Figure 1

Figure 1. Risks related to chikungunya infections among EU travelers, 2012–2018. Countries with infection and reporting countries are indicated. Map produced on January 8, 2020. Administrative boundaries were obtained from EuroGeographics and the...

We identified 13 reporting countries and 59 countries of infection (Figure 1). During 2012–2018, a total of 146 million travelers arrived in reporting countries from countries of infection (Appendix Table). Most of these travelers arrived from Southeast Asia (27%), southern Asia (19%), and the Caribbean (15%). More specifically, 12% arrived from India, 12% from Thailand, and 8% from Brazil. The United Kingdom (31%), France (22%), and Germany (16%) received the highest number of travelers.

Travelers from the Caribbean (41%) and Polynesia (74%) arrived primarily in France. Travelers from South (32%) and Central (29%) America arrived mainly in Spain. Travelers from Southeast (32%) and southern (55%) Asia and from eastern Africa (44%) arrived primarily in the United Kingdom.

The overall yearly number of travelers increased during 2012–2018 from 18 million to 24 million. The highest increases in travelers during that period were for Northern Africa (88%), Central America (71%), and the Caribbean (54%). There were also large annual variations in number of travelers returning from specific countries of infection. For instance, the number of travelers from Venezuela decreased by 58% during 2013–2015 largely because of domestic insecurity and political crisis.

The number of EU travelers exhibited a seasonal pattern with peaks related to holiday periods (January, March, and August). Peak periods varied among reporting countries: March and August for France; January and March for Germany; July–September for Spain; January for Sweden; and January, April, and August for the United Kingdom.

Risk for Infection among Travelers

During 2012–2018, there were 2,616 travel-related chikungunya cases, among which 1,766 were confirmed cases and 850 were probable cases (Table 1). France (918), the United Kingdom (593), Spain (587), and Germany (359) reported 94% of the cases. Although most reporting countries reported mostly confirmed cases, 60% of the cases reported by France and 31% of the cases reported by the United Kingdom were confirmed. The global TIR was 1.8 cases/100,000 travelers (Appendix Table).

Figure 2

Figure 2. Number of travel-related chikungunya cases during 2012–2018, by region of infection and year.

The number of cases and global TIR fluctuated over the study period (Table 1; Figure 2; Appendix Table); both values peaked in 2014. There was a seasonal increase in cases during May–September, with a peak in May–June for Spain, May–August for France, September–November for Germany, and October–November for the United Kingdom. The global TIR was highest in May, June, and July. The median age of travel-related case-patients was 43 years (interquartile range 32–55 years), and the female-to-male ratio was 1.4:1.

Figure 3

Figure 3. Rates of chikungunya infections among European travelers by country, region of infection, and epidemiologic period, 2012–2018. Shown are the 30 countries with the highest rates of infection for each period. A)...

Figure 4

Figure 4. Rates of chikungunya infections among European Union travelers by region of infection and year, 2012–2018.

Figure 5

Figure 5. Rates of chikungunya infections among European Union travelers returning from countries of infection, by reporting country and epidemiologic periods, 2012–2018. Only countries reporting the highest number of cases were included.

We observed 3 successive epidemiologic periods (Figures 2,3,4,5). The first phase, 2012–2013, had few cases, most (84%) associated with southern and Southeast Asia; the global TIR was 0.2. In November 2013, one case was associated with the Caribbean, marking the start of epidemics in the Americas (17).

The second phase, 2014–2015, corresponded to the globalization of virus circulation; the global TIR was 4.8. Most cases were associated with the Caribbean (68%) and South America (17%). In 2014, the TIR for travelers from the Caribbean reached 45.9; in 2015 it decreased in travelers from the Caribbean (1.6), but it increased for travelers from South America (6.3) and Central America (6.1). In 2014, there was a high TIR for travelers returning from Haiti (266.6) and Dominica (193.6), and during 2015, a high TIR was associated with Honduras (78.1) and Nicaragua (76.5).

