The impact of international travel on the epidemiology of enteric infections, British Columbia, 2008.
Taylor, Marsha ; MacDougall, Laura ; Li, Min 等
A significant proportion of enteric infections in developed
countries have been associated with international travel. In Sweden, 54%
of Campylobacter infections notified over a 7-year period were linked to
travel outside of Sweden. (1) A pilot study conducted in an urban region
of British Columbia (BC) demonstrated that 38% of enteric infections
reported between 2002 and 2006 were associated with international
travel. (2)
In BC (population 4,381,603), identification and exclusion of
travel-related infections from analysis is necessary to assess the
burden, temporal and geographic trends of locally-acquired infection and
identify local sources and risk factors for enteric infections in order
to prevent and control them. Additionally, understanding the
epidemiology of enteric infections acquired internationally may help to
direct actions and education for travelers.
The goal of this research was to assess the proportion of enteric
infections in BC reported in 2008 that was associated with international
travel in order to better understand local infection trends. This report
describes the temporal, geographic and demographic features of
infections acquired locally and compares them with those acquired
internationally.
METHODS
Laboratory-confirmed cases of reportable enteric infections are
reported to public health authorities. Individuals with such infections
reported between January 1 and December 31, 2008 were interviewed by
environmental health officers in BC using standard forms * to collect
travel information. All infections of salmonellosis, verotoxigenic E.
coli (VTEC), shigellosis, Vibrio parahaemolyticus, botulism, cholera,
listeriosis, typhoid fever, paratyphoid fever, hepatitis A,
cryptosporidiosis, and cyclosporiasis were included. Since the number of
campylobacteriosis infections is high and they are not routinely
interviewed in BC, only a representative proportion was interviewed and
included. Infections of campylobacteriosis were sampled to maintain
seasonal variation. Monthly targets were set based on expected incidence
from 2002 to 2006 for each regional health authority. Cases were
selected systematically (e.g., every second case) in order to meet this
target.
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Each case was classified as having international travel (travel
outside of Canada), travel within Canada (including BC) or no travel (no
travel outside the health authority of residence). The "no
travel" and "travel within Canada" categories were
combined to represent locally-acquired infections.
Acquisition during international travel was deemed confirmed if,
for infections not endemic to BC (typhoid and paratyphoid fever,
cholera, cyclosporiasis, infections of S. dysenteriae), individuals had
travelled to an endemic area during at least part of the incubation
period or had travelled to a non-endemic area outside of Canada for the
entire incubation period. For all other enteric infections,
international acquisition was deemed confirmed if individuals travelled
outside of Canada for their entire incubation period. * Only infections
confirmed as acquired during international travel were included in the
demographic and destination analysis.
Individuals with multiple infections or multiple episodes of the
same infection reported more than 6 months apart were counted as
separate infections. If the episodes with the same infection were within
6 months of each other, case information was reviewed to determine if
the episodes were different based on available information. If no
exposure information was available for an infection, the exposure was
coded as "missing". If the exposure information did not
include information on travel but did identify other exposures (e.g.,
household exposure), the case was classified as "no travel".
Case data and travel status were entered into an electronic system
locally and transferred electronically to the BC Centre of Disease
Control (BCCDC). Data were extracted in April 2009.
Seasonality was assessed for specific diseases for which there was
a large enough number of infections.
Travel destinations for cases of enteric infections were compared
to travel destinations of the general BC population from the 2006
International Travel Survey, (3) which included all overnight visits by
BC residents to international travel destinations, excluding the United
States.
Data were analyzed using Microsoft Access 2003, Microsoft Excel
2003 and EpiCalc 2000 (version 1.02). Chi-square tests were used to
compare proportions and a p-value of <0.05 was considered
significant. 95% confidence intervals were calculated to compare the pro
portion associated with travel to that locally-acquired, by age group.
Population data were obtained from BC Statistics. (4)
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RESULTS
A total of 3,120 enteric infections were reported during the study
period. Overall, 2,210 (70.8%) infections had travel exposure
information available. Infections of cholera, paratyphoid and typhoid
fever had the most complete travel information (100%, 100% and 96%,
respectively), whereas infections of cryptosporidiosis and shigellosis
had the lowest (62% and 71%, respectively) (Table 1).
