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Regional Variation in Travel-related Illness acquired in Africa, March 1997–May 2011 - Volume 20, Number 4—April 2014 - Emerging Infectious Disease journal - CDC

Regional Variation in Travel-related Illness acquired in Africa, March 1997–May 2011

Marc Mendelson

, Pauline V. Han, Peter Vincent, Frank von Sonnenburg, Jakob P. Cramer, Louis Loutan, Kevin C. Kain, Philippe Parola, Stefan Hagmann, Effrossyni Gkrania-Klotsas, Mark Sotir, Patricia Schlagenhauf, and for the GeoSentinel Surveillance Network

Author affiliations: University of Cape Town Groote Schuur Hospital, Cape Town, South Africa (M. Mendelson); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (P.V. Han, M. Sotir); Tokai Medicross Travel Clinic, Cape Town (P. Vincent);University of Munich, Munich, Germany (F. von Sonnenburg);University Medical Center, Hamburg-Eppendorf, Germany (J.P. Cramer); University of Geneva, Geneva, Switzerland (L. Loutan);University of Toronto, Toronto, Ontario, Canada (K.C. Kain);Assitance Publique Hôpitaux de Marseille–North University Hospital, Marseille, France (P. Parola); Yeshiva University Bronx-Lebanon Hospital Center, Bronx, New York, USA (S. Hagmann); Cambridge University Hospitals National Health Service Trust, Cambridge, UK (E. Gkrania-Klotsas); University of Zurich Centre for Travel Medicine, Zurich, Switzerland (P. Schlagenhauf)

Abstract

To understand geographic variation in travel-related illness acquired in distinct African regions, we used the GeoSentinel Surveillance Network database to analyze records for 16,893 ill travelers returning from Africa over a 14-year period. Travelers to northern Africa most commonly reported gastrointestinal illnesses and dog bites. Febrile illnesses were more common in travelers returning from sub-Saharan countries. Eleven travelers died, 9 of malaria; these deaths occurred mainly among male business travelers to sub-Saharan Africa. The profile of illness varied substantially by region: malaria predominated in travelers returning from Central and Western Africa; schistosomiasis, strongyloidiasis, and dengue from Eastern and Western Africa; and loaisis from Central Africa. There were few reports of vaccine-preventable infections, HIV infection, and tuberculosis. Geographic profiling of illness acquired during travel to Africa guides targeted pretravel advice, expedites diagnosis in ill returning travelers, and may influence destination choices in tourism.

Africa is a popular tourist destination and a focus for international aid work, research, and business travel. In 2011, compared with 2010, international arrivals on the African continent remained relatively stable at ≈50 million, although the number of travelers to northern Africa decreased by 1.7 million (9%) and travel to sub-Saharan Africa increased by 1.3 million (4%) travelers (1). Identification of the types and relative frequencies of illnesses acquired by travelers to Africa would enable targeted prevention strategies before and during travel, as well as diagnosis and management of illness in returnees.

Previously described as “the Dark Continent,” referring to poor knowledge of its interior, Africa’s diverse geography, ecosystems, and climate are now well defined. However, detailed understanding is lacking about the variety of illnesses experienced by travelers who visit different parts of this diverse continent. Prior studies have focused on travel-related illnesses acquired only within sub-Saharan Africa (2) or have concentrated on a single infection (3). The perception of the public and health care practitioners is that the risk of acquiring many travel-related illnesses, including malaria, is uniform throughout the continent. This misconception was particularly evident to practitioners of travel health in South Africa before the 2010 Fédération Internationale de Football Association World Cup in South Africa, an annual event that attracts hundreds of thousands of persons to the hosting country. This erroneous concept and a need for evidence-based travel advice prompted a GeoSentinel study that demonstrated marked variation in morbidity rates for malaria, African tick bite fever, and other travel-related illnesses in persons returning from South Africa compared with persons returning from neighboring countries or other countries in sub-Saharan Africa (4). The objective of the current analysis is to study regional variation in travel-acquired and emerging infections across Africa. Reaching this objective will better inform pretravel clinical consultations, which will help travelers recognize illnesses in the travel destination, take preventive measures, and seek treatment; and will focus differential diagnoses by clinicians among travelers returning from Africa.

Methods

The GeoSentinel Surveillance Network (www.istm.org/geosentinel/main.html) is an international network of specialized travel and tropical medicine providers housed in sites in 23 countries on 5 continents, established through the International Society of Travel Medicine (www.istm.org/) and the Centers for Disease Control and Prevention (www.cdc.gov). Details of patient recruitment, structure, and function of GeoSentinel sites that systematically report on all ill travelers have been described (2). Data for ill travelers are collected during or after travel. Demographics, travel history, reason for travel, clinical symptoms, and diagnostic information are recorded anonymously on a questionnaire, and GeoSentinel sites enter the information into a central database. The best available reference diagnostic tests are used at each site to categorize illness into 1 of 23 syndromic groups and >500 individual diagnoses. Representatives from the sites enter each diagnosis as laboratory confirmed or probable; both are included in the analysis. The country or region of illness acquisition is identified on the basis of itinerary, known endemicity patterns, and incubation periods.

