Secondary Logo

Journal Logo

Epidemiology and Prevention

HIV Infection in Migrant Populations in the European Union and European Economic Area in 2007–2012

An Epidemic on the Move

Hernando, Victoria PhD*,†; Alvárez-del Arco, Débora PhD*,†; Alejos, Belén MSc*,†; Monge, Susana MD†,‡; Amato-Gauci, Andrew J. MD§; Noori, Teymur MD§; Pharris, Anastasia MD§; del Amo, Julia MD*,†

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: October 1, 2015 - Volume 70 - Issue 2 - p 204-211
doi: 10.1097/QAI.0000000000000717

Abstract

INTRODUCTION

The HIV epidemic continues to be a public health issue in the European Union and European Economic Area (EU/EEA).1,2 Although men who have sex with men (MSM) account for the majority of the new HIV cases reported on a yearly basis, migrant populations have been acknowledged by the European Centre for Disease Prevention and Control (ECDC) and the European Commission as one of the priority groups for HIV prevention and care.2–9 Migrants encompass very diverse populations with different migration drivers—economic, social, political, cultural, and environmental—as well as distinct risk contexts for HIV infection. Previous analysis in EU/EEA countries between 1999 and 2006 revealed the large contribution of people from high-endemic countries of Sub-Saharan Africa to reported HIV cases predominantly in Western Europe.10 During that period, more female cases were reported among migrants from Sub-Saharan Africa, mirroring the disproportionate burden of HIV infection among women in Sub-Saharan Africa and, possibly, reflecting patterns of antenatal testing for HIV. Nonetheless, increasing number of MSM of migrant origin, largely from other European countries and from Latin America, has been reported in recent years.9,11–13 Furthermore, migration from Eastern Europe, where injecting drug use (IDU) has been the major driver of the epidemic,1 may also impact on the epidemiology of HIV in migrant populations in the EU/EEA.8

The aim of this study is to describe the epidemiology of reported HIV infections by geographical origin, sex, and transmission category in the EU/EEA for the years 2007–2012. We analyzed late HIV presentation by geographical origin and describe the relative contribution of migrants in the Western, Central, and Eastern regions of the EU/EEA.

METHODS

We analyzed data from the European Surveillance System (TESSy) for 29 countries (Austria, Belgium, Bulgaria, Cyprus, Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Iceland, Ireland, Italy, Latvia, Lithuania, Luxemburg, Malta, the Netherlands, Norway, Poland, Portugal, Romania, Spain, Slovakia, Slovenia, Sweden, and United Kingdom) reported for the period 2007–2012. All new HIV cases reported in the study period were included in these analyses.

The outcomes studied were incident HIV diagnosis and late HIV presentation defined according to the European Late Presenter Consensus Working Group as having a CD4 count below 350 cells per cubic millimeter or an AIDS-defining event at the time of HIV diagnosis.14

HIV surveillance systems throughout the EU/EEA differ with regard to which variables are used to report migrant status. For the current analyses, the main exposure variable geographical origin was generated combining the information on country of birth, country of nationality, and/or region of origin. These data have been systematically collected since 2008, but most countries have uploaded historical data going back until 1998. When more than one of these variables was available, we gave priority to information on country of birth, then country of nationality, and last, region of origin. Geographical origin was classified as native if the reporting country was the same as the country of birth or country of nationality. Migrants were classified as from the following regions: European [subdivided into the subregions as follows: Western Europe: Andorra, Austria*, Belgium*, Denmark*, Finland*, France*, Germany*, Greece*, Iceland, Ireland*, Israel, Italy*, Luxembourg*, Malta*, Monaco, the Netherlands*, Norway, Portugal*, San Marino, Spain*, Sweden*, Switzerland, United Kingdom*; Central Europe: Albania, Bosnia and Herzegovina, Bulgaria*, Croatia, Cyprus*, Czech Republic*, Hungary*, Macedonia, Montenegro, Poland*, Romania*, Serbia, Slovakia*, Slovenia*, Turkey; Eastern Europe: Armenia, Azerbaijan, Belarus, Estonia*, Georgia, Kazahstan, Kyrgyzstan, Latvia*, Lithuania*, Republic of Moldova, Russian Federation, Tajikistan, Turmenistan, Ukraine, Uzbekistan (* denotes countries that constitute the EU as of January 1, 2007)], Sub-Saharan Africa, Latin America, East Asia and Pacific, Australia and New Zealand, South and Southeast Asia, North Africa and Middle East, North America, the Caribbean, and unknown.15 Other variables included sex, age at HIV diagnosis, year of HIV diagnosis, most likely route of HIV transmission, CD4 cell count, and AIDS stage at HIV diagnosis.

