Introduction
Early in 2020, the first reports coming from China and Italy indicated the population group with the highest mortality risk due to the virus were men with comorbidities, which was confirmed globally as the pandemic spread [1, 2]. Numerous studies have shown that the impact of the COVID-19 pandemic is gendered: conferring differential risks attributable to both biological differences (sex), but also marked by social dynamics and socially constructed norms (gender) [3]. Given the differences in mortality, much research and academic commentary has focused on explaining the increased mortality in men compared to women [4]. Such approaches, however, have failed to address how sex and gender differences affect COVID-19 incidence [5, 6].
Since early in the pandemic, few countries have routinely reported sex-disaggregated data on cases and deaths of COVID-19 [7]. The countries reporting cases and deaths disaggregated by sex show mostly higher death rates in men and similar incidence for men and women [5]. Unfortunately, incidence data describing the differential progress of the disease by gender is not routinely collected [8]. Gender has been described as a multidimensional variable that describes identity, norms and relations between individuals and that can influence access to health services, social support, as well as behaviour towards the prevention of the virus [9, 10].
A pre-print published in May 2020 examined the apparent equality between men and women in COVID-19 infection rates adding an age-disaggregated analysis in ten European countries [11]. The study used routine epidemiological data and reported a higher rate of infections among women compared to men of working-age (20–59 years old). The difference became non-significant in the population above 60 years of age. This finding illustrates the potential role that social norms could have in the spread of COVID-19.
As the pandemic was unfolding, countries worldwide tried to control its peak with strict public health policies that included lockdowns and other restrictions, which started in March 2020 [12]. Unfortunately, some of these policies reinforced pre-existing inequalities, including gender inequalities [9, 13].
Despite the growing body of evidence showing differences by gender and other social determinants in COVID-19, very few studies have examined how different phases of the pandemic have impacted men and women differentially with a specific focus on COVID-19 incidence and its policy drivers. We explore whether the overall case burden, even in age groups for whom COVID-19 is not usually fatal, shows a similar pattern between men and women and how COVID-19 prevention policies may have affected it.
For this study, we chose to focus on two European countries: Switzerland and Spain, which were among the European countries with the highest numbers of cases and deaths per capita in the first year of the pandemic [14, 15]. Additionally, the countries’ policies represent different stringency to COVID-19 containment approaches, with Spain going into full “lockdown” (as in people were not allowed to leave their homes freely) for a considerable time, while Switzerland never went into full lockdown.
Methods
We conducted a retrospective longitudinal study using quantitative COVID-19 case and testing data and qualitative data on the containment measures and policies between February 2020 and June 2021 in two European countries, Switzerland and Spain.
Study Setting
Switzerland is a small federal state in central Europe bordering France, Germany, Austria, the Principality of Liechtenstein and Italy. It is divided into 26 cantons (administrative entities). The Swiss health system is based on universally mandated private health insurance [16].
Spain, bordering Portugal and France and the microstate of Andorra, consists of 17 autonomous communities, including two island territories. It has a public, universally accessible National Health System complemented by voluntary private insurance policies.
Healthcare is more privatised in Switzerland than in Spain, where it is more socialised. Both countries have universal access to healthcare and a decentralised public health system. However, both had mechanisms to centralise decision making in times of an emergency like COVID-19. The per capita spending on health care in 2018 was 9,870 USD in Switzerland, the second highest in the world, while in Spain it was 2,736 USD [17].
Both countries ranked similarly in the latest Gender Gap Index: 10th (Switzerland) and 14th (Spain) place out of 156 [18]. However, despite this high ranking, there are prevailing differences in everyday lives for women and men in these countries. In recent years, men and women have achieved a more balanced participation in the labour market, however, in both countries, most domestic tasks and care work are still predominantly carried out by women in the family context [19, 20]. Even during the lockdown, many women had to consider quitting their jobs to be able to take care of their children, since schools were closed [21].
In both countries, women tend to have jobs that include physical interactions with people (teaching, childcare, health workers, supermarket employees, etc.), many of which were considered “essential”, even when most workers were recommended to stay home [20, 22].
Data Collection and Analysis
To understand how COVID-19 incidence among men and women changed over time, we used publicly available case data stratified by sex and age. Data was collected from the Swiss Federal Office of Public Health (FOPH), as well as the Spanish Red Nacional de Vigilancia Epidemiológica (RENAVE). COVID-19 cases were mandatory to be notified to the FOPH since before the first case in Switzerland. The case definitions were adapted through time, based on the diagnostic possibilities (changing from PCR-confirmed to rapid test confirmations). Likewise, the definition of a case was updated in Spain according to the technical reports for the COVID-19 case management [23].
We explored the incidence between men and women from the outbreak of the pandemic (February 2020) until June 2021. We calculated the IRR of cases between women and men, stratified by age groups - for each week of the pandemic:
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For convenience, excess cases per population are shown in two ways: 1) as IRR, 2) as a percentage deviation from equality between both sexes (IRR = 1):
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To test for disparities, we used an exact test assuming that incidence is Poisson-distributed. “Waves” in the COVID-19 pandemic were defined as any time that the test positivity rate exceeded 5%, as defined by the World Health Organization (WHO) [24].
