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SUPPLEMENT ARTICLE Low Risk of Measles Transmission after Exposure on an International Airline Flight Pauli N. Amornkul,1,a Hiroshi Takahashi,3 April K. Bogard,4,a Michele Nakata,4 Rafael Harpaz,2 and Paul V. Effler4 1 Department of Preventive Medicine, Epidemiology Program Office, and 2Division of Epidemiology and Surveillance, National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia; 3Infectious Disease Surveillance Center, National Institute of Infectious Diseases, Tokyo, Japan; 4Epidemiology Branch, Hawaii State Department of Health, Honolulu, Hawaii In May 2000, a passenger with measles traveled aboard a 7-hour flight from Japan to Hawaii. A follow-up survey was sent to 307 (91%) of the 336 exposed passengers to identify susceptible passengers and subsequent occurrences of measles. The median age of the 276 respondents (90%) was 34 years; 268 (97%) were residents of Japan. Self-reports determined that 173 (63%) were immune through prior measles or vaccination; 6 (2%) denied a history of prior measles or immunization, and 97 (35%) were unaware of their status. Only 1 nonimmune respondent received immunoprophylaxis. None of the respondents developed a febrile rash illness 7–21 days after exposure. The risk of in-flight measles transmission among passenger populations with similar susceptibility profiles appears to be low. An aggressive response by health departments may not be warranted after airborne exposure to measles. Each health department should make such determinations on the basis of specific circumstances and availability of resources. In recent years, 1650 million international passenger arrivals occurred worldwide, making air travel the most common means of transport [1]. The epidemiology of measles in the United States is substantially influenced by the high volume of air travel from geographic regions where measles is more prevalent. During 2000, a total of 21 persons developed measles shortly after arriving in the United States. Of these, 7 (33%) had been infected in Japan, including 4 measles case patients entering Hawaii (Redd S, National Immunization Program, Centers for Disease Control and Prevention, personal communication). Because measles is communicable during the prodromal illness, some portion of internationally derived cases could lead to exposure en route. Determining the risk of measles from in-flight exposures is important. Few data currently exist on which to base appropriate public health responses to Financial support: Epidemiology Branch, Hawaii Department of Health. a Present affiliations: Centers for Disease Control and Prevention Field Station, Kisumu, Kenya (P.N.A.); Acute Disease Investigation and Control, Minnesota Department of Health, Minneapolis (A.K.B.). Reprints or correspondence: Dr. Paul V. Effler, State Epidemiologist, Hawaii State Department of Health, 1250 Punchbowl St., Rm. 454, Honolulu, HI 96813 ([email protected]). The Journal of Infectious Diseases 2004; 189(Suppl 1):S81–5 2004 by the Infectious Diseases Society of America. All rights reserved. 0022-1899/2004/18909S1-0013$15.00 such events. We report the findings of an investigation determining the extent of transmission after a documented in-flight exposure to measles aboard an international flight from Japan to Hawaii in May 2000. METHODS On 21 May 2000, the crew aboard a flight from Osaka, Japan, notified the US Public Health Service Quarantine Station in Honolulu that they were arriving with a passenger who had a febrile rash illness. After the plane was docked, a Quarantine Inspection Officer and a nurse boarded the aircraft and made a clinical diagnosis of measles for the patient. Before the passengers deplaned, the US Public Health Service Quarantine staff verbally informed passengers in English of their potential exposure to measles. This information was then repeated verbally in Japanese. A “Health Alert Notice” card written only in English was distributed to the passengers on deplaning. The notice explained the potential exposure to measles and advised any passengers who became ill within 2 weeks to seek medical attention and bring the card with them. The ill passenger, a Japanese boy aged 17 years with no prior measles vaccination history, was transported to a local hospital, where measles was serologically confirmed by detection of rubeola Low Risk of Measles Transmission on Airplanes • JID 2004:189 (Suppl 1) • S81 IgM antibody with a titer of 11:160. The patient had experienced headache, cough, sore throat, conjunctivitis, and fever (38.3C) the day before departure. He developed a rash shortly before the flight, and his fever and cough persisted aboard the aircraft. The patient’s sister