Hostname: page-component-6bf8c574d5-2jptb Total loading time: 0 Render date: 2025-02-26T00:54:15.529Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular prevalence and genetic characterization of piroplasms in dogs from Tunisia

Published online by Cambridge University Press:  15 July 2016

MOHAMED R. RJEIBI ,
SAFA AMAIRIA ,
MARIEM ROUATBI ,
FATMA BEN SALEM ,
MOEZ MABROUK  and
MOHAMED GHARBI
MOHAMED R. RJEIBI
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
SAFA AMAIRIA
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
MARIEM ROUATBI
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
FATMA BEN SALEM
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
MOEZ MABROUK
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
MOHAMED GHARBI*
Affiliation:
Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia
*
*Corresponding author: Laboratoire de Parasitologie, Univ. Manouba, Institution de la Recherche et de l'Enseignement Supérieur Agricoles, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020 Sidi Thabet, Tunisia. Tel: +216 71 552 200×264. Fax: +216 71 552 441. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In this study, the prevalence of piroplasms in dogs was assessed using polymerase chain reaction (PCR) to identify Babesia and Theileria species in 200 dogs from Northern and Central Tunisia between spring and autumn 2014. The overall molecular prevalence for piroplasms was 14·5% ± 0·05 (29/200); PCR detected 2 species, namely Babesia vogeli and Theileria annulata with an overall prevalence of 12·5 ± 0·04 and 2% ± 0·02, respectively. No differences in the molecular prevalences of B. vogeli were revealed for age and sex (P > 0·05). The molecular prevalence of B. vogeli was significantly higher in central Tunisia (26·5% ± 0·01) compared with the North (9·6% ± 0·04) (P < 0·05). More working and companion dogs were infected by B. vogeli (25·8 ± 0·15 and 21·1% ± 0·13, respectively) in comparison with guarding dogs (1·8% ± 0·03) (P < 0·05). Concerning T. annulata, no significant variation was observed for all studied risk factors (P > 0·05). Comparison of the partial sequences of 18S rRNA and Tams 1 genes confirmed the presence of 2 novel B. vogeli and T. annulata genotypes. This is the first molecular detection of T. annulata and genetic characterization of dogs’ piroplasms in Tunisia. Further studies are needed to better assess the epidemiological feature of piroplasms infection in North Africa.

Keywords

Babesia vogeliTheileria annulataDogPCRTunisia
Type
Research Article
Information
Parasitology , Volume 143 , Issue 12 , October 2016 , pp. 1622 - 1628
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aktas, M., Özübek, S., Altay, K., Ipek, N. D. S., Balkaya, İ., Utuk, A. E., Kırbas, A., Şimsek, S. and Dumanli, N. (2015). Molecular detection of tick-borne rickettsial and protozoan pathogens in domestic dogs from Turkey. Parasite & Vectors 8, 157.CrossRefGoogle ScholarPubMed
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Bigdeli, M., Rafie, S. M., Namavari, M. M. and Jamshidi, S. (2012). Report of Theileria annulata and Babesia canis infections in dogs. Comparative Clinical Pathology 21, 375–377.CrossRefGoogle Scholar
Birkenheuer, A. J., Levy, M. G. and Breitschwerdt, E. B. (2003). Development and evaluation of a semi-nested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. Journal of Clinical Microbiology 41, 4172–4177.CrossRefGoogle Scholar
Bouattour, A. (2002). Clé dichotomique et identification des tiques (Acari: Ixodidae) parasites du bétail au Maghreb. Archives de l'Institut Pasteur de Tunis 79, 43–50.Google Scholar
Bourdoiseau, G. (2006). Canine babesiosis in France. Veterinary Parasitology 138, 118–125.CrossRefGoogle ScholarPubMed
Brandao, L. P., Hagiwara, M. K. and Myiashiro, S. I. (2003). Humoral immunity and reinfection resistance in dogs experimentally inoculated with Babesia canis an either treated or untreated with imidocarb dipropionate. Veterinary Parasitology 114, 253–265.CrossRefGoogle ScholarPubMed
Caccio, S. M., Antunovic, B., Moretti, A., Mangili, V., Marinculic, A., Baric, R. R., Slemenda, S. B. and Pieniazek, N. J. (2002). Molecular characterisation of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Veterinary Parasitology 106, 285–292.Google Scholar
