Abstract

Background

Limited data exist on infectious diseases imported to various locations in Europe, particularly after travel within the continent.

Methods

To investigate travel‐related disease relevant to Europe that is potentially preventable through pre‐travel intervention, we analyzed the EuroTravNet database of 5,965 ill travelers reported by 16 centers in “Western” Europe in 2011.

Results

There were 54 cases of vaccine‐preventable disease, mostly hepatitis A (n = 16), typhoid fever (n = 11), and measles (n = 8); 6 cases (including 3 measles cases) were associated with travel within “Western” Europe. Malaria was the most commonly diagnosed infection (n = 482, 8.1% of all travel‐related morbidity). Among patients with malaria, the military most commonly received pre‐travel advice (95%), followed by travelers for missionary, volunteer, research, or aid work (81%) but travelers visiting friends and relatives (VFRs) were least likely to receive pre‐travel advice (21%). The vast majority (96%) of malaria patients were resident in “Western” Europe, but over half (56%) were born elsewhere. Other significant causes of morbidity, which could be reduced through advice and behavioral change, include Giardia (n = 221, 3.7%), dengue (n = 146, 2.4%), and schistosomiasis (n = 131, 2.2%). Of 206 (3.5%) travelers with exposure in “Western” Europe, 75% were tourists; the highest burden of disease was acute gastrointestinal infection (35% cases). Travel from “Eastern” Europe (n = 132, 2.2%) was largely associated with migration‐related travel (53%); among chronic infectious diseases, tuberculosis was frequently diagnosed (n = 20). Travelers VFRs contributed the largest group of malaria patients (46%), but also had the lowest documented rate of pre‐travel health advice in this subset (20%). Overall, 44% of nonimmigrant ill travelers did not receive pre‐travel advice.

Conclusion

There is a burden of infectious diseases in travelers attending European health centers that is potentially preventable through comprehensive pre‐travel advice, chemoprophylaxis, and vaccination. Targeted interventions for high‐risk groups such as travelers VFRs and migration‐associated travelers are of particular importance.

International travel, a major route for the propagation of infectious diseases, is increasing: total international tourism receipts exceeded US$1 trillion for the first time in 2011.1,2 The potential for importing infectious diseases into Europe is considerable, with over half of international travelers (51.3%, 504.0 million arrivals) in 2011 arriving at a European destination.3 Many of the commonly encountered infections among travelers to Europe would be largely preventable through pre‐travel interventions including vaccinations and advice for behavior modification. However, despite the threat of illness and public health concerns, pre‐travel interventions are frequently neglected.4,5

EuroTravNet is a collaborative network of clinicians working as part of the GeoSentinel Global Surveillance Network, a worldwide communication and data collection system for the surveillance of travel‐related morbidity.6 Sixteen EuroTravNet sites from nine European countries (France, Germany, Italy, the Netherlands, Norway, Spain, Sweden, Switzerland, and the UK) collect clinical and epidemiological information on ill returned travelers using the GeoSentinel technology platform.7 EuroTravNet has collected and published data annually since 2008.8,9,10 This report is an account of the infectious diseases reported in ill travelers in 2011, focusing on the disease burden that could be reduced through appropriate pre‐travel care. With increasing international travel within Europe, and the relative scarcity of data in this area, we also describe morbidity associated with travel to European destinations.

Methods

Detailed accounts of patient recruitment, inclusion criteria, geographical definitions, and limitations of the GeoSentinel system have been previously described.7 Key criteria for inclusion are that all patients must have (1) presented to medical services at a EuroTravNet site between January 1, 2011 and December 31, 2011; (2) crossed an international border prior to seeking medical attention; (3) either sought medical advice for a presumed travel‐related symptomatic illness or for screening for asymptomatic infection; and (4) have laboratory confirmation or strong clinical suspicion of an infection associated with recent travel.

Anonymized data were collected and entered into the standardized GeoSentinel electronic database at EuroTravNet sites that were part of the network as of December 31, 2011. Demographic information, including sex, age at presentation, birth country, residential country, and recent travel history was included. Reasons for travel were classified as tourism; business; missionary/volunteer/research/aid work (MVRA); student; immigration; military; medical tourism; or visiting friends and relatives (VFRs). Clinical syndromes were attributed from a list of 21 broad options. Diagnoses, based on the final diagnosis made by a clinician, were assigned codes from a standardized list of 556 possible diagnoses.6 Multiple diagnoses could be recorded for the same patient. Patients who had no clinical or laboratory evidence of disease were excluded from this analysis.

