Hepatotropic viruses: Is Roma population at risk?

Roma people make up a significant ethnic minority in many European countries, with the vast majority living in Central and Eastern Europe. Roma are a vulnerable population group in social, economic, and political terms. Frequent migrations, life in segregated communities, substandard housing, poverty, and limited access to quality health care, including low immunization coverage, affect their health status and predispose them to various diseases, including viral hepatitis. Hepatitis A, B, and E are highly prevalent among Roma and mainly associated with low socioeconomic status. In contrast, hepatitis C does not seem to be more frequent in the Roma population. Enhanced efforts should be directed towards the implementation of screening programs, preventive measures, and treatment of viral hepatitis in Roma communities throughout Europe. ©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.

Core Tip: Roma people constitute the most important transnational minority in Europe. They are a vulnerable population group in social, economic, and political terms. Low socioeconomic conditions and lack of quality health care predispose them to viral hepatitis, especially hepatitis A, B, and E. In the global attempt to eliminate viral hepatitis, Roma should be considered a high priority group for screening and treatment based on the epidemiological and social context.

INTRODUCTION

Roma people are a distinct ethnic minority dispersed worldwide, with an estimated population of around 12 million. In Europe, they are the largest minority group (5.2 million), with the vast majority living in Central and Eastern Europe (Figure 1)[1-3]. However, the exact number is uncertain due to their nomadic life and historical lack of birth and death records[4]. Roma are a vulnerable population group in social, economic, and political terms. This vulnerability is manifested in widespread poverty, unemployment, illiteracy, lack of formal education, segregation in the educational system, and substandard housing[5,6]. Roma people have worse health status, higher infant mortality rates, shorter (10-15 years) life expectancy, and a higher prevalence of chronic diseases than the non-Roma[2,7,8]. Unhealthy habits, smoking, and lack of physical activity are common in Roma population[9,10]. Moreover, Roma experience difficulties accessing healthcare due to fear, lack of trust, and previous bad experiences with health providers[11]. Poor socioeconomic factors predispose Roma to a number of various infectious diseases, including viral hepatitis[6,12,13]. Moreover, many Roma believe in folk medicine and prefer home-made remedies, resulting in low immunization coverage and outbreaks of infectious diseases[4].

Figure 1

Distribution of Roma population in Europe according to the European Commission: Roma Health Report[NA: No available data.

In the attempt of global elimination of viral hepatitis[14], preventive measures, linkage to care, and treatment process may be challenging in vulnerable populations. In this opinion review, we aim to summarize available data and address practical issues related to viral hepatitis in the European Roma population.

HEPATITIS A

According to the European Centre for Disease Prevention and Control[15], there were 11296 hepatitis A cases in 2019 in the European Union. The incidence of hepatitis A globally decreases, but it is still high in developing countries and among minorities living in low socioeconomic conditions in developed countries[16]. In low-income countries, almost 100% of older children and adults are seropositive[17]. As hepatitis A virus (HAV) is transmitted by person-to-person contact or through contaminated water and food[16], access to clean water and hygiene facilities contributes to the reduction of HAV prevalence[18]. Socioeconomic factors are the most important predictors of HAV infection. Better living standards, including higher incomes and higher education degrees, as well as better housing conditions, significantly decrease the risk of HAV infection[17]. Hepatitis A can be prevented with a vaccine that provides long-term immunity[16].

