Investigating the phylogeny and morphological characteristics of a subgroup of the Balantidiidae family identified in chimpanzees(Pan troglodytes) along with the pathogenesis and treatment process.
Subject Areas : Journal of Comparative Pathobiology
پیمان Mohammadzadeh
1
,
ghasem mohammadi
2
1 - گروه علوم درمانگاهی دانشکده دامپزشکی دانشگاه آزاد اسلامی واحد سنندج- ایران
2 - Management of Tehran's Eram Zoo
Keywords: Buxtonella‐like, Pan troglodyte, molecular phylogeny, pathogenesis, vestibuliferid ciliates,
Abstract :
Cysts and trophozoites of vestibuliferid ciliates were found in fecal samples from captive chimpanzees(Pan troglodytes) at Tehran Eram Zoological Gardens. As comparative reference, ciliates from captive gorillas (Gorilla gorilla gorilla) at San Francisco zoo and gardens, in the USA and the Zoological Garden Berlin AG in Europe, were included in the study. Phylogenetic analysis of the detected vestibuliferid ciliates using ITS1‐5.8s‐rRNAITS2 and partial 18S ribosomal deoxyribonucleic acid (rDNA) revealed that the ciliates from chimpanzee clustered with Buxtonella‐like ciliates from other primates. Morphological examination of the cysts and trophozoites using light microscopy did not reveal differences robust enough to identify the genera of the ciliates. As B. coli is a zoonotic parasite and the conditions in captive and semi‐captive settings may facilitate transmission to humans, prophylactic measures should reflect the findings.
1. Islam S, Rahman MK, Uddin MH, Rahman MM, Chowdhury MN, Hassan MM, Magalhaes RS, Islam A. Prevalence and diversity of gastrointestinal parasites in free‐ranging rhesus macaques (Macaca mulatta) in different land gradients of Bangladesh. American Journal of Primatology. 2022 Jan;84(1):e23345.
2. Keita MB, Hamad I, Bittar F. Looking in apes as a source of human pathogens. Microbial pathogenesis. 2014 Dec 1;77:149-54.
3. Dunay E, Apakupakul K, Leard S, Palmer JL, Deem SL. Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth. 2018 Mar;15:148-62.
4. Modrý D., & Escalante, A. 2018. Parasites of orangutans.
5. Sanchez, C. R., & Pich, A. (2018). Manegament of parasitoses of apes under human care settings. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 87–91). Edition Chimaira.
6. Nurcahyo W, Konstanzová V, Foitová I. Parasites of orangutans (primates: ponginae): an overview. American Journal of Primatology. 2017 Jun;79(6):e22650.
7. Malmsten PH. Infusorien als intestinal-thiere beim menschen. Archiv für pathologische Anatomie und Physiologie und für klinische Medicin. 1857 Aug;12(2):302-9.
8. Chistyakova LV, Kostygov AY, Kornilova OA, Yurchenko V. Reisolation and redescription of Balantidium duodeni Stein, 1867 (Litostomatea, Trichostomatia). Parasitology Research. 2014 Nov;113:4207-15.
9. da Silva Barbosa A, Ponce-Gordo F, Dib LV, Uchôa CM, Bastos OM, Pissinatti A, Amendoeira MR. First molecular characterization of Balantioides coli (Malmsten, 1857) isolates maintained in vitro culture and from feces of captive animals, Rio de Janeiro, Brazil. Veterinary Parasitology: Regional Studies and Reports. 2017 Dec 1;10:102-13.
10. Supriadi W, Fitria RW, Nurcahyo RW. Balantidium sp. infection in faeces samples of orangutan (Pongo pygmaeus) from Care center and Tanjung putting national park area, central Borneo. Biology, Medicine & Natural Product Chemistry. 2012;1(1):47-52.
11. Yan W, He K, Qian W, Wang T, Zong YA, Zhang M, Wei Z, Han L. First molecular identification of Buxtonella ciliates from captive-bred mangabeys (Cercocebus torquatus) from China. Parasitology research. 2018 Dec;117:3753-9.
12. Grim JN, Jirků-Pomajbíková K, Ponce-Gordo F. Light microscopic morphometrics, ultrastructure, and molecular phylogeny of the putative pycnotrichid ciliate, Buxtonella sulcata. European journal of protistology. 2015 Oct 1;51(5):425-36.
13. Pomajbíková K, Obornik M, Horák A, Petrželková KJ, Grim JN, Levecke B, Todd A, Mulama M, Kiyang J, Modrý D. Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS neglected tropical diseases. 2013 Mar 28;7(3):e2140.
14. Schuster FL, Ramirez-Avila L. Current world status of Balantidium coli. Clinical microbiology reviews. 2008 Oct;21(4):626-38
15. Schovancová K, Pomajbíková K, Procházka P, Modrý D, Bolechová P, Petrželková KJ. Preliminary insights into the impact of dietary starch on the ciliate, Neobalantidium coli, in captive chimpanzees. Plos one. 2013 Nov 25;8(11):81374.
16. Strait K, Else JG, Eberhard ML. Parasitic diseases of nonhuman primates. Nonhuman primates in biomedical research. 2012;297:197
17. de Oliveira AS, Gómez-Hernández C, Rezende-Oliveira K. Balantidium coli infection, immune status and comorbidities: literature review. Revista de Patologia Tropical/Journal of Tropical Pathology. 2021;50(4):265-84.
