Abstract
The ciliate species Balantioides coli can be cross-transmitted between humans and several animal species. Usually harmless, sometimes it can be pathogenic and cause the death of the host. In birds, B. coli has been confirmed in ostriches by genetic analysis, but the identification from South American greater rheas (Rhea americana) and lesser rheas (Rhea pennata pennata) is tentative. Since these species are reared for commercial purposes and for reintroduction into the wild, it is necessary to elucidate whether the ciliate from rheas is B. coli to minimize health risks for humans and for other domestic and wild animals. Individual parasite cells are collected from Argentinean isolates of reared greater rheas and of wild and reared lesser rheas, and their ITS region was PCR amplified; the cloning products were sequenced and compared with sequences available in public databases. The results have shown that several sequence types are expressed at the same time in the parasite cells, and all correspond to B. coli, confirming the possibility of cross-transmission of the parasite between wild and reared South American rheas and several mammal species and humans.
This is a preview of subscription content, log in via an institution to check access.
References
Alexeieff A (1931) Sur quelques particularités de structure de Balantioides (nom. nov.) coli (Malmsten.). Comptes Rendus Hebdomadaires des Séances et Mémoires la Société de Biologie et de ses Fililiales 107:210–211
Al-Tayib O (2014) Zoonotic balantidiasis in a camel from Saudi Arabia. Sch Acad J Biosci 2:445–447
Ballari SA, Cuevas MF, Ojeda RA, Navarro JL (2014) Diet of wild boar (Sus scrofa) in a protected area of Argentina: the importance of baiting. Mamm Res 60:81–87
Chistyakova LV, Kostygov AY, Kornilova OA, Yurchenko V (2014) Reisolation and redescription of Balantidium duodeni Stein, 1867 (Litostomatea, Trichostomatia). Parasitol Res 113:4207–4215
Cho HS, Shin SS, Park NY (2006) Balantidiasis in the gastric lymph nodes of Barbary sheep (Ammotragus lervia): an incidental finding. J Vet Sci 7:207–209
CITES (2017) Convention on International Trade in Endangered Species of Wild Fauna and Flora https://cites.org/sites/default/files/ eng/app/2017/E-Appendices-2017-10-04.pdf. (accessed 24.04.19.)
Costa AO, da Silva Junior AB, Gruchouskei L, Viott RC, de Carvalho AL, de Viott AM (2013) Balantidíase fatal com envolvimento ocular, pulmonar e cerebral em ratao do banhado (Myocastor coypus). Arch Vet Sci 18(supl. 2):404–406
da Silva Barbosa A, Ponce-Gordo F, Dib LV, Antunes Uchôa CM, Bastos OMP, Pissinatti A, Amendoeira MRR (2017) First molecular characterization of Balantioides coli (Malmsten, 1857) isolates maintained in vitro culture and from feces of captive animals, Rio de Janeiro Brazil. Vet Parasitol Reg Stud Rep 10:102–113
Frixione M, Lamo D De, Olaechea F (2014) Aportes al conocimiento de los endoparásitos del choique (Rhea pennata) en una población silvestre del noroeste patogónico, Argentina. Rev Argentina Parasitol 2:6–10
Hanley RS, Woods LW, Stillian DJ, Dumonceaux GA (1994) Serpulina-like spirochetes and flagellated protozoa associated with a necrotizing typhlitis in the rhea ( Rhea Americana ). In: Assoc. Avian Vet. 1994 Main Conf. Proc.,, pp. 157–162
Hegner R (1934) Specificity in the genus Balantidium based on size and shape of body and macronucleus, with descriptions of six new species. Am J Hyg 19:38–67
Levine ND (1985) Veterinary parasitology. Iowa State University Press, Ames
Martella MB, Navarro JL (2006) Proyecto Ñandú. Manejo de Rhea americana y Rhea pennata en la Argentina. In: Manejo Fauna Silv. en la Argentina. Programas uso sustentable, Dirección de Fauna Silvestre, Secretaría de Ambiente y Desarrollo Sustentable, Buenos Aires, pp. 39–50
