Gender-related response of body systems in COVID-19 affects outcome

Cover Page


Cite item

Full Text

Abstract

Severe acute respiratory syndrome (SARS)-like coronavirus (SARS-CoV-2) is the seventh member of the coronaviruses (CoVs) family that infects humans and causes coronavirus disease 2019 (COVID-19), which is currently a global pandemic. Widespread secretion of cytokines has been shown to occur early in severe cases of the disease and can be an effective factor in the rapid progression of the disease. Systemic inflammation indicates an advanced stage of acute disease, which is characterized by multiple organ failure and elevated key inflammatory markers. Studies have shown a gender difference between the incidence and mortality of COVID-19. In this review, we investigated the gender difference in the systemic effects of COVID-19 and found that this gender difference exists especially in the respiratory, cardiovascular, liver, gastrointestinal and kidney systems. Due to the worse outcome of COVID in males, the role of female sex hormones in causing these gender differences is noticeable. There can be a systemic and local effect of female sex hormones, especially estrogen and possibly progesterone, on various cells. Among the effects of these hormones is the regulation of localized angiotensin-converting enzyme 2 (ACE2) levels. ACE2 is the route of entry for SARS-CoV-2 virus into the cell. It is hoped that this review would address gender differences for better management of COVID-19 treatment.

About the authors

M. Khaksari

Kerman University of Medical Sciences

Email: khaksari@kmu.ac.ir

MD, PhD, Professor of Physiology, Neuroscience Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences; Endocrinology and Metabolism Research Center, Institute of Basic and Clinical Physiology Sciences, Faculty of Medicine, Kerman University of Medical Sciences.

Kerman.

Iran, Islamic Republic of

N. Sabet

Kerman University of Medical Sciences

Email: nazanin_5157@yahoo.com

PhD (Physiology), Senior Assistant, Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences; Endocrinology and Metabolism Research Center, Institute of Basic and Clinical Physiology Sciences, Faculty of Medicine, Kerman University of Medical Sciences, Kerman, Iran; Department of Physiology and Pharmacology, Afzalipour Faculty of Medicine, Kerman University of Medical Sciences.

Kerman.

Iran, Islamic Republic of

Z. Soltani

Kerman University of Medical Sciences

Author for correspondence.
Email: soltaniy@yahoo.com

Zahra Soltani - MD, PhD, Professor of Physiology, Endocrinology and Metabolism Research Center, Institute of Basic and Clinical Physiology Sciences, Faculty of Medicine, Kerman University of Medical Sciences; Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences; Department of Physiology and Pharmacology, Afzalipour Faculty of Medicine, Kerman University of Medical Sciences.

Kerman.

Phone/fax: +98 3433257581.

Iran, Islamic Republic of

H. Bashiri

Kerman University of Medical Sciences; Sirjan University of Medical Sciences

Email: bashiry_h@yahoo.com

MD, PhD, Professor of Pharmacology, Neuroscience Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences; Sirjan Faculty of Medicine, Sirjan University of Medical Sciences.

Kerman; Sirjan.

