Travelers who visited friends or relatives were more likely to receive a diagnosis of malaria or viral hepatitis than those who traveled for other reasons.
We evaluated the epidemiologic factors of patients seeking treatment for travel-associated illness from January 2004 through May 2005 at the University Hospital of Zurich. When comparing persons whose purpose of travel was visiting friends and relatives (VFR travelers; n = 121) with tourists and other travelers (n = 217), VFR travelers showed a distinct infectious disease and risk spectrum. VFR travelers were more likely to receive a diagnosis of malaria (adjusted odds ratio [OR] = 2.9, 95% confidence interval [CI] 1.2–7.3) or viral hepatitis (OR = 3.1, 95% CI 1.1–9) compared with other travelers but were less likely to seek pre-travel advice (20% vs. 67%, p = 0.0001). However, proportionate rates of acute diarrhea were lower in VFR (173 vs. 364 per 1,000 ill returnees). Travel to sub-Saharan Africa contributed most to malaria in VFR travelers. In countries with large migrant populations, improved public health strategies are needed to reach VFR travelers.
More than 800 million tourist arrivals were registered worldwide in 2005, and an estimated 2% of the world’s population lives outside the country of birth (
A recent review of a global surveillance network’s data set showed different demographic characteristics and different types of travel-related illnesses among immigrant-VFR, traveler-VFR, and tourist travelers (
The University Hospital of Zürich serves a large proportion of the city’s population, which includes a multiethnic range of patients and immigrants. The outpatient departments treat ≈120,000 patients each year, and the inpatient departments treat >35,000. We evaluated the epidemiology of imported infectious disease of patients seeking treatment for travel-associated illness at the University Hospital of Zürich from January 2004 through May 2005.
The University Hospital of Zürich, as part of the global GeoSentinel surveillance network, contributed clinician-based surveillance data during a 17-month period, January 2004–June 2005, according to demographic characteristics, risk for infectious disease while traveling, and frequency of pretravel advice. GeoSentinel is a global sentinel surveillance network that was established in 1995 through the International Society for Travel Medicine and the US Centers for Disease Control and Prevention. The network consists of 33 globally distributed member travel/tropical medicine clinics (
To be eligible, patients must have crossed an international border ≤10 years before seeking treatment and must have sought medical advice for a presumed travel-related illness. Relevant travel details focused only on data from the 6 months before the onset of illness. Only final diagnoses were considered, and >1 diagnosis per patient was possible. Data were collected according to a standardized, anonymous questionnaire. The questionnaire asked for demographic data (age, sex, country of birth, country of residence, current citizenship), travel history during the previous 5 years, inpatient or outpatient status, major clinical symptoms (>1 per patient possible), pretravel visit information, reason for most recent travel, and patient classification. Reasons for most recent travel were immigration, tourism, business, research/education, missionary/volunteer work, visit to friends or relatives, and expatriation. Patients were classified as immigrants/refugees, foreign visitors, urban expatriates, nonurban expatriates, students, military personnel, or travelers. Working and final diagnoses were assigned by a physician.
An immigrant/refugee was defined as a foreign-born person who had obtained permanent resident status or immigrant/refugee status in Switzerland. Traveler (or traditional traveler) was defined as a resident of Switzerland who crossed an international border and did not previously immigrate to Switzerland. When the purpose of recent travel was visiting friends and relatives, a traveler was termed VFR. Different patient classifications were possible (i.e., immigrant-VFR, traveler-VFR). The rate of illness was calculated as the number of patients with a specific or a summary diagnosis as a proportion of all VFR or traditional travelers, respectively, expressed as number per 1,000 patients. The percentage of “chief complaints” was expressed as the number of primary symptoms that led to a clinic visit per total patients in each group. More than 1 chief complaint per patient was possible.
Countries were assigned to 1 of 15 regional classifications (
Summary diagnosis were defined as follows: “respiratory tract infection” included upper and lower respiratory infections; “malaria” infections included all malaria-causing species; “diarrhea” included acute diarrhea of parasitic, viral, bacterial or unknown origin; “hepatitis” included chronic or acute viral hepatitis; “viral syndrome” included any nonspecific viral symptoms; and “AIDS/HIV/STI” included asymptomatic HIV, acute HIV, AIDS, gonorrhea, syphilis, and other sexually transmitted infections (STIs). Syndrome groups such as “dermatologic disorder” were defined as previously described (
Stata software (version 9.1, Stata Corporation, College Station, TX, USA) was used for statistical analysis. Odds ratios (OR) of binary, categorical, or continuous variables were determined by logistic regression (multivariate or univariate) and adjusted to age and sex if indicated. Statistical significance of dichotomous variables was achieved by using χ² or nonparametric tests.
