Abstract
Theileriosis caused by Theileria lestoquardi (malignant ovine theileriosis) in sheep and Theileria annulata (tropical theileriosis) in cattle is an important hemoprotozoal tick-borne disease in Iran. Due to major biologic and phylogenic similarities of these two species, this study was carried out to investigate the occurrence of natural infections with T.lestoquardi and T.annulata in cattle with clinical theileriosis in Ahvaz, southwest Iran. Fifty one cattle were selected based on clinical signs of theileriosis and confirmation by microscopic examination of blood smears. Blood samples were collected from each animal and hematologic and microscopic examinations were performed. Theileria piroplasmic forms were detected in all affected cattle. Pale mucous membranes (43.14%), icterus (11.76%) and fever (70.6%) were also observed. PCR-RFLP analysis revealed T. annulata infection in all tested cattle while coinfections with T. lestoquardi were found in two samples (3.92%). All sampled cattle including the two with mixed species Theileria infection were anemic. This is the first report of Theileria species cross infections in cattle with clinical theileriosis in Iran. It can be concluded that cattle can be infected with both pathogenic Theileria species, T. lestoquardi and T. annulata which can be an important issue in the epidemiology and spread of ovine malignant theileriosis.
Acknowledgments
This study was supported by the Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Iran. The authors would like to acknowledge all veterinarians and technicians in the Faculty of veterinary Medicine who helped in sample collection. We declare that there is no conflict of interest in this research.
References
Ahmed B.M., El Hussein A.M., El Ghali A., Salih D.A. 2003. Some Studies on the epidemiology of ovine theileriosis in River Nile State, Northern Sudan. Journal of Animal and Veterinary Advances, 2, 681–685Search in Google Scholar
Asri Rezaei S., Dalir-Naghadeh B. 2006. Evaluation of antioxidant status and oxidative stress in cattle naturally infected with Theileria annulata. Veterinary Parasitology, 142, 179–186. 10.1016/j.vetpar.2006.05.033Search in Google Scholar
Dolan T.T. 1989. Theileriosis: a comprehensive review. Revue Scientifique et Technique (International Office of Epizootics), 8, 11–3610.20506/rst.8.1.398Search in Google Scholar
Hashemi-Fesharki R. 1988. Control of Theileria annulata in Iran. Parasitology Today, 4, 36–40. 10.1016/0169-4758(88)90062-2Search in Google Scholar
Hashemi-Fesharki R. 1997. Tick-borne diseases of sheep and goats and their related vectors in Iran. Parassitologia, 39, 115–117Search in Google Scholar
Heidarpour Bami M., Haddadzadeh H.R., Kazemi B., Khazraiinia P., Bandehpour M., Aktas M. 2009. Molecular identification of ovine Theileria species by a new PCR–RFLP method. Veterinary Parasitology, 161, 171–177. 10.1016/j.vetpar.2009.01.035Search in Google Scholar
Hooshmand-Rad P., Hawa N.J. 1973. Transmission of Theileria hirci in sheep by 246 Hyalomma anatolicum anatolicum. Tropical Animal Health and Production, 5, 103–10910.1007/BF02236145Search in Google Scholar
Jalali S.M., Khaki Z., Kazemi B., Rahbari S., Shayan P., Bandehpour M., Yasini S.P. 2014. Molecular Detection and Identification of Theileria Species by PCR-RFLP Method in Sheep from Ahvaz, Southern Iran. Iranian Journal of Parasitology, 9, 99–106Search in Google Scholar
Kirvar E., Ilhan T., Katzer F., Wilkie G., Hooshmand-Rad P., Brown D. 1998. Detection of Theileria lestoquardi (hirci) in ticks, sheep, and goats using the polymerase chain reaction. Annals of the New York Academy of Sciences, 849, 52–62. 10.1111/j.1749-6632.1998.tb11033.xSearch in Google Scholar
Leemans I., Hooshmand-Rad P., Brown C.G.D., Wilkie G., Uggla A. 1998. In Vitro infectivity and In vivo cross-protectivity of Theileria lestoquardi and T. annulata in sheep and cattle. Annals of the New York Academy of Sciences, 849, 408–411. 10.1111/j.1749-6632.1998.tb11083.xSearch in Google Scholar
