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Malaria in Travelers: A Review of the GeoSentinel Surveillance Network

  1. Karin Leder1,2,
  2. Jim Black1,
  3. Dan O'Brien1,
  4. Zoe Greenwood1,
  5. Kevin C. Kain4,5,
  6. Eli Schwartz6,7,
  7. Graham Brown1,3, and
  8. Joseph Torresi1,3
  1. 1Victorian Infectious Diseases Service, Royal Melbourne Hospital, Victoria
  2. 2Department of Epidemiology and Preventive Medicine, Monash University, Victoria
  3. 3Centre for Clinical Research Excellence in Infectious Diseases and the Department of Medicine, University of Melbourne, Melbourne, Australia
  4. 4Global Health Program, McLaughlin Center for Molecular Medicine, University of Toronto, Toronto, Ontario, Canada
  5. 5Center for Travel and Tropical Medicine, University Health Network—Toronto General Hospital, Toronto, Ontario, Canada
  6. 6Center for Geographic Medicine, Chaim Sheba Medical Center, Tel Hashomer
  7. 7Sakler Faculty of Medicine, Tel Aviv University, Israel
  1. Reprints or correspondence: Dr. Karin Leder, Victorian Infectious Disease Service, Royal Melbourne Hospital, Royal Parade, Parkville, Victoria, 3052, Australia (karin.leder{at}med.monash.edu.au).
 
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Abstract

Background. Malaria is a common and important infection in travelers.

Methods. We have examined data reported to the GeoSentinel surveillance network to highlight characteristics of malaria in travelers.

Results. A total of 1140 malaria cases were reported (60% of cases were due to Plasmodium falciparum, 24% were due to Plasmodium vivax). Male subjects constituted 69% of the study population. The median duration of travel was 34 days; however, 37% of subjects had a travel duration of ⩽4 weeks. The majority of travellers did not have a pretravel encounter with a health care provider. Most cases occurred in travelers (39%) or immigrants/refugees (38%). The most common reasons for travel were to visit friends/relatives (35%) or for tourism (26%). Three-quarters of infections were acquired in sub-Saharan Africa. Severe and/or complicated malaria occurred in 33 cases, with 3 deaths. Compared with others in the GeoSentinel database, patients with malaria had traveled to sub-Saharan Africa more often, were more commonly visiting friends/relatives, had traveled for longer periods, presented sooner after return, were more likely to have a fever at presentation, and were less likely to have had a pretravel encounter. In contrast to immigrants and visitors of friends or relatives, a higher proportion (73%) of the missionary/volunteer group who developed malaria had a pretravel encounter with a health care provider. Travel to sub-Saharan Africa and Oceania was associated with the greatest relative risk of acquiring malaria.

Conclusions. We have used a global database to identify patient and travel characteristics associated with malaria acquisition and characterized differences in patient type, destinations visited, travel duration, and malaria species acquired.

Malaria is the most common cause of fever in returned travelers [1, 2]. Approximately 25–30 million international travelers from nontropical regions visit countries where malaria is endemic annually, with ∼30,000 cases of travel-associated malaria acquired [3, 4]. From 1991 through 2001, a total of 13,900 cases of imported malaria were reported in the United States [5]. Plasmodium falciparum accounted for one-half of all cases in 2001, with 85% acquired in Africa. Similarly, in 1999 and 2000, a total of 1659 cases of P. falciparum malaria were reported in European travelers returning from countries of endemicity [6]. In contrast to the findings of reports from the Northern Hemisphere, Plasmodium vivax malaria is more frequently diagnosed than P. falciparum malaria in Australian travelers returning from surrounding malarious areas in the Asia-Pacific region [7]. Few studies have provided a representative comparison of imported malaria in travelers returning to sites in both the Northern and Southern Hemispheres. Examination of the epidemiology of imported malaria in different categories of travelers may provide evidence-based recommendations regarding chemoprophylaxis and risk of malaria acquisition.

GeoSentinel is a global sentinel surveillance network that was established in 1995 through the International Society for Travel Medicine and the Centers for Disease Control and Prevention [8]. The information gathered by GeoSentinel can be used to ascertain risk factors for diseases among travelers, to monitor geographical and temporal trends in infectious diseases globally, and to enable the early detection of outbreaks of infectious diseases. We have examined the GeoSentinel database to determine demographic features, epidemiology, and travel characteristics associated with acquisition of malaria in travelers and to ascertain the comparative regional risk of presenting to a GeoSentinel site with malaria infection.

