Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon
详细信息    查看全文
  • 作者:Pascal Drakulovski (1) (3)
    Sébastien Bertout (2)
    Sabrina Locatelli (1)
    Christelle Butel (1)
    Sébastien Pion (1)
    Eitel Mpoudi-Ngole (2)
    Eric Delaporte (1)
    Martine Peeters (1)
    Michèle Mallié (1)
  • 关键词:Chimpanzees ; Parasites ; Coprology ; SIV ; Helminths ; Protozoa
  • 刊名:Parasitology Research
  • 出版年:2014
  • 出版时间:July 2014
  • 年:2014
  • 卷:113
  • 期:7
  • 页码:2541-2550
  • 全文大小:
  • 参考文献:1. Boorom KF, Smith H, Nimri L, Viscogliosi E, Spanakos G, Parkar U, Li LH, Zhou XN, Ok UZ, Leelayoova S, Jones MS (2008) Oh my aching gut: irritable bowel syndrome, / Blastocystis, and asymptomatic infection. Parasit Vectors 1:40 CrossRef
    2. Cegielski JP, Msengi AE, Dukes CS, Mbise R, Redding-Lallinger R, Minjas JN, Wilson ML, Shao J, Durack DT (1993) Intestinal parasites and HIV infection in Tanzanian children with chronic diarrhea. AIDS 7:213-21 CrossRef
    3. Cerme?o JR, Hernández De Cuesta I, Uzcátegui O, Páez J, Rivera M, Baliachi N (2003) / Balantidium coli in an HIV-infected patient with chronic diarrhoea. AIDS 17:941-42 CrossRef
    4. Chi F, Leider M, Leendertz F, Bergmann C, Boesch C, Schenk S, Pauli G, Ellerbrok H, Hakenbeck R (2007) New Streptococcus pneumoniae clones in deceased wild chimpanzees. J Bacteriol 189:6085-088 CrossRef
    5. Clyti E, Aznar C, Couppie P, el Guedj M, Carme B, Pradinaud R (1998) A case of coinfection by / Balantidium coli and HIV in French Guiana]. [Article in French. Bull Soc Pathol Exot 91:309-11
    6. Drakulovski P, Locatelli S, Butel C, Pion S, Krasteva D, Mougdi-Pole E, Delaporte E, Peeters M, Mallié M (2013) Use of RNAlater as a preservation method for parasitic coprology studies in wild-living chimpanzees. Exp Parasitol 135:257-61 CrossRef
    7. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, Rousset D, Nana A, Djoko CF, Tamoufe U, Aghokeng AF, Mpoudi-Ngole E, Delaporte E, Peeters M, Wolfe ND, Ayouba A (2011) Characterization of a new simian immunodeficiency virus strain in a naturally infected / Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 8:4
    8. Evans AC, Markus MB, Joubert JJ, Gunders AE (1991) Bushman children infected with the nematode Strongyloides fülleborni. S Afr Med J 80:410-11
    9. Formenty P, Boesch C, Wyers M, Steiner C, Donati F, Dind F, Walker F, Le Guenno B (1999) Ebola virus outbreak among wild chimpanzees living in a rain forest of C?te d’Ivoire. J Infect Dis 179:120-26 CrossRef
    10. Gillespie TR, Greiner EC, Chapman CA (2004) Gastrointestinal parasites of the guenons of western Uganda. J Parasitol 90:1356-360 CrossRef
    11. Gillespie TR, Morgan D, Deutsch JC, Kuhlenschmidt MS, Salzer JS, Cameron K, Reed T, Sanz C (2009) A legacy of low-impact logging does not elevate prevalence of potentially pathogenic protozoa in free-ranging gorillas and chimpanzees in the Republic of Congo: logging and parasitism in African apes. Ecohealth 6:557-64 CrossRef
    12. Gillespie TR, Lonsdorf EV, Canfield EP, Meyer DJ, Nadler Y, Raphael J, Pusey AE, Pond J, Pauley J, Mlengeya T, Travis DA (2010) Demographic and ecological effects on patterns of parasitism in eastern chimpanzees ( / Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Am J Phys Anthropol 143:534-44 CrossRef
