To the Editor: Throughout March and April 2009, internationalair travelers departing from Mexico were unknowingly transportinga novel influenza A (H1N1) virus1 to cities around the world.We analyzed the flight itineraries for all passengers departingfrom commercial airports in Mexico between March and April 2008,using data from the International Air Transport Association(IATA). The purpose of this analysis was to show how travelers— and consequently to predict how H1N1 — would disseminateworldwide during the initial wavefront of this epidemic. Weanalyzed IATA data from March and April 2008 for the followingreasons: the data accounted for more than 95% of all passengertrips worldwide via commercial airlines, they included informationon the flight origins and destinations of actual passengers,data on passenger itineraries for the period from March throughApril 2009 were unavailable at the time of this analysis, theglobal pattern of passenger departures from Mexico between Marchand April varies minimally from year to year, and the epidemicin Mexico was largely unrecognized during the period from Marchthrough April 2009, with passenger departures presumably followingtheir usual seasonal pattern.
Our analysis showed that in March and April 2008, a total of2.35 million passengers flew from Mexico to 1018 cities in 164countries (Figure 1, and Table 1 in the Supplementary Appendix,available with the full text of this letter at NEJM.org). Atotal of 80.7% of passengers had flight destinations in theUnited States or Canada; 8.8% in Central America, South America,or the Caribbean Islands; 8.7% in Western Europe; 1.0% in EastAsia; and 0.8% elsewhere. These flight patterns were very similarto those during the same months in 2007 (see Fig. 1 in the Supplementary Appendix).We then compared the international destinations of travelersdeparting from Mexico with confirmed H1N1 importations associatedwith travel to Mexico, and we found a remarkably strong degreeof correlation. Of the 20 countries worldwide with the highestvolumes of international passengers arriving from Mexico, 16had confirmed importations associated with travel to Mexicoas of May 25, 2009 (Table 1). A receiver-operating-characteristic(ROC) curve plotting the relationship between internationalair-traffic flows and H1N1 importation revealed that countriesreceiving more than 1400 passengers from Mexico were at a significantlyelevated risk for importation. With the use of this passengerthreshold, international air-traffic volume alone was more than92% sensitive and more than 92% specific in predicting importation,with an area under the ROC curve of 0.97 (see Fig. 2 in theSupplementary Appendix).
Table 1. Countries Receiving the Largest Numbers of Passengers from Mexico during March and April 2008 and Importation of the Influenza A (H1N1) Virus Associated with Travel to Mexico (as of May 25, 2009).
Although the correlation between the international movementsof travelers and H1N1 is generally intuitive, our findings suggestthat quantitative analysis of worldwide air-traffic patternscan help cities and countries around the world better anticipatetheir risks of importing global infectious diseases. In responseto the outbreak of the severe acute respiratory syndrome inToronto, an initiative called the Bio.Diaspora Project2 wasdeveloped to conduct rapid assessments of global infectious-diseasealerts3 or confirmed epidemics by evaluating the probable pathwaysof international dissemination from any commercial airport worldwideat any point in time. Operating under the framework of the revisedInternational Health Regulations,4 the initiative also examineshow countries are connected by shared risks of importing globalinfectious diseases and considers the implications for potentialshared responsibilities that could strengthen the fabric ofpublic health security in the world.5
Kamran Khan, M.D., M.P.H. St. Michael's Hospital Toronto, ON M5B 1W8, Canada khank{at}smh.toronto.on.ca
Julien Arino, Ph.D. University of Manitoba Winnipeg, MB R3T 2N2, Canada
Wei Hu, B.Sc. Paulo Raposo, B.Sc. Jennifer Sears, B.Sc. Felipe Calderon, M.Sc. Christine Heidebrecht, M.Sc. St. Michael's Hospital Toronto, ON M5B 1W8, Canada
Michael Macdonald, M.S.A. Ryerson University Toronto, ON M5B 2K3, Canada
Jessica Liauw, B.H.Sc. Queen's University Kingston, ON K7L 3N6, Canada
Angie Chan, M.P.A. St. Michael's Hospital Toronto, ON M5B 1W8, Canada
Michael Gardam, M.D., M.Sc. University Health Network Toronto,ON M5G 2C4, Canada
This letter (10.1056/NEJMc0904559) was published on June 29,2009, at NEJM.org.
References
Outbreak of swine-origin influenza A (H1N1) virus infection -- Mexico, March-April 2009. MMWR Morb Mortal Wkly Rep 2009;58:467-470. [Medline]
The Bio.Diaspora Project. Toronto: St. Michael's Hospital. (Accessed June 18, 2009, at http://www.biodiaspora.com.)
The World Health Report 2007 — a safer future: global public health security in the 21st century. Geneva: World Health Organization. (Accessed June 18, 2009, at http://www.who.int/whr/2007/en/index.html.)
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