SUPPLEMENT ARTICLE
Travel-Associated Enteric Infections Diagnosed
After Return to the United States, Foodborne
Diseases Active Surveillance Network (FoodNet),
2004–2009
Magdalena E. Kendall,1,2 Stacy Crim,1 Kathleen Fullerton,1 Pauline V. Han,1 Alicia B. Cronquist,3
Beletshachew Shiferaw,5 L. Amanda Ingram,6 Joshua Rounds,4 Eric D. Mintz,1 and Barbara E. Mahon1
1Centers for Disease Control and Prevention; 2Atlanta Research and Education Foundation, Atlanta, Georgia; 3Colorado Department of Public Health and
Environment, Denver; 4Minnesota Department of Health, St Paul; 5Oregon State Public Health Division, Portland; 6Tennessee Department of Health,
Nashville
Background. Approximately 40% of US travelers to less developed countries experience diarrheal illness. Using
data from the Foodborne Diseases Active Surveillance Network (FoodNet), we describe travel-associated enteric
infections during 2004–2009, characterizing the patients, pathogens, and destinations involved.
Methods. FoodNet conducts active surveillance at 10 US sites for laboratory-confirmed infections with
9 pathogens transmitted commonly through food. Travel-associated infections are infections diagnosed in the
United States but likely acquired abroad based on a pathogen-specific time window between return from
international travel to diagnosis. We compare the demographic, clinical, and exposure-related characteristics of
travelers with those of nontravelers and estimate the risk of travel-associated infections by destination, using US
Department of Commerce data.
Results. Of 64 039 enteric infections reported to FoodNet with information about travel, 8270 (13%) were
travel associated. The pathogens identified most commonly in travelers were Campylobacter (42%), nontyphoidal
Salmonella (32%), and Shigella (13%). The most common travel destinations were Mexico, India, Peru, Dominican
Republic, and Jamaica. Most travel-associated infections occurred in travelers returning from Latin America and the
Caribbean (LAC). Risk was greatest after travel to Africa (75.9 cases per 100 000 population), followed by Asia (22.7
cases per 100 000), and LAC (20.0 cases per 100 000).
Conclusions. The Latin America and Caribbean region accounts for most travel-associated enteric infections
diagnosed in the United States, although travel to Africa carries the greatest risk. Although FoodNet surveillance
does not cover enterotoxigenic Escherichia coli, a common travel-associated infection, this information about other
key enteric pathogens can be used by travelers and clinicians in pre- and posttravel consultations.
Diarrheal illness is often experienced by US travelers
to other countries [1, 2]. The World Health Organization (WHO) estimates that 15–20 million travelers
to developing countries experience diarrhea annually [3];
40% of US travelers to less developed countries are
estimated to contract diarrheal illness due to Salmonella,
Correspondence: Magdalena E. Kendall, MPH, Centers for Disease Control and
Prevention, 1600 Clifton Rd NE, Mailstop C-09, Atlanta, GA 30333 (mkendall@
cdc.gov).
Clinical Infectious Diseases 2012;54(S5):S480–7
Published by Oxford University Press on behalf of the Infectious Diseases
Society of America 2012.
DOI: 10.1093/cid/cis052
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Campylobacter, enterotoxigenic Escherichia coli (ETEC),
and other enteric pathogens [4]. Travelers usually become infected by ingesting food or water contaminated with these pathogens [5, 6]. Knowledge of the
epidemiology of travel-associated enteric infections
can help improve US traveler health and prevent
morbidity and mortality by improving pre- and
posttravel consultations and enhancing public health
investigations.
