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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A molecular survey of vector-borne pathogens in red foxes (<italic>Vulpes vulpes</italic>) from Bosnia and Herzegovina</title><author><name sortKey="Hodzi, Adnan" sort="Hodzi, Adnan" uniqKey="Hodzi A" first="Adnan" last="Hodži">Adnan Hodži</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Ali, Amer" sort="Ali, Amer" uniqKey="Ali A" first="Amer" last="Ali">Amer Ali</name><affiliation><nlm:aff id="Aff2">Department of Pathology, Veterinary Faculty, University of Sarajevo, Sarajevo, Bosnia and Herzegovina</nlm:aff></affiliation></author><author><name sortKey="Fuehrer, Hans Peter" sort="Fuehrer, Hans Peter" uniqKey="Fuehrer H" first="Hans-Peter" last="Fuehrer">Hans-Peter Fuehrer</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Harl, Josef" sort="Harl, Josef" uniqKey="Harl J" first="Josef" last="Harl">Josef Harl</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Wille Piazzai, Walpurga" sort="Wille Piazzai, Walpurga" uniqKey="Wille Piazzai W" first="Walpurga" last="Wille-Piazzai">Walpurga Wille-Piazzai</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Duscher, Georg Gerhard" sort="Duscher, Georg Gerhard" uniqKey="Duscher G" first="Georg Gerhard" last="Duscher">Georg Gerhard Duscher</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25889961</idno><idno type="pmc">4367825</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4367825</idno><idno type="RBID">PMC:4367825</idno><idno type="doi">10.1186/s13071-015-0692-x</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000018</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000018</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A molecular survey of vector-borne pathogens in red foxes (<italic>Vulpes vulpes</italic>) from Bosnia and Herzegovina</title><author><name sortKey="Hodzi, Adnan" sort="Hodzi, Adnan" uniqKey="Hodzi A" first="Adnan" last="Hodži">Adnan Hodži</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Ali, Amer" sort="Ali, Amer" uniqKey="Ali A" first="Amer" last="Ali">Amer Ali</name><affiliation><nlm:aff id="Aff2">Department of Pathology, Veterinary Faculty, University of Sarajevo, Sarajevo, Bosnia and Herzegovina</nlm:aff></affiliation></author><author><name sortKey="Fuehrer, Hans Peter" sort="Fuehrer, Hans Peter" uniqKey="Fuehrer H" first="Hans-Peter" last="Fuehrer">Hans-Peter Fuehrer</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Harl, Josef" sort="Harl, Josef" uniqKey="Harl J" first="Josef" last="Harl">Josef Harl</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Wille Piazzai, Walpurga" sort="Wille Piazzai, Walpurga" uniqKey="Wille Piazzai W" first="Walpurga" last="Wille-Piazzai">Walpurga Wille-Piazzai</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author><author><name sortKey="Duscher, Georg Gerhard" sort="Duscher, Georg Gerhard" uniqKey="Duscher G" first="Georg Gerhard" last="Duscher">Georg Gerhard Duscher</name><affiliation><nlm:aff id="Aff1">Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</nlm:aff></affiliation></author></analytic><series><title level="j">Parasites & Vectors</title><idno type="eISSN">1756-3305</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Red foxes (<italic>Vulpes vulpes</italic>) have recently been recognized as potential reservoirs of several vector-borne pathogens and a source of infection for domestic dogs and humans, mostly due to their close vicinity to urban areas and frequent exposure to different arthropod vectors. The aim of this study was to investigate the presence and distribution of <italic>Babesia</italic> spp., <italic>Hepatozoon canis</italic>, <italic>Anaplasma</italic> spp., <italic>Bartonella</italic> spp., ‘<italic>Candidatus</italic> Neoehrlichia mikurensis’, <italic>Ehrlichia canis</italic>, <italic>Rickettsia</italic> spp. and blood filaroid nematodes in free-ranging red foxes from Bosnia and Herzegovina.</p></sec><sec><title>Methods</title><p>Spleen samples from a total of 119 red foxes, shot during the hunting season between October 2013 and April 2014 throughout Bosnia and Herzegovina, were examined for the presence of blood vector-borne pathogens by conventional PCRs and sequencing.</p></sec><sec><title>Results</title><p>In the present study, three species of apicomplexan parasites were molecularly identified in 73 red foxes from the entire sample area, with an overall prevalence of 60.8%. The DNA of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> was found in 1 (0.8%), 38 (31.9%) and 46 (38.6%) spleen samples, respectively. In 11 samples (9.2%) co-infections with <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> were detected and one fox harboured all three parasites (0.8%). There were no statistically significant differences between geographical region, sex or age of the host in the infection prevalence of <italic>B.