During the 2014–2015 phase, a high TIR was associated with Polynesia (36.8), which matched the intense epidemic in the region; in French Polynesia for instance, a few months after introduction of the virus, 25% of the population had been affected (18). In Africa, high TIRs were observed in travelers returning from Angola (12.0) during 2014 and Equatorial Guinea (9.2) during 2015. During that phase, travelers arriving in France and Spain had the highest TIRs: 9.5 for France and 9.8 for Spain.

The third phase, 2016–2018, was marked by a decrease in the global TIR. During that phase, a large percentage of case-patients were returning from southern Asia (45%) and South America (24%); regional TIRs were 2.1 for southern Asia and 1.4 for South America. During 2016, there were high TIRs for travelers returning from Bolivia (21.4) and Nicaragua (18.2). In Africa, high TIRs were seen for travelers from Somalia during 2016 (68.3) and Kenya during 2018 (6.6); a large epidemic affected Mombasa County in Kenya during 2018 (19). During 2016–2018, travelers arriving in Germany, Spain, Sweden, and the United Kingdom had TIRs ranging from 1.0 to 2.1, and travelers arriving in France had a TIR of 0.5.

We documented factors associated with increased travel-associated chikungunya cases reported in the EU during 2012–2018. Travel patterns (i.e., volume of travelers, country visited, and period of travel) were specific to each of the reporting countries. These patterns also reflect the geopolitical context, historical and cultural links, and preferences of travelers.

The TIR fluctuated according to the region/country visited, the reporting country, and the period of travel. The difference in TIR and seasonality among reporting countries was likely caused by difference in places visited within the countries of infection, intensity of virus circulation at the time of the visit, and reason for travel (e.g., business versus holidays). Generally, we observed a much higher TIR for travelers visiting a country with historical links to the reporting country (i.e., travelers from Spain visiting countries in Central America or travelers from France visiting French Overseas Countries and Territories). This finding might be explained by a high number of travelers visiting friends or relatives (VFR travelers). These travelers are less likely to receive pretravel advice than other types of travelers (21), might stay longer in the visited country, and might use fewer protective measures. Therefore, EU countries should consider issuing their own specific travel advice on the basis of countries most visited and those that have a higher risk for infection for their citizens. Prevention campaigns could be strengthened before and during peaks of cases and TIR, and be tailored to at-risk populations (e.g., VFR travelers). To reach these populations, travel advice could be provided online when flight tickets are purchased or through social media.

A high number of cases or high TIR might also highlight a sensitive surveillance system. This suggestion explains a slightly higher TIR among travelers from Sweden compared with other travelers during the 2012–2013 and 2016–2018 phases. With an overall number of travelers that is relatively low and a sensitive surveillance system, Sweden was able to test most possible case-patients and therefore detect a high proportion of cases among travelers.

As highlighted in other reports (22,23), travel-related cases are good indicators of the epidemiologic situation of the country visited because outbreaks are reflected by an increase in travel-related cases. Our results accurately highlighted the spread of the virus throughout the Americas, Polynesia, and eastern Africa. Therefore, travelers can be considered as sentinels, particularly in countries in which disease surveillance is limited (e.g., Somalia).

If there are few travelers, the likelihood of observing cases is limited. Therefore, having no cases associated with a specific country does not necessarily mean that no virus is circulating. It is useful to consider traveler data, and TIR provides a more accurate estimation of the risk for infection for travelers.

The higher proportion of female case-patients could be explained by the fact that women are at higher risk for development of severe symptoms and are therefore are more likely to seek medical attention (24). In addition, more female travelers might be exposed. For instance, in Spain, 61% of the travel-related cases were VFR travelers (25); those travelers are expected to be persons who emigrated to Spain from disease-endemic countries, mostly from the Americas. A high proportion of persons born in Central America/Caribbean (64.5%) and South America (55.6%) and living in Spain are women (26). Therefore, we might consider that more female travelers were going to the Americas as VFR travelers and became infected during that visit.