Of the 2,210 infections with travel information available, 1,326
(60.0%) infections were classified as locally-acquired; of the
locallyacquired, 54.0% had not travelled outside of their health
authority of residence and 133 (6.0%) had travelled within Canada.
International travel accounted for 40.0% (n=884) of all enteric
infections; 701 (31.7%) had confirmed international travel (Table 1).
Cholera, typhoid fever, paratyphoid fever and cyclosporiasis had the
highest proportion of infections associated with international travel
(Table 1).
The proportion of illness associated with confirmed international
travel varied from 26.0% to 45.2% for the different age groups and was
highest among 30 to 39 year olds. The proportion of locallyacquired
infections varied from 54.8% to 74.0%, and was highest among those 60
years and older (Figure 1). The proportion of locallyacquired infections
was significantly higher than infections associated with international
travel for all age groups except for those aged 30-39 (p<0.05).
Between January and April, the number of all infections with
confirmed international travel was higher than those that were
locally-acquired. For the remaining months, the number of infections
that were locally-acquired was higher (Figure 2). Patterns for
salmonellosis and campylobacteriosis were similar to overall enteric
trends.
[FIGURE 1 OMITTED]
[FIGURE 2 OMITTED]
Among infections that were associated with international travel,
the most common destinations were Asia (40%) and Mexico (23%) (Table 2).
Further regional assessment for travel to Asia identified that 61.7% of
confirmed travel-related infections were among travelers to South Asia,
26.3% of infections were acquired in Southeast Asia and 9.1% of
infections were acquired in East Asia. Asia was the most common
destination for acquisition of campylobacteriosis (37%), cholera (100%),
cryptosporidiosis (49%), paratyphoid fever (100%), shigellosis (54%),
typhoid fever (89%) and Vibrio para haemolyticus infection (71%). VTEC
(52%), hepatitis A infection (48%), listeriosis (50%) and salmonellosis
(31%) were most commonly reported after travel to Mexico and
cyclosporiasis (48%) was most commonly reported after travel to South
America.
The proportion of infections associated with travel to Europe and
Oceania was significantly lower than the proportion of the general BC
population who travelled to these destinations. However, the proportion
of infections associated with travel to all other destinations, besides
the Caribbean, was significantly higher among enteric infections
(p<0.05).
Among campylobacteriosis cases, the proportion associated with
travel to Africa, Asia (majority to South and Southeast Asia), South
America and Mexico was significantly higher compared to that in the
general population of BC. For infections with VTEC, the proportion of
travelers to South America and Mexico was significantly higher; among
salmonellosis cases, the proportion was significantly higher for
travelers to the Caribbean and Mexico; and among shigellosis cases, the
proportion was significantly higher among travelers to Africa, Asia
(majority to South Asia), Central America and South America.
CONCLUSIONS
Based on this study, 31.7% of enteric infections in BC were
associated with international travel in 2008. For specific enteric
infections, this ranged from 16% to 100%. To our knowledge, this is the
first provincial assessment of the impacts of international travel on
the epidemiology of enteric infections that has been published from
North America.
Notably, 20-30% of common endemic infections (salmonellosis,
campylobacteriosis and VTEC) were associated with international travel.
Other studies have also documented associations between enteric
infections and travel. (5) In BC, a study of risk factors for hepatitis
A identified that 26% of infections reported between 1998 and 2004 were
acquired through travel to another country. (6) Previous work in New
Zealand demonstrated a significant association between infections of
shigellosis and salmonellosis and overseas travel. (7) Four studies from
Sweden showed that the proportions of typhoid fever and paratyphoid
fever associated with international travel (79% and 86%, respectively)
are comparable to our results, whereas the proportions of
campylobacteriosis (54%) and non-typhoidal salmonellosis (78%)
associated with travel were higher in the Swedish studies. This may be
due to a difference in travel habits whereby Europeans frequently travel
to countries within Europe that may have higher rates of enteric
infections than Sweden. (1,8-10) Compared to the Swedish study, the
proportion of shigellosis infections associated with international
travel in our study was higher at 60%. This proportion may be an
over-estimate as the travel status for shigellosis was not as complete
in our analysis. Further assessment by Shigella species may help
understand these trends, but was not possible due to data limitations.