No surveillance system monitors enteric infections
globally, although many countries, including the United
States, have national enteric disease surveillance systems
in place. Indeed, investigators from Sweden and Finland
have used their national surveillance data to examine enteric
diseases in travelers [7–9]. The Global Foodborne Infections
Network builds global capacity for the detection, control, and
prevention of enteric infections and maintains a Web-based
databank of Salmonella infections reported by continent [10],
and the GeoSentinel Global Surveillance Network monitors
travel-related illnesses at 41 sites worldwide [11]. These systems provide useful information on the worldwide distribution of Salmonella serotypes and other enteric infections
causing illness in travelers, but little information is available on
the risk among US travelers.
In 2004, the Foodborne Diseases Active Surveillance Network
(FoodNet) began routinely collecting data about international
travel among US residents who receive a diagnosis of certain
enteric infections after return to the United States. We used
FoodNet data from the period 2004–2009 to describe these
travel-associated infections, characterizing the patients, pathogens, and destinations involved.
METHODS
Surveillance
Established in 1996, FoodNet is the principal foodborne disease
component of the Emerging Infections Program of the Centers for Disease Control and Prevention (CDC). FoodNet
is a population-based active surveillance system that is a collaboration of the CDC, 10 state health departments, the US
Department of Agriculture’s Food Safety and Inspection
Service, and the US Food and Drug Administration [12].
FoodNet actively tracks laboratory-confirmed infections with
9 pathogens transmitted commonly through food, including
Campylobacter, Cryptosporidium, Cyclospora, Listeria, Salmonella,
Shiga toxin–producing Escherichia coli (STEC), Shigella,
Vibrio, and Yersinia. FoodNet does not conduct surveillance
for ETEC infection, because clinical laboratories do not
routinely test for ETEC. The FoodNet surveillance area has remained constant since 2004 and includes 10 sites: 7 states
(Connecticut, Georgia, Maryland, Minnesota, New Mexico,
Oregon, and Tennessee) and selected counties in California,
Colorado, and New York. In 2009, the FoodNet surveillance area
included 46.8 million persons (approximately 15% of the US
population). State health department personnel at the 10 sites
collect clinical and demographic information about each patient.
Definitions
FoodNet defines the international travel exposure window,
hereafter called the exposure window, on the basis of the incubation period for each pathogen. To be considered a traveler in FoodNet, a patient must have returned from an
international destination within 30 days before illness onset
for cases of Listeria and typhoidal and paratyphoidal
Salmonella infection, within 15 days for Cryptosporidium and
Cyclospora infection, and within 7 days for all other infections
due to enteric pathogens. If a patient traveled abroad within
the pathogen-specific exposure window, the infection is assumed to have been acquired abroad and is termed travelassociated. Hospitalization is reported if the patient is admitted
to a hospital within 7 days after specimen collection, and death is
reported as the outcome if it occurs during hospitalization or, for
patients who were not hospitalized, within 7 days after the
specimen collection date.
We categorized travel destinations into 6 world regions and
21 subregions, as defined by the WHO [13]. The North America
region includes only Canada in this analysis. We excluded
travelers who visited multiple regions from regional analyses.
For some pathogens, we analyzed selected species, serogroups,
or serotypes. We considered infections with Salmonella enterica
serotype Typhi to be typhoidal [14]; serotypes Paratyphi A,
Paratyphi B, and Paratyphi C to be paratyphoidal; and all
other or unknown Salmonella serotypes to be nontyphoidal.
We report serotype-specific results for nontyphoidal infections
with serotypes Enteritidis, Typhimurium, and Newport. Infections of paratyphoidal Salmonella exclude infections due
to serotype Paratyphi B var L (1) tartrate 1 (formerly serotype
Java), which do not cause enteric fever [15]. For some analyses of
STEC infections, we considered O157 and non-O157 serogroups
separately. We used data from the Cholera and Other Vibrio
Illness Surveillance system to determine whether isolates from
cases of Vibrio infection were toxigenic and considered cholera
to be infection with toxigenic Vibrio cholerae O1 and O139.
We report species-specific results for Vibrio parahaemolyticus
and Vibrio vulnificus.
Analysis
We analyzed FoodNet reports of cases that indicated whether
the patient had traveled abroad during the exposure window.