For these analyses, we only considered cases with information on sex and geographical origin. Italy recorded whether cases were Italians or foreigners but started reporting the geographical origin of foreign cases only from 2010 onwards. For the purpose of these analyses, and considering that Italy represented 10% of the total HIV diagnoses in the study period, we assumed the distribution of geographical origin countries for non-Italian cases reported from 2007 to 2009 to be the same as in 2010.

Statistical Analyses

We calculated medians and their interquartile ranges (IQRs) for continuous variables and proportions for categorical variables. Differences in age and sex were assessed through the Mann–Whitney U test and χ2 test for independence. Linear regression was used to evaluate the trends by sex among migrant cases. Logistic regression was used to analyze the association between geographical origin and late HIV presentation for men and women. Crude odds ratios (ORs) and their 95% confidence intervals (95% CIs) were calculated, as well as adjusted OR (aOR), controlling for the confounding effect of age and transmission category. We assessed interactions with sex (an a priori effect modifier) through likelihood ratio tests. Robust methods (clustered sandwich estimator) were used to estimate the CIs, assuming correlation among subjects recruited within each country.16 Analyses did not take into account reporting delay given that the underlying assumptions may not hold equally well for some geographical origins (ie, Latin Americans), which seem to be experiencing trend fluctuations.

Sensitivity Analyses

We performed sensitivity analyses to assess potential misclassification of the main exposure variable and reran analyses using country of nationality instead of country of birth. HIV surveillance data reporting changed in Spain where 7 additional reporting regions were incorporated during the study period. Similarly, Italy increased the coverage of the regions reporting data from about half to all regions during the reporting period. All analyses were repeated excluding all cases reported from Italy and all cases from these 7 additional Spanish regions.

Analyses were performed using Stata version 13.1 (Stata Corp, College Station, TX). Maps were created using ArcView version 3.2 and the data source: GISCO—Eurostat (European Commission) and Administrative boundaries: EuroGeographics, UN-FAO, Turkstat.

RESULTS

A total of 181,881 HIV diagnoses were reported during the period 2007–2012. A total of 25,064 cases were excluded because they did not have information on sex (738) or geographical origin (24,326). Data completeness for geographical origin varied widely by country, from over 90% in 18 of the 29 reporting countries to 70% in Belgium, Norway, and France, and 25% and 32% in Estonia and Latvia, respectively (see Table S1 of the Appendix, Supplemental Digital Content, http://links.lww.com/QAI/A700).

Epidemiologic Characteristics by Geographical Origin and Sex

Of the 156,817 HIV diagnoses reported in the EU/EEA between 2007 and 2012 with known geographical origin, 38% (60,446) were classified as migrants (63% of 41,246 female cases and 30% of 115,571 male cases). Migrants accounted for 59,886 (42%) of cases reported in Western EU/EEA countries, 530 (5%) in Central EU/EEA countries, and 30 (1%) in Eastern EU/EEA countries (Baltic States). Information on geographical origin in Central and Eastern EU/EEA countries was generally incomplete (see Table S1 of the Appendix, Supplemental Digital Content, http://links.lww.com/QAI/A700).