Iran, Islamic Republic of

References

  1. Ackermann M., Verleden S.E., Kuehnel M., Haverich A., Welte T., Laenger F., Vanstapel A., Werlein C., Stark H., Tzankov A., Li W.W., Li V.W., Mentzer S.J., Jonigk D. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N. Engl. J. Med., 2020, vol. 383, no. 1, pp. 20–128. doi: 10.1056/NEJMoa2015432
  2. Amadori A., Zamarchi R., De Silvestro G., Forza G., Cavatton G., Danieli G.A., Clementi M., Chieco-Bianchi L. Genetic control of the CD4/CD8 T-cell ratio in humans. Nat. Med., 1995, vol. 11, no. 2, pp. 1279–1283. doi: 10.1038/nm1295-1279
  3. Baig A.M., Khaleeq A., Ali U., Syeda H. Evidence of the COVID-19 virus targeting the CNS: tissue distribution, host–virus interaction, and proposed neurotropic mechanisms. ACS Chem. Neurosci., 2020, vol. 11, no. 7, pp. 995–998. doi: 10.1021/acschemneuro.0c00122
  4. Bartz D., Chitnis T., Kaiser U.B., Rich-Edwards J.W., Rexrode K.M., Pennell P.B., Goldstein J.M., O’Neal M.A., LeBoff M., Behn M., Seely E.W., Joffe H., Manson J.E. Clinical advances in sex-and gender-informed medicine to improve the health of all: a review. JAMA Intern. Med., 2020, vol. 1804, no. 5, pp. 74–83. doi: 10.1001/jamainternmed.2019.7194
  5. Bernheim A., Mei X., Huang M., Yang Y., Fayad Z.A., Zhang N., Diao K., Lin B., Zhu X., Li K., Li S., Shan H., Jacobi A., Chung M. Chest CT findings in coronavirus disease-19 (COVID-19): relationship to duration of infection. Radiology, 2020: 200463. doi: 10.1148/radiol.2020200463
  6. Berthelot J.-M, Drouet L., Lioté F. Kawasaki-like diseases and thrombotic coagulopathy in COVID-19: delayed over-activation of the STING pathway? Emerg. Microbes Infect., 2020, vol. 9, no. 1, pp. 1514–1522. doi: 10.1080/22221751.2020.1785336
  7. Bhasin S., Brito J.P., Cunningham G.R., Hayes F.J., Hodis H.N., Matsumoto A.M., Snyder P.J., Swerdloff R.S., Wu F.C., Yialamas M.A. Testosterone therapy in men with hypogonadism: an Endocrine Society clinical practice guideline. J. Clin. Endocrin. Metabol., 2018, vol. 103, no. 5, pp. 1715–1744. doi: 10.1210/jc.2018-00229
  8. Bianco F., Ranieri A., Paterniti G., Pata F., Gallo G. Acute intestinal ischemia in a patient with COVID-19. Tech. Coloproctology, 2020, vol. 24: 1217–1218. doi: 10.1007/s10151-020-02255-0
  9. Binder E., Künzel H., Nickel T., Kern N., Pfennig A., Majer M., Uhr M., Ising M., Holsboer F. HPA-axis regulation at in-patient admission is associated with antidepressant therapy outcome in male but not in female depressed patients. Psychoneuroendocrinology, 2009, vol. 34, no. 1, pp. 99–109. doi: 10.1016/j.psyneuen.2008.08.018
  10. Blau F.D., Kahn L.M. Gender differences in pay. J. Econ. Perspect., 2000, vol. 14, no. 4, pp. 75–99. doi: 10.1257/jep.14.4.75
  11. Bloom P.P., Meyerowitz E.A., Reinus Z., Daidone M., Gustafson J., Kim A.Y., Schaefer E., Chung R.T. Liver biochemistries in hospitalized patients with COVID-19. Hepatology, 2021, vol. 73, no. 3, pp. 890–900. doi: 10.1002/hep.31326
  12. Bohmwald K., Galvez N., Ríos M., Kalergis A.M. Neurologic alterations due to respiratory virus infections. Front. Cell Neurosci., 2018, vol. 12: 386. doi: 10.3389/fncel.2018.00386
  13. Bösmüller H., Traxler S., Bitzer M., Häberle H., Raiser W., Nann D., Frauenfeld L., Vogelsberg A., Klingel K., Fend F. The evolution of pulmonary pathology in fatal COVID-19 disease: an autopsy study with clinical correlation. Virchows Archiv., 2020, vol. 477, no. 3, pp. 349–357. doi: 10.1007/s00428-020-02881-x
  14. Brown R.P., Josephs R.A. A burden of proof: Stereotype relevance and gender differences in math performance. J. Pers. Soc. Psychol., 1999, vol. 762, no. 2: 46. doi: 10.1037/0022-3514.76.2.246
  15. Bukowska A., Spiller L., Wolke C., Lendeckel U., Weinert S., Hoffmann J., Bornfleth P., Kutschka I., Gardemann A., Isermann B., Goette A. Protective regulation of the ACE2/ACE gene expression by estrogen in human atrial tissue from elderly men. Exp. Biol. Med. (Maywood), 2017, vol. 2421, no. 4, pp. 1412–1423. doi: 10.1177/1535370217718808
  16. Byrnes J.P., Miller D.C., Schafer W.D. Gender differences in risk taking: a meta-analysis. Psychol. Bull., 1999, vol. 125, no. 3, pp. 367–383.
  17. Chai X., Hu L., Zhang Y., Han W., Lu Z., Ke A., Zhou J., Shi G., Fang N., Fan J., Cai J., Fan J., Lan F. Specific ACE2 expression in cholangiocytes may cause liver damage after 2019-nCoV infection. Biorxiv, 2020. doi: 10.1101/2020.02.03.931766
  18. Channappanavar R., Fett C., Mack M., Ten Eyck P.P., Meyerholz D.K., Perlman S. Sex-based differences in susceptibility to severe acute respiratory syndrome coronavirus infection. J. Immunol., 2017, vol. 198, no. 10, pp. 4046–4053. doi: 10.4049/jimmunol.1601896
  19. Chappell M.C., Marshall A.C., Alzayadneh E.M., Shaltout H.A., Diz D.I. Update on the angiotensin converting enzyme 2-angiotensin (1–7)-Mas receptor axis: fetal programing, sex differences, and intracellular pathways. Front. Endocrinol., 2014, vol. 4: 201. doi: 10.3389/fendo.2013.00201
  20. Chen C., Zhang X., Ju Z., He W. Advances in the research of cytokine storm mechanism induced by Corona Virus Disease 2019 and the corresponding immunotherapies. Zhonghua Shao Shang Za Zhi, 2020, vol. 36, no. 6, pp. 471–475. doi: 10.3760/cma.j.cn501120-20200224-00088
  21. Chen N., Zhou M., Dong X., Qu J., Gong F., Han Y., Qiu Y., Wang J., Liu Y., Wei Y., Xia J., Yu T., Zhang X., Zhang L. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet, 2020, vol. 39510223, no. 5, pp. 507–513. doi: 10.1016/S0140-6736(20)30211-7
  22. Chen R., Liang W., Jiang M., Guan W., Zhan C., Wang T., Tang C., Sang L., Liu J., Ni Z., Hu Y., Liu L., Shan H., Lei C., Peng Y., Wei L., Liu Y., Hu Y., Peng P., Wang J., Liu J., Chen Z., Li G., Zheng Z., Qiu S., Luo J., Ye C., Zhu S., Liu X., Cheng L., Ye F., Zheng J., Zhang N., Li Y., He J., Li S., Zhong N; Medical Treatment Expert Group for COVID-19. Risk factors of fatal outcome in hospitalized subjects with coronavirus disease 2019 from a nationwide analysis in China. Chest. 2020, vol. 158, no. 1, pp. 97–105. doi: 10.1016/j.chest.2020.04.010
  23. Cheng Y., Luo R., Wang K., Zhang M., Wang Z., Dong L., Li J., Yao Y., Ge S., Xu G. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int., 2020, vol. 975, no. 8, pp. 829–838. doi: 10.1016/j.kint.2020.03.005
  24. Cheng Y., Luo R., Wang K., Zhang M., Wang Z., Dong L., Li J., Yao Y., Ge S., Xu G. Kidney impairment is associated with in-hospital death of COVID-19 patients. MedRxiv, 2020. doi: 10.1101/2020.02.18.20023242.