Figure 1

Thumbnail of Regions of Africa as defined by the United Nations geoscheme (5). For persons whose country of exposure was unascertainable or missing but for whom all recent travel was to the same region of Africa, data were included in the final dataset.

Figure 1. . . Regions of Africa as defined by the United Nations geoscheme (5). For persons whose country of exposure was unascertainable or missing but for whom all recent travel...

Figure 2

Thumbnail of Flowchart for analysis of ill returned travelers from Africa reported in the GeoSentinel Surveillance Network, March 1997–May 2011. The United Nations geoscheme was used to classify Africa into subregions (5).

Figure 2. . . Flowchart for analysis of ill returned travelers from Africa reported in the GeoSentinel Surveillance Network, March 1997–May 2011. The United Nations geoscheme was used to classify Africa into subregions...

To study regional variation in the pattern of illnesses in persons who traveled to Africa, we used the United Nations geoscheme to classify Africa into subregions: Eastern, Central, Northern, Southern, and Western Africa (Figure 1) (5). An ill traveler returning from a country within an African region was considered to have been exposed to the causative pathogen in that region if the GeoSentinel database had a record of its occurrence there; or if the exposure was not defined in the record but the ill person traveled only to countries within that region. We included in our study all ill travelers listed in the GeoSentinel database during March 14, 1997–May 31, 2011 (Figure 2).

Statistical Analysis

Demographic and travel characteristics of travelers to each African region were described by using frequencies and proportions for categorical variables and median and range for continuous variables. Analysis of Plasmodium falciparum malaria trends during 2007–2011 was calculated on the basis of monthly counts of ill returned travelers with febrile systemic illness that were aggregated over the study period. Of 54 sites in the GeoSentinel database reporting during 2007–2011, a total of 35 sites reported consistently during this period. We used only data from those 35 sites for trend analysis. Data were analyzed by using SAS version 9.2 (http://support.sas.com/software/92/index.html

Results

We identified 16,893 ill travelers who returned from a single country or multiple countries within the same region in Africa during a 14-year period. Most acquired their illness either in Western (35%) or Eastern Africa (33%). Illness associated with travel to Southern Africa (8%) was least frequently reported (Figure 2).

Patient Characteristics

Most ill travelers returning from all regions were 18–64 years of age (Table 1). The residence of travelers spanned 72 countries; travelers were most frequently from Germany (33%), United States (12%), Canada (11%), France (10%), and Switzerland (10%).

Male travelers more commonly visited Central and Western Africa, and female travelers were more likely to visit Eastern and Northern Africa. Travelers visiting friends or relatives (VFR) more commonly visited Central (29%) and Western (33%) Africa than the other regions (2%–11%). Business travelers more frequently traveled to Central Africa (32%) than to other regions (9%–16%). Approximately three quarters of travelers to Northern (74%) and Southern Africa (78%) were tourists. Travelers to Northern Africa were less likely to have had a pretravel medical consultation (35%) than were travelers to other regions (50%–61%). Posttravel hospitalization rates were higher in travelers to Central and Western Africa (21%–25%) than in travelers to Northern and Southern Africa (5%–11%). The most frequent diagnoses among hospitalized travelers were P. falciparum malaria (45%), P.vivax malaria (4%), and unspecified febrile illness (<3 weeks) (3%).

Deaths among Travelers to Africa

Deaths of 11 travelers were recorded after travel to regions of sub-Saharan Africa (Table 2). Ten were of male sex; 10 were adults (median age 50 years). Severe P. falciparum malaria predominantly acquired in Western Africa was the cause of death for 9 of the 11 travelers. Two deaths occurred in expatriates, and 6 male business travelers died of P. falciparum malaria.

Northern Africa

Travel to Northern Africa was predominantly characterized by acquisition of gastrointestinal illnesses, comprising 66% of the 16,893 travel-related illnesses from this region and 7 of the 10 most frequent diagnoses (Table 3). In contrast, gastrointestinal disorders from regions of sub-Saharan Africa represented 27%–40% of cases. There was no difference among regions for acute or chronic diarrhea, schistosomiasis, or other gastrointestinal disorders such as intestinal strongyloidiasis. Of the reported hepatitis A cases, 28 (47%) originated in Northern Africa. Analysis of the data for individual countries in the Northern Africa region did not show variation in type of diarrheal disease or gastrointestinal disease (data not shown).

