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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id>
<journal-title>Frontiers in Microbiology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Microbiol.</abbrev-journal-title>
<issn pub-type="epub">1664-302X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fmicb.2023.1229950</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Microbiology</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Molecular detection of <italic>Coxiella</italic> spp. in ticks (Ixodidae and Argasidae) infesting domestic and wild animals: with notes on the epidemiology of tick-borne <italic>Coxiella burnetii</italic> in Asia</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name><surname>Ali</surname> <given-names>Abid</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="corresp" rid="c001"><sup>&#x0002A;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/453327/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Obaid</surname> <given-names>Muhammad Kashif</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1812522/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Almutairi</surname> <given-names>Mashal M.</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1264813/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Alouffi</surname> <given-names>Abdulaziz</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1087626/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Numan</surname> <given-names>Muhammad</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/2330212/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Ullah</surname> <given-names>Shafi</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/2141420/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Rehman</surname> <given-names>Gauhar</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/460419/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Islam</surname> <given-names>Zia Ul</given-names></name>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1979350/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Khan</surname> <given-names>Sher Bahadar</given-names></name>
<xref ref-type="aff" rid="aff5"><sup>5</sup></xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>Tanaka</surname> <given-names>Tetsuya</given-names></name>
<xref ref-type="aff" rid="aff6"><sup>6</sup></xref>
<xref ref-type="corresp" rid="c002"><sup>&#x0002A;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/84557/overview"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Department of Zoology, Abdul Wali Khan University Mardan, Mardan</institution>, <addr-line>Khyber Pakhtunkhwa</addr-line>, <country>Pakistan</country></aff>
<aff id="aff2"><sup>2</sup><institution>Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University</institution>, <addr-line>Riyadh</addr-line>, <country>Saudi Arabia</country></aff>
<aff id="aff3"><sup>3</sup><institution>King Abdulaziz City for Science and Technology</institution>, <addr-line>Riyadh</addr-line>, <country>Saudi Arabia</country></aff>
<aff id="aff4"><sup>4</sup><institution>Department of Biotechnology, Abdul Wali Khan University Mardan, Mardan</institution>, <addr-line>Khyber Pakhtunkhwa</addr-line>, <country>Pakistan</country></aff>
<aff id="aff5"><sup>5</sup><institution>College of Animal Husbandry and Veterinary Sciences, Abdul Wali Khan University Mardan, Mardan</institution>, <addr-line>Khyber Pakhtunkhwa</addr-line>, <country>Pakistan</country></aff>
<aff id="aff6"><sup>6</sup><institution>Laboratory of Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University</institution>, <addr-line>Kagoshima</addr-line>, <country>Japan</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Hong Yin, Chinese Academy of Agricultural Sciences (CAAS), China</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: Rosa Estela Quiroz Casta&#x000F1;eda, Instituto Nacional de Investigaciones Forestales, Agr&#x000ED;colas y Pecuarias (INIFAP), Mexico; Zhijie Liu, Chinese Academy of Agricultural Sciences (CAAS), China</p></fn>
<corresp id="c001">&#x0002A;Correspondence: Abid Ali <email>uop_ali&#x00040;yahoo.com</email></corresp>
<corresp id="c002">Tetsuya Tanaka <email>k6199431&#x00040;kadai.jp</email></corresp>
</author-notes>
<pub-date pub-type="epub">
<day>27</day>
<month>07</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>14</volume>
<elocation-id>1229950</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>05</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>03</day>
<month>07</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2023 Ali, Obaid, Almutairi, Alouffi, Numan, Ullah, Rehman, Islam, Khan and Tanaka.</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Ali, Obaid, Almutairi, Alouffi, Numan, Ullah, Rehman, Islam, Khan and Tanaka</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>
<p>Tick-borne <italic>Coxiella</italic> spp. are emerging in novel regions infecting different hosts, but information regarding their occurrence is limited. The purpose of this study was the molecular screening of <italic>Coxiella</italic> spp. in various ticks infesting goats, sheep, camels, cattle, wild mice, and domestic fowls (<italic>Gallus gallus domesticus</italic>) in various districts of Khyber Pakhtunkhwa, Pakistan. Morphologically identified tick species were confirmed by obtaining their <italic>cox1</italic> sequences and were molecularly screened for <italic>Coxiella</italic> spp. by sequencing <italic>GroEL</italic> fragments. Almost 345 out of 678 (50.9%) hosts were infested by nine tick species. Regarding the age groups, the hosts having an age &#x0003E;3 years were highly infested (192/345, 55.6%), while gender-wise infestation was higher in female hosts (237/345, 68.7%). In collected ticks, the nymphs were outnumbered (613/1,119, 54.8%), followed by adult females (293/1,119, 26.2%) and males (213/1,119, 19.7%). A total of 227 ticks were processed for molecular identification and detection of <italic>Coxiella</italic> spp. The obtained <italic>cox1</italic> sequences of nine tick species such as <italic>Hyalomma dromedarii, Hyalomma anatolicum, Haemaphysalis cornupunctata, Haemaphysalis bispinosa, Haemaphysalis danieli, Haemaphysalis montgomeryi, Rhipicephalus haemaphysaloides, Rhipicephalus microplus</italic>, and <italic>Argas persicus</italic> showed maximum identities between 99.6% and 100% with the same species and in the phylogenetic tree, clustered to the corresponding species. All the tick species except <italic>Ha. danieli</italic> and <italic>R. microplus</italic> were found positive for <italic>Coxiella</italic> spp. (40/227, 17.6%), including <italic>Coxiella burnetii</italic> (15/40, 6.7%), <italic>Coxiella</italic> endosymbionts (14/40, 6.3%), and different <italic>Coxiella</italic> spp. (11/40, 4.9%). By the BLAST results, the <italic>GroEL</italic> fragments of <italic>Coxiella</italic> spp. showed maximum identity to <italic>C. burnetii, Coxiella</italic> endosymbionts, and <italic>Coxiella</italic> sp., and phylogenetically clustered to the corresponding species. This is the first comprehensive report regarding the genetic characterization of <italic>Coxiella</italic> spp. in Pakistan&#x00027;s ticks infesting domestic and wild hosts. Proper surveillance and management measures should be undertaken to avoid health risks.</p></abstract>
<kwd-group>
<kwd>ticks</kwd>
<kwd><italic>cox1</italic></kwd>
<kwd><italic>Coxiella burnetii</italic></kwd>
<kwd><italic>GroEL</italic></kwd>
<kwd>domestic and wild animals</kwd>
<kwd>Pakistan</kwd>
</kwd-group>
<counts>
<fig-count count="3"/>
<table-count count="4"/>
<equation-count count="0"/>
<ref-count count="110"/>
<page-count count="19"/>
<word-count count="12177"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Infectious Agents and Disease</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec sec-type="intro" id="s1">
<title>Introduction</title>
<p>Ticks are hematophagous ectoparasites, actively contributing to transmitting infectious agents to wild and domestic animals and humans (De la Fuente et al., <xref ref-type="bibr" rid="B34">2017</xref>). Numerous ticks act as distinguished vectors and reservoirs for various pathogens, including bacteria causing rickettsiosis, anaplasmosis, Lyme disease, viruses such as Powassan, and protozoan agents such as <italic>Theileria</italic> spp. and <italic>Babesia</italic> spp. (De la Fuente et al., <xref ref-type="bibr" rid="B34">2017</xref>; Karim et al., <xref ref-type="bibr" rid="B58">2017</xref>; Rochlin and Toledo, <xref ref-type="bibr" rid="B89">2020</xref>; Ali et al., <xref ref-type="bibr" rid="B13">2021</xref>). Aside from transmitting various infectious agents, ticks are hosts to many endosymbionts and a diversified microbiome (&#x00160;pitalsk&#x000E1; et al., <xref ref-type="bibr" rid="B98">2018</xref>).</p>
<p>Among the bacterial genus <italic>Coxiella</italic> having one pathogenic species, <italic>Coxiella burnetii</italic> is a Gram-negative obligate intracellular bacterium distributed worldwide except in New Zealand and French Polynesia (Musso et al., <xref ref-type="bibr" rid="B75">2014</xref>; Eldin et al., <xref ref-type="bibr" rid="B42">2017</xref>). Common reservoirs of <italic>C. burnetii</italic> are domestic mammals, including cattle, sheep, goats, and camels as well as reptiles, birds, and ticks (Anderson et al., <xref ref-type="bibr" rid="B19">2013</xref>; Abdel-Moein and Hamza, <xref ref-type="bibr" rid="B1">2017</xref>), and have the potential to cause query (Q) fever (Musso et al., <xref ref-type="bibr" rid="B75">2014</xref>). The Q-fever was reported for the first time in 1935 from Australia as an outbreak of febrile illness with flu-like symptoms (Derrick, <xref ref-type="bibr" rid="B35">1937</xref>), and its causative agent was initially named <italic>Rickettsia burnetii</italic>, but later on renamed as <italic>C. burnetii</italic> (Philip, <xref ref-type="bibr" rid="B85">1948</xref>). <italic>Coxiella</italic> spp. have been isolated from almost 40 tick species, and hence considered as its tick-borne transmission to animals and humans (Eklund et al., <xref ref-type="bibr" rid="B40">1947</xref>; Beaman and Hung, <xref ref-type="bibr" rid="B23">1989</xref>; Duron et al., <xref ref-type="bibr" rid="B38">2014</xref>). Tick species, including <italic>Hyalomma dromedarii, Hyalomma anatolicum, Hyalomma scupense, Rhipicephalus microplus</italic>, and <italic>Rhipicephalus annulatus</italic>, may serve as vector reservoirs for the transmission of <italic>C. burnetii</italic> in Pakistan (Karim et al., <xref ref-type="bibr" rid="B58">2017</xref>). <italic>Coxiella</italic>-like endosymbionts were also found in various tick species, and an obligatory mutualism between this bacteria and host ticks has been proven (Smith et al., <xref ref-type="bibr" rid="B97">2015</xref>).</p>
<p>Ticks can transmit <italic>Coxiella</italic> spp. both transovarially and transstadially to their offspring. Infected ticks excrete enormous amounts of <italic>Coxiella</italic> spp. in their feces, contaminating the skin of host animals and playing a significant role in the spread of <italic>Coxiella</italic> infection (Cong et al., <xref ref-type="bibr" rid="B31">2015</xref>; Seo et al., <xref ref-type="bibr" rid="B94">2016</xref>). <italic>Coxiella burnetii</italic> may resist harsh environmental factors, for instance, dry and hot weather, desiccation, and other antiseptics. As it may affect the productive and reproductive abilities, humans and animals could face long-term infection risks (Ullah et al., <xref ref-type="bibr" rid="B108">2019</xref>). Various techniques have been effectively followed for the surveillance of <italic>C. burnetii</italic> infection. Still, ELISA is considered an effective technique for its serological diagnosis. In combination with sequencing, PCR is believed to be the best technique for the molecular identification and genetic characterization of <italic>C. burnetii</italic> (Niemczuk et al., <xref ref-type="bibr" rid="B77">2014</xref>; Bontje et al., <xref ref-type="bibr" rid="B24">2016</xref>).</p>