We analyzed 451 patients included in the database: 181 immigrants, 227 travelers, 25 foreign visitors, and 18 others (expatriates, students, military personnel). Age range was 16–87 years (median 33, interquartile range 27–43); 48% were female, and 20% were inpatients. The median duration of travel was 17.5 days (interquartile range 13–29 days). For these patients, 671 diagnoses were counted. Leading complaints were “fever” (43.0%), “gastrointestinal” (42.7%), “head-ear-nose” (25.2%), “respiratory” (24.3%), “musculoskeletal” (12.8%), and “skin” (11.9%, data not shown). The visits were evenly distributed during the calendar year, with no seasonal abnormities or significant associations.
Our analysis included 217 traditional travelers and 121 VFR travelers. For traditional travelers, the reason for most recent travel was tourism or business. Most VFR travelers (86%) were in the category “immigrants.” Birth country regions of VFR travelers were Asia (30%), sub-Saharan Africa (24%), Eastern Europe (17%), and Central or South America (11%). The basic demographic pattern was comparable (
| Travelers, no. (%) n = 217 | VFR, no. (%) n = 121 | p value | |
|---|---|---|---|
| Sex | |||
| Male | 119 (54.8) | 61 (50.4) | 0.43 |
| Female | 98 (45.2) | 60 (49.6) | |
| Age (y) | |||
| Median | 32 | 39 | 0.008 |
| Interquartile range | 32–46 | 26–45 | |
| Patient type | |||
| Outpatient | 185 (84.5) | 84 (70.6) | 0.002 |
| Inpatient | 34 (15.5) | 35 (29.4) | |
| Travel duration (d) | |||
| Median | 15 | 21 | 0.006 |
| Interquartile range | 11–24 | 14–31 | |
| Sought pretravel advice? | |||
| Yes | 65 (67) | 18 (20) | 0.0001 |
| No | 32 (33) | 70 (80) | |
| Traveled region | |||
| Sub-Saharan Africa | 43 (19.81) | 27 (22.31) | |
| Asia | 61 (28.11) | 21 (17.35) | |
| Eastern Europe | 6 (2.76) | 21 (17.35) | |
| Central/South America | 22 (10.13) | 9 (7.43) | |
| All other regions | 85 (39.17) | 43 (35.53) |
| Travelers, no. (%)* | VFR, no. (%)* | |
|---|---|---|
| Primary symptom | ||
| Fever | 108 (49.76) | 57 (47.10) |
| Gastrointestinal | 117 (53.91) | 48 (39.66) |
| Head-ear-nose | 54 (24.88) | 38 (31.40) |
| Respiratory | 52 (23.96) | 34 (28.09) |
| Musculoskeletal | 25 (11.52) | 22 (18.18) |
| Skin | 30 (13.82) | 14 (11.57) |
| Fatigue | 24 (11.05) | 13 (10.74) |
| Other | 18 (8.29) | 16 (13.22) |
| Total | 428 | 242 |
| Summary diagnosis and syndrome groups | ||
| Diarrhea, acute | 79 (26.33) | 21 (11.53) |
| Respiratory infection | 40 (13.33) | 22 (12.09) |
| HIV/AIDS | 12 (4) | 15 (8.24) |
| Malaria, all species | 8 (2.67) | 14 (7.69) |
| Viral syndrome | 23 (7.67) | 10 (5.49) |
| Viral hepatitis, acute/chronic | 6 (2) | 10 (5.49) |
| Urinary tract infection | 3 (1) | 3 (1.65) |
| Febrile illness, unspecified | 10 (3.33) | 1 (0.55) |
| Dengue fever (uncomplicated) | 4 (1.33) | 1 (0.55) |
| Sexually transmitted infection | 1 (0.33) | 3 (1.65) |
| Loa loa | – | 2 (1.1) |
| Cutaneous leishmaniasis | 1 (0.33) | – |
| Typhoid/paratyphoid fever | 1 (0.33) | 1 (0.55) |
| Brucellosis | – | 1 (0.55) |
| Extraintestinal amebiasis | 1 (0.33) | –- |
| Dermatologic disorder | 22 (7.33) | 9 (4.95) |
| Chronic diarrhea | 7 (2.33) | 5 (2.75) |
| Healthy | 4 (1.33) | 2 (1.1) |
| Adverse drug or vaccine reaction | 3 (1) | 1 (0.55) |
| Cardiovascular disorder | 2 (0.67) | 3 (1.65) |
| Neurologic disorder | 2 (0.67) | 2 (1.1) |
| Lost to follow-up | 2 (0.67) | – |
| Pulmonary embolism | 1 (0.33) | 2 (1.1) |
| Psychological disorder | 1 (0.33) | 2 (1.1) |
| Death | 1 (0.33) | 1 (0.55) |
| Other diagnosis | 66 (22) | 51 (28.02) |
| Total | 300 | 182 |
*Percentage expressed as number of primary symptoms that led to a clinic visit per total patients in each group.
