jueves, 19 de marzo de 2015

Animal-Associated Exposure to Rabies Virus among Travelers, 1997–2012 - Volume 21, Number 4—April 2015 - Emerging Infectious Disease journal - CDC


Animal-Associated Exposure to Rabies Virus among Travelers, 1997–2012 - Volume 21, Number 4—April 2015 - Emerging Infectious Disease journal - CDC

Volume 21, Number 4—April 2015


Animal-Associated Exposure to Rabies Virus among Travelers, 1997–2012

Philippe GautretComments to Author , Kira Harvey, Prativa Pandey, Poh Lian Lim, Karin Leder, Watcharapong Piyaphanee, Marc Shaw, Susan C. McDonald, Eli Schwartz, Douglas H. Esposito, Philippe Parola, and for the GeoSentinel Surveillance Network
Author affiliations: Aix Marseille Université, Marseille, France (P. Gautret, P. Parola)Institut Hospitalo-Universitaire Méditerranée Infection, Marseille (P. Gautret, P. Parola)Centers for Disease Control and Prevention, Atlanta, Georgia, USA (K. Harvey, D.H. Esposito)CIWEC Clinic Travel Medicine Center, Kathmandu, Nepal (P. Pandey)Tan Tock Seng Hospital, Singapore (P.L. Lim)Lee Kong Chian School of Medicine, Singapore (P.L. Lim)Monash University, Melbourne, Victoria, Australia (K. Leder)The Royal Melbourne Hospital, Parkville, Victoria, Australia (K. Leder)Mahidol University, Bangkok, Thailand (W. Piyaphanee)Travellers Health and Vaccination Centre, Auckland, New Zealand (M. Shaw)University Hospital of Northern British Columbia, Prince George, British Columbia, Canada (S.C. McDonald)Tel Hashomer and Sackler School of Medicine, Tel Aviv, Israel (E. Schwartz)


Among travelers, rabies cases are rare, but animal bites are relatively common. To determine which travelers are at highest risk for rabies, we studied 2,697 travelers receiving care for animal-related exposures and requiring rabies postexposure prophylaxis at GeoSentinel clinics during 1997–2012. No specific demographic characteristics differentiated these travelers from other travelers seeking medical care, making it challenging to identify travelers who might benefit from reinforced pretravel rabies prevention counseling. Median travel duration was short for these travelers: 15 days for those seeking care after completion of travel and 20 days for those seeking care during travel. This finding contradicts the view that preexposure rabies vaccine recommendations should be partly based on longer travel durations. Over half of exposures occurred in Thailand, Indonesia, Nepal, China, and India. International travelers to rabies-endemic regions, particularly Asia, should be informed about potential rabies exposure and benefits of pretravel vaccination, regardless of demographics or length of stay.
Rabies causes ≈60,000 human deaths annually and is a public health concern in most countries in Asia and Africa (1). By contrast, it is rare among travelers; an average of 3.7 cases were documented each year during 2004–2012 (2). Nevertheless, bites to travelers by potentially rabid animals are relatively frequent; estimated incidence is 0.4% per month of stay, according to a meta-analysis of ≈1,270,000 travelers (3). By inference, expensive postexposure prophylaxis (PEP), which includes administration of rabies vaccine and rabies immunoglobulin, is probably provided to large numbers of travelers annually. Given the severity of rabies virus infection and the high costs associated with caring for large numbers of potentially exposed travelers, rabies pretravel preventive measures need to be reinforced. These measures include systematic pretravel counseling about animal bite avoidance, postexposure wound care and prophylaxis, and preexposure rabies vaccination for some travelers.
Generalizability of data regarding the epidemiology of travel-associated animal-related rabies virus exposures are limited because they come from studies that are small or single center or that focus on travelers returning from specific destinations. As such, travelers at highest risk for rabies cannot be reliably identified on the basis of available data (3,4). The decision as to which travelers should receive predeparture rabies vaccination is complex because of the combination of limited data defining rabies risk among travelers, the high cost of rabies vaccine and rabies immunoglobulin in some countries, and the occasionally limited rabies vaccine and rabies immunoglobulin availability because of production problems.
One way to assess the epidemiology of travel-associated illness in travelers and immigrants involves use of GeoSentinel, a global sentinel surveillance network established in 1995 through a collaborative effort from the International Society for Travel Medicine and the US Centers for Disease Control and Prevention (CDC) (5). We used the GeoSentinel database to assess geographic and demographic factors for a large number of patients who sought care at GeoSentinel sites for animal-related exposure (e.g., bite, scratch, lick on broken skin or mucous membrane) and required rabies PEP.