Fifty-three percent (31,843) of all nonnative HIV cases reported in 2007–2012 originated from Sub-Saharan Africa, followed by 21% (12,492) from European countries (other than the country of report) and 12% (7549) from Latin America (Table 1). Intra-European migrant cases originated from Western, Central, and Eastern European countries in 46%, 33%, and 22% of the cases, respectively. These shares varied among the EU/EEA subregions (Fig. 1A): In Western EU/EEA countries, migrants from Sub-Saharan Africa accounted for the majority of migrant cases with the exception of Spain, where migrants from Latin America accounted for the majority of cases. In Central EU/EEA countries, migrants originating from Eastern Europe accounted for the majority of reported cases (Fig. 1B).

TABLE 1
TABLE 1:
Distribution of the 156,817 Cumulative HIV Diagnoses Reported Between 2007 and 2012 According to Geographical Origin and Sex
FIGURE 1
FIGURE 1:
A, Most common geographical origin of migrants reported with HIV in EU/EEA countries, 2007–2012. B, Proportion migrants within HIV reports in EU/EEA originating from Europe (*), Sub-Saharan Africa, and Latin America, 2007–2012. Europe* includes Western, Central, and Eastern Europe.

The proportion of women (43%) among migrants was higher than in natives with HIV (16%).

Among native cases, sex between men was the reported route of transmission for 51% of the HIV diagnoses where information on transmission route was available. Sex between men was also the most frequent route of transmission reported among migrants from Western (64%) and Central (38%) Europe, Latin America (60%), East Asia and the Pacific (54%), Australia and New Zealand (84%), and North America (81%). Heterosexual transmission was the most common reported route of transmission for migrant cases from Eastern Europe (44%), Sub-Saharan Africa (87%), South and Southeast Asia (56%), North Africa and Middle East (49%), and the Caribbean (65%). IDU accounted for 25% of new HIV diagnoses in migrants from Eastern Europe (see Figure S1 of the appendix, Supplemental Digital Content, http://links.lww.com/QAI/A700).

Of 156,817 subjects, 95.7% (150,080) had information on age. The median age at HIV diagnosis was 37 (IQR: 29–45) for men and 34 (IQR: 28–42) for women. The median age in natives was higher for every geographical origin, both for men and women, except for migrants from the Caribbean and male migrants from Sub-Saharan Africa, although these differences were not statistically significant (see Figure S2 of the appendix, Supplemental Digital Content, http://links.lww.com/QAI/A700).

For the 92,748 HIV reports with available data on CD4 count at HIV diagnosis, median CD4 cell count was 379 (IQR: 177–575) for natives and 304 (IQR: 132–492) for migrants (P < 0.001). Among migrants, it was 317 (IQR: 133–508) in men and 290 (IQR: 131–470) in women (P < 0.001). For all other geographical origins with the exceptions of Sub-Saharan Africa and Eastern Europe, median CD4 cell counts at diagnosis were higher in men than in women (see Figure S3 of the appendix, Supplemental Digital Content, http://links.lww.com/QAI/A700).

Late HIV Presentation by Geographical Origin and Sex

For this analysis, we considered 129,920 cases with information on CD4 count or AIDS stage at HIV diagnosis. Compared with native cases diagnosed with HIV, male migrants from high-income settings (Western Europe, Australia and New Zealand, and North America) had similar proportions of late HIV presentation in analyses that adjusted by age and transmission category, whereas those from middle- and low-income settings had a higher risk of late HIV presentation (Table 2), with aOR of 1.60 (95% CI: 1.22 to 2.09) and 1.66 (95% CI: 1.27 to 2.16) for men from Sub-Saharan Africa and Latin America, respectively (Table 2). For female cases, nearly all migrant groups—except for Australia and New Zealand and North America, which accounted for a very low number —had a higher risk of late HIV presentation than natives, with aOR of 1.67 (95% CI: 1.13 to 2.47) and 1.64 (95% CI: 1.17 to 2.31) for women from Sub-Saharan Africa and Latin America, respectively (Table 2).