Documentation of animal bites and the need for rabies postexposure prophylaxis (PEP) showed striking geographic variation. Of the 193 reports of bites on the continent, 23% were to travelers <18 years of age. Of the 184 who received rabies PEP, 21% were travelers <18 years of age. Travelers to Northern Africa accounted for 105 (54%) of the 193 bites from dogs, cats, and others (including monkey and human) reported in Africa (Table 4); in contrast, 16 (8%) bites were reported from Southern and Central Africa combined. Similarly, 107 (58%) of the 184 exposures requiring rabies PEP were reported from Northern Africa. Although Egypt was the most commonly visited country in Northern Africa (3 times the number of visits to Morocco), travelers to Morocco received the most bites (21 dog bites, 8 cat, 3 other).

Regions within Sub-Saharan Africa

In contrast to the vast numbers of reports of gastrointestinal disease, febrile illnesses were uncommon in travelers to Northern Africa (4%). Conversely, 11%–47% of travelers returning from regions of sub-Saharan Africa had a febrile illness (Table 5). P. falciparum malaria was the most common cause of fever in returning travelers from sub-Saharan Africa, a finding consistent with those of previous studies (6,7). Of travelers who had malaria, 47% were VFR. Of travelers returning with malaria, 6% were <18 years of age. The proportion of febrile illness caused by malaria differed among regions: 2% of travelers returning from Southern Africa with febrile illness had malaria, compared with 69% and 67%, respectively, from Western and Central Africa. Conversely, African tick bite fever was the leading cause of illness in 273 (47%) of 579 travelers with fever returning from Southern Africa.

P. falciparum was the most common cause of malaria from all regions, including 100% of identified malaria cases from Southern Africa. P. vivax was proportionately more common from Eastern Africa (8%) than from other regions (0%–4%), and most of P. ovale and P. malariaecases were acquired in Central or Western Africa. Interregional seasonal variation in malaria acquisition was noted, although Western Africa was the only region that had a recognizable pattern of malaria cases, which the GeoSentinel sites reported more frequently from July through January.

A previous GeoSentinel study identified schistosomiasis as the most frequent helminthic infection reported in travelers returning from Africa, with regional variation noted (8). Seventy-three percent of reported strongyloidiasis cases were acquired in travelers returning from Eastern and Western Africa; 3% were reported in travelers to Southern Africa (Table 4). Acquisition of Strongyloides stercoralis from previous travel to, or birth in, other countries to which this infection is endemic cannot be discounted. Loasis accounted for 86 of 236 filarial infections, 82 (94%) of which were acquired from Central Africa, consistent with known endemicity; 50 (62%) of the 82 were from Cameroon, 12 from Gabon, 10 from Central African Republic, and 3 from Congo. Female travelers (58%) were more often infected by Loa loa than were men; volunteers (45%) and travelers VFR (30%) were the groups most often affected. Only 10% of cases were seen in tourists. Although largely an infection diagnosed in adults, 8% of cases were diagnosed in children (median age 10 years [interquartile range 7.0–16.5 years]).

Vaccine-preventable infections (VPI; i.e., hepatitis A, influenza, measles, and Salmonella typhiinfection [typhoid]) taken together accounted for 0.9% of illnesses in travelers returning from Africa. The proportion of VPI from each region was comparable (Table 4). Among demographic groups, tourists were most likely to have VPI, most commonly hepatitis A and typhoid acquired in Northern Africa. Sex distribution was equal, and apart from 17 (29%) of the 59 hepatitis A cases that occurred in travelers <17 years of age, most VPI were diagnosed in adults. The acquisition of a VPI was not related to whether a pretravel consult had been sought.

During the 14-year study period, 86 cases of symptomatic tuberculosis were diagnosed in travelers returning from Africa, and an additional 159 travelers had positive tuberculin skin tests. Whether the positive skin tests were caused by acquisition of infection during travel or by prior exposure is unknown because no records of pretravel test results are available. Travelers returning from Central and Southern African regions, which are among countries with the highest rates of tuberculosis worldwide (9), accounted for 6 cases of symptomatic tuberculosis (Table 4).

Acute HIV infection was recorded for 44 persons. As was the case for tuberculosis, the number of acute HIV infections from Central and Southern Africa was lower than that from Eastern and Western Africa. No cases were diagnosed in travelers to Northern Africa.

Dengue is a common cause of illness in travelers to the Asia–Pacific region and Latin America (2); however, in our study, dengue acquired in Africa was diagnosed in as few as 113 travelers with febrile illness during the 14-year study period. Our data suggest that 81% of cases were acquired during travel to either Eastern or Western Africa (Table 4). Dengue was diagnosed equally in both sexes, and infection in travelers 18–49 years of age accounted for 81% of cases. Tourists were the major risk group for this illness.