<p><italic>Coxiella</italic> spp. have been detected in different tick species, animals, humans, and soil samples in Asia that have been reported in various studies. <italic>Coxiella burnetii</italic> is the causative agent of Q-fever, one of the ignored zoonoses in developing countries, including Pakistan. To the best of our knowledge, approximately 24 studies from 1955 to 2022 regarding this infection have been reported in Pakistan, and Q-fever in humans, goats, sheep, cattle, buffaloes, as well as rodents has been serologically documented (Ahmed, <xref ref-type="bibr" rid="B3">1987</xref>; Ullah et al., <xref ref-type="bibr" rid="B108">2019</xref>; Ali et al., <xref ref-type="bibr" rid="B12">2022a</xref>; Hussain et al., <xref ref-type="bibr" rid="B55">2022</xref>). The <italic>C. burnetii</italic> is also considered a soil-borne pathogen as its isolation has been confirmed from soil samples (Shabbir et al., <xref ref-type="bibr" rid="B95">2015</xref>). Due to the information dearth regarding numerous tick-borne pathogens (TBPs) that infect ruminants and other animals in Pakistan, substantial research is required to investigate the genetic composition of various TBPs, specifically <italic>Coxiella</italic> spp. Hence, this study aimed to molecularly characterize different tick species infesting domestic and wild animals and screen out the associated <italic>Coxiella</italic> spp. in Pakistan and summarize the association of <italic>Coxiella</italic> spp. with ticks infesting various hosts in Asia.</p></sec>
<sec sec-type="materials and methods" id="s2">
<title>Materials and methods</title>
<sec>
<title>Ethical considerations</title>
<p>The Advance Studies and Research Board (ASRB: Dir/A&#x00026;R/AWKUM/2022/9396) of the Department of Zoology, Abdul Wali Khan University Mardan, Pakistan, approved prior consent for this study. Additionally, permission was taken from the owners of the animals to observe hosts and ticks collection. All the rules regarding animal welfare regulations were followed while handling the animals.</p></sec>
<sec>
<title>Description of the study area and sampling sites</title>
<p>Different districts including Lakki Marwat (32.5993&#x000B0; N, 70.9160&#x000B0; E), Mansehra (34.3271&#x000B0; N, 73.1992&#x000B0; E), Bajaur (34.7522&#x000B0; N, 71.5162&#x000B0; E), Dir Upper (35.3274&#x000B0; N, 72.0907&#x000B0; E), Dir Lower (34.8364&#x000B0; N, 71.8964&#x000B0; E), Abbottabad (34.1534&#x000B0; N, 73.2215&#x000B0; E), Buner (34.459129&#x000B0; N, 72.557252&#x000B0; E), Charsadda (34.161297&#x000B0; N, 71.755377&#x000B0; E), Chitral (35.727064&#x000B0; N, 71.759794&#x000B0; E), and Nowshera (33.998608&#x000B0; N, 71.999144&#x000B0; E) of Khyber Pakhtunkhwa were selected for the current study. These study locations have desertic plains, arid plains, arid hilly, humid plains, and hilly areas with variations in their climatic conditions, altitude, and seasons (winter, spring, summer, and autumn). The summer season is comparatively hot and longer in district Lakki Marwat than in other districts; however, snowfall occurs in winter in the districts of Chitral, Mansehra, Buner, Bajaur, Dir Upper, Dir Lower, and Abbottabad (<ext-link ext-link-type="uri" xlink:href="https://en.climate-data.org/">climate-data.org</ext-link>; accessed on 20 February 2023). Goats, sheep, camels, and cattle are the livestock of the region that are intended for producing dairy products and transportation. These transhumant animals move from one place to another within the district for food and natural pastures. Their diet and resources depend upon climatic conditions that remarkably vary spatiotemporally. The Global Positioning System was used for the geographical coordinates of the districts as mentioned above and designed the study map through ArcGIS v 10.3.1 (<xref ref-type="fig" rid="F1">Figure 1</xref>).</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p>Map showing the collection sites where ticks were collected.</p></caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmicb-14-1229950-g0001.tif"/>
</fig></sec>
<sec>
<title>Tick collection and their morphological identification</title>
<p>The herds of goats, sheep, camels, and cattle were visited for tick collection from September 2021 to August 2022. Moreover, wild mice captured by local farmers on agricultural land and domestic fowls (<italic>Gallus gallus domesticus</italic>) were also examined for tick specimens. Tick specimens were collected manually from different hosts in the study districts. The collected ticks were morphologically identified under a stereomicroscope (SZ61, Olympus, Japan) using available standard morphological keys (Hoogstraal and Kaiser, <xref ref-type="bibr" rid="B52">1959</xref>; Hoogstraal and Varma, <xref ref-type="bibr" rid="B54">1962</xref>; Hoogstraal and Trapido, <xref ref-type="bibr" rid="B53">1966</xref>; Dhanda and Kulkarni, <xref ref-type="bibr" rid="B36">1969</xref>; Kohls et al., <xref ref-type="bibr" rid="B65">1970</xref>; Cern&#x000FD; and Hoogstraal, <xref ref-type="bibr" rid="B26">1977</xref>; Apanaskevich, <xref ref-type="bibr" rid="B20">2003</xref>; Apanaskevich et al., <xref ref-type="bibr" rid="B21">2008</xref>; Ahmad et al., <xref ref-type="bibr" rid="B2">2022</xref>; Ali et al., <xref ref-type="bibr" rid="B14">2022b</xref>). The identified tick species were categorized according to species, gender, and nymph stage or adult stage, and then preserved in 100% ethanol at room temperature before further analyses.</p></sec>
<sec>
<title>DNA extraction and molecular screening</title>
<p>The preserved ticks were washed with 70% ethanol, followed by their immersion in distilled water for 10 min to eliminate the external contamination, and subsequently dried on a sterile filter paper. A subset of 227 (137 N, 49 F, and 41 M) ticks including 65 <italic>Ha</italic>. <italic>cornupunctata</italic> (41 N, 14 F, and 10 M), 28 <italic>Ha. montgomeryi</italic> (17 N, 6 F, and 5 M), 28 <italic>Hy. anatolicum</italic> (17 N, 6 F, and 5 M), 27 <italic>A. persicus</italic> (17 N, 6 F, and 4 M), 23 <italic>R. haemaphysaloides</italic> (15 N, 5 F, and 3 M), 19 <italic>R. microplus</italic> (9 N, 5 F, and 5 M), 19 <italic>Ha. bispinosa</italic> (11 N, 4 F, and 4 M), 12 <italic>Hy. dromedarii</italic> (7 N, 1 F, and 4 M), and 6 <italic>Ha. danieli</italic> (3 N, 2 F, and 1 M) were randomly selected and used individually for DNA extraction. Each stage of the morphologically identified tick species was individually crushed using sterile scissors to extract genomic DNA through the standard protocol of the phenol&#x02013;chloroform method (Sambrook et al., <xref ref-type="bibr" rid="B92">1989</xref>).</p>
<p>The whole extracted genomic DNA of each morphologically identified tick species (each stage) was individually used to amplify <italic>cox1</italic> fragments by utilizing species-specific primers in a conventional PCR (<xref ref-type="table" rid="T1">Table 1</xref>). Nested PCR was performed to amplify the <italic>GroEL</italic> fragment of <italic>Coxiella</italic> spp. (GE-96G, BIOER, Hangzhou, China). In nested PCR, two pairs of primers were used for the said purpose (<xref ref-type="table" rid="T1">Table 1</xref>). PCR reaction mixtures were performed in 25 &#x003BC;L, comprised of 1 &#x003BC;L of each primer at a concentration of 10 pmol/&#x003BC;L (first pair of primers in case of <italic>GroEL</italic>), 8.5 &#x003BC;L PCR water, 2 &#x003BC;L (100 ng/&#x003BC;L) genomic DNA, and 12.5 &#x003BC;L Dream<italic>Taq</italic> MasterMix (2 &#x000D7; ) (Thermo Fisher Scientific, Inc., Waltham, MA, USA). However, 2 &#x003BC;L of PCR product from the first PCR amplified reaction was used instead of genomic DNA in the second PCR run (in the case of <italic>GroEL</italic>) along with the second pair of primers at the same concentration. In each PCR reaction, PCR water was taken as a negative control, while <italic>Hyalomma scupense</italic> and <italic>Rickettsia massiliae</italic> DNA were taken as a positive control for ticks and <italic>Coxiella</italic>, respectively. The amplified products were loaded in 2% agarose gel to observe the expected band through the Gel Documentation System (BioDoc-It&#x02122; Imaging Systems, UVP, LLC, Upland, CA, USA). PCR amplified products were purified <italic>via</italic> GeneClean II Kit (Qbiogene, Il-lkirch, France) following the manufacturer&#x00027;s protocol. The amplified amplicons were sequenced bidirectionally through the Sanger-based sequencing method (Macrogen, Inc., Seoul, South Korea).</p>
<table-wrap position="float" id="T1">
<label>Table 1</label>
<caption><p>Primers and PCR cycling conditions used in the current study.</p></caption> 
<table frame="box" rules="all">
<thead>
<tr style="background-color:#919497;color:#ffffff">
<th valign="top" align="left"><bold>Gene</bold></th>
<th valign="top" align="left"><bold>Sequence (5-3)</bold></th>
<th valign="top" align="left"><bold>Amplicon size</bold></th>
<th valign="top" align="left"><bold>Cycling conditions</bold></th>
<th valign="top" align="left"><bold>References</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" rowspan="2"><italic><bold>cox1</bold></italic></td>
<td valign="top" align="left">HCO2198: TAAACTTCAGGGTGACCAAAAAATCA</td>
<td valign="top" align="left" rowspan="2">710 bp</td>
<td valign="top" align="left" rowspan="2"><inline-formula><mml:math id="M1"><mml:mfrac><mml:mrow><mml:mn>9</mml:mn><mml:msup><mml:mrow><mml:mn>8</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>30</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mn>40</mml:mn><mml:mi>X</mml:mi><mml:mrow><mml:mo>[</mml:mo><mml:mrow><mml:mtext>&#x000A0;</mml:mtext><mml:mfrac><mml:mrow><mml:mn>9</mml:mn><mml:msup><mml:mrow><mml:mn>8</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>10</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac><mml:mtext>&#x000A0;</mml:mtext><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>6</mml:mn><mml:msup><mml:mrow><mml:mn>3</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>7</mml:mn><mml:msup><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>25</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac></mml:mrow><mml:mo>]</mml:mo></mml:mrow><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>7</mml:mn><mml:msup><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>5</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>m</mml:mi><mml:mi>i</mml:mi><mml:mi>n</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mn>1</mml:mn><mml:msup><mml:mrow><mml:mn>0</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:math></inline-formula></td>
<td valign="top" align="left" rowspan="2">Folmer et al., <xref ref-type="bibr" rid="B46">1994</xref></td>
</tr>
 <tr>
<td valign="top" align="left">LCO1490: GGTCAACAAATCATAAAGATATTGG</td>
</tr> <tr>
<td valign="top" align="left" rowspan="4"><italic><bold>GroEL</bold></italic></td>
<td valign="top" align="left">CoxGrF1: <xref ref-type="table-fn" rid="TN1"><sup><bold>&#x0002A;</bold></sup></xref> TTTGAAAAYATGGGCGCKCAAATGGT</td>
<td valign="top" align="left" rowspan="2">655 bp</td>
