174

ORIGINAL ARTICLE

Patient Awareness of Need for Hepatitis A Vaccination (Prophylaxis)

Before International Travel

Stephen J. Liu, MPH, Umid Sharapov, MD, MSc, and Monina Klevens, DDS, MPH
Centers for Disease Control and Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention,
Division of Viral Hepatitis, Epidemiology and Surveillance Branch, Atlanta, GA, USA

DOI: 10.1111/jtm.12186

Downloaded from http://jtm.oxfordjournals.org/ by guest on November 28, 2016

Introduction. Although hepatitis A virus (HAV) infection is preventable through vaccination, cases associated with international
travel continue to occur. The purpose of this study was to examine the frequency of international travel and countries visited among
persons infected with HAV and assess reasons why travelers had not received hepatitis A vaccine before traveling.
Methods. Using data from sentinel surveillance for HAV infection in seven US counties during 1996 to 2006, we examined the
role of international travel in hepatitis A incidence and the reasons for patients not being vaccinated.
Results. Of 2,002 hepatitis A patients for whom travel history was available, 300 (15%) reported traveling outside of the United
States. Compared to non-travelers, travelers were more likely to be female [odds ratio (OR) = 1.74 (95% confidence interval [95%
CI], 1.35, 2.24)], aged 0 to 17 years [OR = 3.30 (1.83, 5.94)], Hispanic [OR = 3.69 (2.81, 4.86)], Asian [OR = 2.00 (1.06, 3.77)], and
were less likely to be black non-Hispanic [OR = 0.30 (0.11, 0.82)]. The majority, 189 (61.6%), had traveled to Mexico. The most
common reason for not getting pre-travel vaccination was Didnt know I could [or should] get shots [100/154 (65%)].
Conclusion. Low awareness of HAV vaccination was the predominant reason for not being protected before travel. Different
modes of traveler education could improve prevention of hepatitis A. To highlight the risk of infection before traveling to endemic
countries including Mexico, travel and consulate websites could list reminders of vaccine recommendations.

H epatitis A is a vaccine-preventable disease

caused by the hepatitis A virus (HAV), pri-
marily transmitted by the fecaloral route, through
either person-to-person contact, or consumption
of HAV-contaminated food or water.1 4 Since the
introduction of the hepatitis A routine childhood
immunization schedule in states west of the Mississippi
River in 1996 and the nationwide universal infant
vaccination in 2006, more cases of HAV infection are
attributable to more international travel to endemic
countries (45.8% of investigated cases).1,5 7
The most common risk factor for hepatitis A
infection is international travel.8 International trav-
elers should be vaccinated, as also supported by a
2009 estimate showing that the risk of infection for
nonimmune travelers who visit areas with interme-
diate and high endemicity is 6 to 30 per 100,000
individuals per month traveled.9 For those less than
Corresponding Author: Stephen J. Liu, MPH, Division of
Viral Hepatitis, Epidemiology and Surveillance Branch, 1600
Clifton Road NE, Mail Stop, G-37, Atlanta, GA 30333, USA.
E-mail: STL45@pitt.edu
40 years of age, one dose of monovalent hepatitis A
vaccine is sufficient for short-term protection.10 Other
vaccination series (three doses in 21 days for rapid
schedule for combined hepatitis A-hepatitis B vaccine)
before visiting an intermediate or highly prevalent
area are also safe and effective against hepatitis A
infection.10
A study based on data from the 2010 National Health
Interview Survey reported that significantly more trav-
elers to hepatitis Aendemic countries (26.6%) received
at least one dose of HAV vaccine compared with 12.7%
among non-travelers.11 However, one study conducted
at a New York airport showed that, despite the large
number of experienced travelers, many did not seek
country-specific immunizations or any travel advice:
only 14% of travelers to hepatitis Aprevalent areas
received HAV vaccination.12
Using data from the Sentinel Counties Study of
Acute Viral Hepatitis,1 the purpose of the present study
was to examine the frequency of international travel
and countries visited among persons infected with HAV
and assess the reasons why travelers had not received
hepatitis A vaccine before traveling.