The risk of diagnosis with a travel-associated infection after
return to the United States was calculated using data from the
US Department of Commerce, Office of Travel and Tourism
Institute, on the number of US residents traveling by air to
various destinations. Overland travelers were not included; thus,
we did not calculate risks for Mexico and Canada. To calculate
risk, we divided the number of travel-associated infections by the
estimated number of air travelers in the FoodNet catchment
area. When calculating destination-specific risks of infection, we
also excluded all reports from sites that reported travel information for ,30% of cases of infection with a given pathogen.
We calculated frequencies for categorical variables and calculated prevalence ratios to compare travelers with nontravelers.
We used SAS software (version 9.2: SAS Institute, Cary, North
Carolina) for statistical analyses. The map was generated using
ArcView GIS software (version 10; ESRI, Redlands, California).
Travel-Associated Enteric Infections
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Table 1. Demographic Characteristics of Patients With Enteric Infection in the United States, by Patient's Travel Status, Foodborne
Diseases Active Surveillance Network (FoodNet), 2004–2009
Total With Known
Travel Status
Characteristic
Non–Travel-Associated Cases
No.
%
No.
%
64 039
8270
12.9
55 769
87.1
,1
3861
193
2.3
3668
6.6
1–4
9808
718
8.7
9090
16.3
0.53
5–17
18–44
11 774
19 424
1093
3568
13.2
43.1
10 681
15 856
19.2
28.4
0.69
1.52
45–64
12 648
2207
26.7
10 441
18.7
1.43
6524
491
5.9
6033
10.8
0.55
1.00
Total
No.
Travel-Associated Casesa
Prevalence Ratio
Age group (years)
$65
Median (years)
26.8
33.1
0.35
25.5
Sex
Female
32 249
4165
50.4
28 084
50.4
Male
31 681
4094
49.5
27 587
49.5
1.00
109
11
0.1
98
0.2
0.76
White
44 676
5718
69.1
38 958
69.9
0.99
Asian
2126
613
7.4
1513
2.7
2.73
Unknown
Race
Black
5743
339
4.1
5404
9.7
0.42
Other
1001
212
2.6
789
1.4
1.81
Multiracial
1632
161
1.9
1471
2.6
0.74
776
16
0.2
760
1.4
0.14
50
8035
10
1201
0.1
14.5
40
6834
0.1
12.3
1.69
1.19
1.05
AI/AN
PI/NH
Unknown
Ethnicity
Hispanic
Non-Hispanic
6717
903
10.9
5814
10.4
47 945
6100
73.8
41 845
75.0
0.98
9377
1267
15.3
8110
14.5
1.05
Unknown
Hospitalizations
by age group (years)
15 021
1015
12.3
14 006
25.1
0.49
,1
1–4
1007
1625
20
94
10.4
13.1
987
1531
26.9
16.8
0.39
0.78
5–17
2283
177
16.2
2106
19.7
0.82
18–44
3730
359
10.1
3371
21.3
0.47
45–64
3193
250
11.3
2943
28.2
0.40
$65
3183
115
23.4
3068
50.9
0.46
Deaths
229
5
0.1
224
0.4
0.15
Abbreviations: AI/AN, American Indian or Alaska Native; PI/NH, Pacific Islander or Native Hawaiian.
a
The window of exposure for travel is within 30 days of illness onset for Listeria and typhoidal and paratyphoidal Salmonella, within 15 days for Cryptosporidium and
Cyclospora, and within 7 days for all other pathogens.
RESULTS
Demographic Characteristics and Clinical Outcomes
During 2004–2009, travel status was known for 64 039 of 104 374
cases (61.4%) of infection reported to FoodNet. Of these, 8270
(12.9%) were travel associated (Table 1). The percentage of
cases that were travel associated varied little over time, ranging from a high of 16% in 2005 to a low of 12% in 2008, with
no apparent trend.