<td valign="top" align="left" rowspan="4"><inline-formula><mml:math id="M2"><mml:mfrac><mml:mrow><mml:mn>9</mml:mn><mml:msup><mml:mrow><mml:mn>5</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>3</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>m</mml:mi><mml:mi>i</mml:mi><mml:mi>n</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mn>30</mml:mn><mml:mi>X</mml:mi><mml:mrow><mml:mo>[</mml:mo><mml:mrow><mml:mtext>&#x000A0;</mml:mtext><mml:mfrac><mml:mrow><mml:mn>9</mml:mn><mml:msup><mml:mrow><mml:mn>5</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>30</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>5</mml:mn><mml:msup><mml:mrow><mml:mn>6</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>30</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>s</mml:mi><mml:mi>e</mml:mi><mml:mi>c</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>7</mml:mn><mml:msup><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>1</mml:mn><mml:mo>.</mml:mo><mml:mn>5</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>m</mml:mi><mml:mi>i</mml:mi><mml:mi>n</mml:mi></mml:mrow></mml:mfrac></mml:mrow><mml:mo>]</mml:mo></mml:mrow><mml:mo>&#x02192;</mml:mo><mml:mfrac><mml:mrow><mml:mn>7</mml:mn><mml:msup><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:mrow><mml:mrow><mml:mn>7</mml:mn><mml:mtext>&#x000A0;</mml:mtext><mml:mi>m</mml:mi><mml:mi>i</mml:mi><mml:mi>n</mml:mi></mml:mrow></mml:mfrac><mml:mo>&#x02192;</mml:mo><mml:mn>1</mml:mn><mml:msup><mml:mrow><mml:mn>0</mml:mn></mml:mrow><mml:mrow><mml:mo>&#x02022;</mml:mo></mml:mrow></mml:msup><mml:mi>C</mml:mi></mml:math></inline-formula></td>
<td valign="top" align="left" rowspan="4">Duron et al., <xref ref-type="bibr" rid="B38">2014</xref></td>
</tr>
 <tr>
<td valign="top" align="left">CoxGrR2: <xref ref-type="table-fn" rid="TN1"><sup><bold>&#x0002A;</bold></sup></xref> CGRTCRCCAAARCCAGGTGC</td>
</tr>
 <tr>
<td valign="top" align="left">CoxGrF2: <xref ref-type="table-fn" rid="TN2"><sup><bold>&#x0002A;&#x0002A;</bold></sup></xref> GAAGTGGCTTCGCRTACWTCAGACG</td>
<td valign="top" align="left" rowspan="2">619 bp</td>
</tr>

<tr>
<td valign="top" align="left">CoxGrFR1: <xref ref-type="table-fn" rid="TN2"><sup><bold>&#x0002A;&#x0002A;</bold></sup></xref> CCAAARCCAGGTGCTTTYAC</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="TN1"><label>&#x0002A;</label><p>First run of nested PCR.</p></fn>
<fn id="TN2"><label>&#x0002A;&#x0002A;</label><p>Second run of nested PCR.</p></fn>
</table-wrap-foot>
</table-wrap></sec>
<sec>
<title>Sequences and phylogenetic analyses</title>
<p>The chromatograms of all the obtained sequences were manually observed and trimmed for purification purposes to remove the contaminated and poor reading regions through SeqMan V. 5 (DNASTAR, Inc., Madison, WI, USA). Final trimmed sequences were subjected to Basic Local Alignment Search Tool (BLAST) (Altschul et al., <xref ref-type="bibr" rid="B17">1990</xref>) at National Center for Biotechnology Information to get the high identity sequences in FASTA format. ClustalW multiple alignments (Thompson et al., <xref ref-type="bibr" rid="B104">1994</xref>) were used to align all the downloaded sequences along with the obtained and selected outgroup sequences in BioEdit Sequence Alignment Editor V.7.0.5 (Raleigh, NC, USA) (Hall et al., <xref ref-type="bibr" rid="B51">2011</xref>). The phylogenetic trees based on partial fragments of <italic>cox1</italic> and <italic>GroEL</italic> were constructed in MEGA-X (Molecular Evolutionary Genetics Analysis) (Kumar et al., <xref ref-type="bibr" rid="B66">2018</xref>) through the neighbor-joining method (Tamura-Nei model) and the Maximum Parsimony method (Tamura-Nei model) (Tamura and Nei, <xref ref-type="bibr" rid="B101">1993</xref>) with support of 1000 bootstrapping replicons, respectively. The coding fragments (<italic>cox1</italic> and <italic>GroEL</italic>) were aligned using MUSCLE (Edgar, <xref ref-type="bibr" rid="B39">2004</xref>).</p></sec>
<sec>
<title>Literature search</title>
<p>The literature search was conducted using databases such as PubMed, Google Scholar, and Web of Sciences, to overview the published studies regarding the detection of <italic>C. burnetii</italic> in different ticks, animals, humans, or soil in Asia. The keywords used for the search were as follows: tick(s), small ruminant(s), livestock, <italic>C. burnetii</italic>, Coxiellosis, and Q-fever. Combinations of the aforementioned various keywords were used to retrieve full-text research articles, review articles, short communications, and conference papers. Reference lists of retrieved articles were screened to identify relevant articles (accessed on 16 April 2023) (<xref ref-type="table" rid="T2">Table 2</xref>).</p>
<table-wrap position="float" id="T2">
<label>Table 2</label>
<caption><p><italic>Coxiella burnetii</italic> detected in different ticks, animals, humans, or soil samples in Asia.</p></caption> 
<table frame="box" rules="all">
<thead>
<tr style="background-color:#919497;color:#ffffff">
<th valign="top" align="left"><bold>Country/year</bold></th>
<th valign="top" align="left"><bold>Tick spp./source</bold></th>
<th valign="top" align="left"><bold>Detected/infested host</bold></th>
<th valign="top" align="left"><bold>Serologically/molecularly</bold></th>
<th valign="top" align="left"><bold>Reference</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Abu Dhabi/2021</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Camels</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">El Tigani-Asil et al., <xref ref-type="bibr" rid="B41">2021</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Afghanistan/2012&#x02013;2013</td>
<td valign="top" align="left" rowspan="2">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left" rowspan="2">Serologically</td>
<td valign="top" align="left" rowspan="2">Akbarian et al., <xref ref-type="bibr" rid="B6">2015</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Livestock</td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Armenia/1971-1974</td>
<td valign="top" align="left" rowspan="2">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left" rowspan="2">Serologically</td>
<td valign="top" align="left" rowspan="2">Tarasevi&#x0010D; et al., <xref ref-type="bibr" rid="B102">1976</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
</tr> <tr>
<td valign="top" align="left">Azerbaijan/2018</td>
<td valign="top" align="left">Milk</td>
<td valign="top" align="left">Goats, sheep</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Khademi et al., <xref ref-type="bibr" rid="B60">2020</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Bangladesh/2018-2021</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Cattle and goats, Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left" rowspan="2">Chakrabartty et al., <xref ref-type="bibr" rid="B27">2021</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Milk samples</td>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left">Molecularly (PCR)</td>
</tr> <tr>
<td valign="top" align="left">Bhutan/2014-2015</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans (patients)</td>
<td valign="top" align="left">Serologically and Molecularly (PCR)</td>
<td valign="top" align="left">Tshokey et al., <xref ref-type="bibr" rid="B106">2018</xref></td>
</tr> <tr>
<td valign="top" align="left">Bhutan/2015</td>
<td/>
<td valign="top" align="left">Goats</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Tshokey et al., <xref ref-type="bibr" rid="B107">2019</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Bangladesh/2007-2008</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Cattle, goats, sheep</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left" rowspan="2">Rahman et al., <xref ref-type="bibr" rid="B87">2016</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Placenta</td>
<td valign="top" align="left">Sheep</td>
<td valign="top" align="left">Molecularly (PCR)</td>
</tr> <tr>
<td valign="top" align="left">Cambodia/2019</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Goats</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Siengsanan-Lamont et al., <xref ref-type="bibr" rid="B96">2023</xref></td>
</tr> <tr>
<td valign="top" align="left">China</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically and Molecularly (PCR)</td>
<td valign="top" align="left">El-Mahallawy et al., <xref ref-type="bibr" rid="B43">2016</xref></td>
</tr> <tr>
<td valign="top" align="left">China/2018</td>
<td valign="top" align="left">Tissue (spleens)</td>
<td valign="top" align="left">Hedgehogs</td>
<td valign="top" align="left">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Gong et al., <xref ref-type="bibr" rid="B48">2020</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="9">China/2018-2019</td>
<td valign="top" align="left"><italic>D. nuttalli</italic></td>
<td valign="top" align="left" rowspan="9">Cattle, sheep</td>
<td valign="top" align="left" rowspan="9">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left" rowspan="9">Ni et al., <xref ref-type="bibr" rid="B76">2020</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>D. pavlovskyi</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>D. silvarum</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>D. niveus</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. rufipes</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. asiaticum</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. sanguineus</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. punctata</italic></td>
</tr> <tr>
<td valign="top" align="left" rowspan="3">Cyprus</td>
<td valign="top" align="left" rowspan="2">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left" rowspan="2">Serologically</td>
<td valign="top" align="left" rowspan="3">Psaroulaki et al., <xref ref-type="bibr" rid="B86">2006</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Goats and sheep</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. sanguineus</italic> and <italic>Hyalomma</italic> spp.</td>
<td valign="top" align="left">Goats and sheep</td>
<td valign="top" align="left">Molecularly (PCR)</td>
</tr> <tr>
<td valign="top" align="left">Hong Kong/2008</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Chan et al., <xref ref-type="bibr" rid="B28">2010</xref></td>
</tr> <tr>
<td valign="top" align="left">India</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Sahu et al., <xref ref-type="bibr" rid="B91">2018</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">India/2018-2019</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Goats</td>
<td valign="top" align="left">Serologically and Molecularly (PCR and sequencing)</td>
<td valign="top" align="left" rowspan="2">Patra et al., <xref ref-type="bibr" rid="B84">2020</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left">Iran/2013-2016</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Esmaeili et al., <xref ref-type="bibr" rid="B44">2019</xref></td>
</tr> <tr>
<td valign="top" align="left">Iran/2017&#x02013;2018</td>
<td valign="top" align="left">Aborted samples</td>
<td valign="top" align="left">Cattle, sheep, and goats</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Mohabati Mobarez et al., <xref ref-type="bibr" rid="B72">2021</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Spleen, liver, and cotyledons</td>
</tr> <tr>
<td valign="top" align="left">Iraq/2019</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Camels</td>
<td valign="top" align="left">Serologically and Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Al-Graibawi et al., <xref ref-type="bibr" rid="B8">2021</xref></td>
</tr> <tr>
<td valign="top" align="left">Iraq/2007</td>
<td valign="top" align="left">Topsoil and airborne dust</td>