  25. Cobo G., Hecking M., Port F.K., Exner I., Lindholm B., Stenvinkel P., Carrero J.J. Sex and gender differences in chronic kidney disease: progression to end-stage renal disease and haemodialysis. Clin. Sci. (Lond.)., 2016, vol. 13014, no. 1, pp. 1147–1463. doi: 10.1042/CS20160047
  26. Conti P., Younes A. Coronavirus COV-19/SARS-CoV-2 affects women less than men: clinical response to viral infection. J. Biol. Regul. Homeost. Agents, 2020, vol. 342, no. 3, pp. 339–343. doi: 10.23812/Editorial-Conti-3
  27. Darnall B.D., Suarez E.C. Sex and gender in psychoneuroimmunology research: past, present and future. Brain Behav. Immun., 2009, vol. 235, no. 5, pp. 595–604. doi: 10.1016/j.bbi.2009.02.019
  28. Das G., Mukherjee N., Ghosh S. Neurological insights of COVID-19 pandemic. ACS Chem. Neurosci., 2020, vol. 119, no. 1, pp. 1206–1209. doi: 10.1021/acschemneuro.0c00201
  29. De Filippis F., Pellegrini N., Vannini L., Jeffery I.B., La Storia A., Laghi L., Serrazanetti D.I., Di Cagno R., Ferrocino I., Lazzi C., Turroni S., Cocolin L., Brigidi P., Neviani E., Gobbetti M., O’Toole P.W., Ercolini D. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. 2016, vol. 651, no. 11, pp. 1812–1821. doi: 10.1136/gutjnl-2015-309957
  30. Desforges M., Le Coupanec A., Dubeau P., Bourgouin A., Lajoie L., Dubé M., Talbot P.J. Human coronaviruses and other respiratory viruses: underestimated opportunistic pathogens of the central nervous system? Viruses. 2020, vol. 12, no. 1: 14. doi: 10.3390/v12010014
  31. Desforges M., Le Coupanec A., Stodola J.K., Meessen-Pinard M., Talbot P.J. Human coronaviruses: viral and cellular factors involved in neuroinvasiveness and neuropathogenesis. Virus Res., 2014, vol. 194, pp. 145–158. doi: 10.1016/j.virusres.2014.09.011
  32. Dhar D., Mohanty A. Gut microbiota and COVID-19-possible link and implications. Virus Res., 2020, vol. 285: 198018. doi: 10.1016/j.virusres.2020.198018
  33. Dobbs M.R. Toxic encephalopathy. Semin. Neurol., 2011, vol. 31, no. 2, pp. 184–193. doi: 10.1055/s-0031-1277989
  34. Earley Z.M., Akhtar S., Green S.J., Naqib A., Khan O., Cannon A.R., Hammer A.M., Morris N.L., Li X., Eberhardt J.M., Gamelli R.L., Kennedy R.H., Choudhry M.A. Burn injury alters the intestinal microbiome and increases gut permeability and bacterial translocation. PLoS One, 2015, vol. 10, no. 7: e0129996. doi: 10.1371/journal.pone.0129996
  35. Elkind M.S. Why now? Moving from stroke risk factors to stroke triggers. Curr. Opin. Neurol., 2007, vol. 20, no. 1, pp. 51–57. doi: 10.1097/WCO.0b013e328012da75
  36. Ellul M., Solomon T. Acute encephalitis — diagnosis and management. Clin. Med. (Lond)., 2018, vol. 18, no. 2, pp. 155–159. doi: 10.7861/clinmedicine.18-2-155
  37. Fan Z., Chen L., Li J., Cheng X., Yang J., Tian C., Zhang Y., Huang S., Liu Z., Cheng J. Clinical features of COVID-19-related liver damage. Clin. Gastroenterol. Hepatol., 2020, vol. 18, no. 7, pp. 1561–1566. doi: 10.1016/j.cgh.2020.04.002
  38. Fang Y., Zhang H., Xie J., Lin M., Ying L., Pang P., Ji W. Sensitivity of chest CT for COVID-19: comparison to RT-PCR. Radiology, 2020, vol. 296, no. 2, pp. 115–117. doi: 10.1148/radiol.2020200432
  39. Feng G., Zheng K.I., Yan Q.Q., Rios R.S., Targher G., Byrne C.D., Poucke S.V., Liu W.Y., Zheng M.H. COVID-19 and liver dysfunction: current insights and emergent therapeutic strategies. J. Clin. Transl. Hepatol., 2020, vol. 8, no. 1, pp. 18–24. doi: 10.14218/JCTH.2020.00018
  40. Ferreira A.J., Murça T.M., Fraga-Silva R.A., Castro C.H., Raizada M.K., Santos R.A. New cardiovascular and pulmonary therapeutic strategies based on the Angiotensin-converting enzyme 2/angiotensin-(1–7)/mas receptor axis. Int. J. Hypertens., 2012: 147825. doi: 10.1155/2012/147825
  41. Fischer M., Baessler A., Schunkert H. Renin angiotensin system and gender differences in the cardiovascular system. Cardiovasc. Res., 2002, vol. 53, no. 3, pp. 672–677. doi: 10.1155/2012/147825
  42. Fu W., Wang C., Zou L., Guo Y., Lu Z., Yan S., Mao J. Psychological health, sleep quality, and coping styles to stress facing the COVID-19 in Wuhan, China. Transl. Psychiatry, 2020, vol. 10: 225. doi: 10.1038/s41398-020-00913-3
  43. Gebhard C., Regitz-Zagrosek V., Neuhauser H.K., Morgan R., Klein S.L. Impact of sex and gender on COVID-19 outcomes in Europe. Biol. Sex Differ., 2020, vol. 11: 29. doi: 10.1186/s13293-020-00304-9
  44. Gemmati D., Bramanti B., Serino M.L., Secchiero P., Zauli G., Tisato V. COVID-19 and individual genetic susceptibility/receptivity: role of ACE1/ACE2 genes, immunity, inflammation and coagulation. Might the double X-chromosome in females be protective against SARS-CoV-2 compared to the single X-chromosome in males? Int. J. Mol. Sci., 2020, vol. 21, no. 10: 3474. doi: 10.3390/ijms21103474
  45. Gowrisankar Y.V., Clark M.A. Angiotensin II regulation of angiotensin-converting enzymes in spontaneously hypertensive rat primary astrocyte cultures. J. Neurochem., 2016, vol. 138, no. 1, pp. 74–85. doi: 10.1111/jnc.13641
  46. Grandi G., Facchinetti F., Bitzer J. The gendered impact of coronavirus disease (COVID-19): do estrogens play a role? Eur. J. Contracept. Reprod. Health Care, 2020, vol. 25, no. 3, pp. 233–234. doi: 10.1080/13625187.2020.1766017
  47. Gu J., Han B., Wang J. COVID-19: gastrointestinal manifestations and potential fecal–oral transmission. Gastroenterology, 2020, vol. 158, no. 6, pp. 1518–1519. doi: 10.1053/j.gastro.2020.02.054
  48. Guan W.J., Ni Z.Y., Hu Y., Liang W.H., Ou C.Q., He J.X., Liu L., Shan H., Lei C.L., Hui D.S.C., Du B., Li L.J., Zeng G., Yuen K.Y., Chen R.C., Tang C.L., Wang T., Chen P.Y., Xiang J., Li S.Y., Wang J.L., Liang Z.J., Peng Y.X., Wei L., Liu Y., Hu Y.H., Peng P., Wang J.M., Liu J.Y., Chen Z., Li G., Zheng Z.J., Qiu S.Q., Luo J., Ye C.J., Zhu S.Y., Zhong NS; China Medical Treatment Expert Group for COVID-19. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med., 2020, vol. 382, pp. 1708–1720. doi: 10.1056/NEJMoa2002032
  49. Guo J., Huang Z., Lin L., Lv J. Coronavirus disease 2019 (COVID-19) and cardiovascular disease: a viewpoint on the potential influence of angiotensin-converting enzyme inhibitors/angiotensin receptor blockers on onset and severity of severe acute respiratory syndrome coronavirus 2 infection. J. Am. Heart Assoc., 2020, vol. 9, no. 7: e016219. doi: 10.1161/JAHA.120.016219
