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Correspondence

Spread of a Novel Influenza A (H1N1) Virus via Global Airline Transportation

N Engl J Med 2009; 361:212-214July 9, 2009

Article

To the Editor:

Throughout March and April 2009, international air travelers departing from Mexico were unknowingly transporting a novel influenza A (H1N1) virus1 to cities around the world. We analyzed the flight itineraries for all passengers departing from 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 disseminate worldwide during the initial wavefront of this epidemic. We analyzed IATA data from March and April 2008 for the following reasons: the data accounted for more than 95% of all passenger trips worldwide via commercial airlines, they included information on the flight origins and destinations of actual passengers, data on passenger itineraries for the period from March through April 2009 were unavailable at the time of this analysis, the global pattern of passenger departures from Mexico between March and April varies minimally from year to year, and the epidemic in Mexico was largely unrecognized during the period from March through April 2009, with passenger departures presumably following their usual seasonal pattern.

Our analysis showed that in March and April 2008, a total of 2.35 million passengers flew from Mexico to 1018 cities in 164 countries (Figure 1Figure 1Destination Cities and Corresponding Volumes of International Passengers Arriving from Mexico between March 1 and April 30, 2008., and Table 1 in the Supplementary Appendix, available with the full text of this letter at NEJM.org). A total of 80.7% of passengers had flight destinations in the United States or Canada; 8.8% in Central America, South America, or the Caribbean Islands; 8.7% in Western Europe; 1.0% in East Asia; and 0.8% elsewhere. These flight patterns were very similar to those during the same months in 2007 (see Fig. 1 in the Supplementary Appendix). We then compared the international destinations of travelers departing from Mexico with confirmed H1N1 importations associated with travel to Mexico, and we found a remarkably strong degree of correlation. Of the 20 countries worldwide with the highest volumes of international passengers arriving from Mexico, 16 had confirmed importations associated with travel to Mexico as of May 25, 2009 (Table 1Table 1Countries 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).). A receiver-operating-characteristic (ROC) curve plotting the relationship between international air-traffic flows and H1N1 importation revealed that countries receiving more than 1400 passengers from Mexico were at a significantly elevated risk for importation. With the use of this passenger threshold, international air-traffic volume alone was more than 92% sensitive and more than 92% specific in predicting importation, with an area under the ROC curve of 0.97 (see Fig. 2 in the Supplementary Appendix).

Although the correlation between the international movements of travelers and H1N1 is generally intuitive, our findings suggest that quantitative analysis of worldwide air-traffic patterns can help cities and countries around the world better anticipate their risks of importing global infectious diseases. In response to the outbreak of the severe acute respiratory syndrome in Toronto, an initiative called the Bio.Diaspora Project2 was developed to conduct rapid assessments of global infectious-disease alerts3 or confirmed epidemics by evaluating the probable pathways of international dissemination from any commercial airport worldwide at any point in time. Operating under the framework of the revised International Health Regulations,4 the initiative also examines how countries are connected by shared risks of importing global infectious diseases and considers the implications for potential shared responsibilities that could strengthen the fabric of public health security in the world.5

Kamran Khan, M.D., M.P.H.
St. Michael's Hospital, Toronto, ON M5B 1W8, Canada

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.

5 References
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    Outbreak of swine-origin influenza A (H1N1) virus infection -- Mexico, March-April 2009. MMWR Morb Mortal Wkly Rep 2009;58:467-470
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  2. 2

    The Bio.Diaspora Project. Toronto: St. Michael's Hospital. (Accessed June 18, 2009, at http://www.biodiaspora.com.)

  3. 3

    Global Public Health Intelligence Network (GPHIN). Ottawa: Public Health Agency of Canada. (Accessed June 18, 2009, at http://www.phac-aspc.gc.ca/media/nr-rp/2004/2004_gphin-rmispbk-eng.php.)

  4. 4

    International Health Regulations. Geneva: World Health Organization. (Accessed June 18, 2009, at http://www.who.int/topics/international_health_regulations/en/.)

  5. 5

    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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