Download Low Risk of Measles Transmission after Exposure on an

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.
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