Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 During Long Flight

Nguyen Cong Khanh1, Pham Quang Thai1, Ha-Linh Quach, Ngoc-Anh Hoang Thi, Phung Cong Dinh, Tran Nhu Duong, Le Thi Quynh Mai, Ngu Duy Nghia, Tran Anh Tu, La Ngoc Quang, Tran Dai Quang, Trong-Tai NguyenComments to Author , Florian Vogt2, and Dang Duc Anh2
Author affiliations: National Institute of Hygiene and Epidemiology, Hanoi, Vietnam (N.C. Khanh, P.Q. Thai, H.-L. Quach, N.-A.H. Thi, T.N. Duong, L.T.Q. Mai, N.D. Nghia, T.A. Tu, D.D. Anh); Hanoi Medical University, Hanoi (P.Q. Thai, T.-T. Nguyen); Australian National University, Canberra, Australian Capital Territory, Australia (H.-L. Quach, N.-A. H. Thi, F. Vogt); Ministry of Science and Technology, Hanoi (P.C. Dinh); Ha Noi University of Public Health, Hanoi (L.N. Quang); Ministry of Health, Hanoi (T.D. Quang)

Disclaimer: Early release articles are not considered as final versions. Any changes will be reflected in the online version in the month the article is officially released. Volume 26, Number 11—November 2020

Source: CDC

CDC: Travel during the COVID-19 Pandemic

Reprinted for educational purposes and social benefit, not for profit. 

Abstract

To assess the role of in-flight transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), we investigated a cluster of cases among passengers on a 10-hour commercial flight. Affected persons were passengers, crew, and their close contacts. We traced 217 passengers and crew to their final destinations and interviewed, tested, and quarantined them. Among the 16 persons in whom SARS-CoV-2 infection was detected, 12 (75%) were passengers seated in business class along with the only symptomatic person (attack rate 62%). Seating proximity was strongly associated with increased infection risk (risk ratio 7.3, 95% CI 1.2–46.2). We found no strong evidence supporting alternative transmission scenarios. In-flight transmission that probably originated from 1 symptomatic passenger caused a large cluster of cases during a long flight. Guidelines for preventing SARS-CoV-2 infection among air passengers should consider individual passengers’ risk for infection, the number of passengers traveling, and flight duration.

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During the first 6 months of 2020, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spread to almost all countries and infected »4 million persons worldwide (1). Air travel is contributing to the extent and speed of the pandemic spread through the movement of infected persons (24); consequently, in March, many countries either completely halted or substantially reduced air travel.

Spread of SARS-CoV-2 across international borders by infected travelers has been well documented (5,6); however, evidence and in-depth assessment of the risk for transmission from infected passengers to other passengers or crew members during the course of a flight (in-flight transmission) are limited. Although the international flight industry has judged the risk for in-flight transmission to be very low (7), long flights in particular have become a matter of increasing concern as many countries have started lifting flight restrictions despite ongoing SARS-CoV-2 transmission (8).

The first case of coronavirus disease (COVID-19) in Vietnam was recorded on January 23, 2020; the patient was a visitor from Wuhan, China (9). On January 24, Vietnam suspended air travel from mainland China, Hong Kong, and Taiwan and, as the epidemic spread worldwide, gradually expanded travel bans, mandatory quarantine, and testing measures to incoming passengers from other countries (10).

In early March, when much of the global community was just beginning to recognize the severity of the pandemic, we detected a cluster of COVID-19 cases among passengers arriving on the same flight from London, UK, to Hanoi, Vietnam, on March 2 (Vietnam Airlines flight 54 [VN54]). At that time, importation of COVID-19 had been documented in association with 3 flights to Vietnam, including a cluster of 6 persons with index cases evacuated from Wuhan; 6 secondary cases resulted from virus transmission in Vietnam (11). No in-depth investigations among passengers on those flights were conducted, and no evidence indicated that transmission had occurred during the flights themselves.

Initial investigations of flight VN54 led us to hypothesize potential in-flight transmission originating from 1 symptomatic passenger in business class (the probable index case). We subsequently launched an extensive epidemiologic investigation that involved testing and isolation/quarantine of all traceable passengers and crew members of the identified flight. Our objectives were to estimate the probability that transmission of SARS-CoV-2 occurred on the flight in question and to identify risk factors associated with transmission.