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Methods

Data source. Demographic data (including patients' age, sex, country of birth, country of residence, and country of current citizenship), travel history, clinical symptoms, and diagnostic information were collected. Travel information included countries visited in the previous 6 months, with corresponding visit dates, and a list of countries visited in the previous 5 years. Clinicians recorded the patient classification, reason for most recent travel, major complaint(s), inpatient or outpatient status, and pretravel visit with a health care provider. Final diagnoses reported by physicians were used to assign diagnostic codes from a standardized list of 500 syndromic or etiologic problems. Patient information was entered anonymously into an Access database (Microsoft).

Inclusion criteria. To be included in the GeoSentinel database, patients must have crossed an international border within 10 years before presentation and be seeking medical advice for a presumed travel-related illness. This analysis focused on destination data from the 6 months before presentation.

Data entered into the GeoSentinel database during the period of November 1997 through December 2002 were examined. Data were extracted for all individuals who had been assigned at least 1 of 12 specific numerical codes corresponding to a diagnosis of malaria.

Definitions and groupings. Patient classifications were immigrant/refugee, foreign visitor, urban/nonurban expatriate, student, military personnel, or traveler; individuals who presented to a GeoSentinel site in their country of residence upon return were classified as “travelers,” whereas nonresidents who visited a GeoSentinel site during their travels were referred to as “foreign visitors.” The reasons for most recent travel were immigration, tourism, business, research/education, missionary/volunteer, visiting friends or relatives, and other. Diagnostic classifications included P. falciparum malaria, P. vivax malaria, Plasmodium ovale malaria, Plasmodium malariae malaria, malaria due to an unknown species, and unconfirmed diagnosis. The diagnosis of malaria was confirmed using thick and thin blood films, immunochromatography test (ICT) for P. falciparum or P. vivax, or positive PCR result together with a positive blood film result. Designation of “cerebral malaria” or “severe but noncerebral malaria” was determined by the treating physicians at the time of clinical presentation.

Individual countries visited were assigned to 1 of the following 15 regional classifications: North America/Canada, Central America, South America, Caribbean, eastern Europe, western Europe, Oceania, Australasia (Australia and New Zealand), south-central Asia, Southeast Asia, east and north Asia, west Asia (including the Middle East), North Africa, sub-Saharan Africa, and Antarctica.

The regional definitions were the same as the United Nations' definitions, except as follows: Southeast Asia also included Christmas Island; east and north Asia also included Taiwan; south-central Asia also included Tibet; North Africa also included the Canary Islands; sub-Saharan Africa encompassed southern, middle, western, and eastern Africa, as defined by the United Nations; and Australia and New Zealand were separated from the rest of Oceania.

For clarification, the Asian regions and North Africa were classified as follows: south-central Asia included Bangladesh, Bhutan, India, Iran, Kazakhstan, Kyrgystan, Maldives, Nepal, Pakistan, Sri Lanka, Afghanistan, Tibet, Turkmenistan, Uzbekistan, and Tajikistan. Southeast Asia included Brunei, Cambodia, Indonesia, Laos, Malaysia, Myanmar, The Philippines, Singapore, Thailand, Vietnam, East Timor, and Christmas Island. East and north Asia included Peoples Republic of China, Hong Kong, Japan, North Korea, South Korea, Macao, Mongolia, and Taiwan. West Asia (including the Middle East) included Armenia, Azerbaijan, Bahrain, Cyprus, Georgia, Iraq, Israel, Jordan, Kuwait, Lebanon, Oman, Palestinian Territory, Qatar, Saudi Arabia, Syrian Arabic Republic, Turkey, United Arab Emirates, and Yemen. North Africa included Algeria, Egypt, Libyan Arab Jamahiriya, Morocco, Sudan, Tunisia, Canary Islands, and Western Sahara.

Comparison of patients with malaria with the entire GeoSentinel database. Patients with cases of malaria were compared with patients with nonmalaria cases in the GeoSentinel database to illustrate differences between individuals with malaria and those with other illnesses.

Relative risks (RRs) of presenting with malaria by region traveled. The RRs of presenting to a GeoSentinel clinic with malaria after travel to different geographic regions were estimated using GeoSentinel data (number of presentations with a diagnosis of malaria among patients who had traveled to the region) as numerators and World Travel Organization (WTO) data (number of tourist arrivals to the region) as denominators.