We have focused on preventable diseases, including those for which vaccines are widely recommended for travelers,11,12 particularly those against hepatitis A, hepatitis B, measles, mumps, pertussis, rubella, Salmonella Typhi, and varicella.

We calculated proportionate morbidity by comparing the number of cases of a specific presentation or diagnosis with all cases of ill returned travelers in the given time period. Significance tests are based on chi‐squared statistics, comparing the proportionate morbidity of one traveler subgroup with that of another subgroup. To calculate the proportion of cases that received pre‐travel advice, we excluded cases where a pre‐travel history was reported as “unknown.”

Results

In 2011, EuroTravNet sites collected data from 5,965 ill returned travelers. The main demographic features of this population are summarized in Table 1. Most patients are seen after travel, are resident in Europe, largely travel for tourism, and are seen in an outpatient setting.

Table 1

Key demographic information of ill returned travelers reported by EuroTravNet sites in 2011

 Number (%) 
Patients N = 5,965 
Female (n, %) 2,934 (49.2) 
Median age (min; max)    34 (0–91) 
Born in Europe (n, %) 4,462 (74.8) 
Residence in Europe (n, %) 5,787 (97.0) 
Reason for travel 
Tourism 2,894 (48.5) 
Immigration  791 (13.3) 
Visiting friends and relatives  778 (13.0) 
Missionary/volunteer/research/aid work  688 (11.5) 
Business  617 (10.3) 
Student 101 (1.7) 
Military  82 (1.4) 
Medical tourism  14 (0.2) 
Patient type 
Outpatient 4,917 (82.4)  
Additional information 
Seen during travel 200 (3.4) 
Seen after travel 4,974 (83.4)  
Immigration travel only  791 (13.3) 
 Number (%) 
Patients N = 5,965 
Female (n, %) 2,934 (49.2) 
Median age (min; max)    34 (0–91) 
Born in Europe (n, %) 4,462 (74.8) 
Residence in Europe (n, %) 5,787 (97.0) 
Reason for travel 
Tourism 2,894 (48.5) 
Immigration  791 (13.3) 
Visiting friends and relatives  778 (13.0) 
Missionary/volunteer/research/aid work  688 (11.5) 
Business  617 (10.3) 
Student 101 (1.7) 
Military  82 (1.4) 
Medical tourism  14 (0.2) 
Patient type 
Outpatient 4,917 (82.4)  
Additional information 
Seen during travel 200 (3.4) 
Seen after travel 4,974 (83.4)  
Immigration travel only  791 (13.3) 

Table 2 shows the proportion of travelers who obtained pre‐travel health advice, grouped by reason for travel. This rate was high in the military and MVRA travelers, in contrast to particularly low rates for travelers VFRs (p < 0.001). Overall, 1,759 (43%) of nonmigrant travelers reported that they did not obtain pre‐travel advice. The destinations where patients acquired their illnesses are summarized in Table 3.

Table 2

Reason for travel in relation to seeking pre‐travel advice for ill returned travelers (excluding migration‐related travel) reported by EuroTravNet sites in 2011

 Pre‐travel advice 
Travel reason Yes (N%* No (N%* Do not know (N
Business 272 55 227 45 118 
Medical tourism 27 73 
Military 69 93 
Missionary/volunteer/research/aid work 418 79 111 21 159 
Student 53 70 23 30 25 
Tourism 1,326 58 962 42 606 
Visiting friends and relatives 136 24 423 76 219 
Total 2,277 56 1,759 44 1,138 
 Pre‐travel advice 
Travel reason Yes (N%* No (N%* Do not know (N
Business 272 55 227 45 118 
Medical tourism 27 73 
Military 69 93 
Missionary/volunteer/research/aid work 418 79 111 21 159 
Student 53 70 23 30 25 
Tourism 1,326 58 962 42 606 
Visiting friends and relatives 136 24 423 76 219 
Total 2,277 56 1,759 44 1,138 
*

Percentage of (yes + no).