Patients with travel-associated infections were generally
older than those who had not traveled (median age, 33.1 years
versus 25.5 years) (Table 1). A substantially greater proportion of travelers (43.1%) than nontravelers (28.4%) were
in the 18–44 years age group. Travelers and nontravelers had
similar sex and ethnicity distribution but differed by race.
Travelers were more likely than nontravelers to be Asian
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(7.4% versus 2.7%) and less likely to be black (4.1% versus
9.7%).
Overall, travelers were about half as likely to be hospitalized as
nontravelers (12.3% versus 25.1%), and the percentage
hospitalized was lower for travelers than for nontravelers in
every age group. Five deaths (0.1%) were reported in travelers, compared with 224 deaths (0.4%) in nontravelers.
Travel-associated deaths were caused by Listeria (n 5 1),
V. vulnificus (n 5 1), and nontyphoidal Salmonella (n 5 3).
Pathogens
Three pathogens accounted for .90% of travel-associated
infections: Campylobacter (n 5 3445 [41.7%]), Salmonella
(n 5 3034 [36.7%], of which nontyphoidal Salmonella accounted for 2680 [88.3%], typhoidal Salmonella 235 [7.7%],
and paratyphoidal Salmonella 119 [3.9%]), and Shigella
(n 5 1071 [13.0%]), although travel-associated infections
with all pathogens under surveillance were reported (Table 2).
The same 3 pathogens were also the most common pathogens
reported for nontravelers, accounting for 84.7% of all non–
travel-associated infections. However, proportions differed,
most notably for Campylobacter, which was less common in
nontravelers (26.5% of infections) and nontyphoidal Salmonella,
which was more common in nontravelers (46.6% of infections).
Salmonella enterica serotype Enteritidis was the most common
serotype isolated from both travelers and nontravelers but
was more common among travelers, accounting for 39.7% of
travel-associated Salmonella infections and 17.2% of non–
travel-associated infections.
The proportion of infections that was travel associated varied
widely by pathogen. A high proportion of cholera (100% of
3 cases), typhoidal Salmonella (67.7% of 347 cases), and paratyphoidal Salmonella infections (50.2% of 237 cases) were travel
associated. Similarly, infections with Shigella flexneri (24.4%),
Shigella boydii (44.3%), and Shigella dysenteriae (56.3%) were
often travel associated (Table 2). However, the proportion of
infections that were travel associated was relatively low for Vibrio
infections other than cholera (5.4% for V. parahaemolyticus,
1.2% for V. vulnificus), Yersinia (6.3%), and Listeria (2.7%).
Overall, 6.6% of STEC infections were travel associated, but
non-O157 serogroup infections were much more likely to be
travel associated (15.6%) than were O157 infections (2.7%).
Destinations and Risks
Data on travel destination were available for 7227 travelassociated cases (87.4%). Of these, 7110 patients reported travel
to a single region and 6489 reported travel to a single country and
were included in the regional and country-specific analyses, respectively. Five countries accounted for the destinations visited by
50.6% of patients who traveled to a single country (Table 3).
Mexico was the most common destination reported, accounting
for 2125 travel-associated infections (32.7% of travelers to a single
destination). Other common travel destinations included India
(n 5 533 [8.2%]), Peru (n 5 257 [4.0%]), Dominican Republic
(n 5 201 [3.1%]), and Jamaica (n 5 169 [2.6%]). Overall, travel
destinations were strongly related to racial and ethnic background. Among Asian travelers, 85.0% reported travel to Asia,
compared with 17.2% of non-Asian travelers. Among black
travelers, 58.4% reported travel to Africa, compared with 5.2%
of non-black travelers. Among Hispanic travelers, 94.6% reported travel to Latin America and the Caribbean (LAC),
compared with 50.6% of non-Hispanic travelers.
