Download Measles Exportation From Japan to the United States, 1994 to 2006

82
Measles Exportation From Japan to the United States,
1994 to 2006
Hiroshi Takahashi, MD* and Hiroshi Saito, MD†
*Overseas Travelers’ Clinic, Nagano Prefectural Suzaka Hospital, Suzaka City, Nagano, Japan; †Director’s Office,
Nagano Prefectural Suzaka Hospital, Suzaka City, Nagano, Japan
DOI: 10.1111/j.1708-8305.2008.00183.x
Background. Imported measles cases and outbreaks involving Japanese travelers have been reported from the United
States and other countries. For the United States, Japan is the top country of origin. The aims of this study were to analyze measles exportation trends from Japan to the United States and to suggest recommendations for improving monitoring and control in both countries.
Methods. Reviewing all exportation cases reported to the Centers for Disease Control and Prevention and sentinel
measles activity data monitored by the Japanese Ministry of Health between January 1994 and December 2006 (observation period).
Results. A total of 63 cases were reported (median = 4 cases per year). Cases ranged in age from 9 months to 53 years
(median = 17 y). Peaks occurred at 13 to 26 years and 12 to 35 months. Six cases were US citizens and 57 Japanese. Ten
cases were reported in July and August, followed by eight in February and March. Twenty-seven cases were reported
from Hawaii, followed by 15 from California and 6 from New York. Seven cases developed the secondary spread. Three
of the cases had previously received one dose of measles vaccine, compared to 35 who were never immunized (25 cases
unknown). During the observation period, measles activity exceeded the warning level in 157 weeks, with measles
exportation occurring the subsequent week for 30 of these weeks. In comparison, during the 521 weeks in which measles
activity was below the warning level, exportation of measles the following week was observed for 21 of those weeks
(OR = 5.62, 95% CI = 3.12–10.2, p < 0.001).
Conclusions. Trend of exported measles cases from Japan to the United States has corresponded with the measles
activity trend in Japan. Most of the cases were unvaccinated. This international health problem should be solved by
strong leadership of Japanese public health professionals.
A
lthough Japan has made significant financial
contributions to global measles control efforts,1
measles remains highly endemic in this country.
During the 1990s, approximately 20,000 to 30,000
cases of measles were reported, although the actual
number of cases was likely 10 times higher.2 The
Ministry of Health, Welfare and Labor research
group reported 33,812 total cases between January
and December 2001, based on sentinel surveillance
data. However, the annual number of measles cases
was estimated to be as high as 286,000.3 Uncontrolled measles in Japan is primarily due to low
Corresponding Author: Hiroshi Takahashi, MD,
Overseas Travelers’ Clinic, Nagano Prefectural Suzaka
Hospital, 1332 Suzaka City, Nagano 382-0091, Japan.
E-mail: [email protected]
vaccination coverage. Since 1976, National law
mandated that one dose of measles vaccine be administered to all children at 1 year of age. Despite
this policy, the estimated measles vaccine coverage
nationwide was only 79.4% in 2004.4 The measles–
mumps–rubella (MMR) vaccine had been introduced during 1989 to 1993 but later withdrawn due
to unexpected increases in cases of aseptic meningitis stemming from use of the Urabe mumps antigen.
Until March 2006, each monovalent vaccine had
been administered separately, further hampering
efforts to increase vaccine coverage.5 Although the
magnitude of measles epidemics in Japan has been
waning, epidemics occur every several years (ie,
1984, 1991), when the virus starts to disseminate
among the accumulated susceptible population.
In recent years, approximately 16 million Japanese
© 2008 International Society of Travel Medicine, 1195-1982
Journal of Travel Medicine, Volume 15, Issue 2, 2008, 82–86
Measles Exportation From Japan to United States
have been traveling abroad annually. As a result, imported measles cases and outbreaks involving Japanese travelers have been reported from the United
States,6 Australia,7 and Brazil.8 In 2000, Japan was
the leading exporter of measles to the United
States.9 Each case has been investigated and reported by state and local health jurisdictions, with
information published periodically by the US Centers for Disease Control and Prevention (CDC) in
the Morbidity and Mortality Weekly Report. However,
demographic information and immunization status
of these cases, in comparison with concurrent measles activity in Japan, have not been previously described. We analyzed measles exportation trends
from Japan to the United States and suggest recommendations for improving epidemic monitoring
and control in both countries.