Martínez-Díaz RA, Martella MB, Navarro JL, Ponce-Gordo F (2013) Gastrointestinal parasites in greater rheas (Rhea americana) and lesser rheas (Rhea pennata) from Argentina. Vet Parasitol 194:75–78
McDonald JD (1922) On Balantidium coli (Malmsten) and Balantidium suis (sp. nov.), with an account of their neuromotor apparatus. Univ. Calif. Publ. Zool 20:243–300
Navarro JL, Martella MB (2008) The relevance of captive breeding to conservation of native ratites in Argentina: an overview. Aust J Exp Agric 48:1302–1307
Navarro JL, Martella MB (2011) Ratite conservation: linking captive-release and welfare. In: Glatz P, Lunam C, Malecki I (eds) The welfare of farmed ratites. Springer, pp 237–258
Navarro JL, Lèche A, Della Costa NS, Vera Cortez M, Marin RH, Martella MB (2019) State of the art knowledge in adrenocortical and behavioral responses to environmental challenges in a threatened South American ratite: implications to in situ and ex-situ conservation. Gen Comp Endocrinol 273:52–60
Neiva A, Marques da Cunha A, Travassos L (1914) Contribuiçoes parazitolojicas. Mem. Inst. Oswaldo Cruz 6:180–191
Norman Grim J, Jirků-Pomajbíková K, Ponce-Gordo F (2015) Light microscopic morphometrics, ultrastructure, and molecular phylogeny of the putative pycnotrichid Ciliate Buxtonella sulcata. Eur J Protistol 51
Pomajbíková K, Oborník M, Horák A, Petrželková KJ, Grim JN, Levecke B, Todd A, Mulama M, Kiyang J, Modrý D (2013) Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS Negl Trop Dis 7:e2140
Ponce Gordo F, Herrera S, Castro AT, García Durán B, Martínez Díaz RA (2002) Parasites from farmed ostriches (Struthio camelus) and rheas (Rhea americana) in Europe. Vet Parasitol 107:137–160
Ponce-Gordo F, Jirků-Pomajbíková K (2017) Balantidium coli. In: Rose JB, Jiménez-Cisneros B (Eds.), Glob. Water Pathog. Proj. Part 3. Protists, Michigan State University, El. Lansing, MI, UNESCO, pp. 1–14
Ponce-Gordo F, Jimenez-Ruiz E, Martínez-Díaz RA (2008) Tentative identification of the species of Balantidium from ostriches (Struthio camelus) as Balantidium coli-like by analysis of polymorphic DNA. Vet Parasitol 157:41–49
Ponce-Gordo F, Fonseca-Salamanca F, Martínez-Díaz RA (2011) Genetic heterogeneity in internal transcribed spacer genes of Balantidium coli (Litostomatea, Ciliophora). Protist 162:774–794
Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli. Clin Microbiol Rev 21:626–638
Solaymani-Mohammadi S, Rezaian M, Anwar MA (2005) Response to Cox: Human balantidiasis in Iran: wild boars or not? Trends Parasitol 21:554–555
Tajik J, Nourollahi Farda SR, Paidar A, Anousheh S, Dehghani E (2013) Balantidiasis in a dromedarian camel. Asian Pac J Trop Med 3:409–412
Vikrant S, Sharma RL, Patya A, Singh PK (2012) An occurrence of clinical balantidiasis in a cross bred cow and its therapeutic management. J Vet Parasitol 26:164–166
Yan W, Zhang L (2011) [Population characterization of Balantidium coli from pigs using ITS1-5.8S rRNA-ITS2 sequence] (in Chinese). Acta Microbiol Sin 51:828–834
Author information
Authors and Affiliations
Contributions
JLN and MBM collected the samples and did their initial processing; RAMD and FPG carried out the laboratory processing and morphological identification; FPG and JJGR carried out the genetic analysis. All authors contributed to the redaction of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Section Editor: Panagiotis Karanis
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 71 kb)
Rights and permissions
About this article
Cite this article
García-Rodríguez, J.J., Martínez-Díaz, R.A., Martella, M. et al. Genetic identification of the ciliates from greater rheas (Rhea americana) and lesser rheas (Rhea pennata) as Balantioides coli. Parasitol Res 119, 755–758 (2020). https://doi.org/10.1007/s00436-019-06559-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06559-5