We collected information from policies (such as Royal Decree in Spain, or the COVID-19 Ordinance in Switzerland) published by the governments for the regulation of tele-working, school closures, which had been previously hypothesised as the biggest drivers behind gender differences, as well as testing strategies that were regularly updated by the Ministry of Health (MoH) in Spain and the FOPH in Switzerland to complement the case data [25, 26]. Two of the authors (FBF and LM) searched publicly available reports such as official government documents/websites or press releases and press conferences of national-level policies and their implementation at the second administrative level (cantons in Switzerland, autonomous communities in Spain) to create a harmonised timeline of policies in each country. This was an extension of the Health Observatory detailed in a previous manuscript [27]. These data were then visualised to show the duration of policies (for home office recommendations and school closures) and the changes in testing policies.
To account for differences in testing behaviour between men and women, supplemental analyses in Switzerland on testing rates by gender were included and the positivity rate was calculated, stratified by gender. In Spain, testing data stratified by gender was not available.
A simple simulation was performed to calculate the theoretical 95% confidence interval of the positivity rate for women had both genders had the same underlying incidence but women were testing at higher rates. This was done by taking 1,000 Monte Carlo samples from a gamma distribution with shape parameter equal to the cases among men and rate parameter equal to the population of men. Then we sampled from a Poisson distribution with rate parameter equal to the gamma distribution draw times the number of women in the population, and we calculated the simulated positivity-rate by the number of tests done on women in the population.
Discussion
Gender differences in relation to COVID-19 incidence rates have been previously discussed, given the higher risk of mortality and hospitalisation in men [35]. However, less attention has been given to the sex-differential impact of public health response on COVID-19 case incidence rates. The COVID-19 burden goes beyond mortality and short-term illness [36]. Women have been shown to be four times as likely than men to suffer from at least one persisting symptom after a COVID-19 infection for an extended period [37].
Global data suggested a similar case burden in women and men during the first year of the pandemic [38]. Our study shows, however, that in Spain and in Switzerland, during the waves in 2020 and the first half of 2021, more women were diagnosed with COVID-19 than men. Testing data from Switzerland suggests that this phenomenon is not due to differential test-seeking behaviour between the genders, but rather different incidence (Figure 2), as the positivity rate was similar in both groups. Yet, higher infection rates in women are only present for the populations of working age (20–59 years old) and above 80 years old (Supplementary Figure S2). In a previous study, Sobotka et al. also found a higher rate of cases in women compared to men, for the working age group [11].
The difference in the stringency of the containment measures between the waves studied seemed to be associated with a different degree of disparity, which could be read similar to a “dose response” relationship. The more stringent the measures, the larger the gender disparity, which could explain the differences seen between Switzerland and Spain; in Switzerland, where the measures were less stringent, the gender disparity in cases was lower than in Spain.
The WHO’s sex and gender in infectious diseases framework [39] describes the interaction of sex and gender with infectious diseases at three different levels: 1) vulnerability to the disease, 2) ability to prevent exposure and 3) decision-making power.
It has been hypothesised before that women are more exposed than men to COVID-19, be it in the domestic or professional setting [40]. Paradoxically, women also self-reported higher compliance with containment measures (namely social distancing and hygiene) [41]. Therefore, even though women aim to act responsibly, they are limited in their ability to prevent exposure. They are subject to more frequent or more precarious exposures than men, which would explain what we observed in Switzerland and in Spain. We discuss below the potential causal pathways between the implementation of COVID-19 prevention policies and the differential protective effect in men and women.
Women Were More Exposed to COVID-19 at Work
In Switzerland, when home office policies were established (recommended from 13 March–6 June, 2020, 19 October–4 December 2020, and starting on 26 June 2021; but moderately or strongly advised from 4 December 2020–26 June 2021) the excess of cases among women increased significantly. However, when we looked at the degree of stringency and the degree of excess cases among women, it suggests that it is the school closure during the first wave that is associated with the excess among women, whereas in the more severe second wave, schools remained open for younger children, and the excess among women was milder (Figure 1). A similar situation was observed in Spain, where an excess of cases was observed among the women of working age, and more marked among women of typically child-bearing age during the closure of schools and day care centres (Figure 3).
During the first wave the stringency of policies differed in Switzerland and Spain: while in Switzerland a “soft-lockdown” was applied, citizens in Spain were forced to stay at home. Face-to-face education at schools and universities were suspended in both countries. Exceptions to the norms of staying and working from home were issued in Switzerland as well as in Spain for workers in sectors considered “essential”. Essential services included those ensuring supply of food and hygiene products, medicines, health care, transport or security [27, 42]. Workers in these sectors are predominantly women in both countries [22, 42, 43]. For context, in Switzerland 68% of the health workforce, 92% of childcare and 67% of retail positions are staffed by women [22]. Similarly, in Spain, more than 70% of the health professionals are women and they are also overrepresented in sectors like social work, retail, health and cleaning services [42]. Studies have shown that workers in some industries, such as meat factories, were predominantly male and at higher risk of contracting COVID-19 due to superspreading events [44]. However, in the case of Spain and Switzerland, these occupations account for a smaller volume of workers than the health, educational and care sectors, where women are overrepresented.
