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Human Mobility and the Global Spread of Infectious Diseases: A Focus on Air Travel

2018; Elsevier BV; Volume: 34; Issue: 9 Linguagem: Inglês

10.1016/j.pt.2018.07.004

1471-5007

Aidan Findlater, Isaac I. Bogoch,

Viral Infections and Outbreaks Research

The volume of global air travel continues to increase annually, and passengers have the capacity to introduce infections to new regions in short time frames. Infections transported through air travel may initiate or facilitate epidemics. Front-line healthcare providers and public health teams require training and tools to properly identify and respond to infectious diseases transported through air travel, some of which may have epidemic potential. Developing more effective global surveillance tools and mechanisms to better communicate and coordinate between countries can facilitate more rapid and effective responses to epidemics. Greater human mobility, largely driven by air travel, is leading to an increase in the frequency and reach of infectious disease epidemics. Air travel can rapidly connect any two points on the planet, and this has the potential to cause swift and broad dissemination of emerging and re-emerging infectious diseases that may pose a threat to global health security. Investments to strengthen surveillance, build robust early-warning systems, improve predictive models, and coordinate public health responses may help to prevent, detect, and respond to new infectious disease epidemics. Greater human mobility, largely driven by air travel, is leading to an increase in the frequency and reach of infectious disease epidemics. Air travel can rapidly connect any two points on the planet, and this has the potential to cause swift and broad dissemination of emerging and re-emerging infectious diseases that may pose a threat to global health security. Investments to strengthen surveillance, build robust early-warning systems, improve predictive models, and coordinate public health responses may help to prevent, detect, and respond to new infectious disease epidemics. Increases in the global mobility of humans, nonhuman animals, plants, and products are driving the introduction of infectious diseases to new locations. In recent years we have witnessed several infectious diseases spread well beyond their previously understood geographic boundaries, as was demonstrated by the introduction of Zika virus to the Americas. We have also witnessed the emergence and spread of novel pathogens, such as the discovery of a previously unknown Middle Eastern respiratory syndrome coronavirus (MERS-CoV) in Saudi Arabia spreading to distant countries such as South Korea [1Tatem A.J. et al.Global transport networks and infectious disease spread.Adv. Parasitol. 2006; 62: 293-343Crossref PubMed Scopus (161) Google Scholar]. Many factors contribute to the global spread of infectious diseases, including the increasing speed and reach of human mobility, increasing volumes of trade and tourism, and changing geographic distributions of disease vectors. In particular, human travel and migration (especially via air travel) is now a major driving force pushing infections into previously nonendemic settings. Year by year, there are increasing numbers of international tourists [2UN World Tourism Organization UNWTO Tourism Highlights.2017 edition. United Nations, 2017Google Scholar], more international refugees and migrants [3United Nations, Department of Economic and Social Affairs, Population Division International Migration Report 2017: Highlights. United Nations, 2017Google Scholar], greater capacity for shipping by sea [4Institute of Shipping Economics and Logistics (2017) World Seaborne Trade and World Port Traffic. Shipping Statistics and Market Review 61Google Scholar], and greater international air travel passenger volumes [5International Air Transport Association IATA Annual Review 2017. IATA, 2017Google Scholar]. Air travel poses a growing threat to global health security, as it is now possible for a traveler harboring an infection in one