. et al. High-density lipoprotein loses its anti-inflammatory properties during acute influenza infection. Circulation. 2001;103:2283–2288. DOI: 10.1161/01.CIR.103.18.2283.
11. Wei X., Zeng W., Su J. et al. Hypolipidemia is associated with the severity of COVID-19. J Clin Lipidol. 2020;14:297–304. DOI: 10.1016/j.jacl.2020.04.008.
12. Farid A.S., Horii Y. Modulation of paraoxonases during infectious diseases and its potential impact on atherosclerosis. Lipids Health Dis. 2012;11:92. DOI: 10.1186/1476-511X-11-92.
13. Ryoo S., Bhunia A., Chang F. et al. OxLDL-dependent activation of arginase II is dependent on the LOX-1 receptor and downstream RhoA signaling. Atherosclerosis. 2011;214:279–287. DOI: 10.1016/j.atherosclerosis.2010.10.044.
14. Stancel N., Chen C.C., Ke L.Y. et al. Interplay between CRP, Atherogenic LDL, and LOX-1 and its potential role in the pathogenesis of atherosclerosis. Clin Chem. 2016;62:320–327. DOI: 10.1373/clinchem.2015.243923.
15. Erol A. Role of oxidized LDL-induced "trained macrophages" in the pathogenesis of COVID-19 and benefits of pioglitazone: a hypothesis. Diabetes Metab Syndr Clin Res Rev. 2020;14:713–714. DOI: 10.1016/j.dsx.2020.05.007.
16. Masana L., Correig E., Ibarretxe D. et al. Low HDL and high triglycerides predict COVID-19 severity. Sci Rep. 2021;11(1):7217. DOI: 10.1038/s41598-021-86747-5.
17. Yıldırım Ö.T., Kaya Ş. The atherogenic index of plasma as a predictor of mortality in patients with COVID-19. Heart Lung. 2021;50(2):329–333. DOI: 10.1016/j.hrtlng.2021.01.016.
18. Lee Н.-Y., Ahn J., Park J. et al. Beneficial effect of statins in COVID-19-related outcomes-brief report: a national population-based cohort study. Arterioscler Thromb Vasc Biol. 2021;41:175–182. DOI: 10.1161/ATVBAHA.121.316224.
19. Rossi R., Talarico M., Coppi F., Boriani G. Protective role of statins in COVID 19 patients: importance of pharmacokinetic characteristics rather than intensity of action. Intern Emerg Med. 2020;15(8):1573–1576. DOI: 10.1007/s11739-020-02504-y.
20. Cariou B., Goronflot T., Rimbert A. et al. Routine use of statins and increased COVID-19 related mortality in inpatients with type 2 diabetes: results from the CORONADO study. Diabetes Metab. 2021;47(2):101202. DOI: 10.1016/j.diabet.2020.10.001.
21. Iqbal Z., Ho J.H., Adam S. et al. Managing hyperlipidaemia in patients with COVID-19 and during its pandemic: an expert panel position statement from HEART UK. Atherosclerosis. 2020;313:126–136. DOI: 10.1016/j.atherosclerosis.2020.09.008.
22. Sterne J.A., Egger M., Smith G.D. Systematic reviews in health care: investigating and dealing with publication and other biases in metaanalysis. BMJ. 2001;323(7304):101–105. DOI: 10.1136/bmj.323.7304.101.
23. Tandaju J.R., Ii W., Barati-Boldaji R., Raeisi-Dehkordi H. Meta-analysis of statin and outcomes of coronavirus disease 2019 (COVID-19): reconsideration is needed. Nutr Metab Cardiovasc Dis. 2021;31(9):2737–2739. DOI: 10.1016/j.numecd.2021.06.009.
24. Hariyanto T.I., Kurniawan A. Authors' response: meta-analysis of statin and outcomes of coronavirus disease 2019 (COVID-19). Nutr Metab Cardiovasc Dis. 2021;31(9):2740–2742. DOI: 10.1016/j.numecd.2021.06.008.
25. Lu Y., Liu D.X., Tam J.P. Lipid rafts are involved in SARS-CoV entry into vero E6 cells. Biochem. Biophys. Res Commun. 2008;369:344–349. DOI: 10.1016/j.bbrc.2008.02.023.
26. Radenkovic D., Chawla S., Pirro M. et al. Cholesterol in relation to COVID-19: should we care about it? J Clin Med. 2020;9(6):1909. DOI: 10.3390/jcm9061909.
27. Reiner Ž., Hatamipour M., Banach M. et al. Statins and the COVID-19 main protease: in silico evidence on direct interaction. Arch Med Sci. 2020;16(3):490–496. DOI: 10.5114/aoms.2020.94655.
28. Baby K., Maity S., Mehta C.H. et al. Targeting SARS-CoV-2 RNA-dependent RNA polymerase: an in silico drug repurposing for COVID-19. F1000Res. 2020;9:1166. DOI: 10.12688/f1000research.26359.1.
29. Coomes E.A., Haghbayan H. Interleukin-6 in Covid-19: a systematic review and meta-analysis. Rev Med Virol. 2020;30(6):1–9. DOI: 10.1002/rmv.2141.
30. Henderson L.A., Cron R.Q. Macrophage activation syndrome and secondary Hemophagocytic Lymphohistiocytosis in childhood inflammatory disorders: diagnosis and management. Pediatr Drugs. 2020;22(1):29–44. DOI: 10.1007/s40272-019-00367-1.
