Estradiol and COVID-19: Does 17-Estradiol Have an Immune-Protective Function in Women Against Coronavirus?
,
Abstract
Objective: Female sex hormones have a pro-inflammatory effect, which may help to minimize inflammation. Estrogen's immunoregulatory properties play a significant role in the bi-directional neuroendocrine-immune activity in females. As a result, sex hormones can play a role in men's high mortality rate from coronavirus-2019 (COVID-19). It is aimed to clarify the role of 17-estradiol (E2) in the battle against COVID-19.
Materials and methods: Until April 2021, a study on PubMed was performed. COVID-19, 17-estradiol (E2), immunoregulatory properties, pregnancy, menopausal symptoms, hormonal therapy,
ER/ expression on immune cells, and mortality were some of the concepts used in the search.
Results: Regulation of pro-inflammatory immune processes against COVID-19 appears to be associated with increased immune function (pro-inflammatory), anti-inflammatory regulation, and antiviral defense. Women with a severe coronavirus infection had higher serum IgG antibody levels than men, and their IgG production was faster in the early stages of infection. 17-estradiol (E2) levels of blood will increase by
100-fold during pregnancy. COVID-19 in pregnant women had a 15-fold lower mortality rate than other women. While menopause replacement therapy (MRT) for pre/post-menopausal women and its effectiveness in reducing COVID-19 infection is debatable.
Conclusion: MRT may be considered as a viable treatment option for pre/post-menopause women with coronavirus, referring to the fact that sex hormones reduce inflammatory responses and modulate
ACE2 expression. The task's difficulty and achieving the desired outcome seem to be challenging.
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2. Schmidt M, Naumann H, Weidler C, Schellenberg M, Anders S, Straub RH. Inflammation and sex hormone metabolism. Ann N Y Acad Sci 2006; 1069: 236-46.
3. Viveiros A, Rasmuson J, Vu J, Mulvagh SL, Yip CYY, Norris CM, et al. Sex differences in COVID-19: candidate pathways, genetics of ACE2, and sex hormones. Am
J Physiol Heart Circ Physiol 2021; 320: H296-H304.
4. Mauvais-Jarvis F, Klein SL, Levin ER. Estradiol, Progesterone, Immunomodulation, and COVID-19 Outcomes. Endocrinology 2020; 161: bqaa127.
5. Morelli SS, Mandal M, Goldsmith LT, Kashani BN, Ponzio NM. The maternal immune system during pregnancy and its influence on fetal development. Research and Reports in Biology 2015; 6: 171-89.
6. Kourtis AP, Read JS, Jamieson DJ. Pregnancy and infection. N Engl J Med 2014; 370: 2211–8.
7. Mor G, Cardenas I, Abrahams V, Guller S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci 2011; 1221: 80–7.
8. Mor G, Cardenas I. The Immune System in Pregnancy: A Unique Complexity. Am J Reprod Immunol 2010; 63: 425-33.
9. Buddola V.Recent Developments in Applied Microbiology and Biochemistry - 1st Edition 2018: 13-20.
10. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan. China. Lancet 2020; 395: 497–506.
11. Beaudette ER, Hudson CB. Cultivation of the virus of infectious bronchitis. J Am Vet Med Assoc 1937; 90: 51-8.
12. Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 2019; 17: 181–92.
13. Robinson DP, Lorenzo ME, Jian W, Klein SL. Elevated 17β-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PloS Pathog 2011; 7: e1002149.
14. Robinson DP, Hall OJ, Nilles TL, Bream JH, Klein SL. 17β-estradiol protects females against influenza by recruiting neutrophils and increasing virus-specific CD8 T cell responses in the lungs. J Virol 2014; 88: 4711-20.
15. Vermillion MS, Ursin RL, Attreed SE, Klein SL. Estriol reduces pulmonary immune cell recruitment and inflammation to protect female mice from severe influenza. Endocrinology. 2018; 159: 3306-20.
16. Mauvais-Jarvis F, Klein SL, Levin ER. Estradiol, Progesterone, Immunomodulation, and COVID-19 Outcomes. Endocrinology 2020; 161: bqaa127.