Methods

We defined cases of SARS-CoV-2 infection according to Vietnam Ministry of Health guidelines in place at the time of our investigation (12). Specifically, we defined flight-associated COVID-19 cases as passengers or crew members on board flight VN54 landing in Hanoi on March 2 who reported fever and cough, with or without shortness of breath, during March 1–16. We defined confirmed flight-associated COVID-19 cases as passengers or crew members on flight VN54, regardless whether signs or symptoms developed, who had positive SARS-CoV-2 real-time reverse transcription PCR results from nasopharyngeal swab samples (13). Flight-associated cases were considered to have very likely acquired infection on board VN54 and were hence classified as probable secondary cases in this analysis if the following 3 criteria were met: 1) they experienced signs/symptoms 2–14 days after arrival or if they were SARS-CoV-2 positive by PCR 2–14 days after arrival in the absence of signs/symptoms; 2) in-depth investigation did not reveal any potential exposure to SARS-CoV-2 before or after the flight during their incubation period; and 3) they had shared cabin space with the probable index case during the flight (1417).

At the time of flight VN54 arrival, all passengers from COVID-19–infected areas, including the United Kingdom, had their body temperature screened by thermal imaging and were required to declare any COVID-19 symptoms; only passengers arriving from China, South Korea, Iran, or Italy were required to undergo SARS-CoV-2 testing and 14-day quarantine. At that time, the use of face masks was not mandatory on airplanes or at airports (18).

As soon as the travel history of the probable index case became evident, the passenger list and flight manifest for flight VN54 was obtained from the Bureau of Immigration and the Civil Aviation Administration and sent to all provincial Centers for Disease Control with instructions for local health staff to trace all passengers and crew members of flight VN54. All successfully traced passengers and crew members were interviewed by use of a standard questionnaire, tested for SARS-CoV-2, and quarantined in designated facilities or at home. Any symptomatic person was isolated immediately until the test result was received. In-depth interviews were conducted with all persons with suspected or confirmed flight-associated cases; the specific focus was detecting any potential SARS-CoV-2 transmission events before and after the flight to investigate potential alternative scenarios for transmission other than during the flight. Furthermore, all persons with suspected or confirmed flight-associated cases were asked to identify persons with whom they had had close contact (<2 meter distance for >15 minutes) between arriving in Vietnam and the start of quarantine/isolation. These close contacts were also contacted, tested, and quarantined for 14 days. All persons in quarantine were checked twice daily for clinical signs/symptoms and fever; oropharyngeal swabs were collected on the day of admission, after 3–5 days, and on day 13, unless signs/symptoms developed, in which instance a specimen was collected immediately and the person was isolated and monitored until receipt of the test result.

Initial investigations of the probable index case generated our working hypothesis of in-flight transmission and guided further investigations. In particular, we investigated all possible exposures of all persons with flight-associated cases during their incubation period in relation to the timing of the flight, including locations where flight-associated cases may have crossed paths before and after the flight. To identify factors associated with in-flight infection risks, we calculated risk ratios and 95% CIs.

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Results

Setting

 

Figure 1. Seating location of passengers on Vietnam Airlines flight 54 from London, UK, to Hanoi, Vietnam, on March 2, 2020, for whom severe acute respiratory syndrome coronavirus 2 infection was later confirmed….

Flight VN54 departed London at 11:10 am local time on March 1, 2020, and arrived in Hanoi at 5:20 am local time on March 2; the nonstop flight lasted about 10 hours. A total of 16 crew members and 201 passengers were on board. The 274 seats on the airplane were divided into business class (28 seats), premium economy class (35 seats), and economy class (211 seats); there were 4 toilets for business and premium economy classes and 5 for economy. The business class was exclusively reserved and separated from the premium economy and economy classes by a service/toilet area (Figure 1). Of the 201 passengers, 21 occupied business (75% seats occupied), 35 premium economy (100%), and 145 economy (67%) seats (Figure 1). Two meals were served, and flight attendants worked in 2 teams, 1 for the business and premium economy sections and 1 for the economy section.

Investigation of Probable Index Case

A 27-year-old businesswoman from Vietnam, whom we identified as the probable index case (hereafter case 1), had been based in London since early February. Our case investigations supplemented by information obtained from media reports indicated that she had traveled to Italy on February 18 with her sister, who was later confirmed to be SARS-CoV-2–positive in London, and back to London on February 20 to stay with her sister for another 2 nights. On February 22, case 1 and her sister returned to Milan, Italy, and subsequently traveled to Paris, France, for the yearly Fashion Week before returning back to London on February 25. They continued to reside in London until February 29, when case 1 started to experience a sore throat and cough while attending meetings and visiting entertainment hubs with friends. On March 1, she boarded flight VN54. She was seated in business class and continued to experience the sore throat and cough throughout the flight. Her signs and symptoms (fever, sore throat, fatigue, and shortness of breath) progressed further after arrival, and she self-isolated at her private residence in Hanoi and had contact with household personnel only. On March 5, she sought care at a local hospital in Hanoi, where an oropharyngeal swab sample was taken and tested; SARS-CoV-2 infection was confirmed by real-time reverse transcription PCR on March 6. On March 7, three of her household personnel received positive SARS-CoV-2 results, as did a friend of hers in London on March 10, whom she had visited on February 29.

