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First Molecular Evidence of Babesia Caballi and Theileria Equi Infections in Horses in Cuba

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First Molecular Evidence of Babesia Caballi and Theileria Equi Infections in Horses in Cuba First molecular evidence of Babesia caballi and Theileria equi infections in horses in Cuba Adrian Alberto Díaz-Sánchez, Marcus Sandes Pires, Carlos Yrurzun Estrada, Ernesto Vega Cañizares, Sergio Luis del Castillo Domínguez, et al. Parasitology Research Founded as Zeitschrift für Parasitenkunde ISSN 0932-0113 Parasitol Res DOI 10.1007/s00436-018-6005-5 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag GmbH Germany, part of Springer Nature. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Parasitology Research https://doi.org/10.1007/s00436-018-6005-5 ORIGINAL PAPER First molecular evidence of Babesia caballi and Theileria equi infections in horses in Cuba Adrian Alberto Díaz-Sánchez1 & Marcus Sandes Pires2 & Carlos Yrurzun Estrada3 & Ernesto Vega Cañizares1 & Sergio Luis del Castillo Domínguez1 & Alejandro Cabezas-Cruz4 & Evelyn Lobo Rivero1 & Adivaldo Henrique da Fonseca2 & Carlos Luiz Massard2 & Belkis Corona-González1,5 Received: 3 April 2018 /Accepted: 4 July 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Equine piroplasmosis is a disease of Equidae, including horses, donkeys, mules, and zebras, caused by either Theileria equi or Babesia caballi. This disease represents a serious problem for the horse industry and its control is critical for the international trade of horses. The objective of the present study was to detect B. caballi and T. equi infections in horses reared in western Cuba. Blood samples from 100 horses were tested for the presence of piroplasms by using Giemsa-stained blood smears and nested PCR (nPCR) assays targeting merozoite antigen genes of B. caballi (bc48) and T. equi (ema-1). All animals were inspected for the detection of tick infestation and tick specimens were collected for species identification. Erythrocyte inclusions were observed in 13 (13%) of the analyzed samples. nPCR analysis showed that 25 (25%) samples were positive for B. caballi, 73 (73%) for T. equi, and 20 (20%) showed dual infections. Only one tick species was found infesting horses, Dermacentor nitens.Inaddition, three nearly full-length sequences of T. equi 18S rRNA gene were obtained and subjected to phylogenetic analyses. This study reports a high prevalence of T. equi and B. caballi single and coinfections in horses in western Cuba. Molecular analysis of the 18S rRNA gene of T. equi suggested that different genotypes of this hemoparasite circulate in Cuba. To the best of our knowledge, this is the first report describing the molecular detection of B. caballi and T. equi in horses in Cuba. Keywords Equine piroplasmosis . Babesia caballi . Theileria equi . nPCR . 18S rRNA Section Editor: Neil Bruce Chilton Introduction * Belkis Corona-González Equine piroplasmosis is a vector-borne disease affecting hors- [email protected] es and other equids (e.g., donkeys, mules, and zebras). This Adrian Alberto Díaz-Sánchez disease is caused by two obligate intraerythrocytic [email protected] hemoprotozoans, Theileria equi and Babesia caballi (Apicomplexa: Piroplasmida), which belong to the families 1 National Center for Animal and Plant Health (CENSA), Carretera de Babesiidae and Theileriidae, respectively (Mehlhorn and Tapaste y Autopista Nacional, km 22 1/2, 32700 San José de las Schein 1998). These parasites are widespread in tropical, sub- Lajas, Mayabeque, Cuba tropical, and some temperate regions, where tick vectors are 2 Department of Epidemiology and Public Health, Federal Rural present. Due to its morbidity and mortality, this disease has a University of Rio de Janeiro (UFRRJ), BR 465, km 7, Seropédica, Rio de Janeiro 23890-000, Brazil negative impact on the equid industry (Knowles Jr. 1996). The distribution of equine piroplasmosis is associated with the 3 Department of Animal Prevention, Veterinary Medicine College, Agrarian University of Habana (UNAH), Carretera de Tapaste y presence of competent vectors, mainly ixodid ticks of the gen- Autopista Nacional, km 23 1/2, San José de las Lajas, Mayabeque, era Dermacentor, Rhipicephalus, Hyalomma, Amblyomma, Cuba and Haemaphysalis (Scoles and Ueti 2015). Currently, 12 4 UMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d’Alfort, and 11 tick species are recognized as vectors of T. equi and Université Paris-Est, 94700 Maisons-Alfort, France B. caballi, respectively. However, the disease can be also 5 