key: cord-0882680-r5x2oyrl authors: Khatib, Aisha N; Carvalho, Anna-Maria; Primavesi, Robert; To, Kent; Poirier, Vincent title: Navigating the Risks of Flying During COVID-19: A Review for Safe Air Travel date: 2020-11-12 journal: J Travel Med DOI: 10.1093/jtm/taaa212 sha: 3482df199967cbad13c5e0022273420aaa500a7c doc_id: 882680 cord_uid: r5x2oyrl Rationale for Review: With air travel restarting, there has been much discourse about the safety of flying during the pandemic. In Travel Medicine, risk assessment includes estimating baseline risk to the traveller, recognizing factors that may modify that risk, considering the role of interventions to decrease that risk, and accounting for a traveller’s perception and tolerance of risk. The goals of this review are: to identify the in-flight transmission risks of commercial air travel, to provide recommendations about the risks of flying during the pandemic, and to propose strategies to mitigate the spread of COVID-19. Key Findings: The airline industry has taken a layered approach to increase passenger safety through effective onboard ventilation, extended ventilation at the gate, boarding and deplaning strategies, improved aircraft disinfection, and pre-flight screening such as temperature checks and COVID-19 testing. Proximity to an index case may contribute to the risk of transmission more than the seat type or location. The use of face masks has significantly reduced onboard transmission and mandatory inflight mask wearing policies are being enforced. Innovations such as digital health passports may help standardize screening entry requirements at airports and borders, allowing for a safer return to travel. Recommendations: In-flight transmission of SARS-CoV-2 is a real risk, which may be minimized by combining mitigation strategies and infection prevention measures including: mandatory masking onboard, minimizing unmasked time while eating, turning on gasper airflow inflight, frequent hand sanitizing, disinfecting high touch surfaces, promoting distancing while boarding and deplaning, limiting onboard passenger movement, implementing effective pre-flight screening measures and enhancing contact tracing capability. Assessing risk is a cornerstone of travel medicine. It is important to evaluate the multiple factors contributing to the cumulative risk of an individual traveller during the COVID-19 pandemic and to employ a multi-pronged approach to reduce that risk. recognizing factors that may modify risk, considering the role of interventions to decrease risk, and accounting for a traveller's perception and tolerance of risk. 11, 12 With air travel restarting, how safe is it to fly during the pandemic? The goals of this review are: (1) to identify the transmission risks of in-flight commercial air travel, (2) to provide recommendations for physicians fielding questions about the risks of flying safely during the COVID- 19 pandemic, and (3) to propose strategies that mitigate the transmission of COVID-19. Air quality aboard modern aircraft is very safe. The cabin air is exchanged every 3 to 4 minutes and about 50% of recirculated air is mixed with outside fresh air, which is free of microorganisms at cruising altitude. 13, 14 First, recirculated air goes through a prefilter which traps the largest particles, then passes through high-efficiency particulate air (HEPA) filters before reentering the passenger cabin. HEPA filters have proven to be highly effective in maintaining the circulating air with very low concentrations of bacteria, fungi and viruses. They are 99.97% effective in removing particles between 0.1 μm and 0.3 μm in diameter and 100% of larger particles. 15, 16 The SARS-CoV-2 virus particle diameter ranges from 0.06 μm to 0.14 μm, however the droplets and aerosols the virus travels in are larger than 5-10 μm in size, and would be captured by the HEPA filters. [17] [18] [19] [20] The risk of being exposed to an airborne pathogen on a plane is lower than in many other enclosed spaces because of the filters and more frequent air exchange. 21 The aircraft cabin airflow is laminar, with vertical movement downward from top to bottom at 1m/sec. 22 2) Does turning on the personal air flow (gaspers) above the seat increase transmission risk? The air from the personal air vents (gaspers) above each passenger seat is either clean air from the air conditioning packs or recirculated filtered air, depending on the model of the aircraft. 21 Using the gasper will create an airflow driving the particles to the floor faster, which are then filtered by the HEPA filters, reducing the exposure time of airborne particles in front of the passenger and the transmission of contaminants between passengers. 30- 33 One study surmised that if a gasper is turned on, it could produce a high contaminant concentration in the region above a passenger's head, bringing in more contaminants into their breathing zone. However, this study found that the overall risk by turning on a gasper was neutral. 34 There is new emerging evidence to support the overall low transmission risk related to personal air vents. Gasper supply (on or off) does not make a significant impact on aerosol risk. 27 Therefore, it is recommended that the gasper airflow be turned on to improve travel comfort, air quality and reduce person-toperson transmission of exhaled contaminants. 24, 27, 35, 36 Further study is needed to examine the interaction of passengers with airflow and the resulting droplet and aerosol dispersion to substantiate the evidence. Infection transmission within the aircraft cabin depends on exposure time, contact points, as well as proximity and movement of passengers. The likelihood of passengers coming into contact with each other and contaminated surfaces is highest during boarding and deplaning. 