TABLE 2
TABLE 2:
Prevalence of Late HIV Diagnosis, Crude and Adjusted Odds Ratios, and 95% Confidence Intervals for Men and Women by Geographical Origin and Adjusted by Age and Category of Transmission, EU/EEA, 2007–2012

Median CD4 cell count at HIV presentation in 2007 was 250 (IQR: 100–430) for migrants from SSA and rose steadily to 271 (IQR: 116–460) in 2012. For migrants from Latin America, a similar pattern was observed: 336 (IQR: 144–550) in 2007 and 344 (IQR: 162–526) in 2012.

Trends in HIV Cases From 2007 to 2012 by Geographical Origin and Sex

For all migrant groups, a decrease of 14% in the number of new HIV reports was observed from 2007 to 2012, although patterns varied by geographical origin and sex. Overall, HIV cases reported among male migrants increased slightly, by an average of 14 cases per year due to growing numbers from Latin America, Central, and Eastern Europe coupled with decreases from Sub-Saharan Africa (Fig. 2A). The number of men from Latin America peaked in 2010 and has since decreased. HIV cases reported among female migrants decreased by an average of 272 cases per year (Fig. 2B). This was mainly driven by heterosexually infected women from Sub-Saharan Africa, which dropped from 3725 cases in 2007 to 2354 in 2012 (Fig. 2B), although other geographical origins, in particular migrants from Latin America, Southeast Asia, the Caribbean, and Western Europe also decreased. Similar to the pattern observed among males, HIV cases reported among women from Latin America peaked in 2009 and have since then decreased.

FIGURE 2
FIGURE 2:
Temporal trends in the numbers of HIV diagnoses by geographical origin in migrant men (n = 34,299) (A) and in migrant women (n = 26,148) (B).

The number of heterosexually acquired HIV reports in migrants has decreased from 7030 in 2007 to 5008 in 2012 (Fig. 3). The decrease is particularly observed among heterosexual migrants from Sub-Saharan Africa from 5391 to 3393. The absolute number of HIV diagnoses in migrant MSM increased from 1927 in 2007 to 2459 in 2012 (Fig. 3), the commonest origins being Latin America and Western Europe. The decreasing trend in the number of HIV diagnoses in native and migrant IDUs (Fig. 3) is disrupted in 2010 and increases are observed in 2011 and 2012. Migrants from Eastern and Central Europe accounted for most of the diagnosed HIV cases among IDU.

FIGURE 3
FIGURE 3:
Trends of new reported HIV diagnoses among native cases and migrants by transmission category, EU/EEA, 2007–2012.

Sensitivity Analyses

Analyses using country of nationality instead of country of origin as the first option to create “geographical origin” yielded identical results (data not shown).

Analyses excluding Italian HIV diagnoses and the 7 new Spanish reporting regions did not change the main findings (data not shown).

DISCUSSION

These are the first analyses with a wide European scope documenting profound changes in the epidemiology of HIV migrant population in Europe from 2007 onwards. Migrants represented nearly two-fifths of all HIV cases reported in the EU/EEA between 2007 and 2012. Most of these cases were reported in countries in the Western part of the EU/EEA, with migrants comprising much smaller proportions of HIV cases reported by countries in the Central and Eastern parts of the EU/EEA. Migrants from Sub-Saharan Africa, Latin America, and from within Western Europe, each with distinct epidemiologic profiles, accounted for the majority of HIV cases among migrants reported in Western EU/EEA countries, whereas most migrant cases reported in Central EU/EEA countries originate from Central and Eastern Europe. Among both male and female HIV cases, migrants from low- and middle-income countries have a higher likelihood of a late HIV presentation than native cases. Overall, there has been a decline in the number of HIV cases reported among migrants in the EU/EEA from 2007 to 2012 largely due to decreases in cases from Sub-Saharan Africa, particularly among females, coupled with clear increases from Central Europe. HIV cases reported among persons from Latin America increased up to 2009–2010 to decrease thereafter. An increase was observed in migrant MSM and recently also in people who injecting drugs.

