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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Vet. Sci.</journal-id>
<journal-title>Frontiers in Veterinary Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Vet. Sci.</abbrev-journal-title>
<issn pub-type="epub">2297-1769</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
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<article-meta>
<article-id pub-id-type="doi">10.3389/fvets.2024.1359974</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Veterinary Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Survey of tick-borne pathogens in grazing horses in Kyrgyzstan: phylogenetic analysis, genetic diversity, and prevalence of <italic>Theileria equi</italic></article-title>
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<name><surname>Altay</surname> <given-names>Kursat</given-names></name>
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<xref ref-type="corresp" rid="c001"><sup>&#x002A;</sup></xref>
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<name><surname>Erol</surname> <given-names>Ufuk</given-names></name>
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<name><surname>Sahin</surname> <given-names>Omer Faruk</given-names></name>
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<name><surname>Ulucesme</surname> <given-names>Mehmet Can</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
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<name><surname>Aytmirzakizi</surname> <given-names>Ayperi</given-names></name>
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<name><surname>Aktas</surname> <given-names>Munir</given-names></name>
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<aff id="aff1"><sup>1</sup><institution>Department of Parasitology, Faculty of Veterinary Medicine, Sivas Cumhuriyet University</institution>, <addr-line>Sivas</addr-line>, <country>T&#x00FC;rkiye</country></aff>
<aff id="aff2"><sup>2</sup><institution>Department of Parasitology, Faculty of Veterinary Medicine, Firat University</institution>, <addr-line>Elazig</addr-line>, <country>T&#x00FC;rkiye</country></aff>
<aff id="aff3"><sup>3</sup><institution>Faculty of Veterinary Medicine, Kyrgyz-Turkish Manas University</institution>, <addr-line>Bishkek</addr-line>, <country>Kyrgyzstan</country></aff>
<author-notes>
<fn fn-type="edited-by" id="fn0007"><p>Edited by: Mingming Liu, Hubei University of Arts and Science, China</p></fn>
<fn fn-type="edited-by" id="fn0008"><p>Reviewed by: Mohammed Hocine Benaissa, Scientific and Technical Research Center on Arid Regions (CRSTRA), Algeria</p><p>Jixu Li, Qinghai University, China</p></fn>
<corresp id="c001">&#x002A;Correspondence: Kursat Altay, <email>kaltay@cumhuriyet.edu.tr</email></corresp>
<fn fn-type="other" id="fn0001"><p><sup>&#x2020;</sup>ORCID: Kursat Altay, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0002-5288-1239">https://orcid.org/0000-0002-5288-1239</ext-link></p><p>Ufuk Erol, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0002-6766-1335">https://orcid.org/0000-0002-6766-1335</ext-link></p><p>Omer Faruk Sahin, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0002-3230-504X">https://orcid.org/0000-0002-3230-504X</ext-link></p><p>Mehmet Can Ulucesme, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0002-4492-143X">https://orcid.org/0000-0002-4492-143X</ext-link></p><p>Ayperi Aytmirzakizi, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0003-3363-0941">https://orcid.org/0000-0003-3363-0941</ext-link></p><p>Munir Aktas, <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0002-3188-8757">https://orcid.org/0000-0002-3188-8757</ext-link></p></fn>
</author-notes>
<pub-date pub-type="epub">
<day>29</day>
<month>04</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>11</volume>
<elocation-id>1359974</elocation-id>
<history>
<date date-type="received">
<day>22</day>
<month>12</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>08</day>
<month>04</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x00A9; 2024 Altay, Erol, Sahin, Ulucesme, Aytmirzakizi and Aktas.</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Altay, Erol, Sahin, Ulucesme, Aytmirzakizi and Aktas</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<sec>
<title>Introduction</title>
<p>Tick-borne pathogens (TBP) are an important group of organisms that can affect animals and humans all over the world. Equine piroplasmosis (EP), caused by <italic>Theileria equi</italic> and <italic>Babesia caballi</italic>, is considered one of the most important tick-borne diseases and can cause significant clinical symptoms and mortality in horses. Moreover, EP plays a restrictive role in international horse traditions and transportation. Although these species can cause similar symptoms, there are different 18S rRNA genotypes of <italic>T. equi</italic> (five genotypes) and <italic>B. caballi</italic> (three genotypes). Besides piroplasma species, <italic>Anaplasma</italic> and hemotropic mycoplasmas (HM) are known as other important tick-borne pathogens reported in horses.</p>
</sec>
<sec>
<title>Methods</title>
<p>In this study, we investigated the presence, prevalence, genetic diversity, and phylogenetic analyses of TBPs using PCRs and DNA sequencing in grazing horses in Kyrgyzstan. For these purposes, a total of 311 blood samples were collected from Chuy, Issyk-Kul, Naryn, Osh, Talas, and Jalal-Abad.</p>
</sec>
<sec>
<title>Results</title>
<p>DNA amplification of TBP revealed that 23 (7.40%) out of 311 samples were found to be positive for <italic>T. equi</italic>. However, <italic>B. caballi</italic>, HM, <italic>A. phagocytophilum</italic>, and <italic>A. capra</italic> were not detected in this study. The infection rate of <italic>T. equi</italic> was higher in males (8.11%) than in females (6.35%) (<italic>p</italic>=0.2880) and in those older than 5 years (9.02%) than in the 1-4 age group (6.35%) (<italic>p</italic>=0.1950). Phylogenetic analysis of 18S <italic>rRNA</italic> revealed that A and E genotypes of <italic>T. equi</italic> have circulated in grazing horses in Kyrgyzstan.</p>
</sec>
<sec>
<title>Discussion</title>