Cardoso, L., Costa, A., Tuna, J., Vieira, L., Eyal, O., Yisaschar-Mekuzas, Y. and Baneth, G. (2008). Babesia canis canis and Babesia canis vogeli infections in dogs from northern Portugal. Veterinary Parasitology 156, 199–204.CrossRefGoogle ScholarPubMed
Carret, C., Walas, F., Carey, B., Grande, N., Precigout, E., Moubri, K., Schetters, T. P. and Gorenfolt, A. (1999). Babesia canis canis, Babesia canis vogeli, Babesia canis rossi: differentiation of the three subspecies by a restriction fragment length polymorphism analysis on amplified small subunit ribosomal RNA genes. Journal of Eukaryotic Microbiology 46, 298–303.Google Scholar
Chabchoub, A., Ghorbel, A., Landolsi, F. and Arfaoui, F. (2001). Population canine admise à la consultation de l'ENMV de Sidi Thabet et dominantes pathologiques en clinique médicale : étude statistique sur 15 ans d'activité. El Baytari 25, 1–4.Google Scholar
Criado-Fornelio, A., Martinez-Marcos, A., Buling-Sarana, A. and Barba-Carretero, J. C. (2003). Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I. Epizootiological aspects. Veterinary Parasitology 113, 189–201.Google Scholar
Criado-Fornelio, A., Rey-Valeiron, C., Buling, A., Barba-Carretero, J. C., Jefferies, R. and Irwin, P. (2007). New advances in molecular epizootiology of canine hematic protozoa from Venezuela, Thailand and Spain. Veterinary Parasitology 144, 261–269.CrossRefGoogle ScholarPubMed
da Costa, A. P., Costa, F. B., Labruna, M. B., Silveira, I., Moraes-Filho, J., Soares, J. F., Spolidorio, M. G. and Guerra Rde, M. (2015). A serological and molecular survey of Babesia vogeli, Ehrlichia canis and Rickettsia spp. among dogs in the state of Maranhão, northeastern Brazil. Revista Brasileira de Parasitologia Veterinaria 24, 28–35.Google Scholar
Dean, A. G., Arner, T. G., Sunki, G. G., Friedman, R., Lantinga, M., Sangam, S., Zubieta, J. C., Sullivan, K. M., Brendel, K. A., Gao, Z., Fontaine, N., Shu, M., Fuller, G., Smith, D. C., Nitschke, D. A. and Fagan, R. F. (2011). EpiInfo™, a Database and Statistics Program for Public Health Professionals. CDC, Atlanta, USA.Google Scholar
d'Oliveira, C., Van Der Weide, M., Habela, M. A., Jacquiet, P. and Jongejan, F. (1995). Detection of Theileria annulata in blood samples of carrier cattle by PCR. Journal of Clinical Microbiology 33, 2665–2669.CrossRefGoogle ScholarPubMed
Duarte, S. C., Linhares, G. F. C., Romanowsky, T. N., Silveira, O. J. N. and Borges, L. M. F. (2008). Assessment of primers designed for the subspecies-specific discrimination among Babesia canis canis, Babesia canis vogeli and Babesia canis rossi by PCR assay. Veterinary Parasitology 152, 16–20.Google Scholar
Duh, D., Tozon, N., Petrovec, M., Strasek, K. and Avsic-Zupanc, T. (2004). Canine babesiosis in Slovenia: molecular evidence of Babesia canis canis and Babesia canis vogeli . Veterinary Research 35, 363–368.CrossRefGoogle ScholarPubMed
Estrada-Peña, A., Bouattour, A., Camicas, J. L. and Walker, A. R. (2004). Ticks of Domestic Animals in the Mediterranean Region: A Guide to Identification of Species. University of Zaragoza, Pza, San Francisco s/n, Zaragoza, Spain.Google Scholar
Gharbi, M. and Darghouth, M. A. (2014). A review of Hyalomma scupense (Acari, Ixodidae) in the Maghreb region: from biology to control. Parasite 21, 2.Google Scholar
Gharbi, M., Rjeibi, M. R. and Darghouth, M. A. (2014). Epidémiologie de la theilériose tropicale bovine (infection par Theileria annulata) en Tunisie: une synthèse. Revue d’élevage et de Médecine Vétérinaire des Pays Tropicaux 67, 241–247.CrossRefGoogle Scholar
Gubbels, J. M., De Vos, A. P., Van Der Weide, M., Viseras, J., Schouls, L. M., De Vries, E. and Jongejan, F. (1999). Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. Journal of Clinical Microbiology 37, 1782–1789.Google Scholar
Hamel, D., Silaghi, C., Knaus, M., Visser, M., Kusi, I., Rapti, D., Rehbein, S. and Pfister, K. (2009). Detection of Babesia canis subspecies and other arthropod-borne diseases in dogs from Tirana, Albania. Wiener Klinische Wochenschrift 121, 42–45.Google Scholar
Harrus, S. and Baneth, G. (2005). Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases. International Journal of Parasitology 35, 1309–1318.CrossRefGoogle ScholarPubMed
Heidarpour Bami, M., Haddadzadeh, H. R., kazemi, B., Khazraiinia, P., Bandehpour, M. and Aktas, M. (2009). Molecular identification of ovine Theileria species by a new PCR–RFLP method. Veterinary Parasitology 161, 171–177.CrossRefGoogle ScholarPubMed
