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Lianne Mccance
In 2016, the World Health Organisation set a goal to eliminate viral hepatitis by 2030. Robust epidemiological information underpins all efforts to achieve elimination and this systematic review provides estimates of HBsAg and anti-HCV prevalence in the European Union/European Economic Area (EU/EEA) among three at-risk populations: people in prison, men who have sex with men (MSM), and people who inject drugs (PWID).
Our results suggest prioritisation of PWID and the prison population as the key populations for HBV/HCV screening and treatment given their dynamic interaction and high prevalence. The findings of this study do not seem to strongly support the continued classification of MSM as a high risk group for chronic hepatitis B infection. However, we still consider MSM a key population for targeted action given the emerging evidence of viral hepatitis transmission within this risk group together with the complex interaction of HBV/HCV and HIV.
Chronic infection with the hepatitis B (HBV) or hepatitis C virus (HCV) is a significant cause of liver disease-related morbidity and mortality in the European Union/European Economic Area (EU/EEA) [1]. Both viruses are transmitted through contact with infected blood, blood products and other bodily fluids. HBV is vaccine preventable which, along with other primary prevention measures including health care infection control and antenatal screening, have led to a decrease in acute and chronic hepatitis B (CHB) incidence in many EU/EEA countries [2]. Health care infection control together with harm reduction programmes among people who inject drugs (PWID) have also led to some decrease in the HCV incidence in many countries [3]. Many EU/EEA countries now face a dichotomy: a declining incidence of new HBV/HCV infections in the general population due to the success of primary prevention [2, 4] alongside a projected increase in liver disease-related morbidity and mortality due to ageing of the chronically infected population [5, 6]. With the availability of antiviral treatment that can effectively halt disease progression in CHB, including progression to cirrhosis and hepatocellular carcinoma, and new direct acting antivirals for chronic hepatitis C (CHC) that report cure rates in more than 90% of cases [7, 8], elimination of chronic viral hepatitis is a possibility. Elimination requires expanded access to screening, efficient linkage to care and retention in treatment among risk populations. Timely, reliable prevalence data are needed to understand which populations are most affected to better target screening and treatment programmes, and to monitor the performance and impact of these activities at a strategic level. Indeed, for screening to have a more favourable cost-effectiveness ratio and lead to an overall net gain in population health, current evidence indicates that it should be targeted to higher prevalence populations including PWID and other risk populations, where the expected case yield would be highest. [9, 10] However, the prevalence threshold above which a favourable cost effectiveness ratio varies considerably between EU/EEA countries.
People detained in prison settings are considered a high risk population for blood-borne virus infection due the criminalisation of high transmission risk behaviour such as injecting drug use and sex work, coupled with pre-detention social vulnerability (such as experience of domestic abuse, poverty and homelessness) among many people detained and convicted. Prison-acquired blood-borne virus infections may also occur due to the continuation of transmission risk behaviour, the limited availability of harm reduction services and the lack of adequate infection control practices [14, 15]. Dolan et al. meta-analysed data in Global Burden of Disease regions: in Western Europe, HBsAg and anti-HCV prevalence among people in prison was reported to be 2.4% and 15.5%, respectively, while in Eastern Europe it was 10.4% for HBsAg and 20.2% for anti-HCV [16]. HBsAg and anti-HCV estimates are also available for nine and 13 EU/EEA countries, respectively, although no study quality assessment nor country-level meta-analysis/pooling were performed.
Of the three at-risk populations included in this study, PWID are considered at highest risk due to the efficacy of unsafe injecting behaviour in transmitting HBV and HCV. This together with clustering of social and environmental risk factors in this marginalised population such as a history of incarceration, poverty, homelessness and multi-morbidity compound their vulnerability [17]. Nelson et al. conducted a global review of HBsAg and anti-HCV prevalence among PWID in 2010, and reported prevalence data for 30 EU/EEA countries for anti-HCV and for 26 EU/EEA countries for HBsAg. The prevalence of anti-HCV ranged from 21.1% in Finland to 90.5% in Latvia, whereas HBsAg prevalence ranged from 0.0% in Ireland and Cyprus to 21.3% in Estonia [17]. Wiessing et al. performed a systematic review of various epidemiological measures of the HCV epidemic among PWID in Europe [18]. Although anti-HCV prevalence was not an included outcome, their findings across the cascade of care show that 72% of anti-HCV infected PWID are viraemic; that 49% are unaware of their infection; and that 9.5% of diagnosed cases are reported to be on treatment. A review focused on the EU/EEA in 2009, Hahné et al. reported HBsAg prevalence among PWID to be between 0.0% and 21.3% and anti-HCV prevalence to be between 5.3% and 90% [13]. An updated synthesis of the prevalence in this priority population is required.