location on earth to travel to virtually any other point on the planet in only 1–2 days. Infections introduced via travel may be sporadic and have little potential for further transmission, such as Lassa fever introduced into European settings [6Haas W.H. et al.Imported Lassa fever in Germany: surveillance and management of contact persons.Clin. Infect. Dis. 2003; 36: 1254-1258Crossref PubMed Scopus (97) Google Scholar]. In other situations, infections introduced by air travel may cause self-limited local epidemics such as Chikungunya virus in Italy [7Angelini R. et al.An outbreak of chikungunya fever in the province of Ravenna, Italy.Euro Surveill. 2007; 12: 12-14Google Scholar]. More recently, there are a growing number of examples of infections introduced to a new region that ultimately become endemic, such as Chikungunya virus in Latin America and the Caribbean [8Khan K. et al.Assessing the origin of and potential for international spread of chikungunya virus from the Caribbean.PLoS Curr. 2014; 6: 1-11Google Scholar]. Vector-borne infections, including arthropod-borne viruses (arboviruses) present unique challenges as disease vectors such as mosquitoes can be carried overland, in boats, or on planes, and may travel between any two points on the globe within their lifespan. Such vectors have the potential to infect nontravelers in their new destination, as is seen in airport malaria [6Haas W.H. et al.Imported Lassa fever in Germany: surveillance and management of contact persons.Clin. Infect. Dis. 2003; 36: 1254-1258Crossref PubMed Scopus (97) Google Scholar]. Even if a vector is not infected, that vector may become endemic to a new region if there are suitable environmental conditions, and then potentially enable future epidemics. The most well-known example of this is the now-global distribution of Aedes aegypti and Ae. albopictus mosquitoes, the vectors responsible for a number of arbovirus infections including dengue, Chikungunya, and Zika viruses [9Kraemer M.U.G. et al.The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus.eLife. 2015; 4e08347Crossref PubMed Scopus (355) Google Scholar]. Vector introduction is further facilitated by ecological factors, such as climate change and urbanization, that may enable vectors to flourish in new regions. Clinical and public health care providers must be aware of the fluid boundaries of infectious diseases and be cognizant of the potential for imported infections. Front-line healthcare providers must now have knowledge of an increasingly broad spectrum of emerging illnesses from around the world, and public health teams must be prepared to respond to individual cases that have epidemic potential (e.g., Ebola virus), and coordinate responses at local, national, and international levels. Preparation for planning mass gatherings, such as large sporting events or an annual religious pilgrimage, require special consideration for the potential of these events to contribute to global outbreaks. Here, we outline emerging and re-emerging infectious diseases that are spread via human mobility, with a focus on air travel. We discuss sporadic cases and localized epidemics, international epidemics, and then focus on clinical and public health implications. Travel-related illnesses are common and mostly mild and self-limited, such as traveler's diarrhea. However, the list of infections imported by returned travelers is growing [10Leder K. et al.GeoSentinel surveillance of illness in returned travelers, 2007–2011.Ann. Intern. Med. 2013; 158: 456-468Crossref PubMed Scopus (180) Google Scholar], and many are capable of causing local epidemics (Table 1).Table 1Recent Emerging and Re-emerging Infectious Diseases of Global Health Significance, Whose Spread Was Facilitated by Air TravelDiseaseOrigin (Year)DestinationInfluenza H1N1Mexico (2009) 48Mena I. et al.Origins of the 2009 H1N1 influenza pandemic in swine in Mexico.eLife. 2016; 5e16777Crossref PubMed Scopus (21) Google ScholarPandemic 50Simonsen L. et al.Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study.PLoS Med. 2013; 10e1001558Crossref PubMed Scopus (140) Google ScholarVibrio choleraeSouth Asia (2002, 2008)Haiti epidemic (2010) 117Chin C.-S. et al.The origin of the Haitian cholera outbreak strain.N. Engl. J. Med. 2011; 364: 33-42Crossref PubMed Scopus (415) Google ScholarNDM-1 carbapenem-resistant Gram-negative bacteriaIndia (2009) 84Yong D. et al.Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India.Antimicrob. Agents Chemother. 2009; 53: 5046-5054Crossref PubMed Scopus (1189) Google ScholarAustralia, Austria, Belgium, Canada, China, Croatia, Czech Republic, Denmark, France, Germany, Ireland, Italy, Japan, Kuwait, Lebanon, The Netherlands, New Zealand, Norway Oman, Singapore, South Africa, Spain, Sweden, Switzerland, Taiwan, Turkey, United Kingdom, USA 85Berrazeg M. et al.New Delhi Metallo-beta-lactamase around the world: an eReview using Google Maps.Euro Surveill. 2014; 19: 20809Crossref PubMed Google Scholarmcr-1 colistin-resistant Gram-negative bacteriaChina (2014) 118Liu Y.-Y. et al.Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study.Lancet Infect. Dis. 2016; 16: 161-168Abstract Full Text Full Text PDF PubMed Scopus (1084) Google ScholarAlgeria, Argentina, Belgium, Brazil, Cambodia, Canada, China, Denmark, Egypt, France, Germany, Great Britain, Italy, Japan, Laos, Lithunia, Malaysia, The Netherlands, Nigeria, Poland, Portugal, South Africa, Spain, Switzerland, Taiwan, Thailand, Tunisia, USA, Vietnam 87Schwarz S. Johnson A.P. Transferable resistance to colistin: a new but old threat.J. Antimicrob. Chemother. 2016; 71: 2066-2070Crossref PubMed Scopus (170) Google ScholarDengue virusPrimarily Southeast Asia (1950s) 55Gubler D.J. Dengue, urbanization and globalization: the unholy trinity of the 21st century.Trop. Med. Health. 2011; 39: 3-11Crossref PubMed Scopus (279) Google ScholarGlobal emergence over the past five decades 55Gubler D.J. Dengue, urbanization and globalization: the unholy trinity of the 21st century.Trop. Med. Health. 2011; 39: 3-11Crossref PubMed Scopus (279) Google ScholarMERS-CoVSaudi Arabia (2012) 25de Groot R.J. et al.Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group.J. Virol. 2013; 87: 7790-7792Crossref PubMed Scopus (303) Google ScholarEpidemics in South Korea and Saudi Arabia, with cases detected in Algeria, Austria, China, Egypt, France, Germany, Greece, Iran, Italy, Jordan, Kuwait, Lebanon, The Netherlands, Oman, Philippines, Qatar, Thailand, Tunisia, Turkey, Turkey, United Arab Emirates, United Kingdom, USA, Yemen 119Mackay I.M. Arden K.E. MERS coronavirus: diagnostics, epidemiology and transmission.Virol. J. 2015; 12: 222Crossref PubMed Scopus (36) Google ScholarZika virusAfrica and Asia 69Duffy M.R. et al.Zika virus outbreak on Yap Island, Federated States of Micronesia.N. Engl. J. Med. 2009; 360: 2536-2543Crossref PubMed Scopus (1169) Google ScholarFirst detected in Latin America and the Caribbean in 2015 with ongoing transmission in the South Pacific, Latin America and the Caribbean 71Faria N.R. et al.Zika virus in the Americas: Early epidemiological and genetic findings.Science. 2016; 352: 345-349Crossref PubMed Scopus (370) Google ScholarChikungunya virusAsia and Africa 8Khan K. et al.Assessing the origin of and potential for international spread of chikungunya virus from the Caribbean.PLoS Curr. 2014; 6: 1-11Google Scholar, 121Leparc-Goffart I. et al.Chikungunya in the Americas.Lancet. 2014; 383: 514Abstract Full Text Full Text PDF PubMed Scopus (266) Google ScholarLatin America and the Caribbean in December 2013 with ongoing transmission in this region 120Pan American Health Organization Number of Reported Cases of Chikungunya Fever in the Americas – EW 51 (December 22, 2017). Pan American Health Organization, 2017Google Scholar, and autochthonous cases in Europe 60Tomasello D. Schlagenhauf P. Chikungunya and dengue autochthonous cases in Europe, 2007-2012.Travel Med. Infect. Dis. 2013; 11: 274-284Abstract Full Text Full Text PDF PubMed Scopus (79) Google ScholarSARS-CoV (2002)Southern China (2002) 22Christian M.D. et al.Severe acute respiratory syndrome.Clin. Infect. Dis. 2004; 38: 1420-1427Crossref PubMed Scopus (97) Google ScholarEpidemics in Hong Kong, Canada, USA, Vietnam, Singapore, Philippines, and Mongolia 22Christian M.D. et al.Severe acute respiratory syndrome.Clin. Infect. Dis. 2004; 38: 1420-1427Crossref PubMed Scopus (97) Google ScholarSchistosomiasisAfricaEpidemic in Corsica (2013), with ongoing transmission 20Ramalli L. et al.Persistence of schistosomal transmission linked to the Cavu river in southern Corsica since 2013.Euro Surveill. 