  50. Guo Y.R., Cao Q.D., Hong Z.S., Tan Y.Y., Chen S.D., Jin H.J., Tan K.S., Wang D.Y., Yan Y. The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) outbreak–an update on the status. Mil. Med. Res., 2020, vol. 7: 11. doi: 10.1186/s40779-020-00240-0
  51. Haeggström A., Östberg B., Stjerna P., Graf P., Hallén H. Nasal mucosal swelling and reactivity during a menstrual cycle. ORL J. Otorhinolaryngol. Relat. Spec., 2000, vol. 62, no. 1, pp. 39–42. doi: 10.1159/000027713
  52. Haist S.A., Wilson J.F., Elam C.L., Blue A.V., Fosson S.E. The effect of gender and age on medical school performance: an important interaction. Adv. Health Sci. Educ. Theory Pract., 2000, vol. 5, no. 3, pp. 197–205. doi: 10.1023/A:1009829611335
  53. Hall A.B., Tolonen A.C., Xavier R.J. Human genetic variation and the gut microbiome in disease. Nat. Rev. Genet., 2017, vol. 181, no. 1, pp. 690–699. doi: 10.1038/nrg.2017.63
  54. Hall O.J., Limjunyawong N., Vermillion M.S., Robinson D.P., Wohlgemuth N., Pekosz A., Mitzner W., Klein S.L. Progesterone-based therapy protects against influenza by promoting lung repair and recovery in females. PLoS Pathog., 2016, vol. 12, no. 9: e1005840. doi: 10.1371/journal.ppat.1005840
  55. Harmer D., Gilbert M., Borman R., Clark K.L. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett., 2002, vol. 532, no. 1–2, pp. 107–110. doi: 10.1016/s0014-5793(02)03640-2
  56. Hashimoto T., Perlot T., Rehman A., Trichereau J., Ishiguro H., Paolino M., Sigl V., Hanada T., Hanada R., Lipinski S., Wild B., Camargo S.M., Singer D., Richter A., Kuba K., Fukamizu A., Schreiber S., Clevers H., Verrey F., Rosenstiel P., Penninger J.M. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature, 2012, vol. 487, no. 7408, pp. 77–81. doi: 10.1038/nature11228
  57. Hassanzadeh K., Perez Pena H., Dragotto J., Buccarello L., Iorio F., Pieraccini S., Sancini G., Feligioni M.Considerations around the SARS-CoV-2 Spike Protein with particular attention to COVID-19 brain infection and neurological symptoms. ACS Chem. Neurosci., 2020, vol. 11, no. 15, pp. 2361–2369. doi: 10.1021/acschemneuro.0c00373
  58. He J., Wu B., Chen Y., Tang J., Liu Q., Zhou S., Chen C., Qin Q., Huang K., Lv J., Chen Y., Peng D. Characteristic ECG manifestations in patients with COVID-19. Can. J. Cardiol., 2020, vol. 36, no. 6, pp. 966.e1–966.e4. doi: 10.1016/j.cjca.2020.03.028
  59. Hill-Burns E.M., Clark A.G. X-linked variation in immune response in Drosophila melanogaster. Genetics, 2009, vol. 183, no. 4, pp. 1477–1491. doi: 10.1534/genetics.108.093971
  60. Hirsch J.S., Ng J.H., Ross D.W., Sharma P., Shah H.H., Barnett R.L., Hazzan A.D., Fishbane S., Jhaveri KD; Northwell COVID-19 Research Consortium; Northwell Nephrology COVID-19 Research Consortium. Acute kidney injury in patients hospitalized with COVID-19. Kidney Int., 2020, vol. 98, no. 1, pp. 209–218. doi: 10.1016/j.kint.2020.05.006
  61. Hu X., Pan X., Zhou W., Gu X., Shen F., Yang B., Hu Zh. Clinical epidemiological analyses of overweight/obesity and abnormal liver function contributing to prolonged hospitalization in patients infected with COVID-19. Int. J. Obes., 2020, vol. 44, pp. 1784– 1789. doi: 10.1038/s41366-020-0634-3
  62. Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., Cheng Z., Yu T., Xia J., Wei Y., Wu W., Xie X., Yin W., Li H., Liu M., Xiao Y., Gao H., Guo L., Xie J., Wang G., Jiang R., Gao Z., Jin Q., Wang J., Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, vol. 395, no. 10223, pp. 497–506. doi: 10.1016/S0140-6736(20)30183-5
  63. Jain S., Workman V., Ganeshan R., Obasare E.R., Burr A., DeBiasi R.M., Freeman J.V., Akar J., Lampert R., Rosenfeld L.E. Enhanced electrocardiographic monitoring of patients with coronavirus disease 2019. Heart Rhythm., 2020, vol. 17, no. 9, pp. 1417–1422. doi: 10.1016/j.hrthm.2020.04.047
  64. Jefferson J.A., Nelson P.J., Najafian B., Shankland S.J. Podocyte disorders: core curriculum 2011. Am. J. Kidney Dis., 2011, vol. 58, no. 4, pp. 666–677. doi: 10.1053/j.ajkd.2011.05.032
  65. Ji H., Menini S., Zheng W., Pesce C., Wu X., Sandberg K. Role of angiotensin-converting enzyme 2 and angiotensin (1–7) in 17β-oestradiol regulation of renal pathology in renal wrap hypertension in rats. Exp. Physiol., 2008, vol. 93, no. 5, pp. 648–657. doi: 10.1113/expphysiol.2007.041392
  66. Jin J.M., Bai P., He W., Wu F., Liu X.F., Han D.M., Liu S., Yang J.K. Gender differences in patients with COVID-19: Focus on severity and mortality. Front. Public Health., 2020, vol. 8: 152. doi: 10.3389/fpubh.2020.00152
  67. Jordan R.E., Adab P., Cheng K. COVID-19: risk factors for severe disease and death. BMJ, 2020, vol. 368: m1198. doi: 10.1136/bmj.m1198
  68. Joyner J., Neves L.A., Granger J.P., Alexander B.T., Merrill D.C., Chappell M.C., Ferrario C.M., Davis W.P., Brosnihan K.B. Temporal-spatial expression of ANG-(1-7) and angiotensin-converting enzyme 2 in the kidney of normal and hypertensive pregnant rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, vol. 293, no. 1, pp. 169–177. doi: 10.1152/ajpregu.00387.2006
  69. Karaahmet F., Karaahmet O.Z. Potential effect of natural and anabolizan steroids in elderly patient with COVID-19. Med. Hypotheses. 2020, vol. 140: 109772. doi: 10.1016/j.mehy.2020.109772
  70. Kelly D.M., Jones T.H. Testosterone: a vascular hormone in health and disease. J. Endocrinol., 2013, vol. 217, no. 3, pp. 47–71. doi: 10.1530/JOE-12-0582
  71. Kissling S., Rotman S., Gerber C., Halfon M., Lamoth F., Comte D., Lhopitallier L., Sadallah S., Fakhouri F. Collapsing glomerulopathy in a COVID-19 patient. Kidney Int., 2020, vol. 98, no. 1, pp. 228–231. doi: 10.1016/j.kint.2020.04.006
  72. Klein S.L., Dhakal S., Ursin R.L., Deshpande S., Sandberg K., Mauvais-Jarvis F. Biological sex impacts COVID-19 outcomes. PLoS Pathog., 2020, vol. 16, no. 6: e1008570. doi: 10.1371/journal.ppat.1008570
  73. Kuba K., Imai Y., Rao S., Gao H., Guo F., Guan B., Huan Y., Yang P., Zhang Y., Deng W., Bao L., Zhang B., Liu G., Wang Z., Chappell M., Liu Y., Zheng D., Leibbrandt A., Wada T., Slutsky A.S., Liu D., Qin C., Jiang C., Penninger J.M. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat. Med., 2005, vol. 11, no. 8, pp. 875– 879. doi: 10.1038/nm1267