Table 3

Region of exposure for ill returned travelers reported by EuroTravNet sites in 2011

Region Number (%) 
Sub‐Saharan Africa 2,074 (34.8) 
North Africa  318 (5.3) 
Caribbean and Central America  298 (5.0) 
South America  579 (9.7) 
North America   29 (0.5) 
Middle East  141 (2.4) 
Northeast Asia   59 (1.0) 
South Central Asia   874 (14.7) 
Southeast Asia   947 (15.9) 
“Eastern” Europe  132 (2.2) 
“Western” Europe  206 (3.5) 
Australia/New Zealand/Oceania   28 (0.5) 
Not specified  259 (4.3) 
Total (%) 5,965 (100) 
Region Number (%) 
Sub‐Saharan Africa 2,074 (34.8) 
North Africa  318 (5.3) 
Caribbean and Central America  298 (5.0) 
South America  579 (9.7) 
North America   29 (0.5) 
Middle East  141 (2.4) 
Northeast Asia   59 (1.0) 
South Central Asia   874 (14.7) 
Southeast Asia   947 (15.9) 
“Eastern” Europe  132 (2.2) 
“Western” Europe  206 (3.5) 
Australia/New Zealand/Oceania   28 (0.5) 
Not specified  259 (4.3) 
Total (%) 5,965 (100) 

Of the 5,965 patients seen in EuroTravNet sites, 206 (3.5%) had traveled within “Western” Europe, contributing a total of 236 diagnoses (summarized in Table 4). The majority (75%) of these travelers were tourists.

Table 4

Common syndromes in patients presenting to EuroTravNet sites in 2011 following travel within Europe

 “Western” Europe “Eastern” Europe 
Syndrome group Number of patients Proportion (%)* Number of patients Proportion (%)* 
Acute diarrhea 71 35 22 17 
Dermatologic 36 18 15 11 
Respiratory 23 11 28 21 
Systemic febrile diseases 21 10 
Other gastrointestinal diagnoses 12 39 30 
Chronic diarrhea 
Genitourinary diagnoses 
Other 32 16 34 32 
 “Western” Europe “Eastern” Europe 
Syndrome group Number of patients Proportion (%)* Number of patients Proportion (%)* 
Acute diarrhea 71 35 22 17 
Dermatologic 36 18 15 11 
Respiratory 23 11 28 21 
Systemic febrile diseases 21 10 
Other gastrointestinal diagnoses 12 39 30 
Chronic diarrhea 
Genitourinary diagnoses 
Other 32 16 34 32 
*

The sum of each column is greater than 100%, as each patient can contribute multiple diagnoses.

In total, 132 cases (2% of all patients) traveled from “Eastern” Europe, contributing 174 diagnoses (summarized in Table 4). Over half (53%) were seen following migration to “Western” Europe, with other major travel reasons including tourism (18%), VFRs (17%), and business (6%).

Spectrum of Diseases

The number of cases and proportionate morbidity of selected diagnoses in the EuroTravNet dataset for 2011 is summarized in Table 5.

Table 5

Number of cases and proportional morbidity of selected diagnoses in all 5,965 EuroTravNet patients in 2011