17. Phiel KL, Henderson RA, Adelman SJ, Elloso MM. Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol Lett 2005; 97: 107-13.
18. Channappanavar R, Fett C, Mack M, Ten Eyck PP, Meyerholz DK, Perlman S. Sex-based differences in susceptibility to severe acute respiratory syndrome coronavirus infection. J Immunol 2017; 198: 4046-53.
19. Peretz J, Pekosz A, Lane AP, Klein SL. Estrogenic compounds reduce influenza A virus replication in primary human nasal epithelial cells derived from female, but not male, donors. Am J Physiol Lung Cell Mol Physiol 2016; 310: L415-25.
20. Tofovic SP, Jackson EK. Estradiol metabolism: Crossroads in pulmonary arterial hypertension. Int J Mol Sci 2019; 21: 116.
21. Iorga A, Cunningham CM, Moazeni S, Ruffenach G, Umar S, Eghbali M. The protective role of estrogen and estrogen receptors in cardiovascular disease and the controversial use of estrogen therapy. Biol Sex Differ 2017; 8: 33.
22. Di Florio DN, Sin J, Coronado MJ, Atwal PS, Fairweather D. Sex differences in inflammation, redox biology, mitochondria and autoimmunity. Redox Biol 2020; 31: 101482.
23. Stelzig KE, Canepa‐Escaro F, Schiliro M, Berdnikovs S, Prakash YS, Chiarella SE. Estrogen regulates the expression of SARS‐CoV‐2 receptor ACE2 in differentiated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2020; 318: L1280–1.
24. Lemes RMR, Costa AJ, Bartolomeo CS, Bassani TB, Nishino MS, Pereira GJDS, et al. 17β‐estradiol reduces SARS‐CoV‐2 infection in vitro. Physiol Rep 2021; 9: e14707.
25. Carey MA, Card JW, Voltz JW, Germolec DR, Korach KS, Zeldin DC. The impact of sex and sex hormones on lung physiology and disease: lessons from animal studies. Am J Physiol Lung Cell Mol Physiol 2007; 293: L272–8.
26. Speyer CL, Rancilio NJ, McClintock SD, Crawford JD, Gao H, Sarma JV, et al. Regulatory effects of estrogen on acute lung inflammation in mice. Am J Physiol Cell Physiol 2005; 288: C881–90.
27. Lahm T, Albrecht M, Fisher AJ, Selej M, Patel NG, Brown JA, et al. 17β-Estradiol attenuates hypoxic pulmonary hypertension via estrogen receptor-mediated effects. Am J Respir Crit Care Med 2012; 185: 965-80.
28. Breithaupt-Faloppa AC, Correia CJ, Prado CM, Stilhano RS, Ureshino RP, Moreira LFP. 17β-Estradiol, a potential ally to alleviate SARS-CoV-2 infection. Clinics (Sao Paulo) 2020; 75: e1980.
29. Magri A, Barbaglia MN, Foglia CZ, Boccato E, Burlone ME, Cole S, et al. 17,β-estradiol inhibits hepatitis C virus mainly by interference with the release phase of its life cycle. Liver Int 2017; 37: 669–77.
30. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC, et al. Hormone replacement therapy and incidence of Alzheimer disease in older women: The Cache County Study. JAMA 2002; 288: 2123–9.
31. Paschou SA, Papanas N. Type 2 Diabetes Mellitus and Menopausal Hormone Therapy: An Update. Diabetes Ther 2019; 10: 2313–20.
32. Temkin SM, Mallen A, Bellavance E, Rubinsak L, Wenham RM. The role of menopausal hormone therapy in women with or at risk of ovarian and breast cancers: Misconceptions and current directions. Cancer 2019; 125: 499-514.
33. Zhu J,Yi M,Xing L, Yu Zh,Guo X,Chen X,et al . Ovarian Hormonal Change-Related Energy Metabolism and Obesity in Menopausal Women. Hormone Therapy and Replacement in Cancer and Aging-related Diseases 2019.
34. Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, et al. Heart Disease and Stroke Statistics-2019 Update: A Report from the American Heart Association. Circulation 2019; 139: e56–e528.
35. Kim JE, Chang JH, Jeong MJ, Choi J, Park J, Baek C, et al. A systematic review and meta-analysis of effects of menopausal hormone therapy on cardiovascular diseases. Sci Rep 2020; 10: 20631.
36. MacLennan AH, Henderson VW, Pain BJ, Mathias J, Ramsay EN, Ryan P, et al. Hormone therapy, timing of initiation, and cognition in women aged older than 60 years: the REMEMBER pilot study. Menopause 2006; 13: 28-36.
37. Bianchia I, Lieo A, Gershwinc ME, Invernizzi P. The X chromosome and immune associated genes.
J Autoimmun 2012; 38: J187-92.
38. Kovats S. Estrogen receptors regulate innate immune cells and signaling pathways. Cell Immunol 2015; 294: 63-9.
39. Leitman DC, Paruthiyil S, Vivar OI, Saunier EF, Herber CB, Cohen I, et al. Regulation of specific target genes and biological responses by estrogen receptor subtype agonists. Curr Opin Pharmacol 2010; 10: 629–36.
40. Hoffmann M, Kleine-Weber H, Schroeder S, Kruger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181: 271–80. e8.
41. Ueda K, Karas RH. Emerging evidence of the importance of rapid, non-nuclear estrogen receptor signaling in the cardiovascular system. Steroids 2013; 78: 589-96.
42. Molloy EJ, O’Neill AJ, Grantham JJ, Sheridan-Pereira M, Fitzpatrick JM, Webb DW, et al. Sex-specific alterations in neutrophil apoptosis: The role of estradiol and progesterone. Blood 2003; 102: 2653–9.
43. Nadkarni S, Cooper D, Brancaleone V, Bena S, Perretti M. Activation of the annexin A1 pathway underlies the protective effects exerted by estrogen in polymorphonuclear leukocytes. Arterioscler Thromb Vasc Bio 2011; 31: 2749–59.
44. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 2011; 118: 5918–27.
45. Kovats S. Estrogen receptors regulate an inflammatory pathway of dendritic cell differentiation: mechanisms and implications for immunity. Horm Behav 2012; 62: 254–62.
46. Villa A, Rizzi N, Vegeto E, Ciana P, Maggi A. Estrogen accelerates the resolution of inflammation in macrophagic cells. Scientific Reports 2015; 5: 15224.
47. Gubbels Bupp MR. Sex, the ageing immune system and chronic disease. Cell Immunol 2015; 294: 102–10.
48. Olsen NJ, Kovacs WJ. Gonadal steroids and immunity. Endocr Rev 1996; 17: 369–84.
49. Monteiro R, Teixeira D, CalhauC. Estrogen Signaling in Metabolic Inflammation. Mediators Inflamm 2014; 2014: 615917.
50. Chakrabarti S, Lekontseva O, Davidge ST. Estrogen is a Modulator of Vascular Inflammation. IUBMB Life 2008;
60: 376–82.
51. Maciuszek M, Pijanowski l, Pekala-Safinska A, Kemenade BML, Chadzinska M. 17β-Estradiol affects the innate immune response in common carp. Fish Physiol Biochem 2020; 46: 1775–94.
52. Robinson DP, Lorenzo ME, Jian W, Klein SL. Elevated 17beta-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PLoS Pathog 2011; 7: e1002149.
53. Bencze D, Fekete T, Pázmándi K. Type I Interferon production of plasmacytoid dendritic cells under control. Int J Mol Sci 2021; 22: 4190.
54. Arruvito L, Sanz M, Banham AH, Fainboim L. Expansion of CD4+CD25+ and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol 2007; 178: 2572–8.
55. Faas M, Bouman A, Moesa H, Heineman MJ, de Leij L, Schuiling G. The immune response during the luteal phase of the ovarian cycle: A Th2-type response? Fertil Steril 2000; 74: 1008-13.
