• 1.

    Cleton NB, Reusken CB, Wagenaar JF, van der Vaart EE, Reimerink J, van der Eijk AA, Koopmans MP, 2015. Syndromic approach to arboviral diagnostics for global travelers as a basis for infectious disease surveillance. PLoS Negl Trop Dis 9: e0004073.

    • Search Google Scholar
    • Export Citation
  • 2.

    Leder K, Torresi J, Libman MD, Cramer JP, Castelli F, Schlagenhauf P, Wilder-Smith A, Wilson ME, Keystone JS, Schwartz E, Barnett ED, von Sonnenburg F, Brownstein JS, Cheng AC, Sotir MJ, Esposito DH, Freedman DO; GeoSentinel Surveillance Network, 2013. GeoSentinel surveillance of illness in returned travelers, 2007–2011. Ann Intern Med 158: 456–468.

    • Search Google Scholar
    • Export Citation
  • 3.

    Musso D, Gubler DJ, 2016. Zika virus. Clin Microbiol Rev 29: 487–524.

  • 4.

    Brathwaite Dick O, San Martin JL, Montoya RH, del Diego J, Zambrano B, Dayan GH, 2012. The history of dengue outbreaks in the Americas. Am J Trop Med Hyg 87: 584–593.

    • Search Google Scholar
    • Export Citation
  • 5.

    Chen LH, Wilson ME, 2012. Dengue and chikungunya in travelers: recent updates. Curr Opin Infect Dis 25: 523–529.

  • 6.

    Staples JE, Breiman RF, Powers AM, 2009. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clin Infect Dis 49: 942–948.

    • Search Google Scholar
    • Export Citation
  • 7.

    Van Bortel W, Dorleans F, Rosine J, Blateau A, Rousset D, Matheus S, Leparc-Goffart I, Flusin O, Prat C, Cesaire R, Najioullah F, Ardillon V, Balleydier E, Carvalho L, Lemaitre A, Noel H, Servas V, Six C, Zurbaran M, Leon L, Guinard A, van den Kerkhof J, Henry M, Fanoy E, Braks M, Reimerink J, Swaan C, Georges R, Brooks L, Freedman J, Sudre B, Zeller H, 2014. Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. Euro Surveill 19: 20759.

    • Search Google Scholar
    • Export Citation
  • 8.

    Khan K, Bogoch I, Brownstein JS, Miniota J, Nicolucci A, Hu W, Nsoesie EO, Cetron M, Creatore MI, German M, Wilder-Smith A, 2014. Assessing the origin of and potential for international spread of chikungunya virus from the Caribbean. PLoS Curr 6.

    • Search Google Scholar
    • Export Citation
  • 9.

    Pan American Health Organization, 2015. Number of Reported Cases of Chikungunya Fever in the Americas, by Country or Territory 2013–2014. Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=7928&Itemid=40931&lang=en. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 10.

    Pan American Health Organization, 2016. Number of Reported Cases of Chikungunya Fever in the Americas, by Country or Territory 2015 (to Epidemiological Week/EW 52). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=7929&Itemid=40931&lang=en. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 11.

    Pan American Health Organization, 2016. Number of Reported Cases of Chikungunya Fever in the Americas, by Country or Territory 2016 (to Epidemiological Week/EW 24). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=8379&Itemid=40931&lang=en. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 12.

    Campos GS, Bandeira AC, Sardi SI, 2015. Zika virus outbreak, Bahia, Brazil. Emerg Infect Dis 21: 1885–1886.

  • 13.

    Cardoso CW, Paploski IA, Kikuti M, Rodrigues MS, Silva MM, Campos GS, Sardi SI, Kitron U, Reis MG, Ribeiro GS, 2015. Outbreak of exanthematous illness associated with Zika, chikungunya, and dengue viruses, Salvador, Brazil. Emerg Infect Dis 21: 2274–2276.

    • Search Google Scholar
    • Export Citation
  • 14.

    Pan American Health Organization, 2016. Zika Epidemiological Update: 23 June 2016. Available at: http://www.paho.org/hq/index.php?option=com_content&view=article&id=11599&ltemid=41691&lang=en. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pan American Health Organization, 2016. Cumulative Zika Suspected and Confirmed Cases Reported by Countries and Territories in the Americas, 2015–2016. Available at: http://ais.paho.org/phip/viz/ed_zika_cases.asp. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 16.