Diagnosis Number (proportional morbidity, %) (N = 5,965) 
Malaria* 482 (8.1) 
Plasmodium falciparum malaria 338 (5.7) 
Plasmodium vivax malaria 86 (1.4) 
Plasmodium ovale malaria 28 (0.5) 
Plasmodium malariae malaria 13 (0.2) 
Dual infection 3 (0.0) 
Severe malaria 21 (0.4) 
Giardia 221 (3.7) 
Campylobacter 159 (2.7) 
Active tuberculosis (all cases) 177 (3.0) 
Pulmonary tuberculosis 96 (1.6) 
MDR‐/XDR‐TB 8 (0.1) 
Cutaneous larva migrans 154 (2.6) 
Dengue 146 (2.4) 
Schistosomiasis 131 (2.2) 
Cutaneous leishmaniasis 46 (0.8) 
Chikungunya 6 (0.1) 
Vaccine‐preventable diseases 54 (0.9) 
Hepatitis A 16 (0.3) 
Salmonella Typhi 11 (0.2) 
Measles 8 (0.1) 
Pertussis 5 (0.1) 
Rubella 5 (0.1) 
Varicella 4 (0.1) 
Hepatitis B 4 (0.1) 
Mumps 3 (0.0) 
Rabies post‐exposure prophylaxis 137 (2.3) 
Diagnosis Number (proportional morbidity, %) (N = 5,965) 
Malaria* 482 (8.1) 
Plasmodium falciparum malaria 338 (5.7) 
Plasmodium vivax malaria 86 (1.4) 
Plasmodium ovale malaria 28 (0.5) 
Plasmodium malariae malaria 13 (0.2) 
Dual infection 3 (0.0) 
Severe malaria 21 (0.4) 
Giardia 221 (3.7) 
Campylobacter 159 (2.7) 
Active tuberculosis (all cases) 177 (3.0) 
Pulmonary tuberculosis 96 (1.6) 
MDR‐/XDR‐TB 8 (0.1) 
Cutaneous larva migrans 154 (2.6) 
Dengue 146 (2.4) 
Schistosomiasis 131 (2.2) 
Cutaneous leishmaniasis 46 (0.8) 
Chikungunya 6 (0.1) 
Vaccine‐preventable diseases 54 (0.9) 
Hepatitis A 16 (0.3) 
Salmonella Typhi 11 (0.2) 
Measles 8 (0.1) 
Pertussis 5 (0.1) 
Rubella 5 (0.1) 
Varicella 4 (0.1) 
Hepatitis B 4 (0.1) 
Mumps 3 (0.0) 
Rabies post‐exposure prophylaxis 137 (2.3) 

N = total number of symptomatic patients presenting to EuroTravNet sites following episodes of travel; XDR‐TB = extensively drug‐resistant tuberculosis; MDR‐/XDR‐TB = multidrug resistant tuberculosis.

*

In some cases, species of malaria could not be identified.

Severe malaria was defined as per World Health Organization criteria.45

Vaccine‐Preventable Disease

Vaccine‐preventable diseases accounted for 54 cases (0.9%). The number of measles cases was eight, acquired in France (n = 3), Thailand (n = 2), Martinique, Senegal, and Uganda (n = 1 for each destination). All cases of measles, mumps, rubella, and pertussis were diagnosed in adults.

Tourists accounted for 26 (48%) cases, with travelers VFRs contributing 16 cases (the remainder were business travelers (n = 4), MVRA travelers (n = 4), immigrants (n = 2), medical tourists (n = 1), and students (n = 1)). The majority (47 patients, 87%) were over the age of 18, but only 8 (20%) had a documented pre‐travel encounter. With the exception of one student, all of the patients were resident in “Western” Europe, although 22% were born elsewhere.

Six cases of vaccine‐preventable disease were acquired in “Western” Europe: one case of acute hepatitis A in a tourist visiting Spain; one case of mumps in a 49‐year‐old tourist visiting Greece; one case of varicella infection in a 17‐year‐old Brazilian student studying in the UK; and three cases of measles in travelers visiting France, two for tourism and one for business. In none of these six patients was pre‐travel advice reported.

Parasitic Infections

A total of 482 (8.1%) ill returned travelers were diagnosed with malaria, 46% of whom were travelers VFRs. Among patients with malaria, the military most commonly received pre‐travel advice (95%), followed by travelers for MVRA (81%) but those VFRs were least likely to receive pre‐travel advice (21%). The vast majority (96%) of malaria patients were resident in “Western” Europe, but over half (56%) were born elsewhere.

Cutaneous leishmaniasis was reported in 46 cases, 11 of which could be attributed to military personnel working in French Guiana. Within “Western” Europe, four cases of cutaneous leishmaniasis were acquired in Spain.

Gastrointestinal Illness

In cases of acute diarrhea where an organism was identified, Giardia lamblia contributed the largest number with 221 cases. Other significant organisms include Campylobacter (159 cases), non‐typhi Salmonella (57 cases), and Shigella sp (49 cases).

Diarrhea and other gastrointestinal diagnoses were reported in 40% of ill travelers returning from “Western” Europe; where a pathogen was identified, Campylobacter was the leading cause of acute diarrhea.