The WTO has published numbers of inbound international tourists by geographic region for the years 2000, 2001, and 2002 [9, 10]. Thus, only the subset of patients in the GeoSentinel database who had traveled during 2000–2002 was examined for the RR calculations. The geographic regions used by GeoSentinel are consistent with those of the WTO, except that, in WTO summaries, Oceania includes Australia and New Zealand, as well as Micronesia, Melanesia, and Polynesia. We adjusted for this using the ratio of tourists visiting Australasia as compared with those visiting the rest of Oceania, with data available from other sources [9]. These data were used to calculate the risk per 10 million travelers of becoming a patient with malaria at a GeoSentinel clinic. Absolute risks could not be ascertained, but RRs of malaria in travelers to different regions were calculated on the basis of ratios of the rates of malaria acquisition by region. In these calculations, a rate of 1.0 was assigned to regions with the lowest malaria rates.

Statistical analysis. Data were managed in Microsoft Access and were analyzed using Stata software, version 6.0 (Stata), and Excel 97 (Microsoft). RRs and 95% CIs were calculated using the method of Rothman [11]. EpiInfo 2000 (Centers for Disease Control and Prevention) was used for calculation of P values. The χ2 test was used for comparison of proportions, and nonparametric testing (the Kruskall-Wallis test) was performed for nonnormally distributed data.

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Results

Demographic data. Malaria was reported to GeoSentinel in 1140 individuals during the period of July 1997 through December 2002, representing 3.7% of all patients entered into the database during this period (figure 1). One-half of the cases were reported from 5 GeoSentinel sites in Europe, 31% of cases were reported from 16 sites in North America, 10% of cases were reported from 2 sites in Australasia, 8% of cases were reported from 1 site in the Middle East, and 1% of cases were reported from 1 site in south-central Asia.

Figure 1
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Figure 1

Malaria cases as a proportion of cases reported to GeoSentinel.

Mixed infection was reported in 21 cases, so a total of 1161 species diagnoses were made. Most cases (60%) consisted of P. falciparum malaria, followed in frequency by P. vivax malaria (24%). Species confirmation was available for 1035 cases (91%) (figure 2).

Figure 2
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Figure 2

Malaria species noted in a study of malaria in travelers. Total number of cases, by pathogen, were as follows: Plasmodium falciparum, 695 (676 single-species infections and 19 mixed infections); Plasmodium vivax, 278 (266 single-species infections and 12 mixed infections); Plasmodium ovale, 56 (52 single-species infections and 4 mixed infections); and Plasmodium malariae, 27 (20 single-species infections and 7 mixed infections). Mixed infections consisted of 10 cases involving P. falciparum and P. vivax, 6 cases involving P. falciparum and P. malariae, 3 cases involving P. falciparum and P. ovale, 1 involving P. vivax and P. ovale, and 1 involving P. malariae and P. vivax.

Sixty-nine percent of patients with malaria who had their sex reported were male. The mean age was 34.8 years (median age, 33 years; range, 1–84 years). Fever was reported at presentation in 93% of patients with P. falciparum malaria, 95% of those with P. vivax malaria, 83% of those with P. ovale malaria, and 95% of those with P. malariae malaria. A pretravel encounter with a health care provider was recorded in only 427 cases (37%). For individuals whose disease status was known, 523 (50%) were treated as inpatients. Sixty percent of patients with P. falciparum malaria were admitted to the hospital, compared with 45% for those with P. vivax malaria, 30% for those with P. ovale malaria, and 13% for those with P. malariae malaria. Cerebral malaria was reported in 17 individuals (2.4%) with P. falciparum infection. Severe complicated noncerebral malaria occurred in 16 cases, 14 of which involved P. falciparum alone, 1 of which involved P. falciparum and P. malariae, and 1 of which involved P. vivax. The median age of patients with cerebral or severe complicated malaria was 42.5 years, which was higher than the median age of those without complications (33 years) (P < .005).

Three deaths (9%) occurred associated with severe P. falciparum infection (patient ages, 30, 50, and 68 years), with 2 cases acquired in sub-Saharan Africa. Two deaths occurred among the travelers, and 1 expatriate traveling for business also died. Seven patients had HIV coinfection, and 13 were known to be pregnant; none of these patients had severe or complicated malaria.