Our study is part of a larger project funded by the European Centre for Disease Prevention and Control (ECDC) that seeks to provide a timely update on available estimates across a number of low risk populations (the general population, pregnant women and first-time blood donors) and as a comparator/contrast to collate prevalence estimates in high risk populations. We describe the results of the study into chronic viral hepatitis low risk populations and among migrants elsewhere [19, 20]. In the study reported here, we seek to update and expand the work of the previous ECDC systematic review (from 2009) by Hahné et al. [21] of prevalence estimates for markers of hepatitis B (HBsAg) and C (anti-HCV) in three key risk groups: MSM, people who inject drugs and people incarcerated in prison. Our study seeks to contribute to the elimination of viral hepatitis in Europe by providing information to support the design and management of primary and secondary prevention strategies.
A systematic search to retrieve original research articles was conducted in PubMed, Embase and Cochrane Library bibliographic databases in March 2015. The search strategy (described in the Additional file 1) combined controlled (i.e. MeSH/Emtree terms) and natural vocabulary (i.e. keywords) to define disease-related (HBV or HCV infection), outcome-related (prevalence), and geographic-related search parameters (EU/EEA). To maximise the yield of the search, no population-specific search terms were included. Population relevancy was instead assessed at the title/abstract and full text assessment stages, as described below. The search was limited to records published from 1 January 2005 to 12 March 2015. Articles in all EU/EEA languages were included. The results of the search were shared with ECDC National Focal Points [26] for viral hepatitis in all EU/EEA Member States in May 2015 to review and validate the list of included references for their country. The data extraction, risk of bias assessment and data analysis described below were all performed in Microsoft Excel.
A total of 17 prevalence estimates, six for HBsAg and 11 for anti-HCV, were extracted from the 13 included studies about HIV negative/unknown HIV sero-status MSM. Key study details, including the risk of bias assessment, for all reported estimates among MSM are available in Annex 8 (HBV) and 9 (HCV) in the Additional file 1 for this article.
Limitations in the estimates reported for people in prison and MSM relate to geographical and population coverage, study quality and heterogeneity of the included estimates. To retrieve estimates for people in prison and for MSM, we conducted a very broad search of the published literature with no language or population restrictions, and validated retrievals directly with countries, yet found many geographical gaps in the data. Indeed, only a third of EU/EEA countries are represented among the studies that met the inclusion criteria for people in prison and only seven countries reported estimates among MSM. It is unlikely we failed to identify and include all existing high quality data, and consider it most likely that the data just do not exist or are not published. In the absence of larger, more robust studies from which prevalence can be derived, we consider the data reported here are the best available although there may have been more recent estimates published since the date of our search (March 2015). Significant heterogeneity in study design within and between risk groups hamper the statistical comparison and pooling of prevalence across countries and populations. To control for strong sources of bias in studies among people in prison when pooling data, we developed and applied a study quality assessment. The five domains were considered equally important sources of bias and it is possible that estimates included in the analysis have residual selection biases. Further, our study quality assessment did not consider sample size and there is clearly more uncertainty in the estimates derived from smaller studies.
Differences in the prevalence among people in prison between countries are related to the differential distribution of risk factors among the prison population together with differences in prison conditions, such as the availability of harm reduction interventions and infection control practices and infrastructure across the EU/EEA countries represented in this study [16]. The high prevalence of HBsAg in the prison population in some countries could be attributable to the incarceration of people born in intermediate or high prevalence countries and consequent over-representation of migrants in the incarcerated population. Recent estimates suggest that the proportion of the prison population that is foreign-born ranges from
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