Transmission of infectious diseases during commercial air travel

Transmission of infectious diseases during commercial
air travel
Alexandra Mangili, Mark A Gendreau Lancet 2005; 365: 989–96
See Comment page 917
Because of the increasing ease and affordability of air travel and mobility of people, airborne, food-borne, vector- Division of Geographic
borne, and zoonotic infectious diseases transmitted during commercial air travel are an important public health Medicine and Infectious
Diseases, Tufts-New England
issue. Heightened fear of bioterrorism agents has caused health officials to re-examine the potential of these agents Medical Center, Boston, MA,
to be spread by air travel. The severe acute respiratory syndrome outbreak of 2002 showed how air travel can have an USA (A Mangili MD); and
important role in the rapid spread of newly emerging infections and could potentially even start pandemics. In
Department of Emergency
addition to the flight crew, public health officials and health care professionals have an important role in the
Medicine, Lahey Clinic Medical
Center, Burlington, MA 01805,
management of infectious diseases transmitted on airlines and should be familiar with guidelines provided by local USA(MAGendreau MD)
and international authorities.
Introduction
cabin can be manipulated by the flight deck.1 When mark.a.gendreau@lahey.org
Over 1 billion passengers travel by air annually; parked at the terminal, fresh air is supplied to the 50 million of these travel to the developing world.1,2 aircraft by auxiliary power units. During flight, fresh air Although infrequently reported and very difficult to is supplied into the cabin from the engines where the air assess accurately, there is a risk of disease transmission is heated, compressed, cooled, and passed into the cabin during commercial air travel and this risk has become to be circulated by the ventilation system.3 The outside the focus of heightened attention. The growing mobility air is assumed to be sterile at typical cruising altitudes.
of people and popularity of airline transportation has Air circulation patterns aboard standard commercial amplified the potential for disease to be transmitted to aircraft are side-to-side (laminar) with air entering the passengers not only during but also before and after cabin from overhead, circulating across the aircraft, and flights. Here, we review knowledge about transmission exiting the cabin near the floor (figure 1). Little front-to- of infectious diseases associated with commercial air back (longitudinal) airflow takes place.3–9 This air travel, with particular emphasis on transmission within circulation pattern divides the air flow into sections within the cabin, thereby limiting the spread of airborneparticles throughout the passenger cabin.
The aircraft cabin environment
Most commercial aircraft in service recirculate 50% of During flight, the aircraft cabin is a ventilated, enclosed the air delivered to the passenger cabin for improved environment that exposes passengers to hypobaric control of cabin circulation, humidity, and fuel hypoxia, dry humidity, and close proximity to fellow efficiency.5–9 This recirculated air usually passes through passengers. This space is regulated by an environmental high efficiency particulate air filters (HEPA) before system that controls pressurisation, temperature,ventilation, and air filtration on the aircraft. Althoughthis system is wholly automated, the number of air-conditioning packs in operation, zone temperatures, andthe mixture of fresh and re-circulated air delivered to the Search strategy and selection criteria
We searched MEDLINE database for articles using: “aircraft”,“cabin air quality“, “infectious diseases“, “tuberculosis“,“severe acute respiratory syndrome“, “measles“, “influenza“,“common cold“, “food-borne“, “water-borne“, and “vector-borne“. We reviewed technical and governmental reportsfrom the UK House of Lords, UK Department of Transport, UKCivil Air Authority, US National Research Council, US Federal Aviation Administration, WHO, US Department of Transportation, and US House of Representatives. Wesearched the internet using the Google search engine withthe same terms. Finally, we contacted medicalrepresentatives from the Civil Air Authority, the FederalAviation Administration, and several international air carriers.