had had a febrile rash illness 2 weeks earlier. The Hawaii Department of Health obtained the flight’s passenger manifest and customs declaration forms. A flyer informing passengers of their potential exposure to measles, its communicability, its clinical manifestations, and the increased risk to special populations (infants, pregnant women, and the immunocompromised) was prepared; it was translated into Japanese because the majority of passengers were from Japan. The flyer emphasized the potential benefit of timely immunoprophylaxis for passengers not already immune to measles and identified facilities at which health care services could be obtained. A brief survey in Japanese requesting contact information and the names of other persons traveling in the same party was attached to the information sheet. Both documents were delivered to passengers in their hotels within 48 h of their arrival and were collected during the following days. With information from this survey, passengers were recontacted on their return to Japan. A follow-up survey was distributed to assess the possibility of measles transmission during the journey to Honolulu. Passengers were asked whether they had experienced any febrile rash illness within the 7- to 21-day period after the flight. To gauge the degree of susceptibility in the exposed population, vaccination and illness histories were collected. A prior history of measles was determined by respondent recall. Respondents were asked to review their vaccination cards for documentation of prior vaccination with a measles-containing vaccine (MCV). Passengers who were returning to their residences in Hawaii or the US mainland were sent follow-up surveys in English. The flight crew was not contacted as part of this study; its health care and follow-up was provided through the airline. The aircraft involved was a Boeing 747-200 with 2 decks. Seating assignment information was unavailable; passengers reported being permitted to move around the aircraft. “Close contact” was defined as having face-to-face conversation contact with the case patient. Information on close contact was assessed through passenger recall. While in Hawaii, adult passengers consented to participate in this study. Parents completed questionnaires for their children. Passengers were defined as immune to measles if they reported having either a history of prior measles or vaccination with ⭓1 dose of MCV. Passengers who denied both a history of measles and vaccination were classified as susceptible to measles. All others were considered to have unknown measles immunity status. Analyses were conducted with EpiInfo 2000 S82 • JID 2004:189 (Suppl 1) • Amornkul et al. and EpiInfo 6.04b (Centers for Disease Control and Prevention [CDC], Atlanta; 2000 and 1994, respectively) and Microsoft Access 1997 SR-1 (Microsoft; 1989–1996). Ninety-five percent confidence intervals (CIs) for percentages were calculated by means of the Fleiss Quadratic equation. RESULTS There were 337 passengers on the flight: 326 (97%) were residents of Japan, 8 (2%) of the United States, and 3 (1%) of Indonesia. Follow-up questionnaires were sent to 307 (91%) of the 337 passengers. Questionnaires were not sent to the index case patient and his father. No contact information was available for 25 Japanese passengers and the 3 residents of Indonesia. Completed questionnaires were received from 276 (90%) of the 307 sent, representing 82% of all exposed passengers. Of the 276 questionnaires returned, residents of Japan completed 268 (97%), and US residents completed 8 (3%). The median passenger age was 34 years (range, 2–88 years). Only 7 (2%) of the responding passengers were aged !10 years (table 1). The majority of the passengers were female; 4 (2%) reported that they were pregnant. Susceptibility to measles. Of the 276 respondents, 173 (63%) reported either a history of measles or vaccination with MCV (table 2). Six passengers (2%) denied both a history of measles and ever having received MCV. The remaining 97 reTable 1. Demographics of and health care received by passengers aboard a flight from Osaka to Honolulu, 21 May 2000, by country of residence (n p 276). Characteristic Japan United States Total passengers 268 (100) 8 (100) Male 111 (41.4) 1 (12.5) Female 157 (58.6) 7 (87.5) Pregnant 4 (2.5) 0 10 to !5 5 (1.9) 0 ⭓5 to !10 1 (0.4) 1 (12.5) ⭓10 to !20 0 0 Age, years ⭓20 to !30 89 (33.2) 1 (12.5) ⭓30 to !40 52 (19.4) 0 ⭓40 to !60 74 (27.6) 3 (37.5) ⭓60 years 44 (16.4) 3 (37.5) Unknown/missing 3 (1.1) 0 Recalled being informed of measles exposure while still on airplane 68 (25.4) 7 (87.5) Consulted health care provider while in Hawaii 17 (6.3) 1 (12.5) Chose to receive immunoprophylaxis for measles while