Unhealthy travelers present challenges to sustainable primate ecotourism

Travel Medicine and Infectious Disease

Volumn 8, Issue 3, 2010, Pages 169-175

  Muehlenbein, Michael P ^a,b   Martinez, Leigh Ann ^a   Lemke, Andrea A ^c   Ambu, Laurentius ^b   Nathan, Senthilvel ^b   Alsisto, Sylvia ^b   Sakong, Rosman ^d  

^a INDIANA UNIVERSITY   (United States)

^b SABAH WILDLIFE DEPARTMENT   (Malaysia)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d Red Ape Encounters   (Malaysia)

Author keywords

Anthropozoonoses; Primate; Sepilok; Tourism; Zoonoses

Indexed keywords

ADULT; AGED; ANIMAL HEALTH; ARTICLE; COUGHING; DIARRHEA; DOMESTIC ANIMAL; ECOTOURISM; EXPOSURE; FEMALE; FEVER; HEALTH CARE PERSONNEL; HEALTH HAZARD; HUMAN; INFECTION; LIVESTOCK; MAJOR CLINICAL STUDY; MALAYSIA; MALE; NOSE CONGESTION; OCCUPATION; PRIMATE; PRIORITY JOURNAL; REHABILITATION CENTER; SELF REPORT; SORE THROAT; STRUCTURED QUESTIONNAIRE; TOURISM; TRAVEL; VOMITING; WILD ANIMAL; WILDLIFE; ADOLESCENT; ANIMAL; ANIMAL DISEASE; DISEASE TRANSMISSION; MIDDLE AGED; ORANG UTAN; QUESTIONNAIRE; RISK ASSESSMENT; STATISTICAL MODEL; ZOONOSIS;

ADOLESCENT; ADULT; AGED; ANIMALS; ANIMALS, WILD; DISEASE TRANSMISSION, INFECTIOUS; FEMALE; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; PONGO; QUESTIONNAIRES; RISK ASSESSMENT; TRAVEL; ZOONOSES;

EID: 77957288353     PISSN: 14778939     EISSN: 18730442     Source Type: Journal    
DOI: 10.1016/j.tmaid.2010.03.004     Document Type: Article

References (68)