Figure 1: Air circulation pattern in typical airline passenger cabin
From WHO4 with permission of the publisher. Arrows show air currents.
www.thelancet.com Vol 365 March 12, 2005
delivery into the cabin. Normal airline cabin air exchange Comments
rates range from 15 to 20 air changes per hour compared of reports
with 12 air changes per hour for a typical office Airborne/fomites
building.3–9 Ventilation capacity varies substantially, Positive TB skin test only. No active TB.
dependent on the aircraft type but typically averages 10 (4·7 L/s) cubic feet per minute.3,6–10 Ventilation rates can also vary within the different cabin sections, such as first and economy class.7,9 In general, HEPA filters used on commercial airlines have a particle-removing efficiency of 99·97% at 0·3 microns.4,6,7,9,11 These filters Food-borne
remove dust, vapours, bacteria, and fungi. HEPA filters also effectively capture viral particles because viruses usually spread by droplet nuclei.7,11 No ventilation operational standards for commercial aircraft are available. Although a survey showed that most air carriers equip their large aircraft with HEPA filters, Vector-borne
neither the Civil Aviation Authority nor the Federal Aviation Administration require their use.9,12,13 Likely to be airport, not aircraft, transmission Cabin air quality has been the focus of many media investigations and criticism from special interest groups.14–16 Most of this concern is associated with the Bioterrorism agents
perception that airborne particles are distributed throughout the entire cabin by the ventilation system.
Table: Reported infections transmitted on commercial airlines
However, no peer-reviewed scientific work links cabinair quality and aircraft ventilation rates to heightenedhealth risks compared with other modes of transport or happens by aerolisation of an infectious agent through with office buildings,4,7,9,12,13,17–22 so this work is limited.7,9,12 droplet nuclei (residua of large droplets containing These shortcomings motivated the UK government to microorganisms that have evaporated to Ͻ5 microns).
form the Aviation Health Working Group in 2000 to These residual droplets become aerosolised and disperse further investigate health aspects of air travel, including widely, dependent on environmental conditions, and cabin air quality and safety. In a detailed study into cabin remain suspended in air for indefinite periods.5,27,28 air quality released in 2004, the group concluded that Common vehicle transmission involves one inanimate temperature, humidity, air speed, and concentrations of vehicle, which transmits infection to many hosts, and carbon monoxide, carbon dioxide, and microbiological typically applies to microorganisms spread by food and flora aboard 14 commercial flights using British water. Vector-borne transmission results from the Aerospace 146 and Boeing 300 aircraft were similar to spread of disease by insects and vermin. The table shows other reported studies.23 The European Cabin Air study the infectious diseases that have been transmitted on coordinated by the Building Research and Consultancy commercial airlines. All types of disease transmission continues to investigate environmental aspects within the passenger cabin. These efforts will probably lead to Large droplet and airborne mechanisms probably improved international regulations for the certification, represent the greatest risk for passengers within the inspection, and maintenance of aircraft environmental aircraft because of the high density and close proximity of passengers. In addition to proximity, successfulspread of contagion to other hosts is dependent on many Modes of disease transmission
factors, including infectiousness of the source; Four routes for the spread of microorganisms exist: pathogenicity of the microorganism; duration of contact, airborne, common vehicle, and vector-borne.25,26 Contact transmission involves direct contact in which humidity, temperature); and host-specific factors such as body-to-body contact takes place, or indirect in which the general health and immune status.4,7,9,22 How these susceptible person comes into contact with a factors affect risk of disease transmission within the contaminated intermediate host (fomite). Large droplet transmission is judged a form of contact transmission inwhich large droplets (Ͼ5 microns) contaminated with Risk of transmission
microorganisms are generated when an infected person The risk of disease transmission within the confined sneezes, coughs, or talks. These droplets are propelled space of the aircraft cabin is difficult to determine.
short distances (Ͻ1 m) and deposited on a susceptible Insufficient data prohibits meta-analysis, which would host’s conjunctiva or mucosa. Airborne transmission allow an idea of the probability of disease transmission www.thelancet.com Vol 365 March 12, 2005
Figure 2: Schematic diagram of SARS outbreak aboard Hong Kong to Beijing flight
From reference 31with permission of the publisher.