</italic> cf. <italic>microti</italic>, although females (52.9%; 18/34) were significantly more infected with <italic>H. canis</italic> than males (32.9%; 28/85). The presence of vector-borne bacteria and filaroid nematodes was not detected in our study.</p></sec><sec><title>Conclusion</title><p>This is the first report of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> parasites in foxes from Bosnia and Herzegovina and the data presented here provide a first insight into the distribution of these pathogens among the red fox population. Moreover, the relatively high prevalence of <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> reinforces the assumption that this wild canid species might be a possible reservoir and source of infection for domestic dogs.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Otranto, D" uniqKey="Otranto D">D Otranto</name></author><author><name sortKey="Dantas Torres, F" uniqKey="Dantas Torres F">F Dantas-Torres</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aguirre, Aa" uniqKey="Aguirre A">AA Aguirre</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dezdek, D" uniqKey="Dezdek D">D Deždek</name></author><author><name sortKey="Vojta, L" uniqKey="Vojta L">L Vojta</name></author><author><name sortKey=" Urkovi, S" uniqKey=" Urkovi S">S Ćurković</name></author><author><name sortKey="Lipej, Z" uniqKey="Lipej Z">Z 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Parasit Vectors</journal-id><journal-id journal-id-type="iso-abbrev">Parasit Vectors</journal-id><journal-title-group><journal-title>Parasites & Vectors</journal-title></journal-title-group><issn pub-type="epub">1756-3305</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25889961</article-id><article-id pub-id-type="pmc">4367825</article-id><article-id pub-id-type="publisher-id">692</article-id><article-id pub-id-type="doi">10.1186/s13071-015-0692-x</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research</subject></subj-group></article-categories><title-group><article-title>A molecular survey of vector-borne pathogens in red foxes (<italic>Vulpes vulpes</italic>) from Bosnia and Herzegovina</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Hodžić</surname><given-names>Adnan</given-names></name><address><email>adnan.hodzic@vetmeduni.ac.at</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Alić</surname><given-names>Amer</given-names></name><address><email>amer.alic@vfs.unsa.ba</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Fuehrer</surname><given-names>Hans-Peter</given-names></name><address><email>hans-peter.fuehrer@vetmeduni.ac.at</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Harl</surname><given-names>Josef</given-names></name><address><email>josef.harl@vetmeduni.ac.at</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Wille-Piazzai</surname><given-names>Walpurga</given-names></name><address><email>walpurga.wille-piazzai@vetmeduni.ac.at</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Duscher</surname><given-names>Georg Gerhard</given-names></name><address><email>georg.duscher@vetmeduni.ac.at</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1"><label></label>Institute of Parasitology, Department for Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria</aff><aff id="Aff2"><label></label>Department of Pathology, Veterinary Faculty, University of Sarajevo, Sarajevo, Bosnia and Herzegovina</aff></contrib-group><pub-date pub-type="epub"><day>8</day><month>2</month><year>2015</year></pub-date><pub-date pub-type="pmc-release"><day>8</day><month>2</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>8</volume><elocation-id>88</elocation-id><history><date date-type="received"><day>10</day><month>12</month><year>2014</year></date><date date-type="accepted"><day>26</day><month>1</month><year>2015</year></date></history><permissions><copyright-statement>© Hodžić et al.; licensee BioMed Central. 