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First Molecular Detection and Characterization of Tick-Borne Pathogens in Water Buffaloes in Bohol, Philippines

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First Molecular Detection and Characterization of Tick-Borne Pathogens in Water Buffaloes in Bohol, Philippines Ticks and Tick-borne Diseases 10 (2019) 815–821 Contents lists available at ScienceDirect Ticks and Tick-borne Diseases journal homepage: www.elsevier.com/locate/ttbdis Original article First molecular detection and characterization of tick-borne pathogens in T water buffaloes in Bohol, Philippines Eloiza May S. Galona, Paul Franck Adjou Moumounia, Rochelle Haidee D. Ybañeza, Aaron E. Ringoa, Artemis Efstratioua, Seung-Hun Leea, Mingming Liua, Huanping Guoa, Yang Gaoa, Jixu Lia, Caro B. Salcesb, Bon Christian A. Maurilloc, Damdinsuren Boldbaatard, ⁎ ⁎ Adrian P. Ybañeze,f, , Xuenan Xuana, a National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Hokkaido, Japan b Philippine Carabao Center at Ubay Stock Farm, Ubay, 6315, Bohol, Philippines c National Dairy Authority, Lomangog, Ubay, 6315, Bohol, Philippines d Institute of Veterinary Medicine, Zaisan, 17024, Ulaanbaatar, Mongolia e Institute of Molecular Parasitology and Vector-borne Diseases at Main Campus and College of Veterinary Medicine at Barili Campus, Cebu Technological University, Cor. M.J. Cuenco and R. Palma St., Cebu City, 6000, Cebu, Philippines f Regional Center for Molecular Diagnostics and Research and College of Science, University of the Philippines Cebu, Lahug, Cebu City, 6000, Cebu, Philippines ARTICLE INFO ABSTRACT Keywords: The water buffalo industry is a vital part of the Philippine livestock economy and is an essential contributor to Anaplasma the developing local dairy industry. Although relatively less susceptible to diseases, water buffaloes can still be Babesia infected and can act as reservoirs of tick-borne pathogens (TBPs). However, limited information is available Theileria regarding the prevalence of tick-borne infections in water buffaloes in the Philippines. This study was conducted Water buffalo to identify TBPs harbored by water buffaloes and to characterize these pathogens molecularly. One hundred Bohol province water buffalo blood samples collected from three areas in Bohol, Visayas region, Philippines were screened for Philippines various TBPs using pathogen-specific PCR assays. TBPs were detected in 46% of the samples (39% singly in- fected, 7% coinfected). The pathogens detected were Anaplasma marginale (29%), Babesia bovis (21%), and B. bigemina (3%). None of the blood samples were positive for Theileria annulata, T. orientalis, and B. ovata. A. marginale infection rates were significantly higher (37.5%) among water buffaloes aged ≤6 years (P=0.046) than those > 6 years old (18.2%) and was detected only in Bulgarian Murrah (36.1%) and US Murrah (25.9%) breeds. Phylogenetic analyses revealed that groEL sequences of A. marginale were 100% identical with isolates from the Philippines (Batangas and Cebu) and China. Two B. bigemina RAP-1a gene sequences were identical to each other and were homologous with previous isolates from Thailand, Indonesia, Uruguay, and the Philippines. Moreover, four B. bovis SBP-2 partial sequences obtained in this study had 92.4–99.7% identities. This study is the first molecular detection and characterization of A. marginale, B. bigemina and B. bovis in water buffaloes in the Visayas region, and the first molecular confirmation of B. bovis infection in water buffaloes in the country. The findings presented in this study may serve as baseline data for crafting effective tick-borne disease sur- veillance and prevention programs in Bohol and in the Philippines. 1. Introduction 2.88 million heads (Philippine Statistics Authority, 2017). Regarded as “farmers’ best friend”, 99.6% of these animals are raised by backyard The water buffalo (Bubalus bubalis) is an integral part of the live- farmers. Often reared together with cattle, it is conspicuous that water stock industry of the Philippines. It is mainly utilized as a source of draft buffaloes are more resistant and tolerant to diseases despite exposure to power for farmers, and as a source of meat and milk. Water buffaloes unsanitary environment and conditions favorable for disease develop- outnumber cattle population in the Philippines with an inventory of ment (National Research Council, 1981). More often, infected water ⁎ Co-corresponding authors at: (X. Xuan) National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Hokkaido, Japan; (A.P. Ybañez) Institute of Molecular Parasitology and Vector-borne Diseases at Main Campus and College of Veterinary Medicine at Barili Campus, Cebu Technological University, Cor. M.J. Cuenco and R. Palma St., Cebu City, 6000, Cebu, Philippines. E-mail addresses: [email protected] (A.P. Ybañez), [email protected] (X. Xuan). https://doi.org/10.1016/j.ttbdis.2019.03.016 Received 16 July 2018; Received in revised form 8 March 2019; Accepted 22 March 2019 Available online 23 March 2019 1877-959X/ © 2019 Elsevier GmbH. All rights reserved. E.M.S. Galon, et al. Ticks and Tick-borne Diseases 10 (2019) 815–821 buffaloes seldom