56. Parker C, Shalev D, Hsu I, Shenoy A, Cheung S, Nash S, et al. Depression, Anxiety, and Acute Stress Disorder Among Patients Hospitalized with COVID-19: A Prospective Cohort Study. J Acad Consult Liaison Psychiatry 2021; 62: 211-19.
57. Endrighi R, Hamer M, Steptoe A. Post-menopausal Women Exhibit Greater Interleukin-6 Responses to Mental Stress Than Older Men. Ann Behav Med 2016; 50: 564–71.
2. Schmidt M, Naumann H, Weidler C, Schellenberg M, Anders S, Straub RH. Inflammation and sex hormone metabolism. Ann N Y Acad Sci 2006; 1069: 236-46.
3. Viveiros A, Rasmuson J, Vu J, Mulvagh SL, Yip CYY, Norris CM, et al. Sex differences in COVID-19: candidate pathways, genetics of ACE2, and sex hormones. Am
J Physiol Heart Circ Physiol 2021; 320: H296-H304.
4. Mauvais-Jarvis F, Klein SL, Levin ER. Estradiol, Progesterone, Immunomodulation, and COVID-19 Outcomes. Endocrinology 2020; 161: bqaa127.
5. Morelli SS, Mandal M, Goldsmith LT, Kashani BN, Ponzio NM. The maternal immune system during pregnancy and its influence on fetal development. Research and Reports in Biology 2015; 6: 171-89.
6. Kourtis AP, Read JS, Jamieson DJ. Pregnancy and infection. N Engl J Med 2014; 370: 2211–8.
7. Mor G, Cardenas I, Abrahams V, Guller S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci 2011; 1221: 80–7.
8. Mor G, Cardenas I. The Immune System in Pregnancy: A Unique Complexity. Am J Reprod Immunol 2010; 63: 425-33.
9. Buddola V.Recent Developments in Applied Microbiology and Biochemistry - 1st Edition 2018: 13-20.
10. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan. China. Lancet 2020; 395: 497–506.
11. Beaudette ER, Hudson CB. Cultivation of the virus of infectious bronchitis. J Am Vet Med Assoc 1937; 90: 51-8.
12. Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 2019; 17: 181–92.
13. Robinson DP, Lorenzo ME, Jian W, Klein SL. Elevated 17β-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PloS Pathog 2011; 7: e1002149.
14. Robinson DP, Hall OJ, Nilles TL, Bream JH, Klein SL. 17β-estradiol protects females against influenza by recruiting neutrophils and increasing virus-specific CD8 T cell responses in the lungs. J Virol 2014; 88: 4711-20.
15. Vermillion MS, Ursin RL, Attreed SE, Klein SL. Estriol reduces pulmonary immune cell recruitment and inflammation to protect female mice from severe influenza. Endocrinology. 2018; 159: 3306-20.
16. Mauvais-Jarvis F, Klein SL, Levin ER. Estradiol, Progesterone, Immunomodulation, and COVID-19 Outcomes. Endocrinology 2020; 161: bqaa127.
17. Phiel KL, Henderson RA, Adelman SJ, Elloso MM. Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol Lett 2005; 97: 107-13.
18. Channappanavar R, Fett C, Mack M, Ten Eyck PP, Meyerholz DK, Perlman S. Sex-based differences in susceptibility to severe acute respiratory syndrome coronavirus infection. J Immunol 2017; 198: 4046-53.
19. Peretz J, Pekosz A, Lane AP, Klein SL. Estrogenic compounds reduce influenza A virus replication in primary human nasal epithelial cells derived from female, but not male, donors. Am J Physiol Lung Cell Mol Physiol 2016; 310: L415-25.
20. Tofovic SP, Jackson EK. Estradiol metabolism: Crossroads in pulmonary arterial hypertension. Int J Mol Sci 2019; 21: 116.
21. Iorga A, Cunningham CM, Moazeni S, Ruffenach G, Umar S, Eghbali M. The protective role of estrogen and estrogen receptors in cardiovascular disease and the controversial use of estrogen therapy. Biol Sex Differ 2017; 8: 33.
