, Volume 5, Issue 3, pp 371–378

Perceived Vaccination Status in Ecotourists and Risks of Anthropozoonoses

  • Michael P. Muehlenbein
  • Leigh Ann Martinez
  • Andrea A. Lemke
  • Laurentius Ambu
  • Senthilvel Nathan
  • Sylvia Alsisto
  • Patrick Andau
  • Rosman Sakong
Original Contributions


Anthropozoonotic (human to nonhuman animal) transmission of infectious disease poses a significant threat to wildlife. A large proportion of travelers to tropical regions are not protected against vaccine-preventable illnesses, and a majority of these travelers demonstrate poor recall of actual vaccination status. Here we characterize self-perceived vaccination status among a large sample of ecotourists at the Sepilok Orangutan Rehabilitation Centre, Sabah, Malaysia. Despite their recognized travel itinerary to view endangered animals, tourists at wildlife sanctuaries are not adequately protected against vaccine-preventable illnesses. Of 633 surveys, over half reported being currently vaccinated against tuberculosis, hepatitis A, hepatitis B, polio, and measles. Fewer participants reported current vaccination status for influenza, rabies, and chickenpox. Despite the fact that the majority of visitors to Sepilok are from temperate regions where influenza is relatively more prevalent, 67.1% of those surveyed with medical-related occupations reported not being currently vaccinated for influenza. Ecotourists concerned about environmental protection are themselves largely unaware of their potential contribution to the spread of diseases to animals. The risks of negatively affecting animal populations must be communicated to all concerned parties, and this may begin by urging travelers to examine their actual vaccination status, particularly as the ecotourism industry continues its rapid expansion, and is seen increasingly as a possible tool to save great ape populations from extinction.


orangutan macaque Sepilok immunization zoonoses tourism zoonotic infection anthropozoonotic infection 


