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Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii)

Published online by Cambridge University Press:  03 March 2016

KATEŘINA JIRKŮ-POMAJBÍKOVÁ ,
IVAN ČEPIČKA ,
BARBORA KALOUSOVÁ ,
MILAN JIRKŮ ,
FIONA STEWART ,
BRUNO LEVECKE ,
DAVID MODRÝ ,
ALEX K. PIEL  and
KLÁRA J. PETRŽELKOVÁ
KATEŘINA JIRKŮ-POMAJBÍKOVÁ
Affiliation:
Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic
IVAN ČEPIČKA
Affiliation:
Department of Zoology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 44 Prague 2, Czech Republic
BARBORA KALOUSOVÁ
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic
MILAN JIRKŮ
Affiliation:
Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 1760, 37005 České Budějovice, Czech Republic
FIONA STEWART
Affiliation:
Department of Archaeology and Anthropology, Pembroke Street, Cambridge CB2 3QG, UK
BRUNO LEVECKE
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium
DAVID MODRÝ
Affiliation:
Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, Palackého 1/3, 612 42 Brno, Czech Republic
ALEX K. PIEL
Affiliation:
School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Rm653, Byrom street, Liverpool, L3 3AF, UK
KLÁRA J. PETRŽELKOVÁ*
Affiliation:
Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Liberec Zoo, Masarykova 1347/31, 460 01 Liberec, Czech Republic Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic
*
*Corresponding author: Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic; Liberec Zoo, Masarykova 1347/31, 460 01 Liberec, Czech Republic and Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic. Phone: +420543422549. Fax: +420543211346. E-mail: [email protected]
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Summary

To address the molecular diversity and occurrence of pathogenic species of the genus Entamoeba spp. in wild non-human primates (NHP) we conducted molecular-phylogenetic analyses on Entamoeba from wild chimpanzees living in the Issa Valley, Tanzania. We compared the sensitivity of molecular [using a genus-specific polymerase chain reaction (PCR)] and coproscopic detection (merthiolate-iodine-formaldehyde concentration) of Entamoeba spp. We identified Entamoeba spp. in 72 chimpanzee fecal samples (79%) subjected to species-specific PCRs for six Entamoeba species/groups (Entamoeba histolytica, Entamoeba nuttalli, Entamoeba dispar, Entamoeba moshkovskii, Entamoeba coli and Entamoeba polecki ST2). We recorded three Entamoeba species: E. coli (47%), E. dispar (16%), Entamoeba hartmanni (51%). Coproscopically, we could only distinguish the cysts of complex E. histolytica/dispar/moshkovskii/nuttalli and E. coli. Molecular prevalence of entamoebas was higher than the prevalence based on the coproscopic examination. Our molecular phylogenies showed that sequences of E. dispar and E. coli from Issa chimpanzees are closely related to sequences from humans and other NHP from GenBank. The results showed that wild chimpanzees harbour Entamoeba species similar to those occurring in humans; however, no pathogenic species were detected. Molecular-phylogenetic methods are critical to improve diagnostics of entamoebas in wild NHP and for determining an accurate prevalence of Entamoeba species.