16 The risk is higher with boarding than deplaning, for all seating configurations in various aircraft, thought to be due to the section-based order in boarding compared to the front-to-back order in deplaning. 37 Zone-based boarding was shown to have a higher rate of contact between passengers than random-based or back-to-front boarding. 23, 38 Contact with other passengers was shown to be further decreased with column-wise exiting during front-to-back deplaning (all aisle seats exit first, followed by middle seats, followed by window seats), though associated with higher time to deplane. 23 In larger aircraft, deplaning had higher risk of transmission. 37 Passengers should be vigilant during boarding and deplaning, with attention to wearing masks, hand hygiene, avoiding fomite contact such as touching seat backs, maintaining physical distancing as feasible, and minimizing carry-on luggage. Aisle seated passengers have more contact with others than those seated in middle or window seats. 38, 39 In a study of norovirus transmission aboard an airplane, sitting in an aisle seat was found to be associated with contracting the illness, whereas using the lavatory on that flight was not. 40 Experimental studies of aerosol dispersion suggest that due to the airflow in the cabin, Passengers seated at the front of the cabin are reported to have longer cumulative duration of contact, presumably due to lavatories often being located at the rear of the airplane. 39 This was reflected in the finding on the Sydney-Perth flight, where being seated in the forward economy cabin conferred a greater risk of secondary SARS-CoV-2 infection. 42 The number of contacts for those in first class are thought to be much lower than for economy class, given that first class seats are closer to the exit and there is larger distance between seats. 37 Evaluation of inflight transmission of SARS-CoV-2 on a flight from London to Hanoi, however, demonstrated one business class passenger secondarily infected 12 other business class passengers, which challenges the thinking of business or first class being safer. 43 Proximity to an index case rather than the seat type may contribute more to risk of transmission. 39 An international flight into Ireland with 13 positive cases onboard were linked by genomic sequencing to a common unknown source. 10 Transmission presumably occurred during the flight since cases were divided into four groups, originating from three different continents, who had minimal contact with each other pre-boarding. Masks were reportedly worn by 9 of the 13 passengers throughout the flight. Flight occupancy was sparse (17%) with positive cases clustered throughout the forward and aft economy cabins, in window, middle and aisle seats. This case illustrates that masking may be more important than seat location, with strict onboard infection prevention measures and limitation of passenger movement also essential to reduce the risk of inflight transmission. Where choice is available, a business class window seat is conventionally thought to be the safest option-though recent studies are questioning this-with a non-aisle seat towards the back of the plane a relatively safe economy class option. Once seated, passengers should avoid moving about the aircraft cabin to minimize exposure to others, which may be more feasible on a shorthaul flight. 39 There has been much discussion about leaving the middle seat empty to promote physical distancing on an aircraft. The highest exposure risk for contagion are economy class passengers seated in a 2-metre diameter surrounding an infected passenger, 5 seats in all directions, up to and including 3 rows in front and 3 rows behind. 39, 44 A recent study examining potential transmission of SARS-CoV-2 during a long flight found a clear association to proximity of an index case to risk of infection when seated less than two seats away. 43 Physical distance between passengers can be increased, although not to the 2m suggested distance, if the middle seat is left empty. Further distancing can be achieved by leaving every other row unoccupied. However, doing so would have a negative economic impact on airline operations as well as a negative environmental impact. 45 IATA has recommended against leaving the middle seat empty. 46 Other measures to decrease droplet spread such as mask-wearing with limited eating (unmasked) time, and decreased passenger and crew movement throughout the aircraft cabin must be employed to offset the risk posed by being unable to physically distance if the middle seat is not left empty. Transmission of disease by contact with contaminated surfaces is less than by inhalation. 47 Horizontal surfaces such as laptops and tray tables are more likely to collect respiratory droplets. 47 High touchpoint surfaces inside the aircraft that are potentially contaminated includes tray tables, armrests, seat covers, door knobs and toilet flush buttons. 48 In August 2020, the CDC confirmed a report of a woman who contracted SARS-CoV-2 during an evacuation flight from Milan to South Korea. An epidemiologic investigation concluded that transmission was most likely from an asymptomatic but infected passenger while using the toilet onboard. 52 ICAO recommends restricting lavatory access while in-flight. Where sufficient lavatories exist, one lavatory should be designated for crew only and passengers should use a designated lavatory based on seat assignment. 53 Lavatories are ventilated with cabin air from an individual air outlet. The ventilation air is exhausted directly overboard. 