2018; (Published online 25 January 2018)https://doi.org/10.2807/1560-7917.ES.2018.23.4.18-00017Crossref PubMed Scopus (1) Google Scholar Open table in a new tab Despite a global push for eradication, malaria continues to cause significant global morbidity and mortality. This protozoal vector-borne infection is transmitted to humans by the bite of infected Anopheles mosquitoes that are found in many tropical and temperate countries [11Sinka M.E. et al.A global map of dominant malaria vectors.Parasit. Vectors. 2012; 5: 69Crossref PubMed Scopus (184) Google Scholar]. Malaria is a common cause of febrile illness in returned travelers [12Boggild A.K. et al.Travel-acquired infections and illnesses in Canadians: surveillance report from CanTravNet surveillance data, 2009-2011.Open Med. 2014; 8: e20-e32PubMed Google Scholar], and delays in diagnosis may lead to poor patient outcomes, including death [13McCarthy A.E. et al.Severe malaria in Canada, 2001–2013.Malar. J. 2015; 14: 151Crossref PubMed Google Scholar]. The incubation period varies from weeks to more than a month depending on the species, which frequently contributes to the delayed diagnosis of imported cases. Airport malaria, where non-travelers near airports are infected by mosquitoes that have been imported by air travel [14Isaäcson M. Airport malaria: a review.Bull. World Health Organ. 1989; 67: 737-743PubMed Google Scholar], is a challenging diagnosis as local clinicians may not suspect this infection. Although the spraying of arriving planes has reduced the incidence of cases, it continues to be a concern as volumes of travel continue to increase [15Tatem A.J. et al.Estimating the malaria risk of African mosquito movement by air travel.Malar. J. 2006; 5: 57Crossref PubMed Scopus (42) Google Scholar] and case reports of malaria in non-travelers continue to grow [16Pomares-Estran C. et al.Atypical aetiology of a conjugal fever: autochthonous airport malaria between Paris and French Riviera: a case report.Malar. J. 2009; 8: 202Crossref PubMed Scopus (5) Google Scholar]. Regions that have eradicated malaria but still have Anopheles vectors present are at risk of malaria reintroduction, for example in Sri Lanka [17Wickremasinghe A.R. et al.Should chemoprophylaxis be a main strategy for preventing re-introduction of malaria in highly receptive areas? Sri Lanka a case in point.Malar. J. 2017; 16: 102Crossref PubMed Scopus (1) Google Scholar]. The global distribution of drug-resistant malaria is also changing, and strains of multidrug-resistant Plasmodium falciparum appear to be spreading [18Imwong M. et al.Spread of a single multidrug resistant malaria parasite lineage (PfPailin) to Vietnam.Lancet Infect. Dis. 2017; 17: 1022-1023Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar]. Although multidrug-resistant strains are still generally rare, there is growing concern that such strains may expand beyond their current boundaries through boat and air travel, heightening the need for better surveillance. Chronic infection with schistosomiasis is associated with gastrointestinal or urogenital pathology [19Ouma J.H. et al.Morbidity in schistosomiasis: an update.Trends Parasitol. 2001; 17: 117-118Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar]. Schistosomiasis is acquired via contact with contaminated fresh water and requires specific snail intermediate hosts for disease transmission [19Ouma J.H. et al.Morbidity in schistosomiasis: an update.Trends Parasitol. 