  1. Adams HR, Sleeman JM, Rwego I, New JC (2001) Self-reported medical history survey of humans as a measure of health risk to the chimpanzees (Pan troglodytes schweinfurthii) of Kibale National Park, Uganda. Oryx 35:308–312CrossRefGoogle Scholar
  2. Advisory Committee on Immunization Practices (2008) Recommended adult immunization schedule—United States, October 2007—September 2008. Morbidity and Mortality Weekly Report 56:Q1–Q4Google Scholar
  3. Ambu L (2007) Strategy of the Sabah Wildlife Department for wildlife conservation in Sabah. First International Conservation Conference in Sabah: the Quest for Gold Standards, Kota Kinabalu. Malaysia: Sabah Wildlife DepartmentGoogle Scholar
  4. Brack M (1987) Agents Transmissible from Simians to Man. Berlin: Springer-VerlagGoogle Scholar
  5. Byers AC, Hastings B (1991) Mountain gorilla mortality and climatic factors in the Parc National des Volcans, Ruhengeri Prefecture, Rwanda, 1988. Mountain Research and Development 2:145–151CrossRefGoogle Scholar
  6. Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 356:991–999CrossRefGoogle Scholar
  7. Crockett M, Keystone J (2005) “I hate needles” and other factors impacting on travel vaccine uptake. Journal of Travel Medicine 12:S41–S46Google Scholar
  8. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449CrossRefGoogle Scholar
  9. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78:103–116CrossRefGoogle Scholar
  10. Daszak P, Tabor GM, Kilpatrick AM, Epstein J, Plowright R (2004) Conservation medicine and a new agenda for emerging diseases. Annals of the New York Academy of Sciences 1026:1–11CrossRefGoogle Scholar
  11. Falvo C, Win PT, Horowitz HW (1996) Assessment of an adult population’s knowledge regarding vaccine-preventable diseases. Journal of Travel Medicine 3:103–106CrossRefGoogle Scholar
  12. Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA (2007) Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation 135:511–517CrossRefGoogle Scholar
  13. Graczyk TK, Nizeyi JB, da Silva AJ, Moura INS, Pieniazek NJ, Cranfield MR, et al. (2002a) A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitology Research 88:926–931CrossRefGoogle Scholar
  14. Graczyk TK, Nizeyi JB, Ssebide B, Thompson RCA, Read C, Cranfield MR (2002b) Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology 88:905–909CrossRefGoogle Scholar
  15. Hamer DH, Connor BA (2004) Travel health knowledge, attitudes and practices among United States travelers. Journal of Travel Medicine 11:23–26Google Scholar
  16. Hilton E, Singer C, Kozarsky P, Smith M, Lardis MP, Borenstein MT (1991) Status of immunity to tetanus, measles, mumps, rubella, and polio among US travelers. Annals of Intern Medicine 115:32–33Google Scholar
  17. Homsy J (1999) Ape tourism and human diseases: how close should we get? International Gorilla Conservation Programme Regional Meeting, RwandaGoogle Scholar
  18. Hosaka K (1995) Epidemics and wild chimpanzee study groups. Pan African News 2:1–4Google Scholar
  19. Jong EC (1998) Immunizations for international travel. Infectious Disease Clinics of North America 12:249–266CrossRefGoogle Scholar
  20. Kaiser J (2006) A one-size-fits-all flu vaccine? Science 312:380–382CrossRefGoogle Scholar
  21. Keystone JS, Kozarsky PE, Freedman DO, Nothdurft HD, Connor BA (editors) (2004) Travel Medicine, 2nd ed., St. Louis: Elsevier ScienceGoogle Scholar
  22. Kilbourn AM, Karesh WB, Wolfe ND, Bosi EJ, Cook RA, Andau M (2003) Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases 39:73–83Google Scholar
  23. Kollaritsch H, Wiedermann G (1992) Compliance of Austrian tourists with prophylactic measures. European Journal of Epidemiology 8:243–251CrossRefGoogle Scholar
  24. Köndgen S, Kühl, N’Goran PK, Walsh PD, Schenk S, Ernst N, et al. (2008) Pandemic human viruses cause decline of endangered great apes. Current Biology 18:1–5CrossRefGoogle Scholar
  25. Kortlandt A (1996) An epidemic of limb paresis (polio?) among the chimpanzee population at Beni (Zaire) in 1964, possibly transmitted by humans. Pan Africa News 3:9–10Google Scholar
  26. Lopez-Velez R, Bayas JM (2007) Spanish travelers to high-risk areas in the tropics: airport survey of travel health knowledge, attitudes, and practices in vaccination and malaria prevention. Journal of Travel Medicine 14:297–305CrossRefGoogle Scholar
  27. Mak JW, Cheong WH, Yen PK, Lim PK, Chan WC (1982) Studies on the epidemiology of subperiodic Brugia malayi in Malaysia: problems in its control. Acta Tropica 39:237–245Google Scholar
  28. McIntosh BM (1970) Antibody against Chikungunya virus in wild primates in southern Africa. South African Journal of Medical Science 35:65–74Google Scholar
  29. Monath TP (2001) Yellow fever: an update. The Lancet Infectious Diseases 1:11–20CrossRefGoogle Scholar
  30. Nizeyi JB, Sebunya D, da Silva AJ, Cranfield MR, Pieniazek NJ, Graczyk TK (2002) Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda. American Journal of Tropical Medicine and Hygiene 66:442–444Google Scholar
  31. Prazuck T, Semaille C, Defayolle M, Bargain P, Clerel M, Lafaix C, et al. (1998) Immunization status of French and European tropical travelers: study of 9,156 subjects departing from Paris to 12 tropical destinations. Revue Epidemiologie et de Sante Publique 46:64–72Google Scholar
  32. Schunk M, Wachinger W, Nothdurft HD (2001) Vaccination status and prophylactic measures of travelers from Germany to subtropical and tropical areas: results of an airport survey. Journal of Travel Medicine 8:260–262Google Scholar
  33. Steffen R, Connor BA (2005) Vaccines in travel health: from risk assessment to priorities. Journal of Travel Medicine 12:26–35Google Scholar
  34. Tacken M, Braspenning J, Spreeuwenberg P, van den Hoogen H, van Essen G, de Bakker D, et al. (2002) Patient characteristics determine differences in the influenza vaccination rate more so than practice features. Preventive Medicine 35:401–406CrossRefGoogle Scholar
  35. Toovey S, Jamieson A, Holloway M (2004) Travelers’ knowledge, attitudes and practices on the prevention of infectious diseases: results from a study at Johannesburg International Airport. Journal of Travel Medicine 11:16–22Google Scholar
  36. Van Herck K, Castelli F, Zuckerman J, Nothdurft H, Van Damme P, Dahlgren AL, et al. (2004) Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. Journal of Travel Medicine 11:3–8Google Scholar
  37. Van Herck K, Zuckerman J, Castelli F, Van Damme P, Walker E, Steffen R (2003) Travelers’ knowledge, attitudes, and practices on prevention of infectious diseases: results from a pilot study. Journal of Travel Medicine 10:75–78Google Scholar
  38. Wallis J, Lee DR (1999) Primate conservation: the prevention of disease transmission. International Journal of Primatology 20:803–826CrossRefGoogle Scholar
  39. Wilder-Smith A, Nor SK, Jae-Hoon S, Ching-Yu C, Torresi J (2004) Travel health knowledge, attitudes and practices among Australasian travelers. Journal of Travel Medicine 11:9–15Google Scholar
  40. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, et al. (2001) Sylvatic transmission of arboviruses among Bornean orangutans. American Journal of Tropical Medicine and Hygiene 64:310–316Google Scholar
  41. Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36:153–160CrossRefGoogle Scholar
  42. Woolhouse M, Gaunt E (2007) Ecological origins of novel human pathogens. Critical Reviews in Microbiology 33:1–12CrossRefGoogle Scholar
  43. Zuckerman JN, Steffen R (2000) Risks of Hepatitis B in travelers as compared to immunization status. Journal of Travel Medicine 7:170–174Google Scholar

Copyright information

© International Association for Ecology and Health 2008

Authors and Affiliations

  • Michael P. Muehlenbein
    • 1
    • 2
  • Leigh Ann Martinez
    • 1
  • Andrea A. Lemke
    • 3
  • Laurentius Ambu
    • 2
  • Senthilvel Nathan
    • 2
  • Sylvia Alsisto
    • 2
  • Patrick Andau
    • 2
  • Rosman Sakong
    • 4
  1. 1.Department of AnthropologyIndiana University–BloomingtonBloomingtonUSA
  2. 2.Sabah Wildlife DepartmentKota KinabaluMalaysia
  3. 3.Department of AnthropologyUniversity of Wisconsin–MilwaukeeMilwaukeeUSA
  4. 4.Red Ape EncountersSukauMalaysia

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