2015</copyright-statement><license license-type="open-access"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">http://creativecommons.org/licenses/by/4.0</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p>Red foxes (<italic>Vulpes vulpes</italic>) have recently been recognized as potential reservoirs of several vector-borne pathogens and a source of infection for domestic dogs and humans, mostly due to their close vicinity to urban areas and frequent exposure to different arthropod vectors. The aim of this study was to investigate the presence and distribution of <italic>Babesia</italic> spp., <italic>Hepatozoon canis</italic>, <italic>Anaplasma</italic> spp., <italic>Bartonella</italic> spp., ‘<italic>Candidatus</italic> Neoehrlichia mikurensis’, <italic>Ehrlichia canis</italic>, <italic>Rickettsia</italic> spp. and blood filaroid nematodes in free-ranging red foxes from Bosnia and Herzegovina.</p></sec><sec><title>Methods</title><p>Spleen samples from a total of 119 red foxes, shot during the hunting season between October 2013 and April 2014 throughout Bosnia and Herzegovina, were examined for the presence of blood vector-borne pathogens by conventional PCRs and sequencing.</p></sec><sec><title>Results</title><p>In the present study, three species of apicomplexan parasites were molecularly identified in 73 red foxes from the entire sample area, with an overall prevalence of 60.8%. The DNA of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> was found in 1 (0.8%), 38 (31.9%) and 46 (38.6%) spleen samples, respectively. In 11 samples (9.2%) co-infections with <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> were detected and one fox harboured all three parasites (0.8%). There were no statistically significant differences between geographical region, sex or age of the host in the infection prevalence of <italic>B.</italic> cf. <italic>microti</italic>, although females (52.9%; 18/34) were significantly more infected with <italic>H. canis</italic> than males (32.9%; 28/85). The presence of vector-borne bacteria and filaroid nematodes was not detected in our study.</p></sec><sec><title>Conclusion</title><p>This is the first report of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> parasites in foxes from Bosnia and Herzegovina and the data presented here provide a first insight into the distribution of these pathogens among the red fox population. Moreover, the relatively high prevalence of <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> reinforces the assumption that this wild canid species might be a possible reservoir and source of infection for domestic dogs.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd><italic>Babesia</italic> cf. <italic>microti</italic></kwd><kwd><italic>Hepatozoon canis</italic></kwd><kwd><italic>Babesia canis</italic></kwd><kwd>Red fox</kwd><kwd><italic>Vulpes vulpes</italic></kwd><kwd>Bosnia and Herzegovina</kwd><kwd>PCR</kwd></kwd-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2015</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Background</title><p>Vector-borne diseases (VBDs) are caused by many protozoan, helminthic, bacterial and viral pathogens, which are transmitted to animals and humans by blood-sucking arthropods, such as ticks, mosquitos, fleas and phlebotomine sand flies [<xref ref-type="bibr" rid="CR1">1</xref>]. The majority of VBDs are classified as emerging infectious diseases and anthropogenic changes, such as global warming, deforestation, globalization and pollution, may have an impact on their prevalence and distribution [<xref ref-type="bibr" rid="CR1">1</xref>,<xref ref-type="bibr" rid="CR2">2</xref>]. However, despite intensive clinical and epidemiological research in the recent past, especially in domestic dogs and cats, the information on the occurrence and prevalence of vector-borne pathogens in wild canids is still scarce [<xref ref-type="bibr" rid="CR3">3</xref>-<xref ref-type="bibr" rid="CR7">7</xref>]. Red foxes (<italic>Vulpes vulpes</italic>) are the most abundant wild canid species in Europe [<xref ref-type="bibr" rid="CR8">8</xref>] and recently they have been recognized as a potential reservoir for blood vector-borne pathogens, such as <italic>Babesia</italic> spp. [<xref ref-type="bibr" rid="CR6">6</xref>,<xref ref-type="bibr" rid="CR9">9</xref>], <italic>Hepatozoon canis</italic> [<xref ref-type="bibr" rid="CR4">4</xref>,<xref ref-type="bibr" rid="CR10">10</xref>,<xref ref-type="bibr" rid="CR11">11</xref>], <italic>Anaplasma phagocytophilum</italic> [<xref ref-type="bibr" rid="CR12">12</xref>-<xref ref-type="bibr" rid="CR15">15</xref>], <italic>Bartonella</italic> spp. [<xref ref-type="bibr" rid="CR16">16</xref>,<xref ref-type="bibr" rid="CR17">17</xref>], <italic>Ehrlichia canis</italic> [<xref ref-type="bibr" rid="CR18">18</xref>] and filaroid nematodes [<xref ref-type="bibr" rid="CR19">19</xref>-<xref ref-type="bibr" rid="CR21">21</xref>]. They represent an excellent sentinel species and a possible source of several VBDs to domestic animals and humans, mostly due to their close proximity to urban or agricultural areas and frequent exposure to different arthropod vectors [<xref ref-type="bibr" rid="CR2">2</xref>,<xref ref-type="bibr" rid="CR6">6</xref>,<xref ref-type="bibr" rid="CR15">15</xref>,<xref ref-type="bibr" rid="CR22">22</xref>,<xref ref-type="bibr" rid="CR23">23</xref>].