<td/>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Leski et al., <xref ref-type="bibr" rid="B70">2011</xref></td>
</tr> <tr>
<td valign="top" align="left">Iraq/2018-2019</td>
<td valign="top" align="left">Blood and milk</td>
<td valign="top" align="left">Cows</td>
<td valign="top" align="left">Serologically and Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Gharban and Yousif, <xref ref-type="bibr" rid="B47">2020</xref></td>
</tr>
<tr>
<td valign="top" align="left">Iraq/2005</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans (US military)</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Royal et al., <xref ref-type="bibr" rid="B90">2013</xref></td>
</tr> <tr>
<td valign="top" align="left">Israel/2005</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically and Molecularly (PCR)</td>
<td valign="top" align="left">Amitai et al., <xref ref-type="bibr" rid="B18">2010</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Israel</td>
<td valign="top" align="left"><italic>Hy. dromedarii</italic></td>
<td valign="top" align="left">Camels</td>
<td valign="top" align="left" rowspan="2">Molecularly (PCR)</td>
<td valign="top" align="left" rowspan="2">Mumcuoglu et al., <xref ref-type="bibr" rid="B74">2022</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. aegyptium</italic></td>
<td valign="top" align="left">Tortoises</td>
</tr> <tr>
<td valign="top" align="left">Indonesia/2017</td>
<td valign="top" align="left">Tissue</td>
<td valign="top" align="left">Cows, goats, sheep</td>
<td valign="top" align="left">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Rini et al., <xref ref-type="bibr" rid="B88">2022</xref></td>
</tr> <tr>
<td valign="top" align="left">Japan/1996&#x02013;1997</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Kato et al., <xref ref-type="bibr" rid="B59">1998</xref></td>
</tr> <tr>
<td valign="top" align="left">Jordan/2015&#x02013;2016</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Obaidat et al., <xref ref-type="bibr" rid="B81">2019</xref></td>
</tr> <tr>
<td valign="top" align="left">Jordan/2015&#x02013;2017</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Goats, sheep</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Lafi et al., <xref ref-type="bibr" rid="B67">2020</xref></td>
</tr> <tr>
<td valign="top" align="left">Kazakhstan/2021&#x02013;2022</td>
<td valign="top" align="left"><italic>D. marginatus</italic> and <italic>Hy. anatolicum</italic></td>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Sultankulova et al., <xref ref-type="bibr" rid="B99">2022</xref></td>
</tr> <tr>
<td valign="top" align="left">Korea/2016</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Lee et al., <xref ref-type="bibr" rid="B68">2020</xref></td>
</tr> <tr>
<td valign="top" align="left">Kuwait/2007</td>
<td valign="top" align="left">Topsoil and airborne dust</td>
<td/>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Leski et al., <xref ref-type="bibr" rid="B70">2011</xref></td>
</tr> <tr>
<td valign="top" align="left">Lebanon/2015</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Dabaja et al., <xref ref-type="bibr" rid="B33">2018</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="6">Lebanon/2014</td>
<td valign="top" align="left"><italic>R. annulatus</italic></td>
<td valign="top" align="left" rowspan="5">Cattle, sheep, goats</td>
<td valign="top" align="left" rowspan="5">Molecularly (PCR)</td>
<td valign="top" align="left" rowspan="6">Dabaja et al., <xref ref-type="bibr" rid="B32">2020</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. turanicus</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. sanguineus</italic></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. bursa</italic></td>
</tr>
 <tr>
<td valign="top" align="left">Milk</td>
<td valign="top" align="left">Serologically</td>
</tr> <tr>
<td valign="top" align="left">Laos/2016&#x02013;2017</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Goats</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Burns et al., <xref ref-type="bibr" rid="B25">2018</xref></td>
</tr> <tr>
<td valign="top" align="left">Malaysia/2012&#x02013;2013</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Khor et al., <xref ref-type="bibr" rid="B63">2018</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="4">Malaysia/2013</td>
<td valign="top" align="left">Blood and vaginal sample</td>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left" rowspan="4">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left" rowspan="4">Nurkunasegran et al., <xref ref-type="bibr" rid="B79">2017</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Amblyomma</italic> and <italic>Dermacentor</italic> spp.</td>
<td valign="top" align="left">Rodents</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Haemaphysalis</italic> spp.</td>
<td valign="top" align="left">Vegetation</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>R. sanguineus</italic> and <italic>Dermacentor</italic> spp.</td>
<td valign="top" align="left">Dogs</td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Mongolia/2008&#x02013;2015</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Snow leopards</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left" rowspan="2">Esson et al., <xref ref-type="bibr" rid="B45">2019</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Ticks</td>
<td/>
<td valign="top" align="left">Molecularly (PCR)</td>
</tr> <tr>
<td valign="top" align="left">Nepal/2016</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Panth et al., <xref ref-type="bibr" rid="B83">2017</xref></td>
</tr> <tr>
<td valign="top" align="left">Oman/2019</td>
<td valign="top" align="left">Blood/bone</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Al-Kindi et al., <xref ref-type="bibr" rid="B15">2022</xref></td>
</tr> <tr>
<td valign="top" align="left">Pakistan</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans, goats, sheep, buffaloes, cows, Rodents</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Ahmed, <xref ref-type="bibr" rid="B3">1987</xref></td>
</tr> <tr>
<td valign="top" align="left">Pakistan</td>
<td valign="top" align="left">Soil</td>
<td valign="top" align="left">Soil</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Shabbir et al., <xref ref-type="bibr" rid="B95">2015</xref></td>
</tr> <tr>
<td valign="top" align="left">Pakistan</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Camels</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Hussain et al., <xref ref-type="bibr" rid="B55">2022</xref></td>
</tr> <tr>
<td valign="top" align="left">Pakistan/2016</td>
<td valign="top" align="left">Ticks and blood</td>
<td valign="top" align="left">Goats and sheep</td>
<td valign="top" align="left">Serologically and Molecularly (PCR)</td>
<td valign="top" align="left">Ullah et al., <xref ref-type="bibr" rid="B108">2019</xref></td>
</tr> <tr>
<td valign="top" align="left">Pakistan</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Ali et al., <xref ref-type="bibr" rid="B12">2022a</xref></td>
</tr> <tr>
<td valign="top" align="left">Palestine/2016</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Rams</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Jalboush and Alzuheir, <xref ref-type="bibr" rid="B56">2017</xref></td>
</tr> <tr>
<td valign="top" align="left">Qatar/2005&#x02013;2006</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans (US military)</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Royal et al., <xref ref-type="bibr" rid="B90">2013</xref></td>
</tr> <tr>
<td valign="top" align="left">Saudi Arabia</td>
<td valign="top" align="left">Blood, milk, feces, and urine</td>
<td valign="top" align="left">Camels, cattle, and goats</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Mohammed et al., <xref ref-type="bibr" rid="B73">2014</xref></td>
</tr>
<tr>
<td valign="top" align="left">Saudi Arabia/2011&#x02013;2013</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Almogren et al., <xref ref-type="bibr" rid="B16">2013</xref></td>
</tr> <tr>
<td valign="top" align="left">South Korea/2007&#x02013;2013</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Horses</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Seo et al., <xref ref-type="bibr" rid="B94">2016</xref></td>
</tr> <tr>
<td valign="top" align="left">Taiwan/2007</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Chang et al., <xref ref-type="bibr" rid="B29">2010</xref></td>
</tr> <tr>
<td valign="top" align="left">Taiwan/2009&#x02013;2011</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Dogs</td>
<td valign="top" align="left">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left">Chou et al., <xref ref-type="bibr" rid="B30">2014</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="3">Thailand/2012&#x02013;2013</td>
<td valign="top" align="left" rowspan="2">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left" rowspan="3">Serologically and Molecularly (PCR)</td>
<td valign="top" align="left" rowspan="3">Doung-Ngern et al., <xref ref-type="bibr" rid="B37">2017</xref></td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
</tr>
 <tr>
<td valign="top" align="left">Milk</td>
<td valign="top" align="left">Cattle</td>
</tr> <tr>
<td valign="top" align="left">Turkey</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Cows, sheep, goats</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Ozgen et al., <xref ref-type="bibr" rid="B82">2022</xref></td>
</tr> <tr>
<td valign="top" align="left">Turkey/2007</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Humans</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Kilic et al., <xref ref-type="bibr" rid="B64">2008</xref></td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Tunisia/2015&#x02013;2017</td>
<td valign="top" align="left"><italic>Hy. impeltatum</italic></td>
<td valign="top" align="left" rowspan="2">Camels</td>
<td valign="top" align="left" rowspan="2">Molecularly (PCR and sequencing)</td>
<td valign="top" align="left" rowspan="2">Selmi et al., <xref ref-type="bibr" rid="B93">2019</xref></td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. dromedarii</italic></td>
</tr> <tr>
<td valign="top" align="left">United Arab Emirates</td>
<td valign="top" align="left">Blood</td>
<td valign="top" align="left">Goats, sheep</td>
<td valign="top" align="left">Serologically</td>
<td valign="top" align="left">Barigye et al., <xref ref-type="bibr" rid="B22">2022</xref></td>
</tr>
<tr>
<td valign="top" align="left">Vietnam</td>
<td valign="top" align="left">Bone marrow</td>
<td valign="top" align="left">Humans (patient)</td>
<td valign="top" align="left">Molecularly (PCR)</td>
<td valign="top" align="left">Thi Vinh An et al., <xref ref-type="bibr" rid="B103">2022</xref></td>
</tr>
</tbody>
</table>
</table-wrap></sec></sec>
<sec sec-type="results" id="s3">
<title>Results</title>
<sec>
<title>Hosts prevalence</title>
<p>The highest number of observed hosts (374/678, 55.2%) were included in a group having age &#x0003E; 3 years, followed by various hosts (192/678, 28.3%) having age 1&#x02013;3 years, and the lowest numbers of observed hosts (112/678, 16.5%) belonging to the age group having age &#x0003C; 1 year. Different hosts having age &#x0003E;3 years were highly infested (192/345, 55.6%), while animals having age &#x02264; 1 year were least infested (62/345, 18.0%). The examined and infested female hosts were more predominant in number (486/678; 71.7%, 237/345; 68.7%) than male hosts (192/678; 28.3%, 108/345; 31.3%). The highest number of infested hosts was recorded in summer (June&#x02013;August) (146/345, 42.3%), followed by spring (March&#x02013;May) (99/345, 28.7%), autumn (September&#x02013;November) (65/345, 18.8%), and winter (December&#x02013;February) (35/345, 10.4%), respectively (<xref ref-type="table" rid="T3">Table 3</xref>).</p>