Adults between the ages of 30-39 years had the highest proportion
of infection associated with international travel. According to
Statistics Canada, individuals between the ages of 45 and 64 most
frequently travel overseas. (11) The higher proportion of illness in the
younger age range may suggest that this is a group that: may not seek
medical advice prior to travel; travels to higher-risk areas; is less
likely to take precautions in regards to food and drink; or participates
in higher-risk activities while traveling. Alternatively, older adults,
who do the majority of travel, may be less likely to seek medical
attention due to their frequency of travel and tolerance for enteric
symptoms. Locally-acquired infections were more common in all age groups
compared to those acquired during international travel, however the
proportion of locally-acquired illness was highest among those 60 years
and older and those less than 19 years. This pattern is typical of
enteric illness, which has a higher incidence and severity in the
elderly and young children--two groups who may also be more likely to
seek medical attention. Travel medicine advice and counseling may need
to be adapted to formats more likely to reach young adults, such as the
use of travel websites and social networking tools.
There were clear seasonal trends in our findings, consistent with
the seasonality of travel from Canada; during the winter, people take
holidays and visit friends and family in warmer destinations, (11)
whereas during summer, people travel locally or to Europe. Historical BC
data suggest that most enteric infections peak through the summer months
and this analysis identified that the majority are locally-acquired.
(12) The reason for this is uncertain and could be due to behavioural,
ecological or food distribution patterns. Public health actions and
messages related to local enteric exposures and risks may be most
effective when communicated before the summer months. For travelers,
health messaging may be most effective if communicated throughout the
fall and early winter seasons. This could be through general public
health messaging or tailored travel health advice.
The proportion of enteric infections associated with travel to
Africa, Asia, Mexico, Central America and South America was
significantly higher than the proportion of all BC visits to these
countries. Improving awareness in travelers before they travel,
particularly among young adults and those travelling to the
aforementioned locations, would be valuable. Pathogen and destination
trends may allow specific interventions to be put in place and may help
us to better understand disease patterns. Our analysis showed that 4.4%
of enteric infections were associated with travel to the US. Although
comparison data were not available, it is likely that a much greater
proportion of BC residents travelled to the US.
As this analysis only represents one year of lab-confirmed BC data,
which did not include all enteric infections and for which travel
information was limited for some infections, there are some limitations
to the interpretation. However, the findings are comparable to other
international studies and review of additional years of data is ongoing.
This study has shown that the proportion of enteric infections in
BC associated with international travel is significant and can have an
impact on the interpretation of trends, rates and burden of enteric
infections in BC. For public health professionals, understanding the
proportions and epidemiology for locally-acquired infections and those
associated with international travel can impact the prioritization and
types of public health actions and interventions taken to prevent
infections in these two very different risk settings.
Acknowledgements: The authors acknowledge representatives from
Fraser Health Authority, Interior Health Authority, Northern Health
Authority, Vancouver Coastal Health Authority and Vancouver Island
Health Authority for their support of this work; Sara Forsting, VCH, for
data extraction; Colette Gaulin, BCCDC, for review of the manuscript;
and the clinical microbiology laboratories in BC responsible for
diagnosis of enteric infections.
Conflict of Interest: None to declare.
Received: December 1, 2009
Accepted: March 20, 2010
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(9.) Ekdahl K, Andersson Y. Regional risks and seasonality in
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(10.) Ekdahl K, de Jong B, Wollin R, Andersson Y. Travel-associated
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(11.) Statistics Canada. International Travel, 2007. Available at:
http://www.statcan.gc.ca/pub/ 66-201-x/2007000/t030-eng.htm (Accessed
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(12.) BC Centre for Disease Control. Annual Summary of Communicable
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* Available at: http://www.bccdc.ca/dis-cond/CDSurveillanceForms/
default.htm#heading2 (Accessed November 2009).
* The exposure periods used were: salmonellosis-3 days, VTEC-10
days, shigellosis-4 days, Vibrio parahemolyticus infection-3 days,
botulism-3 days, cholera-2 days, listeriosis-70 days, typhoid fever-21
days, paratyphoid fever-10 days, hepatitis A-50 days,
cryptosporidiosis-12 days, cyclosporiasis-14 days and
campylobacteriosis-10 days.