in Hawaii 4 (1.5) 1 (12.5) NOTE. Data are no. (%) of passengers from each country. Table 2. Reported history of measles or measles-containing vaccine for passengers aboard a flight from Osaka, Japan, to Honolulu, 21 May 2000, by country of residence (n p 276). Characteristic Japan United States Total Total passengers 268 (100) 8 (100) 276 (100) Reported immunity to measles 168 (63) 5 (63) 173 (63) 5 (2) 1 (13) 6 (2) 95 (35) 2 (25) 97 (35) Reported susceptibility to measles Immune status unknown Reason for measles immunity (among those reporting immunity) Prior measles 129 (77) 3 (60) 132 (76) Prior measles-containing vaccine 63 (38) 3 (60) 66 (38) Prior measles and vaccine 24 (14) 1 (20) 25 (14) NOTE. Data are no. (%) of passengers from each country. spondents (35%) could not provide a definitive history of either having had measles or receiving MCV. Twenty-nine passengers (11%) reported having close contact with the ill passenger before, during, or after the flight. Of these, 23 (79%) reported a history consistent with measles immunity; the remainder had undetermined histories. None of the US or Japanese passengers contacted developed a febrile rash illness within the incubation period after the flight. The overall risk of transmission was thus 0 of 257 (95% confidence interval [CI], 0–1.8%). The risk of transmission among susceptible passengers or those with unknown immunity status was 0 of 103 (95% CI, 0.1%–4.5%). No cases of measles within the incubation period were reported to the airline by flight crew members. Impact of outreach activities. Only 75 passengers (27%) recalled being informed of their potential exposure to measles while detained on the aircraft after landing in Honolulu. Eighteen respondents (7%) saw a health care provider in Hawaii; 5 (2%) received measles immunoprophylaxis. Of the 97 passengers whose measles immunity status was unknown, 2 saw a health care provider in Hawaii, and 1, a 34-year-old woman, reported receiving immunoprophylaxis. Of the 6 susceptible passengers, none saw a health care provider while in Hawaii. Of the 4 pregnant respondents, 1 had unknown immunity to measles and did not seek health care consultation in Hawaii. DISCUSSION In this case of prolonged in-flight exposure to a person with acute, confirmed infection, no evidence of measles transmission to passengers was found. Findings regarding the risk of transmission of other respiratory pathogens during air travel have suggested variable degrees of risk [2–9]. Although measles is an airborne, highly infectious disease, several factors might have contributed to the lack of transmission aboard the aircraft. First, the majority of passengers on this flight reported being immune to measles, through either natural infection or vaccination. Although about one-third of the passengers indicated that they did not know whether they had had measles or had been vaccinated with MCV, only 2% of the passengers provided medical histories indicating that they were likely to be susceptible. Because we were unable to determine serological immunity as part of this study, some misclassification of the passengers’ immunity status might have occurred through errors in recall, misdiagnosis, and/or vaccine failure. Recent serological data from Japan indicate that 95% of the overall population is immune to measles by age 5 years. Among older cohorts, the proportion of immunity surpasses 90%. Among persons not receiving MCV, ∼85% develop measles antibodies by age 10 years [10]. However, among unvaccinated persons aged 20–29 years, the prevalence of measles immunity transiently decreases to 70%–85%. In the United States, a recent cross-sectional study of ∼20,000 persons aged ⭓6 years revealed the prevalence of measles immunity to be 93% overall and 99% in those persons born before the vaccine era (before 1956) [11]. Because most of this flight’s passengers were adults, it is likely that many of the passengers with unknown measles immunity status were actually immune. Second, although the ill passenger was febrile and coughing while aboard the aircraft, his contact with other passengers appears to have been limited. Because most passengers on this flight were part of group package tours, it is not surprising that 11% of passengers reported close contact with the index case patient before, during, or after the flight. Previously documented factors facilitating transmission of other communicable diseases such as tuberculosis include the flight’s duration and ground time [2] (i.e., exposure time to the source patient) and the seating proximity to the index case patient [3, 4]. In this instance, the index case patient was sufficiently ill that he remained in his seat for most of the flight. According