Gastrointestinal illnesses were the second most commonly diagnosed group of diseases associated with travel to “Eastern” Europe, in particular chronic hepatitis C (18 cases, 16 in immigrants and 2 in travelers for business) and asymptomatic hepatitis B carriers (11 cases, all immigrants).

Respiratory Illness

The majority of the 177 active tuberculosis cases were related to migration travel (87%), while most of the remainder was reported in travelers VFRs (6%) and tourists (3%). HIV coinfection was reported in 12 cases (7%). The regions of exposure most commonly implicated were sub‐Saharan Africa (37%), South Central Asia (25%, in particular Pakistan and India) and Eastern Europe (13%). Multidrug resistant tuberculosis (MDR‐TB)/extensively drug‐resistant tuberculosis (XDR‐TB) was confirmed in eight cases, all migrant travelers.

Pulmonary tuberculosis was the most common diagnosis associated with travel from “Eastern” Europe, accounting for 20 cases, 5 of which were MDR‐ or XDR‐TB (2 cases from Lithuania, 1 from each of Estonia, Ukraine, and the Russian Federation). All but one of these cases was related to migration to “Western” Europe; the other was an infant VFR, resident in Italy but with citizenship in Moldova, where she was exposed to the disease.

Discussion

The spectrum of diagnoses reported here highlights the large number of ill returned travelers who suffer from potentially preventable infectious diseases. The strengths and weaknesses of GeoSentinel methods have been described elsewhere.7,13 Although we are unable to provide true incidence and prevalence of diseases, EuroTravNet is able to illustrate the proportionate morbidity in ill travelers presenting to secondary care centers. This may exclude a range of conditions for which patients present to primary care or during their episode of travel, such as acute gastroenteritis, or noncommunicable disorders such as injuries and altitude sickness.14 As a result, this may disproportionally underestimate the burden of disease from nontropical areas, including travel within Europe. Nevertheless, we are able to report data from a large number of travelers, offering a broad insight into the disease burden presenting to a range of specialist centers across “Western” Europe.

Vaccine‐preventable infections represent a proportionally small, but nevertheless important, disease burden. The majority of cases reported had not sought pre‐travel advice; an important minority acquired such diseases despite pre‐travel consultations, including cases of hepatitis A, measles, and rubella for which effective vaccines are routinely advised.15

All infections for which effective childhood immunizations are recommended (ie, measles, mumps, rubella, and pertussis) were reported in adults aged between 20 and 60, half of whom were tourists. This exclusively adult subset may reflect the referral process in many EuroTravNet sites, where children would likely be seen by pediatricians working in separate departments and may therefore not be reported to GeoSentinel.

We report eight cases of measles in 2011, compared to 2 of 6,315 patients in 2010, 3 of 5,415 patients in 2009, and 2 of 5,901 patients in 2008,8,9,10 which is in keeping with a global rise in cases.16 Although the vaccination status of individuals is not recorded in GeoSentinel, it may be important to note that some childhood immunizations, in particular pertussis, do not provide immunity into adulthood.17 A pre‐travel consultation provides an opportunity to check vaccination status, especially in the context of waning immunity. In one study, between 30 and 70% of all people attending a pre‐travel clinic required at least one routine vaccine.18 We suggest that the pre‐travel consultation is an excellent opportunity for reviewing and updating routine vaccinations.

This study also highlights the importance of destination‐specific vaccinations, in particular hepatitis A and Salmonella Typhi. Despite a fall in the number of cases in returning travelers globally,19,20 the burden of disease demonstrated here and the potential for outbreaks in naive populations supports the ongoing use of both vaccines for travel to certain countries. In addition, 137 patients were seen for rabies postexposure prophylaxis; progression of the disease is largely preventable with the administration of pre‐ and postexposure vaccination.21 It is important to consult up‐to‐date guidelines for destination‐specific vaccination,11,12 especially with the changing global distribution of vaccine‐preventable disease as demonstrated by the recent outbreak of yellow fever in Sudan.22

This study is likely to reflect a gross underestimate of all vaccine‐preventable infections, many of which will manifest during travel or will cause patients to present to primary care. Further studies in representative primary care facilities are required to understand the true extent of this problem. Other vaccine‐preventable infections that are not discussed here, such as Streptococcus pneumoniae and influenza, may influence the pattern of travel‐associated disease.23,24 Encouraging attendance at a pre‐travel clinic for a comprehensive vaccination review is therefore of great public health importance.