2001; 17: 117-118Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar]. Locally acquired cases of schistosomiasis were discovered recently in France, and these were most certainly introduced by travelers from endemic settings in Africa [20Ramalli L. et al.Persistence of schistosomal transmission linked to the Cavu river in southern Corsica since 2013.Euro Surveill. 2018; (Published online 25 January 2018)https://doi.org/10.2807/1560-7917.ES.2018.23.4.18-00017Crossref PubMed Scopus (1) Google Scholar]. Snails local to Corsica were found to be competent hosts of Schistosoma haematobium, Schistosoma bovis, and hybrids of the two infections. There is the potential for further disease expansion given ongoing human travel and migration from schistosomiasis-endemic regions to nonendemic areas with the requisite intermediate snail hosts. Air travel has contributed to several epidemics of global health significance in recent years. Typically, an infected individual, either symptomatic or within an incubation period, flies to a distant location and introduces this infection to the local population. Below, we discuss major international epidemics relevant to air travel after 2000. The severe acute respiratory syndrome (SARS) outbreak of 2002–2003 is an example of an emerging infection causing several simultaneous epidemics in noncontiguous geographic regions. SARS is a respiratory tract infection caused by a zoonotic coronavirus (SARS-CoV), and is thought to have arisen in horseshoe bats and subsequently transmitted to humans through civets as intermediate hosts [21Hu B. et al.Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus.PLoS Pathog. 2017; 13e1006698Crossref PubMed Scopus (8) Google Scholar]. The 2002 SARS epidemic originated in southern China and spread via air travel to 29 countries, causing local epidemics in Hong Kong, Taiwan, Canada, Singapore, Vietnam, and the Philippines [22Christian M.D. et al.Severe acute respiratory syndrome.Clin. Infect. Dis. 2004; 38: 1420-1427Crossref PubMed Scopus (97) Google Scholar]. The global epidemic lasted about 8 months, with 8096 probable cases and 774 deaths for a case-fatality rate of 10% [22Christian M.D. et al.Severe acute respiratory syndrome.Clin. Infect. Dis. 2004; 38: 1420-1427Crossref PubMed Scopus (97) Google Scholar]. SARS caused widespread panic and cost an estimated US$11 billion worldwide [23Saywell T. et al.The cost of SARS: $11 billion and rising.Dow Jones Far East. Econ. Rev. 2003; 166: 12-17Google Scholar]. Although the public health response was swift and ultimately effective, this epidemic highlighted the need for increased international cooperation in the era of rapid global transit. This epidemic spurred revisions to the International Health Regulations (IHR) and introduced the most significant changes since their adoption [24Fidler D.P. Gostin L.O. The new International Health Regulations: an historic development for international law and public health.J. Law Med. Ethics. 2006; 34 (4): 85-94Crossref PubMed Scopus (93) Google Scholar]. Another novel zoonotic respiratory coronavirus, MERS-CoV, originated in Saudi Arabia in 2012 [25de Groot R.J. et al.Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group.J. Virol. 2013; 87: 7790-7792Crossref PubMed Scopus (303) Google Scholar]. Its reservoir is thought to be the dromedary camel. Similar to SARS-CoV, MERS-CoV causes a respiratory infection, though with a higher case-fatality rate of about 35% [26Yang Y.-M. et al.Impact of comorbidity on fatality rate of patients with Middle East Respiratory Syndrome.Sci. Rep. 2017; 7: 11307Crossref PubMed Scopus (1) Google Scholar]. Since 2012, over 2000 cases have been detected in 27 countries. South Korea experienced the largest epidemic outside of Saudi Arabia, which was initiated by a single infected business traveler returning from that country. This one index case at a single hospital resulted in an additional 184 confirmed cases at 17 hospitals, and caused 33 deaths before the epidemic ended 2 months later [27Ki M. 2015 MERS outbreak in Korea: hospital-to-hospital transmission.Epidemiol. Health. 