Methods
In the United States, reported cases of measles are
classified by CDC into one of the following categories: imported virus case, importation-linked
case, and unknown-source case. They are published
on CDC’s “Measles Update.”10 Cases were listed
in terms of reporting health jurisdiction in United
States, age, sex, date of onset, immunization histories, and secondary spread (eg, due to an outbreak).
Using this database, we reviewed all importation
cases from Japan between January 1994 and
December 2006.
The Japanese Ministry of Health monitors measles activity weekly by collecting data from approximately 3,000 sentinel medical facilities nationwide.
The Ministry issues an “epidemic warning” if the
number of cases per sentinel site exceeds 0.15, the
normal activity limit.11 We obtained weekly levels of
measles activity in Japan from week 1 of 1994 to week
52 of 2006 from “Infectious Disease Weekly Report.”12 To assess the association between weekly domestic measles activity and the occurrence of measles
exportation, we focused on measles activity 1 week
prior to onset of illness of exported cases, as well as
activity 1 week prior to onset of nonexported cases.
To estimate association between measles exportation (by number of weeks) and level of weekly measles
activity in Japan, odds ratios, 95% confidence intervals, and chi-square tests were calculated using SPSS
version 13.0 (SPSS Institute, Cary, NC, USA).
Results
During the observation period, a total of 63 imported virus cases from Japan (hereafter “index
83
case”) were reported to CDC. In 2001, measles activity was the highest, with the largest 18 index
cases. In 2004, 2005, and 2006, it was low and no
case was reported. The mean was 4.8 cases per year
and the median was 3 (Figure 1). Cases ranged in
age from 9 months to 53 years (median = 17 y). Peaks
occurred at 13 to 26 years, followed by 12 to 35
months of age (the age of one Japanese female was
unknown) (Figure 2). Six cases were US citizens and
57 Japanese citizens. The male-to-female ratio
was 15:16. Ten cases were reported in July and
August, with eight in February and nine in March
(Figure 3).
Twenty-seven (43%) cases were reported from
Hawaii, followed by 15 (24%) from California and 6
(10%) from New York. Two cases each were reported from Washington, Oregon, Texas, and one
case each was reported from Rhode Island, Pennsylvania, Indiana, Michigan, Nebraska, Kansas,
Florida, Colorado, and Alaska. Four clusters involving Japanese group tourists were reported from
California (two clusters involving two cases and
four cases, respectively), Hawaii (three cases), and
New York (four cases). Seven cases resulted in secondary spread in the United States. In August 1998,
a 4-year-old Japanese boy from Yokohama visiting
Anchorage became the index case of a large measles
outbreak involving 33 high school students.
Three (5%) of the cases had previously received
one dose of measles vaccine in compliance with the
national immunization schedule, compared to 35
(56%) who were never immunized. Measles vaccination status was unknown for the remaining 25
cases. Of six US citizen cases, one (41 y old) had vaccine, four (28 y, 16 y, 2 y, and 9 mo old) had none,
and one (53 y old) remained unknown. They traveled Japan on business, tourism, and visiting
relatives.
Figure 1 Index cases of exported measles (n = 63) from
Japan to the United States (left scale) with annual
measles activity (case per sentinel site, right scale), by
year, 1994 to 2006.
J Travel Med 2008; 15: 82–86
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Takahashi and Saito
Table 1 Association between measles exportation (by
number of weeks) and level of weekly measles activity
in Japan
Exportation (+) Exportation (−) OR 95% CI
≤0.15 per 30
sentinel
<0.15 per 21
sentinel
127
5.62 3.12–10.2
500
p < 0.001.
Figure 2 Index cases of exported measles from Japan to
the United States, by age-group and nationality, 1994
to 2006.
*Excluded one Japanese female (age unknown).
From January 1994 through December 2006
(678 wk in total), annual measles activity was higher
in 2001 (12.1 cases per sentinel-per-year), 1996
(9.56), and 1994 (9.14) but has dramatically declined
from 2002 and on. The trend of measles exportation corresponded with this activity (Figure 1).