<p>Information about the genetic diversity of <italic>T. equi</italic> is important for understanding the population dynamics of the species and developing effective control strategies against this pathogen. This is the first molecular investigation of <italic>A. capra</italic> in horses in Kyrgyzstan. Although this pathogen has been detected in different hosts in Kyrgyzstan, it was not detected in this study. However, considering the wide host spectrum of <italic>A. capra</italic>, it is thought that more large-scale studies are needed to understand the effect of horses on the epidemiology of this pathogen.</p>
</sec>
</abstract>
<kwd-group>
<kwd>tick borne pathogens</kwd>
<kwd>Theileria equi</kwd>
<kwd>genotypes</kwd>
<kwd>horse</kwd>
<kwd>Kyrgyzstan</kwd>
</kwd-group>
<counts>
<fig-count count="2"/>
<table-count count="3"/>
<equation-count count="0"/>
<ref-count count="80"/>
<page-count count="9"/>
<word-count count="7415"/>
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<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Parasitology</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec sec-type="intro" id="sec1">
<label>1</label>
<title>Introduction</title>
<p>Tick-borne pathogens (TBP) are an important group of organisms that can affect animal and human health all over the World (<xref ref-type="bibr" rid="ref1">1</xref>). Equine piroplasmosis (EP), equine anaplasmosis (formerly Equine Granulocytic Ehrlichiosis), and hemotropic mycoplasmas (HM) are the main TBPs of horses (<xref ref-type="bibr" rid="ref2 ref3 ref4">2&#x2013;4</xref>). EP is caused by <italic>Theileria equi</italic> (formerly <italic>Babesia equi</italic>), <italic>Babesia caballi</italic>, and the recently described <italic>T. haneyi</italic>. The disease is observed in horses, mules, donkeys, and zebras (<xref ref-type="bibr" rid="ref2">2</xref>, <xref ref-type="bibr" rid="ref5">5</xref>, <xref ref-type="bibr" rid="ref6">6</xref>). EP is a global disease and a few countries such as Australia, Canada, Great Britain, Ireland, Japan, and New Zealand have EP-free status (<xref ref-type="bibr" rid="ref5">5</xref>, <xref ref-type="bibr" rid="ref6">6</xref>). Ixodid ticks such as <italic>Dermacentor</italic>, <italic>Hyalomma</italic>, and <italic>Rhipicephalus</italic> are the biological vectors of EP, and it is mainly transmitted by these vectors. In addition, it has been reported that it is transmitted through contaminated needles, surgical operations, blood transfusion, and transplacental (<xref ref-type="bibr" rid="ref2">2</xref>, <xref ref-type="bibr" rid="ref6">6</xref>, <xref ref-type="bibr" rid="ref7">7</xref>). EP exhibits a clinical course ranging from subclinical to acute. <italic>Theileria equi</italic> causes more severe clinical disease than <italic>B. caballi.</italic> The clinical signs of EP are fever, anemia, jaundice, and hemoglobinuria (<xref ref-type="bibr" rid="ref6">6</xref>, <xref ref-type="bibr" rid="ref8">8</xref>). The mortality can reach up to 50% in <italic>T. equi</italic> infections, while 10% in <italic>B. caballi</italic> infections (<xref ref-type="bibr" rid="ref6">6</xref>, <xref ref-type="bibr" rid="ref8">8</xref>). Horses that recover from the disease remain carriers for a long time. While in <italic>T. equi</italic> the carrier period lasts lifelong, in <italic>B. caballi</italic> this period is about 4&#x2009;years (<xref ref-type="bibr" rid="ref9">9</xref>). EP causes significant economic losses in the equine industry worldwide and even has a restrictive effect on international horse movements (<xref ref-type="bibr" rid="ref2">2</xref>, <xref ref-type="bibr" rid="ref6">6</xref>).</p>
<p>Equine anaplasmosis (formerly Equine Granulocytic Ehrlichiosis) is a tick-borne disease of horses caused by <italic>Anaplasma phagocytophilum</italic> (formerly <italic>Ehrlichia equi</italic>). It has a very wide host spectrum and infects horses, cattle, sheep, goats dogs, cats, and humans (<xref ref-type="bibr" rid="ref10">10</xref>). The clinical signs occur mostly in adult horses, which include fever, anorexia, depression, reluctance to move, limb edema, petechiation, and icterus (<xref ref-type="bibr" rid="ref10 ref11 ref12">10&#x2013;12</xref>). <italic>Anaplasma capra</italic> is discovered for the first time in goats from China in 2012 (<xref ref-type="bibr" rid="ref13">13</xref>). In the short time so far, <italic>A. capra</italic> has been detected in many different countries including Kyrgyzstan from three continents (Africa, Asia, and Europe) (<xref ref-type="bibr" rid="ref14 ref15 ref16 ref17 ref18 ref19 ref20 ref21 ref22 ref23 ref24 ref25 ref26">14&#x2013;26</xref>). The studies show that the <italic>A. capra</italic> can infect a wide range of host groups including sheep, goats, cattle, water buffaloes, dogs, wild animals (e.g., deer, takin, Persian onegar, muntjac, serow), and humans (<xref ref-type="bibr" rid="ref13 ref14 ref15 ref16 ref17 ref18">13&#x2013;18</xref>, <xref ref-type="bibr" rid="ref20 ref21 ref22 ref23 ref24 ref25">20&#x2013;25</xref>). Additionally, it was detected in ticks (<xref ref-type="bibr" rid="ref19">19</xref>). There is no information regarding the presence of <italic>A. capra</italic> in horses. However, <italic>A. capra</italic> has been detected in wild onegars (<italic>Equus hemionus onager</italic>) in Iran (<xref ref-type="bibr" rid="ref24">24</xref>).</p>
<p>Hemotropic mycoplasmas or hemoplasmas refers to the infection caused by small, cell wall-less Gram-negative bacteria (<italic>Mycoplasma</italic> spp., class <italic>Mollicutes</italic>) that attach to the surface of red blood cells, formerly known as eperythrozoonosis and haemobartonellosis. These species infect many animal species (<xref ref-type="bibr" rid="ref26">26</xref>). The diseases may be transmitted by arthropod vectors such as ticks, lice, flies, and mosquitoes. Additionally, the disease can be transmitted through blood transfusion, contaminated needles or surgical equipment, and vertically (<xref ref-type="bibr" rid="ref26">26</xref>). Information about HM in horses is scarce. The disease was first detected in horses by microscopic examination of blood smears in Nigeria in 1978 (<xref ref-type="bibr" rid="ref4">4</xref>). In 2010, the first molecular diagnosis of the disease in horses was made and the species detected in horses from Germany were determined closely related to <italic>Mycoplasma haemofelis</italic> and <italic>Candidatus Mycoplasma haemobos</italic> (<xref ref-type="bibr" rid="ref27">27</xref>). Apart from Germany (<xref ref-type="bibr" rid="ref27">27</xref>) studies on molecular basis determination of HM in horses were conducted in Iran (<xref ref-type="bibr" rid="ref28">28</xref>), Nigeria (<xref ref-type="bibr" rid="ref29">29</xref>), and Brazil (<xref ref-type="bibr" rid="ref30">30</xref>).</p>