2015; 37e2015033Crossref PubMed Google Scholar]. Infection risk appeared to be primarily through hospital-based contact and fomites rather than through household contacts [28Lee S.S. Wong N.S. Probable transmission chains of Middle East respiratory syndrome coronavirus and the multiple generations of secondary infection in South Korea.Int. J. Infect. Dis. 2015; 38: 65-67Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. Although the virus is thought to have low epidemic potential, epidemics such as the one in South Korea are not unexpected [29Kucharski A.J. Althaus C.L. The role of superspreading in Middle East respiratory syndrome coronavirus (MERS-CoV) transmission.Euro Surveill. 2015; 20: 14-18Crossref PubMed Scopus (30) Google Scholar]. There are a number of countries at risk of importing cases via air travel due to close trade and tourism ties to Saudi Arabia [30Gardner L.M. et al.Risk of global spread of Middle East respiratory syndrome coronavirus (MERS-CoV) via the air transport network.J. Travel Med. 2016; 23: 1-8Crossref Scopus (2) Google Scholar]. Additionally, the annual Hajj pilgrimage brings millions of pilgrims from around the world to Saudi Arabia, raising the potential for future epidemics [31Zumla A. et al.Infectious diseases epidemic threats and mass gatherings: Refocusing global attention on the continuing spread of the Middle East Respiratory syndrome coronavirus (MERS-CoV).BMC Med. 2016; 14: 2012-2015Crossref Scopus (5) Google Scholar]. The 2014 Ebola virus disease (EVD) epidemic in West Africa also highlighted the risks of global infectious disease transmission in an increasingly connected world. This zoonotic virus has a probable bat reservoir [32Leendertz S.A.J. et al.Assessing the evidence supporting fruit bats as the primary reservoirs for Ebola viruses.Ecohealth. 2016; 13: 18-25Crossref PubMed Scopus (28) Google Scholar] and is spread between humans through contact with infected body fluids. EVD can incubate for up to 3 weeks before presenting as a severe febrile illness with multisystem organ failure and hemorrhagic tendencies. Epidemics have largely been confined to Africa, with case fatality rates between 30% to upwards of 80% [33Lefebvre A. et al.Case fatality rates of Ebola virus diseases: a meta-analysis of World Health Organization data.Med. Mal. Infect. 2014; 44: 412-416Crossref PubMed Scopus (32) Google Scholar]. The largest EVD epidemic began in Sierra Leone in 2014. Starting in a rural town, the epidemic spread via land travel to bordering Guinea and Liberia. From there, cases began appearing on several continents via international air travel. In the USA, for instance, one returned traveler infected two healthcare workers before local transmission stopped [34Regan J.J. et al.Public health response to commercial airline travel of a person with Ebola virus infection – United States, 2014.MMWR Morb. Mortal. Wkly. Rep. 2015; 64: 63-66PubMed Google Scholar]. Similar imported cases were seen in Italy and the United Kingdom, and a short chain of healthcare-related transmission was documented following the return of an infected Spanish citizen back to Spain [35Bertoli G. et al.Ebola virus disease: Case management in the Institute of Infectious Diseases, University Hospital of Sassari, Sardinia, Italy.J. Infect. Dev. 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During the 2014 EVD epidemic, many countries hastily instituted policies that limited travel to and from EVD-affected countries. Some countries closed land and air borders with Guinea, Liberia, and Sierra Leone [39Cohen N.J. Travel and border health measures to prevent the international spread of Ebola.MMWR. 2016; 65: 57-67Crossref Scopus (7) Google Scholar, 40BBC News (2014) Ivorian land border shut over Ebola. BBC News 23 August 2014Google Scholar], and others, including Australia and Canada, temporarily refused to issue visas to travelers from affected countries [41CBC News (2014) Canada won't issue visas to residents of Ebola outbreak countries. CBC News 21 October 2014Google Scholar], a policy not aligned with the World Health Organization (WHO)'s IHR. The USA imposed enhanced screening procedures that measured the temperature of returned travelers from affected