1. Filion FL, Foley JP, Jacqemot AJ. The economics of global ecotourism. In: Munasinghe M,McNealyJ, editors. Protected area economics and policy: linking conservation and sustainable development. Washington,DC:TheWorld Bank; 1994.p.235-52.
2. Munasinghe M, McNealy J, editors. Protected area economics and policy: linking conservation and sustainable development. Washington, DC: The World Bank; 1994.
3. Mowforth M, Munt I. Tourism and sustainability: development and new tourism in the third world. London: Routledge; 2003.
4. Schoene CUR, Brend SA. Primate sanctuaries e a delicate conservation approach. South African Journal Wildlife Research 2002;32:109-13. (Pubitemid 35372010)
5. Bruner AG, Gullison RE, Rice RE, da Fonseca GAB. Effectiveness of parks in protecting tropical biodiversity. Science 2001;291: 125-8. (Pubitemid 32063075)
6. Jaffe E. Good gone wild: sometimes, ecotourism hurts what it sets out to help. Science 2006;170:218-20.
7. Berman CM, Jinhua L, Ogawa H, Ionica C, Yin H. Primate tourism, range restriction, and infant risk among Macaca thi-betana at Mt. Huangshan, China. International Journal of Primatology 2007;28:1123-41. (Pubitemid 350132206)
8. Walker BG, Dee Boersma P, Wingfield JC. Habituation of adult magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conservation Biology 2006;20:146-54.
9. Romero LM, Wikelski M. Exposure to tourism reduces stress-induced corticosterone levels in Galápagos marine iguanas. Biological Conservation 2002;108:371-4. (Pubitemid 35002839)
10. Romero LM. Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution 2004;19: 249-55. (Pubitemid 38503481)
11. Sapolsky RM, Romero LM, Minck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 2000; 21:55-89. (Pubitemid 32266068)
12. Muehlenbein MP. The application of endocrine measures in primate parasite ecology. In: Huffman M, Chapman C, editors. Primate parasite ecology: the dynamics of host-parasite relationships. New York: Cambridge University Press; 2009. p. 63-81.
13. Muyambi F. The impact of tourism on the behaviour of mountain gorillas. Gorilla Journal 2005;30:14-5.
14. Brack M. Agents transmissible from simians to man. Berlin: Springer-Verlag; 1987.
15. Reinquist DM, Whitney RA. Zoonoses acquired from pet primates. Veterinary Clinics of North America-Small Animal Practice 1987;17:219-40.
16. Woodford MH, Butynski TM, Karesh WB. Habituating the great apes: the disease risks. Oryx 2002;36:153-60. (Pubitemid 43138392)
17. Köndgen S, Kühl H, N'Goran PK, Walsh PD, Schenk S, Ernst N, et al. Pandemic human viruses cause decline of endangered great apes. Current Biology 2008;18:1-5.
18. Graczyk TK, Nizeyi JB, Ssebide B, Thompson RCA, Read C, Cranfield MR. Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology 2002;88: 905-9. (Pubitemid 35278735)
19. Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA. Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation 2007;135: 511-7.
20. Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology 2008;22:1600-7.
21. Rolland RM, Hausfater G, Marshall B, Levy SB. Antibiotic-resistant bacteria in wild primates: increased prevalence in baboons feeding on human refuse. Applied Environmental Microbiology 1985;49:791-4. (Pubitemid 15091173)
22. Ashford RW, Reid GDF, Butynski TM. The intestinal faunas of man and mountain gorillas in a shared habitat. Annals of Tropical Medicine and Parasitology 1990;84:337-40. (Pubitemid 20290520)
23. Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GRNN, Graczyk TK. Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. Journal of Wildlife Diseases 2001;37:239-44. (Pubitemid 33610008)
24. Graczyk TK, Nizeyi JB, da Silva AJ, Moura INS, Pieniazek NJ, Cranfield MR, et al. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitology Research 2002;88:926-31. (Pubitemid 35025143)
25. Mountain Gorilla Veterinary Project 2002 Employee Health Group. Risk of disease transmission between conservation personnel and the mountain gorillas: results from an employee health program in Rwanda. EcoHealth 2004;1:351-61.
26. Goodall J. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Harvard University Press; 1986.
27. Kortlandt A. An epidemic of limb paresis (polio?) among the chimpanzee population at Beni (Zaire) in 1964, possibly transmitted by humans. Pan Africa News 1996;3:9-10.
28. Byers AC, Hastings B. Mountain gorilla mortality and climatic factors in the Parc National des Volcans, Ruhengeri Prefecture, Rwanda, 1988. Mountain Research and Development 1991;2: 145-51.
29. Hosaka K. Epidemics and wild chimpanzee study groups. Pan Africa News 1995;2:1-4.
30. Wallis J, Lee DR. Primate conservation: the prevention of disease transmission. International Journal of Primatology 1999;20:803-26. (Pubitemid 30031290)
31. Macfie L. Case report on scabies infection in Bwindi gorillas. Gorilla Journal 1996;13:19-20.
32. Mueller-Graf CDM, Collins DA, Packer C, Woolhouse MEJ. Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 1997;115:621-7. (Pubitemid 28078658)
33. Van Herck K, Castelli F, Zuckerman J, Nothdurft H, Van Damme P, Dahlgren AL, et al. Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. Journal of Travel Medicine 2004;11:3-8. (Pubitemid 38198768)
34. Van Herck K, Zuckerman J, Castelli F, Van Damme P, Walker E, Steffen R. Traveler's knowledge, attitudes, and practices on prevention of infectious diseases: results from a pilot study. Journal of Travel Medicine 2003;10:75-8. (Pubitemid 36383936)
35. Wilder-Smith A, Khairullah NS, Song JH, Chen CY, Torresi J. Travel health knowledge, attitudes and practices among Australasian travelers. Journal of Travel Medicine 2004;11:9-15. (Pubitemid 38198769)
