Sex differences in sequelae from COVID-19 infection and in long COVID syndrome: a review

References

• World Health Organization. Gender and genetics; [cited 2022 Feb 1]. Available from:https://www.who.int/genomics/gender/en/#:∼:text=Sex%20and%20gender%20are%20both,outcomes%20for%20women%20and%20men.
   Google Scholar
• Alghamdi IG, Hussain II, Almalki SS, et al. The pattern of Middle east respiratory syndrome coronavirus in Saudi Arabia: a descriptive epidemiological analysis of data from the Saudi ministry of health. Int J Gen Med. 2014;7:417–423.
   PubMedGoogle Scholar
• Karlberg J, Chong DS, Lai WY. Do men have a higher case fatality rate of severe acute respiratory syndrome than women do? Am J Epidemiol. 2004;159(3):229–231.
   PubMed Web of Science ®Google Scholar
• Leung GM, Hedley AJ, Ho LM, et al. The epidemiology of severe acute respiratory syndrome in the 2003 Hong Kong epidemic: an analysis of all 1755 patients. Ann Intern Med. 2004;141(9):662–673.
   PubMed Web of Science ®Google Scholar
• Leong HN, Earnest A, Lim HH, et al. SARS in Singapore–predictors of disease severity. Ann Acad Med Singap. 2006;35(5):326–331.
   PubMed Web of Science ®Google Scholar
• Heidari S, Ahumada C, Kurbanova Z. GENDRO gender, evidence and health network. Towards the real-time inclusion of sex- and age-disaggregated data in pandemic responses. BMJ Glob Health. 2020;5(10):e003848.
   PubMed Web of Science ®Google Scholar
• Lancet . The gender dimension to COVID-19. The Lancet. 2020;395(10231):1168.
   Web of Science ®Google Scholar
• Phillips S, Williams MA. Confronting our next national health disaster – long-haul Covid. N Engl J Med. 2021;385(7):577–579.
   PubMed Web of Science ®Google Scholar
• Higgins V, Sohaei D, Diamandis EP, et al. COVID-19: from an acute to chronic disease? Potential long-term health consequences. Crit Rev Clin Lab Sci. 2021;58(5):297–310.
   PubMed Web of Science ®Google Scholar
• Al-Aly Z, Xie Y, Bowe B. High-dimensional characterization of post-acute sequelae of COVID-19. Nature. 2021;594(7862):259–264.
   PubMed Web of Science ®Google Scholar
• Maamar M, Artime A, Pariente E, et al. Post-COVID-19 syndrome, inflammatory markers and sex differences. MedRxiv. 2021;2021:1–9.
   Google Scholar
• Nalbandian A, Sehgal K, Gupta A, et al. Post-acute COVID-19 syndrome. Nat Med. 2021;27(4):601–615.
   PubMed Web of Science ®Google Scholar
• Ayoubkhani D, Khunti K, Nafilyan V, et al. Post-COVID syndrome in individuals admitted to hospital with COVID-19: retrospective cohort study. BMJ. 2021;372:n693.
   PubMed Web of Science ®Google Scholar
• Nabavi N. Long COVID: How to define it and how to manage it. BMJ. 2020;370:m3489.
   PubMed Web of Science ®Google Scholar
• Oronsky B, Larson C, Hammond TC, et al. A review of persistent post-COVID syndrome (PPCS). Clin Rev Allergy Immunol. 2021;2021:1–9.
   Google Scholar
• Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5(11):1265–1273.
   PubMed Web of Science ®Google Scholar
• Khamsi R. Rogue antibodies could be driving severe COVID-19. Nature. 2021;590(7844):29–31.
   PubMed Web of Science ®Google Scholar
• Jarefors S, Bennet L, You E, et al. Lyme borreliosis reinfection: might it be explained by a gender difference in immune response? Immunology. 2006;118(2):224–232.
   PubMed Web of Science ®Google Scholar
• Torcia MG, Nencioni L, Clemente AM, et al. Sex differences in the response to viral infections: TLR8 and TLR9 ligand stimulation induce higher IL10 production in males. PLoS One. 2012;7(6):e39853.
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
   PubMed Web of Science ®Google Scholar
• Schardt C, Adams MB, Owens T, et al. Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med Inform Decis Mak. 2007;7(1):16.
   PubMed Web of Science ®Google Scholar
• Meini S, Suardi LR, Busoni M, et al. Olfactory and gustatory dysfunctions in 100 patients hospitalized for COVID-19: sex differences and recovery time in real-life. Eur Arch Otorhinolaryngol. 2020;277(12):3519–3523.