Leemans I., Brown D., Fossum C., Hooshmand-Rad P., Kirvar E., Wilkie G., Uggla A. 1999a. Infectivity and cross-immunity studies of Theileria lestoquardi and Theileria annulata in sheep and cattle II. In vitro studies. Veterinary Parasitology, 82, 193–204. 10.1016/S0304-4017(99)00014-XSearch in Google Scholar
Leemans I., Brown D., Hooshmand-Rad P., Kirvar E., Uggla A. 1999b. Infectivity and cross-immunity studies of Theileria lestoquardi and Theileria annulata in sheep and cattle I. In vivo responses. Veterinary Parasitology, 82, 179–192. 10.1016/S0304-4017(99)00013-8Search in Google Scholar
Leemans I., Hooshmand-Rad P., Uggla A. 1997. The indirect fluorescent antibody test based on schizont antigen for the study of the sheep parasite Theileria lestoquardi. Veterinary Parasitology, 69, 9–18. 10.1016/S0304-4017(96)01098-9Search in Google Scholar
Li Y., Liu Z., Yang J., Chen Z., Guan G., Niu Q., Zhang X., Luo J., Yin H. 2014. Infection of small ruminants and their red blood cells with Theileria annulata schizonts. Experimental Parasitology, 137, 21–24. 10.1016/j.exppara.2013.11.010Search in Google Scholar
Mans B.J., Pienaar R., Latif A.A. 2015. A review of Theileria diagnostics and epidemiology. International Journal for Parasitology: Parasites and Wildlife, 4, 104–11810.1016/j.ijppaw.2014.12.006Search in Google Scholar
Nabian S., Rahbari S., Changizi A., Shayan P. 2009. The distribution of Hyalomma spp. ticks from domestic ruminants in Iran. Medical and Veterinary Entomology, 23, 281–283. 10.1111/j.1365-2915.2009.00804.xSearch in Google Scholar
Omer O.H., El-Malik K.H., Mahmoud O.M., Haroun E.M., Hawas A., Sweeney D., Magzoub M. 2002. Haematological profiles in pure bred cattle naturally infected with Theileria annulata in Saudi Arabia. Veterinary Parasitology, 107, 161–168. 10.1016/S0304-4017(02)00094-8Search in Google Scholar
Rahbari S., Nabian S., Shayan P. 2007. Primary report on distribution of tick fauna in Iran. Parasitology Research, 101, 175–17710.1007/s00436-007-0692-7Search in Google Scholar PubMed
Razmi G., Yaghfoori S. 2013. Molecular surveillance of Theileria ovis, Theileria lestoquardi and Theileria annulata infection in sheep and ixodid ticks in Iran. Onderstepoort Journal of Veterinary Research, 80, 635–64010.4102/ojvr.v80i1.635Search in Google Scholar PubMed
Robinson P.M. 1982. Theileria annulata and its transmission a review. Tropical Animal Health and Production, 14, 3–1210.1007/BF02281092Search in Google Scholar PubMed
Safapoor Dehkordi F., Parsaei P., Saberian S., Moshkelani S., Hajshafiei P., Hoseini S.R., Babaei M., Ghorbani M.N. 2012. Prevalence study of Theileria annulata by comparison of four diagnostic techniques in southwest Iran. Bulgarian Journal of Veterinary Medicine, 15, 123–130Search in Google Scholar
Schnittger L., Yin H., Jianxun L., Lugwing W., Shayan P., Rahbari S., Voss-Holtmann A., Ahmed J.S. 2000. Ribosomal smallsubunit RNA gene-sequence analysis of Theileria lestoquardi and a Theileria species highly pathogenic for small ruminants in China. Parasitology Research, 86, 352–35810.1007/s004360050680Search in Google Scholar PubMed
Sofizadeh A., Telmadarraiy Z., Rahnama A., Gorganli-Davaji A., Hosseini-Chegeni A. 2014. Hard tick species of livestock and their bioecology in Golestan province, north of Iran. Journal of Arthropod Borne Diseases, 8, 108–116Search in Google Scholar
Taha K.M., Salih D.A., Ali A.M., Omer R.A., El Hussein A.M. 2013. Naturally occurring infections of cattle with Theileria lestoquardi and sheep with Theileria annulata in the Sudan. Veterinary Parasitology, 191, 143–145. 10.1016/j.vetpar. 2012.08.003Search in Google Scholar
Tavassoli M., Tabatabaei M., Esmaeil Nejad B., Hasani Tabatabaei M., Najafabadi A., Pourseyed S.H. 2011. Detection of Theileria annulata by the PCR-RFLP in ticks (Acari, Ixodidae) collected. Acta Parasitologica, 56, 8–13. 10.2478/s11686-011-0001-6Search in Google Scholar
Zaeemi M., Haddadzadeh H., Khazraiinia P., Kazemi B., Bandehpou M. 2011. Identification of different Theileria species (Theileria lestoquardi, Theileria ovis, and Theileria annulata) in naturally infected sheep using nested PCR-RFLP. Parasitology Research, 108, 837–84310.1007/s00436-010-2119-0Search in Google Scholar PubMed
