Acta Parasitologica

, Volume 63, Issue 2, pp 287–298 | Cite as

Balantioides coli: morphological and ultrastructural characteristics of pig and non-human primate isolates

  • Alynne Silva da BarbosaEmail author
  • Helene Santos Barbosa
  • Sandra Maria Oliveira de Souza
  • Laís Verdan Dib
  • Claudia Maria Antunes Uchôa
  • Otilio Machado Pereira Bastos
  • Maria Regina Reis Amendoeira


Balantioides coli is a ciliated protozoon that inhabits the intestine of pigs, non-human primates and humans. Light microscopy studies have described over 50 species of the genus Balantioides but their validity is in doubt. Due to the limited information about this genus, this study is aimed to identify morphological characteristics of Balantioides coli isolated using fluorescence microscopy and both scanning (SEM) and transmission electron microscopy (TEM). Trophozoites isolated from the feces of pig and macaque were washed and subjected to centrifugation. These cells were fixed with paraformaldehyde for immunofluorescence. Other aliquots of these trophozoites were fixed with glutaraldehyde, post fixed with osmium tetroxide and processed for SEM and TEM. Immunofluorescence studies revealed microtubules with a longitudinal distribution to the main axis of the parasite and in the constitution of cilia. SEM demonstrated a high concentration of cilia covering the oral apparatus and a poor presence of such structures in cytopyge. TEM revealed in the plasma membrane, several associated structures were observed to delineate the cellular cortex and mucocysts. The cytoskeleton of the oral region was observed in detail and had an organization pattern consisting of microtubules, which formed files and nematodesmal networks. Organelles such as hydrogenosomes like and peroxisomes were observed close to the cortex. Macronuclei were observed, but structures that were consistent with micronuclei were not identified. Ultrastructural morphological analysis of isolates confirms its similarity to Balantioides coli. In this study were identified structures that had not yet been described, such as hydrogenosomes like and cytoskeletal structures.