Published 2015. This article is a U.S. Government work and is in the public domain in the USA. 1195-1982
Journal of Travel Medicine 2015; Volume 22 (Issue 3): 174178
Patient Awareness of Hepatitis A Vaccination Before Travel
Methods
During 1982 to 2006, the Centers for Disease Con-
trol and Prevention (CDC) supplemented routine
surveillance with the Sentinel Counties Study of Acute
Viral Hepatitis.1 Methods for the Sentinel Coun-
ties Study have been previously described.1 Briefly,
the population-based study collected information on
patients with acute viral hepatitis (A, B, and C) who
reported to one of the seven county health depart-
ments as follows: Contra Costa County, CA (1996
only); San Francisco County, CA (20002006); Mult-
nomah County, OR (19962006); Jefferson County,
AL (19962006); Denver County, CO (19962006);
Pinellas County, FL (19962006); and Pierce County,
WA (19962006).
Serum specimens from patients were collected and
tested for markers of acute infection within 6 weeks
of onset of illness. For the current study, data were
analyzed for persons who were diagnosed with HAV
infection. A case of HAV infection was defined as a
person with a positive test result for IgM antibodies
to HAV (anti-HAV) and who had a discrete onset of
a physician-diagnosed clinical illness compatible with
hepatitis. Each patient was interviewed by a trained
study nurse using a standardized questionnaire. This
questionnaire was 13 pages long and collected infor-
mation on demographic characteristics of the patient,
clinical and laboratory data for HAV infection, and
importantly, all the potential risk factors (travel, immu-
nization, child care, food, work, sexual history, and
drug use). The questionnaire is also described in other
articles.1,13
International travelers were defined as persons who
traveled outside of the United States. HAV patients were
asked to indicate or list up to three countries visited in
the 2 to 6 week time period before the onset of the ill-
ness. The countries reported were grouped into World
Health Organization (WHO) country regions: Africa,
Americas, Eastern Mediterranean, Europe, Southeast
Asia, and Western Pacific.
In 1996, the questionnaires were updated with ques-
tions about international travel during the patients
incubation period and whether the person received
immunoglobulin or hepatitis A vaccine before travel-
ing. In 1998, the questionnaires added reasons for not
receiving hepatitis A vaccine. The questionnaires were
updated in 2001 and 2003 to include additional reasons
(years grouped in Table 3).
We analyzed the data for all the patients with hep-
atitis A from January 1, 1996, to December 31, 2006,
to determine the proportion who reported international
travel and the countries visited and to assess reasons
why travelers had not been vaccinated against hepatitis
A before traveling. Comparisons between HAV-infected
travelers and non-travelers were performed by demo-
graphic characteristics. We calculated the prevalence
estimates, Chi-squared tests for independence, and odds
ratios (ORs) using SAS 9.3 (Cary, NC). Hepatitis A
175
patients who did not provide data about travel were not
included.
All activities were part of the public health surveil-
lance efforts and were determined as non-research
and exempt from Institutional Review Board at
the CDC.
Results
During 1996 to 2006, a total of 2,181 cases of HAV
infection were reported from the seven sites. There
were 2,002 persons with available travel history, of
which 300 (15%) reported travel outside the United
States during the incubation period, 1,702 reported
no international travel during the incubation period,
and 179 patients did not provide information about
travel. These travelers with HAV infections were more
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likely to be female (OR = 1.74, Table 1), children
aged 0 to 17 years (OR = 3.30), Hispanic (OR = 3.69),
Asian (OR = 2.00), and were less likely to be black
non-Hispanic (OR = 0.30). In general, age group and
race/ethnicity were significantly different (p < 0.001)
among these HAV case travelers. Most of the travel-
ers were reported from Denver County, CO (19.0% of
patients) and the least from Pinellas County, FL (9.5%).
The 300 HAV-infected persons who traveled indi-
cated 307 destination countries. There were seven per-
sons who reported traveling in two different regions
in the 2 to 6 week time period before disease onset.
The most common destination region was the Amer-
icas (n = 243, 79.2%), and Mexico was the most com-
mon country (189, 61.6%) (Table 2). The number of
patients reporting travel to other countries varied from
30 (9.8%) in Europe to 6 (2.0%) in Africa.
Table 3 shows the reasons reported by 154 infected
travelers for not receiving HAV vaccine by 2- to 4-year
intervals. The most common reason the HAV-infected
persons selected for not being vaccinated was Didnt
know I could get shots, or Didnt know I needed it
which accounted for a total of 65% of all the reasons.
Discussion
This is the first report describing surveillance data from
multiple US counties about international travel patterns
of confirmed cases of hepatitis A and the travelers rea-
sons for not receiving hepatitis A vaccine. We found
that the most common reason the HAV-infected per-
sons did not get vaccinated was not knowing that one
could or should get shots. This suggests that in this time
period, the patients might not be aware of a vaccine
and/or unaware of the recommendation for immuniza-
tion when visiting countries with intermediate or high
endemicity of hepatitis A. The response: Did not know
it was needed became an option in 2003 to 2006 and
was the most common response during that time. It is
possible that this reason increased in recent years, or was
the true reason in previous years, but was not an explicit
J Travel Med 2015; 22: 174178
176 Liu et al.