  74. Kypreos K.E., Zafirovic S., Petropoulou P.I., Bjelogrlic P., Resanovic I., Traish A., Isenovic E.R. Regulation of endothelial nitric oxide synthase and high-density lipoprotein quality by estradiol in cardiovascular pathology. J. Cardiovasc. Pharmacol. Ther., 2014, vol. 19, no. 3, pp. 256–268. doi: 10.1177/1074248413513499
  75. Larsen C., Bourne T., Wilson J., Saqqa O., Sharshir M. Collapsing glomerulopathy in a patient with coronavirus disease 2019 (COVID-19). Kidney Int. Rep., 2020, vol. 5, no. 6, pp. 935–939. doi: 10.1016/j.ekir.2020.04.002
  76. Leung W.K., To K.F., Chan P.K., Chan H.L., Wu A.K., Lee N., Yuen K.Y., Sung J.J. Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection. Gastroenterology, 2003, vol. 125, no. 4, pp. 1011–1017. doi: 10.1016/s0016-5085(03)01215-0
  77. Li H., Liu Z., Gou Y., Yu H., Siminelakis S., Wang S., Kong D., Zhou Y., Liu Z., Ding Y., Yao D. Estradiol mediates vasculo-protection via ERRα-dependent regulation of lipid and ROS metabolism in the endothelium. J. Mol. Cell Cardiol., 2015, vol. 87, pp. 92–101. doi: 10.1016/j.yjmcc.2015.08.008
  78. Li Y.C., Bai W.Z., Hashikawa T. The neuroinvasive potential of SARS-CoV-2 may play a role in the respiratory failure of COVID-19 patients. J. Med. Virol., 2020, vol. 92, no. 6, pp. 552–555. doi: 10.1002/jmv.25728
  79. Li Y., Li H., Fan R., Wen B., Zhang J., Cao X., Wang C., Song Z., Li S., Li X., Lv X., Qu X., Huang R., Liu W. Coronavirus infections in the central nervous system and respiratory tract show distinct features in hospitalized children. Intervirology, 2016, vol. 59, no. 3, pp. 163–169. doi: 10.1159/000453066
  80. Libert C., Dejager L., Pinheiro I. The X chromosome in immune functions: when a chromosome makes the difference. Nat. Rev. Immunol., 2010, vol. 10, no. 8, pp. 594–604. doi: 10.1038/nri2815
  81. Liu J., Ji H., Zheng W., Wu X., Zhu J.J., Arnold A.P., Sandberg K. Sex differences in renal angiotensin converting enzyme 2 (ACE2) activity are 17β-oestradiol-dependent and sex chromosome-independent. Biol. Sex Differ., 2010, vol. 1: 6. doi: 10.1186/2042-6410-1-6
  82. Looft T., Allen H.K. Collateral effects of antibiotics on mammalian gut microbiomes. Gut Microbes., 2012, vol. 3, no. 5, pp. 463– 467. doi: 10.4161/gmic.21288
  83. Maggio M., Basaria S., Ceda G.P., Ble A., Ling S.M., Bandinelli S., Valenti G., Ferrucci L. The relationship between testosterone and molecular markers of inflammation in older men. J. Endocrinol. Invest., 2005, vol. 28, no. 11, pp. 116–119.
  84. Magro C., Mulvey J.J., Berlin D., Nuovo G., Salvatore S., Harp J., Baxter-Stoltzfus A., Laurence J.Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases. Transl. Res., 2020, vol. 220, pp. 1–13. doi: 10.1016/j.trsl.2020.04.007
  85. Maleki Dana P., Sadoughi F., Hallajzadeh J., Asemi Z., Mansournia M.A., Yousefi B., Momen-Heravi M. An insight into the sex differences in COVID-19 patients: what are the possible causes? Prehosp. Disaster Med., 2020, pp. 1–4. doi: 10.1017/S1049023X20000837
  86. Mantovani A., Beatrice G., Dalbeni A. Coronavirus disease 2019 and prevalence of chronic liver disease: A meta-analysis. Liver Intern., 2020, vol. 40, no. 6, pp. 1316–1320. doi: 10.1111/liv.14465
  87. Mao L., Jin H., Wang M., Hu Y., Chen S., He Q., Chang J., Hong C., Zhou Y., Wang D., Miao X., Li Y., Hu B. Neurological manifestations of hospitalized patients with COVID-19 in Wuhan, China: a retrospective case series study. JAMA Neurol., 2020, vol. 77, no. 6, pp. 683–690. doi: 10.1001/jamaneurol.2020.1127
  88. Mauvais-Jarvis F., Klein S.L., Levin E.R. Estradiol, progesterone, immunomodulation, and COVID-19 outcomes. Endocrinol., 2020, vol. 161, no. 9: bqaa127. doi: 10.1210/endocr/bqaa127
  89. McGonagle D., O’Donnell J.S., Sharif K., Emery P., Bridgewod C. Immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia. Lancet Rheumatol., 2020, vol. 2, no. 7, pp. 437–445. doi: 10.1016/S2665-9913(20)30121-1
  90. Mehta P., McAuley D.F., Brown M., Sanchez E., Tattersall R.S., Manson J.J.; HLH Across Speciality Collaboration, UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet (Lond.), 2020, vol. 395 no. 10229, pp. 1033– 1034. doi: 10.1016/S0140-6736(20)30628-0
  91. Meng Y., Wu P., Lu W., Liu K., Ma K., Huang L., Cai J., Zhang H., Qin Y., Sun H., Ding W., Gui L., Wu P. Sex-specific clinical characteristics and prognosis of coronavirus disease-19 infection in Wuhan, China: a retrospective study of 168 severe patients. PLoS Pathog., 2020, vol. 16, no. 4: e1008520. doi: 10.1371/journal.ppat.1008520
  92. Mikkelsen K., Stojanovska L., Polenakovic M., Bosevski M., Apostolopoulos V. Exercise and mental health. Maturitas. 2017, vol. 106, pp. 48–56. doi: 10.1016/j.maturitas.2017.09.003
  93. Miller V., Larosa J., Barnabei V., Kessler C., Levin G., Smith-Roth A., Griffin M., Stoy D.B., Bush T., Zacur H., Foster D., Anderson J., McKenzie A., Miller S.C., Wood P., Stefanick M., Marcus R., Akana A., Heinrichs W., Kirchner C., O’Hanlan K., Ruyle M., Sheehan M., Judd H., Greendale G., Bayalos R., Lozano K., Kawakami K., Barrett-Connor E., Langer R., Kritz-Silverstein D., Carrion-Petersen M., Cavero C., Schrott H., Johnson S.R., Feddersen D., Krutzfeldt D.L., Benda J., Pauerstein C., Trabal J., Schenken R., Stern M., Rodriguez-Sifuentes M., Easton C., Hb W., Espeland M., Howard G., Byington R., Legault C., Shumaker S., Hogan P., Hire D., Wasilauskas C., James M.K., Lane K., Terrell T., Reece S., Pierce J., Snow M., Anthony S., Mebane-Sims I., Einhorn P., Hunsberger S., Waclawiw M., Lippel K., Lucas D.L., Verter J., Jackson S., Kelaghan J., Perlman J., Wolf P., McGowan J., Gordon S., Heyse S., Fradkin J., Sherman S., Page L., Sorenson A., Hulka B., Brody B., Burkman R., Heaney R., Krauss R., Roberts H., Wittes J., Riggs L., Moss R., Albers J., Marcovina S., Fineberg S., Tracy R., Merino M., Scully R., Livolsi V., Kessler G. Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA, 1995, vol. 273, no. 3, pp. 199–208. doi: 10.1001/jama.1995.03520270033028
  94. Mingels A.M.A., Kimenai D.M. Sex-related aspects of biomarkers in cardiac disease. Adv. Exp. Med. Biol., 2018, vol. 1065, pp. 545–564. doi: 10.1007/978-3-319-77932-4_33
  95. Mizuguchi M., Yamanouchi H., Ichiyama T., Shiomi M. Acute encephalopathy associated with influenza and other viral infections. Acta Neurol. Scand. Suppl., 2007, vol. 115, pp. 45–56.
  96. Mohamad N.V., Wong S.K., Wan Hasan W.N., Jolly J.J., Nur-Farhana M.F., Ima-Nirwana S., Chin K.Y. The relationship between circulating testosterone and inflammatory cytokines in men. Aging Male, 2019, vol. 22, no. 2, pp. 129–140. doi: 10.1080/13685538.2018.1482487