Hii, S. F., Kopp, S. R., Thompson, M. F., O'Leary, C. A., Rees, R. L. and Traub, R. J. (2012). Canine vector-borne disease pathogens in dogs from south-east Queensland and north-east Northern Territory. Australian Veterinary Journal 90, 130–135.CrossRefGoogle ScholarPubMed
Inokuma, H., Oyamada, M., Davoust, B., Boni, M., Dereure, J., Bucheton, B., Hammad, A., Watanabe, M., Itamoto, K., Okuda, M. and Brouqui, P. (2006). Epidemiological survey of Ehrlichia canis and related species infection in dogs in eastern Sudan. Annals of the New York Academy of Sciences 1078, 461–463.CrossRefGoogle ScholarPubMed
Irwin, P. J. (2009). Canine babesiosis: from molecular taxonomy to control. Parasite & Vectors 2, S4.Google Scholar
Irwin, P. J. (2010). Canine babesiosis. Veterinary Clinics of North America: Small Animal Practice 40, 1141–1156.Google Scholar
Lewis, B. D., Penzhorn, B. L., Lopez-Rebollar, L. M. and De Waal, D. T. (1996). Isolation of a South African vector-specific strain of Babesia canis . Veterinary Parasitology 63, 9–16.CrossRefGoogle ScholarPubMed
Matjila, P. T., Penzhorn, B. L., Bekker, C. P. J., Nijhof, A. M. and Jongejan, F. (2004). Confirmation of occurrence Babesia canis vogeli in domestic dogs in South Africa. Veterinary Parasitology 122, 119–125.CrossRefGoogle ScholarPubMed
M'ghirbi, Y. and Bouattour, A. (2008). Detection and molecular characterization of Babesia canis vogeli from naturally infected dogs and Rhipicephalus sanguineus ticks In Tunisia. Veterinary Parasitology 152, 1–7.CrossRefGoogle ScholarPubMed
Oyamada, M., Davoust, B., Boni, M., Dereure, J., Bucheton, B., Hammad, A., Itamoto, K., Okuda, M. and Inokuma, H. (2005). Detection of Babesia canis rossi, B. canis vogeli, and Hepatozoon canis in dogs in a village of eastern Sudan by using a screening PCR and sequencing methodologies. Clinical and Diagnostic Laboratory Immunology 12, 1343–1346.Google Scholar
Passos, L. M. F., Geiger, S. M., Ribeiro, M. F. B., Pfister, K. and Zahler-Rinder, M. (2005). First molecular detection of Babesia vogeli in dogs from Brazil. Veterinary Parasitology 127, 81–85.CrossRefGoogle ScholarPubMed
Saitou, N. and Nei, M. (1987). The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Salem, N. Y. and Farag, H. S. (2015). Clinical, hematologic, and molecular findings in naturally occurring Babesia canis vogeli in Egyptian dogs. Veterinary Medicine International 2014, 6.Google Scholar
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetics and Evolution 12, 1788–1809.CrossRefGoogle ScholarPubMed
Schwartz, D. (1993). Méthodes statistiques à l'usage des médecins et des biologistes. 3ème éd. Flammarion, Paris, France.Google Scholar
Shaw, S. E., Michael, J. D., Richard, J. B. and Breitschwerdt, E. B. (2001). Tick-borne infectious diseases of dogs. Trends in Parasitology 17, 74–80.Google Scholar
Solano-Gallego, L. and Baneth, G. (2011). Babesiosis in dogs and cats-expanding parasitological and clinical spectra. Veterinary Parasitology 181, 48–60.Google Scholar
Solano-Gallego, L., Trotta, M., Carli, E., Carcy, B., Caldin, M. and Furlanello, T. (2008). Babesia canis canis and Babesia canis vogeli clinicopathological findings and DNA detection by means of PCR-RFLP in blood from Italian dogs suspected of tick-borne disease. Veterinary Parasitology 157, 211–221.Google Scholar
Spolidorio, M. G., Minervino, A. H., Valadas, S. Y., Soares, H. S., Neves, K. A., Labruna, M. B., Ribeiro, M. F. and Gennari, S. M. (2013). Serosurvey for tick-borne diseases in dogs from the Eastern Amazon, Brazil. Revista Brasileira de Parasitologica Veterinaria 2, 214–219.CrossRefGoogle Scholar
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
The World Organisation for Animal Health/WAHID Interface. (2013). Viewed 13 March 2015. http://www.oie.int/fr/ Google Scholar
Uilenberg, G., Franssen, F. F. J., Perie, M. and Spanger, A. A. M. (1989). Three groups of Babesia canis distinguished and a proposal for nomenclature. Veterinary Quarterly 11, 33–40.Google Scholar
Zahler, M., Schein, E., Rinder, H. and Gothe, R. (1998). Characteristic genotypes discriminate between Babesia canis isolates of differing vector specificity and pathogenicity to dogs. Parasitology Research 84, 544–548.CrossRefGoogle ScholarPubMed