    13. Goldberg TL, Gillespie TR, Rwego IB, Estoff EL, Chapman CA (2008) Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerg Infect Dis 14:1375-382 CrossRef
    14. Gonzalez-Moreno O, Hernandez-Aguilar RA, Piel AK, Stewart FA, Gracenea M, Moore J (2013) Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla, Western Tanzania. Parasitol Res 1:393-99 CrossRef
    15. Guttierez Y (2000) In Diagnostic pathology of parasitic infections with clinical correlations, Oxford University Press p 287-342
    16. Hira PR, Patel BG (1977) / Strongyloides fülleborni infections in man in Zambia. Am J Trop Med Hyg 4:640-43
    17. Hira PR, Patel BG (1980) Human strongyloidiasis due to the primate species / Strongyloides fülleborni. Trop Geogr Med 1:23-9
    18. Hirsch VM (2004) What can natural infection of African monkeys with simian immunodeficiency virus tell us about the pathogenesis of AIDS? AIDS Rev 1:40-3
    19. Howells ME, Pruetz J, Gillespie TR (2011) Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: the case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli, Senegal. Am J Primatol 73:173-79 CrossRef
    20. Hussein EM, Hussein AM, Eida MM, Atwa MM (2008) Pathophysiological variability of different genotypes of human Blastocystis hominis Egyptian isolates in experimentally infected rats. Parasitol Res 102:853-60 CrossRef
    21. Idris NS, Dwipoerwantoro PG, Kurniawan A, Said M (2010) Intestinal parasitic infections of immunocompromised children with diarrhoea: clinical profile and therapeutic response. J Infect Dev Ctries 5:309-17
    22. Karp CL, Auwaerter PG (2007) Coinfection with HIV and tropical infectious diseases. I. Protozoal pathogens. Clin Infect Dis 45:1208-213 CrossRef
    23. Kaur T, Singh J, Tong S, Humphrey C, Clevenger D, Tan W, Szekely B, Wang Y, Li Y, Alex Muse E, Kiyono M, Hanamura S, Inoue E, Nakamura M, Huffman MA, Jiang B, Nishida T (2008) Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees ( / Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am J Primatol 70:755-65 CrossRef
    24. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F, Loul S, Ngole EM, Bienvenue Y, Delaporte E, Brookfield JF, Sharp PM, Shaw GM, Peeters M, Hahn BH (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523-26 CrossRef
    25. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley TM, Schumacher-Stankey J, Wroblewski E, Mosser A, Raphael J, Kamenya S, Lonsdorf EV, Travis DA, Mlengeya T, Kinsel MJ, Else JG, Silvestri G, Goodall J, Sharp PM, Shaw GM, Pusey AE, Hahn BH (2009) Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460:515-19 CrossRef
    26. Kim JC, Abee CR, Wolf RH (1978) Balantidiosis in a chimpanzee ( / Pan troglodytes). Lab Anim 4:231-33 CrossRef
    27. Krief S, Bories C, Hladik CM (2003) [Results of fecal parasitologic examination performed on a population of wild chimpanzees (Pan troglodytes schweinfurthii) in Uganda ] [Article in French]. Bull Soc Pathol Exot 96:80-2
    28. Krief S, Huffman MA, Sevenet T, Guillot J, Bories C, Hladik CM, Wrangham RW (2005) Noninvasive monitoring of the health of / Pan troglodytes schweinfurthii in the Kibale National Park, Uganda. Int J Primatol 26:467-90 CrossRef
    29. Krief S, Jamart A, Mahé S, Leendertz FH, M?tz-Rensing K, Crespeau F, Bain O, Guillot J (2008) Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? J Med Primatol 4:188-95 CrossRef