Roma people are recognized as a high-risk group for HAV infection, in addition to migrants, travelers to endemic countries, and men who have sex with other men[19,20]. In Slovakia and Greece, the countries with a significant number of Roma residents, several hepatitis A outbreaks were reported over the last 15 years[16,19,21]. In the period between 2009 and 2018, 1193 cases of HAV infection were reported in Greece. Roma people accounted for approximately 20% of all infections, with 80.7% of cases affecting Roma children under 15 years old, whereas in the non-Roma population, the percentage of children was significantly lower (5.3%)[19]. Even though the HAV vaccine is mandatory for all children in Greece since 2008, the study from 2013 showed that only 22.6% of Roma children were vaccinated against HAV[22]. In the Roma population, both genders were equally affected, whereas in the non-Roma population, infection predominantly occurred in males. Almost half of HAV clusters (2009-2018) were reported in the Roma population, which accounts for the minority of the Greek population[19]. The study on the HAV outbreak in south-eastern Greece (2007) demonstrated that Roma are susceptible to HAV infection, which appears at an earlier age than in non-Roma[16,20]. In Portugal, an outbreak of HAV was reported in 2005, which involved Roma children[23]. In 2008, there were 9 HAV outbreaks in Slovakia, and four of them took place in the districts predominantly inhabited by the Roma population. The biggest outbreak was registered in Lomnička village (298 cases), where 99% of the residents are Roma. Living conditions in the village, inadequate clean water supplies, and sewage systems predisposed the outbreak[21]. The only data on hepatitis A in Roma from the Czech Republic derives from the European Commission Roma Health Report (2014), stating two epidemics; one in 2009 and the other in 2010 when 30%-50% of Roma from all reported cases developed symptoms[1]. In the Czech Republic, the vaccination against HAV is easily accessible but not obligatory and not free. The HAV vaccination rates among Roma are estimated as low[1]. In the Plovdiv region in Bulgaria, 3911 cases of HAV were documented between 2005 and 2008, most of them associated with Roma. Notification rate in groups of respondents living in worse socioeconomic conditions, mostly Roma, was remarkably higher than in those living in good sanitary conditions[24]. In France, the hepatitis A outbreak involved a total of 492 cases over the 2008-2009 period, including eight clusters of cases among communities living in sites with poor sanitation[1]. A seroepidemiological study conducted in 1995 in San Sebastian, Spain, showed that 82.2% of Roma children were HAV seropositive compared to 9.3% of non-Roma children[25].

HAV infection in Roma differs from the non-Roma population in terms of the lower age of infection and equal distribution among genders[16,19]. The high prevalence is mainly due to poor socioeconomic factors, inadequate sanitary conditions, and sewage systems, contributing to easier transmission of the disease. Additionally, the vaccination coverage in Roma children is low[22,26,27]. In the attempt to lower the HAV incidence, better vaccination coverage and improvement of living conditions in Roma communities should be continuously and decisively implemented.

HEPATITIS B

Hepatitis B virus (HBV) infection has a chronic course and leads to fibrosis, cirrhosis, and hepatocellular carcinoma. The pattern of HBV transmission is vertical and horizontal by infected blood or sexual contact[28]. The HBV vaccine prevents HBV infection and has significantly decreased HBV-related mortality[29]. As HBV infection is associated with poor socioeconomic conditions[28,30], Roma living in communities with poor hygiene are predisposed to have a higher incidence of HBV infection[31,32].

Several studies addressed the prevalence of HBV in Slovakia, where the Roma minority is very numerous. It is estimated that approximately 400000 Roma people live in Slovakia, which accounts for 7.5% of the Slovak population[8]. Their socioeconomic (lower education, unemployment, social benefits) and living conditions (lack of standard household facilities such as sewage system, water supply, flush toilet, bathroom or shower, electricity) are significantly worse compared with the majority[14]. In 2008-2009, a study was conducted in 9 districts of Eastern Slovakia, comparing districts with higher (> 5%) and lower (< 5%) Roma population. There was no significant difference in the overall prevalence of HBsAg (1.95% vs 1.62%). However, pregnant women showed a higher prevalence of HBV infection in districts with a higher Roma population (2.72% vs 0.98%)[33]. In addition, a cross-sectional epidemiological study on hepatitis B was conducted in 2011 among randomly sampled Roma and non-Roma populations. Roma population had a significantly higher prevalence of HBsAg (12.4% vs 2.8%) and anti-HBc (52.8% vs 15.9%) than the non-Roma population. Furthermore, HBsAg positive Roma population was more commonly HBV DNA positive compared to HBsAg positive non-Roma population (94.3% vs 70.0%). Tattooing, economic factors (unemployment, elementary education, poverty), and male sex were found to be risk factors for HBV positivity[34]. Furthermore, targeted testing in primary care demonstrated a high prevalence of HBV infection within the Slovak-Roma population in Sheffield, United Kingdom. The HBsAg positivity was found to be 9.4%, while 28% had evidence of cleared past HBV infection (anti-HBc positive)[35].

