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In-flight transmission of measles: Time to update the guidelines?

Published:March 31, 2016DOI:https://doi.org/10.1016/j.ajic.2016.02.010
      To the Editor:
      We describe 2 patients traveling in separate parties on the same flight whose presentations with measles to an Australian hospital's emergency department (ED) resulted in 2 large-scale look backs requiring considerable time and financial resources, prompting us to review the literature and guidelines around in-flight transmission of measles.
      The index case was returning from holiday in India with a 2-day history of diarrhea, fever, and rash preceding air travel. He had migrated to Australia as a teenager and had received 1 childhood measles vaccination. He transited via Changi Airport, Singapore, before arriving in Melbourne. He initially attended a general practice medical clinic and was advised to present to our hospital ED where he was in a waiting room queue for 15 minutes. A triage nurse made a provisional diagnosis of measles, and he was immediately isolated using airborne precautions and admitted for observation. Measles was confirmed with positive measles IgM and polymerase chain reaction and with a negative IgG. He made a full recovery and was discharged home.
      Six days later, the second patient presented to the ED with fever and malaise. He was a university student and had attended classes while unwell. He was seen at a general practice clinic before presenting to the hospital. He was in the waiting room briefly before review by the ED triage nurse; he elected not to stay for further assessment. Three days later, we received notification of his positive measles serology and ascertained that he had been on the same 8-hour flight as the index case from Singapore to Melbourne, 4 rows apart. Similar to the index case, he had only received a single-dose measles vaccine in childhood.
      As per the Measles National Guidelines for Public Health Units
      • Communicable Diseases Network Australia (CDNA)
      Measles national guidelines for public health units.
      by Victoria's Department of Health and Human Services, the infection prevention and control team conducted look backs for each case. In total, 325 contacts were identified as potentially exposed in the ED prior to isolation of the patients. Contact tracing was carried out on 149 health care workers, 103 patients, and 73 accompanying visitors. Under the Department of Health and Human Service protocols, 138 (42%) exposed persons received normal human immunoglobulin, whereas 37 (11%) were given prophylactic measles, mumps, and rubella live attenuated vaccinations.
      The 2 cases were on the same flight from Singapore to Melbourne; however, the secondary case was not identified by the look back initiated from the airline manifest because he was not within the contact-tracing target group. This prompted us to review the current literature around in-flight transmission of measles and review the guidelines.
      Measles is an airborne, respiratory virus that manifests in flu-like symptoms and a widespread rash. It is a highly contagious viral infection, and humans are its only reservoir. Mode of transmission is usually by respiratory secretions and airborne droplets. The incubation period is from 7 up to 18 days after exposure.
      • Jost M.
      • Luzi D.
      • Metzler S.
      • Miran B.
      • Mutsch M.
      Measles associated with international travel in the region of the Americas, Australia and Europe, 2001-2013: a systematic review.
      • Coleman K.P.
      • Markey P.G.
      Short report: measles transmission in immunized and partially immunized air travellers.
      Maximum communicability occurs from the onset of prodromal symptoms (fever, cough, and runny nose) through the first 72-96 hours of morbilliform rash. Cases are considered infectious 4 days before appearance of rash until 4 days after. Approximately 30% of reported measles cases have associated complications. Complications are most common among children <5 years of age and adults ≥20 years of age.
      • Centers for Disease Control and Prevention
      Measles.
      Complications of measles include middle ear infection (7%), bronchopneumonia (6%), diarrhea (8%), acute encephalitis (0.1%), and severe sequelae of subacute sclerosing panencephalitis or death (0.2%).
      Current Australian guidelines recommend direct follow-up of all passengers in the same row and 2 rows on either side of the index case during a flight of any duration.
      • Communicable Disease Network Australia
      Revised guidelines for the follow-up of communicable diseases reported among travellers on aeroplanes.
      This is consistent with other guidelines. The U.S. Centers for Disease Control and Prevention (unpublished protocol
      • Edelson P.J.
      Patterns of measles transmission among airplane travelers.
      • Beard F.
      • Franklin L.
      • Donohue S.
      • Moran R.
      • Lambert S.
      • Maloney M.
      • et al.
      Contact tracing of in-flight measles exposures: lessons from an outbreak investigation and case series, Australia, 2010.
      ) recommend contact tracing of passengers in the same row and 2 rows on either side of a laboratory-confirmed case, including all babies in the arms of an adult, regardless of seat location and flight crew from the same cabin as an index case. European guidelines recommend all passengers and crew be considered for contact tracing, starting with children below two years of age and passengers seated in the same row as the index case, proceeding outwards, row by row for as long as it is feasible to carry out post-exposure prophylaxis or containment measures.
      Since the guidelines were published, there have been published reports and anecdotal evidence of secondary transmissions occurring beyond the 2-plus-2 row target contract-tracing group.
      • Jost M.
      • Luzi D.
      • Metzler S.
      • Miran B.
      • Mutsch M.
      Measles associated with international travel in the region of the Americas, Australia and Europe, 2001-2013: a systematic review.
