Crossing Borders: One World, Global Health

Imported Cases Could Impact Elimination of Measles in Countries That Have Achieved Elimination

Eboni M. Taylor, Heather Burke, and Weigong Zhou.

Measles is a highly contagious, acute viral condition that can cause serious illness and sometimes death. Despite the availability of a safe and effective vaccine, measles remains endemic in many countries. Measles was declared eliminated in the United States in 2000, but imported cases continue to occur among US travelers and foreign visitors entering the United States from areas of the world where measles is endemic [1]. During 2011, 222 measles cases and 17 measles outbreaks were reported to the Centers for Disease Control and Prevention (CDC). Of the 222 cases, 200 (90%) were associated with importations from other countries, including 52 (26%) cases in US residents returning from abroad and 20 (10%) cases in foreign visitors. Most patients (86%) were unvaccinated or had unknown vaccination status [2].

Historically and globally, the translocation of measles between countries has been associated with foreign travel. In September 1991, 3 suspected measles cases were reported among athletes from New Zealand participating in an international gymnastics competition in Indianapolis. More than 60 000 persons were potentially exposed, including athletes and coaches, trainers, and managers from 51 countries; volunteers and staff; international media, families, and employees; and spectators attending the competition [3]. At an international youth sporting event with approximately 265 000 participants and spectators, held in Pennsylvania in 2007, a participant who traveled from Japan to the United States became ill with measles and potentially exposed other participants on 8 US teams and 8 international teams from Canada, Chinese Taipei, Curaçao, Japan, the Netherlands, Mexico, Saudi Arabia, and Venezuela [4]. Six additional measles cases were linked to the index case, with 2 generations of secondary transmission. In January 2011, 3 index cases of measles were associated with 8 secondary cases in Australia and Zealand, related to air travel from Singapore to Brisbane, Australia, where they were in transit to Auckland, New Zealand [5].

Outbreaks of measles are common among refugee and displaced populations [6], and these refugees are becoming increasingly urban [7, 8]. A 16-year-old unvaccinated refugee from Burma who had lived in an urban area of Kuala Lumpur, Malaysia, became ill with fever and rash in Malaysia on 18 August. His 15-year-old sibling, also unvaccinated, developed fever on 21 August and rash on 22 August. Both siblings, along with their mother and a 13-year-old sibling, departed Malaysia on 24 August and arrived at Los Angeles International Airport the same day. The 15-year-old refugee (the index patient) was hospitalized on 25 August. On 26 August, the CDC was notified of the suspected measles case [9]. Serologic testing for immunoglobulin M confirmed the diagnosis of measles on 30 August [9]. Serologic testing in Los Angeles indicated evidence of recent measles infection in the 16-year-old sibling; however, the sibling was not infectious during the flight.

On 30 August, the CDC, in collaboration with local and state public health officials and the refugee resettlement community, initiated contact investigations to identify secondary measles cases. Thirty-one refugees who traveled from Malaysia on the same flight as the index patient arrived in 7 states (Maryland, North Carolina, New Hampshire, Oklahoma, Texas, Washington, and Wisconsin). From 26 August to 12 September, 6 secondary measles cases were identified [10]. All secondary cases were in unvaccinated persons: 3 in refugee children, 2 in nonrefugee children who were on the same flight as the index patient, and 1 in a US Customs and Border Protection officer.

On 7 September, the CDC was notified of another laboratory-confirmed measles case in an unvaccinated 23-month-old refugee from Burma, who also traveled from Malaysia on August 24 but on a different flight. One secondary measles case in an unvaccinated 11-month-old nonrefugee child was linked to this case. On 22 May 2012, the CDC was notified from Connecticut of a suspected measles case in an unvaccinated 3-year-old refugee from Cameroon, who had rash onset on 12 May. He, his mother, and unvaccinated older siblings had arrived in Connecticut on 10 May. Persons at a church, including in the church nursery, were exposed. The child was hospitalized for encephalitis and pneumonitis, and the case was laboratory confirmed on 22 May. No secondary cases occurred.

High levels of population immunity to measles from high vaccine coverage and rapid control efforts by state and local public health agencies, combined with guidance provided by CDC, including technical assistance and laboratory testing, were key factors in limiting this outbreak to 6 secondary measles cases and preventing the spread of measles in communities with unvaccinated persons. Refugee travel to the United States from Malaysia, where a measles outbreak was ongoing, was temporarily suspended, which resulted in the cancellation of 31 flights and affected 1028 refugees. Additional measures included vaccinating US-bound refugees in Malaysia with measles, mumps, and rubella (MMR) vaccine; postponing their travel for 21 days after vaccination; encouraging timely postarrival health examinations; creating awareness among the medical and resettlement communities; and promptly reporting cases to local health departments.

Editorial comment. In many countries refugees do not have legal status, as is the case in Malaysia; they thus have limited or no access to health services. Typically urban refugees do not receive vaccinations as part of their routine overseas health assessment. Consequently, the health and vaccination status of urban refugees remains largely unknown. At the time of the outbreak in Malaysia, departing urban refugees did not receive vaccinations as part of their health assessment. Imported measles cases require a time- and resource-intensive public health response. A small number of countries annually take part in United Nations High Commissioner for Refugees resettlement programs [11]. The United States accepts most refugees, while Australia, Canada, and the Nordic countries also provide a number of places. Recently more countries in Europe and Latin America have been involved in resettlement. These countries could potentially be at risk for import-related cases. Providing refugees with protection through vaccination will substantially decrease the risk of measles among the refugees, as well as importation into the United States and potentially other countries, and thus minimize future disruption to scheduled departures. Therefore, if feasible, before departure all US-bound refugees aged 12 months to 54 years should receive 1 or 2 doses of MMR vaccine (with at least 4 weeks separating the doses) [12] during the overseas health assessment. (C. B.)