© 2016 W. Stefański Institute of Parasitology, PAS
Articles in the same Issue
- Review
- Internal parasitic fauna of elk (Alces alces) in Poland
- Research Article
- First report of mixed Entamoeba polecki (ST 1) and E. suis infection in piglets shedding abnormalfeces by histopathological and molecular surveys
- Research Article
- Genotyping of Cryptosporidium spp. in environmental water in Turkey
- Research Article
- Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites
- Research Article
- Characteristics, behaviors and association between Human African Trypanosomiasis and HIV seropositivity among volunteer blood donors in a semi-rural area: A survey from Kikwit, the Democratic Republic of Congo
- Research Article
- Comparison of indirect fluorescent antibody test and the modified agglutination test for the detection of Toxoplasma gondii antibodies in stray dogs from Southern Brazil
- Research Article
- Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India
- Research Article
- A new species of Trichodina Ehrenberg, 1830 (Ciliophora: Trichodinidae) from Rhamdia quelen (Siluriformes: Heptapteridae) and Gymnotus sp. (Teleostei: Gymnotidae) in Brazil
- Research Article
- Monocotyle luquei n. sp. (Monogenea: Monocotylidae), from the gills of diamond stingray Dasyatis dipterura (Jordan and Gilbert, 1880) (Myliobatiformes: Dasyatidae), in the South Pacific
- Research Article
- First record of Hammerschmidtiella diesingi (Hammerschmidt, 1838) (Oxyuridomorpha: Thelastomatidae) parasite of Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) in Japan, morphological and molecular characterization
- Research Article
- The genus Ixodes (Acari: Ixodidae) in China with three new record species
- Research Article
- First insights into indoor and outdoor Culicoides activity related to the risk period for Bluetongue virus transmission in Eastern Slovakia
- Research Article
- Detection of Theileria lestoquardi cross infection in cattle with clinical theileriosis in Iran
- Research Article
- Prevalence of Toxoplasma gondii and Neospora caninum in red foxes in Slovakia
- Research Article
- Epidemiological survey on Leishmania infection in red foxes (Vulpes vulpes) and hunting dogs sharing the same rural area in Southern Italy
- Research Article
- Fasciola hepatica infection in humans: overcoming problems for the diagnosis
- Research Article
- Isolation and molecular characterization of Acanthamoeba genotypes isolated from soil sources of public and recreational areas in Iran
- Research Article
- A genetic structure of novel population of Fascioloides magna from Poland, Podkarpackie Province, indicates an expanding second European natural focus of fascioloidosis
- Research Article
- Genotyping of clinical isolates of Acanthamoeba genus in Venezuela
- Research Article
- The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China
- Research Article
- Ocular symptoms reported by patients infested with Demodex mites
- Research Article
- Norway rat (Rattus norvegicus) as a potential reservoir for Echinococcus granulosus: A public health implication
- Research Article
- Redescription of Rhabdochona papuanensis (Nematoda: Thelazioidea), a parasite of rainbow fishes (Melanotaenia spp.); the first record of the species of Rhabdochona in Australia
- Research Article
- Development of a rapid and reliable assay for in vitro determination of compound cidality against the asexual stages of Plasmodium falciparum
- Research Article
- A case of persisting massive infection of Scomberomorus commerson, a commercially exploited scombrid fish, with Cybicola armatus (Copepoda: Siphonostomatoida: Pseudocycnidae)
- Research Article
- The PCR and nested PCR detection of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in Dermacentor reticulatus F. collected in a new location in Poland (Trzciel, Western Poland)
- Research Article
- Cutaneous leishmaniasis caused by Leishmania infantum in Southern Israel
- Research Note
- A morphological study of Diplodiscus subclavatus (Pallas, 1760) (Trematoda: Diplodiscidae) adults from the accidental host, Viviparus contectus (Millet, 1813) (Caenogastropoda: Viviparidae)