show clinical signs. Thus, their potential as carrier 2.2. Sample population and area animals and pathogen reservoirs is frequently overlooked. Tick-borne diseases (TBDs) are known to cause adverse impacts on A total of 100 female dairy water buffaloes were sampled from three livestock health and impose considerable limitations in enhancing li- areas in Bohol, Philippines (Ubay, N = 92; Mabini, N = 7; Alicia, vestock productivity. In 1999, a model simulated by McLeod and N = 1) from December 2016 to May 2017 (Fig. 1). Selection of sam- Kristjanson estimated an annual cost of 0.6 million US$ for the pling locations was done based on convenience while animals were Philippine livestock industry due to losses and control measures for randomly chosen for sampling. Profile parameters such as breed (Bul- anaplasmosis and babesiosis (Bock et al., 2004). This highlights the garian Murrah, US Murrah, crossbred, Philippine Carabao), age groups significant risk and impact of TBDs to the livestock economy ofthe (≤6 years, > 6 years), body condition score (underweight, optimal, country. overweight) and presence or absence of ticks were recorded for ana- Anaplasma marginale, an obligate intraerythrocytic rickettsia, is the lysis. primary cause of bovine anaplasmosis and the most prevalent bovine vector-borne pathogen worldwide (Suarez and Noh, 2011). It can be 2.3. Blood sample collection and DNA extraction biologically transmitted by ticks, mechanically by biting flies and blood-contaminated fomites, and vertically through the movement of Five milliliters of whole blood were collected from each of 100 infected red blood cells across the placenta in the uterus (Aubry and water buffaloes in Bohol, Philippines. The blood samples were stored at Geale, 2011). Bovine anaplasmosis results in fever, weight loss, abor- −20 °C until DNA extraction. DNA from blood samples was extracted tion, lethargy, icterus, and sometimes, death in adult cattle (Kocan using QIAamp® DNA Blood Mini Kit (QIAGEN, Germany) according to et al., 2010). In water buffaloes, same clinical signs are observed but manufacturer’s instructions. diseased animals also manifest tachycardia, labored respiration, and pale mucous membranes (da Silva et al., 2014; Vatsya et al., 2013). 2.4. PCR assays for the screening of TBPs Although commonly infected, water buffaloes rarely develop the dis- ease and thus have been implicated as reservoir hosts (de la Fuente Oligonucleotide primers and PCR assays used in the screening of the et al., 2005; Kocan et al., 2010; Kuttler, 1984). samples are listed in Table 1. T. orientalis and B. ovata were screened Bovine babesiosis is a disease caused by several species of Babesia utilizing single PCR targeting the major piroplasm surface protein parasites transmitted by ticks (Bock et al., 2004; Uilenberg, 1995). (MPSP) (Ota et al., 2009) and apical membrane antigen (AMA)-1 Significant Babesia species known to infect bovines in Asia include B. (Sivakumar et al., 2012), respectively. Screening for B. bigemina, B. bovis, B. bigemina, B. orientalis, and B. ovata (Uilenberg, 2006). Babe- bovis, T. annulata, and A. marginale used nested PCR assays based on siosis is regarded as an important arthropod-borne disease in bovines rhoptry-associated protein (RAP)-1a (Terkawi et al., 2011), spherical because of the massive economic losses it inflicts on the global livestock body protein (SBP)-2 (Aboulaila et al., 2010), merozoite surface antigen industry (Bock et al., 2004; de Castro, 1997; Minjauw and McLeod, (TAMS)-1 (Martin-Sanchez et al., 1999), and A. marginale groEL 2003; Sackett and Holmes, 2006). (Ybañez et al., 2012) genes. The PCR mixture consisted of 4.9 μL of Members of the genus Theileria are tick-transmitted obligate proto- double-distilled water, 200 μM of dNTP solution mix (New England zoan parasites that infect a broad range of wild and domestic animals. Biolabs, U.S.A.), 1 μL of 10x Ex Taq buffer (Takara, Japan), 0.5 mM of They are characterized by the complex biology among various species each primer, 0.1 μL of Ex Taq polymerase (Takara, Japan) and 1 μL of (Mans et al., 2015). Theileria spp. are known for the millions of annual gDNA. Thermocycling conditions were performed for each pathogen as losses they bring to Asian and Sub-Saharan African agriculture sectors presented in Table 1. Double-distilled water was used as negative (Bishop et al., 2004). Notable species of importance in bovines are T. control and positive cattle DNA samples from a previous study (Ringo annulata, T. parva, and T. orientalis group (Sivakumar et al., 2014). et al., 2018) were used as positive controls. After electrophoresis and Epidemiological surveys on tick-borne pathogens (TBPs) using mo- staining with ethidium bromide, amplicons were visualized in 1.5% lecular detection techniques have been conducted in cattle in various agarose gel under UV light. parts of the Philippines (Belotindos et al., 2014; Foronda et al., 2010; Herrera et al., 2017; Ochirkhuu et al., 2015; Ybañez et al., 2014, 2013, 2.5. Cloning and sequencing of detected pathogens 2012; Yoshinari et al., 2012; Yu et al., 2013). To the best of the authors’ knowledge, only A.
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