Sex and Gender Differences in Health: What the COVID-19 Pandemic Can Teach Us
Authors: Primavera A. Spagnolo, JoAnn E. Manson, Hadine Joffe
Journal: Annals of Internal Medicine (2020)

Ideas and Opinions8 May 2020Sex and Gender Differences in Health: What the COVID-19 Pandemic Can Teach UsFREEPrimavera A. Spagnolo, MD, PhD, JoAnn E. Manson, MD, DrPH, and Hadine Joffe, MD, MScPrimavera A. Spagnolo, MD, PhDNational Institute on Neurological Disorders and Stroke Intramural Research Program, National Institutes of Health, Bethesda, Maryland (P.A.S.), JoAnn E. Manson, MD, DrPHConnors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts (J.E.M., H.J.), and Hadine Joffe, MD, MScConnors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts (J.E.M., H.J.)Author, Article, and Disclosure Informationhttps://doi.org/10.7326/M20-1941 SectionsAboutVisual AbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinkedInRedditEmail Sex; biological and physiologic traits characterizing males and females; and gender, a continuum of socioculturally constructed roles and behaviors associated with men, women, and gender-spectrum diversity, are among the most important determinants of health and disease outcomes. However, these fundamental factors are often ignored in biomedical research and are rarely incorporated into clinical care. We call for sex- and gender-specific and differentiating factors to be urgently included in the research, prevention, and therapeutics implementation response to the coronavirus disease 2019 (COVID-19) pandemic.Although available sex-disaggregated data for COVID-19 show equal numbers of cases between sexes, current evidence indicates that fatality rates are higher in men than in women. A recent report (23 April 2020) from the Italian National Institute of Health shows that of 23 188 deaths from COVID-19 infection in Italy, approximately 70% were in men. In the United States, provisional death counts for COVID-19 from February to April 2020 similarly indicate a sex bias in fatality rates: Of 37 308 deaths reported by the National Center for Health Statistics, 59% were in men. Similar trends have been reported in China (1) and South Korea (2).Taken together, these preliminary data suggest that sex- and gender-related factors may be implicated in COVID-19 vulnerability. As scientists, we may consider this an interesting observation to be explored in post hoc analyses, using available sex and gender data. Or we can investigate a priori the specific role of these factors and potentially leverage the mechanisms implicated in sex and gender differences in COVID-19 risk, progression, and outcomes, to identify effective prevention and treatment interventions for the entire population. Adopting a sex- and gender-informed perspective in research has already shown to improve patient care for cardiovascular diseases and other conditions that affect both women and men (3).Translating this perspective to the study of COVID-19 infection requires the first and essential step of collecting large-scale sex- and gender-disaggregated data. This task may pose some methodological challenges for gender, given the lack of validated tools to assess gender. Using sex when reporting biological factors and gender when reporting gender identity or sociocultural factors, and asking individuals about both their sex assigned at birth and their current gender identity, may facilitate data collection and improve comparability across studies.However, truly sex- and gender-informed research exceeds mere stratification by these variables. Researchers should also systematically assess biological (such as hormonal state, immune function, comorbid conditions, and concurrent treatments) and gender-related (such as lifestyle and socioeconomic status) factors in patients with COVID-19. Furthermore, as clinical trials investigating novel therapeutics to prevent and treat COVID-19 infection are being launched worldwide, it is imperative to incorporate sex- and gender-related data into these trials and to analyze and report treatment outcomes disaggregated by sex and gender.Taking these actions will be crucial to address several fundamental questions related to COVID-19. For example, we may elucidate to what extent sex biases in COVID-19 outcomes are linked to differences in sex hormone profiles. Sex hormones contribute to different immunologic responses in men and women: As a general rule, estrogens promote both innate and adaptive immune responses, which result in faster clearance of pathogens and greater vaccine efficacy. Conversely, testosterone has largely suppressive effects on immune function, which may explain the greater susceptibility to infectious diseases observed in men (3). Notably, changes in sex hormone may