Articles in the same Issue
- Review
- Internal parasitic fauna of elk (Alces alces) in Poland
- Research Article
- First report of mixed Entamoeba polecki (ST 1) and E. suis infection in piglets shedding abnormalfeces by histopathological and molecular surveys
- Research Article
- Genotyping of Cryptosporidium spp. in environmental water in Turkey
- Research Article
- Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites
- Research Article
- Characteristics, behaviors and association between Human African Trypanosomiasis and HIV seropositivity among volunteer blood donors in a semi-rural area: A survey from Kikwit, the Democratic Republic of Congo
- Research Article
- Comparison of indirect fluorescent antibody test and the modified agglutination test for the detection of Toxoplasma gondii antibodies in stray dogs from Southern Brazil
- Research Article
- Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India
- Research Article
- A new species of Trichodina Ehrenberg, 1830 (Ciliophora: Trichodinidae) from Rhamdia quelen (Siluriformes: Heptapteridae) and Gymnotus sp. (Teleostei: Gymnotidae) in Brazil
- Research Article
- Monocotyle luquei n. sp. (Monogenea: Monocotylidae), from the gills of diamond stingray Dasyatis dipterura (Jordan and Gilbert, 1880) (Myliobatiformes: Dasyatidae), in the South Pacific
- Research Article
- First record of Hammerschmidtiella diesingi (Hammerschmidt, 1838) (Oxyuridomorpha: Thelastomatidae) parasite of Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) in Japan, morphological and molecular characterization
- Research Article
- The genus Ixodes (Acari: Ixodidae) in China with three new record species
- Research Article
- First insights into indoor and outdoor Culicoides activity related to the risk period for Bluetongue virus transmission in Eastern Slovakia
- Research Article
- Detection of Theileria lestoquardi cross infection in cattle with clinical theileriosis in Iran
- Research Article
- Prevalence of Toxoplasma gondii and Neospora caninum in red foxes in Slovakia
- Research Article
- Epidemiological survey on Leishmania infection in red foxes (Vulpes vulpes) and hunting dogs sharing the same rural area in Southern Italy
- Research Article
- Fasciola hepatica infection in humans: overcoming problems for the diagnosis
- Research Article
- Isolation and molecular characterization of Acanthamoeba genotypes isolated from soil sources of public and recreational areas in Iran
- Research Article
- A genetic structure of novel population of Fascioloides magna from Poland, Podkarpackie Province, indicates an expanding second European natural focus of fascioloidosis
- Research Article
- Genotyping of clinical isolates of Acanthamoeba genus in Venezuela
- Research Article
- The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China
- Research Article
- Ocular symptoms reported by patients infested with Demodex mites
- Research Article
- Norway rat (Rattus norvegicus) as a potential reservoir for Echinococcus granulosus: A public health implication
- Research Article
- Redescription of Rhabdochona papuanensis (Nematoda: Thelazioidea), a parasite of rainbow fishes (Melanotaenia spp.); the first record of the species of Rhabdochona in Australia
- Research Article
- Development of a rapid and reliable assay for in vitro determination of compound cidality against the asexual stages of Plasmodium falciparum
- Research Article
- A case of persisting massive infection of Scomberomorus commerson, a commercially exploited scombrid fish, with Cybicola armatus (Copepoda: Siphonostomatoida: Pseudocycnidae)
- Research Article
- The PCR and nested PCR detection of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in Dermacentor reticulatus F. collected in a new location in Poland (Trzciel, Western Poland)
- Research Article
- Cutaneous leishmaniasis caused by Leishmania infantum in Southern Israel
- Research Note
- A morphological study of Diplodiscus subclavatus (Pallas, 1760) (Trematoda: Diplodiscidae) adults from the accidental host, Viviparus contectus (Millet, 1813) (Caenogastropoda: Viviparidae)