Table 1 Demographic characteristics of hepatitis A patients by international travel history, Sentinel Counties, United States,
1996 to 2006

Travel outside the United States

Yes (%) No (%) Total Odds ratio (95% CIs)

Male 177 (12.7) 1215 (87.3) 1392 Ref.

Female 123 (20.2) 486 (79.8) 609 1.74 (1.35, 2.24)
Total 300 (15.0) 1701 (85.0) 2001*
017 106 (32.0) 225 (68.0) 331 3.30 (1.83, 5.94)
1829 53 (10.8) 436 (89.2) 489 0.85 (0.46, 1.57)
3044 79 (9.8) 725 (90.2) 804 0.76 (0.42, 1.37)
4559 47 (18.2) 211 (81.8) 258 1.56 (0.83, 2.92)
60+ 15 (12.5) 105 (87.5) 120 Ref.
Total 300 (15.0) 1702 (85.0) 2002*
Race
White non-Hispanic 156 (11.7) 1175 (88.3) 1331 Ref.
Black non-Hispanic 4 (3.8) 101 (96.2) 105 0.30 (0.11, 0.82)

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Amer Indian/AK Native, non-Hispanic 1 (3.7) 26 (96.3) 27 0.29 (0.04, 2.15)
Asian/Pacific Islander non-Hispanic 13 (21.0) 49 (79.0) 62 2.00 (1.06, 3.77)
Hispanic 120 (32.9) 245 (67.1) 365 3.69 (2.81, 4.86)
Other/unknown 6 (5.4) 106 (94.6) 112 0.43 (0.18, 0.99)
Total 300 1702 2002*
CIs = confidence intervals.
*Different totals due to missing data on travel and demographic characteristics.

Table 2 Regions/countries visited by hepatitis A patients
during the 2 to 6 weeks before illness, Sentinel Counties,
1996 to 2006
WHO region
Africa
Americas (total)
Caribbean
Central America
Mexico
South America
Eastern Mediterranean
Europe
Southeast Asia
Western Pacific
Total
Results from WHO regions are shown in bold.
WHO = World Health Organization.
option at the time. There is also a possibility that some
medical providers are simply not recommending vac-
cine to at-risk patients. A sample of patients with chronic
liver disease showed that only 63% were recommended
hepatitis A vaccine by their care provider.14
The CDC and other researchers have been recom-
mending hepatitis A vaccine for persons traveling to
or working in countries that have high or intermedi-
ate endemicity of infection since the vaccine became
available in 1996.3,10 Hepatitis A vaccination coverage
among US travelers to endemic countries is twice as
high as coverage for non-travelers (26.6% vs 12.7%),
but is still low overall and needs to be improved.11
Most (61.6% or 189 of the 307 countries visited
by the travelers) hepatitis A patients who traveled did
so to Mexico, and, while hepatitis A is endemic in
Mexico, hepatitis A vaccination is not routine there.15
In countries of high and intermediate endemicity, there
is a greater chance for children to be exposed and
Frequency (%)
develop asymptomatic infection.3 In addition, the sero-
6 (2.0) prevalence of anti-HAV among adults decreased slightly
243 (79.2 ) in the United States from 1988 to 2006.16 Patients in
2 (0.7) this study could have been either unvaccinated Ameri-
33 (10.8) can tourists or unexposed (those unvaccinated and not
189 (61.6) exposed to prior HAV infection) Mexican-Americans
19 (6.2) who traveled from the United States to Mexico, where
7 (2.3) they became infected with HAV.
30 (9.8)
There is a large amount of traffic between the
14 (4.6)
United States and Mexico, due in part to its prox-
7 (2.3)
307
imity and land border access. According to the US
Department of Transportation, about 164 million peo-
ple crossed a USMexico port of entry via truck, train,
bus, personal vehicle, or by pedestrian travel in 2012.17
According to one study, which analyzed data from the
Border Infectious Disease Surveillance (BIDS), there
are more than three times more cases of hepatitis A
in Mexican jurisdictions than in the US counties.15
In another study, almost one-half of the US patients
traveled across the border during their incubation
periods.8
In this analysis, Hispanics encompassed the highest
percentage of persons to have traveled before the onset
of illness than those of other race/ethnicities. This is
consistent with the large number of persons of Mexican
and Hispanic descent who may be visiting friends and
relatives.
Females and persons aged less than 18 years were
more likely to be HAV-infected travelers. This could
be because women may travel more frequently with