Sub-Saharan Africa remains the most common region of origin for HIV cases reported among migrants to the EU/EEA, and the reasons for this have been well documented.10,17 Although this applies to the majority of countries in Europe, our study shows that in Spain, Latin Americans accounted for most HIV notifications among migrants, reflecting migration trends in the population as a whole.18,19 The HIV transmission mechanisms in migrants from Sub-Saharan Africa are also well known and mimic epidemics in the countries of origin with heterosexually transmitted HIV infections predominating and women outnumbering men among the newly diagnosed HIV cases.1 A different picture is observed among migrants from Latin America and the Caribbean, where HIV cases due to sex between men are far more common and may reflect selective migration of MSM from these regions to the EU/EEA due the more permissive attitudes toward same sex relationships.12 A nonnegligible proportion of HIV cases reported among IDU are migrants, and trends among both native and migrant IDU from Central and Eastern Europe have increased from 2010 onward. The increase in new HIV notifications among native IDU reflects the well-documented outbreaks in Greece and Romania20,21 associated with underfunded harm-reduction programs.22

Although higher prevalence of late HIV presentation in migrants has been reported previously,23–27 ours are the first data stratified by sex including a comprehensive breakdown by geographical origin. Male and female HIV-positive migrants from low- and middle-income regions have a higher proportion of late HIV presentation as compared with native populations, whereas the proportions in migrants from high-income countries are similar to those of the native population. This exemplifies that not all migrants are excluded from social and health services and that efforts should target those groups exposed to poverty and socioeconomic disadvantage.28,29 Indeed, a recent publication by Alvarez-delet al30 highlights that not all EU/EEA countries explicitly recommend HIV testing for migrant and calls for expanding HIV testing to help reducing health inequity. Some of the diagnoses in migrant populations classified as “late presentation” may have been diagnosed with HIV in their country of origin, but it is impossible to obtain comprehensive data on this at European level through routine surveillance. Nevertheless, given that their clinical and immunological situation when presenting to care in Europe is a late presentation, programs should aim to facilitate earlier engagement to care. Similarly, our data cannot answer which are the likely countries of HIV acquisition. A recent report by the ECDC has recognized that acquisition of HIV in migrant populations in European countries of destination is taking place but that is difficult to quantify. It is thought that this is particularly affecting migrant MSM and, to a lesser extent, heterosexually transmitted HIV.6

A novel and important finding in this study is the overall decline in the number of HIV diagnoses in migrants from 2007 to 2012. This decline takes into account the changes in the HIV reporting mechanisms in the different EU/EEA countries, namely Italy and Spain. This decline is largely driven by striking decreases in the number of HIV diagnoses in women from Sub-Saharan Africa and to a lesser extent men from Sub-Saharan Africa and women from other regions. After steady increases in the number of HIV diagnoses in migrants from Latin America, decreases are seen from 2010 onwards. In contrast, diagnoses in males and females from Central and Eastern Europe have increased. The reasons for these changes are likely to be multifactorial and beyond the scope of our current analyses. However, it is well known that migration flows are determined by socioeconomic inequality and work opportunities.31 The global financial crisis that has affected many EU/EEA countries since 2008 has led to high unemployment rates and job insecurity, and these effects have been more dramatic among migrant laborers.20 In some EU/EEA countries, this has led to decreases in the number of registered migrants and increased remigration to countries of origin or to places less affected by the economic crisis.32,33 Changes in migration flows, including that of irregular migrants, should be taken into account and studied further to explain observed changes in the trends of newly reported HIV diagnoses. Unfortunately, toughened immigration laws and restrictions to accessing health care and social rights, largely but not solely, for undocumented migrants have also emerged, and our data may be reflecting lower uptake of HIV testing in recent years.34,35 Nonetheless, our data do not support lower uptake of HIV testing as yet, given median CD4 cell counts for Sub-Saharan Africa and Latin America migrants have not declined during the study period.