countries for up to 3 weeks. The 2014 EVD epidemic highlighted how governments may rapidly impose policy related to an emerging infection of epidemic potential, although the effectiveness of many of these policies is still debated. Influenza A virus causes predictable seasonal epidemics in both northern and southern hemispheres. Influenza A virus also circulates in birds and pigs and has the potential to mutate more rapidly compared to influenza B virus, allowing the virus to recombine with different strains and cause epidemics. Many individuals infected with influenza A virus will experience a self-limited febrile illness punctuated with myalgia and malaise, and this infection is also associated with severe illness and is responsible for roughly 300 000–600 000 deaths per year, globally [42Iuliano A.D. et al.Estimates of global seasonal influenza-associated respiratory mortality: a modelling study.Lancet. 2018; 391: 1285-1300Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar]. The 1918 influenza pandemic demonstrated the ability of influenza A virus to cause a global catastrophe in the era of increasing global mobility, as it resulted in an estimated 50 million deaths worldwide [43Johnson N.P.A.S. Mueller J. Updating the accounts: global mortality of the 1918–1920 'Spanish' influenza pandemic.Bull. Hist. Med. 2002; 76: 105-115Crossref PubMed Google Scholar]. Seasonal influenza strains are now more mobile than ever, and the effect of air travel is a well-established mechanism for facilitating global influenza transmission [44Grais R.F. et al.Modeling the spread of annual influenza epidemics in the U.S.: the potential role of air travel.Health Care Manag. Sci. 2004; 7: 127-134Crossref PubMed Scopus (74) Google Scholar, 45Brownstein J.S. et al.Empirical evidence for the effect of airline travel on inter-regional influenza spread in the United States.PLoS Med. 2006; 3: e401Crossref PubMed Scopus (127) Google Scholar, 46Rvachev L.A. Longini I.M. A mathematical model for the global spread of influenza.Math. Biosci. 1985; 75: 3-22Crossref Scopus (313) Google Scholar, 47Flahault A. et al.A mathematical model for the European spread of influenza.Eur. J. Epidemiol. 1994; 10: 471-474Crossref PubMed Scopus (43) Google Scholar]. The 2009 H1N1 influenza pandemic demonstrated the potential for global air travel networks to rapidly disseminate a novel influenza virus that emerged on a pig farm in Mexico and spread to the rest of the world [48Mena I. et al.Origins of the 2009 H1N1 influenza pandemic in swine in Mexico.eLife. 2016; 5e16777Crossref PubMed Scopus (21) Google Scholar, 49Khan K. et al.Spread of a novel influenza A (H1N1) virus via global airline transportation.N. Engl. J. Med. 2009; 361: 212-214Crossref PubMed Scopus (247) Google Scholar], resulting in approximately 123 000–203 000 deaths, globally [50Simonsen L. et al.Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study.PLoS Med. 2013; 10e1001558Crossref PubMed Scopus (140) Google Scholar]. Human mobility continues to introduce infections to new geographic locations, and air travel contributes to this process. Occasionally, infections introduced to new regions may become endemic. The global emergence of arboviruses, such as dengue, Zika, and Chikungunya viruses, demonstrates how certain infections may become endemic in new regions if they are imported to areas with suitable ecological conditions. These arboviruses require Ae. aegypti or Ae. albopictus mosquito vectors for transmission, and at least one of these species of mosquito is now present on every continent except Antarctica [9Kraemer M.U.G. et al.The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus.eLife. 2015; 4e08347Crossref PubMed Scopus (355) Google Scholar]. Ae. albopictus, the Asian tiger mosquito, is well adapted to urban environments [51Bonizzoni M. et al.The invasive mosquito species Aedes albopictus: current knowledge and future perspectives.Trends Parasitol. 2013; 29: 460-468Abstract Full Text Full Text PDF PubMed Scopus (157) Google Scholar] and has contributed to recent arboviral epidemics. Thes