The number of cases and TIR do not seem to correlate with the likelihood of occurrence of autochthonous outbreaks in reporting countries and the origin of the imported outbreak strain. We found no autochthonous outbreaks associated with epidemics in the Americas during 2014–2015. In contrast, we found 2 autochthonous outbreaks during 2017 despite the relatively lower number of imported cases than in previous years. The autochthonous outbreaks that occurred in the EU were not consistently associated with regions/countries of infections with most cases or high TIRs. In addition, although we estimated that pressure of introduction in receptive areas in Spain was higher than that for those in Italy, no outbreaks were reported in Spain. Also, outbreaks have not occurred in years that had higher pressure of introduction. Many other factors account for allowing an autochthonous outbreak, including activity and abundance of the vector, environmental factors, adaptation of the virus strain to the local vector, surveillance sensitivity, and timeliness of control measures implemented for imported cases (27–29). Consequently, although monitoring of outbreaks worldwide is relevant for estimating the risk for infection to travelers, this monitoring does not seem to be as relevant for estimation of the risk for secondary transmission.

In the absence of valid data on vector competence of local Ae. Albopictus mosquito populations and the particular chikungunya virus strain, each imported case should be considered as a potential index case. Control measures should then be implemented for the case to limit the likelihood of virus and disease spread.

In the context of the global climatic and ecologic changes, it is expected that Ae. albopictus mosquitoes will colonize new areas of the EU, thus creating new areas at risk for local transmission (30,31). Furthermore, the Ae. aegypti mosquito, another competent vector, is threatening to establish itself on the continent, increasing even more the risk for local transmission (32).

Surveillance systems in EU countries are diverse and have evolved over time (e.g., chikungunya became a mandatory reportable disease in Spain during 2014). Detailed information about national surveillance systems is available in the ECDC annual epidemiologic reports (33). Large outbreaks worldwide increased awareness among physicians, potentially enhancing testing of potential cases. Consequently, comparisons between years and between reporting countries should be made cautiously.

Vector presence and activity in countries of infection vary at the local level, whereas we analyzed country level data. We did not have information about the reason for travel (e.g., tourism, business, VFR) and length of stay, 2 variables that are likely to influence the risk for infection (34,35). This limitation prevented us from identifying recommendations at the subnational level and targeted to the travelers categories.

The reported travel-related cases only represent a fraction of the actual infections because <25% of infected persons remain asymptomatic (36). In parallel, 34% of cases were probable cases, diagnosed with 1 IgM test, a highly unspecific test that leads to a high number of false-positive results and, in some instances, indicates a previous infection (15,16,37,38). These biases were likely to be constant over time and place and therefore did not affect interpretation of our results.

We considered that all reported case-patients had viremia while in the EU and therefore could have contributed to secondary transmission. However, a study published in 2007 estimated that 63% of infected travelers were viremic upon return to their home country (39), which would suggest that we overestimated the number of potential index cases.

Several studies that assessed risk for travelers related to chikungunya and dengue used travelers data from the United Nation World Tourism Organization (22,40) or national databases 41,42). As highlighted in another report (43), there are major differences in the number of travelers between databases. The International Air Transport Association collects the number of flight passengers from 1 departure airport to an arrival airport, whereas other databases also include multicountry journeys and other types of travel mode, such as cruise ships; in addition, some databases might count travelers on the basis of their nationality instead of place of departure. We compared our results with those of 1 study that assessed the risk for chikungunya infection among travelers from Spain during 2008–2014 (22). Although results from the 2 studies are not in disagreement, they are not directly comparable. We believe that main difference in methods was that we used travelers data adjusted per year (except for 2018) and that the authors of the other study used mean annual number of travelers from previous years. If one considers major variations in number of travelers per year (e.g., Venezuela), we recommend researchers to used yearly number of travelers to estimate TIR. This recommendation emphasizes that comparison of TIRs between studies should be made with caution.

In conclusion, monitoring the number of travel-related chikungunya cases and the TIR among travelers can support travel advice. However, our results showed no indication that these factors can be useful in estimating the risk for autochthonous outbreaks in EU countries.