When comparing VFR with traditional travelers, VFR travelers were more likely to receive a diagnosis of malaria, acute or chronic viral hepatitis, and HIV/AIDS/STI (
| Odds ratio | p value | 95% CI | |
|---|---|---|---|
| Univariate analysis | |||
| HIV/AIDS/STI | 2.42 | 0.019 | 1.15–5.07 |
| Malaria | 3.04 | 0.014 | 1.25–7.40 |
| Diarrhea, acute | 0.36 | 0.0001 | 0.21–0.61 |
| Viral hepatitis | 2.84 | 0.046 | 1.01–7.97 |
| Respiratory infection | 0.89 | 0.692 | 0.51–1.55 |
| Viral syndrome | 0.7 | 0.362 | 0.32–1.50 |
| Multivariate analysis (adjusted to age and sex) | |||
| HIV/AIDS/STI | 2.63 | 0.014 | 1.21–5.69 |
| Malaria | 2.93 | 0.021 | 1.17–7.32 |
| Diarrhea, acute | 0.47 | 0.007 | 0.27–0.81 |
| Viral hepatitis | 3.15 | 0.032 | 1.10–9.02 |
*CI, confidence interval; STI, sexually transmitted infection.
A different infectious disease spectrum and a trend toward a distinct pattern in both VFR and traditional travelers were also found when selecting different travel regions (
Percentage of disease diagnoses in travelers visiting friends and relatives (VFR) and traditional travelers (trav) who reported illnesses after returning to Switzerland, classified by geographic region visited.
The GeoSentinel site based at the University Hospital of Zürich represents a large population in Switzerland. However, GeoSentinel is a health facility–based surveillance system and does not actively screen for certain diseases. Patients included in the database do not necessarily represent the whole population or the epidemiology or frequency of the disease. Besides the unknown number of ill returned travelers going to general practitioners or nonspecialized clinics, the number of travelers returning in good health is also unknown. Incidence rates or relative risks therefore cannot be estimated. Similarly, patients with mild or self-limiting disease are likely to see a general practitioner rather than to go to a specialized center, although many VFR travelers do not have a regular general practitioner. On the other hand, Zürich is a large city with a socioculturally mixed population that offers an opportunity to study immigrant-VFR travelers, and many of these patients may prefer to go to a more anonymous university hospital than to a general practitioner. A limitation of the study is the relatively small number of patients included in the database during the 17-month period, which made it necessary to form summary diagnoses and regions.
In our analysis, VFR travelers showed a different infectious disease and risk spectrum than did traditional travelers; were more likely to receive a diagnosis of malaria, viral hepatitis, or HIV/AIDS/STI; and were less likely to seek pretravel advice. Traditional travelers (mainly tourists) were significantly more likely to seek advice before traveling and to have a posttravel diagnosis of acute diarrhea. This is consistent with previous studies from European migrants returning to their home countries (
By contrast, acute diarrhea was the greatest problem in traditional travelers, with an illness rate of 364 per 1,000 ill returned travelers compared with 173/1,000 in VFR travelers. Acute diarrhea, or traveler’s diarrhea, is known to affect >50% of travelers, depending on the destination (
Acute or chronic viral hepatitis was also significantly associated with VFR travel, which correlates with a recent study of hepatitis A virus infections in Swiss travelers during a period of 12 years that identified VFR travelers as a high-risk group, especially children of immigrants (
Systemic febrile illnesses, including malaria and typhoid fever, tuberculosis, and respiratory syndromes, are more frequently diagnosed among VFR travelers (
This study shows that VFR travelers are at greater risk for certain infectious diseases and have a disease spectrum distinct from that of traditional travelers. Malaria is the most important, life-threatening imported disease for both nonimmune and VFR travelers, and malaria acquisition is even more likely in VFR travelers. For other infectious diseases, HIV and STIs must also be included in the differential diagnosis, particularly for VFR travelers. VFR travelers are vulnerable because they may visit more rural destinations, live under poor sanitary conditions, and stay away for longer periods (
In addition, VFR travelers often did not seek pretravel advice. Thus, culturally sensitive strategies for pretravel contact with VFR travelers are greatly needed. Further surveillance of traveler groups with denominator data is needed, and prospective studies focusing on behavioral aspects of disease prevention would allow for evidence-based interventions as part of a public health strategy.
Illness rates in persons whose purpose of travel was visiting friends and relatives (VFR) versus traditional travelers (travelers). Points indicate number of illnesses per 1,000 ill returned travelers.
We are grateful to Elena Axelrod for help in preparing the data set, Leisa Weld for statistical consultancy, and Hanspeter Jauss for technical assistance. We also thank the GeoSentinel network, the local site at Zürich, and the medical staff at Zürich University Hospital for their cooperation.
Dr Fenner obtained his medical degree from the Medical Faculty of Basel, Switzerland, and is resident microbiologist at the University Hospital, Basel. His research interests include international health and infectious diseases epidemiology.