<table-wrap position="float" id="T3">
<label>Table 3</label>
<caption><p>Age, gender, and season-wise infestation rate of hosts.</p></caption> 
<table frame="box" rules="all">
<thead>
<tr style="background-color:#919497;color:#ffffff">
<th valign="top" align="center" colspan="2"><bold>Variables</bold></th>
<th valign="top" align="center"><bold>Observed host (%)</bold></th>
<th valign="top" align="center"><bold>Infested hosts (%)</bold></th>
<th valign="top" align="center"><bold>Total infested/total observed (%)</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" rowspan="3">Age</td>
<td valign="top" align="left">&#x0003C; 1 year</td>
<td valign="top" align="center">112 (16.5)</td>
<td valign="top" align="center">62 (18.0)</td>
<td valign="top" align="center" rowspan="3">345/678 (52.1)</td>
</tr>
 <tr>
<td valign="top" align="left">1&#x02013;3 years</td>
<td valign="top" align="center">192 (28.3)</td>
<td valign="top" align="center">91 (26.4)</td>
</tr>
 <tr>
<td valign="top" align="left">&#x0003E;3 years</td>
<td valign="top" align="center">374 (55.2)</td>
<td valign="top" align="center">192 (55.6)</td>
</tr> <tr>
<td valign="top" align="left" rowspan="2">Gender</td>
<td valign="top" align="center">Female</td>
<td valign="top" align="center">486 (71.7)</td>
<td valign="top" align="center">237 (68.7)</td>
<td valign="top" align="center" rowspan="2">345/678 (52.1)</td>
</tr>
 <tr>
<td valign="top" align="left">Male</td>
<td valign="top" align="center">192 (28.3)</td>
<td valign="top" align="center">108 (31.3)</td>
</tr> <tr>
<td valign="top" align="left" rowspan="4">Seasons</td>
<td valign="top" align="left">Spring (March&#x02013;May)</td>
<td valign="top" align="center">163 (24.0)</td>
<td valign="top" align="center">99 (28.7)</td>
<td valign="top" align="center" rowspan="4">345/678 (52.1)</td>
</tr>
 <tr>
<td valign="top" align="left">Summer (June&#x02013;August)</td>
<td valign="top" align="center">191 (28.2)</td>
<td valign="top" align="center">146 (42.3)</td>
</tr>
 <tr>
<td valign="top" align="left">Autumn (September&#x02013;November)</td>
<td valign="top" align="center">165 (24.3)</td>
<td valign="top" align="center">65 (18.8)</td>
</tr>

<tr>
<td valign="top" align="left">Winter (December&#x02013;February)</td>
<td valign="top" align="center">159 (23.4)</td>
<td valign="top" align="center">35 (10.1)</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>A total of 678 different hosts such as goats, sheep, camels, cattle, wild mice, and domestic fowls were examined for tick collection in the selected localities, of which other hosts (number = 345/678, 50.9%), including goats (78/149, 52.3%), sheep (75/136, 55.1%), camels (36/93, 38.7%), cattle (69/129, 53.5%), wild mice (15/48, 31.2%), and domestic fowls (72/123, 58.5%) were found tick infested. The highest prevalence of infested hosts was recorded in district Lakki Marwat (44/351, 12.5%), followed by Charsadda (36/351, 10.3%), Nowshera, Buner, Mansehra, and Abbottabad (35/351, 9.7%), Chitral (34/351, 9.7%), Dir Upper and Dir Lower (33/351, 9.4%), while least infestation rate was recorded in district Bajaur (31/351, 8.8%) (<xref ref-type="table" rid="T4">Table 4</xref>).</p>
<table-wrap position="float" id="T4">
<label>Table 4</label>
<caption><p>Occurrence of ticks and molecular detection of <italic>Coxiella</italic> spp. in different districts of Khyber Pakhtunkhwa.</p></caption> 
<table frame="box" rules="all">
<thead>
<tr style="background-color:#919497;color:#ffffff">
<th valign="top" align="left"><bold>Districts</bold></th>
<th valign="top" align="left" colspan="3"><bold>Hosts</bold></th>
<th valign="top" align="left"><bold>Tick species</bold></th>
<th valign="top" align="left"><bold>Ticks life stages</bold></th>
<th valign="top" align="left"><bold>Molecularly analyzed (DNA extraction and PCR)</bold></th>
<th valign="top" align="left" colspan="8"><bold>Molecularly screened</bold> <italic><bold>Coxiella</bold></italic> <bold>spp</bold>.</th>
</tr>
<tr style="background-color:#919497;color:#ffffff">
<th/>
<th valign="top" align="left"><bold>Animal type</bold> </th>
<th valign="top" align="center"><bold>Observed</bold> </th>
<th valign="top" align="center"><bold>Infested</bold> </th>
<th/>
<th valign="top" align="center"><bold>(N, F, M) Total</bold> </th>
<th valign="top" align="center"><bold>(N, F, M) Total</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella burnetii</bold></italic> <bold>(OQ883856)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>endosymbiont (OQ883857)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>endosymbiont (OQ883858)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>sp. (OQ883859)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>sp. (OQ883860)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>sp. (OQ883861)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>sp. (OQ883862)</bold> </th>
<th valign="top" align="center"><italic><bold>Coxiella</bold></italic> <bold>sp. (OQ883863)</bold> </th>
</tr>
</thead>
<tbody>
 <tr>
<td valign="top" align="left" rowspan="12">Lakki Marwat</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="center" rowspan="3">19</td>
<td valign="top" align="center" rowspan="3">8</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="center">(6 N, 2 F, 3 M) 11</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="center" rowspan="3">18</td>
<td valign="top" align="center" rowspan="3">7</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(5 N, 2 F, 1 M) 8</td>
<td valign="top" align="center">(2 N, 1 F) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(7 N, 2 F, 3 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 1 F, 3 M) 9</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Camels</td>
<td valign="top" align="center" rowspan="2">31</td>
<td valign="top" align="center" rowspan="2">13</td>
<td valign="top" align="center"><italic>Hy. dromedarii</italic></td>
<td valign="top" align="center">(6 N, 3 F, 3 M) 12</td>
<td valign="top" align="center">(3 N, 1 F, 2 M) 6</td>
<td valign="top" align="center">2 N, 1 F</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(8 N, 4 F, 3 M) 15</td>
<td valign="top" align="center">(2 N, 1 F, 1 M) 4</td>
<td valign="top" align="center">1 N, 1 F</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="center" rowspan="2">17</td>
<td valign="top" align="center" rowspan="2">8</td>
<td valign="top" align="center"><italic>R. microplus</italic></td>
<td valign="top" align="center">(10 N, 3 F, 4 M) 17</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(6 N, 4 F, 1 M) 11</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="center">4</td>
<td valign="top" align="center">2</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(4 N, 3 F) 7</td>
<td valign="top" align="center">(2 N, 1 F) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="center">17</td>
<td valign="top" align="center">6</td>
<td valign="top" align="center"><italic>A. persicus</italic></td>
<td valign="top" align="center">(8 N, 4 F, 2 M) 14</td>
<td valign="top" align="center">(2 N, 1 F, 1 M) 4</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="12">Charsadda</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="center" rowspan="3">17</td>
<td valign="top" align="center" rowspan="3">7</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(6 N, 3 F, 3 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="center">(5 N, 2 F, 2 M) 9</td>
<td valign="top" align="center">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="center" rowspan="3">15</td>
<td valign="top" align="center" rowspan="3">5</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(4 N, 2 F, 2 M) 8</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="center">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 2 F, 2 M) 9</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Camels</td>
<td valign="top" align="center" rowspan="2">26</td>
<td valign="top" align="center" rowspan="2">8</td>
<td valign="top" align="center"><italic>Hy. dromedarii</italic></td>
<td valign="top" align="center">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(5 N, 4 F, 2 M) 11</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="left" rowspan="2">15</td>
<td valign="top" align="left" rowspan="2">7</td>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td valign="top" align="left">(10 N, 6 F, 1 M) 17</td>
<td valign="top" align="left">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="left">(8 N, 4 F, 3 M) 15</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="left">11</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(4 N, 3 M) 7</td>
<td valign="top" align="left">(4 N, 1 F) 5</td>
<td valign="top" align="left">3 N, 1 F</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="left">13</td>
<td valign="top" align="left">6</td>
<td valign="top" align="left"><italic>A. persicus</italic></td>
<td valign="top" align="left">(9 N, 4 F, 3 M) 16</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="8">Nowshera</td>
<td valign="top" align="left" rowspan="2">Goats</td>
<td valign="top" align="left" rowspan="2">19</td>
<td valign="top" align="left" rowspan="2">7</td>
<td valign="top" align="left"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="left">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(6 N, 3 F, 3 M) 12</td>
<td valign="top" align="left">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Sheep</td>
<td valign="top" align="left" rowspan="2">11</td>
<td valign="top" align="left" rowspan="2">6</td>
<td valign="top" align="left"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="left">(5 N, 4 F, 1 M) 10</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="left">(4 N, 2 F, 2 M) 8</td>
<td valign="top" align="left">(2 N) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Camels</td>
<td valign="top" align="left">21</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left"><italic>Hy. dromedarii</italic></td>
<td valign="top" align="left">(7 N, 2 F, 3 M) 12</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left">13</td>
<td valign="top" align="left">6</td>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td valign="top" align="left">(8 N, 4 F, 2 M) 14</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(4 N, 1 F, 1 M) 6</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="left">15</td>
<td valign="top" align="left">7</td>
<td valign="top" align="left"><italic>A. persicus</italic></td>
<td valign="top" align="left">(9 N, 2 F, 3 M) 14</td>
<td valign="top" align="left">(2 N, 1 F) 3</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="9">Dir Upper</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="left" rowspan="3">16</td>
<td valign="top" align="left" rowspan="3">9</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(7 N, 3 F, 3 M) 13</td>
<td valign="top" align="left">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="left">(6 N, 2 F, 3 M) 11</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">1 N, 1 M</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. danieli</italic></td>
<td valign="top" align="left">(8 N, 4 F, 2 M) 14</td>
<td valign="top" align="left">(3 N, 2 F, 1 M) 6</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="left" rowspan="3">15</td>
<td valign="top" align="left" rowspan="3">7</td>
<td valign="top" align="left"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="left">(5 N, 3 F, 2 M) 10</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="left">(6 N, 2 F, 1 M) 9</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="left">12</td>