54 There is sufficient ventilation in aircraft lavatories to minimize virus transmission between users, even if they demask. Mainstream media recently reported on the possibility of COVID-19 being transmitted during the flush of a toilet since there is evidence of SARS-CoV-2 virus in faecal matter. 55 A study using CFD calculated that a toilet flush can generate upward velocity capable of expelling aerosol particles out of the toilet bowl to cause large-area-spread. However, the height of these particles reach 106.5 cm from the ground, insufficiently high to be inhaled for most people. 56 Although potential risk of contagion is indirect from droplet deposition on and around the toilet, rather than by inhalation, it is advisable to remain masked in the lavatory. Further safe procedures to adopt when using a toilet include lowering the toilet lid before flushing, cleaning the toilet seat before using, washing hands carefully after flushing, and sanitizing hands after touching the door handle. Given asymptomatic people can transmit the SARS-Cov-2 virus, the WHO encourages the use of fabric face coverings in public places. As of April 2020, Transport Canada made it mandatory for all air passengers over 2 years of age to wear a face-covering. 57 Wearing a mask while flying is also recommended by IATA, ICAO and the CDC. 46 boarding process, throughout the flight except when eating, and while exiting the aircraft until they are inside the air terminal building. 60 The type of mask worn is also an important consideration. A new study regarding the effectiveness of different masks and mask alternatives to suppress the spread of respiratory droplets during regular speech shows that some masks, particularly neck gaiters, disperse the largest droplets into a multitude of smaller droplets which may be aerosolized. The valved N95 mask performance was also reduced due to the exhalation valve, which opens for outwards airflow and might contaminate nearby persons. In comparison, the performance of the fitted non-valved N95 mask or surgical mask was far superior. 61 Although masks are not 100% effective, wearing them does decrease viral spread. 62,63 Therefore, standard surgical masks or a two-layer fabric (cotton or cotton/propylene) pleated-style mask should be worn. Bandanas, gaiters or masks with exhalation valves should not be permitted onboard. 64 Should passengers forget to bring their own mask, a small "health kit" will be offered to passengers at check-in or onboard by several airlines as part of passenger protection and reassurance. As the cost of surgical masks is nominal and the supply chain has improved, airlines should provide them to passengers free of charge. Between January and March 2020, there have been three in-flight transmissions reported by IATA, and several other reports of probable in-flight transmission, although these lack genomic evidence. [6] [7] [8] [9] Of note, all the suspected cases of in-flight transmission occurred prior to mandatory masking on flights. 9, 43 The limited number of cases of in-flight transmission reported after mandatory masking support the major role that masking may have in disease transmission mitigation. 65 Mask wearing is a key measure to decrease the spread of COVID-19 on airplanes and should be enforced as mandatory. Further studies on inflight COVID-19 transmission before and after masking requirements is needed. Contracting COVID-19 from food or food packaging is unlikely. 66 The main concern stems from eating in proximity to others within an enclosed space. A study published by the CDC suggested that adults diagnosed with COVID-19 were twice as likely to have dined at a restaurant in the previous two weeks, likely due to the increased risk of being in close contact, defined by being within 2m of an infected person for a cumulative total of 15 minutes or more. According to IATA, removal of face-coverings for short periods to eat and drink "is permitted, necessary and Airlines and aviation authorities have been proactive in protecting their cabin crew and passengers. Cabin crew are required to wear masks onboard with or without face shields or goggles. Due to fomite transmission risk, crew members also wear gloves and gowns, depending on the airline. Aviation authorities have required passengers to wear face coverings as an effective means of reducing droplet spread. 62, 63, 68, 69 Failure to do so may result in a denial of boarding or removal from a flight. CDC, IATA and Transport Canada do not recommend wearing gloves inflight except for cleaning or taking care of someone who is sick. 46, 70, 71 People who wear gloves are less likely to wash their hands between tasks and are more likely to contaminate themselves. Thermal screening has been implemented in many airports around the world as one of the many accuracies and effectiveness. One study suggests that infrared thermal image scanners for mass screening of travellers at airport has a specificity of 71% and sensitivity of 86% to detect fever, but there are variations depending on where the camera is positioned, which part of the body is being scanned, and other environmental and individual factors that can affect the precision of these thermal scanners. 74, 75 Overall, temperature screening at airports may offer some reassurance to travellers, and could act as some form of barrier to prevent individuals with fever from entering the airport or from boarding a flight. It certainly cannot detect every traveller infected with COVID-19, and by itself is not an effective tool to prevent entry and spread of COVID-19 into another country. According to the World Health Organization, several dogs, ferrets, and cats in contact with infected humans have tested positive for COVID-19. There is currently no evidence that these animals play a role in transmission of the disease to humans. 