Malaria continues to represent a significant proportion of all morbidity reported from EuroTravNet sites, despite being largely preventable.25,26 In keeping with previous studies, the largest subset of malaria patients were VFRs,27,28 a group particularly at risk of travel‐related diseases but who are less likely to seek pre‐travel advice or take antimalarial prophylaxis.29 Providing appropriate pre‐travel services for VFR travelers is challenging27 but new approaches to this problem have been reported, including culturally sensitive media campaigns targeted at high‐risk communities.30

Military travelers accounted for 8.5% of malaria cases, a group where pre‐travel consultations should be routine. However, inadequate use of chemoprophylaxis and personal protection measures has previously been documented in military personnel, associated with malaria outbreaks.31,32 Effective education of this high‐risk group is therefore of ongoing importance.

The high proportionate morbidity of malaria and dengue reported here is of particular concern, given the potential for autochthonous transmission in some areas of Europe.33,34,35

The importance of monitoring such diseases and their vectors is reflected in international surveillance systems,36,37 but should be complemented by public health interventions targeting high‐risk travelers and reducing the risk of ongoing transmission.34

Gastrointestinal and helminth disease cause significant morbidity in visitors to developing countries. Risk factors for acquiring these infections are well established and basic advice to travelers may prevent a proportion of diarrheal and helminth disease.38,39

Morbidity in ill travelers exposed in “Western” Europe (in particular, diarrheal and vaccine‐preventable disease) is potentially reducible with basic pre‐travel advice among this predominantly tourist group. By contrast, the majority of clinical episodes following travel from “Eastern” Europe were associated with migration and display a different spectrum of disease, in particular chronic infections such as tuberculosis and hepatitis B and C. Providing prompt access to screening and treatment for this group is important for optimum management of these conditions and to prevent their spread. For example, recent studies have suggested that targeted screening for latent tuberculosis40 and hepatitis B play an important public health role in countries receiving migrant travelers and long‐term visitors.41

Reducing the risk of infection and the subsequent transmission of organisms has important implications for the health of both travelers and the populations to which they return. Our study shows that, among ill returned travelers, the pre‐travel consultation is potentially underused, especially by high‐risk groups such as travelers VFRs. Although the practice of travel medicine in Europe is not standardized,42 pre‐travel health advice and vaccination can be effective in preventing disease43 and can be cost‐effective.44

Conclusion

We have demonstrated a burden of infectious diseases in ill returned travelers that is potentially preventable, highlighting the importance of thorough pre‐travel consultations pertinent to destination. Efforts should be made to target groups that are at high risk of travel‐related infections, including travelers VFRs and military personnel. This has important implications when organizing and providing travel medicine services. We have demonstrated the high burden of chronic infections such as TB and HBV in migrants who travel from high‐prevalence areas, supporting targeted screening for these groups. Finally, we have also shown that international travel within Europe is itself associated with a notable burden of disease.

We are grateful to D. Freedman for helpful comments. In addition to the authors, members of the EuroTravNet/GeoSentinel Networks, who contributed data are S. Odolini, M. van Vugt, P.P.A.M. van Thiel, A. Goorhuis, C. Stijnis, B. Goorhuis, F. Simon, H. Savini. EuroTravNet (http://www.eurotravnet.eu) is the European Centre for Disease Prevention and Control corresponding network for tropical and travel medicine, funded through the public tenders OJ/2008/07/08‐PROC/2008/019 and OJ/2010/ 03/16‐PROC/2010/011. It has been created by grouping the European sites of GeoSentinel (http://www.geosentinel.org), the Global Surveillance Network of the International Society of Travel Medicine, supported by Cooperative Agreement U50 CI000359 from the US CDC. EuroTravNet is supported by the Mediterranée Infection foundation. Cambridge receives support for the EuroTravNet GeoSentinel activities from the Cambridge Biomedical Research Centre.

Declaration of Interests

The authors state they have no conflicts of interest to declare.

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The EuroTravNet countries by region are available from the corresponding author on request (http://www.eurotravnet.eu).