Dr. Gautret is a physician, parasitologist, and director of the Rabies Treatment Centre and of the Travel Clinic at Marseille University Hospital. He coordinates the Epidemic Intelligence and Response program for EuroTravNet. His professional interests include zoonoses, tropical and travel medicine, Hajj medicine, and medical parasitology.


Additional members of the GeoSentinel Surveillance Network who contributed data are (listed in descending order of amount contributed): Holly Murphy, CIWEC Clinic Travel Medicine Center, Kathmandu, Nepal; Annelies Wilder-Smith, Tan Tock Seng Hospital, Singapore; Jean Delmont, Hôpital Nord, Marseille, France; Joseph Torresi and Graham Brown, Royal Melbourne Hospital, Melbourne, Australia; Yukihiro Yoshimura, Natsuo Tachikawa, Hanako Kurai, and Hiroko Sagara, Yokohama Municipal Citizen's Hospital, Yokohama, Japan; Frank von Sonnenburg; University of Munich, Munich, Germany; Shuzo Kanagawa, Yasuyuki Kato, and Yasutaka Mizunno, International Medical Center of Japan, Tokyo, Japan; Annemarie Hern, Worldwise Travellers Health and Vaccination Centre, Auckland, New Zealand; François Chappuis and Louis Loutan, University of Geneva, Geneva, Switzerland; Jay S. Keystone and Kevin Kain, University of Toronto, Toronto, Ontario, Canada; Martin Grobusch, Peter de Vries, and Kartini Gadroen, University of Amsterdam, Amsterdam, the Netherlands; Johan Using, Gabrielle Fröberg, Helena Hervius Askling and Ulf Bronner, Karolinska University Hospital, Stockholm, Sweden; Michael D. Libman, Brian Ward, and J. Dick Maclean, McGill University, Montreal, Quebec, Canada; Christophe Rapp and Olivier Aoun, Hôpital d'Instruction des Armées Bégin, Saint Mandé, France; Luis M. Valdez and Hugo Siu, Clínica Anglo Americana, Lima, Peru; JaKob Cramer and Gerd-Dieter Burchard, Bernhard-Nocht-Institute for Tropical Medicine, Hamburg, Germany; Phi Truong Hoang Phu, Nicole Anderson, Trish Batchelor, and Dominique Meisch, International SOS Clinic, Ho Chi Minh City, Vietnam; Mogens Jensenius, Oslo University Hospital, Oslo, Norway; David G. Lalloo and Nicholas J. Beeching, Liverpool School of Tropical Medicine, Liverpool, UK; William Stauffer and Patricia Walker, University of Minnesota, St. Paul, Minnesota, USA; Kass, Robert, Travellers Medical and Vaccination Centres of Australia, Adelaide, Australia (Dec 1997–Mar 2001 only); N. Jean Haulman, David Roesel, and Elaine C. Jong, University of Washington and Harborview Medical Center, Seattle, Washington, USA; Andy Wang and Jane Eason, Beijing United Family Hospital and Clinics, Beijing, Peoples Republic of China; Brian Kendall, DeVon C. Hale, Rahul Anand, and Stephanie S. Gelman, University of