<td valign="top" align="left">10</td>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td valign="top" align="left">(9 N, 2 F, 4 M) 15</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="left">2</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(4 N, 2 F, 2 M) 8</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
<tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="left">10</td>
<td valign="top" align="left">6</td>
<td valign="top" align="left"><italic>A. persicus</italic></td>
<td valign="top" align="left">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="8">Dir Lower</td>
<td valign="top" align="left" rowspan="2">Goats</td>
<td valign="top" align="left" rowspan="2">13</td>
<td valign="top" align="left" rowspan="2">10</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(5 N, 2 F, 2 M) 9</td>
<td valign="top" align="left">(5 N, 2 F, 1 M) 8</td>
<td valign="top" align="left">1 N, 1 F</td>
<td valign="top" align="left">2 N, 1 F</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">1 N, 1 M</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="left">(6 N, 3 F, 3 M) 12</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Sheep</td>
<td valign="top" align="left" rowspan="2">14</td>
<td valign="top" align="left" rowspan="2">9</td>
<td valign="top" align="left"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="left">(4 N, 2 F, 2 M) 8</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(8 N, 3 F, 3 M) 14</td>
<td valign="top" align="left">(2 N, 1 F, 2 M) 5</td>
<td valign="top" align="left">1 N, 1 F, 2 M</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="left" rowspan="2">13</td>
<td valign="top" align="left" rowspan="2">5</td>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td valign="top" align="left">(7 N, 4 F, 2 M) 13</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="left">(9 N, 4 F, 2 M) 15</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(5 N, 5 F) 10</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="left">11</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left"><italic>A. persicus</italic></td>
<td valign="top" align="left">(8 N, 3 F, 3 M) 14</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="10">Buner</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="left" rowspan="3">14</td>
<td valign="top" align="left" rowspan="3">7</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(5 N, 4 F, 2 M) 11</td>
<td valign="top" align="left">(2 N) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="left">(8 N, 3 F, 5 M) 16</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="left">(6 N, 4 F) 10</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="left" rowspan="3">13</td>
<td valign="top" align="left" rowspan="3">10</td>
<td valign="top" align="left"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="left">(5 N, 2 F, 2 M) 9</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="left">(6 N, 5 F, 1 M) 12</td>
<td valign="top" align="left">(2 N, 1 F) 3</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">2 N, 1 F</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(5 N, 4 F, 1 M) 10</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="left" rowspan="2">11</td>
<td valign="top" align="left" rowspan="2">9</td>
<td valign="top" align="left"><italic>R. microplus</italic></td>
<td valign="top" align="left">(8 N, 4 F, 3 M) 15</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="left">(7 N, 3 F, 3 M) 13</td>
<td valign="top" align="left">(1 N, 1 M) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="left">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="left">(1 N) 1</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="left">13</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left"><italic>A. persicus</italic></td>
<td valign="top" align="left">(6 N, 5 F, 2 M) 13</td>
<td valign="top" align="left">(1 N, 1 F) 2</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="9">Mansehra</td>
<td valign="top" align="left" rowspan="2">Goats</td>
<td valign="top" align="center" rowspan="2">12</td>
<td valign="top" align="center" rowspan="2">8</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 2 F, 1 M) 8</td>
<td valign="top" align="center">(2 N, 1 F) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(7 N, 3 F, 4 M) 14</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="center" rowspan="3">10</td>
<td valign="top" align="center" rowspan="3">9</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(6 N, 2 F, 3 M) 11</td>
<td valign="top" align="center">(3 N, 1 F, 2 M) 6</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">2 N, 1 F, 1 M</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(4 N, 3 F) 7</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(6 N, 2 F, 2 M) 10</td>
<td valign="top" align="center">(2 N) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="center" rowspan="2">14</td>
<td valign="top" align="center" rowspan="2">9</td>
<td valign="top" align="center"><italic>R. microplus</italic></td>
<td valign="top" align="center">(9 N, 4 F, 3 M) 16</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(7 N, 3 F, 4 M) 14</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="center">5</td>
<td valign="top" align="center">2</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 2 F, 3 M) 10</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="center">9</td>
<td valign="top" align="center">7</td>
<td valign="top" align="center"><italic>A. persicus</italic></td>
<td valign="top" align="center">(9 N, 3 F, 4 M) 16</td>
<td valign="top" align="center">(2 N, 1 F) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="8">Bajaur</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="center" rowspan="3">16</td>
<td valign="top" align="center" rowspan="3">6</td>
<td valign="top" align="center"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="center">(5 N, 4 F, 3 M) 12</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(9 N, 3 F, 4 M) 16</td>
<td valign="top" align="center">(3 N, 1 F, 1 M) 5</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(4 N, 5 F) 9</td>
<td valign="top" align="center">(2 N, 1 F) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">1 F</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Sheep</td>
<td valign="top" align="center" rowspan="2">17</td>
<td valign="top" align="center" rowspan="2">7</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(6 N, 3 F, 3 M) 12</td>
<td valign="top" align="center">(2 N) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(8 N, 2 F, 4 M) 14</td>
<td valign="top" align="center">(3 N, 1 F, 1 M) 5</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">2 N</td>
<td valign="top" align="center">1 F</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="center">12</td>
<td valign="top" align="center">8</td>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(7 N, 4 F, 3 M) 14</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="center">8</td>
<td valign="top" align="center">1</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 4 F, 1 M) 10</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="center">14</td>
<td valign="top" align="center">9</td>
<td valign="top" align="center"><italic>A. persicus</italic></td>
<td valign="top" align="center">(8 N, 3 F, 3 M) 14</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="11">Abbottabad</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="center" rowspan="3">13</td>
<td valign="top" align="center" rowspan="3">9</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(6 N, 2 F, 4 M) 12</td>
<td valign="top" align="center">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(5 N, 2 F, 3 M) 10</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="left">(4N, 3 F, 1M) 8</td>
<td valign="top" align="left">(3N, 1 F, 1M) 5</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">&#x02013;</td>
<td valign="top" align="left">2N,1F</td>
<td valign="top" align="left">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="center" rowspan="3">12</td>
<td valign="top" align="center" rowspan="3">6</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(7 N, 2 F, 3 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(6 N, 4 F, 2 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Camels</td>
<td valign="top" align="center" rowspan="2">15</td>
<td valign="top" align="center" rowspan="2">7</td>
<td valign="top" align="center"><italic>Hy. dromedarii</italic></td>
<td valign="top" align="center">(6 N, 4 F, 1 M) 11</td>
<td valign="top" align="center">(2 N) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(9 N, 5 F, 14</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Cattle</td>
<td valign="top" align="center">9</td>
<td valign="top" align="center">7</td>
<td valign="top" align="center"><italic>R. microplus</italic></td>
<td valign="top" align="center">(9 N, 4 F, 3 M) 16</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="center">3</td>
<td valign="top" align="center">1</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 2 M) 7</td>
<td valign="top" align="center">(2 N, 1 M) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="center">9</td>
<td valign="top" align="center">5</td>
<td valign="top" align="center"><italic>A. persicus</italic></td>
<td valign="top" align="center">(8 N, 4 F, 3 M) 15</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr> <tr>
<td valign="top" align="left" rowspan="10">Chitral</td>
<td valign="top" align="left" rowspan="3">Goats</td>
<td valign="top" align="center" rowspan="3">10</td>
<td valign="top" align="center" rowspan="3">7</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 2 F, 2 M) 9</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(8 N, 3 F, 1 M) 12</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. bispinosa</italic></td>
<td valign="top" align="center">(6 N, 2 F, 2 M) 10</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="3">Sheep</td>
<td valign="top" align="center" rowspan="3">11</td>
<td valign="top" align="center" rowspan="3">9</td>
<td valign="top" align="center"><italic>R. haemaphysaloides</italic></td>
<td valign="top" align="center">(5 N, 3 F) 8</td>
<td valign="top" align="center">(2 N) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. montgomeryi</italic></td>
<td valign="top" align="center">(7 N, 3 F, 2 M) 12</td>
<td valign="top" align="center">(1 N, 1 M) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(5 N, 3 F, 1 M) 9</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left" rowspan="2">Cattle</td>
<td valign="top" align="center" rowspan="2">13</td>
<td valign="top" align="center" rowspan="2">6</td>
<td valign="top" align="center"><italic>Hy. anatolicum</italic></td>
<td valign="top" align="center">(5 N, 3 F, 3 M) 11</td>
<td valign="top" align="center">(1 N, 1 F) 2</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="center"><italic>R. microplus</italic></td>
<td valign="top" align="center">(7 N, 4 F, 3 M) 14</td>
<td valign="top" align="center">(1 N, 1 F, 1 M) 3</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Wild mice</td>
<td valign="top" align="center">4</td>
<td valign="top" align="center">2</td>
<td valign="top" align="center"><italic>Ha. cornupunctata</italic></td>
<td valign="top" align="center">(4 N, 2 F, 1 M) 7</td>
<td valign="top" align="center">(1 N) 1</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
 <tr>
<td valign="top" align="left">Domestic fowls</td>
<td valign="top" align="center">12</td>
<td valign="top" align="center">10</td>
<td valign="top" align="center"><italic>A. persicus</italic></td>
<td valign="top" align="center">(9 N, 5 F, 4 M) 18</td>
