Background

A large proportion of people living with HIV/AIDS in most European Union/European Economic Area (EU/EEA) countries are migrants, that is, people currently living outside their country of birth [1]. In 2013, around one third (33 %; 3 160) of those in EU/EEA who were reported to have contracted HIV through heterosexual contact were migrants from countries with generalised HIV epidemics (mainly sub Saharan Africa) [2]. While most of these diagnoses were made for the first time in Europe, HIV acquisition is predominantly assumed to have occurred in the home country [3].

This assumption is often based on reports from clinicians who make deductive inferences according to a patient’s country of birth, time of arrival in the new country of residence, CD4 cell counts and the natural history of HIV infection. Clinicians may also use algorithms that are biased towards determining that patients born in countries with a generalised epidemic contracted HIV prior to migrating to Europe [4]. Often these estimates do not take into account additional factors. For example, it has been reported that CD4 cell counts close to seroconversion are considerably lower among those living with non-B HIV-1 viral subtypes, which are most common among migrants from outside Europe, particularly in Sub-Saharan Africa. [3, 5, 6]. Consequently, a lower CD4 cell value at diagnosis in those with non-B sub-types may wrongly suggest that individuals have been living with HIV for longer than they have; leading to the conclusion that HIV was acquired before migration. The presence of non-B subtypes among Europe-born populations may also be interpreted as evidence of sexual mixing between migrants and non-migrants.

Funding for primary prevention among migrant communities may be reduced or redirected if surveillance data suggest that individuals do not have HIV prevention needs after they have left their home country or that significant numbers of migrants are coming to Europe as “HIV health tourists” [7, 8]. There have been no previous efforts to collate the information about the proportion of people from countries with a generalised epidemic that contract HIV post-migration. If programme managers and policy-makers underestimate the degree of HIV acquisition within the EU/EEA for migrants from countries with generalised epidemics this may undermine the potential for reducing HIV prevalence and incidence through targeted primary and secondary prevention programmes and policy.

This paper presents a review of the evidence of post-migration HIV acquisition among migrants from countries with a generalised epidemic living in Europe. We examine quantitative studies and surveillance reports based on data on populations from countries with a generalised epidemic which include outcomes that estimate the probable country of acquisition, incident infections, or evidence of sexual mixing. In addition this paper profiles the ability of EU Member States surveillance systems to provide accurate monitoring information about probable country of HIV acquisition. We discuss the implications of these results in HIV prevention programming and policy across the EU/EEA region.

Methods

Systematic review

Nine electronic databases (Allied and Complementary Medicine; Cochrane Database of Systematic Reviews; Cumulative Index to Nursing & Allied Health Literature; Database of Abstracts of Reviews of Effects; EMBASE; Health Management Information Consortium; Health Technology Assessment; Medline; PsychInfo) were searched during May 2012Footnote 1. A detailed search strategy was used which combined synonyms for “HIV”, “migrant”, “assortative sexual mixing”, “sexual transmission” with demonyms for all countries with a generalised HIV epidemic (for the complete list search terms, a full description the review protocol please see report [9]). Searches were limited to studies conducted between 01/0/1/2002 and 31/12/2014 to provide the most up-to-date estimates. Studies written in English, French, Italian, Portuguese and Spanish were included. Additional grey literature was retrieved from four websites (United Nations Department of Economic and Social Affairs Population Division; European Health for All database, World Health Organization Regional Office for Europe; European Centre for Disease Prevention and Control), and relevant data were requested from individuals participating in the Member States Survey (see below). The search process was documented by compiling the search strategies used to explore each resource.

Selection criteria

Only studies conducted in countries with programmatic or surveillance links within the European Centre for Disease Prevention and Control (ECDC) were included in this reviewFootnote 2. Studies were eligible for inclusion if: the study population included migrant men or women from countries with a generalised HIV-1 epidemic AND the study included sub-group analysis based on race/ethnicity or country/region of origin OR at least 80 % of the study populations were from countries with a generalised HIV epidemic. Studies were only included if they reported on any of the following outcomes: proportion of target population infected with HIV in country of origin; proportion of target population infected in country of migration; estimate of incident HIV infections (not diagnoses) in target population in country of migration; probable country of infection/HIV acquisition and evidence of sexual mixing. Studies that reported mode of transmission but made no reference to whether sexual transmission took place pre- or post-migration were excluded at full paper screening stage. Qualitative studies (using in-depth interviews, focus group discussions, and document analysis), conference communications, pilots or feasibility studies were excluded.

Quality assessment

Studies were selected using a two-stage screening approach. Reviewers devised a checklist to independently screen all retrieved titles and abstracts. Studies were given an overall quality score which incorporated a number of factors drawn from the PRISMA [10] and NICE guidelines [11] including risk of bias, internal and external validity (See Table 1). Papers were graded as having an overall quality score of “Low”, “Medium” or “High”. We were aware that within this review few cohort or intervention studies would be retrieved which may lead to a systemic bias in quality assessment. As a result studies were rated within the paradigm of their study type and studies based on surveillance or cross sectional data were able to achieve overall quality scores of “Medium” or “High”. Studies that received a “Low” score or for which no information to perform quality assessment was available were excluded from the final review. Inter-reviewer reliability scores (Cohen κ) were calculated using Kappa in Microsoft Excel: a kappa of 0.68 for full paper screening and 0.64 for quality appraisal, indicated a high level of agreement between reviewers.