Keywords

Entamoebamolecular diversitygreat apeschimpanzeesavannah
Type
Research Article
Information
Parasitology , Volume 143 , Issue 6 , May 2016 , pp. 741 - 748
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Ash, L. R. and Orihel, T. C. (2007). Atlas of Human Parasitology, 5th Edn. American Society for Clinical Parasitology, Singapore.Google Scholar
Ashford, R. W., Reid, G. D. F. and Wrangham, R. W. (2000). Intestinal parasites of the chimpanzee, Pan troglodytes, in Kibale Forest, Uganda. Annals of Tropical Medicine and Parasitology 94, 173–179.CrossRefGoogle ScholarPubMed
Blagg, W., Schloegel, E. L., Mansour, N. S. and Khalaf, G. I. (1955). A new concentration technic for the demonstration of protozoa and helminth eggs in feces. American Society of Tropical Medicine and Hygiene 4, 23–28.CrossRefGoogle ScholarPubMed
Chapman, C. A. and Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. American Journal of Primatology 50, 169–185.Google Scholar
Gillespie, T. R., Lonsdorf, E. V., Canfield, E. P., Meyer, D. J., Nadler, Y., Raphael, J., Pusey, A. E., Pond, J., Pauley, J., Mlengeya, T. and Travis, D. A. (2010). Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. American Journal of Physical Anthropolgy 143, 534–544.Google Scholar
Hamzah, Z., Petmitr, S., Mungthin, M., Leelayoova, S. and Chavalitshewinkoon-Petmitr, P. (2006). Differential detection of Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii by a single-round PCR assay. Journal of Clinical Microbiology 44, 3196–3200.CrossRefGoogle ScholarPubMed
Hernandez-Aguilar, R. A., Moore, J. and Stanford, C. B. (2013). Chimpanzee nesting patterns in savanna habitat: environmental influences and preferences. American Journal of Primatology 75, 979–994.Google Scholar
Howells, M. E., Pruetz, J. and Gillespie, T. R. (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. American Journal of Primatology 73, 173–179.Google Scholar
Kalousová, B., Piel, A. K., Pomajbíková, K., Modrý, D., Stewart, F. A. and Petrželková, K. J. (2014). Gastrointestinal parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) in Ugalla, Tanzania. International Journal of Primatology 35, 463–475.CrossRefGoogle Scholar
Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Kebede, A., Verweij, J. J., Petros, B. and Polderman, A. M. (2004). Short communication: misleading microscopy in amoebiasis. Tropical Medicine and International Health 9, 651–652.CrossRefGoogle ScholarPubMed
Kooriyama, T., Hasegawa, H., Shimozuru, M., Tsubota, T., Nishida, T. and Iwaki, T. (2012). Parasitology of five primates in Mahale Mountains National Park, Tanzania. Primates 53, 365–375.CrossRefGoogle ScholarPubMed
Levecke, B., Dreesen, L., Dorny, P., Verweij, J. J., Vercammen, F., Casaert, S., Vercruysse, J. and Geldhof, P. (2010). Molecular identification of Entamoeba spp. in captive nonhuman primates. Journal of Clinical Microbiology 48, 2988–2990.CrossRefGoogle ScholarPubMed
Levecke, B., Dorny, P., Vercammen, F., Visser, L. G., Van Esbroeck, M., Vercruysse, J. and Verweij, J. J. (2015). Transmission of Entamoeba nuttalli and Trichuris trichiura from nonhuman primates to humans. Emerging Infectious Diseases 21, 1871–1872.CrossRefGoogle ScholarPubMed
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika research site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555–573.Google Scholar
Moore, J. (1994). Plants of the Tongwe East Forest Reserve (Ugalla), Tanzania. Tropics 3, 333–340.CrossRefGoogle Scholar
Muehlenbein, M. P. (2005). Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. American Journal of Primatology 65, 167–179.Google Scholar
Pedersen, A. B., Altizer, S., Poss, M., Cunningham, A. A. and Nunn, C. L. (2005). Patterns of host specificity and transmission among parasites of wild primates. International Journal For Parasitology 35, 647–657.CrossRefGoogle ScholarPubMed
Petrášová, J., Uzlíková, M., Kostka, M., Petrželková, K. J., Huffman, M. A. and Modrý, D. (2011). Diversity and host specificity of Blastocystis in syntopic primates on Rubondo Island, Tanzania. International Journal For Parasitology 41, 1113–1120.Google Scholar
Piel, A. K., Lenoel, A., Johnson, C. and Stewart, F. (2015). Deterring poaching in western Tanzania: the presence of wildlife researchers. Global Ecology and Conservation 15, 188–199.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Regan, C. S., Yon, L., Hossain, M. and Elsheikha, H. M. (2014). Prevalence of Entamoeba species in captive primates in zoological gardens in the UK. Peer J 2, e492.CrossRefGoogle ScholarPubMed