Table 4 displays the risk per 100 000 air travelers of travelassociated infection, that is, the risk of a laboratory-confirmed
infection diagnosed after return to the United States. Travel to
Africa carried the greatest risk of travel-associated infection
(75.9 cases per 100 000 travelers), followed by Asia (22.7 cases
per 100 000 travelers), and LAC (20.0 cases per 100 000
travelers) (Table 4). Figure 1 displays, by region, both the risk
of travel-associated infection (differentiated by map shading)
and the total number of travel-associated infections and proportion caused by each pathogen.
Over half of all travel-associated infections were in travelers
to LAC, 54.4% of whom reported travel to Mexico (Table 4). In
LAC, the risk of returning with enteric illness varied by subregion and pathogen. Travelers to South America had the region’s highest risk of returning with Campylobacter infection
(26.4 cases per 100 000 travelers) but the lowest of nontyphoidal Salmonella infection (3.4 cases per 100 000 travelers). Travelers to the Caribbean, on the other hand, had
a lower risk of Campylobacter infection (5.2 cases per 100 000
travelers) but had the region’s highest risk of nontyphoidal
Salmonella infection (8.6 cases per 100 000 travelers, Table 4).
Travelers to Central America (Mexico not included because
risks could not be calculated) had the region’s greatest risks of
diagnosis with Shigella (8.6 cases per 100 000 travelers),
Cryptosporidium (2.8 cases per 100 000 travelers), and STEC
(1.0 cases per 100 000 travelers, 69.7% STEC non-O157)
infection after return. In travelers to Mexico, nontyphoidal
Salmonella infection was reported most frequently (870 cases),
followed by Campylobacter (686 cases) and Shigella (378 cases).
Most Cyclospora infections (79.4%) were reported in travelers
returning from LAC, a third of whom had traveled to Guatemala (12 cases). Typhoidal Salmonella (15 cases, 11 in travelers
to Central America) and paratyphoidal Salmonella infections
(9 cases, all Paratyphi B, 8 in travelers to South America) were
both uncommonly reported after travel to LAC.
Asia was the second most common destination, associated
with 1556 infections (21.9%) (Table 4). Over one-third (533) of
these patients reported travel to India. In travelers returning
from Asia, the risk of any enteric infection was 22.7 cases per
100 000 travelers, with Campylobacter infection identified
Travel-Associated Enteric Infections
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Table 2. Distribution of Enteric Infections in the United States by Pathogen, Selected Serotypes, and Patient's Travel Status, Foodborne
Diseases Active Surveillance Network (FoodNet), 2004–2009
Travel-Associated Casesa
Non–Travel-Associated Cases
No.
%
No.
%
Travel-Associated
Cases, %
Campylobacter
3445
41.7
14 782
26.5
18.9
Salmonella
3034
36.7
25 961
46.6
10.5
2680
88.3
25 731
99.1
9.4
1065
39.7
4428
17.2
19.4
Serotype Typhimurium
189
7.1
3630
14.1
4.9
Serotype Newport
104
3.9
2322
9.0
4.3
1245
77
46.5
2.9
14 141
1210
55.0
4.7
8.1
6.0
Typhoidal Salmonella entericab
235
7.7
112
0.4
67.7
Paratyphoidal Salmonella enterica
119
3.9
118
0.5
50.2
Serotype Paratyphi A
102
85.7
32
27.1
76.1
Serotype Paratyphi B
16
13.4
84
71.2
16.0
Serotype Paratyphi C
1
1.0
2
1.7
33.3
1071
13.0
6472
11.6
14.2
689
297
64.3
27.7
5218
922
80.6
14.2
11.7
24.4
S. boydii
31
2.9
39
0.6
44.3
S. dysenteriae
18
1.7
14
0.2
56.3
Unknown
36
3.4
279
4.3
11.4
Pathogen
Nontyphoidal Salmonella enterica
Serotype Enteritidis
Other
Unknown
Shigella
S. sonnei
S. flexneri
Cryptosporidium
317
3.8
3263
5.9
8.9
STEC
257
3.1
3647
6.5
6.6
166
64.6
895
24.5
15.6
75
16
29.2
6.2
2679
73
73.5
2.0
2.7
18.0
Cyclospora
54
0.7
70
0.1
43.5
Vibrio
44
0.5
530
1.0
7.7
16
36.4
282
53.2
5.4
3
6.8
0
0.0
100.0
STEC non-O157
STEC O157
Other
V. parahaemolyticus
V. choleraec
V. vulnificus
1
2.3
83
15.7
1.2
Other
24
54.5
165
31.1
12.7
Yersinia
Listeria
32
16
0.4
0.2
475
569
0.9
1.0
6.3
2.7
Total
8270
100
55 769
100
12.9
a
The window of exposure for travel is within 30 days of illness onset for Listeria and typhoidal and paratyphoidal Salmonella, within 15 days for Crytopsporidium and
Cyclospora, and within 7 days for all other pathogens.