Table 1 Criteria used to assess the quality of papers included in full paper review
Full size table

Data extraction and analysis

Data were extracted using forms detailing study objectives; thematic areas; data collection; methodology (design; setting; population; sample size; geographical scope); results and outcomes (n or %); author defined strengths and limitations and gender specific issues. After data extraction for each paper, studies were grouped according to outcomes of interest. Narrative summaries of each outcome of interest are presented.

Member states survey

During August 2012, a survey was conducted among 30 EU/EEA Member states using an online survey software package SelectSurveyNet (ClassApps). The questionnaire was developed to gather information from representatives of each member state regarding their knowledge and surveillance of HIV and HIV transmission among migrants from countries with a generalised HIV epidemic. Nationally nominated HIV surveillance contact points were invited to complete the short, 14-item questionnaire which contained mainly open questions, allowing respondents to provide detailed responses. Survey questions were tailored to each country based on information that had been recently submitted to ECDC as part of the Dublin Declaration reporting processFootnote 3. Participants were also able to upload documents to support their responses and these documents were added to the systematic literature review process described above.

Results

In total 8125 documents were retrieved from all sources. Twenty-seven peer-reviewed papers (representing 26 studies) were found to fulfil the inclusion and quality assessment criteria and were therefore included in the final review. Fig. 1 summarises the outcome of the paper selection process.

Fig. 1
figure 1

Summary of study selection process

Full size image

Papers were included from six EU countries: United Kingdom (9); Netherlands (4); France (4); Spain (2); Belgium (1) and Italy (3). Two papers were also included from Switzerland and two further papers covered the entire European region. Studies were grouped according to outcomes of interest within three categories: Probable country of HIV acquisition; Estimates of incident HIV infections; and Evidence of sexual mixing. Tables 2 and 3 summarise the 26 studies’ characteristics and includes the quality appraisal process results.

Table 2 Summary of included studies: population characteristics
Full size table
Table 3 Outcomes and limitations of included studies
Full size table

Probable country of HIV acquisition and estimates of incident HIV infection

Estimates of probable country of infection and/or estimates of incident infection were found in 18 of the 27 papers selected for systematic review. In most of the papers, the study population included people from countries not considered to have a generalised HIV epidemic, but data were disaggregated which allowed reviewers to perform data extraction and compare data across countries. The estimates varied both within countries and across Europe, and covered a range of subgroups, including men who have sex with men (MSM) as well as heterosexuals. Table 4 shows the proportion of infections acquired among sub Saharan Africans post–migration in France, Netherlands, Switzerland and the UK. Table 5 shows infections acquired post-migration among individuals from the Caribbean and Asia in Italy, Netherlands, Switzerland and the UK.

Table 4 Proportion of infections acquired in European countries among people born in Africa or with Black African ethnicity
Full size table
Table 5 Proportion of infections acquired in European countries among people born in Caribbean or Asia or with Black Caribbean ethnicity
Full size table

While the generilisability and validity of all these papers were medium or high, there are some limitations to the data presented (Table 3). Data estimating the proportion of post-migration HIV acquisition from cross sectional studies in France, Italy, Switzerland and the UK relied on samples that were either very small [12] or were reported to be possibly biased and unrepresentative of the wider population from which the samples were drawn [13–15]. Estimates from The Netherlands were derived from mathematical models. The authors provided very little information about the data used to source the models nor did they discuss the consequent limitations such data placed on the models [35]. Treatment as a means of reducing sexual transmission of HIV now forms a key part of the prevention paradigm, like other conditions of paramount public health importance such as tuberculosis [36]. However, policy responses such as mandatory screening contravene the WHO policy framework for HIV testing in Europe which states mandatory HIV testing for migrants and asylum seekers upon arrival violates basic rights and ethical principles and cannot be justified on public health grounds [37]. Improving access to HIV treatment for all infected persons, regardless of their administrative and or immigration status, could positively impact on reducing incident infections both within and beyond migrant communities. This would necessitate addressing the already identified barriers to HIV prevention, testing and care that exist for migrant communities [31]. Failure to ensure access to HIV treatment for all persons in need could prove detrimental to efforts to ameliorate the HIV epidemic.

Conclusion

There is limited published evidence about the acquisition of HIV within Europe among migrants from countries with a generalised epidemic. Individuals are certainly contracting HIV through sexual contact after they have moved to Europe and MSM appear to be at particular risk of post-migration HIV acquisition, yet this is rarely acknowledged within the literature. Only a few countries collect and publish data to enable robust estimates to quantify or monitor the place of HIV infection, which may have a detrimental impact on HIV prevention interventions.

The majority of countries that identify migrants as an important at risk population for HIV infection have put in place measures to estimate the distribution of HIV in these groups. Despite the many areas of concordance and agreement in Member States surveillance systems there remain a number of gaps in the processing and availability of this data. This therefore limits the ability of policymakers and programme managers who wish to have an impact on HIV incidence at country and regional levels.