Another potential explanation for the decreases in new HIV cases in migrants from Sub-Saharan Africa origin may be the changes in HIV epidemiology in their countries of origin and the increases in ART coverage. Indeed, more than a 30% reduction in HV incidence has been reported in many countries in Sub-Saharan Africa in the last decade,17 partly due to scaled up ART coverage in many low- and middle-income countries, also leading to increases in overall HIV prevalence.36

A number of limitations should be acknowledged when interpreting these data. A relatively high proportion (13.8%) of HIV cases had to be excluded because of unknown geographical origin, particularly in Eastern EU/EEA countries. As a result, it is difficult to draw any firm conclusions on the epidemiology of HIV infections in migrant cases from this part of the EU/EEA. However, these countries generally do not receive a large number of migrants so that missing data from this region would not be expected to greatly affect the description and interpretation of overall EU/EEA trends of HIV cases among migrants. Relevant changes in HIV reporting systems during the study period took place in Italy (coverage of HIV surveillance increased over the period, and data on the geographical origin of migrants were only collected from 2010 onwards) and, to a lesser extent, in Spain (coverage of HIV surveillance increased over the period). These changes, if not taken into account, would have led to biased trends in the number of HIV-positive migrants reported. The sensitivity analyses performed to take the above into considerations did not change the main conclusions. Our results are robust to sensitivity analyses using country of nationality instead of country of origin to generate “geographical origin.” Finally, the decreases of HIV diagnoses observed for Sub-Saharan African and Latin American migrants are also seen for year 2011 minimizing the role of delayed reporting as an alternative explanation.

In the light of our findings, HIV prevention programs in the EU/EEA should continue to focus on migrants from Sub-Saharan Africa but also address the significant proportions of migrants from Latin America and Central and Eastern Europe taking into consideration the epidemics among migrant MSM and IDUs. Improving reporting of country of origin in Central and Eastern European countries is critical to have a picture of the migration trends in this area. Our results indicate that the HIV epidemic in migrant populations in EU/EEA member states is changing, probably reflecting global changes in the HIV pandemic, the impact of large-scale ART implementation, a selective migration from MSM from repressive countries to more permissive European societies, and migration fluctuations secondary to the economic crisis in Europe.

ACKNOWLEDGMENTS

The authors thank the operational contact points for HIV surveillance from EU/EEA Member States participating in the European network for HIV/AIDS surveillance: Austria: Jean-Paul Klein; Belgium: Andre Sasse; Bulgaria: Tonka Varleva; Cyprus: Maria Koliou; Czech Republic: Marek Maly; Denmark: Susan Cowan; Estonia: Kristi Rüütel; Finland: Kirsi Liitsola; France: Florence Lot; Germany: Barbara Gunsenheimer-Bartmeyer; Greece: Georgios Nikolopoulos, Dimitra Paraskeva; Hungary: Mária Dudás; Iceland: Guðrún Sigmundsdóttir, Haraldur Briem; Ireland: Kate O'Donnell, Derval Igoe; Italy: Barbara Suligoi, Laura Camoni; Latvia: Šarlote Konova; Lithuania: Saulius Čaplinskas, Irma Čaplinskienė; Luxembourg: Jean-Claude Schmit; Malta: Jackie Maistre Melillo, Tanya Melillo; the Netherlands: Eline Op de Coul; Norway: Hans Blystad; Poland: Magdalena Rosinska; Portugal: Helena Cortes Martins; Romania: Mariana Mardarescu; Slovakia: Peter Truska; Slovenia: Irena Klavs; Spain: Mercedes Diez Ruiz-Navarro; Sweden: Maria Axelsson; United Kingdom: Valerie Delpech.