    30. Labes EM, Hegglin D, Grimm F, Nurcahyo W, Harrison ME, Bastian ML, Deplazes P (2010) Intestinal parasites of endangered orangutans ( / Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia. Parasitology 137:123-35 CrossRef
    31. Lankester F, M?tz-Rensing K, Kiyang J, Jensen SA, Weiss S, Leendertz FH (2008) Fatal ulcerative colitis in a western lowland gorilla (Gorilla gorilla gorilla). J Med Primatol 6:297-02
    32. Lee RV, Prowten AW, Anthone S, Satchidanand SK, Fisher JE, Anthone R (1990) Typhlitis due to / Balantidium coli in captive lowland gorillas. Rev Infect Dis 12:1052-059 CrossRef
    33. Leendertz FH, Lankester F, Guislain P, Néel C, Drori O, Dupain J, Speede S, Reed P, Wolfe N, Loul S, Mpoudi-Ngole E, Peeters M, Boesch C, Pauli G, Ellerbrok H, Leroy EM (2006) Anthrax in Western and Central African great apes. Am J Primatol 68:928-33 CrossRef
    34. Legesse M, Erko B (2004) Zoonotic intestinal parasites in / Papio anubis (baboon) and / Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Trop 90:231-36 CrossRef
    35. Levecke B, Dorny P, Geurden T, Vercammen F, Vercruysse J (2007) Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium. Vet Parasitol 148:236-46 CrossRef
    36. Lilly AA, Mehlman PT, Doran D (2002) Intestinal Parasites in Gorillas, Chimpanzees, and Humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int J Primatol 23:555-73 CrossRef
    37. Locatelli S, Butel C, Esteban A, Drakulovski P, Krasteva D, Mpoudi Ngole E, Mallié M, Delaporte E, Peeters M (2012) Long-term monitoring of opportunistic diseases in SIV infected non-habituated apes from Cameroon: a pilot study. Communication. XXIV Congress of the international Primatological Society, August 12-17, Mexico
    38. Masi S, Chauffour S, Bain O, Todd A, Guillot J, Krief S (2012) Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS ONE 7(12):e49805. doi:10.1371/journal.pone.0049805. Epub 2012 Dec 5 CrossRef
    39. Mbaya AW, Udendeye UJ (2011) Gastrointestinal parasites of captive and free-roaming primates at the Afi Mountain Primate Conservation Area in Calabar, Nigeria and their zoonotic implications. Pak J Biol Sci 14:709-14 CrossRef
    40. Miller MJ, Bray RS (1966) Entamoeba histolytica infections in the Chimpanzee (Pan satyricus). J Parasitol 52:386-88 CrossRef
    41. Modry D, Petrzelková KJ, Pomajbíková K, Tokiwa T, Krízek J, Imai S, Vallo P, Profousová I, Slapeta J (2009) The occurrence and ape-to-ape transmission of the entodiniomorphid ciliate / Troglodytella abrassarti in captive gorillas. J Eukaryot Microbiol 1:83-7 CrossRef
    42. Morgan D, Whitworth J, Eotu H, Omoding N, Moore M (1996) Gastrointestinal parasite infections. Lancet 348:965-66 CrossRef
    43. Mortelmans J, Vercruysse J, Kageruka P (1971) Three pathogenic intestinal protozoa of anthropoid apes:Entamoeba histolytica, Balantidium coli and Troglodytella abrassarti In: Proceeding of the Third International Congress of Primatology. Zürich. p 187-91
    44. Muehlenbein MP (2005) Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol 65:167-79 CrossRef
    45. Nakauchi K (1999) The prevalence of / Balantidium coli infection in fifty-six mammalian species. J Vet Med Sci 61:63-5 CrossRef
    46. Pandrea I, Apetrei C (2010) Where the wild things are: pathogenesis of SIV infection in African nonhuman primate hosts. Curr HIV AIDS Rep 7:28-6 CrossRef
