Assessing the Risk of International Spread of Yellow Fever Virus: A Mathematical Analysis of an Urban Outbreak in Asunción, 2008

Michael A. Johansson Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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Neysarí Arana-Vizcarrondo Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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Brad J. Biggerstaff Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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Nancy Gallagher Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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Nina Marano Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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J. Erin Staples Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico; Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, Georgia

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Yellow fever virus (YFV), a mosquito-borne virus endemic to tropical Africa and South America, is capable of causing large urban outbreaks of human disease. With the ease of international travel, urban outbreaks could lead to the rapid spread and subsequent transmission of YFV in distant locations. We designed a stochastic metapopulation model with spatiotemporally explicit transmissibility scenarios to simulate the global spread of YFV from a single urban outbreak by infected airline travelers. In simulations of a 2008 outbreak in Asunción, Paraguay, local outbreaks occurred in 12.8% of simulations and international spread in 2.0%. Using simple probabilistic models, we found that local incidence, travel rates, and basic transmission parameters are sufficient to assess the probability of introduction and autochthonous transmission events. These models could be used to assess the risk of YFV spread during an urban outbreak and identify locations at risk for YFV introduction and subsequent autochthonous transmission.

Author Notes

*Address correspondence to Michael A. Johansson, Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, 1324 Calle Cañada, San Juan, Puerto Rico 00920. E-mail: mjohansson@cdc.gov

Authors’ addresses: Michael A. Johansson and Neysarí Arana-Vizcarrondo, Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, Puerto Rico, E-mails: mjohansson@cdc.gov and nnarana@gmail.com. Brad J. Biggerstaff and J. Erin Staples, Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, E-mails: bbiggerstaff@cdc.gov and estaples@cdc.gov. Nancy Gallagher and Nina Marano, Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: ngallagher@cdc.gov and nmarano@cdc.gov.

  • 1.

    Vainio J, Cutts F, 1998. Yellow Fever. Geneva, Switzerland: World Health Organization.

  • 2.

    Pan American Health Organization, 2008. Outbreak of yellow fever in Paraguay. Epidemiol Bull 27: 2.

  • 3.

    Soper FL, 1963. The elimination of urban yellow fever in the Americas through the eradication of Aedes aegypti. Am J Public Health Nations Health 53: 716.

  • 4.

    Robertson SE, Hull BP, Tomori O, Bele O, LeDuc JW, Esteves K, 1996. Yellow fever: a decade of reemergence. JAMA 276: 11571162.

  • 5.

    Gubler DJ, 1989. Aedes aegypti and Aedes aegypti-borne disease control in the 1990s: top down or bottom up. Charles Franklin Craig Lecture. Am J Trop Med Hyg 40: 571578.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Heintze C, Velasco Garrido M, Kroeger A, 2007. What do community-based dengue control programmes achieve? A systematic review of published evaluations. Trans R Soc Trop Med Hyg 101: 317325.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Nathan N, Barry M, Van Herp M, Zeller H, 2001. Shortage of vaccines during a yellow fever outbreak in Guinea. Lancet 358: 21292130.

  • 8.

    2008. Yellow fever preparedness. Lancet 371: 786.

  • 9.

    Roukens AH, Visser LG, 2008. Yellow fever vaccine: past, present and future. Expert Opin Biol Ther 8: 17871795.

  • 10.

    Lindsey NP, Schroeder BA, Miller ER, Braun MM, Hinckley AF, Marano N, Slade BA, Barnett ED, Brunette GW, Horan K, Staples JE, Kozarsky PE, Hayes EB, 2008. Adverse event reports following yellow fever vaccination. Vaccine 26: 60776082.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Whittembury A, Ramirez G, Hernandez H, Ropero AM, Waterman S, Ticona M, Brinton M, Uchuya J, Gershman M, Toledo W, Staples E, Campos C, Martinez M, Chang GJ, Cabezas C, Lanciotti R, Zaki S, Montgomery JM, Monath T, Hayes E, 2009. Viscerotropic disease following yellow fever vaccination in Peru. Vaccine 27: 59745981.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Staples JE, Gershman M, Fischer M, 2010. Yellow fever vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 59: 127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Codeco CT, Luz PM, Struchiner CJ, 2004. Risk assessment of yellow fever urbanization in Rio de Janeiro, Brazil. Trans R Soc Trop Med Hyg 98: 702710.

  • 14.

    Johansson MA, Arana-Vizcarrondo N, Biggerstaff BJ, Staples JE, Gallagher N, Marano N, 2011. On the treatment of airline travelers in mathematical models. PLoS One 6: e22151.

  • 15.