Rivera, W. L., Yason, J. and Adao, D. E. V. (2010). Entamoeba histolytica and E. dispar infections in captive macaques (Macaca fascicularis) in the Philippines. Primates 51, 69–74.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Rudicell, R. S., Piel, A. K., Stewart, F., Moore, D. L., Learn, G. H., Li, Y., Takehisa, J., Pintea, L., Shaw, G. M., Moore, J., Sharp, P. M. and Hahn, B. H. (2011). High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees. Journal of Virology 85, 9918–9928.CrossRefGoogle Scholar
Sak, B., Petrželková, K. J., Květoňová, D., Mynarová, A., Shutt, K. A., Pomajbíková, K., Kalousová, B., Modrý, D., Benavides, J., Todd, A. and Kváč, M. (2013). Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. Plos ONE 8, e71840.CrossRefGoogle ScholarPubMed
Sak, B., Petrželková, K. J., Květoňová, D., Mynářová, A., Pomajbíková, K., Kalousová, B., Modrý, D., Cranfield, M. R. and Kváč, M. (2014). Microsporidia, Cryptosporidium and Giardia infections in mountain gorillas (Gorilla beringei beringei) in National Park Virunga Volcanoes, Rwanda. Plos ONE 9, e109751.Google Scholar
Sard, B. G., Navarro, R. T. and Sanchis, J. G. E. (2011). Non-pathogenic intestinal amoebae: a clinical-analytical overview. Enfermedades Infecciosas y Microbiología Clínica 29, 20–28.CrossRefGoogle ScholarPubMed
Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. and Patton, S. (2000). Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. Journal of Zoo and Wildlife Medicine 31, 322–328.Google ScholarPubMed
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.Google Scholar
Stensvold, C. R., Lebbad, M., Verweij, J. J., Jespersgaard, C., von Samson-Himmelstjerna, G., Nielsen, S. S. and Nielsen, H. V. (2010). Identification and delineation of members of the Entamoeba complex by pyrosequencing. Molecular and Cellular Probes 24, 403–406.CrossRefGoogle ScholarPubMed
Stensvold, C. R., Lebbad, M., Victory, E. L., Verweij, J. J., Tannich, E., Alfellani, M., Legarraga, P. and Clark, C. G. (2011). Increased sampling reveals novel lineages of Entamoeba: consequences of genetic diversity and host specificity for taxonomy and molecular detection. Protist 162, 525–541.CrossRefGoogle ScholarPubMed
Suzuki, J., Kobayashi, S., Murata, R., Tajima, H., Hashizaki, F., Yanagawa, Y. and Takeuchi, T. (2008). A survey of amoebic infections and differentiation of an Entamoeba histolytica-like variant (JSK2004) in nonhuman primates by a multiplex polymerase chain reaction. Journal of Zoo and Wildlife Medicine 39, 370–379.CrossRefGoogle ScholarPubMed
Tachibana, H., Cheng, X. J., Kobayashi, S., Fujita, Y. and Udono, T. (2000). Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitology Research 86, 537–541.CrossRefGoogle ScholarPubMed
Tachibana, H., Yanagi, T., Pandey, K., Cheng, X. J., Kobayashi, S., Sherchand, J. B. and Kanbara, H. (2007). An Entamoeba sp. strain isolated from rhesus monkey is virulent but genetically different from Entamoeba histolytica . Molecular and Biochemical Parasitology 153, 107–114.CrossRefGoogle ScholarPubMed
Tachibana, H., Yanagi, T., Akatsuka, A., Kobayashi, S., Kanbara, H. and Tsutsumi, V. (2009). Isolation and characterization of a potentially virulent species Entamoeba nuttalli from captive Japanese macaques. Parasitology 136, 1169–1177.CrossRefGoogle ScholarPubMed
Tachibana, H., Yanagi, T., Feng, M., Bandara, K. B., Kobayashi, S., Cheng, X., Hirayama, K. and Rajapakse, R. P. (2015). Isolation and molecular characterization of Entamoeba nuttalli strains showing novel isoenzyme patterns from wild toque macaques in Sri Lanka. Journal of Eukaryotic Microbiology, ahead of print.Google Scholar
Verweij, J. J., Polderman, A. M. and Clark, C. G. (2001). Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. Journal of Clinical Microbiology 39, 1644–1646.CrossRefGoogle ScholarPubMed
Verweij, J. J., Vermeer, J., Brienen, E. A. T., Blotkamp, C., Laeijendecker, D., van Lieshout, L. and Polderman, A. M. (2003). Entamoeba histolytica infections in captive primates. Parasitology Research 90, 100–103.Google Scholar
Visser, L. G., Verweij, J. J., Van Esbroeck, M., Edeling, W. M., Clerinx, J. and Polderman, A. M. (2006). Diagnostic methods for differentiation of Entamoeba histolytica and Entamoeba dispar in carriers: performance and clinical implications in a non-endemic setting. International Journal of Medical Microbiology 296, 397–403.CrossRefGoogle Scholar
Wuyts, J., Van de Peer, Y. and Wachter, R. D. (2001). Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Research 29, 5017–5028.CrossRefGoogle ScholarPubMed
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