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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 84 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. 85 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. References 1. Gomi H, Takahashi H. Why is measles still endemic in Japan? Lancet 2004; 364:328–329. 2. Tsuji T, Suzuki M. Current status of measles in Japan, with US aspects [in Japanese]. J Jpn Med Assoc 2003; 129:530–534. 3. National Institute of Infectious Diseases. Measles, Japan, 2001-2003. Infect Agent Surveillance Report 2004; 25:60–61. Available at: http://idsc.nih.go.jp/ iasr/25/289/tpc289.html. (Accessed 2007 Jun 30) 4. National Institute of Infectious Diseases. Measles and rubella in Japan, as of March 2006. Infect Agent Surveillance Report 2006; 27:85–86. Available at: http://idsc.nih.go.jp/iasr/27/314/tpc314.html . (Accessed 2007 Jun 30) 5. Andreae MC, Freed GL, Katz SL. Safety concerns regarding combination vaccines: the experience in Japan. Vaccine 2004; 22:3911–3916. 6. Vukshich N, Harpaz R, Redd SB, Papania MJ. International importation of measles virus—United States, 1993-2001. J Infect Dis 2004; 189(Suppl 1):S48–S53. 7. Chibo D, Riddell M, Catton M, et al. Studies of measles viruses circulating in Australia between 1999 and 2001 reveals a new genotype. Virus Res 2003; 91:213–221. 8. Oliveira MI, Curti SP, Figueiredo CA, et al. Molecular analysis of a measles virus isolate from Brazil: a case originating in Japan. Acta Virologica 2004; 48:9–14. 9. Centers for Disease Control and Prevention. Measles—United States, 2000. MMWR Morb Mortal Wkly Rep 2002; 51:120–123. 10. Centers for Disease Control and Prevention. Measles update. Available at: http://www.cdc.gov/ncidod/ dvrd/revb/measles/news.htm#measles_update_usa. (Accessed 2007 Jun 30) 11. Murakami Y, Hashimoto S, Taniguchi K, et al. Evaluation of a method for issuing warnings pre-epidemics and epidemics in Japan by infectious disease surveillance. J Epidemiol 2004; 14:33–40. 12. National Institute of Infectious Diseases. Infectious disease weekly report. Available at: http://idsc.nih. go.jp/idwr/index.html. (Accessed 2007 Jun 30) 13. ProMED-mail.Measles—Japan(4):Update,ProMEDmail 2007 June 9: 20070609.1887. Available at: http:// www.promedmail.org/. (Accessed 2007 Aug 1) 14. Centers for Disease Control and Prevention. Transmission of measles among a highly vaccinated school population—Anchorage, Alaska, 1998. MMWR Morb Mortal Wkly Rep 1999; 47(51 and 52):1109. 15. Centers for Disease Control and Prevention. Elimination of measles—South Korea, 2001-2006. MMWR Morb Mortal Wkly Rep 2007; 56:304–307. 16. National Institute of Infectious Diseases. The present status of measles in Japan as of 1998. Infect Agent J Travel Med 2008; 15: 82–86 86 Takahashi and Saito Surveillance Report. 1999. Infectious Disease Surveillance Center, NIID, Toyama 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan. Available at: http://idsc.nih.go.jp/iasr/20/228/tpc228.html . (Accessed 2007 Jun 30) 17. National Institute of Infectious Diseases. Measles, Japan, 1999-2001. Infect Agent Surveillance Report 2001; 22:273–274. Available at: http://idsc. nih.go.jp/iasr/22/261/tpc261.html. (Accessed 2007 Jun 30) 18. Nakayama T, Zhou J, Fujino M. Current status of measles in Japan. J Infect Chemother 2003; 9:1–7. 19. World Health Organization, Western Pacific Regional Office. Field guidelines for measles elimination. Manila, Philippines: World Health Organization, 2004. 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. 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