36. Steffen R, Tornieporth N, Costa Clemens SA, Chatterjee S, Cavalcanti AM, Collard F, et al. Epidemiology of travelers' diarrhea: details of a global survey. Journal of Travel Medicine 2004;11:231-8. (Pubitemid 39062177)
37. Toovey S, Jamieson A, Holloway M. Travelers' knowledge, attitudes and practices on the prevention of infectious diseases: results from a study at Johannesburg International Airport. Journal of Travel Medicine 2004;11:16-22. (Pubitemid 38198770)
38. Hilton E, Singer C, Kozarsky P, Smith M, Lardis MP, Borenstein MT. Status of immunity to tetanus, measles, mumps, rubella, and polio among US travelers. Annals of Internal Medicine 1991;115:32-3.
39. Rack J, Wichmann O, Kamara B, Gunther M, Cramer J, Schonfeld C, et al. Risk and spectrum of diseases in travelers to popular tourist destinations. Journal of Travel Medicine 2005; 12:248-53. (Pubitemid 43074385)
40. Muehlenbein MP, Martinez LA, Lemke AA, Ambu L, Nathan S, Andau P, et al. Perceived vaccination status in ecotourists and risks of anthropozoonoses. EcoHealth 2008;5:371-8.
41. Adams HR, Sleeman JM, Rwego I, New JC. 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 2001;35:308-12. (Pubitemid 33055872)
42. Mawdsley JL, Bardgett RD, Merry RJ, Pain BF, Theodorou MK. Pathogens in livestock waste, their potential movement through soil and environmental pollution. Applied Soil Ecology 1995;2:1-15.
43. Cleaveland S, Laurenson MK, Taylor LH. 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 2001;356:991-9. (Pubitemid 32696244)
44. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, et al. Sylvatic transmission of arboviruses among Bornean orangutans. American Journal of Tropical Medicine and Hygiene 2001;64:310-6.
45. Kilbourn AM, Karesh WB, Wolfe ND, Bosi EJ, Cook RA, Andau M. Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases 2003;39:73-83. (Pubitemid 38836251)
46. Wolfe ND, Karesh WB, Kilbourn AM, Cox-Singh J, Bosi EJ, Rahman HA, et al. The impact of ecological conditions on the prevalence of malaria among orangutans. Vector-Borne and Zoonotic Diseases 2002;2:97-103.
47. Woolhouse M, Gaunt E. Ecological origins of novel human pathogens. Critical Reviews in Microbiology 2007;33:1-12.
48. Mak JW, Cheong WH, Yen PK, Lim PK, Chan WC. Studies on the epidemiology of subperiodic Brugia malayi in Malaysia: problems in its control. Acta Tropica 1982;39:237-45. (Pubitemid 12002224)
49. McIntosh BM. Antibody against Chikungunya virus in wild primates in Southern Africa. South African Journal of Medical Sciences 1970;35:65-74.
50. Monath TP. Yellow fever: an update. Lancet Infectious Diseases 2001;1:11-20. (Pubitemid 33586036)
51. Nizeyi JB, Sebunya D, Dasilva AJ, Cranfield MR, Pieniazek NJ, Graczyk TK. Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda. American Journal of Tropical Medicine and Hygiene 2002;66:442-4. (Pubitemid 34810502)
52. Singh B, Kim Sing L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, et al. A large focus of naturally acquired Plas-modium knowlesi infections in human beings. Lancet 2004; 363:1017-24. (Pubitemid 38410774)
53. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999;397:436-41.
54. Wolfe ND, Henien W, Carr JK, Garcia AD, Shanmugam V, Tamoufe U, et al. Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proceedings of the National Academy of Sciences USA 2005;102:7994-9. (Pubitemid 40781051)
55. Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, et al. Naturally acquired simian retrovirus infections in central African hunters. Lancet 2004;363:932-7. (Pubitemid 38388326)
56. Jones-Engel L, Engel GA, Schillaci MA, Rompis A, Putra A, Suaryana KG, et al. Primate-to-human retroviral transmission in Asia. Emerging Infectious Diseases 2005;11:1028-35. (Pubitemid 40880901)
57. Engel GA, Jones-Engel L, Schillaci MA, Suaryana KG, Putra A, Fuentes A, et al. Human exposure to herpesvirus B-seropositive macaques, Bali, Indonesia. Emerging Infectious Diseases 2002; 8:789-95.
58. Ostrowski SR, Leslie MJ, Parrott T, Abelt S, Piercy PE. B-virus from pet macaque monkeys: an emerging threat in the United States? Emerging Infectious Diseases 1998;4:117-21. (Pubitemid 28347425)
59. Homsey J. Ape tourism and human diseases: how close should we get? Report for the International Gorilla Conservation Programme Regional Meeting. Rwanda; 1999.
60. Jane Goodall Institute. Chimpanzee ecotourism health protocol manual. Entebbe: Uganda: Jane Goodall Institute; 2006.
61. Leendertz FH. Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biological Conservation 2006;131: 325-37. (Pubitemid 43849648)
62. Muehlenbein MP, Ancrenaz M. Minimizing pathogen transmission at primate ecotourism destinations: the need for input from travel medicine. Journal of Travel Medicine 2009;16: 229-32.
63. Ceballos-Lascurán H. Tourism, ecotourism, and protected areas: the state of nature-based tourism around the world and guidelines for its development. Gland, Switzerland: World Conservation Union; 1996.
64. Eagles PFJ, McCool SF, Haynes CD. Sustainable tourism in protected areas: guidelines for planning and management. Gland, Switzerland: World Conservation Union; 2002.
65. Ecotourism Society. Ecotourism guidelines for nature tour operators. North Bennington, Vermont: The Ecotourism Society; 1993.
66. World Tourism Organization. World ecotourism summit e final report. Madrid, Spain: World Tourism Organization and the United Nations Economic Programme; 2002.
67. Horvath LL, Murray CK, DuPont HL. Travel health information at commercial travel websites. Journal of Travel Medicine 2003;10:272-9. (Pubitemid 37280028)
68. Sandbrook C, Semple S. The rules and reality of mountain gorilla Gorilla beringei beringei tracking: how close do tourists get? Oryx 2006;40:428-33. (Pubitemid 46058438)