<td valign="top" align="center">(5 N, 1 F, 1 M) 7</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">2 N, 1 F, 1 M</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
<td valign="top" align="center">&#x02013;</td>
</tr>
<tr>
<td valign="top" align="left">Total</td>
<td valign="top" align="center"><bold>678</bold></td>
<td valign="top" align="center"><bold>345</bold> (50.9%)</td>
<td valign="top" align="center">(613 N, 293 F, 213 M) <bold>1,119</bold></td>
<td valign="top" align="center">(137 N, 49 F, 41 M) <bold>227</bold></td>
<td valign="top" align="center"><bold>15</bold> (6.7%)</td>
<td valign="top" align="center"><bold>14</bold> (6.3%)</td>
<td valign="top" align="center" colspan="6"><bold>11</bold> (4.9%)</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec>
<title>Ticks and their molecular analyses</title>
<p>Altogether, 1,119 ticks including nymphs (613/1,119, 54.8%), adult females (293/1,119, 26.2%), and males (213/1,119, 19.0%) were collected from infested hosts and were categorized into four genera (<italic>Haemaphysalis, Hyalomma, Rhipicephalus</italic>, and <italic>Argas</italic>). The highest number of collected tick species was <italic>Ha. cornupunctata</italic> (258/1,119, 23.1%), followed by <italic>Hy. anatolicum</italic> (209/1,119, 18.7%), <italic>A. persicus</italic> (146/1,119, 13.0%), <italic>R. microplus</italic> (137/1,119, 12.2%), <italic>Ha. montgomeryi</italic> (119/1,119, 10.6%), <italic>R. haemaphysaloides</italic> (97/1,119, 8.7%), <italic>Ha. bispinosa</italic> (92/1,119, 8.2%), <italic>Hy. dromedarii</italic> (47/1,119, 4.2%), and <italic>Ha. danieli</italic> (14/1,119, 1.2%). Genomic DNA was extracted from 227 morphologically identified ticks (137 N, 49 F, and 41 M), and all identified tick species were molecularly confirmed <italic>via</italic> sequencing of the <italic>cox1</italic> partial fragment (<xref ref-type="table" rid="T4">Table 4</xref>).</p></sec>
<sec>
<title>Screening of <italic>Coxiella</italic> in various ticks</title>
<p>Extracted DNA of 227 (20.3%) was used to amplify the fragments of <italic>GroEL</italic> of <italic>Coxiella</italic> spp. A total of 40/227 (17.6%) ticks were found positive for <italic>Coxiella</italic> spp., including <italic>C. burnetii</italic> (15, 6.7%), <italic>Coxiella</italic> endosymbionts (14, 6.3%), and <italic>Coxiella</italic> sp. (11, 4.9%). <italic>Coxiella burnetii</italic> was detected in ticks collected from camels (<italic>Hy. dromedarii</italic> and <italic>Hy. anatolicum</italic>) in the district of Lakki Marwat, wild mice (<italic>Ha. cornupunctata</italic>) in Charsadda, and goats and sheep (<italic>Ha. cornupunctata</italic>) in Dir Lower. <italic>Coxiella</italic> endosymbionts were detected in ticks collected from goats (<italic>Ha. cornupunctata</italic>) in district Dir Lower sheep (<italic>Ha. montgomeryi</italic> and <italic>R. haemaphysaloides</italic>) in Buner and Mansehra, and domestic fowls (<italic>A. persicus</italic>) in Chitral. <italic>Coxiella</italic> spp. were detected in ticks collected from goats (<italic>Ha. bispinosa</italic>) in the district of Dir Upper, from goats (<italic>Ha. cornupunctata</italic>) in Dir Lower, from goats and sheep (<italic>Ha. cornupunctata</italic> and <italic>Ha. montgomeryi</italic>) in Bajaur, and from goats (<italic>Ha. bispinosa</italic>) in Abbottabad (<xref ref-type="table" rid="T4">Table 4</xref>).</p></sec>
<sec>
<title>Phylogenetic analyses of the obtained sequences</title>
<p>All amplified PCR products were separately sequenced. The identical sequences were considered as a single consensus sequence. Trimmed and purified sequences of <italic>cox1</italic> fragments were obtained from nine tick species, including <italic>Ha. cornupunctata, Ha. bispinosa, Ha. danieli, Ha. montgomeryi, Hy. anatolicum, Hy. dromedarii, R. haemaphysaloides, R. microplus</italic>, and <italic>A. persicus</italic>. The BLAST results showed that the <italic>cox1</italic> fragments of the nine tick species were 99.6&#x02013;100% identical to the corresponding species. Additionally, these sequences were phylogenetically clustered to the corresponding species reported from Pakistan, China, India, Bangladesh, Kazakhstan, Kenya, and Iran (<xref ref-type="fig" rid="F2">Figure 2</xref>).</p>
<fig id="F2" position="float">
<label>Figure 2</label>
<caption><p>Phylogenetic tree based on <italic>cox1</italic> fragments of tick species. The sequence of <italic>Alveonasus lahorensis</italic> (KX530868) was used as an outgroup. The levels of bootstrap support (&#x02265;60%) for phylogenetic groupings are given at each node. The obtained sequences are represented with bold and underlined fonts.</p></caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmicb-14-1229950-g0002.tif"/>
</fig>
<p>Based on the <italic>GroEL</italic> fragment, eight <italic>GroEL</italic> fragments of <italic>Coxiella</italic> spp. were detected in the aforementioned tick species except for <italic>Ha. danieli</italic> and <italic>R. microplus</italic>. By the BLAST results, the obtained <italic>GroEL</italic> fragment of <italic>Coxiella</italic> sp. (detected in <italic>Ha. cornupunctata, Hy. dromedarii</italic>, and <italic>Hy. anatolicum</italic>) showed maximum identity (99.8&#x02013;100%) with the <italic>C. burnetii</italic> and phylogenetically clustered with the corresponding species reported from Slovakia (MG860513), China (ON455116), Russia (EF627450), USA (CP040059), and Thailand (MZ327921).</p>
<p>The obtained <italic>GroEL</italic> fragment of <italic>Coxiella</italic> spp. (detected in <italic>Ha. cornupunctata, A. persicus</italic>, and <italic>R. haemaphysaloides</italic>) showed 100% identity with the <italic>Coxiella</italic> endosymbiont reported from China (MZ367034 and MZ367036). Another <italic>GroEL</italic> fragment of <italic>Coxiella</italic> sp. (detected in <italic>Ha. montgomeryi</italic>) showed 99.8% maximum identity with the <italic>Coxiella</italic> endosymbiont reported from France (KP985488) and China (KP985490). Both partial fragments clustered with the corresponding <italic>Coxiella</italic> endosymbiont in the phylogenetic tree.</p>
<p>The BLAST results of the obtained <italic>GroEL</italic> fragments of <italic>Coxiella</italic> sp. OQ883859 (detected in <italic>Ha. cornupunctata</italic>) showed 88&#x02013;90% maximum identity with <italic>Coxiella</italic> endosymbiont reported from the United Kingdom (KP985492), <italic>Coxiella</italic> sp. OQ883860 (detected in <italic>Ha. montgomeryi</italic>) showed 90.23% identity with <italic>Coxiella</italic> sp. reported from France (KP985502 and KP985500), Tunisia (KP985456), and Algeria (KP985472). The <italic>Coxiella</italic> sp. OQ883861 (detected in <italic>Ha. montgomeryi</italic>) showed 95.4% identity with <italic>Coxiella</italic> sp. reported from Chile (KJ459055) and Spain (MW287611), while <italic>Coxiella</italic> sp. OQ883862 (detected in <italic>Ha. bispinosa</italic>) showed 93.9% identity with <italic>Coxiella</italic> sp. reported from China (OK625731 and OK625732), and <italic>Coxiella</italic> sp. OQ883863 (detected in <italic>Ha. bispinosa</italic>) showed 91.3% identity with <italic>Coxiella</italic> sp. reported from China (OK625731 and OK625732). In the phylogenetic tree, all the obtained aforementioned <italic>Coxiella</italic> sp. sequences were clustered to the corresponding <italic>Coxiella</italic> sp. sequences (<xref ref-type="fig" rid="F3">Figure 3</xref>).</p>
<fig id="F3" position="float">
<label>Figure 3</label>
<caption><p>Phylogenetic tree based on <italic>GroEL</italic> fragments of <italic>Coxiella</italic> spp. detected in tick species. The sequence of <italic>Legionella jordanis</italic> (LR134383) was used as an outgroup. The levels of bootstrap support (&#x02265; 60%) for phylogenetic groupings are given at each node. The obtained sequences are represented with bold and underlined fonts.</p></caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmicb-14-1229950-g0003.tif"/>
</fig>
<p>The obtained <italic>cox1</italic> partial fragments of ticks were submitted to GenBank under accession numbers: <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860250">OQ860250</ext-link> (<italic>Ha. cornupunctata</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860248">OQ860248</ext-link> (<italic>Ha. bispinosa</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860704">OQ860704</ext-link> (<italic>Ha. danieli</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860705">OQ860705</ext-link> (<italic>Ha. montgomeryi</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860706">OQ860706</ext-link> (<italic>Hy. anatolicum</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860725">OQ860725</ext-link> (<italic>Hy. dromedarii</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ861058">OQ861058</ext-link> (<italic>R. haemaphysaloides</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ861080">OQ861080</ext-link> (<italic>R. microplus</italic>), and <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860245">OQ860245</ext-link> (<italic>A. persicus</italic>). The obtained <italic>GroEL</italic> partial fragments of <italic>Coxiella</italic> spp. were submitted to GenBank under accession numbers: <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883856">OQ883856</ext-link> (<italic>C. burnetii</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883857">OQ883857</ext-link> (<italic>Coxiella</italic> endosymbiont), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883858">OQ883858</ext-link> (<italic>Coxiella</italic> endosymbiont), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883859">OQ883859</ext-link> (<italic>Coxiella</italic> sp.), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883860">OQ883860</ext-link> (<italic>Coxiella</italic> sp.), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883861">OQ883861</ext-link> (<italic>Coxiella</italic> sp.), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883862">OQ883862</ext-link> (<italic>Coxiella</italic> sp.).</p></sec></sec>
<sec sec-type="discussion" id="s4">
<title>Discussion</title>
<p>Various ticks and their associated pathogens ideally propagate in Pakistan&#x00027;s humid and variable climatic conditions (Karim et al., <xref ref-type="bibr" rid="B58">2017</xref>; Ali et al., <xref ref-type="bibr" rid="B9">2019</xref>, <xref ref-type="bibr" rid="B10">2020</xref>, <xref ref-type="bibr" rid="B13">2021</xref>; Obaid et al., <xref ref-type="bibr" rid="B80">2023</xref>). Microbiota belonging to different bacterial genera have been detected in different tick species in Pakistan (Karim et al., <xref ref-type="bibr" rid="B58">2017</xref>; Ali et al., <xref ref-type="bibr" rid="B13">2021</xref>; Alam et al., <xref ref-type="bibr" rid="B7">2022</xref>; Khan Z. et al., <xref ref-type="bibr" rid="B62">2022</xref>; Khan S. M. et al., <xref ref-type="bibr" rid="B61">2023</xref>; Numan et al., <xref ref-type="bibr" rid="B78">2022</xref>). Some serological surveys of Q-fever in small ruminants, large ruminants, rodents, and humans have been reported from Pakistan (Ahmed, <xref ref-type="bibr" rid="B3">1987</xref>; Ali et al., <xref ref-type="bibr" rid="B12">2022a</xref>). There is limited information available regarding the molecular characterization of <italic>C. burnetii</italic> and thus it remains an ignored zoonotic disease in the country. The association of <italic>Coxiella</italic> spp. with different ticks infesting various hosts has been reviewed globally (Guatteo et al., <xref ref-type="bibr" rid="B49">2011</xref>); therefore, in this study, we summarized this association of <italic>Coxiella</italic> spp. with different ticks in Asia. Nine tick species including <italic>Ha. cornupunctata, Ha. bispinosa, Ha. montgomeryi, Ha. danieli, Hy. anatolicum, Hy. dromedarii, R. haemaphysaloides, R. microplus</italic>, and <italic>A. persicus</italic> infesting goats, sheep, camels, cattle, wild mice, and domestic fowls were genetically characterized. In addition, this is the first report regarding the molecular detection and phylogenetic positioning of <italic>Coxiella</italic> spp. associated with ticks in Pakistan. Overall, <italic>C. burnetii</italic>, two <italic>Coxiella</italic> endosymbionts, and five undetermined <italic>Coxiella</italic> sp. were genetically characterized based on <italic>GroEL</italic> fragments in various tick species.</p>
