Establishing a high level of vaccination coverage is high on the agenda of the European Vaccine Action Plan 2015-20 (WHO Europe, 2015b), through which all EU Member States have committed to eliminating measles. Measles is a highly contagious vaccine-preventable disease that still forms a major cause of severe disability and childhood death (Simons et al., 2012). Despite the availability of an effective and inexpensive vaccine since the 1960s, measles caused roughly 140,000 deaths globally in 2010 (Simons et al., 2012). In the World Health Organization (WHO) European region, a significant decline in reported measles cases has occurred over the last two decades, with incidence rates declining from 304.184 in 1991, to 67.759 in 2001, and 8.617 in 2009 (WHO Europe, 2019). Although this shows a significant reduction, the goal of eradicating endemic measles cases in the WHO European region by 2010 for a period of at least twelve months (WHO Europe, 2014), was not met, and the number of measles cases in recent years has started to increase (WHO Europe, 2019). The process of measles elimination has been hindered as more children are either not immunised on time or are not immunised at all. Insufficient vaccination coverage often occurs in risk groups such as minorities (i.e. Irish travellers, the Roma, and orthodox religious communities). This results in pockets or clusters of unvaccinated people who contribute to the spread of the disease to other parts of the population and reduces overall population coverage that is required for elimination (Steffens, Martin, and Lopalco, 2010).
Migrants form another group that is thought to be at higher risk of measles due to suboptimal coverage rates. In 2016, WHO–UNHCR–UNICEF stated that migrants, asylum seekers, and refugees should be provided with equitable and non-discriminatory access to vaccinations. The international organisations recommended to vaccinate migrants in accordance with the vaccination schedule of the Member State, and to provide migrants with documents or registers of the vaccinations administered to avoid duplications (WHO Europe, 2015a). Although migration itself is not a risk factor for health – migrants are often comparatively healthy, a phenomenon explained by the ‘healthy migrant effect’ (Razum, 2006) – a few studies found that particular groups of migrants in Europe are more vulnerable to infectious diseases than the majority population (Gushulak et al., 2010; Wörmann & Krämer, 2011) and recent outbreaks of measles have been reported in migrant population in Europe (Mipatrini et al. 2017). However, substantial knowledge on the extent to which migrants in EU Member States are affected by measles currently remains limited.
The challenge for comparing of migrant health across Europe is in part due to the presence of undocumented migrants. Therefore, the true size of migrant populations is often unknown and data may be misleading (WHO Europe, 2010). Furthermore, the information collected is affected by the lack of a universally agreed definition of who constitutes a migrant. Definitions and classifications are determined by national policy, legislative, and administrative needs (Ingleby, 2009). Therefore, countries may define migrants in various ways, e.g. by their citizenship, country of birth, residency, or duration of stay (IOM, 2010; Rechel, Mladovsky, & Devillé, 2012). As a result, the overall quality of the data collected still varies highly between countries. In the EU region, measles is a notifiable disease in all Member States. Surveillance data is collected by the European Centre for Disease Prevention and Control (ECDC) (ECDC, 2019). Despite the efforts that have been made to harmonise the collection of surveillance data on migrant-specific classifications for measles cases, such as whether a case is endemic or imported, in most Member States this information is inadequately reported.
Measuring and meeting the health needs of migrants affected by vaccine-preventable diseases is becoming increasingly important, with the proportion of migrants in Europe at unprecedented levels (Rechel et al., 2013). In 2017, the number of international migrants worldwide reached 258 million, which is the highest ever recorded and represented over 3% of the world population (Migration data portal, 2018). During 2017 alone, a total of 4.4 million people immigrated to one of the EU-28 Member States, including 2.4 million immigrants from non-Member countries (EUROSTAT, 2019). Over 65 million people were displaced by force during 2015, with more than half originating from three war-torn countries: the Syrian Arab Republic, Afghanistan, and Somalia, which represented the highest forced displacement globally since the aftermath of World War II (UNHCR, 2015). However, in contrast to the prior population movements that unfolded in Europe, the current influx consists of a highly heterogeneous population of third country nationals with varied migration motives, ethnical, cultural, and social backgrounds, and legal status individuals may have on arrival (i.e., refugees, migrants, asylum seekers, and undocumented migrants) (Puchner et al. 2018).
As Europe’s population diversifies, new challenges for health systems are inevitably created (Kalengayi et al., 2012; Rechel et al., 2013). If the goal of eliminating measles is to be met, it is necessary to target the groups at risk of remaining unvaccinated with specific health information and disease prevention campaigns (ECDC, 2012). At present, the lack of data makes it difficult to determine if migrant populations are at higher risk of contracting measles. In light of these gaps in evidence, this paper aims to provide an overview of the burden of measles in migrants in the EU/EEA and to give an assessment of the quality, completeness, and comparability of data. Evidence was collected through a literature review.