   PubMed Web of Science ®Google Scholar
• Middeldorp S, Coppens M, van Haaps TF, et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost. 2020;18(8):1995–2002.
   PubMed Web of Science ®Google Scholar
• Santoliquido A, Porfidia A, Nesci A, et al. Incidence of deep vein thrombosis among non-ICU patients hospitalized for COVID-19 despite pharmacological thromboprophylaxis. J Thromb Haemost. 2020;18(9):2358–2363.
   PubMed Web of Science ®Google Scholar
• Pelayo J, Lo KB, Bhargav R, et al. Clinical characteristics and outcomes of community- and hospital-acquired acute kidney injury with COVID-19 in a US inner city hospital system. Cardiorenal Med. 2020;10(4):223–231.
   PubMed Web of Science ®Google Scholar
• Lodigiani C, Iapichino G, Carenzo L, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14.
   PubMed Web of Science ®Google Scholar
• Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L, et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thromb Res. 2020;192:23–26.
   PubMed Web of Science ®Google Scholar
• COVIDSurg Collaborative. Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study. Lancet. 2020;396(10243):27–38. Erratum in: Lancet. 2020.
   PubMed Web of Science ®Google Scholar
• Whyte MB, Kelly PA, Gonzalez E, et al. Pulmonary embolism in hospitalised patients with COVID-19. Thromb Res. 2020;195:95–99.
   PubMed Web of Science ®Google Scholar
• Zhang LI, Feng X, Zhang D, et al. Deep vein thrombosis in hospitalized patients with COVID-19 in Wuhan, China. Prevalence, risk factors, and outcome. Circulation. 2020;142(2):114–128.
   PubMed Web of Science ®Google Scholar
• Deng Q, Hu B, Zhang Y, et al. Suspected myocardial injury in patients with COVID-19: Evidence from front-line clinical observation in Wuhan, China. Int J Cardiol. 2020;311:116–121.
   PubMed Web of Science ®Google Scholar
• Ma YF, Li W, Deng HB, et al. Prevalence of depression and its association with quality of life in clinically stable patients with COVID-19. J Affect Disord. 2020;275:145–148.
   PubMed Web of Science ®Google Scholar
• Chen W, Li Z, Yang B, et al. Delayed-phase thrombocytopenia in patients with Coronavirus disease 2019 (COVID-19). Br J Haematol. 2020;190(2):179–184.
   PubMed Web of Science ®Google Scholar
• Hirsch JS, Ng JH, Ross DW, et al. Acute kidney injury in patients hospitalized with COVID-19. Kidney Int. 2020;98(1):209–218.
   PubMed Web of Science ®Google Scholar
• Yao N, Wang SN, Lian JQ, et al. [Clinical characteristics and influencing factors of patients with novel coronavirus pneumonia combined with liver injury in Shaanxi region]. Zhonghua Gan Zang Bing Za Zhi. 2020;28(3):234–239. Chinese.
   PubMedGoogle Scholar
• Jiang S, Wang R, Li L, et al. Liver injury in critically ill and non-critically ill COVID-19 patients: a multicenter, retrospective, observational study. Front Med. 2020;7:347.
   Web of Science ®Google Scholar
• Sierpiński R, Pinkas J, Jankowski M, et al. Sex differences in the frequency of gastrointestinal symptoms and olfactory or taste disorders in 1942 nonhospitalized patients with coronavirus disease 2019 (COVID-19). Pol Arch Intern Med. 2020;130(6):501–505.
   PubMedGoogle Scholar
• Biadsee A, Biadsee A, Kassem F, et al. Olfactory and oral manifestations of COVID-19: sex-related symptoms-a potential pathway to early diagnosis. Otolaryngol Head Neck Surg. 2020;163(4):722–728.
   PubMed Web of Science ®Google Scholar
• Yu M, Liu Y, Xu D, et al. Prediction of the development of pulmonary fibrosis using serial thin-section CT and clinical features in patients discharged after treatment for COVID-19 pneumonia. Korean J Radiol. 2020;21(6):746–755.
   PubMed Web of Science ®Google Scholar
• Stokes EK, Zambrano LD, Anderson KN, et al. Coronavirus disease 2019 case surveillance – United States, 22 January–30 May, 2020. MMWR Morb. Mortal. Wkly. Rep. 2020;69(24):759–765.