b
Salmonella enterica serotype Typhi.
c
V. cholerae includes toxigenic Vibrio cholerae O1 and O139; data were linked to the Cholera and Other Vibrio Illness Surveillance system to determine if isolates
were toxigenic.
most commonly (15.2 cases per 100 000 travelers) (Table 4).
The risk of nontyphoidal Salmonella infection among travelers
to Asia (5.8 cases per 100 000 travelers) was similar to that
among travelers to LAC, but typhoidal Salmonella (151 cases,
2.4 cases per 100 000 travelers) and paratyphoidal Salmonella
infections (79 cases, 97.5% Paratyphi A, 2.5% Paratyphi B,
1.2 cases per 100 000 travelers) were much more common.
Most of these travelers (89.4% with typhoidal Salmonella and
92.4% with paratyphoidal Salmonella infection) reported travel
to countries in the Indian subcontinent (Bangladesh, India,
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and Pakistan) [16]. STEC infections were uncommon after travel
to Asia (12 cases), but most were STEC O157 (58.3%).
Europe was the third most common destination, with 937
travel-associated infections reported, but travelers to the
European region had the lowest overall risk (8.7 cases per
100 000 travelers). Campylobacter infection was most common
(66.8% of infections) (Table 4). Few infections were reported in
travelers who had returned from Oceania (73 cases, 9.6 cases
per 100 000 travelers), but similar to Europe, Campylobacter
infection was most common (58.9% of infections).
Table 3. Top Destinations to Which US Patients With TravelAssociated Enteric Infections Traveled, Foodborne Diseases
Active Surveillance Network (FoodNet), 2004–2009
Rank
Country
No.
%
2125
32.7
India
Peru
533
257
8.2
4.0
4
Dominican Republic
201
3.1
5
Jamaica
169
2.6
6
China
157
2.4
7
Spain
144
2.2
8
France
135
2.1
9
Costa Rica
116
1.8
10
11
Canada
Thailand
111
111
1.7
1.7
12
Guatemala
109
1.7
13
Ecuador
99
1.5
14
Israel
86
1.3
15
Ethiopia
84
1.3
16
Pakistan
81
1.2
17
Philippines
76
1.2
18
19
Bahamas
El Salvador
72
63
1.1
1.0
20
Italy
1
Mexico
2
3
62
1.0
Other
1698
26.2
Total
6489
100
Travelers returning from the Africa region accounted for
only 7.4% of all travel-associated infections but had the
highest region-specific risk for each infection. Compared
with other world regions, the risk for travelers to Africa was
.2.5 times greater for Campylobacter infection (41.3 cases per
100 000 travelers), .3 times greater for nontyphoidal Salmonella
infection (25.8 cases per 100 000 travelers), .5 times greater for
Shigella infection (19.8 cases per 100 000 travelers, Table 4), and
.7 times greater for Cryptosporidium infection (9.6 cases per
100 000 travelers). The risk of typhoidal Salmonella infection
(2.6 cases per 100 000 travelers) was similar to that among
travelers to Asia, but paratyphoidal Salmonella infections
were rare (1 case).