<p>To date, no record of equine-TBPs has been found in the literature in Kyrgyzstan. Recently, it has been reported first molecular presence and prevalence of the important TBPs such as canine and bovine hemotropic mycoplasma species (<xref ref-type="bibr" rid="ref31">31</xref>, <xref ref-type="bibr" rid="ref32">32</xref>), <italic>B. vogeli, B. vulpes</italic> in dogs (<xref ref-type="bibr" rid="ref33">33</xref>), <italic>A. centrale, A. capra</italic>, <italic>A. phagocytophilum</italic>-like 1, <italic>B. major, T. annulata,</italic> and <italic>T. orientalis</italic> in cattle (<xref ref-type="bibr" rid="ref14">14</xref>, <xref ref-type="bibr" rid="ref15">15</xref>, <xref ref-type="bibr" rid="ref34">34</xref>, <xref ref-type="bibr" rid="ref35">35</xref>), <italic>A. ovis, A. capra</italic>, <italic>and A. phagocytophilum</italic>-like 1 in sheep (<xref ref-type="bibr" rid="ref36">36</xref>) in Kyrgyzstan. In this study, we aimed to survey of TBPs (EP, HM, <italic>Anaplasma phagocytophilum,</italic> and <italic>Anaplasma capra</italic>) in grazing horses in Kyrgyzstan and to detect the genetic diversity of the pathogens.</p>
</sec>
<sec sec-type="materials|methods" id="sec2">
<label>2</label>
<title>Materials and methods</title>
<sec id="sec3">
<label>2.1</label>
<title>Study area, collection of blood samples, and DNA extraction</title>
<p>The Republic of Kyrgyzstan is a Central Asia country bordered by Uzbekistan to the west, China to the east and southeast, Tajikistan to the south, and Kazakhstan to the north. The country is generally covered with high mountains and has a continental climate, with hot summers and cold winters. While the summers in low-altitude settlements can get quite hot, the high mountains remain colder even in the hottest months. It consists of seven geographical regions (Talas, Naryn, Batken, Issyk-Kul, Chuy, Osh, and Jalal-Abad) (<xref ref-type="fig" rid="fig1">Figure 1</xref>) (<xref ref-type="bibr" rid="ref37">37</xref>).</p>
<fig position="float" id="fig1">
<label>Figure 1</label>
<caption>
<p>Location of Kyrgyzstan on the world map (Yellow). Neighbors and geographical regions of Kyrgyzstan. Sampling regions were shown with circles.</p>
</caption>
<graphic xlink:href="fvets-11-1359974-g001.tif"/>
</fig>
<p>The blood samples were collected from 311 grazing horses from 35 flocks in 21 settlements in 6 geographical regions (Chuy, Osh, Naryn, Talas, Jalal-Abad, and Issyk-Kul) of Kyrgyzstan (<xref ref-type="fig" rid="fig1">Figure 1</xref>) between March 2022 and July 2023. Horse flocks in the settlements selected for the study and the animals from which blood was obtained in the flocks were randomly selected. The age and gender of the animals were recorded (<xref ref-type="table" rid="tab1">Table 1</xref>). There were not any clinical signs on horses at first examination and they were recorded as healthy.</p>
<table-wrap position="float" id="tab1">
<label>Table 1</label>
<caption>
<p>The numbers of blood samples by location, age and gender.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left" valign="top" rowspan="2">Locations</th>
<th align="center" valign="top" colspan="2">Age (year)</th>
<th align="center" valign="top" colspan="2">Gender</th>
<th align="center" valign="top" rowspan="2">Total</th>
</tr>
<tr>
<th align="center" valign="top">1&#x2013;4</th>
<th align="center" valign="top">5&#x2264;</th>
<th align="center" valign="top">Male</th>
<th align="center" valign="top">Female</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="top">Chuy</td>
<td align="center" valign="top">102</td>
<td align="center" valign="top">86</td>
<td align="center" valign="top">124</td>
<td align="center" valign="top">64</td>
<td align="center" valign="top">188</td>
</tr>
<tr>
<td align="left" valign="top">Issyk-Kul</td>
<td align="center" valign="top">30</td>
<td align="center" valign="top">6</td>
<td align="center" valign="top">19</td>
<td align="center" valign="top">17</td>
<td align="center" valign="top">36</td>
</tr>
<tr>
<td align="left" valign="top">Naryn</td>
<td align="center" valign="top">20</td>
<td align="center" valign="top">10</td>
<td align="center" valign="top">12</td>
<td align="center" valign="top">18</td>
<td align="center" valign="top">30</td>
</tr>
<tr>
<td align="left" valign="top">Osh</td>
<td align="center" valign="top">15</td>
<td align="center" valign="top">7</td>
<td align="center" valign="top">12</td>
<td align="center" valign="top">10</td>
<td align="center" valign="top">22</td>
</tr>
<tr>
<td align="left" valign="top">Talas</td>
<td align="center" valign="top">13</td>
<td align="center" valign="top">7</td>
<td align="center" valign="top">10</td>
<td align="center" valign="top">10</td>
<td align="center" valign="top">20</td>
</tr>
<tr>
<td align="left" valign="top">Jalal-Abad</td>
<td align="center" valign="top">9</td>
<td align="center" valign="top">6</td>
<td align="center" valign="top">8</td>
<td align="center" valign="top">7</td>
<td align="center" valign="top">15</td>
</tr>
<tr>
<td align="left" valign="top">Total</td>
<td align="center" valign="top">189</td>
<td align="center" valign="top">122</td>
<td align="center" valign="top">185</td>
<td align="center" valign="top">126</td>
<td align="center" valign="top">311</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>The total genomic DNAs were obtained from blood samples using a commercial DNA isolation kit (GeneAll Exgene<sup>&#x2122;</sup> Clinic SV kit, 108&#x2013;152, GeneAll<sup>&#x00AE;</sup>, Seoul, South Korea). These gDNA samples were sored &#x2212;20&#x00B0;C until use.</p>
</sec>
<sec id="sec4">
<label>2.2</label>
<title>Survey of equine piroplasmosis, hemotropic mycoplasmas, <italic>Anaplasma phagocytophilum</italic>, and <italic>Anaplasma capra</italic> by polymerase chain reaction</title>