</p><p>Tick-borne parasitic hematozoa of the genus <italic>Babesia</italic> (order Piroplasmida) infect erythrocytes of a wide range of domestic and wild animals [<xref ref-type="bibr" rid="CR6">6</xref>,<xref ref-type="bibr" rid="CR9">9</xref>,<xref ref-type="bibr" rid="CR24">24</xref>]. In the past, it was assumed that only <italic>B. canis</italic> and <italic>B. gibsoni</italic> can cause diseases in dogs [<xref ref-type="bibr" rid="CR9">9</xref>]. However, a piroplasm closely related to zoonotic <italic>B. microti</italic> (denominated as <italic>B.</italic> cf. <italic>microti</italic>, <italic>B. microti</italic>-like, <italic>B. annae</italic> or <italic>Theileria annae</italic>) was detected from dogs with clinical signs of hemolytic anemia, azotemia and renal failure [<xref ref-type="bibr" rid="CR25">25</xref>-<xref ref-type="bibr" rid="CR28">28</xref>]. Recently, <italic>B.</italic> cf. <italic>microti</italic> parasites were also molecularly confirmed in red foxes from Austria [<xref ref-type="bibr" rid="CR29">29</xref>], Croatia [<xref ref-type="bibr" rid="CR3">3</xref>], Germany [<xref ref-type="bibr" rid="CR9">9</xref>], Italy [<xref ref-type="bibr" rid="CR7">7</xref>], Poland [<xref ref-type="bibr" rid="CR4">4</xref>], Portugal [<xref ref-type="bibr" rid="CR6">6</xref>] and Spain [<xref ref-type="bibr" rid="CR30">30</xref>]. Furthermore, <italic>B. canis</italic> and <italic>B. gibsoni</italic> were described in foxes based on morphological characteristics [<xref ref-type="bibr" rid="CR24">24</xref>], and the first molecular report of <italic>B. canis</italic> was described in a single fox from Portugal [<xref ref-type="bibr" rid="CR6">6</xref>].</p><p><italic>Hepatozoon canis</italic> (order Eucoccidiorida) is an apicomplexan protozoan parasite infecting domestic dogs and wild canids worldwide [<xref ref-type="bibr" rid="CR10">10</xref>,<xref ref-type="bibr" rid="CR31">31</xref>]. The main vector of <italic>H. canis</italic> is the brown dog tick, <italic>Rhipicephalus sanguineus</italic>, and the pathogen occurrence is mostly related to the geographical distribution of the tick host [<xref ref-type="bibr" rid="CR32">32</xref>]. Transmission to the vertebrate host typically takes place by ingestion of a tick containing mature oocysts [<xref ref-type="bibr" rid="CR33">33</xref>], although vertical transmission of the parasite from female foxes to the progeny might also occur [<xref ref-type="bibr" rid="CR34">34</xref>]. The infection in dogs is often subclinical, but it could be manifested as a severe life-threatening disease with fever, cachexia, lethargy and anemia [<xref ref-type="bibr" rid="CR35">35</xref>]. In foxes, <italic>H. canis</italic> is highly prevalent and it has been recorded in Austria [<xref ref-type="bibr" rid="CR29">29</xref>], Croatia [<xref ref-type="bibr" rid="CR3">3</xref>], Germany [<xref ref-type="bibr" rid="CR36">36</xref>], Hungary [<xref ref-type="bibr" rid="CR31">31</xref>], Poland [<xref ref-type="bibr" rid="CR4">4</xref>], Portugal [<xref ref-type="bibr" rid="CR10">10</xref>], Romania [<xref ref-type="bibr" rid="CR11">11</xref>], Slovakia [<xref ref-type="bibr" rid="CR37">37</xref>] and Spain [<xref ref-type="bibr" rid="CR38">38</xref>].</p><p>In recent years, the interest of the scientific community in vector-borne bacteria from the genera <italic>Anaplasma</italic>, <italic>Bartonella</italic>, <italic>Ehrlichia</italic>, <italic>Rickettsia</italic> and the recently described cluster ‘<italic>Candidatus</italic> Neoehrlichia’ is growing worldwide since they were recognized as important human and animal pathogens. Thus <italic>A. phagocytophilum</italic>, <italic>A. ovis</italic>, <italic>A. bovis</italic>, <italic>B. rochalimae</italic> and <italic>E. canis</italic> were molecularly identified in foxes from many European countries [<xref ref-type="bibr" rid="CR12">12</xref>,<xref ref-type="bibr" rid="CR13">13</xref>,<xref ref-type="bibr" rid="CR15">15</xref>-<xref ref-type="bibr" rid="CR17">17</xref>,<xref ref-type="bibr" rid="CR23">23</xref>,<xref ref-type="bibr" rid="CR39">39</xref>]. Moreover, ‘<italic>Candidatus</italic> N. mikurensis’ and <italic>Rickettsia</italic> spp. were found in humans, domestic and wild animals, and arthropods collected from foxes [<xref ref-type="bibr" rid="CR13">13</xref>,<xref ref-type="bibr" rid="CR23">23</xref>,<xref ref-type="bibr" rid="CR40">40</xref>-<xref ref-type="bibr" rid="CR42">42</xref>], but they have never been molecularly confirmed in that wild canid species itself.