31. Bonsu K.O., Reidpath D.D., Kadirvelu A. Effects of statin treatment on inflammation and cardiac function in heart failure: an adjusted indirect comparison Meta-analysis of randomized trials. Cardiovasc Ther. 2015;33(6):338–346. DOI: 10.1111/1755-5922.12150.
32. Pawlos A., Niedzielski M., Gorzelak-Pabiś P. et al. COVID-19: direct and indirect mechanisms of statins. Int J Mol Sci. 2021;22(8):4177. DOI: 10.3390/ijms22084177.
33. Chansrichavala P., Chantharaksri U., Sritara P., Chaiyaroj S.C. Atorvastatin attenuates TLR4-mediated NF-κB activation in a MyD88-dependent pathway. Asian Pac J Allergy Immunol. 2009;27:49–57.
34. Wang S., Xie X., Lei T. et al. Statins attenuate activation of the NLRP3 Inflammasome by oxidized LDL or TNF α in vascular endothelial cells through a PXR-dependent mechanism. Mol Pharmacol. 2017;92(3):256–264. DOI: 10.1124/mol.116.108100.
35. Oikonomou E., Siasos G., Zaromitidou M. et al. Atorvastatin treatment improves endothelial function through endothelial progenitor cells mobilization in ischemic heart failure patients. Atherosclerosis. 2015;238(2):159–164. DOI: 10.1016/j.atherosclerosis.2014.12.014.
36. Al-Samkari H., Karp Leaf R.S., Dzik W.H. et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020;136(4):489–500. DOI: 10.1182/blood.2020006520.
37. Biere-Rafi S., Hutten B.A., Squizzato A. et al. Statin treatment and the risk of recurrent pulmonary embolism. Eur Heart J. 2013;34(24):1800–1806. DOI: 10.1093/eurheartj/eht046.
38. Sahebkar A., Catena C., Ray K.K. et al. Impact of statin therapy on plasma levels of plasminogen activator inhibitor-1. A systematic review and meta-analysis of randomised controlled trials. Thromb Haemost. 2016;116(1):162–171. DOI: 10.1160/TH15-10-0770.
39. Sahebkar A., Serban C., Ursoniu S. et al. The impact of statin therapy on plasma levels of von Willebrand factor antigen: systematic review and meta-analysis of randomised placebo-controlled trials. Thromb Haemost. 2016;115(03):520–532. DOI: 10.1160/th15-08-0620.
40. Li G., Du L., Cao X. et al. Follow-up study on serum cholesterol profiles and potential sequelae in recovered COVID-19 patients. BMC Infect Dis. 2021;21(1):299. DOI: 10.1186/s12879-021-05984-1.
41. Yildirim M., Kayalar O., Atahan E., Oztay F. Anti-fibrotic effect of atorvastatin on the lung fibroblasts and myofibroblasts. Eur Resp J. 2018;52:PA991. DOI: 10.1183/13993003.congress-2018.PA991.
42. Yang T., Chen M., Sun T. Simvastatin attenuates TGF-β1-induced epithelialmesenchymal transition in human alveolar epithelial cells. Cell Physiol Biochem. 2013;31(6):863–874. DOI: 10.1159/000350104.
43. Saewong S., Thammasitboon K., Wattanaroonwong N. Simvastatin induces apoptosis and disruption of the actin cytoskeleton in human dental pulp cells and periodontal ligament fibroblasts. Arch Oral Biol. 2013;58(8):964–974. DOI: 10.1016/j.archoralbio.2013.03.002.
44. Lee R.-P., Lin N.T., Chao Y.-F.C. et al. High-density lipoprotein prevents organ damage in endotoxemia. Res Nurs Health. 2007;30(3):250–260. DOI: 10.1002/nur.20187.
45. Feingold K.R., Grunfeld C. Lipids: a key player in the battle between the host and microorganisms. J Lipid Res. 2012;53(12):2487–2489. DOI: 10.1194/jlr.E033407.
46. Stasi A., Franzin R., Fiorentino M. Multifaced roles of HDL in sepsis and SARS-CoV-2 infection: renal implications. Int J Mol Sci. 2021;22(11):5980. DOI: 10.3390/ijms22115980.
47. Hoxha M. What about COVID-19 and arachidonic acid pathway? Eur J Clin Pharmacol. 2020;76(11):1501–1504. DOI: 10.1007/s00228-020-02941-w.
48. Risé P., Pazzucconi F., Sirtori C.R., Galli C. Statins enhance arachidonic acid synthesis in hypercholesterolemic patients. Nutr Metab Cardiovasc Dis. 2001;11(2):88–94.
49. Goc A., Niedzwiecki A., Rath M. Polyunsaturated ω-3 fatty acids inhibit ACE2-controlled SARS-CoV-2 binding and cellular entry. Sci Rep. 2021;11(1):5207. DOI: 10.1038/s41598-021-84850-1.
50. Fijen L.M., Grefhorst A., Levels J.H.M. et al. Severe acquired hypertriglyceridemia following COVID-19 BMJ Case Rep. 2021;14:e246698. DOI: 10.1136/bcr-2021-246698.
51. Bhaskar S., Sinha A., Banach M. et al. Cytokine storm in COVID-19-immunopathological mechanisms, clinical considerations, and therapeutic approaches: the REPROGRAM Consortium Position Paper. Front Immunol. 2020;11:1648. DOI: 10.3389/fimmu.2020.01648.
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