Viruses | Free Full-Text | Trends of Hepatitis A Virus Infection in Poland: Assessing the Potential Impact of the COVID-19 Pandemic and War in Ukraine

Hepatitis A is caused by a nonenveloped, positive-sense, single-stranded RNA virus (HAV) with a 7.5 kb genome, represented by one serotype and seven genotypes [1]. It is globally prevalent and remains the most common form of acute viral hepatitis worldwide [2]. Humans, its only natural host (though some nonhuman primates have been experimentally infected), are infected predominantly through the oral-fecal route due to the consumption of contaminated food and water, but can also acquire infection through close physical contact with an infected individual, mainly during sexual and anal intercourse [3]. A blood-borne route of transmission, e.g., through intravenous drug use, is possible, although rarely [4]. According to data provided by the World Health Organization (WHO), up to 1.5 million HAV infections are reported annually; this figure refers only to symptomatic cases, thus not fully reflecting the scale of the phenomenon [2,5]. It is estimated that their actual number may be several-fold higher, with some assessments indicating that over 150 million infections can occur annually. Such a high number is plausible because the clinical course of infection is mostly asymptomatic in highly endemic countries where HAV is acquired in childhood [6,7].

The high prevalence of HAV infections is closely related to poor sanitary and hygienic conditions and lack of access to safe and good-quality drinking water, meaning that highly endemic regions include developing countries, while in developed areas, the infection rates are low [8]. However, in recent years, an unfavorable trend has been outlined, with hepatitis A continuing to occur in hyperendemic regions and emerging in areas of low endemicity [7]. Not only are improvements in socioeconomic, sanitary, and hygienic conditions contributing to changes in HAV epidemiology, but it is also influenced by increased economic interdependence and social integration, along with changing human behavior and interactions, including those in the sexual sphere, the globalization of trade, the increasing pace of international travel, and migration movements [9]. Many adults in low-prevalence countries are susceptible to HAV infection, which, in the face of increasing social integration, intensified travel, and trade that crosses national borders, poses a high risk of compensatory outbreaks. At particular risk of HAV infection are people traveling to highly endemic areas, child care workers, men who have sex with men (MSM), users of illegal drugs, persons living in isolated communities including jails, those experiencing homelessness, migrants and refugees, and people with occupational exposure, such as healthcare workers and persons working with food and municipal waste [8,10]. Groups with a high risk of severe consequences due to hepatitis A include people living with HIV/AIDS and patients with chronic hepatitis [10].

Prevention efforts in the form of vaccinations, which have been available since the early 1990s, should focus on those populations at high risk of HAV infection in low-endemic areas [5,11]. Although acute symptomatic hepatitis A is generally a mild self-limiting disease with a low risk of fulminant hepatitis and death, patients with chronic liver disease are at risk of a more severe course and should also be vaccinated [12]. However, it should be noted that HAV vaccination in many low-endemic countries is not mandatory but is only recommended, so despite the availability of this form of prophylaxis, its impact in practice depends on the implementation of guidelines [4,13].

Over the past few decades, the most significant impact on the epidemiology of HAV infections in Poland has been due to improvements in socioeconomic and sanitary-hygienic conditions, which led to a transition from the high endemicity category in the 1970s and 1980s to low endemicity in the early 2000s [14]. However, there is a lack of studies summarizing trends in HAV epidemiology that have taken place in Poland in recent years in the face of the globalization phenomena, the COVID-19 pandemic, and the inflow of war refugees from Ukraine [15]. Therefore, there is a pivotal need to fill this knowledge gap in order to assess the effectiveness of prevention measures. To this end, the present study aimed to track HAV epidemiological trends in Poland from 2009 to 2022, taking into account place of residence, age, and gender, along with the identification and characterization of epidemic outbreaks and an assessment of the potential impact of the COVID-19 pandemic and migratory movements related to the war in Ukraine, which began in February 2022.