Travel duration was known for 863 (76%) of the 1140 individuals. The median duration overall was 34 days (mean duration, 187 days; range, 1 to >1000 days); the median duration was in the range of 30–34.5 days for those with P. falciparum, P. vivax, or P. ovale malaria, and it was 63 days for those with P. malariae malaria. Five percent of individuals who presented with malaria had traveled for ⩽1 week, 32% had traveled for 1–4 weeks, 25% had traveled for 1–2 months, 21% had traveled for 2–6 months, and 16% had trip durations of >6 months.

Most individuals with malaria were either travelers (448 subjects [39%]) or immigrants/refugees (429 subjects [38%]) (figure 3A). The most common reasons for travel were visiting friends or relatives (401 subjects [35%]) and tourism (299 subjects [26%]) (figure 3B). A greater proportion of immigrants than nonimmigrants had P. falciparum malaria diagnosed (75% vs. 52%, respectively; P < .001), and a greater proportion of nonimmigrants than immigrants developed P. vivax malaria (29% vs. 15%, respectively; P < .001).

Figure 3
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Figure 3

Patient classification (A) and reason for travel (B) in a study of malaria in travelers

The region of acquisition was identified in 1107 cases (97%), with 839 cases (74%) acquired in sub-Saharan Africa (89% of P. falciparum infections and 33% of P. vivax infections were acquired there; table 1). Of the 1107 cases, 510 (46%) were exposed to malaria in the same region in which they were born. Of these, the majority (386 subjects [76%]) were immigrants/refugees from an area of endemicity who had migrated to a country without malaria, and many (331 subjects [65%]) were traveling back to their country of origin to visit friends and relatives. Approximately 10% were foreign visitors living in an area where malaria is endemic who were traveling to an area where it is not when they presented. Of note, 85% of the immigrants and of those visiting friends or relatives did not have a pretravel encounter with a health care provider (figure 4).

Table 1
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Table 1

Region of acquisition, by species, in a study of malaria in travelers.

Figure 4
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Figure 4

Reason for travel, by pretravel encounter with a health care provider, in a study of malaria in travelers.

Twenty-nine people (3%) presented to a GeoSentinel site during their trip. For those for whom it could be determined, the median time from the end of the trip to presentation was 13 days (mean duration, 35.5 days), but this varied by species (median duration for those with P. falciparum infection, 11 days; median duration for those with P. vivax infection, 44 days; P < .001) (table 2). Of patients with P. falciparum infection, 61% presented within 14 days of return, and 82% presented by day 28 after return. In contrast, 28% of individuals with P. vivax malaria presented within 14 days of return, and 39% presented by day 28 (P < .001). Individuals who developed P. vivax malaria and who had a pretravel encounter with a health care provider presented to a GeoSentinel site after a median of 58 days, whereas those with P. vivax malaria who did not have a pretravel encounter presented after a median of 15.5 days (P < .001). The presence or absence of a pretravel encounter did not significantly affect the time to presentation for individuals with P. falciparum malaria (median, 11 vs. 10 days, respectively; P > .5). The type of traveler (immigrant versus nonimmigrant) also had no significant influence on median times to presentation (data not shown).

Table 2
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Table 2

Time to presentation to GeoSentinel site in a study of malaria in travelers.

Demographic and travel data for patients with malaria and for all other GeoSentinel patients reported during the same time period were compared (table 3). A significantly greater proportion of patients with malaria were male (69% vs. 49%), had a higher median age (33 vs. 31 years), and had a longer median duration of travel (34 vs. 29 days). Individuals who had visited friends or relatives were significantly more likely to receive a diagnosis of malaria than other diagnoses (35% vs. 7%) and were more likely to present with malaria as their illness than were tourists (16.9% vs. 2.1%). The malaria group was also significantly more likely to present sooner after travel completion than were others (median time to presentation, 13 vs. 21 days) and were more likely to have a fever (90% vs. 17.7%), and hospital admission was more common in this group (50% vs. 5%). Patients with malaria had traveled to sub-Saharan Africa more commonly than did others (71% vs. 17%) and were less likely to have had a pretravel encounter with a health care provider (44% vs. 65%), especially if they had traveled to sub-Saharan Africa (44% vs. 79%).

Table 3
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Table 3

Comparison of demographic characteristics, reasons for travel, and durations and regions of travel in patients with and patients without malaria.