To review the immunisation rates and the burden of disease of measles among migrants in Europe, a literature review was carried out. Studies were identified by searching the online database PubMed. The search was conducted in April 2019. The following search strategy was adopted:
Measles[Title/Abstract] AND (vaccin*[Title/Abstract] OR varicella[Title/Abstract]) AND (migrant*[Title/Abstract] OR asylum seeker*[Title/Abstract]OR refugee*[Title/Abstract]) AND (EU[Title/Abstract] OR Europe[Title/Abstract])
The process resulted in several studies identified after the search were screened on the basis of abstract and reference lists were screened in order to identify more relevant literature. Only studies published in English after 2006 were included, as it was beyond the scope of this review to cover more languages and older literature. On the basis of study design and sample size, no exclusion criteria were selected. All studies that were identified providing information on the incidence of measles cases/antibodies, measles immunisation coverage, and outbreaks of measles among migrants in Europe were included. Related websites, such as the WHO, the World Health Organization, Regional Office for Europe (WHO-EURO), ECDC, and Global migration group, International Organization for Migration (IOM) were also searched for additional data.
Reported measles cases have been linked to communities with low vaccination coverage in some EU countries (WHO Regional Office for Europe, 2009). Unfortunately, data on immunisation rates in migrant populations is limited and not routinely collected. Additionally, migrants are more likely to not be registered in national healthcare systems than the majority population. However, data on the motivation and numbers of non-immunisation are of high importance as Muscat (2011) recorded that in 2005-09 most measles cases in Europe were reported in unvaccinated people, with outbreaks facilitated by pockets of low vaccine and susceptible individuals (Curtale et al. 2010).
A couple of studies that investigated immunisation rates in individuals, while also clearly identifying migrants by country of birth, were identified. Most studies reported lower vaccination coverage against measles in migrant populations compared to the majority population in the study. A German study used data from the German Health Interview and Examination Survey for Children and Adolescents (KiGGS) and reported that in vaccinated children, migrant status was linked to a higher level of susceptibility to measles (Poethko-Müller & Mankertz, 2011). A further analysis of the same dataset found that children born outside of Germany had a higher chance of lacking protection against measles, while children born in Germany but with a migration background were more often vaccinated to measles than their German peers (Poethko-Müller & Mankertz, 2012). In contrast, however, another German study from a rural region in Bavaria, where socio-demographic information, including variables related to migration background, were assessed, found no difference in vaccination coverage between non-migrant and migrant children (Mikolajczyk et al. 2008).
A study in Catalonia, Spain, reported a statistically significant difference in immunisation rates as primary vaccination rates covered 96.5% of indigenous children and only 85% in migrant children (Borràs et al. 2007). A study conducted in Italy found that the measles vaccination rate in migrant children (identified as born outside of Italy or with parents born outside of Italy) was 87,3% compared to national data which reported 89,6% (Chiaradia et al. 2011). However, it was not clarified if the stated difference was statistically significant. A Belgian study identified migrants as having one or both parents or one or more grandparents born abroad (Vandermeulen et al. 2008). The study reported that lower measles vaccination coverage was noted in adolescents with a non-European background and in primary schoolchildren with a European (but non-Belgian) background. In Denmark, Nakken (2018) retrospectively researched the Danish Red Cross database for children with active asylum applications. Accordingly, 2.126 asylum-seeking children were identified who represented a total of 8 nationalities, 293 (14%) of whom were identified in need of measles vaccination, leaving 86% immunised for measles in accordance with Danish national guidelines.
Three European studies were identified that investigated the susceptibility to measles among migrants and refugees by measuring the seroprevalence of the measles virus among migrant populations. Seroprevalence studies conduct blood tests to determine whether a person is immune for the disease tested, indicating the individual has not been vaccinated when no antibodies are found. According to these studies, the prevalence of seronegativity for measles among migrants was estimated between 6 and 13% (Gétaz et al. 2011; Jablonka et al. 2017; Takla et al. 2012).
Measles is not only a vaccine preventable disease, it is also somewhat of a predictable disease since it is one of the highest infectious diseases (Lopalco & Martin, 2010). Outbreaks are to be expected as soon as vaccine coverage levels are found to be below the recommended 95% for a definite period of time as pockets of vulnerable groups are left unprotected. The biggest challenge that occurs when reviewing studies that examined measles cases within migrant populations in Europe is that papers which mention migrants frequently merged them with native ethnic or religious groups. Hence, many studies do not specify the extent to which and whether the reported measles cases cover the aforementioned definition of migrants.
The most recent widely accepted definition of who constitutes a migrant was provided by the International Organisation for Migration (IOM) (IOM, 2019). The IOM defined migrants as “any person who is moving or has moved across an international border or within a State away from his or her habitual place of residence, regardless of (1) the person’s legal status; (2) whether the movement is voluntary or involuntary; (3) what the causes for the movement are; or (4) what the length of the stay is.” Some studies did make a distinction between ‘imported’ and other cases but did not verify whether these imported cases were originating from endemic individuals who returned infected after travelling abroad or not. Therefore, meaningful information on the burden of disease of measles within migrant populations was difficult to identify.