    New M, Lister D, Hulme M, Makin I, 2002. A high-resolution data set of surface climate over global land areas. Clim Res 21: 125.

  • 16.

    Christophers SR, 1960. Aedes aegypti (L.): The Yellow Fever Mosquito. Cambridge, United Kingdom: The University Press.

  • 17.

    World Health Organization Department of Immunization Vaccines and Biologicals, 2009. Vaccine Preventable Diseases: Monitoring System. Available at: http://www.who.int/immunization_monitoring/en/globalsummary/timeseries/tsincidenceyfe.htm. Accessed November 4, 2009.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Johansson MA, Arana-Vizcarrondo N, Biggerstaff BJ, Staples JE, 2010. Incubation periods of yellow fever virus. Am J Trop Med Hyg 83: 183188.

  • 19.

    Focks DA, Haile DG, Daniels E, Mount GA, 1993. Dynamic life table model for Aedes aegypti (Diptera: Culicidae): analysis of the literature and model development. J Med Entomol 30: 10031017.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Getz WM, Lloyd-Smith JO, 2006. Basic methods for modeling the invasion and spread of contagious disease. Feng Z, Dieckmann U, Levin SA, eds. Disease Evolution: Models, Concepts, and Data Analysis. Providence, RI: American Mathematical Society, 87109.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Koopman JS, Prevots DR, Vaca Marin MA, Gomez Dantes H, Zarate Aquino ML, Longini IM Jr, Sepulveda Amor J, 1991. Determinants and predictors of dengue infection in Mexico. Am J Epidemiol 133: 11681178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Marques CA, Forattini OP, Massad E, 1994. The basic reproduction number for dengue fever in Sao Paulo State, Brazil—1990–1991 epidemic. Trans R Soc Trop Med Hyg 88: 5859.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Ferguson NM, Donnelly CA, Anderson RM, 1999. Transmission dynamics and epidemiology of dengue: insights from age-stratified sero-prevalence surveys. Philos Trans R Soc Lond B Biol Sci 354: 757768.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Massad E, Burattini MN, Coutinho FA, Lopez LF, 2003. Dengue and the risk of urban yellow fever reintroduction in Sao Paulo State, Brazil. Rev Saude Publica 37: 477484.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Favier C, Degallier N, Rosa-Freitas MG, Boulanger JP, Costa Lima JR, Luitgards-Moura JF, Menkes CE, Mondet B, Oliveira C, Weimann ET, Tsouris P, 2006. Early determination of the reproductive number for vector-borne diseases: the case of dengue in Brazil. Trop Med Int Health 11: 332340.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Chowell G, Diaz-Duenas P, Miller JC, Alcazar-Velazco A, Hyman JM, Fenimore PW, Castillo-Chavez C, 2007. Estimation of the reproduction number of dengue fever from spatial epidemic data. Math Biosci 208: 571589.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Nagao Y, Koelle K, 2008. Decreases in dengue transmission may act to increase the incidence of dengue hemorrhagic fever. Proc Natl Acad Sci USA 105: 22382243.

  • 28.

    Rogers DJ, Wilson AJ, Hay SI, Graham AJ, 2006. The global distribution of yellow fever and dengue. Adv Parasitol 62: 181220.

  • 29.

    Monath TP, Nasidi A, 1993. Should yellow fever vaccine be included in the expanded program of immunization in Africa? A cost-effectiveness analysis for Nigeria. Am J Trop Med Hyg 48: 274299.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Massad E, Coutinho FA, Burattini MN, Lopez LF, 2001. The risk of yellow fever in a dengue-infested area. Trans R Soc Trop Med Hyg 95: 370374.

  • 31.

    Tabachnick WJ, Wallis GP, Aitken TH, Miller BR, Amato GD, Lorenz L, Powell JR, Beaty BJ, 1985. Oral infection of Aedes aegypti with yellow fever virus: geographic variation and genetic considerations. Am J Trop Med Hyg 34: 12191224.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Mitchell CJ, Miller BR, Gubler DJ, 1987. Vector competence of Aedes albopictus from Houston, Texas, for dengue serotypes 1 to 4, yellow fever and Ross River viruses. J Am Mosq Control Assoc 3: 460465.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Lourenco de Oliveira R, Vazeille M, de Filippis AMB, Failloux AB, 2002. Oral susceptibility to yellow fever virus of Aedes aegypti from Brazil. Mem Inst Oswaldo Cruz 97: 437439.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Johnson BW, Chambers TV, Crabtree MB, Filippis AM, Vilarinhos PT, Resende MC, Macoris Mde L, Miller BR, 2002. Vector competence of Brazilian Aedes aegypti and Ae. albopictus for a Brazilian yellow fever virus isolate. Trans R Soc Trop Med Hyg 96: 611613.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Massad E, Coutinho FA, Burattini MN, Lopez LF, Struchiner CJ, 2005. Yellow fever vaccination: how much is enough? Vaccine 23: 39083914.