    Centers for Disease Control and Prevention, 2016. Zika Virus Disease in the United States, 2015–2016. Available at: www.cdc.gov/zika/geo/united-states.html. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 17.

    Morens DM, Fauci AS, 2008. Dengue and hemorrhagic fever: a potential threat to public health in the United States. JAMA 299: 214–216.

    • Search Google Scholar
    • Export Citation
  • 18.

    Pan American Health Organization, 2015. Number of Reported Cases of Dengue and Severe Dengue (SD) in the Americas, by Country: Figures for 2014 (to Epidemiological Week/EW 53). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=6290&Itemid=40734. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 19.

    Pan American Health Organization, 2016. Number of Reported Cases of Dengue and Severe Dengue (SD) in the Americas, by Country: Figures for 2015 (to Epidemiological Week/EW 52). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=6290&Itemid=40734. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 20.

    Pan American Health Organization, 2016. Number of Reported Cases of Dengue and Severe Dengue (SD) in the Americas, by Country: Figures for 2016 (to Epidemiological Week/EW 22). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=6290&Itemid=40734. Accessed June 27, 2016.

    • Search Google Scholar
    • Export Citation
  • 21.

    LaRocque RC, Rao SR, Lee J, Ansdell V, Yates JA, Schwartz BS, Knouse M, Cahill J, Hagmann S, Vinetz J, Connor BA, Goad JA, Oladele A, Alvarez S, Stauffer W, Walker P, Kozarsky P, Franco-Paredes C, Dismukes R, Rosen J, Hynes NA, Jacquerioz F, McLellan S, Hale D, Sofarelli T, Schoenfeld D, Marano N, Brunette G, Jentes ES, Yanni E, Sotir MJ, Ryan ET; Global TravEpiNet Consortium, 2012. Global TravEpiNet: a national consortium of clinics providing care to international travelers: analysis of demographic characteristics, travel destinations, and pretravel healthcare of high-risk US international travelers, 2009–2011. Clin Infect Dis 54: 455–462.

    • Search Google Scholar
    • Export Citation
  • 22.

    Harvey K, Esposito DH, Han P, Kozarsky P, Freedman DO, Plier DA, Sotir MJ; Centers for Disease Control and Prevention, 2013. Surveillance for travel-related disease: GeoSentinel Surveillance System, United States, 1997–2011. MMWR Surveill Summ 62: 1–23.

    • Search Google Scholar
    • Export Citation
  • 23.

    Sanchez-Vegas C, Hamer DH, Chen LH, Wilson ME, Benoit C, Hunsperger E, Macleod WB, Jentes ES, Ooi WW, Karchmer AW, Kogelman L, Yanni E, Marano N, Barnett ED, 2013. Prevalence of dengue virus infection in US travelers who have lived in or traveled to dengue-endemic countries. J Travel Med 20: 352–360.

    • Search Google Scholar
    • Export Citation
  • 24.

    Baaten GG, Sonder GJ, Zaaijer HL, van Gool T, Kint JA, van den Hoek A, 2011. Travel-related dengue virus infection, The Netherlands, 2006–2007. Emerg Infect Dis 17: 821–828.

    • Search Google Scholar
    • Export Citation
  • 25.

    Cobelens FG, Groen J, Osterhaus AD, Leentvaar-Kuipers A, Wertheim-van Dillen PM, Kager PA, 2002. Incidence and risk factors of probable dengue virus infection among Dutch travellers to Asia. Trop Med Int Health 7: 331–338.

    • Search Google Scholar
    • Export Citation
  • 26.

    Evans MR, Shickle D, Morgan MZ, 2001. Travel illness in British package holiday tourists: prospective cohort study. J Infect 43: 140–147.

    • Search Google Scholar
    • Export Citation
  • 27.

    Hill DR, 2000. Health problems in a large cohort of Americans traveling to developing countries. J Travel Med 7: 259–266.

  • 28.

    Potasman I, Srugo I, Schwartz E, 1999. Dengue seroconversion among Israeli travelers to tropical countries. Emerg Infect Dis 5: 824–827.

    • Search Google Scholar
    • Export Citation
  • 29.

    Horvath LL, Murray CK, Dooley DP, 2005. Effect of maximizing a travel medicine clinic's prevention strategies. J Travel Med 12: 332–337.

    • Search Google Scholar
    • Export Citation
  • 30.

    Ansari MZ, Shope RE, Malik S, 1993. Evaluation of vero cell lysate antigen for the ELISA of flaviviruses. J Clin Lab Anal 7: 230–237.