<p>The four different polymerase chain reaction (PCR) were used for the survey of equine piroplasmosis (EP), hemotropic mycoplasmas (HM), <italic>Anaplasma phagocytophilum,</italic> and <italic>Anaplasma capra</italic> DNAs in the study. A nested PCR was carried out for the amplification of <italic>Theileria</italic> spp. and <italic>Babesia</italic> spp. <italic>18S rRNA</italic> gene. First, 1,600&#x2009;bp of the <italic>18S rRNA</italic> gene of <italic>Theileria</italic> spp. and <italic>Babesia</italic> spp. was amplified by PCR from the samples with Nbab-1F and Nbab-1R primers (<xref ref-type="bibr" rid="ref38">38</xref>). In nested PCR using these PCR products as templates, ~500&#x2009;bp fragments of the same gene was amplified with BJ1 and BN2 primers (<xref ref-type="bibr" rid="ref39">39</xref>). To survey of HM species in the samples, the primers amplifying 192&#x2009;bp fragments of <italic>16S rRNA</italic> gene were used in the PCR (<xref ref-type="bibr" rid="ref40">40</xref>). To survey of <italic>A. phagocytophilum</italic> in the samples SSAP2f and SSAP2r primers amplifying 641/642&#x2009;bp fragments of <italic>16S rRNA</italic> gene were used in the PCR (<xref ref-type="bibr" rid="ref41">41</xref>). <italic>Anaplasma capra</italic> was researched by a nested PCR in the samples. First, 1,031&#x2009;bp fragments of the <italic>gltA</italic> gene (<xref ref-type="bibr" rid="ref20">20</xref>) and then 594&#x2009;bp fragments of the same gene (<xref ref-type="bibr" rid="ref19">19</xref>) were amplified by PCR. The detailed information about PCRs and the primers is presented in <xref ref-type="table" rid="tab2">Table 2</xref>.</p>
<table-wrap position="float" id="tab2">
<label>Table 2</label>
<caption>
<p>The characteristics of the primers used in this study.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left" valign="top">Species</th>
<th align="left" valign="top">Primer name</th>
<th align="left" valign="top">Primer sequence (5&#x2032;-3&#x2032;)</th>
<th align="center" valign="top">Target gene</th>
<th align="center" valign="top">Amplicon size (bp)</th>
<th align="center" valign="top">Annealing temperature (&#x00B0;C)</th>
<th align="left" valign="top">References</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="top" rowspan="4"><italic>EP</italic> (<italic>Theileria</italic> spp. and <italic>Babesia</italic> spp.)</td>
<td align="left" valign="top">&#x002A;Nbab_1F</td>
<td align="left" valign="top">AAGCCATGCATGTCTAAGTATAAGCTTTT</td>
<td align="center" valign="top" rowspan="4"><italic>18S rRNA</italic></td>
<td align="center" valign="top" rowspan="2">1,600</td>
<td align="center" valign="top" rowspan="2">56</td>
<td align="left" valign="top" rowspan="2">Oosthuizen et al. (<xref ref-type="bibr" rid="ref38">38</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">&#x002A;Nbab_1R</td>
<td align="left" valign="top">CTTCTCCTTCCTTTAAGTGATAAGGTTCAC</td>
</tr>
<tr>
<td align="left" valign="top">&#x002A;&#x002A;BJ1</td>
<td align="left" valign="top">GTCTTGTAATTGGAATGATGG</td>
<td align="center" valign="top" rowspan="2">~500</td>
<td align="center" valign="top" rowspan="2">56</td>
<td align="left" valign="top" rowspan="2">Casati et al. (<xref ref-type="bibr" rid="ref39">39</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">&#x002A;&#x002A;BN2</td>
<td align="left" valign="top">TAGTTTATGGTTAGGACTACG</td>
</tr>
<tr>
<td align="left" valign="top" rowspan="2">HM</td>
<td align="left" valign="top">Forwad</td>
<td align="left" valign="top">ACGAAAGTCTGATGGAGCAATA</td>
<td align="center" valign="top" rowspan="2"><italic>16S rRNA</italic></td>
<td align="center" valign="top" rowspan="2">192</td>
<td align="center" valign="top" rowspan="2">52</td>
<td align="left" valign="top" rowspan="2">Jensen et al. (<xref ref-type="bibr" rid="ref40">40</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">Reverse</td>
<td align="left" valign="top">ACGCCCAATAAATCCG(A/G)ATAAT</td>
</tr>
<tr>
<td align="left" valign="top" rowspan="2"><italic>A. phagocytophilum</italic></td>
<td align="left" valign="top">SSAP2f</td>
<td align="left" valign="top">GCTGAATGTGGGGATAATTTAT</td>
<td align="center" valign="top" rowspan="2"><italic>16S rRNA</italic></td>
<td align="center" valign="top" rowspan="2">641&#x2013;642</td>
<td align="center" valign="top" rowspan="2">54</td>
<td align="left" valign="top" rowspan="2">Kawahara et al. (<xref ref-type="bibr" rid="ref41">41</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">SSAP2r</td>
<td align="left" valign="top">ATGGCTGCTTCCTTTCGGTTA</td>
</tr>
<tr>
<td align="left" valign="top" rowspan="4"><italic>A.capra</italic></td>
<td align="left" valign="top">Outer-f</td>
<td align="left" valign="top">GCGATTTTAGAGTGYGGAGATTG</td>
<td align="center" valign="top" rowspan="4"><italic>gltA</italic></td>
<td align="center" valign="top" rowspan="2">1,031</td>
<td align="center" valign="top" rowspan="2">50</td>
<td align="left" valign="top" rowspan="2">Li et al. (<xref ref-type="bibr" rid="ref20">20</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">Outer-r</td>
<td align="left" valign="top">TACAATACCGGAGTAAAAGTCAA</td>
</tr>
<tr>
<td align="left" valign="top">Inner-f</td>
<td align="left" valign="top">TCATCTCCTGTTGCACGGTGCCC</td>
<td align="center" valign="top" rowspan="2">594</td>
<td align="center" valign="top" rowspan="2">57</td>
<td align="left" valign="top" rowspan="2">Yang et al. (<xref ref-type="bibr" rid="ref19">19</xref>)</td>
</tr>
<tr>
<td align="left" valign="top">Inner-r</td>
<td align="left" valign="top">CTCTGAATGAACATGCCCACCCT</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>EP, equine prioplasmosis, HM, hemotropic mycoplasmas, &#x002A;: outer primers, &#x002A;&#x002A;: inner primers.</p>
</table-wrap-foot>
</table-wrap>
<p>The PCR assays were performed as described before (<xref ref-type="bibr" rid="ref19">19</xref>, <xref ref-type="bibr" rid="ref20">20</xref>, <xref ref-type="bibr" rid="ref38 ref39 ref40 ref41">38&#x2013;41</xref>), and the genomic DNA of <italic>B. vogeli</italic> (Accession number: OR116199) (<xref ref-type="bibr" rid="ref33">33</xref>), <italic>A. phagocytophilum</italic> (Accession number: OP828919) (<xref ref-type="bibr" rid="ref42">42</xref>), <italic>A. capra</italic> (Accession number: ON783818) (<xref ref-type="bibr" rid="ref22">22</xref>), and <italic>M. wenyonii</italic> (Accession number: OM468183) (<xref ref-type="bibr" rid="ref43">43</xref>) were used as the positive controls, and DNase-RNase-free sterile water (Cat No.: 129114, Qiagen<sup>&#x00AE;</sup>, Germany) was used as the negative control in the PCRs.</p>
<p>PCR products were loaded on 1.5% agarose gel containing ethidium bromide and visualized under a UV transilluminator. The DNA extraction, PCR, and gel electrophoresis were performed in separate compartments of the laboratory to minimize the risk of contamination.</p>