An approximate RR of malaria acquisition (by region) was determined using GeoSentinel data, with areas visited as numerators and WTO data as estimates for denominators (table 4). Sub-Saharan Africa (RR, 208) and Oceania (RR, 77) were associated with the greatest risk of acquiring malaria, followed by south Asia (RR, 54), central America (RR, 38), Southeast Asia (RR, 11.5), and South America (RR, 8). A similar analysis, which used regions in which malaria was reportedly acquired instead of regions visited, resulted in an identical order of RRs (data not shown).

Table 4
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Table 4

Cases of malaria and regions visited in a study of malaria in travelers, 2000–2002.

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Discussion

Malaria poses a serious health threat to individuals visiting areas where it is endemic. We have described important epidemiological features of imported malaria in 1140 individuals reported to a global sentinel surveillance network, GeoSentinel. Through the GeoSentinel surveillance program and its worldwide network of collaborating travel medicine centers, we have collated information on travelers with malaria from diverse backgrounds traveling to different regions and presenting to different travel medicine centers, thus providing a global perspective.

The majority of P. falciparum infections were acquired in sub-Saharan Africa. In contrast to previous reports, we found a greater regional diversity of acquisition for P. vivax infection, with ∼30% of infections acquired in sub-Saharan Africa, 30% acquired in Asia, 15% acquired in Central/South America, and 15% acquired in Oceania, reflecting the large diversity of traveler origins and destinations incorporated in the GeoSentinel database. Previous reports in European and US travelers have generally shown that >70% of P. vivax infections were acquired in Asia or Latin America [6, 12].

Short durations of exposure in areas of endemicity are sufficient for malaria acquisition. We found that 5% of malaria infections occurred after a trip with a duration of ⩽1 week. Of concern is the finding that 3% of travelers overall and 3% of patients with P. falciparum malaria developed symptoms of infection while abroad.

A limitation of our study is that strict WHO definitions for cerebral malaria and severe noncerebral malaria were not used; instead, the designation of cerebral and/or complicated malaria was based on the clinical presentation, as determined by treating physicians. Despite this, our study reminds us of the risk of fatality associated with P. falciparum malaria, with 3 deaths noted among the 33 reported patients with severe malaria. Individuals with complicated malaria had a higher median age than did the overall group (44 vs. 33 years), consistent with previous reports suggesting age as a risk factor for a severe outcome [13].

We found that 80% of patients with P. falciparum malaria and 40% with P. vivax malaria presented within 4 weeks of their return, which is similar to the findings of other studies [14]. A substantial proportion of our travelers presented several months after returning from travel, reinforcing the need to remain vigilant to ensure that this diagnosis is not missed.

Subjects with P. vivax malaria who had a pretravel encounter with a health care provider had a delayed presentation, compared with subjects who did not have a pretravel encounter. It is possible those with a pretravel encounter were prescribed chemoprophylaxis, and the late presentation may be due to delayed onset of malaria associated with blood-stage prophylaxis [15]. Late presentations may also represent relapses of infection. A recent study examining malaria surveillance data from Israel and the United States showed that more than one-third of travelers who were infected with P. vivax or P. ovale and who received chemoprophylaxis developed illness >2 months after their return [15].

Individuals in the GeoSentinel database are not representative of all international travelers, but comparison of malaria cases with all others in the database nevertheless enables identification of demographic and travel characteristics associated with malaria acquisition. We found that individuals with malaria were significantly more likely to have traveled to sub-Saharan Africa and were less likely than other GeoSentinel patients to have had a pretravel encounter with a health care provider. A greater proportion of travelers with malaria had a longer median duration of travel and presented earlier after completing their trip, compared with travelers without malaria. Most notable was the significantly greater proportion of patients with malaria who were visiting friends or relatives.

Eighty- five percent of immigrants or persons visiting friends or relatives did not have a pretravel encounter and were therefore unlikely to have taken antimalarial prophylaxis. In addition, immigrants were relatively more likely to present with P. falciparum malaria than were other types of travelers. People who were born and/or who visit family and friends in areas where malaria is endemic represent high-risk groups for malaria acquisition [12, 14, 16–19]. These individuals may not realize the exposure risks they face and need to be specifically targeted for education regarding malaria prevention.

In contrast to the immigrant group and those who were visiting friends or relatives, 73% of the missionary/volunteer group who developed malaria had had a pretravel encounter with a health care provider. This group highlights the difficulty of adherence to appropriate regimens in those with prolonged travel durations.