    • Search Google Scholar
    • Export Citation
  • 31.

    Russell PK, Nisalak A, Sukhavachana P, Vivona S, 1967. A plaque reduction test for dengue virus neutralizing antibodies. J Immunol 99: 285–290.

    • Search Google Scholar
    • Export Citation
  • 32.

    Simmons M, Myers T, Guevara C, Jungkind D, Williams M, Houng HS, 2016. Development and validation of a quantitative, one-step, multiplex, real-time RT-PCR assay for the detection of dengue and chikungunya viruses. J Clin Microbiol 54: 1766–1773.

    • Search Google Scholar
    • Export Citation
  • 33.

    Schreck CE, Haile DG, Kline DL, 1984. The effectiveness of permethrin and deet, alone or in combination, for protection against Aedes taeniorhynchus. Am J Trop Med Hyg 33: 725–730.

    • Search Google Scholar
    • Export Citation
  • 34.

    Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J; GeoSentinel Surveillance Network, 2006. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43: 1185–1193.

    • Search Google Scholar
    • Export Citation
  • 35.

    LaRocque RC, Deshpande BR, Rao SR, Brunette GW, Sotir MJ, Jentes ES, Ryan ET; Global TravEpiNet Consortium, 2013. Pre-travel health care of immigrants returning home to visit friends and relatives. Am J Trop Med Hyg 88: 376–380.

    • Search Google Scholar
    • Export Citation
  • 36.

    Massad E, Wilder-Smith A, 2009. Risk estimates of dengue in travelers to dengue endemic areas using mathematical models. J Travel Med 16: 191–193.

    • Search Google Scholar
    • Export Citation
  • 37.

    de Laval F, Dia A, Plumet S, Decam C, Leparc Goffart I, Deparis X, 2013. Dengue surveillance in the French armed forces: a dengue sentinel surveillance system in countries without efficient local epidemiological surveillance. J Travel Med 20: 259–261.

    • Search Google Scholar
    • Export Citation
  • 38.

    Chahar HS, Bharaj P, Dar L, Guleria R, Kabra SK, Broor S, 2009. Co-infections with chikungunya virus and dengue virus in Delhi, India. Emerg Infect Dis 15: 1077–1080.

    • Search Google Scholar
    • Export Citation
  • 39.

    Leroy EM, Nkoghe D, Ollomo B, Nze-Nkogue C, Becquart P, Grard G, Pourrut X, Charrel R, Moureau G, Ndjoyi-Mbiguino A, De-Lamballerie X, 2009. Concurrent chikungunya and dengue virus infections during simultaneous outbreaks, Gabon, 2007. Emerg Infect Dis 15: 591–593.

    • Search Google Scholar
    • Export Citation
  • 40.

    Manimunda SP, Sugunan AP, Rai SK, Vijayachari P, Shriram AN, Sharma S, Muruganandam N, Chaitanya IK, Guruprasad DR, Sudeep AB, 2010. Outbreak of chikungunya fever, Dakshina Kannada District, south India, 2008. Am J Trop Med Hyg 83: 751–754.

    • Search Google Scholar
    • Export Citation
  • 41.

    Yoon IK, Alera MT, Lago CB, Tac-An IA, Villa D, Fernandez S, Thaisomboonsuk B, Klungthong C, Levy JW, Velasco JM, Roque VG Jr, Salje H, Macareo LR, Hermann LL, Nisalak A, Srikiatkhachorn A, 2015. High rate of subclinical chikungunya virus infection and association of neutralizing antibody with protection in a prospective cohort in the Philippines. PLoS Negl Trop Dis 9: e0003764.

    • Search Google Scholar
    • Export Citation
  • 42.

    Chastel C, 2012. Eventual role of asymptomatic cases of dengue for the introduction and spread of dengue viruses in non-endemic regions. Front Physiol 3: 70.

    • Search Google Scholar
    • Export Citation
  • 43.

    Chen LH, Wilson ME, 2010. Dengue and chikungunya infections in travelers. Curr Opin Infect Dis 23: 438–444.

  • 44.

    Laras K, Sukri NC, Larasati RP, Bangs MJ, Kosim R, Djauzi Wandra T, Master J, Kosasih H, Hartati S, Beckett C, Sedyaningsih ER, Beecham HJ 3rd, Corwin AL, 2005. Tracking the re-emergence of epidemic chikungunya virus in Indonesia. Trans R Soc Trop Med Hyg 99: 128–141.