for each respective contagion. Many of the available Airborne and large droplet-transmitted diseases
epidemiological studies are compromised by reporting Tuberculosis
bias caused by incomplete passenger manifests, thereby Tuberculosis is a serious global threat, and estimates complicating risk assessment. Despite these limitations, suggest that about a third of the world’s population has data suggest that risk of disease transmission to other the disease.4,38 The transmission of Mycobacterium symptom-free passengers within the aircraft cabin is tuberculosis is the most studied model of the spread of associated with sitting within two rows of a contagious airborne pathogens aboard aircraft. Several studies passenger for a flight time of more than 8 h.3,4,7,9,12,29–31 This about in-flight transmission of tuberculosis have been association is mainly derived from investigations of in- reported, with most being done in the mid-1990s.4,29,30,39–41 flight transmission of tuberculosis, but is believed to be Two of the seven investigations revealed a probable link relevant to other airborne infectious diseases.3,4,7,9,32–34 Some of onboard transmission. In the first occurrence, a flight variation in this association has been reported, with one attendant was the index case, and two documented outbreak of severe acute respiratory syndrome (SARS) in tuberculin skin test conversions occurred during which passengers seated as far as seven rows from the 5 months in 1992 in 212 fellow crew members and 59 frequent flyer passengers.39 The second, and largest, Risk of disease transmission within the aircraft cabin incident was of a passenger with pulmonary also seems to be affected by cabin ventilation.4,5,7,9,12,29,30,35–37 tuberculosis travelling from Baltimore to Chicago and In general, proper ventilation within any confined space then on to Honolulu.29 Four of 15 fellow passengers reduces the concentration of airborne organisms in a seated within two rows of the index passenger had logarithmic fashion, and one air exchange removes 63% positive tuberculin skin test conversion. Although there of airborne organisms suspended in that particular is a risk of tuberculosis within the aircraft cabin, no space.27,28 The main laminar flow pattern within the cases of active disease have been reported as a result of aircraft cabin (figure 1) with the practice of frequent cabin air travel. Transmission within the aircraft cabin seems air exchanges and use of HEPA filtration for recirculated to be more likely with close proximity to a contagious air clearly limits transmission of contagion.4,7,9,12,36 passenger (within two rows) over a long time (greater Transmission becomes widespread within all sections of than 8 h) and not as a result of the practice of the passenger cabin when the ventilation system is recirculating 50% of the cabin air.4,9,12,29 An overall nonoperational, as shown by an influenza outbreak when probability of infection in the order of one in 1000 when passengers were kept aboard a grounded aircraft with an a symptomatic source is present has been suggested,35 and this probability of risk is similar to, if not less than, Risk assessment incorporating epidemiological data into mathematical models may show how proximity andventilation commercial airlines. Deterministic modelling with data SARS is a non-typical pneumonia caused by a from an in-flight tuberculosis investigation revealed that coronavirus.32,43–45 The global spread by air travellers and doubling ventilation rate within the cabin reduced in-flight spread of SARS has been documented.31,32,46–48 infection risk by half.35 Risk also reduced exponentially to The disease is believed to usually be spread by large almost zero in passengers seated 15 seats from the aerosolised droplets or by direct and indirect contact, but infectious source.35 Clearly ventilation provides a crucial airborne or small droplet transmission better explains determinant of risk, and efforts to increase ventilation will the distribution of SARS cases that has occurred on www.thelancet.com Vol 365 March 12, 2005
transmission of SARS during the Amoy Gardens The fact that influenza outbreaks worldwide have been outbreak in Hong Kong was a result of airborne spread via affected by influenza strains imported by air travel is well a viral plume.49 A total of 40 flights have been investigated established;52–54 however, only three studies of in-flight for carrying SARS-infected passengers.31,32,46–48 Five of transmission of influenza have been reported.33,37,55 The these flights have been associated with probable on-board first was in an outbreak of influenza A/Texas strain transmission of SARS in 37 passengers.31,32,46 Most of those aboard a commercial carrier in 197937 that resulted in 72% passengers were seated within five rows of the index of all passengers aboard the airline contracting influenza