</sec>
<sec id="sec5">
<label>2.3</label>
<title>Sequencing and phylogenetic analysis</title>
<p>All positive samples obtained in the study were sequenced using the primers listed in <xref ref-type="table" rid="tab1">Table 1</xref>.</p>
<p>The amplicons were purified from agarose gel using a commercial gel extraction kit (PCR Clean-Up &#x0026; Gel Extraction Kit, GeneDireX<sup>&#x00AE;</sup>, Cat.No.: NA006-0300). The purified products were sent to bidirectionally sequence (ABI 3730XL analyzer, Applied Biosystems, Foster City, CA). The BigDye Terminator v3.1&#x2009;Cycle Sequencing Kit was used in the reactions (Applied Biosystems, Foster City, CA).</p>
<p>The obtained sequences were aligned with each other with the MUSCLE algorithm of MEGA-11 software (<xref ref-type="bibr" rid="ref44">44</xref>), and consensus sequences were constructed. Accession numbers were obtained by submitting them to GenBank. Phylogenetic analyses of gene sequences identified in this study were performed and genotypes of the <italic>T. equi</italic> were determined.</p>
<p>The best-fit model for maximum likelihood was determined as the TN93&#x2009;+&#x2009;G parameter model (<xref ref-type="bibr" rid="ref45">45</xref>) using the Find Best-Fit Substitution Model in MEGA-11 (<xref ref-type="bibr" rid="ref44">44</xref>). The phylogenetic trees were created using maximum likelihood analysis in Mega 11 (<xref ref-type="bibr" rid="ref44">44</xref>) (<xref ref-type="fig" rid="fig2">Figure 2</xref>).</p>
<fig position="float" id="fig2">
<label>Figure 2</label>
<caption>
<p>Phylogenetic trees according to <italic>18S rRNA</italic> sequences of <italic>Theileria equi</italic> genotypes. The figure was created using the ML method. Bootstrap values were performed with 1,000 replicates. The evolutionary history was performed by using the ML method TN93&#x2009;+&#x2009;G model were used of <italic>T. equi</italic> genotypes (<xref ref-type="bibr" rid="ref45">45</xref>). Evolutionary analyses were conducted in MEGA-11 (<xref ref-type="bibr" rid="ref44">44</xref>). <italic>T. annulata</italic> was used as an outgroup.</p>
</caption>
<graphic xlink:href="fvets-11-1359974-g002.tif"/>
</fig>
</sec>
<sec id="sec6">
<label>2.4</label>
<title>Statistical analysis</title>
<p>The chi-square test (&#x03C7;<sup>2</sup>) was used to determine the differences among various parameters. <italic>p</italic>&#x2009;&#x003C;&#x2009;0.05 was accepted to be statistically significant.</p>
</sec>
<sec id="sec7">
<label>2.5</label>
<title>Ethics statement</title>
<p>The ethical permission was granted from the Kyrgyz-Turkish Manas University Animal Experiments Local Ethics Committee with number 2023/12. The owners of the horses also gave their oral permission to collect the blood samples from their animals.</p>
</sec>
</sec>
<sec sec-type="results" id="sec8">
<label>3</label>
<title>Results</title>
<sec id="sec9">
<label>3.1</label>
<title>The results of PCRs</title>
<p>A total of 311 horse blood samples were analyzed by equine piroplasmosis (EP), hemotropic mycoplasmas (HM), <italic>Anaplasma phagocytophilum,</italic> and <italic>Anaplasma capra</italic> specific-PCRs. As a result of PCRs, positivity was detected in 23 samples only with EP specific PCR, while no positivity was detected in the other three PCRs.</p>
<p>The 23 positive samples were identified as <italic>T. equi</italic> by sequencing (section of sequencing of <italic>18S rRNA</italic> gene and phylogenetic analysis). Accordingly, PCR results based on sequence analyses are given in <xref ref-type="table" rid="tab3">Table 3</xref>. The total prevalence of <italic>T. equi</italic> was determined as 7.40% (23/311). This rate was found to be 8.11% in males (15/185) and 6.35% in females (8/126) (<italic>p</italic>&#x2009;=&#x2009;0.2880). It was determined as 6.35% (12/189) in the 1&#x2013;4 age group and 9.02% (11/122) in those aged 5 and older (<italic>p</italic>&#x2009;=&#x2009;0.1950) (<xref ref-type="table" rid="tab3">Table 3</xref>).</p>
<table-wrap position="float" id="tab3">
<label>Table 3</label>
<caption>
<p><italic>Theileria equi</italic> positive samples by location, age and gender.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="left" valign="top" rowspan="2">Locations</th>
<th align="center" valign="top" colspan="2">Age</th>
<th align="center" valign="top" colspan="2">Gender</th>
<th align="center" valign="top" rowspan="2">Total</th>
</tr>
<tr>
<th align="center" valign="top">1&#x2013;4</th>
<th align="center" valign="top">5&#x2264;</th>
<th align="center" valign="top">Male</th>
<th align="center" valign="top">Female</th>
</tr>
<tr>
<th/>
<th align="center" valign="top">% (+/<italic>n</italic>)</th>
<th align="center" valign="top">% (+/<italic>n</italic>)</th>
<th align="center" valign="top">% (+/<italic>n</italic>)</th>
<th align="center" valign="top">% (+/<italic>n</italic>)</th>
<th align="center" valign="top">% (+/<italic>n</italic>)</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="top">Chuy</td>
<td align="char" valign="top" char="(">8.82 (9/102)</td>
<td align="char" valign="top" char="(">11.63 (10/86)</td>
<td align="char" valign="top" char="(">10.48 (13/124)</td>
<td align="char" valign="top" char="(">9.38 (6/64)</td>
<td align="char" valign="top" char="(">10.11 (19/188)</td>
</tr>
<tr>
<td align="left" valign="top">Issyk-Kul</td>
<td align="char" valign="top" char="(">6.67 (2/30)</td>
<td align="char" valign="top" char="(">16.67 (1/6)</td>
<td align="char" valign="top" char="(">10.53 (2/19)</td>
<td align="char" valign="top" char="(">5.88 (1/17)</td>
<td align="char" valign="top" char="(">8.33 (3/36)</td>
</tr>
<tr>
<td align="left" valign="top">Naryn</td>
<td align="char" valign="top" char="(">5 (1/20)</td>
<td align="char" valign="top" char="(">0 (0/10)</td>
<td align="char" valign="top" char="(">0 (0/12)</td>
<td align="char" valign="top" char="(">5.56 (1/18)</td>
<td align="char" valign="top" char="(">3.33 (1/30)</td>
</tr>
<tr>
<td align="left" valign="top">Osh</td>
<td align="char" valign="top" char="(">0 (0/15)</td>
<td align="char" valign="top" char="(">0 (0/7)</td>
<td align="char" valign="top" char="(">0 (0/12)</td>
<td align="char" valign="top" char="(">0 (0/10)</td>
<td align="char" valign="top" char="(">0 (0/22)</td>
</tr>
<tr>
<td align="left" valign="top">Talas</td>