76,77 However, since animals can carry the disease, some carriers suspended all international and domestic pet travel. Other airlines are not allowing animals on flights with connections. Animals may also be required to undergo a 14-day quarantine prior to departure or show a document signed by an accredited veterinarian stating that the pet has not been in contact with any humans or animals infected with COVID-19. It is advisable to check with the airline before travelling with an animal. In September 2020, IATA called for the development and deployment of systematic COVID-19 testing for all passengers before departure as an alternative to quarantine measures to re-establish countries to establish "travel bubbles", "travel corridors" or "corona corridors", permitting quarantine-free travel between countries. 78 Limitations to pre-testing include high rates of false negative tests, potential exposure between date of test and date of travel, and potential exposure during pre-boarding, inflight, or post flight journey. Travellers need to source specific entry requirements through national and international health agencies and ministries, airline websites or travel specialists, as regulations continue to change. 14) What is a digital health passport or an immunity passport? Several new innovative ideas are underway to standardize documentation and presentation of COVID-19 status. One such idea is using a digital health passport for international travel. CommonPass, a project initiated by the World Economic Forum, is a digital health passport currently under trial with Cathay Pacific Airways and United Airlines. CommonPass functions as an adaptable secure platform allowing travellers to document their COVID-19 status electronically, which can then be presented at boarding or borders. 79, 80 The pass could be used to verify test results or vaccination status, while protecting the privacy of health information. It aims to support a range of country to country health screening entry requirements, be interoperable between and across countries, and be operated openly, independently and on a notfor-profit-basis. Depending on the success of these trials, the pass will expand to other airlines and routes globally, with the sustainable goal to safely increase travel and trade. The concept of an 'Immunity Passport' or 'Immunity Certificate' is based on the idea that a passenger could be documented as having recovered from COVID-19 infection and thus be immune. 81, 82 Immunity status would essentially exempt a traveller from airport and onboard processes such as temperature checks, and they would not require protective measures such as face masks, distancing, quarantine or testing. However, medical evidence of immunity from COVID-19 is still inconclusive, with many unknowns such as duration of protective immunity. 83 As such, WHO, IATA, and ICAO currently do not support immunity passports, but they may be a possibility in the future, when a vaccine is introduced or when there is more evidence supporting immunity. 84 Currently, contact tracing is not being done by airlines for positive cases inflight. Some public health authorities are indirectly providing contact tracing. For example, the Government of Canada hosts a webpage that lists the locations or flights where people may have been exposed to COVID-19. 85 The data includes the airline, flight number, route, date and flight row numbers affected if known. This data is gathered from public health authorities but is not exhaustive. Although updated daily, contact information that is more than 14 days old is deleted. Moreover, flight manifests are not kept indefinitely, do not contain contact information on all travellers and are not immediately available to public health authorities. Airlines should work closer with public health authorities to make contract tracing more robust and timelier. Three well-documented in-flight mass transmission events showed evidence of case-clustering, and the overall limited data suggests proximity to a SARS-COV-2 infected person as a major risk factor for in-flight transmission. 9 Canada uses a Bluetooth application called COVIDAlert that anonymously notifies close contacts of positive casesdefined as anyone who has been within 2 meters for longer than 15 minutes. Accordingly, the airline industry could implement a similar universal Bluetooth application that can be downloaded pre-flight, would be functionable inflight and for two weeks post travel. Ideally this would be combined with a digital health pass. This is an area for innovation as contact tracing is a key component to contain transmission. Travellers have played a critical role in spreading the disruptive SARS-CoV-2 virus worldwide, resulting in a paralyzing pandemic, with the number of scheduled flights worldwide down by 47.5% as of August 2020. 86 Flying during the pandemic presents increased risks, whether directly or indirectly related to COVID-19 infection. The risk of infectious disease transmission aboard commercial flights is a real and significant concern. 16 should be consistent across the airline industry and used in addition to the preventive measures enforced onboard. The implementation of a standardized digital health pass for COVID-19 and more robust contact tracing may be key factors to allow for a gradual safe return to sustainable and responsible travel. 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