  • 36.

    Codeco CT, Luz PM, Coelho F, Galvani AP, Struchiner C, 2007. Vaccinating in disease-free regions: a vaccine model with application to yellow fever. J R Soc Interface 4: 11191125.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Benedict MQ, Levine RS, Hawley WA, Lounibos LP, 2007. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 7: 7685.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Miller BR, Monath TP, Tabachnick WJ, Ezike VI, 1989. Epidemic yellow fever caused by an incompetent mosquito vector. Trop Med Parasitol 40: 396399.

  • 39.

    Lourenco de Oliveira R, Vazeille M, de Filippis AM, Failloux AB, 2003. Large genetic differentiation and low variation in vector competence for dengue and yellow fever viruses of Aedes albopictus from Brazil, the United States, and the Cayman Islands. Am J Trop Med Hyg 69: 105114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Morrison AC, Gray K, Getis A, Astete H, Sihuincha M, Focks D, Watts D, Stancil JD, Olson JG, Blair P, Scott TW, 2004. Temporal and geographic patterns of Aedes aegypti (Diptera: Culicidae) production in Iquitos, Peru. J Med Entomol 41: 11231142.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Mammen MP, Pimgate C, Koenraadt CJ, Rothman AL, Aldstadt J, Nisalak A, Jarman RG, Jones JW, Srikiatkhachorn A, Ypil-Butac CA, Getis A, Thammapalo S, Morrison AC, Libraty DH, Green S, Scott TW, 2008. Spatial and temporal clustering of dengue virus transmission in Thai villages. PLoS Med 5: e205.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Honorio NA, Nogueira RMR, Codeco CT, Carvalho MS, Cruz OG, Magalhaes MDFM, de Araujo JMG, de Araujo ESM, Gomes MQ, Pinheiro LS, Pinel CD, Lourenco-de-Oliveira R, 2009. Spatial evaluation and modeling of dengue seroprevalence and vector density in Rio de Janeiro, Brazil. PLoS Negl Trop Dis 3: e545.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Vazquez-Prokopec GM, Kitron U, Montgomery B, Horne P, Ritchie SA, 2010. Quantifying the spatial dimension of dengue virus epidemic spread within a tropical urban environment. PLoS Negl Trop Dis 4: e920.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Ackers ML, Puhr ND, Tauxe RV, Mintz ED, 2000. Laboratory-based surveillance of Salmonella serotype Typhi infections in the United States: antimicrobial resistance on the rise. JAMA 283: 26682673.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Steinberg EB, Bishop R, Haber P, Dempsey AF, Hoekstra RM, Nelson JM, Ackers M, Calugar A, Mintz ED, 2004. Typhoid fever in travelers: who should be targeted for prevention? Clin Infect Dis 39: 186191.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J, 2006. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43: 11851193.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Skarbinski J, James EM, Causer LM, Barber AM, Mali S, Nguyen-Dinh P, Roberts JM, Parise ME, Slutsker L, Newman RD, 2006. Malaria surveillance—United States, 2004. MMWR Morb Mortal Wkly Rep 55: 2337.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Fenner L, Weber R, Steffen R, Schlagenhauf P, 2007. Imported infectious disease and purpose of travel, Switzerland. Emerg Infect Dis 13: 217222.

  • 49.

    US Department of Commerce International Trade Administration, 2009. Profile of US Resident Travelers Visiting Overseas Destinations: 2008 Outbound. Washington, DC: Manufacturing and Services, Office of Travel and Tourism Industries.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Theiler M, Anderson CR, 1975. The relative resistance of dengue-immune monkeys to yellow fever virus. Am J Trop Med Hyg 24: 115117.

  • 51.

    Monath TP, 1989. The absence of yellow fever in Asia: hypotheses. A cause for concern? Virus Inf Exch Newsl South East Asia West Pac 6: 106107.

  • 52.

    Focks DA, Brenner RJ, Hayes J, Daniels E, 2000. Transmission thresholds for dengue in terms of Aedes aegypti pupae per person with discussion of their utility in source reduction efforts. Am J Trop Med Hyg 62: 1118.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Pant CP, Yasuno M, 1973. Field studies on the gonotrophic cycle of Aedes aegypti in Bangkok, Thailand. J Med Entomol 10: 219223.

  • 54.

    Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Edman JD, 2000. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol 37: 89101.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Hindle E, 1930. The transmission of yellow fever. Lancet 219: 835842.

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