  97. Moieni M., Muscatell K.A., Jevtic I., Breen E.C., Irwin M.R., Eisenberger N.I. Sex differences in the effect of inflammation on subjective social status: a randomized controlled trial of endotoxin in healthy young adults. Front. Psychol., 2019: 02167. doi: 10.3389/fpsyg.2019.02167
  98. Moreau K.L. Intersection between gonadal function and vascular aging in women. J. Appl. Physiol. (1985), 2018, vol. 125, no. 12, pp. 1881–1887. doi: 10.1152/japplphysiol.00117.2018
  99. Moriguchi T., Harii N., Goto J., Harada D., Sugawara H., Takamino J., Ueno M., Sakata H., Kondo K., Myose N., Nakao A., Takeda M., Haro H., Inoue O., Suzuki-Inoue K., Kubokawa K., Ogihara S., Sasaki T., Kinouchi H., Kojin H., Ito M., Onishi H., Shimizu T., Sasaki Y., Enomoto N., Ishihara H., Furuya S., Yamamoto T., Shimada S. A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int. J. Infect. Dis., 2020, vol. 94, pp. 55–58. doi: 10.1016/j.ijid.2020.03.062
  100. Mosca A., Leclerc M., Hugot J.P. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? Front. Microbiol., 2016, vol. 7: 455. doi: 10.3389/fmicb.2016.00455
  101. Muhammad S., Haasbach E., Kotchourko M., Strigli A., Krenz A., Ridder D.A., Vogel A.B., Marti H.H., Al-Abed Y., Planz O., Schwaninger M. Influenza virus infection aggravates stroke outcome. Stroke, 2011, vol. 42, no. 3, pp. 783–791. doi: 10.1161/STROKEAHA.110.596783
  102. Nettleship J., Jones R., Channer K., Jones T. Testosterone and coronary artery disease. Advances in the management of testosterone deficiency. Front. Horm. Res. Basel, Karger, 2009, vol. 37, pp. 91–107. doi: 10.1159/000176047
  103. Nichols B., Jog P., Lee J.H., Blackler D., Wilmot M., D’Agati V., Markowitz G., Kopp J.B., Alper S.L., Pollak M.R., Friedman D.J. Innate immunity pathways regulate the nephropathy gene apolipoprotein L1. Kidney Int., 2015, vol. 87, no. 2, pp. 332–342. doi: 10.1038/ki.2014.270
  104. Oudit G.Y., Kassiri Z., Jiang C., Liu P.P., Poutanen S.M., Penninger J.M., Butany J. SARS-coronavirus modulation of myocardial ACE2 expression and inflammation in patients with SARS. Eur. J. Clin. Invest., 2009, vol. 39, no. 7, pp. 618–625. doi: 10.1111/j.1365-2362.2009.02153.x
  105. Papadopoulos V., Li L., Samplaski M. Why does COVID-19 kill more elderly men than women? Is there a role for testosterone? Andrology, 2021, vol. 9, no. 1, pp. 65–72. doi: 10.1111/andr.12868
  106. Peleg Y., Kudose S., D’Agati V, Siddall E., Ahmad S., Nickolas T., Kisselev S., Gharavi A., Canetta P. Acute kidney injury due to collapsing glomerulopathy following COVID-19 infection. Kidney Int. Rep., 2020, vol. 5, no. 6, pp. 940–945. doi: 10.1016/j.ekir.2020.04.017
  107. Phiel K.L., Henderson R.A., Adelman S.J., Elloso M.M. Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol. Lett., 2005, vol. 97, no. 1, pp. 107–113. doi: 10.1016/j.imlet.2004.10.007
  108. Piccinni M.P., Giudizi M.G., Biagiotti R., Beloni L., Giannarini L., Sampognaro S., Parronchi P., Manetti R., Annunziato F., Livi C. Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J. Immunol., 1995, vol. 155, no. 1, pp. 128–133.
  109. Pinzon R.T., Wijaya V.O., Buana R.B., Al Jody A., Nunsio P.N. Neurologic characteristics in coronavirus disease 2019 (COVID-19): a systematic review and meta-analysis. Front. Neurol., 2020, vol. 11: 565. doi: 10.3389/fneur.2020.00565
  110. Pirola C.J., Sookoian S.C. COVID-19 and ACE2 in the liver and gastrointestinal tract: Putative biological explanations of sexual dimorphism. Gastroenterology, 2020, vol. 159, no. 4, pp. 1620–1621. doi: 10.1053/j.gastro.2020.04.050
  111. Pisitkun P., Deane J.A., Difilippantonio M.J., Tarasenko T., Satterthwaite A.B., Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science, 2006, vol. 312, no. 5780, pp. 1669–1672. doi: 10.1126/science.1124978
  112. Poyiadji N., Shahin G., Noujaim D., Stone M., Patel S., Griffith B. COVID-19–associated acute hemorrhagic necrotizing encephalopathy: CT and MRI features. Radiology, 2020, vol. 296, no. 2, pp. E119–E120. doi: 10.1148/radiol.2020201187
  113. Regitz-Zagrosek V., Oertelt-Prigione S., Seeland U., Hetzer R. Sex and gender differences in myocardial hypertrophy and heart failure. Circ. J., 2010, vol. 74, no. 7, pp. 1265–1273. doi: 10.1253/circj.cj-10-0196
  114. Rettew J.A., Huet-Hudson Y.M., Marriott I. Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod., 2008, vol. 78, no. 3, pp. 432–437. doi: 10.1095/biolreprod.107.06354
  115. Romero-Sánchez C.M., Díaz-Maroto I., Fernández-Díaz E., Sánchez-Larsen Á., Layos-Romero A., García-García J., González E., Redondo-Peñas I., Perona-Moratalla A.B., Del Valle-Pérez J.A., Gracia-Gil J., Rojas-Bartolomé L., Feria-Vilar I., Monteagudo M., Palao M., Palazón-García E., Alcahut-Rodríguez C., Sopelana-Garay D., Moreno Y., Ahmad J., Segura T. Neurologic manifestations in hospitalized patients with COVID-19: The ALBACOVID registry. Neurology, 2020, vol. 95, no. 8, pp. 1060–1070. doi: 10.1212/WNL.0000000000009937
  116. Ronco C., Reis T. Kidney involvement in COVID-19 and rationale for extracorporeal therapies. Nat. Rev. Nephrol., 2020, vol. 16, pp. 308–310. doi: 10.1038/s41581-020-0284-7
  117. Ronco C., Reis T., Husain-Syed F. Management of acute kidney injury in patients with COVID-19. Lancet Respir. Med., 2020, vol. 8, no. 7, pp. 738–742. doi: 10.1016/S2213-2600(20)30229-0
  118. Rossi A. Imaging of acute disseminated encephalomyelitis. Neuroimaging Clin. N. Am., 2008, vol. 18, no. 1, pp. 149–161. doi: 10.1016/j.nic.2007.12.007
  119. Ruan Q., Yang K., Wang W., Jiang L., Song J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med., 2020, vol. 46, no. 5, pp. 846–848. doi: 10.1007/s00134-020-05991-x
  120. Santos R.A.S., Sampaio W.O., Alzamora A.C., Motta-Santos D., Alenina N., Bader M., Campagnole-Santos M.J. The ACE2/angiotensin-(1–7)/MAS axis of the renin-angiotensin system: focus on angiotensin-(1–7). Physiol. Rev., 2018, vol. 98, no. 1, pp. 505–553. doi: 10.1152/physrev.00023.2016
  121. Sarkaki A.R., Khaksari H.M., Soltani Z., Shahrokhi N., Mahmoodi M. Time-and dose-dependent neuroprotective effects of sex steroid hormones on inflammatory cytokines after a traumatic brain injury. J. Neurotrauma., 2013, vol. 30, no. 1, pp. 47–54. doi: 10.1089/neu.2010.1686