    • Search Google Scholar
    • Export Citation
  • 45.

    Kilpatrick AM, Randolph SE, 2012. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380: 1946–1955.

    • Search Google Scholar
    • Export Citation
  • 46.

    Doucoure S, Mouchet F, Cornelie S, DeHecq JS, Rutee AH, Roca Y, Walter A, Herve JP, Misse D, Favier F, Gasque P, Remoue F, 2012. Evaluation of the human IgG antibody response to Aedes albopictus saliva as a new specific biomarker of exposure to vector bites. PLoS Negl Trop Dis 6: e1487.

    • Search Google Scholar
    • Export Citation
  • 47.

    Doucoure S, Drame PM, 2015. Salivary biomarkers in the control of mosquito-borne diseases. Insects 6: 961–976.

  • 48.

    Ridge SE, Vizard AL, 1993. Determination of the optimal cutoff value for a serological assay: an example using the Johne's Absorbed EIA. J Clin Microbiol 31: 1256–1261.

    • Search Google Scholar
    • Export Citation
  • 49.

    Thomas SJ, Nisalak A, Anderson KB, Libraty DH, Kalayanarooj S, Vaughn DW, Putnak R, Gibbons RV, Jarman R, Endy TP, 2009. Dengue plaque reduction neutralization test (PRNT) in primary and secondary dengue virus infections: how alterations in assay conditions impact performance. Am J Trop Med Hyg 81: 825–833.

    • Search Google Scholar
    • Export Citation
  • 50.

    Salje H, Rodriguez-Barraquer I, Rainwater-Lovett K, Nisalak A, Thaisomboonsuk B, Thomas SJ, Fernandez S, Jarman RG, Yoon IK, Cummings DA, 2014. Variability in dengue titer estimates from plaque reduction neutralization tests poses a challenge to epidemiological studies and vaccine development. PLoS Negl Trop Dis 8: e2952.

    • Search Google Scholar
    • Export Citation
  • 51.

    Mardekian SK, Roberts AL, 2015. Diagnostic options and challenges for dengue and chikungunya viruses. BioMed Res Int 2015: 834371.

  • 52.

    Prat CM, Flusin O, Panella A, Tenebray B, Lanciotti R, Leparc-Goffart I, 2014. Evaluation of commercially available serologic diagnostic tests for chikungunya virus. Emerg Infect Dis 20: 2129–2132.

    • Search Google Scholar
    • Export Citation
  • 53.

    Yap G, Pok KY, Lai YL, Hapuarachchi HC, Chow A, Leo YS, Tan LK, Ng LC, 2010. Evaluation of chikungunya diagnostic assays: differences in sensitivity of serology assays in two independent outbreaks. PLoS Negl Trop Dis 4: e753.

    • Search Google Scholar
    • Export Citation
  • 54.

    Kam YW, Pok KY, Eng KE, Tan LK, Kaur S, Lee WW, Leo YS, Ng LC, Ng LF, 2015. Sero-prevalence and cross-reactivity of chikungunya virus specific anti-E2EP3 antibodies in arbovirus-infected patients. PLoS Negl Trop Dis 9: e3445.

    • Search Google Scholar
    • Export Citation
  • 55.

    Timiryasova TM, Bonaparte MI, Luo P, Zedar R, Hu BT, Hildreth SW, 2013. Optimization and validation of a plaque reduction neutralization test for the detection of neutralizing antibodies to four serotypes of dengue virus used in support of dengue vaccine development. Am J Trop Med Hyg 88: 962–970.

    • Search Google Scholar
    • Export Citation
  • 56.

    Rainwater-Lovett K, Rodriguez-Barraquer I, Cummings DA, Lessler J, 2012. Variation in dengue virus plaque reduction neutralization testing: systematic review and pooled analysis. BMC Infect Dis 12: 233.

    • Search Google Scholar
    • Export Citation
  • 57.

    Houghton-Trivino N, Montana D, Castellanos J, 2008. Dengue-yellow fever sera cross-reactivity; challenges for diagnosis. Rev Salud Publica (Bogota) 10: 299–307.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Mosquito Exposure and Chikungunya and Dengue Infection Among Travelers During the Chikungunya Outbreak in the Americas

View More View Less
  • 1 San Antonio Military Medical Center, San Antonio, Texas.
  • 2 Naval Infectious Diseases Diagnostic Laboratory, Silver Spring, Maryland.
  • 3 Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, Maryland.
  • 4 Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, Maryland.
  • 5 Naval Medical Center, Portsmouth, Virginia.
  • 6 Madigan Army Medical Center, Tacoma, Washington.
  • 7 Walter Reed National Military Medical Center, Bethesda, Maryland.
  • 8 Naval Health Research Center, San Diego, California.