The present study provides novel insights into the epidemiological situation of HAV infections in Poland, which are pivotal for shaping the policy on prevention measures and targeting specific groups. HAV vaccines, which are highly immunogenic and are effective in preventing infection when given as a two-dose series to children and adults [26,27], have been available in Poland since 1995 but are currently completely voluntary, resulting in low vaccine coverage (0.80 per 1000 inhabitants in 2020–2022 [16]), even among high-risk groups, e.g., MSM [28]. This is because Poland is currently considered a region of low endemicity [14]. However, the present study shows that temporary spikes in newly diagnosed HAV cases can occur, as evidenced especially for the 2014–2017 period, while the epidemiological situation may be significantly affected in both a downward and upward manner by novel circumstances, such as a pandemic of respiratory disease and war in a neighboring country. These findings highlight the need for the continuous monitoring of HAV in Poland and for potentially targeting specific groups with vaccination.

As shown, HAV infections were more common in men. This observation is in line with observations made previously in Poland [29], although there are reports of a slightly higher prevalence of hepatitis E in women in some countries [30]. Contrary to infections with the hepatitis E virus, which are often clinically indistinguishable from HAV infections, the latter are not more likely to present clinically in men compared to women [31], implying that other factors responsible for higher morbidity within males. Firstly, hepatitis A disproportionately affects MSM due to increased transmission risk, particularly during oro-anal and genito-oral sexual intercourse, as also shown when analyzing the multi-country outbreak that occurred in countries in the European Economic Area in 2016/2017 [32]. Secondly, independently from sexual behavior, the higher frequency in men may also result from worse hygiene habits in men, e.g., several studies have documented that men wash their hands less often than women, as also seen during the period of the COVID-19 pandemic, when frequent handwashing was particularly recommended by the health authorities [33,34,35]. In turn, handwashing, including only with tap water, is known to reduce HAV particles significantly and is considered one of the best prevention measures against direct and indirect spread [36].

The present study found that a spike in HAV infections occurred, regardless of sex, in individuals aged 15–44, especially in the 25–34-year-old group. This observation is likely a result of age-related increased sexual activities, including the exploration of sexual novelty [37]. Notably, there was no increase in HAV infections among children in 2018–2022, though their incidence was higher than in 2009–2013. HAV infections in children are concerning, due to the potential long-term health effects [38]. Despite low vaccination coverage in Poland, HAV circulation in this group remains low and is not expected to increase since socioeconomic and sanitary conditions are improving.

Our study also reports that HAV infections were consistently more common in individuals, both women and men, who inhabit urban areas. This is an interesting finding, especially if one considers that some epidemiological studies conducted in other world regions point to the contrary, implying that the urbanization process is generally associated with a reduction in hepatitis A morbidity due to comprehensive improvement in sanitary facilities related to water supply, excrement disposal, and environmental hygiene compared to rural areas [39]. Conversely, a study in Korea evidenced a higher prevalence of HAV infections in urban areas with a high population density [40], which is in line with our observations. This heterogeneity in the relationship between urbanization and hepatitis A epidemiology is likely due to different factors playing leading roles in HAV spread in a particular population. In developing countries, urbanization may curb the incidence of HAV due to improved access to clean water. In turn, in high-income areas, where discrepancies in this access are not so profound between urban and rural areas, the spread in adults may be driven by imported food and particular sexual behaviors, especially those typical of MSM, who tend to reside in or move to urban areas [9,41]. It is also plausible that individuals inhabiting urban areas in Poland have better access to healthcare services, including diagnostics, and may be more frequently tested for HAV infections, resulting in their higher identification. Therefore, the possibility cannot be excluded that the HAV prevalence reported in the present study for rural areas may be underestimated due to differences in access to medical care.