Utah, Salt Lake City, Utah, USA; Lin H. Chen and Mary E. Wilson, Mount Auburn Hospital, Harvard University, Cambridge, Massachusetts, USA; Udomsak Silachamroon, Mahidol University, Bangkok, Thailand; Sarah Borwein, TravelSafe Medical Centre, Hong Kong Special Administrative Region, China; Perry J. van Genderen, Havenziekenhuis en Instituut voor Tropische Ziekten, Rotterdam, the Netherlands; Jean Vincelette, Centre Hospitalier de l’Université de Montréal, Montreal,; Alejandra Gurtman, Mount Sinai Medical Center, New York City, New York, USA (Oct 2002–Aug 2005 only); Phyllis E. Kozarsky, Henry Wu, Jessica Fairley, and Carlos Franco-Paredes, Emory University, Atlanta, Georgia, USA; Patricia Schlagenhauf, Rainer Weber, and Robert Steffen, University of Zürich, Zurich, Switzerland; Johnnie Yates, Vernon Ansdell, Kaiser Permanente, Honolulu, Hawaii, USA (Oct 1997–Jan 2003 only); Marc Mendelson and Peter Vincent, University of Cape Town and Tokai Medicross Travel Clinic, Cape Town, South Africa; Frank Mockenhaupt and Gunder Harms, Berlin, Germany; Cecilia Perret and Francisca Valdivieso, Pontificia Universidad Católica de Chile, Santiago, Chile; Patrick Doyle and Wayne Ghesquiere, Vancouver General Hospital and Vancouver Island Health Authority, Vancouver and Victoria, British Columbia, Canada; John D. Cahill and George McKinley, St. Luke’s-Roosevelt Hospital Center, New York; Anne McCarthy, University of Ottawa, Ottawa, Ontario, Canada; Eric Caumes and Alice Pérignon, Hôpital Pitié-Salpêtrière, Paris, France; Susan Anderson, Palo Alto Medical Foundation, Palo Alto, California, USA; Noreen A. Hynes, R. Bradley Sack, and Robin McKenzie, Johns Hopkins University, Baltimore, Maryland, USA; Vanessa Field, InterHealth, London, UK; Bradley A. Connor, Cornell University, New York, New York, USA; Robert Muller, Travel Clinic Services, Johannesburg, South Africa (May 2004–Jun 2005 only); David O. Freedman, University of Alabama at Birmingham, Birmingham, Alabama, USA; Stefan Hagmann and Andy O. Miller, Bronx-Lebanon Hospital Center, Bronx, New York, USA; Effrossyni Gkrania-Klotsas, Addenbrooke's Hospital, Cambridge, UK; Shiri Tenenboim, Klinik Kominote IsraAid Community Health Clinic, Léogâne, Haiti (only); Nancy Piper Jenks and Christine Kerr, Hudson River Health Care, Peekskill, New York, USA; Carmelo Licitra and Antonio Crespo, Orlando Regional Health Center, Orlando, Florida, USA; Francesco Castelli and Giampiero Carosi, University of Brescia, Brescia, Italy; Paul Holtom, Jeff Goad, and Anne Anglim, University of Southern California, Los Angeles, California, USA (Apr 2007–Dec 2009 only).
This work was supported by CDC (cooperative agreement U50 CK000189).