      • Coleman K.P.
      • Markey P.G.
      Short report: measles transmission in immunized and partially immunized air travellers.
      • Beard F.
      • Franklin L.
      • Donohue S.
      • Moran R.
      • Lambert S.
      • Maloney M.
      • et al.
      Contact tracing of in-flight measles exposures: lessons from an outbreak investigation and case series, Australia, 2010.
      • de Barros F.R.
      • Danovaro-Holliday M.C.
      • Toscano C.
      • Segatto T.C.
      • Vicari A.
      • Luna E.
      Measles transmission during commercial air travel in Brazil.
      • Hoad V.C.
      • O'Connor B.A.
      • Langley A.J.
      • Dowse G.K.
      Risk of measles transmission on aeroplanes: Australian experience 2007-2011.
      • Hoskins R.
      • Vohra R.
      • Vlack S.
      • Young M.
      • Humphrey K.
      • Selvey C.
      • et al.
      Multiple cases of measles after exposure during air travel- Australia and New Zealand, January 2011.
      A retrospective review of all airplane travel-related measles notifications in Australia between 2007 and 2011 by Hoad et al
      • Hoad V.C.
      • O'Connor B.A.
      • Langley A.J.
      • Dowse G.K.
      Risk of measles transmission on aeroplanes: Australian experience 2007-2011.
      highlighted more than half of secondary transmissions occur beyond the 5-row contact tracing target. Factors predictive of secondary transmission include cases with active cough, younger-aged cases who may be less able to control their respiratory symptoms, or if there were multiple infectious cases on board.
      • Jost M.
      • Luzi D.
      • Metzler S.
      • Miran B.
      • Mutsch M.
      Measles associated with international travel in the region of the Americas, Australia and Europe, 2001-2013: a systematic review.
      • Hoad V.C.
      • O'Connor B.A.
      • Langley A.J.
      • Dowse G.K.
      Risk of measles transmission on aeroplanes: Australian experience 2007-2011.
      Transmission risk did not consistently appear to be related to flight duration, with secondary cases occurring in flight times of 1.5-12 hours.
      • Edelson P.J.
      Patterns of measles transmission among airplane travelers.
      • Beard F.
      • Franklin L.
      • Donohue S.
      • Moran R.
      • Lambert S.
      • Maloney M.
      • et al.
      Contact tracing of in-flight measles exposures: lessons from an outbreak investigation and case series, Australia, 2010.
      Aircraft cabin design and inflight air circulation with use of high-efficiency particulate filters are thought to limit transmission of infectious diseases.
      • Hoad V.C.
      • O'Connor B.A.
      • Langley A.J.
      • Dowse G.K.
      Risk of measles transmission on aeroplanes: Australian experience 2007-2011.
      • Mangili A.
      • Gendreau M.A.
      Transmission of infectious diseases during commercial air travel.
      However, this does not take into account other potential confounding factors such as pre- and postflight exposure, air flow disturbances, or passenger movement.
      • Hoad V.C.
      • O'Connor B.A.
      • Langley A.J.
      • Dowse G.K.
      Risk of measles transmission on aeroplanes: Australian experience 2007-2011.
      • Mangili A.
      • Gendreau M.A.
      Transmission of infectious diseases during commercial air travel.
      The World Health Organization has announced that measles has been eliminated in Australia and United States
      • Australian Department of Health
      ; however, international travel to countries where measles is endemic is a well-known risk factor for measles. Adolescents and young adults have been identified as a susceptible cohort, with young adult travelers being a major source of imported infection.
      • Martin N.
      • Foxwell A.
      As the large, multistate sustained outbreak linked to Disneyland, California, in December 2014
      • Zipprich J.
      • Winter K.
      • Hacker J.
      • Xia D.
      • Watt J.
      • Harriman K.
      • et al.
      Measles outbreak—California.
      • Centers for Disease Control and Prevention
      U.S. multi-state measles outbreak, December 2014–January 2015.
      demonstrates, measles outbreaks continue to occur sporadically secondary to imported cases with local transmission among susceptible groups, resulting in associated morbidity, mortality, and health care costs.
      Guidelines on follow-up of communicable diseases in airline passengers should be reviewed to take into consideration likelihood of transmission, severity of the disease, and logistics and time required performing look backs. Extending contact tracing of passengers beyond 2-plus-2 rows, including targeting those who are between 6 and 12 months old who have minimal immunity, may significantly reduce the risk and consequences of secondary transmission. Other possible strategies to consider include one-off targeted mass vaccination campaigns for those in the susceptible age group and increasing stringency of requirements for up-to-date vaccination records for entry overseas for further education or overseas travel. Health practitioners also need to have raised awareness in considering measles in returning travelers and overseas visitors presenting with fever and rash.

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      Linked Article

      • Response to Lim et al regarding “In-flight transmission of measles: Time to update the guidelines?”
        American Journal of Infection ControlVol. 45Issue 1
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          In their recent letter, Lim et al1 describe the events that led to 2 large-scale public health investigations involving 325 individuals, after presentation of 2 measles cases at an emergency department in Victoria, Australia. The index case had traveled while infectious with measles from India to Australia, transiting via Singapore. The second case had been on the same flight as the index case from Singapore to Australia, but was not identified during contact tracing, because they were not seated in the same row or within two rows of the index case.
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