Case Finding and Epidemiologic Investigations

By March 10, all 16 (100%) of the flight crew and 168 (84%) of the passengers who remained in Vietnam had been traced; 33 (16%) passengers had already transited to other countries. We were able to quarantine, interview, and collect swab specimens for PCR testing from all passengers and crew members who remained in Vietnam. Passengers and crew had traveled on to 15 provinces in Vietnam, ranging from Lao Cai and Cao Bang in the north to Kien Giang in the south.

Figure 2. Epidemiologic and clinical timeline for passengers on Vietnam Airlines flight 54, from London, UK, to Hanoi, Vietnam, March 2, 2020, for whom SARS-CoV-2 infection was later confirmed. Because the flight arrived…

Through these efforts, we identified an additional 15 PCR-confirmed COVID-19 cases, 14 among passengers and 1 among crew members, resulting in a total of 16 confirmed flight-associated cases. Ages of affected persons ranged from 30 to 74 years (median 63.5 years); 9 (>50%) were male, and 12 (75%) were of British nationality (Table 1). Of the 15 persons with flight-associated cases, 12 (80%) had traveled in business class with case 1, and 2 travelers (cases 14 and 15) and 1 flight attendant (case 16) had been in economy class (Figure 1). Among persons in business class, the attack rate was 62% (13/21). Among passengers seated within 2 meters from case 1, which we approximated in business class to be <2 seats away, 11 (92%) were SARS-CoV-2–positive compared with 1 (13%) located >2 seats away (risk ratio 7.3, 95% CI 1.2–46.2) (Table 2). Of the 12 additional cases in business class, symptoms subsequently developed in 8 (67%); median symptom onset was 8.8 days (interquartile range 5.8–13.5) after arrival (Figure 2). None of the additional cases showed COVID-19 symptoms while on board VN54. All 12 additional cases in business class met the definition of probable secondary cases.

Our investigation did not reveal strong evidence supporting potential SARS-CoV-2 exposure either before or after the flight for any of the additional persons with flight-associated cases other than having traveled on the same flight as case 1 (Appendix). There were 4 traveling companion couples on board, and individuals within each couple sat next to each other in business class. None of the couples or individual cases traveled or stayed with another couple or individual case before the flight or after arrival in Vietnam. Of these case-pairs, 3 (6 persons) were positive for SARS-CoV-2 on the same date: 6 days after arrival in Vietnam.

Among >1,300 close contacts of VN54 passengers and crew members, 5 confirmed cases were identified, 3 of whom were household personnel linked to case 1. The timing of last contact of the remaining 2 confirmed close contacts with their respective flight-associated cases suggests that infection of the flight-associated cases occurred at the same time and that time of infection coincided with the time of the flight (Appendix).

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Discussion

Among the 217 passengers and crew members on a direct flight from London to Hanoi in early March 2020, we identified a cluster of 16 laboratory-confirmed COVID-19 cases. In-depth epidemiologic investigations strongly suggest that 1 symptomatic passenger (case 1) transmitted SARS-CoV-2 infection during the flight to at least 12 other passengers in business class (probable secondary cases).

Case 1 was the only symptomatic person on board and was the only person with a flight-associated case who had established contact with a person with a confirmed case (her sister) during her incubation period. The incubation periods for all persons with confirmed flight-associated cases overlapped with the timing of the flight (Figure 2). Our interviews did not reveal that any of the additional persons with flight-associated cases had been exposed to SARS-CoV-2 before or after the flight during their incubation periods other than having taken the same flight as case 1, nor did they suggest exposure for any of the 4 travel companion couples after the flight (Appendix). Similar intervals between arrival and positive SARS-CoV-2 test results among 3 case-pairs suggest a common exposure event rather than subsequent infection from one partner to the other. Last, we found a clear association between sitting in close proximity to case 1 and risk for infection (Table 2).