</p><p>Canine dirofilariosis, caused by <italic>Dirofilaria immitis</italic> and <italic>D. repens</italic>, was diagnosed in Bosnia and Herzegovina for the first time in 2009, with the prevalence of 3.1% and 1.9% in dogs, respectively [<xref ref-type="bibr" rid="CR43">43</xref>]. These nematodes infect mainly dogs, but also wild carnivores, cats and humans [<xref ref-type="bibr" rid="CR20">20</xref>]. Several studies have shown that foxes represent an important wild reservoir for filaroid nematodes (e.g., <italic>Dirofilaria</italic>, <italic>Acanthocheilonema</italic>) and in fact they support the circulation and transmission of microfilariae to companion animals and humans [<xref ref-type="bibr" rid="CR20">20</xref>,<xref ref-type="bibr" rid="CR21">21</xref>,<xref ref-type="bibr" rid="CR44">44</xref>].</p><p>To the best of our knowledge, there is no information on vector-borne pathogens in the red fox population from Bosnia and Herzegovina. Therefore, the aim of this study was to investigate the presence and distribution of <italic>Babesia</italic> spp., <italic>Hepatozoon canis</italic>, <italic>Anaplasma</italic> spp., <italic>Bartonella</italic> spp., ‘<italic>Candidatus</italic> N. mikurensis’, <italic>Ehrlichia canis</italic>, <italic>Rickettsia</italic> spp. and blood filaroid nematodes in free-ranging red foxes from Bosnia and Herzegovina.</p></sec><sec id="Sec2" sec-type="methods"><title>Methods</title><sec id="Sec3"><title>Collection of samples</title><p>The present study was conducted in Bosnia and Herzegovina, which covers 51,209 km<sup>2</sup> and is located in the western part of the Balkan Peninsula (43° 52’ N, 18° 25’ E). A total of 119 red foxes (85 males, 34 females; 7 juveniles <1 yr., 112 adults >1 yr.) from 29 municipalities of six different regions were shot during the hunting season between October 2013 and April 2014. All animals were immediately delivered to the Department of Pathology at the Veterinary Faculty in Sarajevo and stored at 4°C for no more than 72 h. Data on sex, age and area of origin was recorded for each individual animal. During necropsy, small pieces of spleen tissue were collected, stored at −20°C and sent to the Institute of Parasitology at the University of Veterinary Medicine in Vienna, Austria for further analysis. Additionally, hearts, pulmonary arteries and lungs were dissected and examined visually for the presence of <italic>D. immitis</italic>.</p></sec><sec id="Sec4"><title>DNA extraction, PCR amplification and sequencing</title><p>Total DNA was extracted from up to 20 mg of spleen tissue using the High Pure PCR Template Preparation Kit (Roche Diagnostics, Germany) according to the manufacturer’s instructions. The PCR primers (Table <xref rid="Tab1" ref-type="table">1</xref>) and amplification conditions for molecular detection of <italic>Babesia</italic> spp., <italic>Anaplasma</italic> spp., <italic>Bartonella</italic> spp., ‘<italic>Candidatus</italic> N. mikurensis’, <italic>E. canis</italic> and <italic>Rickettsia</italic> spp. have been published elsewhere [<xref ref-type="bibr" rid="CR45">45</xref>-<xref ref-type="bibr" rid="CR48">48</xref>]. PCR products were separated by electrophoresis in 2% agarose gels stained with Midori Green Advance DNA stain (Nippon Genetics Europe, Germany). All positive samples were purified and directly sequenced by a commercial company (LGC Genomics, Germany). Obtained sequences were edited using the software BioEdit (<ext-link ext-link-type="uri" xlink:href="http://www.mbio.ncsu.edu/BioEdit/bioedit.html">www.mbio.ncsu.edu/BioEdit/bioedit.html</ext-link>) and compared for similarity to sequences available in GenBank (<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/BLAST">http://www.ncbi.nlm.nih.gov/BLAST</ext-link>).