18. HODEČEK S. Přenos infekčních onemocnění mezi člověkem a lidoopy.
19. Strait K, Else JG, Eberhard ML. Parasitic diseases of nonhuman primates. Nonhuman primates in biomedical research. 2013;297:197
20. Jirků‐Pomajbíková K, Vlčková K. Intestinal amoebas. Parasites of Apes. An atlas of coproscopic diagnostics. 2016:104.
21. Kváč, M., & McEvoy, J. (2018). Chilomastix mesnili. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 100–101).
22. Foitová I, Huffman MA, Wisnu N, Olsansky M. Parasites and their impacts on orangutan health. Orangutans–Geographic Variation in Behavioral Ecology and Conservation. 2009:157.
23. Nurcahyo W, Konstanzová V, Foitová I. Parasites of orangutans (primates: ponginae): an overview. American Journal of Primatology. 2017 Jun;79(6):22650.
24. 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 Jan 1;39(1):73-83.
25Kuze N, Kanamori T, Malim TP, Bernard H, Zamma K, Kooriyama T, Morimoto A, Hasegawa H. Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae). Journal of Parasitology. 2010 Oct 1;96(5):954-60.
26. Labes EM, Wijayanti N, Deplazes P, Mathis A. Genetic characterization of Strongyloides spp. from captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia. Parasitology. 2011 Sep;138(11):1471-22.
27Mul IF, Paembonan W, Singleton I, Wich SA, van Bolhuis HG. Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology. 2007 Apr;407:20-28.
28. Poirotte C, Basset D, Willaume E, Makaba F, Kappeler PM, Charpentier MJ. Environmental and individual determinants of parasite richness across seasons in a free‐ranging population of M andrills (M andrillus sphinx). American Journal of Physical Anthropology. 2016 Mar;159(3):442-54.
29Setchell JM, Bedjabaga IB, Goossens B, Reed P, Wickings EJ, Knapp LA. Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. International Journal of Primatology. 2007 Dec;134:28.
30. Burnside RJ, Collar NJ, Dolman PM. Dataset on the numbers and proportion of mortality attributable to hunting, trapping, and powerlines in wild and captive-bred migratory Asian houbara Chlamydotis macqueenii. Data in brief. 2018 Dec 1;21:1848-52.
31. da Silva Barbosa A, Ponce-Gordo F, Dib LV, Uchôa CM, Bastos OM, Pissinatti A, Amendoeira MR. First molecular characterization of Balantioides coli (Malmsten, 1857) isolates maintained in vitro culture and from feces of captive animals, Rio de Janeiro, Brazil. Veterinary Parasitology: Regional Studies and Reports. 2017 Dec 1;10:102-13.
32. Pomajbíková K, Obornik M, Horák A, Petrželková KJ, Grim JN, Levecke B, Todd A, Mulama M, Kiyang J, Modrý D. Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS neglected tropical diseases. 2013 Mar 28;7(3):2140.
33. Hassell JM, Blake DP, Cranfield MR, Ramer J, Hogan JN, Noheli JB, Waters M, Hermosilla C. Occurrence and molecular analysis of Balantidium coli in mountain gorilla (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Journal of Wildlife Diseases. 2013 Oct 1;49(4):1063-5.
34. Nurcahyo W, Konstanzová V, Foitová I. Parasites of orangutans (primates: ponginae): an overview. American Journal of Primatology. 2017 Jun;79(6):e22650.
35. Pomajbíková K, Petrželková KJ, Profousová I, Petrášová J, Modrý D. Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes. Journal of Parasitology. 2010 Dec 1;96(6):1139-44.
36. Yan W, He K, Qian W, Wang T, Zong YA, Zhang M, Wei Z, Han L. First molecular identification of Buxtonella ciliates from captive-bred mangabeys (Cercocebus torquatus) from China. Parasitology research. 2018 Dec;117:3753-9.
37. Edwards MS, Ullrey DE. Effect of dietary fiber concentration on apparent digestibility and digesta passage in non‐human primates. II. Hindgut‐and foregut‐fermenting folivores. Zoo Biology: Published in Affiliation with the American Zoo and Aquarium Association. 1999;18(6):537-49.
38. Kuhar CW, Fuller GA, Dennis PM. A survey of diabetes prevalence in zoo‐housed primates. Zoo Biology. 2013 Jan;32(1):63-9.
39. Plowman A. Diet review and change for monkeys at Paignton Zoo Environmental Park. Journal of Zoo and Aquarium Research. 2013 Oct 31;1(2):73-7.
40. Kuze N, Kanamori T, Malim TP, Bernard H, Zamma K, Kooriyama T, Morimoto A, Hasegawa H. Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae). Journal of Parasitology. 2010 Oct 1;96(5):954-60.
41. Mul IF, Paembonan W, Singleton I, Wich SA, van Bolhuis HG. Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology. 2007 Apr;28:407-20.
42. Pafčo B, Tehlárová Z, Jirků Pomajbíková K, Todd A, Hasegawa H, Petrželková KJ, Modrý D. Gastrointestinal protists and helminths of habituated agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic. American Journal of Primatology. 2018 Feb;80(2):e22736.