<td align="char" valign="top" char="(">0 (0/13)</td>
<td align="char" valign="top" char="(">0 (0/7)</td>
<td align="char" valign="top" char="(">0 (0/10)</td>
<td align="char" valign="top" char="(">0 (0/10)</td>
<td align="char" valign="top" char="(">0 (0/20)</td>
</tr>
<tr>
<td align="left" valign="top">Jalal-Abad</td>
<td align="char" valign="top" char="(">0 (0/9)</td>
<td align="char" valign="top" char="(">0 (0/6)</td>
<td align="char" valign="top" char="(">0 (0/8)</td>
<td align="char" valign="top" char="(">0 (0/7)</td>
<td align="char" valign="top" char="(">0 (0/15)</td>
</tr>
<tr>
<td align="left" valign="top">Total</td>
<td align="char" valign="top" char="(">6.35 (12/189)</td>
<td align="char" valign="top" char="(">9.02 (11/122)</td>
<td align="char" valign="top" char="(">8.11 (15/185)</td>
<td align="char" valign="top" char="(">6.35 (8/126)</td>
<td align="char" valign="top" char="(">7.40 (23/311)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>%: percentage, +: number of positive samples, n: number of samples.</p>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="sec10">
<label>3.2</label>
<title>Sequencing of <italic>18S rRNA</italic> gene and phylogenetic analysis</title>
<p>Equine piroplasmos (EP) was detected in 23 samples by PCR. The partial sequence analyses of <italic>18S rRNA</italic> revealed that 19 positive samples were matched with the <italic>T. equi</italic> E genotype, whereas four samples were <italic>T. equi</italic> A genotypes. The consensus sequences were uploaded to the GenBank under accession numbers <italic>T. equi</italic> E genotypes: OR794371-OR794389, <italic>T. equi</italic> A genotypes: OR794390-OR794393.</p>
<p>The sequences of <italic>T. equi</italic> E genotypes identified in this study were 100% identical to each other. High nucleotide similarities (99.78&#x2013;100%) were seen between <italic>T. equi</italic> E genotypes obtained in this study and <italic>T. equi</italic> E genotype uploaded to the GenBank in different parts of the world. Furthermore, 100% nucleotide identities were present between our isolate and <italic>T. equi</italic> isolates identified from Ukraine (KP868757), China (OQ692565 and MZ327270), Russia (OM475525), Austria (MW446331), and Portugal (MT767169).</p>
<p><italic>Theileria equi</italic> A genotypes obtained in this study had 100% nucleotide identities with each other. The 99.35&#x2013;100% nucleotide similarities were determined between our sequence and <italic>T. equi</italic> A genotypes present in the GenBank deposited from various countries. The <italic>T. equi</italic> A genotype sequences obtained in this study showed 100% nucleotide similarities to those of <italic>T. equi</italic> A genotypes identified in T&#x00FC;rkiye (MG569905), France (MK732476, MF510478), Portugal (MT767167), Israel (MK392060, MK063843), Saudi Arabia (LC431545, KJ801931), Egypt (MN625898), Chile (MT463613), Brazil (MG052917, KY952237), Cuba (KY111762), and United States (CP099438 and JX177673).</p>
<p>The phylogenetic tree showed that our <italic>T. equi</italic> Genotype-E and Genotype-A clustered with Genotype-E and Genotype-A identified from different countries, respectively.</p>
</sec>
</sec>
<sec sec-type="discussion" id="sec11">
<label>4</label>
<title>Discussion</title>
<p>The factors such as global warming, increased use of rural areas, animal movements, and the contribution of migratory birds increase the spread and importance of TBPs (<xref ref-type="bibr" rid="ref1">1</xref>). Knowing basic epidemiological information plays a critical role in the development and implementation of effective and widespread control methods for these diseases. Obtaining the most epidemiological data can undoubtedly be achieved through studies using methods with high specificity and sensitivity in different regions of the world. Equine piroplasmosis, an important TBP of horses, can be diagnosed by microscopic, serological, and molecular techniques (<xref ref-type="bibr" rid="ref6">6</xref>). Microscopic examination of stained blood smears has the disadvantage of low sensitivity, especially in chronic infections with low parasitemia. The complement fixation technique, the indirect fluorescence antibody test, and the competitive inhibition enzyme-linked immunosorbent assay are used to detect parasite-specific antibodies (<xref ref-type="bibr" rid="ref6">6</xref>). The most important disadvantage of serological methods is that they do not distinguish between current and previous infections (<xref ref-type="bibr" rid="ref8">8</xref>). Molecular diagnostic techniques, especially PCR, stand out with their superiority in both specificity and sensitivity in the diagnosis of EP. In recent years, these methods have been widely used in epidemiological studies (<xref ref-type="bibr" rid="ref46 ref47 ref48 ref49 ref50">46&#x2013;50</xref>). Although the presence of different TBPs in cattle, sheep, and dogs (HM species, <italic>B. vogeli, B. vulpes, A. centrale, A. capra</italic>, <italic>A. phagocytophilum-</italic>like 1, <italic>A. ovis</italic>, <italic>B. major, T. annulata,</italic> and <italic>T. orientalis</italic>) has been previously reported in Kyrgyzstan (<xref ref-type="bibr" rid="ref14">14</xref>, <xref ref-type="bibr" rid="ref15">15</xref>, <xref ref-type="bibr" rid="ref31 ref32 ref33 ref34 ref35 ref36">31&#x2013;36</xref>), this study is the first molecular study investigating TBPs in horses in the country.</p>
<p>In recent studies, it has been shown that EP agents are divided into five genotypes (A, B, C, D, and E) based on the <italic>18S rRNA</italic> gene (<xref ref-type="bibr" rid="ref46">46</xref>, <xref ref-type="bibr" rid="ref51 ref52 ref53">51&#x2013;53</xref>). Moreover, it has been reported that the <italic>T. equi</italic>-C genotype includes the species described as <italic>T. haneyi</italic> (<xref ref-type="bibr" rid="ref5">5</xref>). In 2001, it was reported that <italic>T. equi</italic> has two genotypes (Florida (United States) and Pelotas (Southern Brazil) genotypes) based on the <italic>EMA-1</italic> gene (<xref ref-type="bibr" rid="ref54">54</xref>). The <italic>18S rRNA</italic> gene has advantages in genotyping studies due to the fact that it has multiple copies in the genome and the hypervariable region is also located here (<xref ref-type="bibr" rid="ref55">55</xref>, <xref ref-type="bibr" rid="ref56">56</xref>). It has been used