DISCUSSION
This study provides new insights into the overall contribution
of international travel to enteric infections in the United States
and into large differences in overall and pathogen-specific risks
by destination. Almost 13% of enteric infections reported
to FoodNet were travel-associated. Campylobacter was the
most common infection reported in travelers, followed by
nontyphoidal Salmonella. Our results are strongly driven by
differences in the volume of travel to different destinations;
travel to Africa carried by far the greatest risk of travelassociated infection; however, because Africa is a relatively uncommon destination, it accounted for only a small fraction
of reported cases. By contrast, the risk of travel-associated
infection was much lower among travelers returning from
the LAC region; however, this region accounted for most reports of travel-associated infection. Mexico has long been the
single most common travel destination for US travelers [17];
Table 4. Number and Risk (per 100 000 Air Travelers) of Campylobacter, Nontyphoidal Salmonella, and Shigella Infections in US
Travelers, by Pathogen and World Health Organization Region, Foodborne Diseases Active Surveillance Network (FoodNet), 2004–2009
Total Travel-Associated Infections
Shigellab
Infections
From
No. Region, % Risk
No.
Total, all regionsc
7110
100.0
26 114 000
17.4 3068
43.2
12.8
2313
32.5
5.4
926
13.0
2.5
Latin America and
Caribbeand
3906
54.9
8 367 000
20.0 1459
37.4
13.3
1462
37.4
7.1
618
15.8
3.5
No.
No.
Infections
From
Region, % Risk
Nontyphoidal Salmonella
Infections
From
Region, %
Region
Total
Travelers
Infections, in Catchment
%
Area, No.
Risk
Campylobactera
Risk
Central Americad 2605
66.7
1 568 000
28.4
884
33.9
17.6
980
37.6
7.0
488
18.7
8.6
Caribbean
653
16.7
4 595 000
13.9
154
23.6
5.2
394
60.3
8.6
53
8.1
1.4
South America
616
15.8
2 204 000
25.5
412
66.9
26.4
75
12.2
3.4
70
11.4
3.9
1556
21.9
6 297 000
22.7
700
45.0
15.2
368
23.7
5.8
180
11.6
3.4
Europe
937
13.2
10 097 000
8.7
626
66.8
9.2
255
27.2
2.5
13
1.4
0.2
Africa
527
7.4
652 000
75.9
189
35.9
41.3
168
31.9
25.8
106
20.1
19.8
Canada
Oceania
111
73
1.6
1.0
.
701 000
.
9.6
51
43
45.9
58.9
.
8.6
39
21
35.1
28.8
.
3.0
4
5
3.6
6.8
.
0.9
Asia
a
Campylobacter risks calculated with a denominator of 16 093 000 total travelers. Excludes data from California, Georgia, and Oregon, all years.
b
Shigella risks calculated with a denominator of 20 384 000 total travelers. Excludes data from Georgia, all years.
c
Risk calculations exclude travelers to Mexico and Canada and excludes data from New Mexico and New York for years 2004–2006.
d
Risk calculations exclude travelers to Mexico.
Travel-Associated Enteric Infections
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Figure 1. Risk and distribution of travel-associated enteric infections in US travelers, Foodborne Diseases Active Surveillance Network (FoodNet),
2004–2009. a Canada and Mexico excluded from the risk calculations.
it was also the most common destination in reports of travelassociated infections.
Travelers with enteric infections were typically older than
nontravelers, possibly because young children are less likely
to travel internationally, compared with older children and
adults. Travelers of all ages were less likely to be hospitalized
than nontravelers, even among children and older persons,
the groups more likely to be hospitalized with enteric infections [18]. Travelers may be healthier overall, a phenomenon
known as the ‘‘healthy traveler effect’’ [19]; or other reasons,
such as healthcare received while traveling, might be responsible
for the observation.