Travelers are at risk for arbovirus infection. We prospectively enrolled 267 Department of Defense beneficiaries traveling to chikungunya-outbreak regions in the Americas between December 2013 and May 2015 and assessed travel characteristics and serologic exposure to chikungunya virus (CHIKV) and dengue virus (DENV). Ten ill-returning travelers were also assessed retrospectively. Self-reported mosquito exposure was common (64% of 198 evaluable travelers saw mosquitoes; 53% of 201 reported ≥ 1 bite). Increased exposure was associated with active-duty travelers (odds ratio [OR] = 2.6 [1.3–5.4] for seeing mosquitoes) or travelers visiting friends and relatives (VFR) (OR = 3.5 [1.0–10.0] for high-intensity bite exposure). Arbovirus infection was defined as seroconversion on plaque reduction neutralization testing (PRNT) of pre- and posttravel sera. For ill subjects enrolled posttravel, infection was defined by a positive convalescent PRNT and/or a positive reverse transcription polymerase chain reaction for CHIKV or DENV. We identified seven cases of arbovirus infection: four with CHIKV, five with DENV, and two with both. The composite attack rate for CHIKV and DENV infection was 3.7% of 108 evaluable, immunologically naïve, prospectively assessed travelers; there was serologic and/or polymerase chain reaction evidence of arbovirus infection in three of four evaluable (three of 10 total) ill-returning travelers. We identified both symptomatic and asymptomatic cases. Military purpose of travel and VFR travel accounted for five of seven cases. Pretravel counseling is important and should target higher risk groups. Given a shared vector between CHIKV, DENV, and Zika virus (ZIKV), this study can also help guide counseling for travelers to ZIKV-outbreak regions.

Author Notes

* Address correspondence to David A. Lindholm, Infectious Disease Service, Wright-Patterson Medical Center, 4881 Sugar Maple Dr., Wright-Patterson Air Force Base, OH 45433. E-mail: david.lindholm@us.af.mil

Financial support: The study was supported by the Infectious Disease Clinical Research Program (IDCRP), a Department of Defense (DoD) program executed through the Uniformed Services University of the Health Sciences, the National Institute of Allergy and Infectious Diseases, and National Institutes of Health (NIH), under the Inter-Agency Agreement Y1-AI-5072.

Copyright statement: Some authors are employees of the U.S. Government. This work was prepared as part of their official duties. Title 17 U.S.C. 105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. 101 defines a U.S. Government work as a work prepared by a military service member or employee of the U.S. Government as part of that person's official duties.

Authors' addresses: David A. Lindholm, San Antonio Military Medical Center, San Antonio, TX, E-mail: david.lindholm@us.af.mil. Todd Myers and Susana Widjaja, Naval Infectious Diseases Diagnostic Laboratory, Silver Spring, MD, E-mails: todd.e.myers.mil@mail.mil and susana.widjaja.ctr@mail.mil. Edward M. Grant, Kalyani Telu, and David R. Tribble, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, E-mails: edward.m.grant@gmail.com, ktelu@idcrp.org, and dtribble@idcrp.org. Tahaniyat Lalani, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, and Naval Medical Center, Portsmouth, VA, E-mail: tlalani@idcrp.org. Jamie Fraser, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, and Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, E-mail: jamie.fraser.ctr@usuhs.edu. Mary Fairchok, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, and Madigan Army Medical Center, Tacoma, WA, E-mail: mary.p.fairchok.ctr@mail.mil. Anuradha Ganesan, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, and Walter Reed National Military Medical Center, Bethesda, MD, E-mail: anuradha.ganesan.ctr@mail.mil. Mark D. Johnson, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, and Naval Health Research Center, San Diego, CA, E-mail: mark.d.johnson292.mil@mail.mil. Anjali Kunz, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, and Madigan Army Medical Center, Tacoma, WA, E-mail: anjali.n.kunz.mil@mail.mil. Heather C. Yun, Infectious Disease Clinical Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, and San Antonio Military Medical Center, San Antonio, TX, E-mail: heather.c.yun.mil@mail.mil.

Save