extensively in studies on this subject. Firstly, <italic>B. equi</italic> Spain 1 and <italic>B. equi</italic> Spain 2 were reported in 2003, based on the <italic>18S rRNA</italic> gene (<xref ref-type="bibr" rid="ref57">57</xref>). In another conducted in Spain in 2004, <italic>B. equi</italic> Spain 1 and <italic>B. equi</italic> Spain 2 isolates were located in the same cluster, while <italic>T. equi</italic>-like was located in a different cluster, thus supporting the existence of two genotypes based on two <italic>18S rRNA</italic> genes (<xref ref-type="bibr" rid="ref58">58</xref>). In a more comprehensive study conducted in South Africa in 2009, a third genotype was detected, and the genotypes up to that time were named genotypes A, B, and C (<xref ref-type="bibr" rid="ref59">59</xref>). According to the study, <italic>B. equi</italic> Spain-1 and <italic>B. equi</italic> Spain-2 isolates detected from horses and <italic>T. equi</italic> isolate detected from dogs in Spain (<xref ref-type="bibr" rid="ref57">57</xref>) were collected under genotype A; <italic>T. equi</italic>-like isolates detected from horses in Spain and (<xref ref-type="bibr" rid="ref58">58</xref>), and from zebra in South Africa (<xref ref-type="bibr" rid="ref59">59</xref>) were collected genotype B, and <italic>T. equi</italic> isolates detected from horses in South Africa (<xref ref-type="bibr" rid="ref59">59</xref>) were collected under genotype C (<xref ref-type="bibr" rid="ref59">59</xref>). Following these, the presence of genotype D in horses in Sudan was revealed in 2010 (<xref ref-type="bibr" rid="ref60">60</xref>), and genotype E was revealed in 2012 based on previous South Korean-<italic>T. equi</italic> sequences (<xref ref-type="bibr" rid="ref61">61</xref>). In this study, 23 samples were sequenced. As a result of phylogenetic analysis based on <italic>18S rRNA</italic> gene DNA sequences, we identified two genetically distinct <italic>T. equi</italic> genotypes (A&#x2014;4 samples and E&#x2014;19 samples) in grazing horses from Kyrgyzstan. This is the first study that reports of <italic>T. equi</italic> and its genotypes in Kyrgyzstan. Our results confirm that different genotypes of <italic>T. equi</italic> coexist within the same population and the heterogeneous nature of this species, in agreement with previous studies (<xref ref-type="bibr" rid="ref46">46</xref>, <xref ref-type="bibr" rid="ref51 ref52 ref53">51&#x2013;53</xref>, <xref ref-type="bibr" rid="ref62">62</xref>). However, there is still a need for molecular surveys to determine the geographical distribution of the genotypes and their impact on the course of clinical infections, as well as studies on differences in vectors.</p>
<p>The PCR-positivity for <italic>T. equi</italic> was found to be 7.40% (23/311). While it is close to the rate previously reported in horses in T&#x00FC;rkiye (8.8%) (<xref ref-type="bibr" rid="ref63">63</xref>), it is generally lower than the positivity rates reported in many parts of the world such as 19.7% in T&#x00FC;rkiye (<xref ref-type="bibr" rid="ref49">49</xref>), 38.9% in China (<xref ref-type="bibr" rid="ref50">50</xref>), 44.5% in Spain (<xref ref-type="bibr" rid="ref64">64</xref>), 61.9% in Gambia (<xref ref-type="bibr" rid="ref65">65</xref>), 70.3% in Italy (<xref ref-type="bibr" rid="ref66">66</xref>), 73.0% in Cuba (<xref ref-type="bibr" rid="ref47">47</xref>). The differences among <italic>T. equi</italic> positivity rates may be related to sample numbers, the method used in the studies, age groups, animal management system, ecological factors, tick species in the region, and other risk factors.</p>
<p>The age of horses may be considered a risk factor for <italic>T. equi</italic> infections due to longer tick exposure. Additionally, the fact that <italic>T. equi</italic> is a lifelong carrier in horses may increase the percentage of positive older horses (<xref ref-type="bibr" rid="ref6">6</xref>, <xref ref-type="bibr" rid="ref67">67</xref>). Bartolom&#x00E9; del Pino et al. (<xref ref-type="bibr" rid="ref66">66</xref>) reported <italic>T. equi</italic>-PCR-positivity significantly decreases with age in Itay. On the other hand, Rueg et al. (<xref ref-type="bibr" rid="ref68">68</xref>) reported that <italic>T. equi</italic> positivity increased with age in Mongolia. Unlike both cases, it has been reported that the <italic>T. equi</italic>-PCR-positivity rate has no connection with age in T&#x00FC;rkiye (<xref ref-type="bibr" rid="ref69">69</xref>). These different results may be due to multivariate factors related to long-term parasite host circulation processes, which need to be explained on the basis of host&#x2013;parasite interaction, and the sensitivity of the methods used may also affect this situation. Although the prevalence of <italic>T. equi</italic> was high in horses older than 5 years of age in this study, this difference was found to be statistically insignificant (<italic>p</italic>&#x2009;=&#x2009;0.1950). On the other hand, all animals examined in this study appear healthy. When all the data are evaluated together, it may contribute to the understanding of the long-term carrier status of horses. The decrease in prevalence with age in <italic>B. caballi</italic> is attributed to the clearance of the agents in 4&#x2009;years and the loss of antibodies in the following period (<xref ref-type="bibr" rid="ref66">66</xref>). This may be related to the overall low prevalence of <italic>B. caballi</italic> and the fact that it was not detected in this study.</p>
<p>While there are studies showing that gender is related to <italic>T. equi</italic> positivity (<xref ref-type="bibr" rid="ref64">64</xref>, <xref ref-type="bibr" rid="ref70">70</xref>, <xref ref-type="bibr" rid="ref71">71</xref>), there are also studies showing that gender is not a risk factor (<xref ref-type="bibr" rid="ref72">72</xref>, <xref ref-type="bibr" rid="ref73">73</xref>). In our study, <italic>T. equi</italic> prevalence by gender was found to be statistically insignificant (<italic>p</italic>&#x2009;=&#x2009;0.2880). It is thought that this situation may be due to the husbandry techniques.</p>