  1. World Health OrganizationWHO Expert Consultation on Rabies. Second report. World Health Organ Tech Rep Ser2013;982:1139 .PubMed
  2. Carrara PParola PBrouqui PGautret PImported human rabies cases worldwide, 1990–2012. PLoS Negl Trop Dis2013;7:e2209.DOIPubMed
  3. Gautret PParola PRabies vaccination for international travelers. Vaccine2012;30:12633DOIPubMed
  4. Gautret PParola PRabies pretravel vaccination. Curr Opin Infect Dis2012;25:5006DOIPubMed
  5. Freedman DOKozarsky PEWeld LHCetron MSGeoSentinel: the global emerging infections sentinel network of the International Society of Travel Medicine. J Travel Med1999;6:948 . DOIPubMed
  6. Harvey KEsposito DHHan PKozarsky PFreedman DOPlier DA, et al. Surveillance for travel-related disease—GeoSentinel Surveillance System, United States, 1997–2011. MMWR Surveill Summ. 2013;62:1–23.
  7. Tamashiro HMatibag GCDitangco RAKanda KOhbayashi YRevisiting rabies in Japan: is there cause for alarm? Travel Med Infect Dis.2007;5:26375DOIPubMed
  8. Tobiume MSato YKatano HNakajima NTanaka KNoguchi A, et al. Rabies virus dissemination in neural tissues of autopsy cases due to rabies imported into Japan from the Philippines: immunohistochemistry. Pathol Int. 2009;59:555–6.
  9. Rabies—Canada (ON). human, ex Dominican Republic. ProMed. 2012 Apr 17. http://www.promedmail.org, archive no. 20120417.1104531 [cited 2014 May 29].
  10. Wilcox MEPoutanen SMKrajden SAgrid RKiehl TRTang-Wai DFA case of rabies encephalitis: new dog, old tricks. Neurology2014;82:1101.DOIPubMed
  11. Rabies—China: (ex India) human, exposure unknown. ProMED mail. 2012 Sep 21 [cited 2014 May 29]. http://www.promedmail.org, archive no. 20120921.1304335.
  12. World Tourism Organization. UNWTO tourism highlights: 2013 edition [cited 2014 Mar 14]. http://mkt.unwto.org/publication/unwto-tourism-highlights-2013-edition
  13. Piyaphanee WKittitrakul CLawpoolsri SGautret PKashino WTangkanakul W, et al. Risk of potentially rabid animal exposure among foreign travelers in Southeast Asia. PLoS Negl Trop Dis 2012;6:e1852. PMID: 23029598DOI
  14. Gautret PSchwartz EShaw MSoula GGazin PDelmont J, et al. Animal-associated injuries and related diseases among returned travellers: a review of the GeoSentinel Surveillance Network. Vaccine. 2007;25:2656–63.
  15. Leder KTorresi JLibman MDCramer JPCastelli FSchlagenhauf P, et al. GeoSentinel surveillance of illness in returned travelers, 2007–2011. Ann Intern Med. 2013;158:456–68.
  16. Rupprecht CEShlim SD. Infectious diseases related to travel—rabies. In: CDC health information for international travel 2014 [cited 2014 May 29].http://wwwnc.cdc.gov/travel/yellowbook/2014/chapter-3-infectious-diseases-related-to-travel/rabies
  17. Tenzin, Ward MP. Review of rabies epidemiology and control in South, South East and East Asia: past, present and prospects for elimination.Zoonoses Public Health2012;59:45167DOIPubMed
  18. Guo ZTao XYin CHan NYu JLi H, et al. National borders effectively halt the spread of rabies: the current rabies epidemic in China is dislocated from cases in neighboring countries. PLoS Negl Trop Dis. 2013;7:e2039.
  19. Song MTang QWang DMMo ZJGuo SHLi H, et al. Epidemiological investigations of human rabies in China. BMC Infect Dis.2009;9:210.
  20. Putra AAHampson KGirardi JHiby EKnobel DMardiana IW, et al. Response to a rabies epidemic, Bali, Indonesia, 2008–2011. Emerg Infect Dis. 2013;19:648–51.
  21. Susilawathi NMDarwinata AEDwija IBBudayanti NSWirasandhi GASubrata K, et al. Epidemiological and clinical features of human rabies cases in Bali 2008–2010. BMC Infect Dis. 2012;12:81.
  22. National Health and Family Planning Commission. Chinese notifiable disease surveillance monthly report [cited 2014 May 29].http://www.microsofttranslator.com/bv.aspx?from=zh-CHS&to=en&a=http%3A%2F%2Fwww.chinacdc.cn%2Ftjsj%2Ffdcrbbg%2F