case.31,32 One 3-hour flight carrying 120 passengers within 72 h. The secondary attack rate in their families travelling from Hong Kong to Beijing on March 15, was estimated to be 20% within 2 weeks. The high 2003,31 began a superspreading event accounting for 22 of transmission rate in this particular case was believed the 37 people who contracted SARS after air travel.31,32,48 attributable to passengers being kept aboard the aircraft for 3 h with an inoperative ventilation system while repair occurred in 16 people, two passengers had a diagnosis of work was being done. The second study described an probable SARS, and four were reported to have SARS but outbreak of influenza A/Taiwan/1/86 at a naval air station could not be interviewed.31 The number of secondary cases in 1989 in military personnel who were returning from from that flight remains under investigation, but more temporary duty.55 Transmission of influenza occurred than 300 people might have been affected.32,50 Figure 2 both on the ground and aboard two DC-9 aircraft that shows the distribution pattern of the SARS outbreak transported the squadron from Puerto Rico to a Florida naval station. The third outbreak happened in 1999 in This pattern could be important because it did not mine workers travelling on a 75-seat aircraft.33 15 follow the typical example of in-flight transmission of passengers travelling with the index case developed airborne pathogens—ie, risk of disease transmission is symptoms within 4 days. Nine of the 15 were seated associated with a flight time of more than 8 h and sitting within two rows, and all were seated within five rows, of within two rows of the index passenger.4,7,9,12,29 The the index case. No further influenza outbreaks aboard duration of the Hong Kong to Beijing flight was 3 h and commercial aircraft have been reported since 1999.
affected passengers were seated seven rows in front andfive rows behind the index passenger.31 Possible Other airborne diseases
explanations for this outbreak distribution include: Meningococcal disease occurs after direct contact with airborne transmission rather than direct contact spread; a respiratory secretions and is associated with high malfunctioning cabin filtration system; and passengers morbidity and mortality rates.42 A case of meningococcal infected before or after the flight.31 No on-board disease associated with air travel is defined as the transmissions have occurred since late March, 2003, development of the illness within 14 days of travel on a when the WHO issued specific guidelines for in-flight flight lasting at least 8 h, including ground delay, take off, containment of SARS.47,51 As the first severe contagious and landing.34 The US Centers for Disease Control disease of the 21st century, SARS exemplifies the ever- received 21 reports of suspected air travel-associated present threat of new infectious diseases and the real meningococcal disease from 1999 to 2001.34 In all cases potential for rapid spread made possible by the volume the index person was contagious while aboard a and speed of air travel. Finally, the distribution pattern of commercial flight, but no secondary cases of the disease SARS transmission aboard the flight emphasises the need were reported. People seated next to an ill passenger to study airborne transmission patterns aboard should be quickly contacted and given chemoprophylaxis within 24 h of identifying the index case.
Chemoprophylaxis given more than 14 days after onset of Common cold
illness in the index case is probably of little or no value.56 Common cold outbreaks as a result of air travel have not Measles is an airborne and highly contagious viral been reported, which could be attributable to the infection with an attack rate of about 80%.57 Transmission difficulties of investigating such outbreaks in view of the can occur during the prodromal illness and passengers ubiquitous nature of the common cold. One study might be unaware of their diagnosis at the time of travel.
compared the risk of developing an upper respiratory tract Measles is no longer endemic in the USA and infection during air travel in passengers flying on aircraft importations from developing countries account for most that recirculated 50% cabin air versus aircraft using 100% outbreaks. Imported measles and associated cases fresh air in the passenger cabin.36 Recirculation of aircraft accounted for at least 17% of all reported cases within the cabin air was not a risk factor for contracting upper USA during 1982.58 From 1996 to 2000 30% of all imported measles cases were estimated to be in peoplewho flew while symptomatic with the disease.59,60 Influenza
Three case studies have described measles The aircraft as a vector for global spread of influenza transmission during commercial air travel.58,60–62 A case strains is a greater concern than is in-flight transmission.