22. Di Florio DN, Sin J, Coronado MJ, Atwal PS, Fairweather D. Sex differences in inflammation, redox biology, mitochondria and autoimmunity. Redox Biol 2020; 31: 101482.
23. Stelzig KE, Canepa‐Escaro F, Schiliro M, Berdnikovs S, Prakash YS, Chiarella SE. Estrogen regulates the expression of SARS‐CoV‐2 receptor ACE2 in differentiated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2020; 318: L1280–1.
24. Lemes RMR, Costa AJ, Bartolomeo CS, Bassani TB, Nishino MS, Pereira GJDS, et al. 17β‐estradiol reduces SARS‐CoV‐2 infection in vitro. Physiol Rep 2021; 9: e14707.
25. Carey MA, Card JW, Voltz JW, Germolec DR, Korach KS, Zeldin DC. The impact of sex and sex hormones on lung physiology and disease: lessons from animal studies. Am J Physiol Lung Cell Mol Physiol 2007; 293: L272–8.
26. Speyer CL, Rancilio NJ, McClintock SD, Crawford JD, Gao H, Sarma JV, et al. Regulatory effects of estrogen on acute lung inflammation in mice. Am J Physiol Cell Physiol 2005; 288: C881–90.
27. Lahm T, Albrecht M, Fisher AJ, Selej M, Patel NG, Brown JA, et al. 17β-Estradiol attenuates hypoxic pulmonary hypertension via estrogen receptor-mediated effects. Am J Respir Crit Care Med 2012; 185: 965-80.
28. Breithaupt-Faloppa AC, Correia CJ, Prado CM, Stilhano RS, Ureshino RP, Moreira LFP. 17β-Estradiol, a potential ally to alleviate SARS-CoV-2 infection. Clinics (Sao Paulo) 2020; 75: e1980.
29. Magri A, Barbaglia MN, Foglia CZ, Boccato E, Burlone ME, Cole S, et al. 17,β-estradiol inhibits hepatitis C virus mainly by interference with the release phase of its life cycle. Liver Int 2017; 37: 669–77.
30. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC, et al. Hormone replacement therapy and incidence of Alzheimer disease in older women: The Cache County Study. JAMA 2002; 288: 2123–9.
31. Paschou SA, Papanas N. Type 2 Diabetes Mellitus and Menopausal Hormone Therapy: An Update. Diabetes Ther 2019; 10: 2313–20.
32. Temkin SM, Mallen A, Bellavance E, Rubinsak L, Wenham RM. The role of menopausal hormone therapy in women with or at risk of ovarian and breast cancers: Misconceptions and current directions. Cancer 2019; 125: 499-514.
33. Zhu J,Yi M,Xing L, Yu Zh,Guo X,Chen X,et al . Ovarian Hormonal Change-Related Energy Metabolism and Obesity in Menopausal Women. Hormone Therapy and Replacement in Cancer and Aging-related Diseases 2019.
34. Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, et al. Heart Disease and Stroke Statistics-2019 Update: A Report from the American Heart Association. Circulation 2019; 139: e56–e528.
35. Kim JE, Chang JH, Jeong MJ, Choi J, Park J, Baek C, et al. A systematic review and meta-analysis of effects of menopausal hormone therapy on cardiovascular diseases. Sci Rep 2020; 10: 20631.
36. MacLennan AH, Henderson VW, Pain BJ, Mathias J, Ramsay EN, Ryan P, et al. Hormone therapy, timing of initiation, and cognition in women aged older than 60 years: the REMEMBER pilot study. Menopause 2006; 13: 28-36.
37. Bianchia I, Lieo A, Gershwinc ME, Invernizzi P. The X chromosome and immune associated genes.
J Autoimmun 2012; 38: J187-92.
38. Kovats S. Estrogen receptors regulate innate immune cells and signaling pathways. Cell Immunol 2015; 294: 63-9.
39. Leitman DC, Paruthiyil S, Vivar OI, Saunier EF, Herber CB, Cohen I, et al. Regulation of specific target genes and biological responses by estrogen receptor subtype agonists. Curr Opin Pharmacol 2010; 10: 629–36.