In the absence of genomic analysis, we were unable to completely rule out alternative transmission routes. However, all persons with flight-associated cases departed from the United Kingdom (none transited from other countries); and until the departure date of flight VN54, only 23 COVID-19 cases had been recorded in the United Kingdom. Although testing had not been implemented on a large scale nationwide at that time (19), community transmission in the United Kingdom was not yet widely established (20), making the presence of multiple persons on board incubating the illness unlikely. Similarly, for case 4, who reported having visited India before the United Kingdom during his incubation period, the possibility of preflight transmission remains slim because by March 1, only 3 cases of COVID-19 had been reported in India, although testing in India was still limited (2022). Furthermore, none of the 30 colleagues of case 4, who shared the same preflight travel history but were all seated in economy class, were infected (Appendix).

We consider local transmission after arrival in Vietnam unlikely. As of March 1, 2020, only 16 cases of COVID-19 had been reported in Vietnam, and 17 days had passed since the last reported case (case 1 reported here became Vietnam case no. 17) (18). At that time, 1,593 persons had tested negative for SARS-CoV-2 infection in Vietnam, and according to official policy at that time, another 10,089 contacts and travelers returning from COVID-19–affected areas overseas were under preemptive quarantine directly at the time of arrival. In early March 2020, there was no evidence of community transmission of SARS-CoV-2 in Vietnam (18). We also note that cases 3 and 14 experienced symptom onset 17 days after flight VN54. Whether these cases reflect unusually long incubation periods or symptoms caused by conditions other than COVID-19 is unknown.

The most likely route of transmission during the flight is aerosol or droplet transmission from case 1, particularly for persons seated in business class (23). Contact with case 1 might also have occurred outside the airplane at the airport, in particular among business class passengers in the predeparture lounge area or during boarding. Although Vietnam Airlines keeps business class passengers separated from economy class passengers during most procedures before and during the flight, contact with the 2 economy class cases might have occurred after arrival during immigration or at baggage claim. We also note that 2 passengers, in the seats between the 2 cases in economy class, were lost to follow-up. Whether either of these passengers could represent a separate index case in economy class is unknown.

The role of fomites and on-board surfaces such as tray tables and surfaces in toilets remains unknown. For example, airline crew often use business class toilets while on board, which might explain the case among the crew serving in economy class, for whom no other potential source of infection could be established. Of note, the temporal sequence of symptom onset among cases in economy class and the crew member serving in economy class also allows for the possibility of a second in-flight transmission event, independent of the cluster in economy class (Figure 2).

Our study has several limitations. First, we did not have genomic sequencing data available to support our hypothesis of in-flight transmission. However, the conclusiveness and unambiguity of our in-depth epidemiologic upstream and downstream investigations coupled with extensive laboratory testing make us confident of our main findings. Second, we lacked detailed data on activities of the cases while on board (e.g., movements or seat changes, use of toilets, or sharing meals), which might have enabled us to pinpoint the precise route of transmission. Third, our assessment of passengers’ preflight exposure to other confirmed cases relied on interviews only. Fourth, we had no data available on individual passenger use of face masks while on board, which would have enabled a more refined risk analysis. Face masks were neither recommended nor widely used on airplanes in early March, in particular not among travelers from Europe (2426), who constituted the majority of passengers on flight VN54. Last, given the delay between arrival and confirmation of the probable index case, no environmental samples could be collected from the airplane.

Our findings have several implications for international air travel, especially because several countries have resumed air travel despite ongoing SARS-CoV-2 transmission. First, thermal imaging and self-declaration of symptoms have clear limitations, as demonstrated by case 1, who boarded the flight with symptoms and did not declare them before or after the flight. Second, long flights not only can lead to importation of COVID-19 cases but also can provide conditions for superspreader events. It has been hypothesized that a combination of environmental factors on airplanes (humidity, temperature, air flow) can prolong the presence of SARS-CoV-2 in flight cabins (27). No evidence indicated that the regular air conditioning and exchange system on flight VN54 were malfunctioning. The number of probable secondary cases detected in our study is on the upper end of hypothesized estimations for SARS-CoV-2 transmission on airplanes in the absence of face mask use, although the movement of aerosols and droplets in the specific conditions of a flight cabin remains poorly understood (27). A study of a COVID-19 cluster with 16 infected flight passengers from Singapore in February 2020 identified only 1 instance of potential in-flight transmission (28). In-flight transmission has been hypothesized but not substantiated sufficiently in a non–peer-reviewed report of a cluster of 10 flight-associated cases in China in February (N. Yang et al., unpub. data, https://www.medrxiv.org/content/10.1101/2020.03.28.20040097v1.full.pdfExternal Link). In January 2020, no secondary cases were detected after a 15-hour flight to Canada with a symptomatic person with COVID-19 on board (29), although contact tracing and monitoring were limited (30). Similar results with similar limitations have been reported from flights arriving in France (31,32) and Thailand (33) in January and February. All of these studies limited contact tracing to passengers within 2 rows of the index cases, which could explain why secondary flight-related transmission was not detected by those studies.