  122. Seeland U., Regitz-Zagrosek V. Sex and gender differences in pharmacology. Handb. Exp. Pharmacol., 2012, vol. 214, pp. 13–22. doi: 10.1007/978-3-642-30726-3_1
  123. Shenoy V., Grobe J.L., Qi Y., Ferreira A.J., Fraga-Silva R.A., Collamat G., Bruce E., Katovich M.J. 17-Estradiol modulates local cardiac renin-angiotensin system to prevent cardiac remodeling in the DOCA-salt model of hypertension in rats. Peptides, 2009, vol. 30, no. 12, pp. 2309–2315. doi: 10.1016/j.peptides.2009.09.005
  124. Shi S., Qin M., Shen B., Cai Y., Liu T., Yang F., Gong W., Liu X., Liang J., Zhao Q., Huang H., Yang B., Huang C. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiology, 2020, vol. 5, no. 7, pp. 802–810. doi: 10.1001/jamacardio.2020.0950
  125. Siddiqi H.K., Mehra M.R. COVID-19 illness in native and immunosuppressed states: a clinical–therapeutic staging proposal. J. Heart Lung Transplant., 2020, vol. 39, no. 5, pp. 405–407. doi: 10.1016/j.healun.2020.03.012
  126. Sierpiński R., Pinkas J., Jankowski M., Zgliczyński W.S., Wierzba W., Gujski M., Szumowski Ł. Gender differences in the frequency of gastrointestinal symptoms and olfactory or taste disorders among 1942 non-hospitalized patients with COVID-19. Pol. Arch. Intern. Med., 2020, vol. 130, no. 6, pp. 501–505. doi: 10.20452/pamw.15414
  127. Simonnet A., Chetboun M., Poissy J., Raverdy V., Noulette J., Duhamel A., Labreuche J., Mathieu D., Pattou F., Jourdain M; LICORN and the Lille COVID-19 and Obesity study group. High prevalence of obesity in severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) requiring invasive mechanical ventilation. Obesity, 2020, vol. 28, no. 7, pp. 1195–1199. doi: 10.1002/oby.22831
  128. Soltani Z., Shahrokhi N., Karamouzian S., Khaksari M., Mofid B., Nakhaee N., Reihani H. Does progesterone improve outcome in diffuse axonal injury? Brain Inj., 2017, vol. 31, no. 1, pp. 16–23. doi: 10.1080/02699052.2016.1213421
  129. Spagnolo P.A., Manson J.E., Joffe H. Sex and gender differences in health: What the COVID-19 pandemic can teach us. Ann. Intern. Med., 2020, vol. 173, no. 5, pp. 385–386. doi: 10.7326/M20-1941
  130. Stanhewicz A.E., Wenner M.M., Stachenfeld N.S. Sex differences in endothelial function important to vascular health and overall cardiovascular disease risk across the lifespan. Am. J. Physiol. Heart Circ. Physiol., 2018, vol. 315, no. 6, pp. 1569–1588. doi: 10.1152/ajpheart.00396.2018
  131. Stelzig K.E., Canepa-Escaro F., Schiliro M., Berdnikovs S., Prakash Y., Chiarella S.E. Estrogen regulates the expression of SARS-CoV-2 receptor ACE2 in differentiated airway epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 2020, vol. 318, no. 6, pp. 1280–1281. doi: 10.1152/ajplung.00153.2020
  132. Straub R.H. The complex role of estrogens in inflammation. Endocrine Rev., 2007, vol. 28, no. 5, pp. 521–574. doi: 10.1210/er.2007-0001
  133. Su H., Yang M., Wan C., Yi L.X., Tang F., Zhu H.Y., Yi F., Yang H.C., Fogo A.B., Nie X., Zhang C. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int., 2020, vol. 98, no. 1, pp. 219–227. doi: 10.1016/j.kint.2020.04.003
  134. Suba Z. Prevention and therapy of COVID-19 via exogenous estrogen treatment for both male and female patients. J. Pharm. Pharm. Sci., 2020, vol. 23, no. 1, pp. 75–85. doi: 10.18433/jpps31069
  135. Szekeres-Bartho J., Wegmann T. A progesterone-dependent immunomodulatory protein alters the Th1Th2 balance. J. Reprod. Immunol., 1996, vol. 31, no. 1–2, pp. 81–95. doi: 10.1016/0165-0378(96)00964-3
  136. Tam A., Wadsworth S., Dorscheid D., Man S.-F.P., Sin D.D. Estradiol increases mucus synthesis in bronchial epithelial cells. PloS One, 2014, vol. 9, no. 6: e100633. doi: 10.1371/journal.pone.0100633
  137. Taneja V. Sex hormones determine immune response. Front. Immunol., 2018, vol. 9: 1931. doi: 10.3389/fimmu.2018.01931
  138. Tauber S.C., Eiffert H., Brück W., Nau R. Septic encephalopathy and septic encephalitis. Expert Rev. Anti Infect. Ther., 2017, vol. 15, no. 2, pp. 121–132. doi: 10.1080/14787210.2017.1265448
  139. Tisoncik J.R., Korth M.J., Simmons C.P., Farrar J., Martin T.R., Katze M.G. Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev., 2012, vol. 76, no. 1, pp. 26–32. doi: 10.1128/MMBR.05015-11
  140. Toljan K. Letter to the editor regarding the viewpoint “Evidence of the COVID-19 virus targeting the CNS: tissue distribution, host–virus interaction, and proposed neurotropic mechanism”. ACS Chem. Neurosci., 2020, vol. 11, no. 8, pp. 1192–1194. doi: 10.1021/acschemneuro.0c00174
  141. Toppozada H., Toppozada M., El-Ghazzawi I., Elwany S. The human respiratory nasal mucosa in females using contraceptive pills: an ultramicroscopic and histochemical study. J. Laryngol. Otol., 1984, vol. 98, no. 1, pp. 43–51. doi: 10.1017/s002221510014616x
  142. Tukiainen T., Villani A.C., Yen A., Rivas M.A., Marshall J.L., Satija R., Aguirre M., Gauthier L., Fleharty M., Kirby A., Cummings B.B., Castel S.E., Karczewski K.J., Aguet F., Byrnes A; GTEx Consortium; Laboratory, Data Analysis &Coordinating Center (LDACC)—Analysis Working Group; Statistical Methods groups—Analysis Working Group; Enhancing GTEx (eGTEx) groups; NIH Common Fund; NIH/NCI; NIH/NHGRI; NIH/NIMH; NIH/NIDA; Biospecimen Collection Source Site—NDRI; Biospecimen Collection Source Site—RPCI; Biospecimen Core Resource—VARI; Brain Bank Repository—University of Miami Brain Endowment Bank; Leidos Biomedical—Project Management; ELSI Study; Genome Browser Data Integration &Visualization—EBI; Genome Browser Data Integration & Visualization—UCSC Genomics Institute, University of California Santa Cruz, Lappalainen T., Regev A., Ardlie K.G., Hacohen N., MacArthur D.G. Landscape of X chromosome inactivation across human tissues. Nature, 2017, vol. 550, no. 7675, pp. 244–248. doi: 10.1038/nature24265
  143. Turner A.J., Hiscox J.A., Hooper N.M. ACE2: from vasopeptidase to SARS virus receptor. Trends Pharmacol. Sci., 2004, vol. 25, no. 6, pp. 291–294. doi: 10.1016/j.tips.2004.04.001
  144. Varga Z., Flammer A.J., Steiger P., Haberecker M., Andermatt R., Zinkernagel A.S., Mehra M.R., Schuepbach R.A., Ruschitzka F., Moch H. Endothelial cell infection and endotheliitis in COVID-19. Lancet, 2020, vol. 395, no. 10234, pp. 1417– 1418. doi: 10.1016/S0140-6736(20)30937-5