One Greek study (2002) analyzed the prevalence and risk factors of hepatitis B in Roma and non-Roma children who lived in a deprived suburb of Athens. Among Roma children, 22.0% were identified with evidence of past HBV infection (anti-HBc positive), of whom 4.2% were chronic carriers (HBsAg positive), whereas no past infection was detected among the non-Roma. The evidence of HBV vaccination (anti-HBs positive) was detected in only 13.6% Roma, but in 95.9% non-Roma children. Among possible risk factors, unfavorable living conditions, frequent residency change, lack of child insurance and primary healthcare delivery were significantly associated with HBV seroprevalence among Roma[36]. Although overall vaccination coverage in Roma children is low[22], it varies in different European countries. For instance, in Slovakia, 59.2% of Roma children are vaccinated against HBV[23]. In the Doctors of the World report (2011) the HBV vaccination coverage in Roma children under two years of age was 43.5%[37]. On the other hand, in the Czech Republic, 95% of Roma children are vaccinated for obligatory diseases, including HBV[1].

Tattooing, blood transfusions, drug use, and imprisonment carry a high risk for HBV and are more common in Roma people[38]. However, it is considered that sexual intercourse is more significant for horizontal transmission of HBV among Roma, since a minority of them use preventive methods against sexually transmitted diseases[34,38]. Vaccination against HBV is less common in Roma; it is not completed because of lack of compliance[38]. Lastly, the efficacy of HBV treatment in Roma is concerning, mainly due to non-compliance and poor availability of healthcare[34].

HEPATITIS C

Hepatitis C virus (HCV) is a widespread cause of acute and chronic hepatitis and a significant risk factor for liver cirrhosis and hepatocellular carcinoma. Around 71 million people worldwide are suffering from chronic hepatitis C infection[39]. It is a blood-borne virus, most commonly transmitted by contaminated needles (intravenous drug users), through blood transfusions or sexual intercourse[40,41]. Vertical transmission is also possible[39].

Some of the risky behaviors appear to be common among Roma. For instance, studies reported an increase in Roma women participating in sex work and a higher prevalence of injection drug use among Roma[3,42,43].

In 2010, a seroprevalence study on HCV was conducted among Roma youth aged 15–24 years in two cities in Serbia-Belgrade (the nation's capital and largest city with 1.2% of residents estimated to be Roma) and Kragujevac (the fourth largest city in Serbia with up to 14% Roma by estimates). Although some of the risk factors were highly prevalent (intravenous drug use, 0.5%-3%; experience with sex workers, 5%-10%; tattooing in non-sterile conditions, 2%-14%; the use of a condom with a constant partner, 1%-25%), only four of 240 (1.7%) participants tested positive for HCV antibodies. Two reported intravenous drug use and three reported having a tattoo[44].

Similar results were found in Slovakia among 441 Roma with HCV seropositivity of 0.7% (1.5% in the general population). Predisposing factors for HCV were tattooing, blood transfusions, and having more sexual partners[32]. In a study conducted among students of two elementary schools in Greece (2002), none of the 118 Roma children involved were positive for HCV antibodies[36]. According to these studies, HCV infection is not as frequent as other hepatitis viruses among Roma.

HEPATITIS E

Hepatitis E virus (HEV) is an emerging viral disease, with 20 million infection cases and 55000 deaths worldwide. Its prevalence is higher in developing countries; however, lately, it has been recognized as a significant cause of hepatitis in resource-rich countries[45]. HEV can be transmitted through contaminated water; however, food-borne, blood transfusion-related transmission by gained significant attention in recent decades[45,46].

The data about HEV among Roma in Europe are scarce and conducted only in Slovakia. The Roma population's HEV prevalence ranged from 21.5% to 45.5%, and the only significant risk factor appeared to be the consumption of raw meat[47,48].

CONCLUSION

In 2016, the World Health Organization adopted the first Global Health Sector Strategy on Viral Hepatitis, calling for its elimination as a public health threat. The strategy presented a target for 2030–of reducing new hepatitis B and C infections by 90% and mortality by 65%[14]. Roma constitute the most important transnational minority in Europe and a highly vulnerable population affected by viral hepatitis. Based on their epidemiological and social context, living conditions, lack of access to clean water, safe food, and medical services to maintain effective infection control measures, Roma should be considered a high priority group in managing viral hepatitis.

Screening is of particular importance as data on viral hepatitis prevalence in European Roma are scarce and limited to specific regions (Table 1). In Roma, hepatitis B prevalence is high, and mother-to-child transmission is likely a major mode of transmission and early childhood infection based on low vaccination. In addition, the fecal-oral and/or food-borne hepatitis (HAV and HEV) are more common in Roma than in the non-Roma population. In contrast, HCV infection does not seem to be more frequent in Roma.