This difficulty was demonstrated in one of the larger studies which used surveillance data (Muscat et al. 2009). Muscat examined data from 32 European countries between 2006 and 2007. For the 2 years of the study, 12.132 cases of measles were recorded with most cases (n=10.329; 85%) originating from five countries: Germany, Romania, UK, Italy, and Switzerland, the last of which is not a EU Member State but does apply to the Schengen Area. The measles cases were predominantly seen in unvaccinated or incompletely or ill-timed vaccinated children. A total of 210 cases were reported as being ‘imported’, 117 (56%) of which came from another country within Europe and 43 (20%) from Asia. The same researcher investigated the presence of measles outbreaks in 2005–09 among indigenous populations, such as Travellers, the Roma and Sinti, and ultra-orthodox Jewish communities, but provided little information on migrant populations specifically (Muscat, 2011).
The same difficulty appears in case studies of measles outbreaks: many papers mention migrants as part of other (often indigenous) minorities. Accordingly, a French outbreak in 2008–10 was reported to have particularly affected socially vulnerable communities such as Roma communities and itinerant minorities (‘gens du voyage’) (Parent du Châtelet et al. 2010). However, it was unclear if these were either migrant populations, non-migrant nomadic groups, or both. In Ireland, a study on a measles outbreak in 2009–10 found that nearly two-thirds of the cases were reported in unvaccinated individuals. A substantial number of them were linked to the Traveller community, identified as “an indigenous minority group many of whom maintain a nomadic way of life”, with some cases also reported among “others citizens from Eastern Europe” (Gee et al. 2010). Curtale (2010) reported on two Italian measles outbreaks which occurred in 2006 and 2007 and disproportionately affected the local Roma/Sinti community after unvaccinated children of a Romanian Roma/Sinti family presumably imported a new serotype of measles virus. Correspondingly, an epidemiological study on a 2008 German measles outbreak stated that a new strain of measles virus was spread from London through Hamburg and eventually to Bulgaria, with the importation of the virus being predominantly but not exclusively associated with travel by individuals of the Roma community (Mankertz et al. 2011). Supplementary information was given in a case study of a measles outbreak in Greece in 2010, which found the Roma ethnic group to bear an excessively high caseload, also reporting that the Roma people came from both Bulgaria and Greece (Pervanidou et al. 2010).
Only two case studies on measles outbreaks were identified that made a clear distinction in measles cases among migrants. Vianio (2011) reported on a Norwegian outbreak in 2011 and stated that 8 out of a total of 10 cases were identified within the Somali immigrant community in Oslo. Secondly, in a refugee camp in Calais, France, during an outbreak in early 2016 measles were diagnosed in 10 migrants, 2 healthcare workers, and 1 volunteer (Jones et al. 2016). After the outbreak, a large scale vaccination campaign was conducted in the settlement, eventually covering 60% of the estimated 3.500 migrants.
A major barrier in the progress towards high and comparable vaccination coverage rates among migrants is that there is no general measles immunisation policy for European immigrants (Bica & Clemens, 2018). Local and national policies vary widely from no policy at all, to vaccination of all migrants, or vaccination of selected population groups based on serum antibody analysis or vaccination history.
Furthermore, even with a unified vaccination policy in place, full access for migrants to the vaccination schedule through follow-up vaccinations is challenging to guarantee. In many countries, children in socioeconomically disadvantaged families and ethnic minorities, both of which might include migrants, are less likely to be vaccinated (Peña-Rey et al. 2009). A French study also reported that having parents who are not fluent in the local language results in significant delays in vaccination uptake among children (Bouhamam et al. 2012). Mipatrini (2017) identified several difficulties healthcare systems are faced with when aiming for higher immunisation coverage among migrant populations. First, many vaccines must be given at regular pre-scheduled time intervals in consecutive doses; however, migrants are moving all over European countries. Secondly, there is often little or no information available on the immunisation status of migrant populations since there is a lack of systematic data collection covering incidence and vaccination rates of measles in European countries. Additionally, there is a lack of harmonised indicators among the various European countries. Thirdly, Screening services for vaccination are not always provided or accessible to migrants and or often not centred on migrants’ needs. Furthermore, migrants often refuse registration by the hosting medical authorities and vaccination as they fear the presence of legal consequences. Finally, the lack of coordination among public health authorities of neighbouring countries may determine either duplications or lack of vaccine administration.
Additionally, information on the incidence of measles cases among migrant populations in the EU is hard to identify, as data is not routinely collected or do not record migrant-specific variables such as country of birth, but instead only state the importation status of cases. This does not provide an optimal definition for migration, as it only gives an indication of travelling in the days before the onset of the disease. Likewise, many identified studies focused on minorities that are thought to be more susceptible to measles, such as the Roma communities, which may or may not include migrants.
This literature review conceded important findings in relation to the burden of measles in migrant populations. Several studies did report migrant children being less likely to be vaccinated than their indigenous peers and some measles outbreaks were associated with sub-optimal vaccination coverage in migrant populations. A renewed European focus is needed to improve methods to identify population groups with low immunisation coverage and to develop clear-cut strategies to target susceptible groups. An improvement in health service delivery may be needed to facilitate and reach equitable access to measles vaccines for all, including migrants. EU policymakers, healthcare workers, and researchers have a responsibility to ensure European healthcare systems develop and adapt to an increasingly mobile and globalising world.