40. Hoffmann M, Kleine-Weber H, Schroeder S, Kruger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181: 271–80. e8.
41. Ueda K, Karas RH. Emerging evidence of the importance of rapid, non-nuclear estrogen receptor signaling in the cardiovascular system. Steroids 2013; 78: 589-96.
42. Molloy EJ, O’Neill AJ, Grantham JJ, Sheridan-Pereira M, Fitzpatrick JM, Webb DW, et al. Sex-specific alterations in neutrophil apoptosis: The role of estradiol and progesterone. Blood 2003; 102: 2653–9.
43. Nadkarni S, Cooper D, Brancaleone V, Bena S, Perretti M. Activation of the annexin A1 pathway underlies the protective effects exerted by estrogen in polymorphonuclear leukocytes. Arterioscler Thromb Vasc Bio 2011; 31: 2749–59.
44. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 2011; 118: 5918–27.
45. Kovats S. Estrogen receptors regulate an inflammatory pathway of dendritic cell differentiation: mechanisms and implications for immunity. Horm Behav 2012; 62: 254–62.
46. Villa A, Rizzi N, Vegeto E, Ciana P, Maggi A. Estrogen accelerates the resolution of inflammation in macrophagic cells. Scientific Reports 2015; 5: 15224.
47. Gubbels Bupp MR. Sex, the ageing immune system and chronic disease. Cell Immunol 2015; 294: 102–10.
48. Olsen NJ, Kovacs WJ. Gonadal steroids and immunity. Endocr Rev 1996; 17: 369–84.
49. Monteiro R, Teixeira D, CalhauC. Estrogen Signaling in Metabolic Inflammation. Mediators Inflamm 2014; 2014: 615917.
50. Chakrabarti S, Lekontseva O, Davidge ST. Estrogen is a Modulator of Vascular Inflammation. IUBMB Life 2008;
60: 376–82.
51. Maciuszek M, Pijanowski l, Pekala-Safinska A, Kemenade BML, Chadzinska M. 17β-Estradiol affects the innate immune response in common carp. Fish Physiol Biochem 2020; 46: 1775–94.
52. Robinson DP, Lorenzo ME, Jian W, Klein SL. Elevated 17beta-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PLoS Pathog 2011; 7: e1002149.
53. Bencze D, Fekete T, Pázmándi K. Type I Interferon production of plasmacytoid dendritic cells under control. Int J Mol Sci 2021; 22: 4190.
54. Arruvito L, Sanz M, Banham AH, Fainboim L. Expansion of CD4+CD25+ and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol 2007; 178: 2572–8.
55. Faas M, Bouman A, Moesa H, Heineman MJ, de Leij L, Schuiling G. The immune response during the luteal phase of the ovarian cycle: A Th2-type response? Fertil Steril 2000; 74: 1008-13.
56. Parker C, Shalev D, Hsu I, Shenoy A, Cheung S, Nash S, et al. Depression, Anxiety, and Acute Stress Disorder Among Patients Hospitalized with COVID-19: A Prospective Cohort Study. J Acad Consult Liaison Psychiatry 2021; 62: 211-19.
57. Endrighi R, Hamer M, Steptoe A. Post-menopausal Women Exhibit Greater Interleukin-6 Responses to Mental Stress Than Older Men. Ann Behav Med 2016; 50: 564–71.
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| Issue | Vol 15, No 3 (September 2021) | |
| Section | Review Articles | |
| DOI | https://doi.org/10.18502/jfrh.v15i3.7132 | |
| Keywords | ||
| Estradiol Estrogen Receptor Alpha Coronavirus Hormone Replacement Therapy | ||
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How to Cite
1.
Zafari Zangeneh F, Sarmast Shoushtari M. Estradiol and COVID-19: Does 17-Estradiol Have an Immune-Protective Function in Women Against Coronavirus?. J Family Reprod Health. 2021;15(3):150-159.