The latest guidance from the international air travel industry classifies the in-flight transmission risk as very low (34) and recommends only the use of face masks without additional measures to increase physical distance on board, such as blocking the middle seats (7,35). Our findings challenge these recommendations. Transmission on flight VN54 was clustered in business class, where seats are already more widely spaced than in economy class, and infection spread much further than the existing 2-row (36) or 2 meters (37) rule recommended for COVID-19 prevention on airplanes and other public transport would have captured. Similar conclusions were reached for SARS-CoV superspreader events on a flight in 2003, in which a high risk for infection was observed for passengers seated farther than 3 rows from the index case (4). This finding also concurs with transmission patterns observed for influenza virus (38) and is generally in line with the mounting evidence that airborne transmission of SARS-CoV-2 is a major yet underrecognized transmission route (39,40).

Our findings call for tightened screening and infection prevention measures by public health authorities, regulators, and the airline industry, especially in countries where substantial transmission is ongoing (37). Making mask wearing obligatory and making hand hygiene and cough etiquette standard practice while on board and at airports seems an obvious and relatively simple measure (27). Blocking middle seats, currently recommended by the airline industry (7,35), may in theory prevent some in-flight transmission events but seems to be insufficient to prevent superspreading events. Also, systematic testing, quarantine policies, or both, for inbound passengers at arrival might be justified for countries with low levels of community transmission, high risk for case importation, and limited contact tracing capacity (5). In Vietnam, for example, as a result of this investigation, national policy was changed toward mandatory testing at arrival irrespective of departure location and 14-day quarantine irrespective of test result or clinical signs/symptoms (41). This policy change eliminated the need for resource-intensive contact tracing of flight passengers altogether and enabled detection of another 106 cases among »5,000 passengers on 44 flights until all international flights were halted on March 28. However, given the logistic and economic implications of such policies, the development of a quick and reliable point-of-care test that covers the entire infectious period remains paramount.

We conclude that the risk for on-board transmission of SARS-CoV-2 during long flights is real and has the potential to cause COVID-19 clusters of substantial size, even in business class–like settings with spacious seating arrangements well beyond the established distance used to define close contact on airplanes. As long as COVID-19 presents a global pandemic threat in the absence of a good point-of-care test, better on-board infection prevention measures and arrival screening procedures are needed to make flying safe.

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Dr. Khanh is an epidemiologist at the Department of Communicable Diseases Control, National Institute of Hygiene and Epidemiology. He is a member of Rapid Response Team of Vietnam’s National Steering Committee for COVID-19 Prevention and Control. His research interests include epidemiology of viral and bacterial respiratory infectious diseases and zoonotic diseases including COVID-19, severe acute respiratory syndrome, avian influenza (H5N1), and seasonal influenza.

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Acknowledgment

We acknowledge important contributions and guidelines from the following committee and institutions: Vietnam National Steering Committee for COVID-19 Prevention and Control, Ministry of Health, Ministry of Science and Technology, and National Institute of Hygiene and Epidemiology. We also recognize Matt Moore for his suggestions and support in the course of investigation and writing the paper. We thank healthcare workers from provincial Centers for Disease Control and local authorities from cities and provinces in Vietnam for their great work with case finding, contact tracing, disease control, and prevention measures. We also thank the Civil Avian Administration, Immigration Bureau, Vietnam Airlines, and all passengers on flight VN54 for their cooperation and support.