further shape the immune response to pathogens, highlighting the importance of studying factors that affect such levels (for example, age, pregnancy, menstrual cycle, exogenous sex-hormone therapies, men, and transgender individuals).Sex-related biological data may also be critical to investigate the contribution of sex hormones to sex differences in inflammatory response. In particular, reduction in testosterone levels in aging men has been associated with increased proinflammatory cytokine levels (4), which may contribute to worse COVID-19 progression in older men. Sex differences in disease progression may also be linked to estrogen-induced decreased expression of angiotensin-converting enzyme 2 (5), which acts as a functional receptor for SARS-CoV-2 (the virus causing COVID-19) to enter host target cells.Investigating sex hormone–influenced mechanisms and, more broadly, conducting sex- and gender-informed research may optimize the development of novel therapeutics and shed light on drug efficacy, safety profiles, and adherence to treatments currently tested for COVID-19, given that sex differences in pharmacokinetics and pharmacodynamics influence therapeutic effects and risk profiles of numerous medications, and that gender-related factors affect adherence to treatment, access to health care, and health-seeking behaviors (3).Stress-related disorders and the long-term consequences of COVID-19 on health outcomes highlight another important effect of sex and gender. Beyond being a pandemic infectious disease, COVID-19 also acts as a potent stressor, with millions of individuals experiencing fear and social isolation over a prolonged period. Exposure to persistent stress is associated with increased vulnerability to and severity of stress-related psychiatric disorders (such as posttraumatic stress disorder, panic disorder, and major depression), which occur more frequently in women than men (6). Indeed, preliminary evidence from China during the initial phase of the COVID-19 outbreak shows an increased prevalence and severity of depressive, anxious, and posttraumatic symptoms in women than in men (7).This gender bias is supported by evidence of sex differences in stress response systems, which increase endocrine, affective, and arousal responses to stress in females (6, 8), who also appear to be more susceptible to social isolation (9). Gender-related factors, such as the predominant roles of women as family caregivers and as frontline health care workers, further exacerbate stress exposure. We have the unprecedented opportunity to conduct large longitudinal studies to directly test whether the relationship between stress exposures and the prevalence and presentation of stress-related psychiatric disorders is mediated by sex- and gender-related factors.On the basis of these observations, we call on scientists and biomedical institutions to recognize the importance of investigating sex- and gender-specific and differentiating effects of COVID-19 to develop and implement prevention and treatment interventions able to address the acute and long-term effects of this pandemic on the health and well-being of the population. By doing so, we will reshape the way we think about diseases as we conceive and conduct research, thus optimizing health for the entire population.References1. Chen T, Wu D, Chen H, et al. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ. 2020;368:m1091. [PMID: 32217556] doi:10.1136/bmj.m1091 CrossrefMedlineGoogle Scholar2. Dudley JP, Lee NT. Disparities in age-specific morbidity and mortality from SARS-CoV-2 in China and the Republic of Korea. Clin Infect Dis. 2020. [PMID: 32232322] doi:10.1093/cid/ciaa354 CrossrefMedlineGoogle Scholar3. Bartz D, Chitnis T, Kaiser UB, et al. Clinical advances in sex- and gender-informed medicine to improve the health of all: a review. JAMA Intern Med. 2020. [PMID: 32040165] doi:10.1001/jamainternmed.2019.7194 CrossrefMedlineGoogle Scholar4. Bianchi VE. The anti-inflammatory effects of testosterone. J Endocr Soc. 2019;3:91-107. [PMID: 30582096] doi:10.1210/js.2018-00186 CrossrefMedlineGoogle Scholar5. La Vignera S, Cannarella R, Condorelli RA, et al. Sex-specific SARS-CoV-2 mortality: among hormone-modulated ACE2 expression, risk of venous thromboembolism and hypovitaminosis d. Int J Mol Sci. 2020;21. [PMID: 32331343] doi:10.3390/ijms21082948 CrossrefMedlineGoogle Scholar6. Hodes GE, Epperson CN. Sex differences in vulnerability and resilience to stress across the life span. Biol Psychiatry. 2019;86:421-432. [PMID: 31221426] doi:10.1016/j.biopsych.2019.04.028 CrossrefMedlineGoogle Scholar7. Liu N, Zhang F, Wei C, et al. Prevalence and predictors of PTSS during COVID-19 outbreak in China hardest-hit areas: gender differences matter. Psychiatry Res. 2020;287:112921. [PMID: 32240896] doi:10.1016/j.psychres.2020.112921 CrossrefMedlineGoogle Scholar8. Bangasser DA, Wicks B. Sex-specific mechanisms for responding to stress. J Neurosci Res. 2017;95:75-82. [PMID: 27870416] doi:10.1002/jnr.23812 CrossrefMedlineGoogle Scholar9. Senst L, Baimoukhametova D, Sterley TL, et al. Sexually dimorphic neuronal responses to social isolation. Elife. 2016;5. [PMID: 27725087] doi:10.7554/eLife.18726 CrossrefMedlineGoogle Scholar Comments 0 Comments Sign In to Submit A Comment Olav T. Muurlink, PhD, MAPS, 1 Andrew W. Taylor-Robinson, PhD, FRCPath 2,*1 Centre for Sustainable Innovation, Central Queensland University 2 Infectious Diseases Research Group, Central Queensland University20 August 2020 Sex and Gender Differences in Health: What the COVID-19 Pandemic Can Teach Us Puzzling differences are emerging between male and female morbidity and mortality rates for COVID-19, as highlighted by Spagnolo et al. in this journal (1) and by others (2-4). While the reasons for this sex- and gender-related disparity are undoubtedly multifactorial, we predict that this may be amplified in the developing world due to prevailing cultural factors (5). Currently, credible data from non-industrialized nations on COVID-19 are sparse, with recorded case numbers seemingly suppressed by unreliable surveillance, lower testing capacity and an underlying burden of infectious diseases that may mimic key symptoms, notably pyrexia. Indeed, acute undifferentiated febrile illness is a common feature of resource-limited tropical regions. Patterns of prevalence of vector-borne diseases in the developing world, however, offer an indication of likely COVID-19 infection and morbidity gender trends. Cultural factors, in particular the extent to which long or ‘modest’ clothing is worn and the convention of separating adults by gender, may inadvertently determine the rapidity and extent of the spread of communicable diseases including COVID-19. A study of six Asian countries on the prevalence of dengue showed a striking tendency towards greater infection rates for males compared to females, but only for those aged 15 or over for whom cultural differences in work patterns outside the home, social interaction and dress all apply (6). This disparity is plausibly explained as a difference in exposure to the mosquito vector and is linked to established recommendations on wearing protective clothing. However, it is noteworthy that in Brazil, where standards of modesty for male and female clothing are equivalent (7), this gender difference in dengue incidence disappears (8). Cultures that place greater restrictions on the movement and dress of women are likely to see fewer opportunities for both vector- and air-borne pathogen transmission for women relative to men. One of the known routes of infection with SARS-CoV-2 is touching one’s face, leading to public health agency advisories against this practice (9). This presents a challenge to community education since this behaviour is instinctive (10), habitual and very frequent (11). Yet, in conservative Muslim cultures in particular, where wearing a burka or niqab, providing full or partial coverage of the face, respectively, is relatively common in public, touching of mouth, nose and eyes by females is correspondingly restricted. Facial covering additionally affords a limited level of filtration of air-borne droplets (12), such as those carrying virus particles. In contrast, the cultural predilection for facial hair among male Muslims is likely to further increase male exposure to the virus, particularly amongst health professionals where facial hair compromises the seal of P2/N95-standard particulate filtering respirators and surgical masks (13). References Spagnolo PA, Manson JE, Joffe H. Sex and gender differences in health: what the COVID-19 pandemic can teach us. Ann Intern Med. 2020; May 8: M20-1941. doi: 10.7326/M20-1941 Wenham C, Smith J, Morgan R; Gender and COVID-19 Working Group. COVID-19: the gendered impacts of the outbreak. Lancet 2020; 395: 846-8. doi: 10.1016/S0140-6736(20)30526-2 Dana PK, Sadoughi F, Hallajzadeh J, et al. An insight into the sex differences in COVID-19 patients: what are the possible causes? Prehosp Disaster Med. 2020; 35: 438-41. doi: 10.1017/S1049023X20000837 Stoian AC, Toth PP, Kempler P, et al. Gender differences in the battle against COVID-19: impact of genetics, comorbidities, inflammation and lifestyle on differences in outcomes. Int J Clin Pract. 2020 Aug 8; e13666. doi: 10.1111/ijcp.13666. Online ahead of print Muurlink OT, Taylor-Robinson AW. COVID-19: Cultural predictors of gender differences in global prevalence patterns. Front. Public Health 2020; 8: 174. doi: 10.3389/fpubh.2020.00174 Anker M, Arima Y. Male–female differences in the number of reported incident dengue fever cases in six Asian countries. Western Pac Surveill Response J. 2011; 2: 17-23. doi: 10.5365/WPSAR.2011.2.1.002 Hussain A. Carnival reveals much about gender, sexuality, and culture in Brazil. March 6, 2013. https://berkleycenter.georgetown.edu/posts/carnival-reveals-much-about-gender-sexuality-and-culture-in-brazil Date accessed: August 20, 2020 Teixeira M da G, Nascimento Costa M da C, Guerra Z, et al. Dengue in Brazil: Situation-2001 and trends. Dengue Bull. 2002; 26: 70-6 World Health Organization. Coronavirus disease (COVID-19) advice for the public. Last updated June 4, 2020. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public Date accessed: August 20, 2020 Suarez SD, Gallup GG Jr. Face touching in primates: a closer look. Neuropsychologia 1986; 24: 597-600 Benning SD, Labus B, Barchard KA. How to stop touching your face to minimize spread of coronavirus and other germs. The Conversation, March 19, 2020. https://theconversation.com/how-to-stop-touching-your-face-to-minimize-spread-of-coronavirus-and-other-germs-133683 Date accessed: August 20, 2020 Rengasamy S, Eimer B, Shaffer RE. Simple respiratory protection — evaluation of the filtration performance of cloth masks and common fabric materials against 20–1000 nm size particles. Ann Occup Hyg. 2010; 54: 789-98. doi: 10.1093/annhyg/meq044 Sandaradura I, Goeman E, Pontivivo G, et al. A close shave? Performance of P2/N95 respirators in healthcare workers with facial hair: results of the BEARDS (BEnchmarking Adequate Respiratory DefenceS) study. J Hosp Infect., 2020; 104: 529-33. doi: 10.1016/j.jhin.2020.01.006 Disclosures: We declare no conflicts of interest. Primavera A. Spagnolo, MD, PhD; JoAnn E. Manson, MD, DrPH; Hadine Joffe MD, MScConnors Center for Women’s Health and Gender Biology, Brigham and Women’s Hospital, and Harvard Medical School12 November 2020 Authors' Response The comment from Muurlink and Taylor-Robinson in response to our recent opinion article highlights the role that cultural factors, among other gender-related factors across the world, may play in exacerbating gender-differences in infectious disease risk and outcomes, including during the current coronavirus disease 2019 (COVID-19) pandemic. The authors discussed how gendered modesty clothing norms present in several cultures may explain sex-differences in the transmission of vector-borne diseases and suggest that this could also lead to sex-biases in COVID-19 transmission. While protecting clothing is an integral part of infection control and prevention, and face covering has been shown to reduce droplets and aerosol transmission1, we believe that the gendered dimension of COVID-19 pandemic is more multifaceted. Gender, which comprises cultural and societal norms, roles, and behaviors, influences both patterns of exposure to infectious agents and their treatment. For example, gender roles influence where men and women spend their time throughout the day, the infectious agents they are exposed to, as well as the frequency and intensity of exposure. Gender disparities are also observed in access to, and use of, preventive and treatment modalities in health care, which, may influence the course and outcome of infections and other illnesses2. The COVID-19 pandemic appears to be no exception. In a recent study, Tadiri and colleagues analyzed male: female ratio of cases for all countries reporting sex-disaggregated data, as a function of the country’s gender inequality (per the 2017 United Nations Development report)3. Men accounted for more cases in countries with higher gender inequality, although it was not clear whether these differences were related to employment status, disparities in access to rationed SARS-CoV-2 tests or other reasons. A further study analyzing data from eight countries reported large gender differences in COVID-19−related beliefs and behaviors, with women more likely to perceive the pandemic as a serious health problem and to agree and comply with restraining measures4. Thus, gender appears to be a crucial factor influencing important aspects of the COVID-19 pandemic, as well as of other infectious disease epidemics2. However, differences in COVID-19 severity of disease and mortality rates between men and women also call for the investigation of biological sex-specific mechanisms affecting COVID-19 disease progression. Attributing differences in disease susceptibility, course and outcome uniquely to either sex or gender can be extremely complex and, in the case of the COVID-19 pandemic, even premature. Sex and gender are strongly inter-related and both factors should be investigated to develop effective, equitable, and sex-and gender-informed policies