<p>Equine anaplasmosis is mainly common in regions where <italic>Ixodes</italic> species occur, especially in northern America, and is also seen in Europe, Africa, and Southern America (<xref ref-type="bibr" rid="ref3">3</xref>, <xref ref-type="bibr" rid="ref12">12</xref>, <xref ref-type="bibr" rid="ref74">74</xref>). It has been determined that the prevalence of <italic>A. phagocytophilum</italic> in Germany peaked in relation to the activity of <italic>I. ricinus</italic> (<xref ref-type="bibr" rid="ref75">75</xref>). <italic>Anaplasma phagocytophilum-</italic>PCR positivity in horses was detected as 13% in the humid region of Tunisia (<xref ref-type="bibr" rid="ref76">76</xref>), 8% in Italy (<xref ref-type="bibr" rid="ref77">77</xref>), 4.3% in Pakistan (<xref ref-type="bibr" rid="ref77">77</xref>), and 15% in the island of Sardinia (<xref ref-type="bibr" rid="ref74">74</xref>). Although <italic>A. capra</italic> was detected in 2012 (<xref ref-type="bibr" rid="ref13">13</xref>), it was included in this study because it was found in a very large host group and was found in wild onegar in Iranian (<xref ref-type="bibr" rid="ref24">24</xref>), a species relatively close to horses. There has been no previous study investigating <italic>A. capra</italic> in horses. <italic>Anaplasma capra</italic> and <italic>A. phagocytophilum</italic> could not be detected in horses in our study. Unlike the above regions, Kyrgyzstan is a very mountainous country with no sea borders. The continental climate of the country and the related tick fauna may directly affect the presence and prevalence of TBPs. In our study, the animals whose blood was collected appeared healthy and no ticks were found. However, more comprehensive studies including tick species in the country are needed.</p>
<p>There is a paucity of information on the prevalence and distribution of hemotropic mycoplasma species in horses. Molecular-based studies have shown that the hemoplasma species detected in horses are species associated with different animal species (<xref ref-type="bibr" rid="ref27 ref28 ref29 ref30">27&#x2013;30</xref>). In these studies, <italic>Canditus M. haemobos</italic> and <italic>M. haemofelis</italic>, which are related to cattle and cats, respectively, in Germany (<xref ref-type="bibr" rid="ref27">27</xref>), <italic>M. ovis</italic> which is mostly related to sheep in Brazil (<xref ref-type="bibr" rid="ref30">30</xref>), <italic>Mycoplasma ovis</italic>-like and <italic>Candidatu</italic>s <italic>M. haemocervae</italic> were detected in horses from Iran and Nigeria, respectively (<xref ref-type="bibr" rid="ref28">28</xref>, <xref ref-type="bibr" rid="ref29">29</xref>). Besides this, in three different studies investigating TBPs in horses in Brazil, the presence of <italic>T. equi</italic> and <italic>B. caballi</italic> was reported, but hemotropic mycoplasma could not be detected in the horses (<xref ref-type="bibr" rid="ref78 ref79 ref80">78&#x2013;80</xref>). Additionally, some researchers have stated that hemoplasma infections may be accidental or an uncommon disease in horses (<xref ref-type="bibr" rid="ref78">78</xref>). In this study, hemoplasma species were not detected in horses, and this may be related to the absence of hemoplasma species in other animals in the sampling areas.</p>
</sec>
<sec sec-type="conclusions" id="sec12">
<label>5</label>
<title>Conclusion</title>
<p>The global importance of TBPs is increasing among hosts, and equine piroplasmosis is the most important TBD in horses. Although different genotypes of <italic>B. caballi</italic> and <italic>T. equi</italic> have been detected, the clinical relationship, geographical distribution, and vectors of these genotypes need to be revealed. This study revealed the existence of A and E genotypes of <italic>T. equi</italic> in grazing horses from Kyrgyzstan, and this information helps to understand the epidemiology of these <italic>T. equi</italic> genotypes. In this study, <italic>A. phagocytophilum, A. capra,</italic> and HM were detected in horses. <italic>A. capra</italic>, a relatively novel species, is thought to have a global distribution, and large-scale studies are still needed to understand the prevalence, distribution, and pathogenesis of this pathogen in horses.</p>
</sec>
<sec sec-type="data-availability" id="sec13">
<title>Data availability statement</title>
<p>The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: <ext-link xlink:href="https://www.ncbi.nlm.nih.gov/genbank/" ext-link-type="uri">https://www.ncbi.nlm.nih.gov/genbank/</ext-link>, OR794390; <ext-link xlink:href="https://www.ncbi.nlm.nih.gov/genbank/" ext-link-type="uri">https://www.ncbi.nlm.nih.gov/genbank/</ext-link>, OR794391; <ext-link xlink:href="https://www.ncbi.nlm.nih.gov/genbank/" ext-link-type="uri">https://www.ncbi.nlm.nih.gov/genbank/</ext-link>, OR794392; <ext-link xlink:href="https://www.ncbi.nlm.nih.gov/genbank/" ext-link-type="uri">https://www.ncbi.nlm.nih.gov/genbank/</ext-link>, OR794393.</p>
</sec>
<sec sec-type="ethics-statement" id="sec14">
<title>Ethics statement</title>
<p>The animal studies were approved by Kyrgyzs-Turkish Manas Un&#x0131;versity Animal Experiments Local Ethics Committee with decision number 2023/12. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent was obtained from the owners for the participation of their animals in this study.</p>
</sec>
<sec sec-type="author-contributions" id="sec15">
<title>Author contributions</title>
<p>KA: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing. UE: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Writing &#x2013; review &#x0026; editing. OS: Data curation, Formal analysis, Investigation, Methodology, Writing &#x2013; review &#x0026; editing. MU: Data curation, Formal analysis, Investigation, Writing &#x2013; review &#x0026; editing. AA: Data curation, Formal analysis, Investigation, Methodology, Writing &#x2013; review &#x0026; editing. MA: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing.</p>
</sec>
</body>
<back>
<sec sec-type="funding-information" id="sec16">
<title>Funding</title>
<p>The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.</p>
</sec>
<ack>
<p>The material for this study was obtained from horses owned in Kyrgyzstan. We would like to thank the animal owners for their cooperation.</p>
</ack>
<sec sec-type="COI-statement" id="sec17">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
<p>The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.</p>
</sec>
<sec id="sec100" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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