It is known that the COVID-19 pandemic has affected the epidemiology of various viral infections through two main pathways: (i) limited access to diagnostics as a result of the reorganization of the healthcare system and imposed lockdown measures, and (ii) attenuated transmissibility due to sanitary measures and social distancing [42,43]. We found that during the early phase of the pandemic and during the dominance of the Delta SARS-CoV-2 variant, the rate of newly diagnosed HAV infections was lower than in preceding years. In the pre-pandemic period, an increasing trend in hepatitis A notifications was generally noted in Europe, with clustered outbreaks in MSM noted in 2017 [44,45]. However, HAV infections in Poland were more frequent than in earlier periods between March 2013 and February 2017. This is an interesting finding since, according to the European Centre for Disease Prevention and Control, the hepatitis A notification rate during the pandemic, especially in 2021, was exceptionally low in the European Economy Area, a phenomenon attributed not only to the lockdowns, restrictions, and reduced international travel but also to practicing good hygiene and improved vaccine uptake among at-risk groups [46]. However, some regions reported an increased hepatitis A occurrence during the COVID-19 pandemic, e.g., in Bulgaria, when the prevalence of HAV infections among patients hospitalized with viral hepatitis was approximately two-fold higher between May 2020 and April 2021 than in the two preceding years [47]. There are also some reports indicating that increasing HAV susceptibility is correlated with increased COVID-19 severity [48]. Therefore, it is plausible that a relatively stable prevalence of HAV infections during the COVID-19 pandemic in Poland, also encompassing periods of strict sanitary restrictions, is, at least to some extent, a by-product of increased SARS-CoV-2 surveillance in patients revealing various symptoms, including liver-related symptoms.

Notably, the rate of HAV infection increased during the period dominated by the Omicron SARS-CoV-2 lineage, compared to the preceding pandemic waves. This phenomenon can be explained two-fold. Firstly, in February 2022, a war in neighboring Ukraine began, leading to the largest number of displaced people since the Second World War and massive refugee inflow [49]. Within only the first month of the war, 1.8 million people crossed the Polish–Ukrainian border, while, a year later, 1.4 million Ukrainian citizens had a valid residence permit in Poland, predominantly women and children [50]. Before the war, Ukraine was a low-endemicity zone in urban areas and an intermediate-endemicity zone in rural regions [10,51]. However, the movement of refugees in response to war, coupled with the high number of susceptible individuals among children and adolescents in Ukraine, due to low vaccination rates and deteriorated sanitary conditions while in transit, posed a risk of HAV spread [52]. In addition, in Western Ukraine, the incidence of hepatitis A was reported to exceed the country’s average level, a phenomenon attributed to technological challenges in water supply, sewage networks, and wastewater treatment [53]. Our data indicates that the inflow of refugees likely contributed to newly diagnosed HAV infections in Poland since the rate of HAV infections systematically increased from February to August 2022—by 440%. One should also note that the Ministry of Health of Ukraine does not list HAV vaccinations among the recommended vaccinations [54], and interest in receiving such a vaccine is also very low among war refugees—between 24 February 2022 and 30 January 2024, HAV vaccination was received by only 123 individuals of over 2 million Ukrainian citizens who had a valid residence permit (resulting in a rate of 0.06 per 1000, which is 13-fold lower than the average vaccination rate among the inhabitants of Poland in 2022 [55]).

However, one should note that according to the Regulation of the Council of Ministers of 25 March 2022 on establishing specific restrictions, orders, and prohibitions in relation to the state of the epidemic from 28 March 2022 onward, all restrictions related to the COVID-19 pandemic were lifted in Poland [56]. This decision was made despite the fact that it took another 13 months for the WHO to announce that COVID-19 has the status of a Public Health Emergency of International Concern [57]. Therefore, it is likely that a notable spike in HAV infections was a joint result of lifted restrictions and the associated changes to social behaviors and access to healthcare services (including diagnostics), as well as an inflow of imported cases from Ukraine.

We wish to stress the limitations of this study. It did not include information on sexual orientation or nationality, due to the lack of data. Therefore, the discussed associations of hepatitis A occurrence in MSM and in Ukrainian war refugees must be treated with caution but also considered a motivation for further epidemiological studies focusing on HAV in Poland. This is especially important if one considers that the war-related crisis in Ukraine has led to internal HAV outbreaks in 2023 [58,59].