Travelers’ racial and ethnic background was strongly associated with travel destination. The high proportion of Asians traveling to Asia, Hispanics traveling to LAC, and blacks traveling
to Africa suggests that many travelers may travel to destinations
in which they have relatives or from which they or their family
emigrated. Other studies have found that travelers visiting
friends and relatives generally have a greater risk of acquiring
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Kendall et al
infection, including intestinal infections, than do tourists or
business travelers [20].
Patterns of infection varied greatly by destination. For example, nontyphoidal Salmonella caused approximately 60% of
travel-associated infections associated with the Caribbean but
,40% of infections associated with Central America and only
12% of infections associated with South America; the pattern
for Campylobacter was the reverse. As another example, the
risk of nontyphoidal Salmonella infection was somewhat lower
for travel to Asia than to LAC, but the risk of typhoidal and
paratyphoidal Salmonella infections was much higher in Asia,
with .80% of these infections associated with travel to Asia. It
is possible that some misclassification of serotype Paratyphi B
var L (1) tartrate1 as serotype Paratyphi B exists in these
data, if testing for tartrate fermentation was not performed to
differentiate these serotypes. As a final example, .80% of
STEC infections were associated with travel to LAC, and most
were caused by STEC non-O157. Among STEC infections associated with travel to Asia, however, most were caused by
STEC O157. Domestically acquired STEC infections are also
more often caused by STEC O157 than by non-O157; our results are consistent with previous studies showing that STEC
non-O157 infections are relatively less common in the United
States than in other countries [21].
The results of this study are most useful for comparisons
across regions and pathogens, not as an indication of the
absolute risks of enteric illness with travel to specific regions.
The data on air travelers do not capture the amount of time
spent abroad and are a unit of arrivals, not persons, but are the
best proxy for person-time exposed to other countries of which
we are aware. In FoodNet, travel-associated infections are
reported only if diagnosed after return to the United States.
Even if symptoms continue after return to the United States,
ill persons may not seek medical care or may not submit
a specimen for laboratory testing. When a specimen is submitted, it may not yield the pathogen causing the illness, or
as is commonly the case for ETEC, the laboratory may not
seek evidence of the pathogen [2, 5, 22]. These factors all tend
to lead to an underestimate of the number of infections. On the
other hand, because all infections diagnosed in the FoodNet
postreturn exposure window are attributed to travel, some
infections acquired in the United States may have been incorrectly categorized as travel associated. Other investigators
have used shorter travel windows before illness onset to define
travel-associated infections [23]. Any overestimation resulting
from misclassification of illnesses as travel associated is likely
to be small, though, and, to the extent that these illnesses were
caused by exposures occurring in the United States, would tend
to obscure differences between travel destinations.
Patterns of risk of enteric infection vary greatly in and among
world regions; these patterns likely provide insights into the
exposures not only of travelers but also of residents. Travelers
and clinicians may use this information and pre- and posttravel
consultations to aid in assessing health risks and to help in
differential diagnosis of infections.
Notes
Acknowledgments. We thank Effie Booth and Mark Sotir for their
contributions to this manuscript, and the health departments and public
health laboratories at FoodNet sites.
Disclaimer. The contents of this work are solely the responsibility of
the authors and do not necessarily represent the official views of the
Centers for Disease Control and Prevention.
Supplement sponsorship. This article was published as part of a supplement entitled ‘‘Studies From the Foodborne Diseases Active Surveillance Network,’’ sponsored by the Division of Foodborne, Waterborne,
and Environmental Diseases of the National Center for Emerging and
Zoonotic Infectious Diseases from the Centers for Disease Control and
Prevention, and the Association of Public Health Laboratories.
Potential conflicts of interest. All authors: No reported conflicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conflicts of Interest. Conflicts that the editors consider relevant to the
content of the manuscript have been disclosed.
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