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References

  1. World Health Organization. Coronavirus disease (COVID-19) situation reports [cited 2020 Jul 8]. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reportsExternal Link
  2. Grout  AHoward  NCoker  RSpeakman  EMGuidelines, law, and governance: disconnects in the global control of airline-associated infectious diseases. Lancet Infect Dis2017;17:e11822DOIExternal LinkPubMedExternal Link
  3. Hsu  CIShih  HHTransmission and control of an emerging influenza pandemic in a small-world airline network. Accid Anal Prev2010;42:93100DOIExternal LinkPubMedExternal Link
  4. Olsen  SJChang  HLCheung  TYYTang  AFYFisk  TLOoi  SPLet al. Transmission of the severe acute respiratory syndrome on aircraft. N Engl J Med2003;349:241622DOIExternal LinkPubMedExternal Link
  5. Myers  JFSnyder  REPorse  CCTecle  SLowenthal  PDanforth  MEet al.Traveler Monitoring TeamIdentification and monitoring of international travelers during the initial phase of an outbreak of COVID-19—California, February 3–March 17, 2020. MMWR Morb Mortal Wkly Rep2020;69:599602DOIExternal LinkPubMedExternal Link
  6. Gostic  KGomez  ACRMummah  ROKucharski  AJLloyd-Smith  JOEstimated effectiveness of symptom and risk screening to prevent the spread of COVID-19. eLife2020;9:e55570. DOIExternal LinkPubMedExternal Link
  7. Richard  M. Safely restarting aviation: ACI and IATA joint approach [cited 2020 Jul 8]. https://www.iata.org/contentassets/5c8786230ff34e2da406c72a52030e95/safely-restart-aviation-joint-aci-iata-approach.pdfExternal Link
  8. European Commission. Commission recommends gradual lifting of travel restrictions [cited 2020 Jul 8]. https://ec.europa.eu/commission/presscorner/detail/en/ip_20_1035External Link
  9. Phan  LTNguyen  TVLuong  QCNguyen  TVNguyen  HTLe  HQet al. Importation and human-to-human transmission of a novel coronavirus in Vietnam. N Engl J Med2020;382:8724DOIExternal LinkPubMedExternal Link
  10. Shira  D. COVID-19 in Vietnam: travel updates and restrictions [cited 2020 Jul 8]. https://www.vietnam-briefing.com/news/covid-19-vietnam-travel-updates-restrictions.htmlExternal Link
  11. Le  TQMTakemura  TMoi  MLNabeshima  TNguyen  LKHHoang  VMPet al. Severe acute respiratory syndrome coronavirus 2 shedding by travelers, Vietnam, 2020. Emerg Infect Dis2020;26:16246DOIExternal LinkPubMedExternal Link
  12. Vietnam Ministry of Health. Decision 343/QD-BYT regarding guidelines for surveillance, prevention and control of novel pneumonia disease caused by nCoV [in Vietnamese]. 2020 Feb 7 [cited 2020 Jul 8]. https://moh.gov.vn/web/dich-benh/huong-dan-chuyen-mon/-/asset_publisher/NxZAa8ST2KXb/content/quyet-inh-so-343-q-byt-ngay-07-02-2020-ve-viec-ban-hanh-huong-dan-tam-thoi-giam-sat-va-phong-chong-benh-viem-uong-ho-hap-cap-do-chung-moi-cua-vi-rut-cExternal Link
  13. Corman  VMLandt  OKaiser  MMolenkamp  RMeijer  AChu  DKWet al. Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR. Euro Surveill2020;25:2000045. DOIExternal LinkPubMedExternal Link
  14. Dietz  LHorve  PFCoil  DAFretz  MEisen  JAVan Den Wymelenberg  K2019 Novel coronavirus (COVID-19) pandemic: built environment considerations to reduce transmission. mSystems2020;5:e0024520DOIExternal LinkPubMedExternal Link
  15. Wang  JDu  GCOVID-19 may transmit through aerosol. Ir J Med Sci2020Epub ahead of printDOIExternal LinkPubMedExternal Link
  16. Yu  ITSLi  YWong  TWTam  WChan  ATLee  JHWet al. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N Engl J Med2004;350:17319DOIExternal LinkPubMedExternal Link
  17. World Health Organization. Transmission of SARS-CoV-2: implications for infection prevention precautions [cited 2020 Aug 10]. https://www.who.int/news-room/commentaries/detail/transmission-of-sars-cov-2-implications-for-infection-prevention-precautionsExternal Link
  18. Vietnam Ministry of Health. COVID-19 updates in Vietnam [in Vietnamese] [cited 2020 May 1]. https://ncov.moh.gov.vn/External Link
  19. Department of Health and Social Care. Coronavirus (COVID-19) in the UK: UK summary [cited 2020 Jul 13]. https://coronavirus.data.gov.uk/External Link