to anecdotal reports, passengers mixed little during the flight. The actual Low Risk of Measles Transmission on Airplanes • JID 2004:189 (Suppl 1) • S83 Boeing 747-200 aircraft for this flight was equipped with HEPA filters to filter outside air coming into the aircraft. Reports of exposure to measles during international air travel are not uncommon on flights to the United States. During 1996–2000, a total of 63(30%) of 207 imported measles cases have been in persons who entered with rash onset either directly before the flight, on the day of the flight, or within 4 days after the flight (Redd S, National Immunization Program, Centers for Disease Control and Prevention, personal communication). All 63 case patients were, therefore, infectious while aboard the aircraft. Of these, the only documented case of in-flight measles transmission was reported by Seattle–King County, Washington. The index case patient was not seated in the same section as the passenger who developed measles, although they may have had brief contact while embarking or disembarking the plane (Duchin J, Chief Epidemiologist, Seattle–King County Health Department, personal communication). These episodes raise difficult questions for public health authorities in determining whether all passengers should be contacted immediately and alerted to seek medical attention and postexposure immunoprophylaxis. Differences in the passenger profiles regarding demographics, country from which the passenger is departing, passenger’s country of origin and residence, and, most important, measles immunity status are factors that would influence the probability of measles transmission aboard an aircraft. The exceptional return rate of 90% from an internationally mailed questionnaire is the result of intense effort and collaboration between the Hawaii Department of Health and the Infectious Disease Surveillance Center of the National Institute of Infectious Diseases in Tokyo. In this investigation, only 18 (7%) of 276 passengers sought immediate medical consultation for their potential exposure; none of those who later indicated measles susceptibility sought medical consultation for immunoprophylaxis while in Hawaii. A potential explanation for this may be the cultural perception of measles being a relatively benign illness, similar to varicella, for which urgent medical attention is neither critical nor necessary. However, if this experience is generalizable to other populations of international travelers, notifying passengers of their potential exposure might have limited impact on preventing additional measles cases among the passengers. Given limited resources, health departments must prioritize how they respond to disease exposures. Without evidence suggesting that in-flight exposures are likely to result in secondary infections, several factors should be weighed in deciding whether to contact passengers. First, available information about the likelihood that passengers are susceptible should be considered. The passenger age distribution should be examined in assessing susceptibility, particularly age-specific seroprevalence of measles antibodies, beS84 • JID 2004:189 (Suppl 1) • Amornkul et al. cause age is closely related to level of immunity. In this investigation, domestic data from Japan and the United Sates indicated high levels of immunity among adults, who constituted nearly all of the passengers on this flight. The risk of secondary infections on flights with similar passenger characteristics is therefore assessed to be generally low. Second, logistical considerations, such as the ability to locate passengers within the “window of opportunity” for preventing infection, may be useful. In our setting, most passengers were staying in Hawaii for at least several days, and many of these passengers were traveling in well-scheduled tour groups. These features helped us to locate the passengers in a timely manner. Had these persons been individual travelers in transit to multiple sites throughout the mainland United States, efforts to locate them within a period of days might have been futile. Third, a system for prioritizing contact of passengers, focusing on those at high risk of exposure, infection, or severe disease after an in-flight measles exposure, could also be useful. If the flight originates overseas, customs records will identify young children who might not have yet received 2 doses of MCV. Airline records will indicate whether parents are traveling with an infant or child who has not been assigned a separate seat. More work is needed to determine the role of seating proximity to and duration of contact with the index case patient for in-flight measles transmission. Such information would