<table-wrap id="Tab1"><label>Table 1</label><caption><p><bold>Primers used for the amplification of DNA of</bold><bold><italic>Babesia</italic></bold><bold>spp.,</bold><bold><italic>Hepatozoon</italic></bold><bold>spp.,</bold><bold><italic>Anaplasma</italic></bold><bold>spp.,</bold><bold><italic>Bartonella</italic></bold><bold>spp</bold><bold><italic>.,</italic></bold><bold>‘</bold><bold><italic>Candidatus</italic></bold><bold>Neoehrlichia mikurensis’,</bold><bold><italic>Ehrlichia canis</italic></bold><bold>,</bold><bold><italic>Rickettsia</italic></bold><bold>spp. and filaroid nematodes</bold></p></caption><table frame="hsides" rules="groups"><thead><tr valign="top"><th><bold>Specifity</bold></th><th><bold>Genetic marker</bold></th><th><bold>Sequences of primers (5’-3’)</bold></th><th><bold>Lenght of amplicons (bp)</bold></th><th><bold>Reference</bold></th></tr></thead><tbody><tr valign="top"><td rowspan="2">Apicomplexa</td><td rowspan="5">18S rRNA</td><td><bold>BTH-1 F</bold>: CCT GAG AAA CGG CTA CCA CAT CT</td><td align="left" rowspan="5">561</td><td rowspan="5">[<xref ref-type="bibr" rid="CR45">45</xref>]</td></tr><tr valign="top"><td><bold>BTH-1R</bold>: TTG CGA CCA TAC TCC CCC CA</td></tr><tr valign="top"><td><italic>Babesia</italic> spp.</td><td>Nested PCR:</td></tr><tr valign="top"><td rowspan="2"><italic>Theileria</italic> spp.</td><td><bold>GF2</bold>: GTC TTG TAA TTG GAA TGA TGG</td></tr><tr valign="top"><td><bold>GR2</bold>: CCA AAG ACT TTG ATT TCT CTC</td></tr><tr valign="top"><td rowspan="2"><italic>Hepatozoon canis</italic></td><td rowspan="2">18S rRNA</td><td><bold>H14Hepa18SFw</bold>: GAA ATA ACA ATA CAA GGC AGT TAA AAT GCT</td><td align="left" rowspan="2">620</td><td rowspan="2">present study</td></tr><tr valign="top"><td><bold>H14Hepa18SRv</bold>: GTG CTG AAG GAG TCG TTT ATA AAG A</td></tr><tr valign="top"><td rowspan="2"><italic>Anaplasmataceae</italic></td><td rowspan="2">16S rRNA</td><td><bold>EHR16SD</bold>: GGT ACC YAC AGA AGA AGT CC</td><td align="left" rowspan="2">345</td><td rowspan="2">[<xref ref-type="bibr" rid="CR46">46</xref>]</td></tr><tr valign="top"><td><bold>EHR16SR</bold>: TAG CAC TCA TCG TTT ACA GC</td></tr><tr valign="top"><td rowspan="2"><italic>Bartonella</italic> spp.</td><td rowspan="2">16S-23S rRNA</td><td><bold>bartg_for</bold>: GAT GAT GAT CCC AAG CCT TC</td><td rowspan="2">134 - 315</td><td rowspan="2">modified [<xref ref-type="bibr" rid="CR47">47</xref>]</td></tr><tr valign="top"><td><bold>B1623_rev</bold>: AAC CAA CTG AGC TAC AAG CC</td></tr><tr valign="top"><td rowspan="2"><italic>Rickettssia</italic> spp.</td><td rowspan="2">23S/5S rRNA</td><td><bold>ITS-F</bold>: GAT AGG TCG GGT GTG GAA G</td><td rowspan="2">342 - 533</td><td rowspan="2">[<xref ref-type="bibr" rid="CR48">48</xref>]</td></tr><tr valign="top"><td><bold>ITS-R</bold>: TCG GGA TGG GAT CGT GTG</td></tr><tr valign="top"><td rowspan="2">Filaroid nematodes</td><td rowspan="2"><italic>COI</italic></td><td><bold>H14FilaCOIFw</bold>: GCC TAT TTT GAT TGG TGG TTT TGG</td><td align="left" rowspan="2">724</td><td rowspan="2">present study</td></tr><tr valign="top"><td><bold>H14FilaCOIRv</bold>: AGC AAT AAT CAT AGT AGC AGC ACT AA</td></tr></tbody></table></table-wrap></p><p>In order to detect apicomplexan parasites of the genera <italic>Babesia</italic> and <italic>Hepatozoon</italic>, the primer pair BTH-1 F and BTH-1R [<xref ref-type="bibr" rid="CR45">45</xref>] was used. In those cases where the electropherograms showed superimposed signals, indicating mixed infections with different apicomplexan parasites, additional PCR reactions were performed with the specific primer pairs. The nested primers GF2 and GR2 [<xref ref-type="bibr" rid="CR45">45</xref>] were used to detect <italic>Babesia</italic> spp., whereas new primers were designed for screening of <italic>Hepatozoon</italic> spp.: H14Hepa18SFw (5’- GAA ATA ACA ATA CAA GGC AGT TAA AAT GCT −3’) and H14Hepa18SRv (5A’- GTG CTG AAG GAG TCG TTT ATA AAG A −3’).</p><p>For PCR screening of spleens on the blood filaroid nematodes (e.g. <italic>Dirofilaria</italic>, <italic>Acanthocheilonema</italic>) another primer set, H14FilaCOIFw (5’- GCC TAT TTT GAT TGG TGG TTT TGG −3’) and H14FilaCOIRv (5’- AGC AAT AAT CAT AGT AGC AGC ACT AA −3’), was designed and used to amplify a 724 bp fragment of the mitochondrial cytochrome c oxidase subunit I (<italic>COI</italic>) gene (Table <xref rid="Tab1" ref-type="table">1</xref>). The PCR mixture for the newly designed primer pairs was as follows: 1 μl of extracted DNA was added to 24 μl of reaction mixture containing 5 μl of 5X Green Reaction Buffer (7.5 mM MgCl<sub>2</sub>; pH 8.5), 0.5 μl of dNTPs (10 mM), 0.125 μl of Taq polymerase (5 u/μl), 2 μl of each primer (10 pmol/μl), and made up to a final volume of 25 μl with PCR grade water. Amplifications were conducted in a Mastercycler Pro (Eppendorf, Germany) under the following conditions: 95°C for 2 min followed by 35 cycles of 95°C for 60 s, 58°C (H14Hepa18S)/53°C (H14FilaCOI) for 60 s, 72°C for 60 s. Final extension was performed at 72°C for 5 min then held at 15°C.