Calculation of absolute risks of malaria acquisition after travel to different regions would be ideal for clinicians giving pretravel advice. This requires determination of the numbers of travelers to each destination who become ill and of the total number visiting that destination; logistically, this is almost impossible to accurately ascertain. Instead, we determined the numbers of presentations to GeoSentinel clinics with malaria and, using WTO data as an estimate of all visitors to a region potentially at risk of malaria, have calculated relative rates of infection in travelers visiting different destinations. We are not aware of WTO data having been used in this way previously. Although it is impossible to verify the accuracy of WTO data, the relative rates of malaria acquisition by region are unlikely to be significantly affected. These calculations significantly underestimate the true risk of malaria acquisition, but to the extent that patients in the GeoSentinel database represent the larger population of travelers, their experience can be used to estimate relative regional risks for future travelers. These data generalize risk by region, and within particular regions, there may still be both low- and high-risk areas, so pretravel consultations need to be individualized.

We found the greatest RR occurred for travelers to sub-Saharan Africa, followed by travelers to Oceania. Other studies have attempted to estimate the malaria risk for travelers using malaria surveillance data and the numbers of travelers to specific destinations. These studies also showed that the risk of malaria in travelers who were not taking chemoprophylaxis was highest in sub-Saharan Africa and Oceania, intermediate on the Indian subcontinent, and lowest in Asia and Central and South America [4, 19–22]. Other data have suggested annual rates of malaria of 41 cases per 1000 travelers to Oceania; 3.75 and 1.7 cases per 1000 travelers for west and east Africa, respectively; and 0.01–0.1 cases per 1000 travelers to Latin America, the Far East, and the Middle East [23]. Our data support the general trend of risk but suggest a greater RR estimate for Central America than has previously been reported.

In conclusion, we have used a global database to highlight patient and travel characteristics of a large number of patients presenting with malaria. This study confirms and extends the findings of previous reports of imported malaria, and it enables analyses of differences in patient type, travel destinations, travel duration, and malaria species acquired. We have identified high-risk travel groups for malaria, and this may serve to guide clinicians who give pretravel health advice or assess unhealthy travelers on their return.

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The Geosentinel Surveillance Network

GeoSentinel Surveillance Network members contributing data were the following: Vernon Ansdell, Kaiser Permanente, Honolulu, Hawaii; Elizabeth Barnett, Boston University, Boston, Massachusetts; Graham Brown, Royal Melbourne Hospital, Melbourne, Australia; Giampiero Carosi, University of Brescia, Brescia, Italy; Lin Chen, Harvard University, Cambridge, Massachusetts; Bradley Connor, Weill Medical College of Cornell University, New York, New York; David Freedman, University of Alabama, Birmingham, Alabama; Alejandra Gurtman, Mount Sinai Medical Center, New York, New York; Devon Hale, University of Utah, Salt Lake City, Utah; Nancy Piper Jenks, Hudson River Health Care, Peekskill, New York; Jay Keystone, University of Toronto, Toronto, Ontario, Canada; Phyllis Kozarsky, Emory University, Atlanta, Georgia; Carmelo Licitra, Orlando Regional Health Center, Orlando, Florida; Louis Loutan, University of Geneva, Geneva, Switzerland; Susan McLellan, Tulane University, New Orleans, Louisiana; Elaine Jong, University of Washington, Seattle, Washington; Thomas Nutman, National Institutes of Health, Bethesda, Maryland; Prativa Pandey, CIWEC Clinic Travel Medicine Center, Kathmandu, Nepal; Bradley Sack, Johns Hopkins University, Baltimore, Maryland; Eli Schwartz, Sheba Medical Center, Tel Hashomer, Israel; Marc Shaw, Travellers Health and Vaccination Centre, Auckland, New Zealand; Frank von Sonnenburg, University of Munich, Munich, Germany; Murray Wittner, Albert Einstein School of Medicine, Bronx, New York; Jane Zuckerman, Royal Free and University College Medical School, London, England.

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Acknowledgments

We wish to acknowledge all contributors to the GeoSentinel surveillance program.

Financial support. GeoSentinel, the Global Surveillance Network of the International Society of Travel Medicine, is supplied by the Centers for Disease Control and Prevention (Cooperative Agreement U50/CCU412347).

Conflict of interest. All authors: No conflict.

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Footnotes

  • Members of the GeoSentinel Surveillance Network are listed at the end of the text.

  • Received January 29, 2004.
  • Accepted March 7, 2004.
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