During the 678 weeks, measles activity exceeded
the warning level in 157 weeks, with measles exportation occurring the subsequent week for 30 of these
weeks. In comparison, during the 521 weeks in
which measles activity was below the warning level,
exportation of measles the following week was observed for 21 of those weeks. Association between
measles exportation (by number of weeks) and level
of weekly measles activity in Japan was OR = 5.62,
95% CI = 3.12 to 10.2 (p < 0.001) (Table 1).
Discussion
Our investigation demonstrated that trend of exported measles cases from Japan to the United
States has corresponded with the measles activity
trend in Japan. Most of the cases were unvaccinated.
They were namely reported from states that are
considered popular destinations among Japanese
travelers. Measles exportation often occurred after
Figure 3 Index cases of exported measles from Japan to the
United States, by month and nationality, 1994 to 2006.
J Travel Med 2008; 15: 82–86
high measles activity the previous week. In contrast,
over the past 3 years, no cases of exported measles
have been detected, corresponding to overall low
measles activity throughout Japan. In spring 2007,
the measles activity trend in Japan had resurgence
and 1,121 pediatric and 387 adult (15 y old or more)
measles cases were reported.13 In the United States,
five exportation cases from Japan—among them two
were responsible for three secondary cases—have
been reported by Measles Update. These findings
help elucidate the fact that occurrence of measles
exportation reflected the concurrent level of measles activity in Japan.
Measles exportation from endemic areas is an
important emerging health problem in areas where
the disease has been eliminated. Due to increasing
numbers of international travelers, measles exportation can lead to serious public health consequences, such as outbreaks. The exportation of
measles from Japan to Anchorage in 1998 resulted
in the largest measles outbreak in the United States
within the past decade.14 Should these susceptible
young and senior individuals gather in large numbers in Japanese communities, cases of measles may
occur, with some of them sporadically exporting the
virus overseas.
To solve this international health problem,
strengthening immunization is the only counter
measure. In April 2006, the Government implemented the use of measles–rubella vaccine for childhood immunization programs. In addition, measles
immunization has been expanded from a one-dose
regimen (12–24 mo of age) to a two-dose regimen
(12–24 mo and 5–7 y). The Government expects the
number of pediatric cases of measles to decrease
as low as that observed in the United States. Even
after receiving two doses of vaccine, unimmunized
teenagers will remain susceptible over the next 10
years or longer. In recent years, measles cases have
been decreasing in the United States and Japan, resulting in reduced opportunities for virus exposure
in the community.
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Measles Exportation From Japan to United States
Therefore, Japanese public health professionals
should also plan measles catch-up campaigns, such as
successfully carried out in South Korea in 2001.15
Moreover, the Japanese Government should consider the reintroduction of the MMR vaccine for
future use in the national childhood immunization
programs, among many reasons, to prevent the subsequent exportation of mumps to the rest of the world.
Until the community immunization level sufficiently gets improved, US public health professionals
have to closely monitor international measles activity
and maintain close communications with their country counterparts. In our investigation, the majority of
export cases were young Japanese who visited the
United States for leisurely travel or language training. During 1993 to 2001, measles importation rates
per 1 million travelers were 1.3 and 2.4 from Japan
and Germany, respectively.6 Consideration should
be made to require written documentation of measles
immunization prior to issuing US student visas.
There are several limitations in our investigation.
First, sentinel measles surveillance in Japan, in spite
of strong association of measles exportation with
the measles activity in our study, has demonstrated
low sensitivity (43.7%), specificity (89.3%), and
positive predictive value (16.7%).11 Some prefectural governments have categorized measles as a notifiable disease, thereby monitoring the occurrence
of all measles cases in these prefectures. To improve
the surveillance data quality, such efforts should be
regulated by national law. Second, the US surveillance database contained 25 index cases with unknown immunization status. Because of these cases,
we could not compare the demography between
the immunized versus the nonimmunized. Third, as
the database did not have the genotyping information for the isolated measles virus, analysis was not
conducted in terms of molecular epidemiology.
The Japanese Government has recognized the
global health impact of measles exportation to the
United States and other countries. Over the past
several years, Japan has made efforts to increase
immunization coverage in collaboration with academia, local governments, and medical associations.
National vaccination coverage increased from 75%
in 199616 to 81% in 2000.17 But the Japanese Ministry of Health, Labor and Welfare has not yet played
a leading, decisive, or prominent role in promoting
measles vaccine coverage.18 This preventable health
problem should be solved by strong leadership of
Japanese public health professionals. Such efforts
should contribute to measles elimination in the
Western Pacific Region by 2012, a campaign initiated by the World Health Organization.19
Declaration of Interests
The authors state that they have no conflicts of
interest.