</p></sec><sec id="Sec5"><title>Statistical analyses</title><p>All statistical analyses were performed with SPSS 20.0 statistical software. The Kolmogorov-Smirnov test was used to test for normal distribution of the data. The Kruskal-Wallis test was chosen to compare proportions of positivity by geographical region, and the Mann–Whitney-U test was used to test pathogen distribution according to sex and age. Differences were considered significant at p < 0.05.</p></sec><sec id="Sec6"><title>Ethical statement</title><p>The study was conducted under the frame of Project ID: BIH-PSD-G-EC 30, Sub project ID: CRIS Number: 2010/022-259, for the improvement of animal health control through the vaccination against rabies and in accordance with the Veterinary law of Bosnia and Herzegovina.</p></sec></sec><sec id="Sec7" sec-type="results"><title>Results</title><p>In the present study, three species of apicomplexan parasites, <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic>, were identified in 73 red foxes by using molecular methods, with an overall prevalence of 60.8%. All infected foxes were in a good body condition and came from 23 municipalities of all six surveyed regions. The highest prevalence was detected in the region of North West Bosnia (Figure <xref rid="Fig1" ref-type="fig">1</xref>, Table <xref rid="Tab2" ref-type="table">2</xref>). DNA of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> was detected in 1 (0.8%; 95% confidence interval [CI]: 0.8–2.4%), 38 (31.9%; 95% CI: 23–40%) and 46 (38.6%; 95% CI: 30–48%) spleen samples, respectively. The geographical distribution of these pathogens overlap in many sampled areas (Figure <xref rid="Fig1" ref-type="fig">1</xref>) and co-infections with <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> were confirmed in 11 animals (9.2%), while a single fox harboured all three pathogens (0.8%). There were no statistically significant differences in the prevalence of <italic>B.</italic> cf. <italic>microti</italic> infections between geographical regions, sex or age of the host. However, females (52.9%; 18/34) were significantly more infected with <italic>H. canis</italic> (p = 0.044) than males (32.9%; 28/85) (Table <xref rid="Tab3" ref-type="table">3</xref>). Also, there was no statistically significant differences between the age and sex groups (p = 0.085).<fig id="Fig1"><label>Figure 1</label><caption><p><bold>Map of Bosnia and Herzegovina showing geographical locations of</bold><bold><italic>Babesia canis</italic></bold><inline-graphic xlink:href="13071_2015_692_Figa_HTML.gif" id="d30e1210"></inline-graphic><bold>,</bold><bold><italic>Babesia</italic></bold><bold>cf.</bold><bold><italic>microti</italic></bold><inline-graphic xlink:href="13071_2015_692_Figb_HTML.gif" id="d30e1226"></inline-graphic><bold>and</bold><bold><italic>Hepatozoon canis</italic></bold><inline-graphic xlink:href="13071_2015_692_Figc_HTML.gif" id="d30e1235"></inline-graphic><bold>infected foxes.</bold></p></caption><graphic xlink:href="13071_2015_692_Fig1_HTML" id="MO1"></graphic></fig><table-wrap id="Tab2"><label>Table 2</label><caption><p><bold>The prevalence and geographical distribution of</bold><bold><italic>B. canis</italic></bold><bold>,</bold><bold><italic>Babesia</italic></bold><bold>cf.</bold><bold><italic>microti</italic></bold><bold>, and</bold><bold><italic>Hepatozoon canis</italic></bold><bold>infected foxes in Bosnia and Herzegovina</bold></p></caption><table frame="hsides" rules="groups"><thead><tr valign="top"><th rowspan="2"><bold>Region</bold></th><th rowspan="2"><bold>No. of examined foxes</bold></th><th colspan="2"><bold><italic>Babesia canis</italic></bold></th><th colspan="2"><bold><italic>Babesia</italic></bold><bold>cf.