Animal Health Division, National Center for Animal and Plant transmitted through infected blood transfusion, as well as con- Health (CENSA), Carretera de Tapaste y Autopista Nacional, km 22 taminated syringes and surgical instruments (Short et al. 1/2, 32700 San José de las Lajas, Mayabeque, Cuba Author's personal copy Parasitol Res 2012). Transplacental transmission was also reported in increasingly important and plays a critical role in maintaining T. equi (Santetal.2016). the international market open to the horse industry. Per-acute, acute, sub-acute, and chronic forms of equine Although, the presence of equine piroplasmosis within the piroplasmosis have been described. The clinical signs of the Caribbean region is still controversial, the disease has been disease are diverse including anorexia, pyrexia, edema, hemo- reported on most islands, including Cuba (Asgarali et al. globinuria, anemia, intravascular hemolysis, jaundice, re- 2007;Oliveretal.1985; Zhang et al. 2015). However, limited duced work efficiency, weight loss, abortion in mares, and information is available on the status of this disease in equine death can occur in the acute phase of the infection (Zobba et herds of Cuba. The study on equine piroplasmosis in Cuba al. 2008). In general, infection with T. equi exhibits a more conducted by Salabarria et al. (1982) was largely based on severe clinical disease than B. caballi, although the signs and conventional blood smear examination and serological tests, severity can vary significantly from one region to another which as previously mentioned, are not the most suitable tools (Wise et al. 2013). Infection recovery is possible, but recov- for epidemiological assessments. Therefore, the present study ered animals may become carriers for long periods. The horses was aimed at detecting B. caballi and T. equi infections in that recover from the infection with T. equi may remain life- horses reared in western Cuba using microscopic and molec- long carriers, whereas infection by B. caballi is generally self- ular methods. limited up to 4 years (Rothschild 2013). B. caballi and T. equi infections can be diagnosed by dif- ferent methods including conventional parasitological tech- Materials and methods niques (i.e., examination of stained thin blood smears) and serological and molecular techniques (Wise et al. 2013). The Study area utility of the microscopic examination of stained blood smears is limited because of its poor sensitivity, particularly in carrier The present study was performed on local horses of four prov- animals during chronic infection due to low parasitemia inces of the western region of Cuba. The island climate is (Malekifard et al. 2014). Several serological methods, such tropical and humid with two distinct climatic periods, a dry as the complement fixation technique (CFT), the indirect fluo- season from November to April and a warmer and rainy sea- rescence antibody test (IFAT), and the competitive inhibition son from May to October. In the dry season, the average tem- enzyme-linked immunosorbent assay (cELISA), are also perature varies between 15 and 26 °C, while temperatures available for the detection of parasite-specific antibodies in typically range between 22 and 32 °C in the wet season. the infected horse sera (Asgarali et al. 2007). Currently, the The horses studied were from six municipalities of the cELISA is considered by the World Organization for Animal provinces Mayabeque (San José de las Lajas, Jaruco, and Health (OIE) as the preferred test for international horse trade Madruga), Artemisa (Artemisa), Havana (Boyeros), and (OIE 2014). However, these serological assays are time con- Matanzas (Unión de Reyes) (Fig. 1). suming and labor intensive and cannot differentiate between current and previous infections due to persistence of antibod- ies after the infections were resolved (Wise et al. 2013). In Sample collection contrast, for the diagnosis of active infection, molecular methods are more sensitive than other diagnostic techniques One hundred blood samples were randomly taken from horses to detect carrier animals. Polymerase chain reaction (PCR) of different herds from September 2014 to August 2015. assays based on ribosomal 18S rRNA, B. caballi 48-kDa mer- Approximately 3–4 ml of blood was collected from each an- ozoite rhoptry-associated protein 1 (bc48), and T. equi mero- imal by puncturing the jugular vein using vacutainer zoite antigen 1 (ema-1) genes are routinely used to detect collecting tubes containing EDTA (BD Vacutainer®), and piroplasmosis
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