    47. Pandrea I, Sodora DL, Silvestri G, Apetrei C (2008) Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol 29:419-28 CrossRef
    48. Parija SC, Jeremiah S (2013) Blastocystis: taxonomy, biology and virulence. Trop Parasitol 3:17-5 CrossRef
    49. Petrá?ová J, Modry D, Huffman MA, Mapua MI, Bobáková L, Mazoch V, Singh J, Kaur T, Petr?elková KJ (2010) Gastrointestinal parasites of indigenous and introduced primate species of Rubondo Island National Park, Tanzania. Int J Primatol 31:920-36 CrossRef
    50. Petrá?ová J, Uzlíková M, Kostka M, Petr?elková KJ, Huffman MA, Modry D (2011) Diversity and host specificity of / Blastocystis in syntopic primates on Rubondo Island, Tanzania. Int J Parasitol 41:1113-120 CrossRef
    51. Petrzelková KJ, Hasegawa H, Appleton CC, Huffman MA, Archer CE, Moscovice LR, Mapua MI, Singh J, Kaur T (2010) Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. Am J Primatol 72:307-16
    52. Petr?elková KJ, Schovancová K, Profousová I, Ki?idayová S, Váradyová Z, Pekár S, Kamler J, Modry D (2012) The effect of low- and high-fiber diets on the population of entodiniomorphid ciliates Troglodytella abrassarti in captive chimpanzees (Pan troglodytes). Am J Primatol 74:669-75 CrossRef
    53. Poirier P, Wawrzyniak I, Vivarès CP, Delbac F, El Alaoui H (2012) New insights into / Blastocystis spp.: a potential link with irritable bowel syndrome. PLoS Pathog.8(3):e1002545. doi: 10.1371/journal.ppat.1002545 . Epub 2012 Mar 15
    54. Pomajbíková K, Petrzelková KJ, Profousová I, Petrásová J, Kisidayová S, Varádyová Z, Modry D (2010a) A survey of entodiniomorphid ciliates in chimpanzees and bonobos. Am J Phys Anthropol 142:42-8
    55. Pomajbíková K, Petr?elková KJ, Profousová I, Petrá?ová J, Modry D (2010b) Discrepancies in the occurrence of / Balantidium coli between wild and captive African great apes. J Parasitol 96:1139-344 CrossRef
    56. Profousová I, Mihaliková K, Laho T, Váradyová Z, Petr?elková KJ, Modry D, Ki?idayová S (2011) The ciliate, / Troglodytella abrassarti, contributes to polysaccharide hydrolytic activities in the chimpanzee colon. Folia Microbiol (Praha) 56:339-43 CrossRef
    57. Qadri SM, al-Okaili GA, al-Dayel F (1989) Clinical significance of / Blastocystis hominis. J Clin Microbiol 27:2407-409
    58. Rijpstra AC (1967) Sporocysts of / Isospora sp. in a chimpanzee / (Pan troglodytes, L.). Proc K Ned Akad Wet C 70:395-01
    59. Rothman JM, Bowman DD, Kalema-Zikusoka G, Nkurunungi JB (2006) The parasites of the gorillas in Bwindi Impenetrable National Park Uganda. In: Newton-Fisher NE, Notman H, Paterson JD, Vernon R (eds) Primates of Western Uganda. Springer, New York, pp 171-93 CrossRef
    60. Rothman JM, Pell AN, Bowman DD (2008) Host-parasite ecology of the helminths in mountain gorillas. J Parasitol 94:834-40 CrossRef
    61. Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol 22:1600-607 CrossRef
    62. Sak B, Kvác M, Petrzelková K, Kvetonová D, Pomajbíková K, Mulama M, Kiyang J, Modry D (2011) Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission? Folia Parasitol (Praha) 58:81-6 CrossRef
    63. Schuster FL, Ramirez-Avila L (2008) Current world status of / Balantidium coli. Clin Microbiol Rev 21:626-38 CrossRef
    64. Silvestri G, Paiardini M, Pandrea I, Lederman MM, Sodora DL (2007) Understanding the benign nature of SIV infection in natural hosts. J Clin Invest 117:3148-154 CrossRef