  20. Government of India. #IndiaFightsCorona COVID-19 in India, corona virus tracker [cited 2020 Jul 13]. https://www.mygov.in/covid-19/External Link
  21. Indian Council of Medical Research. SARS-CoV-2 (COVID-19) testing status [cited 2020 Jul 13]. https://www.icmr.gov.in/External Link
  22. van Doremalen  NBushmaker  TMorris  DHHolbrook  MGGamble  AWilliamson  BNet al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med2020;382:15647DOIExternal LinkPubMedExternal Link
  23. Elachola  HEbrahim  SHGozzer  ECOVID-19: Facemask use prevalence in international airports in Asia, Europe and the Americas, March 2020. [Internet]Travel Med Infect Dis2020;35:101637. DOIExternal LinkPubMedExternal Link
  24. Sunjaya  APJenkins  CRationale for universal face masks in public against COVID-19. Respirology2020;25:6789DOIExternal LinkPubMedExternal Link
  25. Keshtkar-Jahromi  MSulkowski  MHolakouie-Naieni  KPublic masking: an urgent need to revise global policies to protect against COVID-19. Am J Trop Med Hyg2020;102:11601DOIExternal LinkPubMedExternal Link
  26. Jayaweera  MPerera  HGunawardana  BManatunge  JTransmission of COVID-19 virus by droplets and aerosols: A critical review on the unresolved dichotomy. Environ Res2020;188:109819. DOIExternal LinkPubMedExternal Link
  27. Chen  JHe  HCheng  WLiu  YSun  ZChai  Cet al. Potential transmission of SARS-CoV-2 on a flight from Singapore to Hangzhou, China: An epidemiological investigation. Travel Med Infect Dis2020;36:101816. DOIExternal LinkPubMedExternal Link
  28. Silverstein  WKStroud  LCleghorn  GELeis  JAFirst imported case of 2019 novel coronavirus in Canada, presenting as mild pneumonia. Lancet2020;395:734DOIExternal LinkPubMedExternal Link
  29. Schwartz  KLMurti  MFinkelstein  MLeis  JAFitzgerald-Husek  ABourns  Let al. Lack of COVID-19 transmission on an international flight. CMAJ2020;192:E410. DOIExternal LinkPubMedExternal Link
  30. Eldin  CLagier  JCMailhe  MGautret  PProbable aircraft transmission of Covid-19 in-flight from the Central African Republic to France. Travel Med Infect Dis2020;35:101643. DOIExternal LinkPubMedExternal Link
  31. Bernard Stoecklin  SRolland  PSilue  YMailles  ACampese  CSimondon  Aet al. Investigation Team. First cases of coronavirus disease 2019 (COVID-19) in France: surveillance, investigations and control measures, January 2020. Euro Surveill2020;25:2000094. DOIExternal Link
  32. Okada  PBuathong  RPhuygun  SThanadachakul  TParnmen  SWongboot  Wet al. Early transmission patterns of coronavirus disease 2019 (COVID-19) in travellers from Wuhan to Thailand, January 2020. Euro Surveill2020;25:2000097. DOIExternal LinkPubMedExternal Link
  33. International Air Transport Association. IATA calls for passenger face covering and crew masks [cited 2020 Jul 8]. https://www.iata.org/en/pressroom/pr/2020-05-05-01/External Link
  34. Richard  M. Biosecurity for air transport a roadmap for restarting aviation v.2 [cited 2020 Jul 8]. https://www.iata.org/contentassets/4cb32e19ff544df590f3b70179551013/roadmap-safely-restarting-aviation.pdfExternal Link
  35. Hertzberg  VSWeiss  HOn the 2-row rule for infectious disease transmission on aircraft. Ann Glob Health2016;82:81923DOIExternal LinkPubMedExternal Link
  36. World Health Organization. Operational considerations for managing COVID-19 cases or outbreak in aviation: interim guidance, 18 Mar 2020 [cited 2020 Jul 8]. https://apps.who.int/iris/handle/10665/331488External Link
  37. Leitmeyer  KAdlhoch  CReview article: influenza transmission on aircraft. Epidemiology2016;27:74351DOIExternal LinkPubMedExternal Link
  38. Yao  MZhang  LMa  JZhou  LOn airborne transmission and control of SARS-Cov-2. Sci Total Environ2020;731:139178. DOIExternal LinkPubMedExternal Link
  39. Morawska  LMilton  DK. It is time to address airborne transmission of COVID-19. Clin Infect Dis. 2020 Jul 6:ciaa939. Epub ahead of print.
  40. Ha  BTTNgoc Quang  LMirzoev  TTai  NTThai  PQDinh  PCCombating the COVID-19 Epidemic: Experiences from Vietnam. Int J Environ Res Public Health2020;17:3125DOIExternal LinkPubMedExternal Link