be useful in setting priorities for passenger notification. Limitations of this investigation should be noted. Measles immunity was based on self-reported illness and/or receipt of MCV and was not confirmed serologically. Documentation of prior measles or prior vaccination with MCV was not abstracted from medical records. Some misclassification of immunity or susceptibility to measles was therefore likely. Also, the study focused solely on flight passengers. The 17 crew members, based in Thailand, Japan, and the United States, were excluded. However, follow-up with the airline revealed that crew members are required to be vaccinated against measles. No crew members were reported to have developed measles within the appropriate incubation period after exposure to the index case. Furthermore, susceptibility patterns vary from population to population. Susceptibility depends on the epidemiology of measles virus infection in the geographic areas where the passengers reside, the age distribution among the passengers, and the success of local immunization efforts. Therefore, one must exercise caution in generalizing the risk of measles transmission aboard this flight to those with different passenger populations, age demographics, and countries of residence. In summary, this investigation found no evidence of measles transmission aboard an international flight in which 1 passenger had serious illness and confirmed infection and was traveling when probably infectious. Most of the passengers reported a history of prior measles virus infection and/or vaccination. Despite written materials that urged them to do otherwise, very few passengers who did not recall having prior infection or vaccination sought medical consultation. Further research is needed to better characterize risk of measles transmission among air travelers. In the interim, our experience indicates that an aggressive response by health departments may not be indicated after airborne exposure to measles. However, health departments should make such determinations on the basis of local considerations and the specific circumstances of the flight’s passengers. Acknowledgments We thank the following for their assistance with this investigation: M. Ching-Lee, J. Sasaki, T. Smalley, J. Chang, A. Ieong, L. Inouye, B. Pang, T. Tom, J. Fukunaga, M. Taira, and A. Ho’omanawanui from the Hawaii State Department of Health; A. Andale, L. Pacheco, R. Tapia from the Honolulu Station, Division of Quarantine, CDC; Japan Airlines; the Japanese Infectious Disease Surveillance Center; the hotels involved in this investigation; the State Health Departments of California and Minnesota; J. Duchin of the Seattle–King County Health Department; M. Papania and Susan Redd from the National Immunization Program, CDC; and L. Fehrs from the Epidemiology Program Office, CDC. References 1. Handszuh H. Tourism patterns and trends. In: Steffen R, Dupont H, Decker BC, eds. Textbook of travel medicine. 2nd ed. London: Hamilton, 2001:34. 2. Driver CR, Valway SE, Morgan WM, Onorato IM, Castro KG. Transmission of M. tuberculosis associated with air travel. JAMA 1994; 272: 1031–5. 3. Centers for Disease Control and Prevention. Exposure of passengers and flight crew to Mycobacterium tuberculosis on commercial aircraft, 1992–1995. MMWR Morb Mortal Wkly Rep 1995; 44:137–40. 4. Miller MA, Valway S, Onorato IM. Tuberculosis risk after exposure on airplanes. Tuber Lung Dis 1996; 77:414–9. 5. Kenyon TA, Valway SE, Ihle WW, Onorato IM, Castro KG. Transmission of multidrug-resistant Mycobacterium tuberculosis during a long airplane flight. N Engl J Med 1996; 334:933–8. 6. Moore M, Fleming KS, Sands L. A passenger with pulmonary/laryngeal tuberculosis: no evidence of transmission on two short flights. Aviat Space Environ Med 1996; 67:1097–100. 7. Klontz KC, Hynes NA, Gunn RA, Wilder MH, Harmon MW, Kendal AP. An outbreak of influenza A/Taiwan/1/86 (H1N1) infections at a naval base and its association with airplane travel. Am J Epidemiol 1989; 129:341–8. 8. Moser MR, Bender TR, Margolis HS, Noble GR, Kendal AP, Ritter DG. An outbreak of influenza aboard a commercial airliner. Am J Epidemiol 1979; 110:1–6. 9. Exposure to patients with meningococcal disease on aircrafts—United States, 1999–2001. MMWR Morb Mortal Wkly Rep 2001; 50:485–9. 10. National epidemiological surveillance of vaccine-preventable diseases, Japan, 1997. Available at: http://idsc.nih.go.jp/yosoku99/Annual-E/ yosoku97-E/index-97E.html. Accessed 22 March 2001. 11. Hutchins SS, Redd SC, Schrag S, et al. National serologic survey of measles immunity among persons 6 years of age or older, 1988–1994. MedGenMed 2001; 3:E5. Low Risk of Measles Transmission on Airplanes • JID 2004:189 (Suppl 1) • S85