REFERENCES

1. European Centre for Disease Control and Prevention. HIV/AIDS surveillance in Europe. Available at: http://www.ecdc.europa.eu/en/publications/Publications/hiv-aids-surveillance-report-2012-20131127.pdf. Accessed June 30, 2015.
2. European Commission. Action plan on HIV/AIDS in the EU and neighbouring countries: 2014-2016. Available at: http://ec.europa.eu/health/sti_prevention/docs/ec_hiv_actionplan_2014_en.pdf. Accessed June 30, 2015.
3. European Centre for Disease Control and Prevention. Migrant health: background note to the ECDC Report on migrantion and infectious diseases in the EU. Available at: http://www.ecdc.europa.eu/en/publications/Publications/0907_TER_Migrant_health_Background_note.pdf. Accessed June 30, 2015.
4. European Centre for Disease Control and Prevention. Migrant health: access to HIV prevention, treatment and care for migrant populations in EU/EEA countries. Available at: http://ecdc.europa.eu/en/publications/publications/0907_ter_migrant_health_hiv_access_to_treatment.pdf. Accessed June 30, 2015.
5. European Centre for Disease Control and Prevention. Migrant health: improving HIV data comparability in migrant populations and ethnic minorities in EU/EEA/EFTA countries: finding from a literature review and expert panel. Available at: http://www.ecdc.europa.eu/en/publications/Publications/1108_TER_Improving_HIV_data_comparability_in_migrants.pdf. Accessed June 30, 2015.
6. European Centre for Disease Control and Prevention. Migrant health: sexual transmission of HIV within migrant groups in the EU/EEA and implications for effective interventions. Available at: http://www.ecdc.europa.eu/en/publications/Publications/Migrant-health-sexual-transmission.pdf. Accessed June 30, 2015.
7. European Centre for Disease Control and Prevention. Thematic report: migrants monitoring implementation of the dublin declaration on partnership to fight HIV/AIDS in Europe and Central Asia: 2012 progress. Available at: http://ecdc.europa.eu/en/publications/Publications/dublin-declaration-monitoring-report-migrants-september-2013.pdf. Accessed June 30, 2015.
8. European Centre for Disease Control and Prevention. Assessing the burden of key infectious diseases affecting migrant populations in the EU/EEA. Available at: http://www.ecdc.europa.eu/en/publications/Publications/assessing-burden-disease-migrant-populations.pdf. Accessed June 30, 2015.
9. European Centre for Disease Control and Prevention. Migrant health: epidemiology of HIV and AIDS in migrant communites and ethnics minorities in EU/EEA countries. Available at: http://www.ecdc.europa.eu/en/publications/Publications/1108_TER_HIV_in_migrants.pdf. Accessed June 30, 2015.
10. Del Amo J, Likatavicius G, Perez-Cachafeiro S, et al.. The epidemiology of HIV and AIDS reports in migrants in the 27 European Union countries, Norway and Iceland: 1999-2006. Eur J Public Health. 2011;21:620–626.
11. Elford J, Doerner R, McKeown E, et al.. HIV infection among ethnic minority and migrant men who have sex with men in Britain. Sex Transm Dis. 2012;39:678–686.
12. European Centre for Disease Control and Prevention. EMIS 2010: the European men-who-have-sex-with-men internet survey. Available at: http://ecdc.europa.eu/en/publications/Publications/EMIS-2010-european-men-who-have-sex-with-men-survey.pdf. Accessed June 30, 2015.
13. Evans AR, Hart GJ, Mole R, et al.. European migrant men who have sex with men: an exploration of sexual risk in the UK. Sex Transm Infect. 2011;87:325–330.
14. Antinori A, Coenen T, Costagiola D, et al.. Late presentation of HIV infection: a consensus definition. HIV Med. 2011;12:61–64.
15. World Health Organization. Global Report. UNAIDS Report on the Global AIDS Epidemic 2010. Available at: http://www.unaids.org/sites/default/files/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf. Accessed June 30, 2015.
16. Williams RL. A note on robust variance estimation for cluster-correlated data. Biometrics. 2000;56:645–646.