  23. Ministry of Public Health T. Annual epidemiological surveillance report 2012 [in Thai] [cited 2014 May 29].http://www.boe.moph.go.th/Annual/AESR2012/main/AESR55_Part1/file4/2055_Rabies.pdf
  24. Suraweera WMorris SKKumar RWarrell DAWarrell MJJha P Deaths from symptomatically identifiable furious rabies in India: a nationally representative mortality survey. PLoS Negl Trop Dis. 2012;6(10):e1847. PMCID: PMC3464588DOI
  25. Guo DZhou HZou YYin WYu HSi Y, et al. Geographical analysis of the distribution and spread of human rabies in China from 2005 to 2011. PLoS ONE. 2013;8:e72352.
  26. Pandey PShlim DRCave WSpringer MFRisk of possible exposure to rabies among tourists and foreign residents in Nepal. J Travel Med.2002;9:12731DOIPubMed
  27. Wang CZhang XSong QTang KPromising rabies vaccine for postexposure prophylaxis in developing countries, a purified Vero cell vaccine produced in China. Clin Vaccine Immunol2010;17:68890DOIPubMed
  28. Si HGuo ZMHao YTLiu YGZhang DMRao SQ, et al. Rabies trend in China (1990–2007) and post-exposure prophylaxis in the Guangdong province. BMC Infect Dis. 2008;8:113.
  29. Kositprapa CWimalratna OChomchey PChareonwai SBenjavongkulchai MKhawplod P, et al. Problems with rabies postexposure management: a survey of 499 public hospitals in Thailand. J Travel Med. 1998;5:30–2.
  30. Gautret PLim PLShaw MLeder KRabies post-exposure prophylaxis in travellers returning from Bali, Indonesia, November 2008 to March 2010.Clin Microbiol Infect2011;17:4457DOIPubMed
  31. Environmental hazards in Nepal: altitude illness, environmental exposures, injuries, and bites in travelers and expatriates. J Travel Med.2007;14:3618 Boggild AK and Costiniuk C and Kain KC and Pandey PDOIPubMed
  32. Borwein ST. China. In: CDC health information for international travel 2014 [cited 2014 May 29].http://wwwnc.cdc.gov/travel/yellowbook/2014/chapter-4-select-destinations/china
  33. Mills DJLau CLWeinstein PAnimal bites and rabies exposure in Australian travellers. Med J Aust2011;195:6735DOIPubMed
  34. Carroll HJMcCall BJChristiansen JC. Surveillance of potential rabies exposure in Australian travellers returning to South East Queensland. Commun Dis Intell Q Rep. 2012;36:E186–7.
  35. Shaw MTO’Brien BLeggat PARabies postexposure management of travelers presenting to travel health clinics in Auckland and Hamilton, New Zealand. J Travel Med2009;16:137DOIPubMed
  36. Wijaya LFord LLalloo DRabies postexposure prophylaxis in a UK travel clinic: ten years’ experience. J Travel Med2011;18:25761.DOIPubMed
  37. Warrell MJCurrent rabies vaccines and prophylaxis schedules: preventing rabies before and after exposure. Travel Med Infect Dis2012;10:115.DOIPubMed
  38. Gautret PBlanton JDacheux LRibadeau-Dumas FBrouqui PParola P, et al. Rabies in nonhuman primates and potential for transmission to humans: a literature review and examination of selected French national data. PLoS Negl Trop Dis. 2014;8:e2863.
  39. Leder KChen LHWilson MEAggregate travel vs. single trip assessment: arguments for cumulative risk analysis. Vaccine2012;30:26004.DOIPubMed
  40. Wieten RWLeenstra Tvan Thiel PPvan Vugt MStijnis CGoorhuis A, et al. Rabies vaccinations: are abbreviated intradermal schedules the future? Clin Infect Dis. 2013;56:414–9.



Technical Appendix

Suggested citation for this article: Gautret P, Harvey K, Pandey P, Lim PL, Leder K, Piyaphanee W, et al. Animal-associated exposure to rabies virus among travelers, 1997–2012. Emerg Infect Dis. 2015 Apr [date cited]. http://dx.doi.org/10.3201/eid2104.141479
DOI: 10.3201/eid2104.141479
1Additional members of the GeoSentinel Surveillance Network who contributed data are listed at the end of this article.

No hay comentarios:

Publicar un comentario