  145. Vermillion M.S., Ursin R.L., Kuok D.I.T., Vom Steeg L.G., Wohlgemuth N., Hall O.J., Fink A.L., Sasse E., Nelson A., Ndeh R., McGrath-Morrow S., Mitzner W., Chan M.C.W., Pekosz A., Klein S.L. Production of amphiregulin and recovery from influenza is greater in males than females. Biol. Sex Differ., 2018, vol. 9: 24. doi: 10.1186/s13293-018-0184-8
  146. Voigt R.M., Forsyth C.B., Green S.J., Mutlu E., Engen P., Vitaterna M.H., Turek F.W., Keshavarzian A. Circadian disorganization alters intestinal microbiota. PLoS One, 2014, vol. 9, no. 5: e97500. doi: 10.1371/journal.pone.0097500
  147. Vom Steeg L.G., Klein S.L. SeXX matters in infectious disease pathogenesis. PLoS Pathog., 2016, vol. 12, no. 2: e1005374. doi: 10.1371/journal.ppat.1005374
  148. Wang D., Hu B., Hu C., Zhu F., Liu X., Zhang J., Wang B., Xiang H., Cheng Z., Xiong Y., Zhao Y., Li Y., Wang X., Peng Z. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus–infected pneumonia in Wuhan, China. JAMA, 2020, vol. 323, no. 11, pp. 1061–1069. doi: 10.1001/jama.2020.1585
  149. Wang S., Han P., Xiao F. Manifestations of liver injury in 333 hospitalized patients with coronavirus disease 2019. Chinese J. Digest., 2020, vol. 40, no. 00: E008. doi: 10.3760/cma.j.issn.0254-1432.2020.0008
  150. Warren-Gash C., Blackburn R., Whitaker H., McMenamin J, Hayward A.C. Laboratory-confirmed respiratory infections as triggers for acute myocardial infarction and stroke: a self-controlled case series analysis of national linked datasets from Scotland. Eur. Respir. J., 2018, vol. 513, no. 1: 701794. doi: 10.1183/13993003.01794-2017
  151. Lv D., Qin C., Gu D., Zhang B., Chen W., Hou J., Song N., Zeng G., Ren S. Sex differences in severity and mortality among patients with COVID-19: evidence from pooled literature analysis and insights from integrated bioinformatic analysis. ArXiv, 2020. doi: 2003.13547
  152. WHO. WHO Coronavirus Disease (COVID-19) Dashboard. URL: https://covid19.who.int/
  153. Wong S.H., Lui R.N., Sung J.J. COVID19 and the digestive system. J. Gastroenterol. Hepatol., 2020, vol. 35, no. 5, pp. 744–748. doi: 10.1111/jgh.15047
  154. Wu Y., Xu X., Chen Z., Duan J., Hashimoto K., Yang L., Liu C., Yang C. Nervous system involvement after infection with COVID-19 and other coronaviruses. Brain Behav. Immun., 2020, vol. 87, pp. 18–22. doi: 10.1016/j.bbi.2020.03.031
  155. Xia H., Lazartigues E. Angiotensin-converting enzyme 2: central regulator for cardiovascular function. Curr. Hypertens. Rep., 2010, vol. 12, no. 3, pp. 170–175. doi: 10.1007/s11906-010-0105-7
  156. Xiang P., Xu X.M., Gao L.L., Wang H.Z., Xiong H.F., Li R.H. First case of 2019 novel coronavirus disease with Encephalitis. ChinaXiv, 2020, vol. 202003: 00015.
  157. Xiao F., Tang M., Zheng X., Liu Y., Li X., Shan H. Evidence for gastrointestinal infection of SARS-CoV-2. Gastroenterology, 2020, vol. 158, no. 6, pp. 1831–1833. doi: 10.1053/j.gastro.2020.02.055
  158. Xu Y., Li X., Zhu B., Liang H., Fang C., Gong Y., Guo Q., Sun X., Zhao D., Shen J., Zhang H., Liu H., Xia H., Tang J., Zhang K., Gong S. Characteristics of pediatric SARS-CoV-2 infection and potential evidence for persistent fecal viral shedding. Nat. Med., 2020, vol. 26, no. 4, pp. 502–505. doi: 10.1038/s41591-020-0817-4
  159. Xu Z., Shi L., Wang Y., Zhang J., Huang L., Zhang C., Liu S., Zhao P., Liu H., Zhu L., Tai Y., Bai C., Gao T., Song J., Xia P., Dong J., Zhao J., Wang F.S. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir. Med., 2020, vol. 8, no. 4, pp. 420–422. doi: 10.1016/S2213-2600(20)30076-X
  160. Zhang W.C., Kaushal S., Yeo D. Enteric involvement of coronaviruses: is faecal–oral transmission of SARS-CoV-2 possible? Lancet Gastroenterol. Hepatol., 2020, vol. 5, no. 4, pp. 335–337. doi: 10.1016/S2468-1253(20)30048-0
  161. Young G.B. Encephalopathy of infection and systemic inflammation. J. Clin. Neurophysiol., 2013, vol. 305, no. 4, pp. 454–461. doi: 10.1097/WNP.0b013e3182a73d83
  162. Zhang C., Shi L., Wang F.-S. Liver injury in COVID-19: management and challenges. Lancet Gastroenterol. Hepatol., 2020, vol. 5, no. 5, pp. 428–430. doi: 10.1016/S2468-1253(20)30057-1
  163. Zhang H., Kang Z., Gong H., Xu D., Wang J., Li Z., Cui X., Xiao J., Meng T., Zhou W., Liu J., Xu H. The digestive system is a potential route of 2019-nCoV infection: a bioinformatics analysis based on single-cell transcriptomes. BioRxiv, 2020. doi: 10.1101/2020.01.30.927806
  164. Zhang H., Baker A. Recombinant human ACE2: acing out angiotensin II in ARDS therapy. Crit. Care, 2017, vol. 21, no. 1: 305. doi: 10.1186/s13054-017-1882-z
  165. Zhang J., Wang X., Jia X., Li J., Hu K., Chen G., Wei J., Gong Z., Zhou C., Yu H., Yu M., Lei H., Cheng F., Zhang B., Xu Y., Wang G., Dong W. Risk factors for disease severity, unimprovement, and mortality of COVID-19 patients in Wuhan, China. Clin. Microbiol. Infect., 2020, vol. 26, no. 6, pp. 767–772. doi: 10.1016/j.cmi.2020.04.012
  166. Zhang W., Du R.H., Li B., Zheng X.S., Yang X.L., Hu B., Wang Y.Y., Xiao G.F., Yan B., Shi Z.L., Zhou P. Molecular and serological investigation of 2019-nCoV infected patients: implication of multiple shedding routes. Emerg. Microbes Infect., 2020, vol. 9, no. 1, pp. 386–389. doi: 10.1080/22221751.2020.1729071
  167. Zhang Y., Xiao M., Zhang S., Xia P., Cao W., Jiang W., Chen H., Ding X., Zhao H., Zhang H., Wang C., Zhao J., Sun X., Tian R., Wu W., Wu D., Ma J., Chen Y., Zhang D., Xie J., Yan X., Zhou X., Liu Z., Wang J., Du B., Qin Y., Gao P., Qin X., Xu Y., Zhang W., Li T., Zhang F., Zhao Y., Li Y., Zhang S. Coagulopathy and antiphospholipid antibodies in patients with COVID-19. N. Engl. J. Med., 2020, vol. 382: e38. doi: 10.1056/NEJMc2007575
  168. Zheng Y.-Y., Ma Y.-T., Zhang J.-Y., Xie X. COVID-19 and the cardiovascular system. Nat. Rev. Cardiol., 2020, vol. 17, no. 5, pp. 259–260. doi: 10.1038/s41569-020-0360-5
  169. Zhou F., Yu T., Du R., Fan G., Liu Y., Liu Z., Xiang J., Wang Y., Song B., Gu X., Guan L., Wei Y., Li H., Wu X., Xu J., Tu S., Zhang Y., Chen H., Cao B. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet, 2020, vol. 395, no. 10229, pp. 1054–1062. doi: 10.1016/S0140-6736(20)30566-3
  170. Zhou Z., Zhao N., Shu Y., Han S., Chen B., Shu X. Effect of gastrointestinal symptoms in patients with COVID-19. Gastroenterology, 2020, vol. 158, no. 8, pp. 2294–2297. doi: 10.1053/j.gastro.2020.03.020

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Khaksari M., Sabet N., Soltani Z., Bashiri H.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies