key: cord-0871674-8sa977k8
authors: Connor, Jade; Madhavan, Sarina; Mokashi, Mugdha; Amanuel, Hanna; Johnson, Natasha R.; Pace, Lydia E.; Bartz, Deborah
title: Health Risks and Outcomes that Disproportionately Affect Women during the Covid-19 Pandemic: A Review
date: 2020-09-13
journal: Soc Sci Med
DOI: 10.1016/j.socscimed.2020.113364
sha: 5f91593e262883768d4fad93c4f7e87d1b18ba14
doc_id: 871674
cord_uid: 8sa977k8

BACKGROUND: The Covid-19 pandemic is straining healthcare systems in the US and globally, which has wide-reaching implications for health. Women experience unique health risks and outcomes influenced by their gender, and this narrative review aims to outline how these differences are exacerbated in the Covid-19 pandemic. OBSERVATIONS: It has been well described that men suffer from greater morbidity and mortality once infected with SARS-CoV-2. This review analyzed the health, economic, and social systems that result in gender-based differences in the areas healthcare workforce, reproductive health, drug development, gender-based violence, and mental health during the Covid-19 pandemic. The increased risk of certain negative health outcomes and reduced healthcare access experienced by many women are typically exacerbated during pandemics. We assess data from previous disease outbreaks coupled with literature from the Covid-19 pandemic to examine the impact of gender on women’s SARS-CoV-2 exposure and disease risks and overall health status during the Covid-19 pandemic. CONCLUSIONS: Gender differences in health risks and implications are likely to be expanded during the Covid-19 pandemic. Efforts to foster equity in health, social, and economic systems during and in the aftermath of Covid-19 may mitigate the inequitable risks posed by pandemics and other times of healthcare stress.

Pandemics, as we are learning from the Covid-19 outbreak, can infect and sicken societal institutions and systems just as effectively as the virus weakens its organic host. Much as the SARS-CoV-2 virus confers disproportionate morbidity to individuals on the periphery of health-the elderly and those with chronic medical conditions-the societal effects of the pandemic disproportionately impact marginalized populations. As the Covid-19 crisis exacerbates system-level deficits, disparities in disease risk and outcomes are widening for vulnerable populations.

Gender is a social determinant of health, unique from but entangled with sex differences (Springer et al., 2012; Rich-Edwards et al., 2018) , and an axis along which the Covid-19 pandemic is widening health disparities. Outside of the pandemic, women on average report more physical and mental unhealthy days per year than men despite utilizing more preventive care services (Centers for Disease Control and Prevention [CDC] , 2013). Women also have worse outcomes for prevalent health conditions including asthma (CDC, 2013) , diabetes (Roche women vulnerable to the structural dysfunction impacting their health status. In this review, we use evidence from past global disease outbreaks and the current understanding of the pandemic to highlight the pandemic-related challenges present for women, particularly women in the United States (US), associated with healthcare workforce capacity, reproductive health, drug development, intimate partner violence (IPV), and mental health. Our discussion is centered around those issues that have direct impacts on clinical care both during and in the aftermath of this pandemic. Social determinants of health-including economic, sociopolitical, cultural factors-affect each of these topics, and where possible, we have included discussions of these issues from an intersectional lens (Crenshaw, 1989) . Moreover, we note that the impact of multiple overlaid identities on health outcomes are not simply additive, but uniquely interactive (Hankivsky, 2012) . We recognize that gender encompasses a spectrum of non-binary identities including transgender and gender-diverse individuals, and these groups are subject to unique disparities that this pandemic has the potential to exacerbate (Daniel & Butkus, 2015) .

However, this review predominantly explores issues related to people who identify as women.

The gender disparities outlined here demonstrate the need for deliberate action to foundationally address these issues at baseline and mitigate their amplification during pandemics. We conclude by recommending interventions to promote a more gender-equitable paradigm during and after disease outbreaks.

Women compose the majority of the healthcare workforce; 76% of US healthcare workers are women ( Figure 1 ) (US Census Bureau, 2020) . Reports from the CDC emphasize J o u r n a l P r e -p r o o f healthcare workers' increased risk of contracting SARS-CoV-2 given the close interaction with high concentrations of patients and visitors amidst shortages of personal protective equipment (PPE) (CDC, 2020a) . Women are concentrated in roles requiring the most close, prolonged contact with patients ( Figure 1 ) (US Census Bureau, 2020).

The disproportionate economic impacts of the pandemic on women further exacerbate this risk. Eleven percent of women, compared to 4% of men, currently face underemployment (Center for Law and Social Policy, 2020). With increased job loss due to the pandemic (Nicola et al., 2020) , many women are forced to work part-time in multiple healthcare facilities without paid sick leave, thereby increasing their risk of SARS-CoV-2 exposure and transmission to others (Pichler et al., 2020) . Beyond this, although PPE is often marketed as "unisex," findings show that they are manufactured according to traditional male proportions (Trades Union Congress, 2017) . This has led to some women wearing ill-fitting PPE, potentially compromising their degree of protection (Pugh, 2020). These gender-based occupational exposure risks must be addressed in workforce planning and in assessing risk for families as women return home after their shifts.

should they become sick from their caregiving roles. This sparse legal protection has been demonstrated to place workers in jobs that make them more vulnerable to SARS-CoV2 infection and prevent these workers from adhering to Covid-19 social distancing recommendations, accessing testing and treatment, and receiving economic relief from government programs (Page et al., 2020; KFF, 2020) .

Beyond the paid workforce, 65% of informal family caregivers in the US are women (Feinburg et al., 2011) . Roughly 87% of individuals with long-term care needs living in the community rely exclusively on unpaid caregivers for assistance (Kaye et al., 2010) , making female informal caregivers a significant proportion of the caregiving workforce. Due to their personal caregiving responsibilities, working women lose roughly $5000 annually in income from wage penalties and reduced hours (Van Houtven et al., 2013) . Conversely, male informal caregivers do not experience any difference in income for these responsibilities (Van Houtven et al., 2013) .

Outside of disease outbreaks, female caregivers are more likely to experience a specific stress termed "caregiver burden," the multidimensional toll that caregivers experience to their social, emotional, spiritual, financial, and physical wellbeing (Adelman et al., 2014) . Perceived lack of agency in choosing the role, financial stress, and social isolation are associated with higher caregiver burden (Adelman et al., 2014) . The Covid-19 pandemic is already exacerbating women's caregiver responsibilities with schools and childcare centers preventatively closed nationwide in the US (Graves, 2020). The societal norms and structures dictating that women assume caregiving roles are augmented during disease outbreaks (Smith, 2019) , limiting J o u r n a l P r e -p r o o f women's choice in becoming a caregiver. As a result, the tasks of daytime childcare fall disproportionately on women who may already be working formal jobs, maintaining their households, and fulfilling their original caregiving responsibilities. Consequently, it is likely that women are experiencing more caregiver burden during the pandemic while being isolated from the social supports needed to reduce this burden.

Pandemics limit access to the healthcare system, notably to preventative and reproductive healthcare. Evidence from prior pandemics and current experience reveal that obstetric care is particularly compromised. According to Ellington et al. (2020) , pregnant women infected with SARS-CoV-2 are at greater risk for severe illness when compared to nonpregnant women with SARS-CoV-2, including increased risk of hospitalization (aRR=5.4, 95% CI 5.1-5.6), intensive care unit admission (aRR=1.5, 95% CI 1.2-1.8) and mechanical ventilation (aRR=1.7, 95% CI 1.2-2.4). This study found no difference in death among pregnant and nonpregnant women. The reported medical vulnerability among pregnant people are likely due in part to physiological changes that occur during pregnancy and increased exposure risk due to clinical settings and procedures. However, this study was limited by missing data points among its participants including pregnancy status (missing for nearly 75% of participants) and medical comorbidities (missing in close to 80% of cases). More broadly, differences in screening, While reproductive healthcare is often reduced to obstetric medicine during pandemics (Smith, 2019) , it is equally critical to ensure access to comprehensive family planning. A survey of US women indicates that since the inception of shelter-in-place restrictions in early 2020, women have experienced shifts in family planning preferences (i.e., wanting to delay or avoid pregnancy during the Covid-19 pandemic) (Lindberg et al., 2020) . Despite the decreased desire to become pregnant, women have experienced logistical and political threats to contraception and abortion access during the Covid-19 pandemic. Shelter-in-place restrictions and decreased J o u r n a l P r e -p r o o f outpatient visits limit access to and anticipatory stockpiling of contraception. One-third of US women reported delays or cancellations in sexual and reproductive healthcare, with a higher proportion of reports from Black, Latinx, LGBTQIA, and low-income women. Women in these groups also report more concern about their ability to access sexual and reproductive healthcare services, particularly contraception (Lindberg et al., 2020) . Despite this potential increase in unintended pregnancies and financial strain of the pandemic's economic fall-out, some states are threating to halt abortion services (Ollstein, 2020) , inaccurately denoting these procedures as elective and able to be delayed (Smith et al., 2018; Watson, 2018; Bayefsky et al., 2020) . In response, the American Medical Association (AMA) and ACOG have reaffirmed the authority of physicians to make decisions about essential healthcare in line with patient wellbeing and reproductive autonomy (AMA, 2020; ACOG, 2020a).

Abortion, chosen by nearly one million women annually in the US, affords many women and families improved health and economic status (Jones & Jerman, 2017) . Abortions are timesensitive procedures (Bayefsky et al., 2020; AMA, 2020). With each week of gestation, surgical complexity and risks increase, as does the amount of PPE, supplies, and clinic staff for each procedure. Since the majority of states impose upper gestational age limits on abortion procedures, delays will cause many women to "time-out," resulting in forced childbearing.

Access to abortion is limited at baseline in the US, particularly for poor and rural-dwelling women (Jones & Jerman, 2017) . Despite the challenges in access to family planning in a pandemic, medication abortion facilitated by telemedicine is prohibited in eighteen US states 

Women are underrepresented in drug development trials; many researchers fail to design studies with adequate samples of women, and even fewer analyze results according to gender and sex (Liu & Mager, 2016; Nowogrodzki, 2017) . For example, women were excluded from all phases of development of a formulation of tenofovir alafenamide/emtricitabine for HIV pre-exposure prophylaxis. This drug has been approved by the Food and Drug Administration (FDA) for men only, despite the trial failing to meet FDA sex-specific standards (Goldstein & Walensky, 2019). Racial and ethnic minorities in the US are also vastly underrepresented in clinical research for structural and historical reasons, making non-white women rare demographics in studies (Rochon et al., 2004; Hussain-Gambles et al., 2004) . The trend toward excluding women is likely to continue with trials for SARS-CoV-2 vaccines and treatment.

J o u r n a l P r e -p r o o f Furthermore, pregnant and lactating people are at increased risk of exclusion from clinical trials for SARS-CoV-2 medications. At baseline, pregnant and lactating people are systematically excluded from most drug and vaccine trials, given the risks of teratogenicity (Shields & Lyerly, 2013) . Out of the over 2400 research studies registered on ClinicalTrials.gov as of July 2020, only 54 trials specify the inclusion of pregnant people (ClinicalTrials.gov, 2020).

A review of industry-sponsored clinical trials suggests that researchers may overinterpret federal guidelines on exclusion criteria and make flawed assumptions about pregnant people's willingness to participate (Shields & Lyerly, 2013) . This hinders patients and healthcare providers from making informed decisions about the efficacy and safety of medications and vaccines for use during pregnancy (Shields & Lyerly, 2013) . Furthermore, most data on efficacy of drugs in pregnant people are gathered retrospectively from inadvertent exposures, which impose greater risk than that incurred during regulated research trials (Shields & Lyerly, 2013) . (North, 2020) . Shelter-in-place restrictions socially and physically isolate families together. This, coupled with the mental and economic strains of the pandemic, is likely initiating and exacerbating IPV and GBV (Van Gelder et al., 2020) . Due to these circumstances, it is estimated that 15 million additional instances of GBV will occur globally every 3 months while shelter-inplace restrictions are in place (United Nations Population Fund, 2020).

Beyond its direct implications for physical and mental health, IPV is a social determinant of health and is associated with higher morbidity and mortality for co-occurring diseases (Miller & Mccaw, 2019) . Within routine circumstances, interfacing with healthcare professionals serves as an important intervention to detect IPV; 37% of survivors of IPV who chose to disclose abuse told their healthcare provider (US Senate Committee on the Judiciary, 2005) . A year-long study in a managed care setting demonstrated that healthcare providers trained to detect IPV made twice as many referrals to an on-site IPV evaluator as untrained providers (US Senate Committee on the Judiciary, 2005). Provider awareness of IPV screening and appropriate referral channels will be essential in patient care as shelter-in-place restrictions are lifted.

During the Covid-19 pandemic, resources for survivors are under increased strain due to the higher incidence of IPV (North, 2020; Townsend, 2020) . One-third of women experiencing IPV reported difficulty accessing resources after these incidents due to the pandemic in a May 2020 survey (Lindberg et al., 2020) . Additionally, the CEO of Young Women's Christian J o u r n a l P r e -p r o o f recently reported that most of the YWCA shelters nationwide were at or near capacity at the peak of the pandemic, especially in states that have felt the impact of Covid-19 for the longest period of time (North, 2020) . Many of these densely-populated shelters have a high risk of viral transmission between residents. This has led some sites to use recreational vehicles as makeshift shelters in an effort to adhere to social distancing recommendations (North, 2020) .

Finally, while shelters have remained open, they rely on now-closed institutions like judicial courts to conduct much of their legal advocacy work. Together, these circumstances represent dangerous, often tragic, public health emergencies that disproportionately affect women.

Furthermore, the effect of the Covid-19 pandemic and response warrants heightened vigilance for the healthcare workforce to detect IPV, advocate for survivors, and incorporate IPV protections into emergency response planning.

Threatened and actual experiences of harm present challenges to mental health for survivors of Covid-19 infection, healthcare workers, and community members alike. During the SARS (2003), Ebola (2014), and Zika (2016) outbreaks, survivors of the illness experienced isolation, threat to life, stigma, and guilt as well as neuropsychiatric sequelae of the primary viral disease and treatment (Mak et al., 2009; Tucci et al., 2017) . Healthcare workers during the SARS and Ebola outbreaks experienced unique stressors related to working on the front lines, including increased occupational risk of infection, job stress, and fear of transmitting the disease to loved ones (Tucci et al., 2017; Wu et al., 2009) . Community members experienced J o u r n a l P r e -p r o o f distress related to media messaging, resource insecurity, distrust of the healthcare system, trauma from the illness or death of others, isolation, burden of caregiving, and fear of infection (Tucci et al., 2017; Shultz et al., 2015; Vetter et al., 2016) . Subsequent studies demonstrated that outbreak-specific stressors resulted in poorer mental health outcomes for all groups, with increased rates of sleep disturbance, post-traumatic stress disorder (PTSD), depression, and anxiety in the short and long term (Mak et al., 2009; Tucci et al., 2017; Wu et al., 2009; Vetter et al., 2016) . While these risk factors can affect the mental health of all populations during the Covid-19 pandemic, there is likely a differential impact on women.

Previous work suggests that gendered differences in mental health disorders outside of the disease outbreaks exist largely due to structurally imposed strains on women (Afifi, 2007) , with disproportionate impacts on Black, Latinx, Native, and immigrant populations, partially due to discrimination (American Psychiatric Association, 2007; Greenwood et al., 2017) .

Gendered social roles and power differentials contribute to increased risk of chronic stress and loss of agency (Afifi, 2007; World Health Organization [WHO], 2002; Williams & Kurina, 2002; Thomas, 1997) . Sociological research on women's social roles hypothesize several sources of chronic stress: empathic vicarious stress, lack of social support, workforce participation, parenthood, and caregiving responsibilities (Williams & Kurina, 2002; Thomas, 1997) . Follow-up studies demonstrate that greater dissatisfaction with social roles correlates with increased levels of stress in women (Thomas, 1997; Sumra & Schillaci, 2015) .

The unique experience of stress that women encounter at baseline contributes to a higher prevalence of mental health disorders, including depression, anxiety, and PTSD (Afifi, 2007) . Among people with substance use disorders, women often have faster progression to J o u r n a l P r e -p r o o f 13 addiction and are more likely to have co-occurring mental disorders than men, supporting the theory that substance use serves as a coping mechanism for many women (McHugh et al., 2014) . Despite greater utilization of mental health resources, women in the US are twice as likely to have unmet needs for mental health services as men, often because of inadequate insurance coverage and stigma associated with seeking care (US Department of Health and Human Services, 2010).

Although literature regarding gender disparities in mental health during disease outbreaks is limited, the above-mentioned gender differences in stress experience and exposure are likely exacerbated by pandemics. Gender roles tend to be reinforced during times of disease outbreak (Smith, 2019; Davies & Bennett, 2016) . This likely increases feelings of stress, dissatisfaction, and lack of autonomy among women as they try to reconcile their selfidentity with their imposed roles. Therefore, when insults to mental wellbeing occur, they are added to women's baseline stress and feelings of disempowerment, increasing the risk of mental health disorders.

Women disproportionately shoulder factors (e.g., social isolation, caregiving roles, resource insecurity) demonstrated in past pandemics to increase the risk of mental health disorders. A multinational survey found that women without social support are more vulnerable to negative mental health outcomes than men without social connections, due to women's greater reliance on social support (Dalgard et al., 2006) . Because women cannot access previously cultivated supportive relationships during Covid-19 due to social distancing, they may feel the effects of isolation more acutely.

Some of the behavior changes motivated by the stress of this pandemic may prove beneficial to women, however. A May 2020 survey conducted by the CDC demonstrated that although men and women largely had similar beliefs and behaviors regarding public health measures, a greater proportion of women reported avoiding public places and wearing face coverings while in public (Czeisler et al., 2020) . Other surveys conducted in the US show that a higher proportion of women than men self-report adherence to public health measures including avoiding social gatherings and travel, engaging in frequent hand hygiene, and stockpiling of food and medications (Frederiksen et al., 2020 , Park et al., 2020 . Stricter adherence to social distancing guidelines and avoidance of risky behaviors may be protective for SARS-CoV-2-related disease and death for women.

In the 2003 SARS outbreak, female healthcare workers were at higher risk of psychiatric morbidity (OR=1.58, 95% CI 1.07-2.33) (Chong et al., 2004) than their male counterparts due to their caregiving role (Chong et al., 2004; Tam et al., 2004) . Similarly, in the Covid-19 pandemic, the high proportion of female healthcare workers makes these women at occupational risk of poor mental health outcomes. The Covid-19 pandemic also presents a perfect storm for female informal caregivers to experience increased burden, as mentioned above, which has demonstrated negative outcomes such as poor self-care, depression, and anxiety (Adelman, 2014). Furthermore, this pandemic has incited a rapid economic downturn, severely affecting industries with high proportions of female employees (i.e., hospitality, travel, food service, education) (Alon et al., 2020). Limited access to healthcare resources during the Covid-19 pandemic affects non-white, immigrant, and low-income women in particular, who are less likely to have adequate health insurance and financial resources (Alon et al., 2020) . These issues will both contribute to the development of mental health disorders and limit access to mental health resources for women during and after the pandemic.

The disparate impacts of stressors among genders during the Covid-19 pandemic are already being seen. A study of the Hubei Province in China showed that women endorsed significantly more post-traumatic stress symptoms than men in the aftermath of the Covid-19 outbreak (Liu et al., 2020) . Figure 2 shows the results of a KFF survey from March 2020 in which women in the US expressed significantly more concern than men about risks of Covid-19 exposure, lost income, and overwhelming treatment costs (Frederiksen et al., 2020) . More women also reported poor mental health than men ( Figure 2 ) (Frederiksen et al., 2020) . A study of US individuals' stress and coping during the Covid-19 pandemic showed similar results, with women experiencing more stress-inducing events and reporting more severe stress than men (Park et al., 2020) . Among pregnant women, anxiety related to Covid-19 is widespread. A survey of pregnant women in May 2020 showed that the prevalence of anxiety was 78.9%, with 21.7% of those surveyed experiencing severe anxiety (Preis et al., 2020) . High risk pregnancy (aOR 1.52, 95% CI 1.06-2.19), abuse history (aOR 1.85, 95% CI 1.24-2.75), and pandemic-related stress surrounding birth preparedness (aOR 1.75, 95% CI 1.35-2.26) and Sars-CoV-2 infection (aOR 1.55, 95% CI 1.28-1.88), were predictive of higher levels of anxiety (Preis et al., 2020) . It remains to be seen whether long-term mental health effects will persist after the Covid-19

pandemic, but these too will likely be influenced by gender.

J o u r n a l P r e -p r o o f Discussion During disease outbreaks, "gender blindness"-the systemic failure to acknowledge gender differences in health-pervades and hinders response efforts (Smith, 2019) . Although actions by government and health organizations toward preparedness planning and relief are ongoing, these efforts exclude investigating and mitigating the unique effects that pandemics impose on women. The only published CDC recommendations on women's health during the pandemic to date are related to obstetric care (CDC, 2020b), failing to acknowledge other gender-specific health effects. Notably, the Coronavirus Aid, Relief, and Economic Security (CARES) Act has no provisions accounting for the differing effects of Covid-19 on various genders (CARES Act, 2020). Omitting gender analysis from public health research, interventions, and policy development fails to acknowledge the gendered impacts of disease outbreaks on healthcare access and utilization, labor practices, healthcare financing, data collection, and program evaluation. Gender blindness leads to health interventions that may be less effective for women at best and directly harmful to their wellbeing at worst-outcomes demonstrated in previous disease outbreaks (Smith, 2019; Davies & Bennett, 2016) .

The response to Covid-19 requires a paradigm shift in healthcare delivery and policy, fostering interventions that account for the differing effects of pandemics on different genders. In the recovery phase after the pandemic, gender should be considered when setting agendas and allocating resources. The healthcare workforce should be adequately trained and staffed to address the increased demand for critical services-including obstetrics, family planning, therapy, and social work-after the pandemic. Healthcare providers, especially primary care providers, should screen for Covid-19-related trauma in addition to depression and anxiety. Providers should be prepared to address the mental health consequences of Covid-19, acknowledging the structural influences that disproportionately impact women. Throughout the outbreak planning and response periods, institutions must engage stakeholders most affected by Covid-19 policies in the decision-making process, centering the concerns of women, especially those from marginalized populations. In these ways, leaders and healthcare providers can respond more effectively to disease outbreaks.

Due to the evolving nature of this pandemic, data regarding gendered health differences during Covid-19 are limited. Much of the literature cited here regarding gender and disease outbreaks come from the SARS, Ebola, and Zika outbreaks. Although these outbreaks affected women in the US, most of the literature is written from a global perspective, which reduces its generalizability to a US context.

While this article addresses topics related to women's health, we acknowledge that manifestations of systemic oppression in society affects all genders. Additionally, the current body of knowledge overwhelmingly focuses on differences among genders that are detrimental to women. There may be aspects of women's experiences during the Covid-19 pandemic and other disease outbreaks that are beneficial to women's health, but our discussion of those topics is limited by the negativity bias of reporting in the literature. Future research may elucidate many of the protective effects that women's gender has on their experiences during this pandemic. Furthermore, we recognize that gender is often framed through a lens of ethnocentrism, classism, and heteronormativity, which limits our description of the literature.

Many gendered health disparities can be attributable to pervasive ideologies and behaviors that manifest in historically-rooted systems regulating the identity and expression of cisgender, transgender, and gender-diverse individuals. As such, any efforts at alleviating these disparities must address underlying social norms and structures, which is beyond the scope of our review.

The Covid-19 pandemic amplifies existing gender health disparities in the US, and its impacts are felt acutely among women most vulnerable to poverty, housing insecurity, IPV, incarceration, racism, and other sources of inequity. The pandemic will have immediate and long-term effects on women's health, highlighting the importance of gender analysis in its planning and response. When preparing for the aftermath of Covid-19, healthcare providers and administrators should take a gender-inclusive approach to developing screening guidelines, instituting treatment plans, and delivering patient care. Particularly during disease outbreaks, when normal processes may be forgone in order to act expeditiously, intersectional gender analyses are integral to addressing issues that arise and mitigating the exacerbation of inequities.

J o u r n a l P r e -p r o o f They or someone in their family will get sick from COVID-19

They will lose income due to workplace closure or reduced hours because of COVID-19

They would put themselves at risk of exposure to COVID-19 because they can't afford to stay home and miss work 

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