    65. Storgaard M, Lauren AL, Anderson PL (1996) The occurrence of / Blastocystis hominis in HIV-infected patients. AIDS 10:444-45 CrossRef
    66. Teare JA, Loomis MR (1982) Epizootic of balantidiasis in lowland gorillas. J Am Vet Med Assoc 181:1345-347
    67. Terio KA, Kinsel MJ, Raphael J, Mlengeya T, Lipende I, Kirchhoff CA, Gilagiza B, Wilson ML, Kamenya S, Estes JD, Keele BF, Rudicell RS, Liu W, Patton S, Collins A, Hahn BH, Travis DA, Lonsdorf EV (2011) Pathologic lesions in chimpanzees ( / Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010. J Zoo Wildl Med 42:597-07 CrossRef
    68. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-882 CrossRef
    69. Van der Kuyl AC, Kuiken CL, Dekker JT, Goudsmit J (1995) Phylogeny of African monkeys based upon mitochondiral 12S rRNA sequence. J Mol Evol 40:173-80 CrossRef
    70. Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y, Ngolle EM, Sharp PM, Shaw GM, Delaporte E, Hahn BH, Peeters M (2006) Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444:164 CrossRef
    71. Van Heuverswyn F, Li Y, Bailes E, Neel C, Lafay B, Keele BF, Shaw KS, Takehisa J, Kraus MH, Loul S, Butel C, Liegeois F, Yangda B, Sharp PM, Mpoudi-Ngole E, Delaporte E, Hahn BH, Peeters M (2007) Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 368:155-71 CrossRef
    72. Wiwanitkit V (2006) Intestinal parasite infestation in HIV-infected patients. Curr HIV Res 4:87-6 CrossRef
  • 作者单位:Pascal Drakulovski (1) (3)
    Sébastien Bertout (2)
    Sabrina Locatelli (1)
    Christelle Butel (1)
    Sébastien Pion (1)
    Eitel Mpoudi-Ngole (2)
    Eric Delaporte (1)
    Martine Peeters (1)
    Michèle Mallié (1)

    1. UMI 233 “TransVIHMI-Institut de Recherche pour le Developpement (IRD) and University of Montpellier 1 (UM1), Montpellier, France
    3. Laboratoire de Parasitologie et Mycologie Médicale, UFR de Pharmacie, 15 Avenue Charles Falhault, 34093, Montpellier, Cedex 05, France
    2. Virology Laboratory, CREMER/IMPM/IRD, Yaoundé, Cameroon
  • ISSN:1432-1955
文摘
We tested 114 faecal samples from wild simian immunodeficiency virus (SIV)-positive (n--3) and SIV-negative (n--1) chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon for the presence of gastrointestinal parasites by direct smear. We observed cysts from different protozoa (Entamoeba coli and Entamoeba histolytica?/ Entamoeba dispar, Endolimax nana, Iodamoeba butschlii, Chilomastix mesnili, Balantidium coli and Blastocystis cells) and trophozoites from Troglodytella abrassarti and Balantidium coli. Eggs from different helminths (strongylids, Ascaris lumbricoides, Abbreviata caucasica, Trichuris sp., Capillaria sp., Enterobius anthropopeci, Bertiella sp., Hymenolepis diminuta and an undetermined fluke) were also observed. Finally, we observed eggs that could not be properly identified and classified. We did not observe any differences between the SIV-?and SIV???samples except for the unidentified eggs. The studied chimpanzees were highly parasitised by strongylid (85.1?% of prevalence), Troglodytella (43.8?%) and Blastocystis (2.9?%), and the frequency of the other parasites ranged from 0.9 to 8.8?%. These high levels of parasite infections could represent an additional burden in a population where there is a high rate of the SIV virus in circulation.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700