   PubMed Web of Science ®Google Scholar
• Wei JF, Huang FY, Xiong TY, et al. Acute myocardial injury is common in patients with COVID-19 and impairs their prognosis. Heart. 2020;106(15):1154–1159.
   PubMed Web of Science ®Google Scholar
• Dogra S, Jain R, Cao M, et al. Hemorrhagic stroke and anticoagulation in COVID-19. J Stroke Cerebrovasc Dis. 2020;29(8):104984.
   PubMed Web of Science ®Google Scholar
• Kremer S, Lersy F, de Sèze J, et al. Brain MRI findings in severe COVID-19: a retrospective observational study. Radiology. 2020;297(2):E242–E251.
   PubMed Web of Science ®Google Scholar
• Aggarwal A, Shrivastava A, Kumar A, et al. Clinical and epidemiological features of SARS-CoV-2 patients in SARI ward of a tertiary care Centre in New Delhi. J Assoc Physicians India. 2020;68(7):19–26.
   PubMedGoogle Scholar
• Gaber TAK, Ashish A, Unsworth A. Persistent post-covid symptoms in healthcare workers. Occup Med. 2021;71(3):144–146.
   Google Scholar
• Prieto MA, Prieto O, Castro HM. Long COVID: cross sectional study. Rev Fac Cien Med Univ Nac Cordoba. 2021;78(1):33–36.
   PubMedGoogle Scholar
• Jacobson KB, Rao M, Bonilla H, et al. Patients with uncomplicated Coronavirus disease 2019 (Covid-19) have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic. Clin Infect Dis. 2021;73(3):e826–e829.
   PubMed Web of Science ®Google Scholar
• Perlis RH, Green J, Santillana M, et al. Persistence of symptoms up to 10 months following acute COVID-19 illness. medRxiv [Preprint]. 2021; Mar 8:2021.03.07.21253072.
   Google Scholar
• Sudre CH, Murray B, Varsavsky T, et al. Attributes and predictors of long COVID. Nat Med. 2021;27(4):626–631.
   PubMed Web of Science ®Google Scholar
• Sykes DL, Holdsworth L, Jawad N, et al. Post-COVID-19 symptom burden: what is long-COVID and how should we manage it? Lung. 2021;199(2):113–119.
   PubMed Web of Science ®Google Scholar
• Cortés-Telles A, López-Romero S, Figueroa-Hurtado E, et al. Pulmonary function and functional capacity in COVID-19 survivors with persistent dyspnoea. Respir Physiol Neurobiol. 2021;288:103644.
   PubMed Web of Science ®Google Scholar
• Makaronidis J, Firman C, Magee CG, et al. Distorted chemosensory perception and female sex associate with persistent smell and/or taste loss in people with SARS-CoV-2 antibodies: a community based cohort study investigating clinical course and resolution of acute smell and/or taste loss in people with and without SARS-CoV-2 antibodies in London, UK. BMC Infect Dis. 2021;21(1):221.
   PubMed Web of Science ®Google Scholar
• Townsend L, Dyer AH, Jones K, et al. Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection. PLoS One. 2020;15(11):e0240784.
   PubMed Web of Science ®Google Scholar
• Venturelli S, Benatti SV, Casati M, et al. Surviving COVID-19 in Bergamo province: a post-acute outpatient re-evaluation. Epidemiol Infect. 2021;149:e32.
   PubMed Web of Science ®Google Scholar
• Huang C, Huang L, Wang Y, et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet. 2021;397(10270):220–232.
   PubMed Web of Science ®Google Scholar
• Gomez JMD, Du-Fay-de-Lavallaz JM, Setri Fugar S, et al. Sex differences in COVID-19 hospitalization and mortality. J Womens Health. 2021;30(5):646–653.
   Web of Science ®Google Scholar
• Vahidy FS, Pan AP, Ahnstedt H, et al. Sex differences in susceptibility, severity, and outcomes of coronavirus disease 2019: cross-sectional analysis from a diverse US metropolitan area. PLoS One. 2021;16(1):e0245556.
   PubMed Web of Science ®Google Scholar
• Takahashi T, Ellingson MK, Wong P, et al. Sex differences in immune responses that underlie COVID-19 disease outcomes. Nature. 2020;588(7837):315–320.
   PubMed Web of Science ®Google Scholar
• Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study. Eur Arch Otorhinolaryngol. 2020;277(8):2251–2261.
   PubMed Web of Science ®Google Scholar
• Elibol E. Otolaryngological symptoms in COVID-19. Eur Arch Otorhinolaryngol. 2021;278(4):1233–1236.