report in 1982 identified seven secondary cases of www.thelancet.com Vol 365 March 12, 2005
measles epidemiologically linked to the index case as a attributable to greater use of prepackaged frozen meals, result of in-transit exposure; one was a passenger flying improved food handling, and inspection, but might on the same aircraft as the index case and five others represent under-reporting by passengers or reporting were people who had visited at least one common departure gate with the index case.58 In the same year,another study reported an index passenger who infected Vector-borne and zoonotic diseases
two fellow passengers on a flight from Venezuela to Vector-borne diseases are very frequent causes of Miami.61 A third report recorded eight cases of in-flight morbidity and mortality in many parts of the world, and transmitted measles during a 10-h flight from New York the potential of their importation via commercial aircraft to Tel Aviv in 1994.62 The source case was not identified remains a risk. Many cases of malaria occurring in and but was speculated to be a crew member. In 2004, a around airports all over the world in people who had not passenger with measles travelled from Japan to Hawaii, travelled to endemic areas, known as airport malaria, is but this did not result in any transmission to other air evidence that malaria-carrying mosquitoes can be travellers.59 International adoptions have a significant imported on aircraft.69,70 A total of 87 cases of airport role in the number of imported measles cases. In April, malaria have been reported, 75 of which happened in 2004, an outbreak in children adopted from an Europe.70 Dengue and yellow fever are both transmitted orphanage in China resulted in temporary suspension of by mosquitoes of the genus Aedes. The Aedes mosquito adoptions from that particular orphanage.60 Nine of the has been introduced into countries where it had not ten confirmed cases were thought to be infectious while previously been present and many of these mosquitoes travelling. One secondary case was a female student in were likely to have spread by aircraft.69 A case of dengue close contact with an infected child.
fever was reported in Germany in a couple returningfrom a trip to Hawaii.71 Airport transmission of dengue Common vehicle diseases
fever was suspected in this particular case. The The most commonly reported diseases transmitted on disinsection of aircraft—spraying aircraft before landing aircraft have been spread by the fecal-oral route via to kill insects—and vector control around airports, as contaminated food. A total of 41 in-flight food-borne well as immunisation requirements, seem to have been outbreaks resulting in 11 deaths were documented effective in preventing outbreaks in non-endemic areas.
between 1947 and 1999.63–68 Salmonella is the most Although International Health Regulations recommend usually reported food-borne pathogen spread via a disinsecting aircraft travelling from countries with commercial airline, with fifteen documented outbreaks malaria and other vector-borne diseases, only five between 1947 and 1999 infecting nearly 4000 passengers countries do so.69,72,73 Common and exotic animals are and resulting in seven deaths.63,64 Eight food-borne regularly transported on aircraft and may carry disease.
outbreaks caused by Staphylococcus and one associated Many zoonotic pathogens cause emerging and re- death were reported between 1947 and 1999.63,65 One of emerging diseases.74,75 Up to now, no zoonotic outbreaks the largest cases involved 57% of the passengers served a associated with air travel have been reported; however, ham omelette on an international flight in 1975.65 continued monitoring of air transport of animals, Surprisingly, only one viral-induced enteritis outbreak especially from developing countries, is needed.