J Travel Med 2015; 22: 174178

Patient Awareness of Hepatitis A Vaccination Before Travel 177

Table 3 Reasons HAV patients reported for not receiving hepatitis A vaccination before international travel, Sentinel
Counties, 1998 to 2006

1998 to 2000 2001 to 2002 2003 to 2006 Total

Time period* (% ) (% ) (% ) (% )

Reason for no vaccine/ Did not know could or should get shots
immune globulin Did not know could get shots 62 (70) 17 (50) 2 (6) 81 (53)
Did not know it was needed 19 (61) 19 (12)
Too late to receive shot 1 (1) 1 (3) 0 2 (1)
Too expensive 1 (1) 0 0 1 (1)
Did not know where to get shots 1 (1) 1 (3) 0 2 (1)
MD did not recommend 7 (20) 1 (3) 8 (5)
Do not believe in shots 1 (3) 0 1 (1)
Never got around to it 2 (6) 2 (1)
Other 24 (27) 7 (20) 7 (26) 38 (25)
Total 89 34 31 154
HAV = hepatitis A virus.
*Time periods were grouped based on questionnaire responses.

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Percent of all reasons in the time period.
Response was not collected in these years.

families to other countries, and children may not prac- Acknowledgments

tice careful hygiene compared with others.
Electronic platforms could be a source of
educating travelers about hepatitis A and other
vaccine-preventable diseases. Research shows that 83%
of leisure and 76% of business travelers make travel
plans on web sites.18 There are potential ways to take
advantage of the large proportion of travelers accessing
online resources. On travel search and airline-booking
websites, there could be a link or pop-up of health
recommendations for travelers alerting them to diseases
endemic in certain regions. Obtaining travel visas often
requires visiting the consulate, where travelers could
also receive health information. In addition, consulate
web sites could be a source of health information
for travelers.
There are several study limitations that should be
noted. About 8% of persons did not provide information
about international travel, and approximately one-half
of the 300 hepatitis A patients who traveled to the
endemic countries did not provide reasons for not being
vaccinated. Further, the questionnaires differed slightly
through the addition of new questions over the study
period. Also, there were a large number of unknown
responses and invalid answers for reasons of no vaccina-
tion before travel, as well as missing race/ethnicity infor-
mation. Finally, the counties included in our study may
not be representative of other counties in the United
States, and other counties/states might have a higher
proportion of the population traveling to Mexico or
other endemic countries.
Despite these limitations, our findings suggest that
the public needs to be more informed about hepatitis A,
options for vaccination, and the risks of infection while
traveling. This could increase the immunization rates to
decrease hepatitis A transmission by limiting the persons
carrying HAV from endemic countries.
This work was supported in part by the Research
Participation Program at the CDC, administered by the
Oak Ridge Institute for Science and Education through
an interagency agreement between the US Department
of Energy and CDC. The CDC funded the primary
authors salary.
Declaration of Interests
None of the authors have financial and personal rela-
tionships with other people or organizations that could
inappropriately influence this paper.
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