Marsha Taylor, MSc, [1] Laura MacDougall, MSc, [1] Min Li, mha, [1]
Eleni Galanis, MD, mph, frcpc, [1,2] BC Enteric Policy Working Group *
Author Affiliations
[1.] British Columbia Centre for Disease Control, Vancouver, BC
[2.] School of Population and Public Health, University of British
Columbia, Vancouver, BC
* Working Group Members: Judi Ekkert, Interior Health Authority
(IHA); Larry Gustafson, Fraser Health Authority (FHA); Jessica Ip,
Vancouver Coastal Health Authority; Jennifer Jeyes, Northern Health
Authority; Craig Nowakowski, Vancouver Island Health Authority; Robert
Parker, IHA; Jason Stone, FHA
Correspondence: Marsha Taylor, BC Centre for Disease Control, 655
West 12th Ave, Vancouver, BC V5Z 4R4, Tel: 604-707-2544, Fax:
604-707-2516, E-mail: marsha.taylor@bccdc.ca
Table 1. Number, Rate, Proportion and Location of Acquisition of
Enteric Infections, January 1-December 31, 2008, BC
Infection Number of Rate/100,000
Infections
Campylobacteriosis 1646 37.6
Cholera 2 0.0
Cryptosporidiosis 118 2.7
Cyclosporiasis 32 0.7
Verotoxigenic E. coli infection 114 2.6
Hepatitis A 39 0.9
Listeriosis 22 0.5
Paratyphoid Fever 29 0.7
Salmonellosis 845 19.3
Shigellosis 203 4.6
Typhoid Fever 48 1.1
Vibrio Parahaemolyticus infection 22 0.5
Total 3120 71.2
Infection Number Number of
with Travel Unconfirmed
Information International
Available Travel Infections
(%)
Campylobacteriosis 1005 45 (4.5)
Cholera 2 0 (0.0)
Cryptosporidiosis 73 11 (15.1)
Cyclosporiasis 27 8 (29.6)
Verotoxigenic E. coli infection 98 12 (12.2)
Hepatitis A 34 7 (20.6)
Listeriosis 19 1 (5.3)
Paratyphoid Fever 29 6 (20.7)
Salmonellosis 713 71 (10.0)
Shigellosis 145 13 (9.0)
Typhoid Fever 46 6 (13.0)
Vibrio Parahaemolyticus infection 19 3 (15.8)
Total 2210 183 (8.3)
Infection Number of Number of
Confirmed Locally-acquired
International Infections (%)
Travel
Infections (%)
Campylobacteriosis 273 (27.2) 687 (68.4)
Cholera 2 (100.0) 0 (0.0)
Cryptosporidiosis 24 (32.9) 38 (52.1)
Cyclosporiasis 17 (63.0) 2 (7.4)
Verotoxigenic E. coli infection 17 (17.3) 69 (70.4)
Hepatitis A 12 (35.3) 15 (44.1)
Listeriosis 3 (15.8) 15 (78.9)
Paratyphoid Fever 21 (72.4) 2 (6.9)
Salmonellosis 202 (28.3) 440 (61.7)
Shigellosis 88 (60.7) 44 (30.3)
Typhoid Fever 38 (82.6) 2 (4.3)
Vibrio Parahaemolyticus infection 4 (21.1) 12 (63.2)
Total 701 (31.7) 1326 (60.0)
Table 2. Comparison of Travel Destinations for BC Residents
(2006) and Enteric Infections Associated with
International Travel (2008)
Destination Proportion of Proportion of P-value
BC Residents Enteric Infections
with Travel to with Travel to
Destination (%) Destination (%)
Europe 42.3 6.9 0.00
Africa 3.7 6.8 0.00
Asia 27.3 39.8 0.00
Central America 0.8 2.2 0.01
Caribbean 6.9 7.0 0.94
South America 1.5 6.8 0.00
Oceania 5.4 1.0 0.00
Mexico 12.0 23.4 0.00
US --* 4.4
* US travel data not available for BC residents