has been described.66 In this incident, contaminatedorange juice was the vehicle of transmission and a Bioterrorism agents
Norwalk-like agent was isolated from fecal samples of The potential for spread of bioterrorism agents via air travel exists. A well written, comprehensive review of There have been a few reported cases of ill passengers bioterrorism agents and the implications of air transport as a result of food or water contaminated with Vibrio is available,5 and a new interest in previously eradicated cholerae consumed during international air travel.63,67,68 smallpox has emerged. In-flight spread of this disease The first documented in-flight outbreak was in 1972 on a has been documented, and so the potential for in-flight flight from London to Sydney via Singapore.67 Of the spread of smallpox is of public health concern.76,77 In 47 people who developed cholera, which was attributed 1963 an epidemic was reported in Sweden, in which the to a cold appetiser served during the flight, one died. The index case was attributed to in-transit exposure, either at largest outbreak of airline-associated cholera occurred in the air terminal or on the aeroplane, and caused 1992, during a cholera epidemic in Latin America.68 During a flight from Buenos Aires via Lima to Los Viruses causing viral haemorrhagic fever, such as Angeles, 75 passengers developed cholera, resulting in ebola and lassa, have also been the focus of media ten passengers being admitted and one death. A cold attention and have been investigated for potential seafood dish, prepared in one of the cholera-affected transmission while aboard an aircraft.5 Although aerosol countries, was implicated as the source of transmission.
spread of ebola has not been documented in man, this No food-borne or water-borne outbreaks have been mode of transmission occurs in non-human primates.
reported over the past 5 years, which is probably Lassa, known to be transmitted via large droplets, is www.thelancet.com Vol 365 March 12, 2005
thought to have an incubation period of up to 3 weeks, of passengers.4,29 Although air carriers are under no making infectious passengers potentially symptom-free obligation to archive passenger manifests, most have and unaware of their status at the time of travel.76–81 internal policies to do so for up to 3 months.24 A study of passengers exposed to an index case of lassafever in-flight noted no evidence of transmission, even Conclusions
in the 19 passengers seated within two rows of the index Commercial airlines are a suitable environment for the passenger.81 Because both lassa and ebola viruses have spread of pathogens carried by passengers or crew. The frequent fatal outcomes and no vaccine is available, environmental control system used in commercial appropriate infection control procedures should be aircraft seems to restrict the spread of airborne followed to prevent the transmission of these pathogens, and the perceived risk is greater than the diseases.79,80 Lassa fever is treatable with ribavirin if the actual risk.12 Transmission of infectious diseases probably drug is given within the first 6 days of illness, making happens more frequently than reported for various reasons, including reporting bias and the fact that mostdiseases have a longer incubation period than air travel.
Management of infectious disease exposures
Important questions include: what factors affect the aboard commercial aircraft
transmission of infectious diseases within the aircraft Early recognition and appropriate infection control cabin? How effective are the ventilation systems used measures are needed when passengers become exposed within commercial aircraft with regard to emerging to an infectious or potentially infectious passenger.
infections? Further assessment of risk through Government and international laws provide legal mathematical modelling is needed and will provide authority to control the movement of passengers with insight into disease transmission within the aircraft communicable diseases.82,83 This authority ranges from cabin as well as control of outbreaks of different diseases. issuing travel alerts to quarantine of passengers arriving The International Health Regulations adopted at airports. Although air carriers have the right to refuse worldwide in 1969 to limit the international spread of to take passengers who are ill with a communicable disease are being revised to provide a means for disease or medically unfit for air travel, systematic immediate notification of all disease outbreaks of screening of passengers for contagious diseases and excluding passengers with infectious symptoms is characterised by clinical syndrome rather than specific impractical.84 Health care professionals are expected to diagnosis to expedite reporting.88 These new regulations identify individuals who are unfit for air travel, or advise and continued vigilance by countries, health authorities, the flying public of how to safely travel by air. Prevention airlines, and passengers will keep to a minimum but not of a disease outbreak is the most important means of eliminate the risk of disease spread by aircraft. The control, and travellers should therefore be advised to aviation industry and medical community should postpone any air travel when they are ill.
educate the general public on health issues related to air Good hand hygiene has been proven to reduce the risk of disease transmission, and air travellers should make it Conflict of interest statement
part of their normal travel routine.85 Although masks We declare that we have no conflict of interest.
play a crucial part in infection control in health care Acknowledgments
settings, their use is unproven in disease control within We thank our colleagues for their helpful suggestions.
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