   PubMed Web of Science ®Google Scholar
• Toth-Manikowski SM, Caldwell J, Joo M, et al. Sex-related differences in mortality, acute kidney injury, and respiratory failure among critically ill patients with COVID-19. Medicine. 2021;100(50):e28302.
   PubMed Web of Science ®Google Scholar
• Munblit D, Bobkova P, Spiridonova E, et al. Incidence and risk factors for persistent symptoms in adults previously hospitalized for COVID-19. Clin Exp Allergy. 2021;51(9):1107–1120.
   PubMed Web of Science ®Google Scholar
• Sigfrid L, Drake TM, Pauley E, et al. Long COVID in adults discharged from UK hospitals after COVID-19: a prospective, multicentre cohort study using the ISARIC WHO clinical characterisation protocol. Lancet Reg Health Eur. 2021;8:100186.
   PubMedGoogle Scholar
• Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev Immunol. 2016;16(10):626–638.
   PubMed Web of Science ®Google Scholar
• Sharma G, Volgman AS, Michos ED. Sex differences in mortality from COVID-19 pandemic: Are men vulnerable and women protected? JACC Case Rep. 2020;2(9):1407–1410.
   PubMedGoogle Scholar
• Stewart S, Newson L, Briggs TA, et al. Long COVID risk – a signal to address sex hormones and women’s health. Lancet Regional Health. 2021;11:100242.
   PubMedGoogle Scholar
• Global Health 5050: The Sex, Gender and COVID-19 Project. Tracking differences in COVID-19 infection, illness and death among women and men and producing the world’s largest analysis of sex and gender in national COVID-19 health policies [internet]. Washington DC: ICRW; 2021. Oct 27. Available from: https://globalhealth5050.org/the-sex-gender-and-covid-19-project/
   Google Scholar
• Nordhues HC, Bhagra A, Stroud NN, et al. COVID-19 gender disparities and mitigation recommendations: a narrative review. Mayo Clin Proc. 2021;96(7):1907–1920.
   PubMed Web of Science ®Google Scholar
• Westergaard D, Moseley P, Sørup FKH, et al. Population-wide analysis of differences in disease progression patterns in men and women. Nat Commun. 2019;10(1):666.
   PubMed Web of Science ®Google Scholar
• Wormser GP, Shapiro ED. Implications of gender in chronic Lyme disease. J Womens Health. 2009;18(6):831–834.
   Web of Science ®Google Scholar
• UK Health Security Agency. The effectiveness of vaccination against long COVID: A rapid evidence briefing. February 2022; [cited 2022 May XX]. Available from:https://ukhsa.koha-ptfs.co.uk/cgi-bin/koha/opac-retrieve-file.pl?id=fe4f10cd3cd509fe045ad4f72ae0dfff.
   Google Scholar
• Ledford H. Do vaccines protect against long COVID? What the data say. Nature. 2021;599(7886):546–548.
   PubMed Web of Science ®Google Scholar
• Bischof E, Wolfe J, Klein SL. Clinical trials for COVID-19 should include sex as a variable. J Clin Invest. 2020;130(7):3350–3352.
   PubMed Web of Science ®Google Scholar
• Kocher K, Delot-Vilain A, Spencer D, et al. Paucity and disparity of publicly available sex-disaggregated data for the COVID-19 epidemic hamper evidence-based decision-making. Arch Sex Behav. 2021;50(2):407–426.
   PubMed Web of Science ®Google Scholar
• Sugimoto CR, Ahn YY, Smith E, et al. Factors affecting sex-related reporting in medical research: a cross-disciplinary bibliometric analysis. Lancet. 2019;393(10171):550–559.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Breaking barriers towards more gender-responsive and equitable health systems, 18 October 2019; [cited 2022 Feb 1]. Available from: https://www.who.int/publications/m/item/breaking-barriers-towards-more-gender-responsive-and-equitable-health-systems.
   Google Scholar
• Brady E, Nielsen MW, Andersen JP, et al. Lack of consideration of sex and gender in COVID-19 clinical studies. Nat Commun. 2021;12(1):4015.
   PubMed Web of Science ®Google Scholar
• United Nations Population Fund (UNFPA). COVID-19: A gender lens. Protecting sexual and reproductive health and rights, and promoting gender equality (March 2020); [cited 2022 Feb 1]. Available from: https://www.unfpa.org/resources/covid-19-gender-lens.
   Google Scholar