<p>Environmental factors such as humidity and temperature mainly affect the distribution of ticks, TBDs, and their zoonotic threats to human and animal health (L&#x000E9;ger et al., <xref ref-type="bibr" rid="B69">2013</xref>). Since the current study area&#x00027;s existing environmental and climatic conditions are favorable for tick infestation and propagation of various pathogens (Aiman et al., <xref ref-type="bibr" rid="B5">2022</xref>; Ali et al., <xref ref-type="bibr" rid="B11">2023</xref>), many ticks were collected during this survey. Contrary to previous studies, <italic>Ha. cornupunctata</italic> tick was more prevalent than other tick species such as <italic>R. microplus</italic> and <italic>Hy. anatolicum</italic> in Pakistan (Karim et al., <xref ref-type="bibr" rid="B58">2017</xref>; Ali et al., <xref ref-type="bibr" rid="B9">2019</xref>, <xref ref-type="bibr" rid="B13">2021</xref>; Khan Z. et al., <xref ref-type="bibr" rid="B62">2022</xref>). It may be due to examining different hosts, such as goats, sheep, and wild mice attributing a closed association with this species.</p>
<p>The age of the host is a significant factor to tick infestation. According to previous reports, a high tick burden was recorded on adult hosts compared with young ones (Ali et al., <xref ref-type="bibr" rid="B13">2021</xref>; Kamran et al., <xref ref-type="bibr" rid="B57">2021</xref>; Khan Z. et al., <xref ref-type="bibr" rid="B62">2022</xref>). Large body surfaces and free grazing practices of adult animals make them more vulnerable due to high tick infestation. In contrast, the robust immune system, less grazing, and low body surface of the younger hosts contribute to less tick infestation (Swai et al., <xref ref-type="bibr" rid="B100">2005</xref>). Female hosts were highly tick infested compared with the male hosts, which is consistent with previous findings (Ullah et al., <xref ref-type="bibr" rid="B109">2023</xref>). Higher levels of progesterone and prolactin hormones in females make them susceptible to tick infestation (Anderson et al., <xref ref-type="bibr" rid="B19">2013</xref>; Ahmed et al., <xref ref-type="bibr" rid="B4">2023</xref>). The higher levels of progesterone and prolactin hormones may increase the susceptibility of females to tick&#x00027;s infections (Lloyd, <xref ref-type="bibr" rid="B71">1983</xref>; Ahmed et al., <xref ref-type="bibr" rid="B4">2023</xref>). Additionally, in the current study, ticks were predominantly reported in summer (June&#x02013;August) compared with other seasons because the warm and humid climatic conditions in the region provide a suitable environment for the development of all stages of ticks (Ali et al., <xref ref-type="bibr" rid="B9">2019</xref>, <xref ref-type="bibr" rid="B13">2021</xref>). The comparatively wide host range noted for different <italic>Haemaphysalis, Hyalomma</italic>, and <italic>Rhipicephalus</italic> ticks may be due to frequent practices such as putting various hosts in the same shelter and over-crowded livestock and concurrent grazing in the survey area.</p>
<p>Major consequences have been revealed in the epidemiology of Q-fever upon the molecular detection of <italic>C. burnetii</italic> DNA in ticks collected from the environment, domestic and wild animals (Yessinou et al., <xref ref-type="bibr" rid="B110">2022</xref>). It has been observed that ticks may transmit the Q-fever agent and pollute the environment as well as the host&#x00027;s body in Pakistan (Ullah et al., <xref ref-type="bibr" rid="B108">2019</xref>). The association between different ticks and <italic>C. burnetii</italic> and its transstadially and transovarially transmission has been reported, suggesting the Q-fever transmission from infected to healthy animals through blood meal (Gong et al., <xref ref-type="bibr" rid="B48">2020</xref>). In this study, molecular detection of <italic>Coxiella</italic> spp. varied in the aforementioned seven tick species collected from various hosts. A high prevalence of Q-fever in camels in this study may be attributable to the camels&#x00027; vulnerability regarding <italic>C. burnetii</italic> infection or camel tick competence as a reservoir for this pathogen (Gumi et al., <xref ref-type="bibr" rid="B50">2013</xref>). Common reservoirs for <italic>C. burnetii</italic> are small ruminants that may excrete a diverse number of these bacteria in their birth byproducts (placenta). <italic>Coxiella</italic> spp. were highly detected in ticks collected from small ruminants (goats and sheep), and these findings agreed with the previous serosurvey conducted in Pakistan (Ullah et al., <xref ref-type="bibr" rid="B108">2019</xref>). <italic>Coxiella</italic> sp. detected in <italic>A. persicus</italic> ticks collected from domestic fowls suggest that different soft ticks may also be investigated as host reservoirs for various undetermined <italic>Coxiella</italic> spp., as reported in other studies (Trinachartvanit et al., <xref ref-type="bibr" rid="B105">2018</xref>).</p>
<p>In the current study, phylogenetic analysis <italic>via cox1</italic> fragments of nine different tick species revealed a close evolutionary relationship with the same species reported from Pakistan, China, India, Bangladesh, and Iran, and these findings were supported by previous studies (Ahmad et al., <xref ref-type="bibr" rid="B2">2022</xref>; Alam et al., <xref ref-type="bibr" rid="B7">2022</xref>; Ali et al., <xref ref-type="bibr" rid="B12">2022a</xref>; Khan S. M. et al., <xref ref-type="bibr" rid="B61">2023</xref>). Phylogenetic analysis of <italic>Coxiella</italic> spp., detected in different tick species, showed close association with their respective species reported from the same or different tick species and humans. This association of <italic>Coxiella</italic> spp. may be due to the close interaction of infested animals with humans, which enhances zoonotic infections such as Q-fever in humans. So-far neglected surveillance of <italic>Coxiella</italic> spp. in the region demands immediate attention to its pathogenic consequences.</p></sec>
<sec sec-type="conclusions" id="s5">
<title>Conclusion</title>
<p><italic>Coxiella</italic> spp. were molecularly detected in ticks infesting goats, sheep, camels, cattle, wild mice, and domestic fowls and were confirmed through sequencing for the first time in Pakistan. Further research is essential to investigate any potential health risks due to these agents. The veterinarian livestock holders and farm workers lack knowledge regarding the epidemiology of Q-fever and its causative agents in Pakistan. Livestock holders should be adequately educated regarding Q-fever prevention and management practices because the occurrence of this agent can lead to long-term environmental contamination, which is a potential threat to animals and humans. Consequently, effective measures associated with Q-fever must be implemented, including limiting contact between herds, quarantining newly purchased animals, and using disinfectants that can reduce the spread of infection and possible transmission to humans.</p>
<sec>
<title>Institutional review board statement</title>
<p>The Advance Studies and Research Board (ASRB: Dir/A&#x00026;R/AWKUM/2022/9396) of the Department of Zoology, Abdul Wali Khan University Mardan, Pakistan, approved prior consent for this study. Additionally, permission was taken from the owners of the animals to observe hosts and ticks collection. All the rules regarding animal welfare regulations were followed while handling the animals.</p></sec></sec>
<sec sec-type="data-availability" id="s6">
<title>Data availability statement</title>
<p>The datasets presented in the study have been deposited to the NCBI GenBank repository, accession numbers <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860250">OQ860250</ext-link> <italic>(Ha. cornupunctata</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860248">OQ860248</ext-link> (<italic>Ha. bispinosa</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860704">OQ860704</ext-link> (<italic>Ha. danieli</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860705">OQ860705</ext-link> (<italic>Ha. montgomeryi</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860706">OQ860706</ext-link> (<italic>Hy. anatolicum</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860725">OQ860725</ext-link> (<italic>Hy. dromedarii</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ861058">OQ861058</ext-link> (<italic>R. haemaphysaloides</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ861080">OQ861080</ext-link> (<italic>R. microplus</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ860245">OQ860245</ext-link> (<italic>A. persicus</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883856">OQ883856</ext-link> (<italic>C. burnetii</italic>), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883857">OQ883857</ext-link> (<italic>Coxiella</italic> endosymbiont), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883858">OQ883858</ext-link> (<italic>Coxiella</italic> endosymbiont), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883859">OQ883859</ext-link> (<italic>Coxiella</italic> sp.), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883860">OQ883860</ext-link> (<italic>Coxiella</italic> sp.), <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883861">OQ883861</ext-link> (<italic>Coxiella</italic> sp.), and <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="OQ883862">OQ883862</ext-link> (<italic>Coxiella</italic> sp.).</p></sec>
<sec sec-type="ethics-statement" id="s7">
<title>Ethics statement</title>
<p>The animal study was reviewed and approved by the Advance Studies and Research Board (ASRB: Dir/A&#x00026;R/AWKUM/2022/9396) of the Department of Zoology, Abdul Wali Khan University Mardan, Pakistan, approved prior consent for this study. 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="s8">
<title>Author contributions</title>
<p>AAli designed the study. AAli, MMA, TT, SBK, and AAlo carried out the experiments of the study. AAli, MN, ZUI, GR, MKO, SBK, and SU collected the tick samples and performed the experiments. AAli, MKO, and MN performed the phylogenetic and statistical analyses. All authors have read and agreed to the published version of the manuscript.</p></sec>
</body>
<back>
<sec sec-type="funding-information" id="s9">
<title>Funding</title>
<p>The authors acknowledge the financial support provided by the Higher Education Commission of Pakistan and the Pakistan Science Foundation. The researchers support project number (RSP2023R494), King Saud University, Riyadh, Saudi Arabia. This work was supported by JSPS KAKENHI Grant Numbers JP20KK0154 and JP22H02522, JSPS Bilateral Program (Grant number JPJSBP120239937).</p>
</sec>
<sec sec-type="COI-statement" id="conf1">
<title>Conflict of interest</title>
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