and interventions. The COVID-19 pandemic is a powerful reminder that we cannot ignore the role of sex and gender in health any longer. References World Health Organization. Advice on the use of masks in the context of COVID-19: interim guidance, 6 April 2020. Geneva: WHO; 2020 [Available from: https://apps.who.int/iris/handle/10665/331693. World Health Organization. Addressing Sex and Gender in Epidemic-Prone Infectious Diseases Geneva: WHO; 2007 [Available from: https://www.who.int/csr/resources/publications/SexGenderInfectDis.pdf. Tadiri CP, Gisinger T, Kautzy-Willer A, et al. The influence of sex and gender domains on COVID-19 cases and mortality. Canadian Medical Association Journal 2020;192(36):E1041-E45. doi: 10.1503/cmaj.200971 Galasso V, Pons V, Profeta P, et al. Gender differences in COVID-19 attitudes and behavior: Panel evidence from eight countries. Proceedings of the National Academy of Sciences 2020;117(44):27285-91. doi: 10.1073/pnas.2012520117 Author, Article, and Disclosure InformationAuthors: Primavera A. Spagnolo, MD, PhD; JoAnn E. Manson, MD, DrPH; Hadine Joffe, MD, MScAffiliations: National Institute on Neurological Disorders and Stroke Intramural Research Program, National Institutes of Health, Bethesda, Maryland (P.A.S.)Connors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts (J.E.M., H.J.)Disclaimer: The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of their funders, which had no role in the development of this manuscript.Financial Support: By the National Institute on Neurological Disorders and Stroke Intramural Research Program Intramural Research Programs (P.A.S.) and Brigham & Women's Hospital and Harvard Medical School (H.J. and J.E.M.).Disclosures: Disclosures can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M20-1941.Corresponding Author: Hadine Joffe, MD, MSc, Connors Center for Women's Health and Gender Biology, Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, 75 Francis Street, Thorn 1111, Boston, MA 02115; e-mail, hjoffe@bwh.harvard.edu.Current Author Addresses: Dr. Spagnolo: National Institute on Neurological Disorders and Stroke, National Institutes of Health, 10 Center Drive, CRC Building 10, 7D42, Bethesda, MD 22314.Dr. Manson: Brigham and Women's Hospital, Harvard Medical School, 900 Commonwealth Avenue, 3rd Floor, Boston, MA 02215.Dr. Joffe: Connors Center for Women's Health and Gender Biology, Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, 75 Francis Street, Thorn 1111, Boston, MA 02115.Author Contributions: Conception and design: P.A. Spagnolo, J.E. Manson, H. Joffe.Analysis and interpretation of the data: J.E. Manson.Drafting of the article: P.A. Spagnolo.Critical revision for important intellectual content: J.E. Manson, H. Joffe.Final approval of the article: P.A. Spagnolo, J.E. Manson, H. Joffe.Administrative, technical, or logistic support: J.E. Manson.This article was published at Annals.org on 8 May 2020. PreviousarticleNextarticle Advertisement FiguresReferencesRelatedDetailsSee AlsoSex and Gender Differences in Health Primavera A. Spagnolo , JoAnn E. Manson , Hadine Joffe Sex and Gender Differences in Health Olav T. Muurlink , Andrew W. 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Taylor-Robinson, PhDSex Differences in the Coronavirus Disease 2019Sex and Gender Differences in Lung DiseaseEffect of Sex on Clinical Outcomes in Patients with Coronavirus Disease: A Population-Based StudyRole of short-term estradiol supplementation in symptomatic postmenopausal COVID-19 females: A randomized controlled trialGender differences in emotional response to the COVID‐19 outbreak in SpainStatus of Novel Coronavirus Disease and Analysis of Mortality in Mexico, Until June 30th, 2020: An Ecological StudyTemporal dynamics in total excess mortality and COVID-19 deaths in Italian citiesSex differences in clinical phenotype and transitions of care among individuals dying of COVID-19 in ItalySex‐ and Age‐Specific Differences in COVID ‐19 Testing, Cases, and Outcomes: A Population‐Wide Study in Ontario, CanadaCOVID-19 Pandemic in Women–Rheumatologist’s PerspectiveAn Insight into the Sex Differences in COVID-19 Patients: What are the Possible Causes?Inpatient Mortality According to Level of Respiratory Support Received for Severe Acute Respiratory Syndrome Coronavirus 2 (Coronavirus Disease 2019) Infection: A Prospective Multicenter Study 1 September 2020Volume 173, Issue 5 Page: 385-386 Keywords COVID-19 Infectious diseases Obstetrics and gynecology Pathogens Scientists Sex hormones Sexual identity Stroke Testosterone Treatment guidelines ePublished: 8 May 2020 Issue Published: 1 September 2020 Copyright & PermissionsCopyright © 2020 by American College of Physicians. 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