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Peer Reviewers, Journal of Travel Medicine 2007
On behalf of all the authors of articles published in Volume 14 of the Journal of Travel Medicine the Editorial Office wishes to
express its gratitude to the peer reviewers:
Abu Abdullah
Adachi Javier
Alexander James
Anderson Susan
Antinori Spinello
Arya Subhash
Askling Helena
Backer Howard
Barnett Elizabeth
Barreto Miranda Isabel
Bartoloni Alessandro
Basnyat Buddha
Basto Filipe
Bauer Irmgard
Beeching Nicholas
Behrens Ron
Beltrame Anna
Billinghurst Kelvin
Bisoffi Zeno
Blum Johannes
Blumberg Lucille
Boggild Andrea
Bolin Ingrid
Brown Amy C
Brusaferro Silvio
Buhl Mads
Buma Adriaan
Burchard Gerd-Dieter
Calleri Guido
Carosi Giampiero
Castelli Francesco
Cater Carl
Caumes Eric
Chatterjee Santanu
Chen Lin
Cobelens Frank
Croft Ashley
Dahl Eilif
Deschrijver Koen
Diaz James
DuPont Herbert
Eichner Martin
J Travel Med 2008; 15: 82–86
Ericsson Charles
Espié Emmanuell E
Fabris Paolo
Farina Claudio
Feldmeier Hermann
Fischer Doris
Fisher Melanie
Fooks Anthony
Forde Andrea
Franco-Paredes Carlos
Freedman David O.
Genton Blaise
Ghosn Jade
Goebels Klaus
Goldsmid John
Goodyer Larry
Gramiccia Marina
Guse Clare
Gushulak Brian
Hackett Peter
Haditsch Martin
Hale Devon
Hamer Davidson
Hammer David
Hargarten Stephen
Hatz Christoph
Henrich Timothy
Herzog Christian
Heukelbach Jorg
Hill, David
Hoffmann-Tonn Katja
Holzer Benedikt
Hornick Richard
Hotez P.J.
Imbert Patrick
Jelinek Tomas
Jensenius Mogens
Jones Michael
Kain Kevin
Kalantri S.
Karagiannis Ioannis
Goh Kee Tai
Keystone Jay
Kimura Mikio
Kitsutani Paul
Kolars Joseph
Kollaritsch Herwig
Koopmans Marion
Kozarsky Phyllis
Kuepper Thomas
Lanfranco Sam
Lautenschlager Stephan
Leder Karin
Leggat Peter
Leuthold Claudine
Loescher Thomas
Loutan Louis
Macpherson Douglas
Madhavan Tomas
Maggiorini Marco
Magill Alan
Malerczyk Claudius
Malone John
Matteelli Alberto
McKenzie Robin
Memish Ziad
Menzies Dick
Merla Arcangelo
Meslin François-Xavier
Meyer Juerg
Mulhall Brian
Murray Clinton
Musch Eugen
Nawa Yukifumi
Nikolic Nebojsa
Nothdurft Hans-Dieter
Nygard K.
Okhuysen Pablo
Olsson Lisa
Pandey Prativa
Parola Philippe
Pitchforth Emma
Potasman Israel
Poudel Krishna
Ramirez DeArellano A
Reed Christie
Rendi-Wagner Pamela
Rey Michel
Richter Joachim
Riddell Michaela
Rieder Hans
Rogenmoser Philipp
Ross Mary
Rudolph Robert
Schlagenhauf Patricia
Schöffl Volker
Schwartz Eli
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Shanks George
Shaw Marc
Shlim David
Simon Fabrice
Smith, Kitty
Speare Richard
Stickel Felix
Struchiner Claudio
Thibeault Claude
Thybo Sören
Toovey Stephen
Torresi Joseph
Torrico Faustino
Van Gompel Alfons
Van Herck Koen
Verhoef Linda
Visser Leo
Walker Thomas
Walser Sabine
Watters Michael
Weinke Thomas
Wichmann Ole
Wilde Henry
Wilder-Smith Annelies
Wiwanitkit Viroj
Zafren Kenneth
Zimmer Rudy