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Suggested citation for this article: Khanh NC, Thai PQ, Quach H-L, Thi NA-H, Dinh PC, Duong TN, et al. Transmission of severe acute respiratory syndrome coronavirus 2 during long flight. Emerg Infect Dis. 2020 Nov [date cited]. https://doi.org/10.3201/eid2611.203299

DOI: 10.3201/eid2611.203299

Original Publication Date: September 18, 2020

1These first authors contributed equally to this article.

2These last authors contributed equally to this article.

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Even more evidence shows the coronavirus spreads easily on long plane flights – Business Insider

Susie Neilson Sep 19, 2020, 12:12 PM

  • A CDC study offers even more evidence that the coronavirus spreads on airplanes.
  • Epidemiologists traced 16 coronavirus cases back to a single 10-hour flight where one symptomatic passenger was seated in business class.
  • The case study showed that 92% of passengers sitting two seats or fewer away from the passenger contracted the coronavirus.
  • It’s unlikely most of the passengers on the flight were wearing masks.

On March 1, 217 people boarded a plane in London, England, bound for Hanoi, Vietnam.

Healthcare workers had already examined each passenger, asking them to report any potential COVID-19 symptoms and doing temperature scans.

But a 27-year-old businesswoman didn’t report that she had a sore throat and a cough. And her temperature scan was normal.

However, the woman’s symptoms progressed over the following days; she tested positive for COVID-19 on March 6.

Subsequent contact tracing revealed that on that 10-hour flight alone, the woman had passed the virus to 15 other passengers.

The case study, described in a new report from the Centers for Disease Control and Prevention, offers even stronger evidence that the coronavirus can spread on planes – particularly when passengers aren’t wearing masks. In early March, face masks weren’t yet mandatory on flights, so it’s likely most passengers weren’t wearing them.

92% of passengers within 2 seats of the infected woman got sick

Upon learning of the businesswoman’s infection, researchers at Vietnam’s National Institute of Hygiene and Epidemiology contact traced the people on the flight — passengers and crew members. Local health staff interviewed everyone they could reach (184 people), and told anyone with a suspected COVID-19 case to self-quarantine, along with their close contacts.

The 15 cases health workers identified were all considered “flight-associated,” meaning they could be reliably traced back to the flight and not another event. None of the other infected passengers had displayed COVID-19 symptoms before or during the flight. And nobody had been around anyone else with a confirmed case of coronavirus except the businesswoman, who’d traveled to Italy with her sister (who later tested positive in London).

Twelve of the infected passengers were in business class, and all but one of those were sitting two or fewer seats away from the woman – 92% of all the passengers sitting that close got sick. The virus also spread to two passengers in economy class and one crew member.

The researchers concluded that the woman most likely spread the coronavirus to other business-class passengers and the crew member via infected droplets or aerosols (tiny particles that get expelled from the mouth when someone breathes, talks, or yells).

The two economy-class passengers could have been infected in the airport during customs or at baggage claim, by touching a contaminated surface or standing near the woman for an extended period of time.

Although the researchers said they couldn’t completely rule out the possibility that the passengers got infected in other ways, they noted that on March 1, the UK had only 23 recorded COVID-19 cases. Likewise, at the time the passengers arrived in Vietnam, the country had only recorded 16 cases – making it unlikely they’d contracted the disease after they left the airport.

Plus, most of the cases were clustered together in business class – which would be unlikely if they’d come from different sources.

Airlines may need stricter rules to stop the coronavirus’ spread

Based on their findings, the researchers think airlines might be downplaying the risks of coronavirus transmission on flights.

“The latest guidance from the international air-travel industry classifies the in-flight transmission risk as very low, and recommends only the use of face masks without additional measures to increase physical distance on board, such as blocking the middle seats,” the authors wrote. “Our findings challenge these recommendations.”

However, MIT researchers calculated in a July paper that filling middle seats could double the risk of COVID-19 transmission on a plane flight. (That study has not yet been peer-reviewed, however.)

The epidemiologists behind the new CDC study said even blocking off middle seats can’t fully prevent super-spreader events on planes, though, given that the sick passenger on the flight studied spread the virus to those two seats away. Plus, those people were in business class, where seats are larger and more spread out than in economy.

So the researchers suggested that airlines and government officials = implement stricter screening policies for travelers, test everyone who gets off a flight, and make all newly arrived passengers quarantine for 14 days.

Currently, every major US airline requires passengers to wear masks for their entire flight, except while eating or drinking. But not all passengers cooperate, and getting everyone to wear masks for the entirety of a long flight, like the 10-hour one from London to Hanoi, can be even more difficult.