Table 1

The epidemiology of hepatitis A, B, C and E among Roma population in Europe

Region	Year	Population, N	(Sero) Prevalence	Acute cases/outbreaks	Ref.
Northeastern Greece	2007	124 inhabitants of Xanthi, Rodopi and Evros, mostly Roma		54% males, 46% females, age 2–17 yr	Vantarakis et al[16], 2010
Greece	2004–2013	295 Roma/995 confirmed cases		Median age 5.9 yr; 2007 outbreak: 139 cases, 82% Roma	Mellou et al[20], 2015
Greece	2009-2018	240 Roma/1193 confirmed cases		51.2% males, 80.4% < 15 years old, median age 7 yr; 20 clusters recorded among Roma; 2013: Greatest outbreak, 112 cases among Roma	Mellou et al[19], 2020
Athens, Greece	1999-2013	467 children hospitalized with hepatitis A, age 0-14 yr		HAV hospitalization rates per 1000 admissions, among Roma: 233.1 (1999-2008), 54.3 (2009-2013)	Papaevangelou et al[27], 2016
Western Athens, Greece	2002	216 children from two elementary schools, 118 Roma	Anti-HAV IgG: Roma children 98%, non-Roma children 33%		Michos et al[36], 2008
Slovakia	2008	667 cases reported to Epidemiological Information System database		536 cases in “low hygienic standards” areas; considered Roma; 4/9 outbreaks in areas with mostly Roma population; Lomnička outbreak (99% Roma population): 298 cases, 297 < 18 years old	Hrivniaková et al[21], 2009
South Bulgaria	2005-2008	3911 patients with hepatitis A treated in Clinics of Infectious Diseases, Plovdiv		Incidence rate in group living in poor hygienic conditions (mostly Roma): 450.66/100000; Outbreak in Stolipinovo quarter (2006); 1004 cases, mostly Roma	Stoycheva et al[24], 2011
San Sebastian, Spain	1995	73 Roma, age 2-16 yr	Total anti-HAV 82.2 %, total anti-HAV 50% in children 2-5 yr, total anti-HAV 92.7% in children > 5 yr		Cilla et al[25], 1995
Eastern Slovakia (9 regions)	2008-2009	59279 serum samples (13798were part of the pregnancy screening)	HBsAg overall 2.18%-9.07%; pregnant women 0.82%-4.13%		Kristian et al[33], 2013
Eastern Slovakia	2011	452 Roma, adult population	HBsAg 12.4%; anti-HBc 52.8%; HBV DNA 94.3%		Drazilova et al[34], 2018
Sheffield, United Kingdom	2007-2013	436 Slovak-Roma adult population	HBsAg 9.4%; anti-HBc 28%		Gregory et al[35], 2014
Western Athens, Greece	2002	118 Roma children	HBsAg 4.2%; anti-HBs 13.6%; anti-HBc 22.0%		Michos et al[36], 2008
Serbia (Belgrade and Kragujevac)	2010	240 Roma, age 20-24 yr	Anti-HCV 1.7%		Djonic et al[44], 2013
Eastern Slovakia, Košice region	2011	441 Roma, age 18-55 yr	Anti-HCV 0.7%		Veselíny et al[32], 2014
Western Athens, Greece	2002	216 children from two elementary schools, age 5-15 yr, 118 Roma	Anti-HCV 0%		Michos et al[36], 2008
Eastern Slovakia	2011	195 Roma living in Roma settlements, age 18-55 yr	Total anti-HEV 21.5%, highest in Roma men–29.4%		Halánová et al[47], 2018
Košice, eastern Slovakia	2018	175 patients hospitalized in Department of Infectology and Travel Medicine, age 19-94 yr, 11 Roma	Total anti-HEV 45.5%		Paraličová et al[48], 2020

HAV: Hepatitis A virus; HBV: Hepatitis B virus; HCV: Hepatitis C virus; HEV: Hepatitis E virus.

The challenges in the Roma population are high. However, in the attempt to improve Roma's health and reduce health inequalities, viral hepatitis screening programs, facilitated linkage to care with access to affordable antivirals and vaccines should be continuously implemented through Roma communities. Effectively combating viral hepatitis may also reduce maternal and child mortality, as the mortality from non-communicable diseases. This strategy and its far-fetched implications may alleviate poverty and facilitate further development in terms of managing sanitation and water, reducing inequality in access to services, and promoting non-discrimination.

All European countries approved the WHO strategy, and now we have just one decade left to reach the goals and fulfill these promises.