17. UNAIDS. UNAIDS report on the global AIDS epidemic 2013. Available at: http://epp.eurostat.ec.europa.eu/cache/ITY_OFFPUB/KE-ET-10-001/EN/KE-ET-10-001-EN.PDF. Accessed June 30, 2015.
18. National Epidemiology Center. Vigilancia Epidemiologica del VIH/SIDA en España. Situación a 30 de junio de 2013. Available at: http://www.isciii.es/ISCIII/es/contenidos/fd-servicios-cientifico-tecnicos/fd-vigilancias-alertas/fd-enfermedades/fd-sida/Informe_VIH_sida_Junio_2013.pdf. Accessed June 30, 2015.
19. National Statistics Institute. Continuous register statistics, Spain. Available at: http://www.ine.es/jaxi/menu.do?type=pcaxis&path=%2Ft20%2Fe245&file=inebase&L=0. Accessed June 30, 2015.
20. Paraskevis D, Nikolopoulos G, Fotiou A, et al.. Economic recession and emergence of an HIV-1 outbreak among drug injectors in Athens metropolitan area: a longitudinal study. PLoS One. 2013;8:e78941.
21. Pharris A, Wiessing L, Sfetcu O, et al.. Human immunodeficiency virus in injecting drug users in Europe following a reported increase of cases in Greece and Romania, 2011. Euro Surveill. 2011;16:20032.
22. Karanikolos M, Mladovsky P, Cylus J, et al.. Financial crisis, austerity, and health in Europe. Lancet. 2013;381:1323–1331.
23. Mocroft A, Lundgren JD, Sabin ML, et al.. Risk factors and outcomes for late presentation for HIV-positive persons in Europe: results from the Collaboration of Observational HIV Epidemiological Research Europe Study (COHERE). PLoS Med. 2013;10:e1001510.
24. Monge S, Alejos B, Dronda F, et al.. Inequalities in HIV disease management and progression in migrants from Latin America and sub-Saharan Africa living in Spain. HIV Med. 2013;14:273–283.
25. Camoni L, Raimondo M, Regine V, et al.. Late presenters among persons with a new HIV diagnosis in Italy, 2010-2011. BMC Public Health. 2013;13:281.
26. Helleberg M, Engsig FN, Kronborg G, et al.. Late presenters, repeated testing, and missed opportunities in a Danish nationwide HIV cohort. Scand J Infect Dis. 2012;44:282–288.
27. Zoufaly A, an der Heiden M, Marcus U, et al.. Late presentation for HIV diagnosis and care in Germany. HIV Med. 2012;13:172–181.
28. Chadborn TR, Delpech VC, Sabin CA, et al.. The late diagnosis and consequent short-term mortality of HIV-infected heterosexuals (England and Wales, 2000-2004). AIDS. 2006;20:2371–2379.
29. Prost A, Elford J, Imrie J, et al.. Social, behavioural, and intervention research among people of Sub-Saharan African origin living with HIV in the UK and Europe: literature review and recommendations for intervention. AIDS Behav. 2008;12:170–194.
30. Alvarez-del AD, Monge S, Caro-Murillo AM, et al.. HIV testing policies for migrants and ethnic minorities in EU/EFTA member states. Eur J Public Health. 2014;24:139–144.
31. IOM. International Organization for Migration. World Migratiion Report 2013. Migrant Well-Being and Development. Geneva, Switzerland: International Organization for Migration; 2013.
32. European Commission Eurostat. Demography report 2010. older, more numerous and diverse Europeans. Available at: http://epp.eurostat.ec.europa.eu/cache/ITY_OFFPUB/KE-ET-10-001/EN/KE-ET-10-001-EN.PDF. Accessed June 30, 2015.
33. IOM. International Organization for Migration. Migration and the Economic Crisis in the European Union: Implications for Policy. Available at: http://publications.iom.int/bookstore/free/Migration_and_the_Economic_Crisis.pdf. Accessed June 30, 2015.
34. O'Donnell C, Burns N, Dowrick C, et al.. Health-care access for migrants in Europe. Lancet. 2013;382:393–6736.
35. Royo-Bordonada MA, Diez-Cornell M, Llorente JM. Health-care access for migrants in Europe: the case of Spain. Lancet. 2013;382:393–394.
36. UNAIDS. Global update on HIV treatment 2013: results, impact and opportunities. Available at: www.unaids.org/en/media/unaids/contentssets/documents/unaidspublication/2013/20130630_treatmetn_report_en.pdf. Accessed June 30, 2015.
Keywords:

migration; HIV infection; late HIV presentation; Europe; trends

Supplemental Digital Content

Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.