Balantioides coli ciliates SEM TEM hydrogenosomes like peroxisomes 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Auerbach E. 1953. The study of Balantidium coli (Stein, 1863) in relation to cytology and behavior in culture. Journal of Morphology, 93, 405–445. DOI: 10.1002/jmor.1050930302CrossRefGoogle Scholar
  2. Barbosa, A.S., Bastos O.M.P., Uchôa C.M.A., Pissinatti, A., Filho P.R.F., Dib, L.V., et al. 2015. Isolation and maintenance of Balantidium coli (Malmsteim, 1857) cultured from fecal samples of pigs and non-human primates. Veterinary Parasitology, 210, 240–245. DOI: 10.1016/j.vetpar.2015.03.030CrossRefGoogle Scholar
  3. Barbosa, A.S., Ponce-Gordo, F., Dib, L.V., Uchôa C.M.A., Bastos O.M.P., Pissinatti, A., Amendoeira M.R.R. 2017. 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, 10, 102–113. DOI: Scholar
  4. Benchimol M. 2009. Hydrogenosomes under microscopy. The Cell, 41, 151–168. DOI: 10.1016/j.tice.2009.01.001Google Scholar
  5. Chistyakova, L.V., Kostygov, A.Y., Kornillova, A.O., Yurchenko V. 2014. Reisolation and redescription of Balantidium duodeni Stein, 1867 (Litostomatea, Trichostomatia). Parasitology Research, 113, 4207–15. DOI: 10.1007/s00436-014-4096-1CrossRefGoogle Scholar
  6. Ewing, M.S., Kocan, K.M., Ewing S.A. 1985. Icthyophthirius multifis invasion of gill epithelium. Journal of Protozoology, 32, 305–310. DOI: 10.1111/j.1550-7408.1985.tb03055.xCrossRefGoogle Scholar
  7. Frasson, A.P., Vieira, P.B., De Carli, G.A., Tasca T. 2010. Giardia lamblia: Distribuição de microtúbulos no citoesqueleto de trofozoítose cistos utilizando taxóide fluorescente. Revista de Patologia Tropical, 39, 21–32. DOI: Scholar
  8. Grim, J.N., Clements, K.D., Byfield T. 2002. New species of Balantidium and Paracichlidotherus (Ciliophora) inhabiting the intestines of four surgeonfish species form the Tuvalu islands, Pacific ocean. The Journal of Eukaryotic Microbiology, 49, 146–153. DOI: 10.1111/j.1550-7408.2002.tb00359.xCrossRefGoogle Scholar
  9. Grim, J.N., Buonanno F. 2009. A re-description of the ciliate genus and type species Balantidium entozoon. European Journal of Protistology, 45, 174–182. DOI: 10.1016/j.ejop.2008.10.001CrossRefGoogle Scholar
  10. Hegner R. 1934. Specifity in the genus Balantidium based on size and shape of body and macronucleus, with descriptions of six new species. American Journal of Hygiene, 19, 38–67Google Scholar
  11. Huttenlauch, I., Peck, R.K., Stick R. 1998. Articulins and epiplasmins: two distinct classes of cytoskeletal proteins of the membrane skeleton in protists. Journal of Cell Science, 111, 3367–3378PubMedGoogle Scholar
  12. Jones W.R. 1946. The experimental infection of rats with Entamoeba histolytica; Method for Evaluating with the anti-amoebic properties of new compounds. Annals of Tropical Medicine and Parasitology, 40, 130–140. DOI: Scholar
  13. King, R.L., Beams, H.W., Tahmisian, T.N., Devine R.L. 1961. The ciliature and infraciliature of Nyctotherus ovalis Leidy. The Journal of Protozoology, 8, 98–111. DOI: 10.1111/j.1550-7408.1961.tb01189.xCrossRefGoogle Scholar
  14. Krascheninnikow, S., Wenrich D.H. 1958. Some observations on the morphology and Division of Balantidium coli and Balantidium caviae. The Journal of Protozoology, 5, 196–202. DOI: 10.1111/j.1550-7408.1958.tb02551.xCrossRefGoogle Scholar
  15. Levine N.D. 1940. Changes in the dimensions of Balantidium from swine upon cultivation. American Journal of Hygiene, 32, 1–7Google Scholar
  16. Li, M., Wang, J., Zhang, J., Gu, Z., Ling, F., Ke, X., Gong X. 2008. First report of two Balantidium species from the Chinese giant salamander, Andrias davidianus: Balantidium sinensis Nie 1935 and Balantidium andianusis sp. Parasitology Research, 102, 605–611. DOI: 10.1007/s00436-007-0795-1CrossRefGoogle Scholar
  17. Lynn D.H. (Ed.) 2008. The Ciliated protozoa. Characterization Classification and Guide to the Literature. Third Ed. Springer, New York, pp. 638Google Scholar
  18. Ming, L., Chong, W., Grim, J.N., Jianguo, W., Xiaoning G. 2014. Ultrastructural study of Balantidium ctenopharyngodoni Chen, 1955 (Class: Litostomatea) form China with an emphasis on its vestibulum. Acta Parasitologica, 59, 413–419. DOI: 10.2478/s11686-014-0262-yGoogle Scholar
  19. Nilles-Bije, M.L., Rivera W.L. 2010. Ultrastructural and molecular characterization of Balantidium coli isolated in the Philippines. Parasitology Research, 106, 387–394. DOI: 10.1007/s00436-009-1673-9CrossRefGoogle Scholar
  20. Novikoff A.B. 1969. Visualization of peroxisomes (microbodies) and mitochondria with diaminobenzidine. The Journal Histochemistry and Cytochemistry, 17, 675–680. DOI: 10.1177/17.10.675CrossRefGoogle Scholar
  21. Pavlova E.A. 1938. Sur les Méthodes de la culture d’ Entamoeba histolytica. Meditsinskaia Parazitologiia I Parazitarnye Bolezni, 7, 224–227. (In French)Google Scholar
  22. Pomajbiková K., Oboromik, M., Horák, A., Petrzelkova, K.J., Grim, J.N., 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 Neglected Tropical Disease, 7, 1–10. DOI: 10.1371/journal.pntd.0002140CrossRefGoogle Scholar
  23. Schuster, F.L., Ramirez-Avila L. 2008. Current World Status of Balantidium coli. Clinical Microbiology Reviews, 21, 626–638. DOI: 10.1128/CMR.00021-08CrossRefGoogle Scholar
  24. Silveira M. 2010. Scanning microscopy of ciliary organelles. In: (Eds: A. Mendes-Vilas and J. Diaz) Microscopy: Science, Technology, Applications and Education. Vol. 1. Microscopy Book Series, Formatex Research Center, 156–161Google Scholar
  25. Solaymani-Mohammadi, S., Petri Jr W.A. 2006. Zoonotic implications of the swine- transmitted protozoal infections. Veterinary Parasitology, 140, 189–203. DOI: Scholar
  26. Skotarczak B. 1997. Ultrastructural and Cytochemical identification of peroxisomes in Balantidium coli, Ciliophora. Folia biologica (Kraków), 45, 117–120Google Scholar
  27. Skotarczak B. 1999. Cytochemical identification of mucocysts in Balantidium coli trophozoites. Folia biologica (Kraków), 47, 61–65Google Scholar
  28. Thompson R.C.A., Smith A. 2011. Zoonotic enteric protozoa. Veterinary Parasitology, 182, 70–78. DOI: 10.1016/j.vetpar.2011.07.016CrossRefGoogle Scholar
  29. Van Hoek A.H.A.M, Akhmanova, A.S., Huynen, M.A., Hackstein H.P. 2000. A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Molecular Biology and Evolution, 17, 202–206CrossRefGoogle Scholar
  30. Yarllet, N., Hann, A.C., Lloyd D. 1983. Hydrogenosomes in a mixed isolate of Isotricha prostoma and Isotricha intestinalis from ovine rumen contents. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry. 74, 357–364. DOI: Scholar
  31. Zaman V. 1978. Balantidium coli. In: (Ed. J.P. Kreier). Parasitic protozoa. Vol. 2. Academic Press, New York, pp. 633–653Google Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2018

Authors and Affiliations

  • Alynne Silva da Barbosa
    • 1
    • 3
    Email author
  • Helene Santos Barbosa
    • 2
  • Sandra Maria Oliveira de Souza
    • 2
  • Laís Verdan Dib
    • 3
  • Claudia Maria Antunes Uchôa
    • 3
  • Otilio Machado Pereira Bastos
    • 3
  • Maria Regina Reis Amendoeira
    • 1
  1. 1.Laboratório de Toxoplasmose e outras ProtozoosesInstituto Oswaldo CruzManguinhosBrasil
  2. 2.Laboratório de Biologia EstruturalInstituto Oswaldo CruzManguinhosBrazil
  3. 3.Universidade Federal FluminenseInstituto Biomédico, Departamento de Microbiologia e Parasitologia. Rua Professor Hernani de Mello, São DomingosNiteróiBrasil

Personalised recommendations