There is little to no evidence in both countries on case burden by sex and occupation. However, several studies have shown a higher case burden among the health workforce. Furthermore, Perez-Romero et al. found that most health and social care professionals in several high incidence areas in Spain were infected in their workplaces, while the general population were infected mostly at home [45]. One study in Switzerland found increased seroprevalence in hospitals treating COVID-19 patients compared to hospitals without COVID-19 patients, but overall only a small difference between healthcare workers and the general population was observed [46].
Care-Giving in Switzerland and Spain
Evidence suggests that women were not only more exposed at work, they were also more exposed to the virus at home compared to men. In Switzerland, women take on more of the unpaid care work than men (31.2% of women reported to take care of either children, adults or both compared to 11.6% of men) [47]. In both countries, if a family member gets ill, it has been shown that the closest care (with the highest infection risks) falls to the women of the household [48]. Additionally, most (known) transmissions in Switzerland happened within households [46].
The closure of schools and nursery homes implied that two out of three mothers had to stay at home in Spain, shouldering the highest burden of domestic and care work [21]. Moreover, the additional burden on women due to caregiving activities did not only increase their risk to contract the virus, but it also led to additional secondary effects, such as loss of jobs.
Over-Representation of Women in Nursing Homes
Finally, our results also show that women above 80 years old were at higher risk of contracting the disease than men in the same age group. The difference was, however, more prominent in Spain (Supplementary Figures S2 vs. S6), where the difference was maintained throughout the pandemic, reaching 102% of infections in April 2020. The Spanish MoH estimates that almost 20 thousand people died between January and June 2020 in nursing homes nationwide due to COVID-19, where most of the residents are women [21]. Several studies and media reports addressed the problem of nursing homes during the COVID-19 pandemic, as elderly people were abandoned by the State, leaving especially old women in a vulnerable situation [49].
Switzerland could have faced similar challenges, as there was an excess of COVID-19 cases in women above 80 years old during the second wave of the pandemic (November 2020–January 2021). According to the Swiss Federal Statistical Office, in 2020, 1.8% of the Swiss population lived in care homes (either short-term or long-term), and among those living in care homes 67% are women [50]. In a recently published report, an increase of 80% of deaths in care homes was reported during autumn of 2020 [51]. The press release does not differentiate, however, between deaths of men and women. Our study findings, which show an excess of cases in women over age 80 in the second wave (Supplementary Figure S2), highlight the importance of understanding if this increase of deaths was attributable to transmission within care homes.
We hypothesize that the reason for the overrepresentation of women in old-age nursing homes is partly an overall decline in the proportion of men with increasing age, but also that women of that age have often lost their partners, while men could potentially benefit from at-home care from their wives or partners [21, 52]. This circumstance could be attributed to the fact that men tend to have younger partners and a lower life expectancy.
The COVID-19 crisis has affected everyone, but in different ways. Social determinants and inequalities have been described as key factors behind the drivers of this pandemic. Social determinants have influenced the risk of contracting the disease, the outcomes of it, as well as the unintended effects of the containment measures [52]. Our findings for two exemplary countries, Spain and Switzerland, suggest that the differences in the sex-ratio of cases are not only due to biological differences, but rather to social and gender norms and how policies affected population groups differently. These associations were seen despite both of our selected countries ranking high in the Global Gender Gap report; it is likely that our findings are transferable to many other countries.
Limitations
Our results are probably showing an underrepresentation of disparities, given changing testing policies. Until May 2020, the testing strategy only covered inpatients and severe cases, which were borne in a slightly higher proportion by elderly men. Furthermore, data on testing disaggregated by both age and sex were not available for either country.
Conclusion
Our study shows that while the mortality of COVID-19 is disadvantageous to men, the incidence of COVID-19 disproportionately burdens women, in particular women of child-bearing and working age (20–59 years old). This has long-term implications due to fourfold higher odds of developing “long COVID” borne by women.
Evidence is emerging about the protective benefits and effectiveness of certain policies and non-pharmaceutical interventions to reduce COVID-19 incidence. These studies are, however, often looking at overall numbers and may overlook how policies may reduce the risk differently among population groups, including those defined by gender. When different effects are observed this is often attributed to the levels of compliance, rather than structural exposures or risks that are unaddressed by the policies. We argue that there is a need to search for drivers beyond compliance and understand how policies enable certain groups to shield from the pandemic more than others.
Policy and decision-makers have embedded gender in their discourse, but this has often been limited to rhetoric or implementing policies to alleviate socioeconomic effects of the pandemic. Our study highlights that a gender perspective is also crucial to implement incidence-prevention measures, like non-pharmaceutical interventions.