</bold><bold><italic>microti</italic></bold></th><th colspan="2"><bold><italic>Hepatozoon canis</italic></bold></th><th colspan="2"><bold>Total infection</bold><sup><bold>A</bold></sup></th></tr><tr valign="top"><th><bold>n</bold></th><th><bold>%</bold></th><th><bold>n</bold></th><th><bold>%</bold></th><th><bold>n</bold></th><th><bold>%</bold></th><th><bold>n</bold></th><th><bold>%</bold></th></tr></thead><tbody><tr valign="top"><td>East Bosnia (EB)</td><td>32</td><td>0</td><td>0.0</td><td>13</td><td>40.6</td><td>10</td><td>31.2</td><td>23</td><td>71.8</td></tr><tr valign="top"><td>Central Bosnia (CB)</td><td>53</td><td>0</td><td>0.0</td><td>12</td><td>22.6</td><td>23</td><td>43.4</td><td>35</td><td>66.0</td></tr><tr valign="top"><td>North Bosnia (NB)</td><td>9</td><td>1</td><td>11.1</td><td>2</td><td>22.2</td><td>3</td><td>33.3</td><td>6</td><td>66.6</td></tr><tr valign="top"><td>Herzegovina (HER)</td><td>6</td><td>0</td><td>0.0</td><td>4</td><td>66.6</td><td>0</td><td>0.0</td><td>4</td><td>66.6</td></tr><tr valign="top"><td>North East Bosnia (NEB)</td><td>15</td><td>0</td><td>0.0</td><td>6</td><td>40.0</td><td>7</td><td>46.6</td><td>13</td><td>86.6</td></tr><tr valign="top"><td>North West Bosnia (NWB)</td><td>4</td><td>0</td><td>0.0</td><td>1</td><td>25.0</td><td>3</td><td>75.0</td><td>4</td><td>100</td></tr><tr valign="top"><td>Total</td><td>119</td><td>1</td><td>0.8</td><td>38</td><td>31.9</td><td>46</td><td>38.3</td><td>85</td><td>70.8</td></tr></tbody></table><table-wrap-foot><p><sup>A</sup>Refers to total number of infections, not total number of infected animals.</p></table-wrap-foot></table-wrap><table-wrap id="Tab3"><label>Table 3</label><caption><p><bold>Number of foxes infected with</bold><bold><italic>Babesia canis</italic></bold><bold>,</bold><bold><italic>Babesia</italic></bold><bold>cf.</bold><bold><italic>microti</italic></bold><bold>and</bold><bold><italic>Hepatozoon canis</italic></bold><bold>in Bosnia and Herzegovina categorized by sex and age</bold></p></caption><table frame="hsides" rules="groups"><thead><tr valign="top"><th rowspan="2"><bold>Region</bold></th><th colspan="4"><bold><italic>Babesia canis</italic></bold></th><th colspan="4"><bold><italic>Babesia</italic></bold><bold>cf.</bold><bold><italic>microti</italic></bold></th><th colspan="4"><bold><italic>Hepatozoon canis</italic></bold></th></tr><tr valign="top"><th><bold>Male</bold></th><th><bold>Female</bold></th><th><bold>>1 yr.</bold></th><th><bold><1 yr.</bold></th><th><bold>Male</bold></th><th><bold>Female</bold></th><th><bold>>1 yr.</bold></th><th><bold><1 yr.</bold></th><th><bold>Male</bold></th><th><bold>Female</bold></th><th><bold>>1 yr.</bold></th><th><bold><1 yr.</bold></th></tr></thead><tbody><tr valign="top"><td>East Bosnia (EB)</td><td>-</td><td>-</td><td>-</td><td>-</td><td>6</td><td>7</td><td>13</td><td>-</td><td>5</td><td>5</td><td>10</td><td>-</td></tr><tr valign="top"><td>Central Bosnia (CB)</td><td>-</td><td>-</td><td>-</td><td>-</td><td>8</td><td>4</td><td>10</td><td>2</td><td>14</td><td>9</td><td>22</td><td>1</td></tr><tr valign="top"><td>North Bosnia (NB)</td><td>1</td><td>-</td><td>1</td><td>-</td><td>2</td><td>-</td><td>2</td><td>-</td><td>2</td><td>1</td><td>3</td><td>-</td></tr><tr valign="top"><td>Herzegovina (HER)</td><td>-</td><td>-</td><td>-</td><td>-</td><td>4</td><td>-</td><td>2</td><td>2</td><td>-</td><td>-</td><td>-</td><td>-</td></tr><tr valign="top"><td>North East Bosnia (NEB)</td><td>-</td><td>-</td><td>-</td><td>-</td><td>6</td><td>-</td><td>6</td><td>-</td><td>6</td><td>1</td><td>7</td><td>-</td></tr><tr valign="top"><td>North West Bosnia (NWB)</td><td>-</td><td>-</td><td>-</td><td>-</td><td>1</td><td>-</td><td>1</td><td>-</td><td>1</td><td>2</td><td>3</td><td>-</td></tr><tr valign="top"><td>Positive/Total sampled</td><td>1/85</td><td>0/34</td><td>1/112</td><td>0/7</td><td>27/85</td><td>11/34</td><td>34/112</td><td>4/7</td><td>28/85</td><td>18*/34</td><td>45/112</td><td>1/7</td></tr></tbody></table><table-wrap-foot><p>*(p < 0.05).</p></table-wrap-foot></table-wrap></p><p>A total of 90 PCR-positive samples were sequenced. Of these, 38 samples showed 99–100% similarity to 18S sequences attributed to <italic>Theileria annae</italic> [GenBank accession no. HM212628.1] found in foxes from Croatia [<xref ref-type="bibr" rid="CR3">3</xref>] and <italic>Babesia</italic> sp. ‘Spanish dog’ [GenBank accession no. AY457974.1] isolated from dogs in Spain [<xref ref-type="bibr" rid="CR27">27</xref>]. A sequence of one sample showed 100% identity with sequences of <italic>B. canis canis</italic> [GenBank accession no. FJ209024.1] reported from dogs in Croatia [<xref ref-type="bibr" rid="CR49">49</xref>].</p><p>PCRs performed with the Apicomplexa-specific 18S primers BTH-1 F and BTH-1R detected <italic>H. canis</italic> in 41 (89.1%) out of a total of 46 positive samples confirmed by <italic>Hepatozoon</italic>-specific PCR and sequencing. Moreover, five PCR products were positive on gel, but the occurrence of pathogens could not be confirmed by sequencing and all were noted as false positive.</p><p>Out of 46 18S sequences of <italic>H. canis</italic>, 38 were 100% identical to a sequence from a Spanish fox [GenBank accession no. AY150067.2] [<xref ref-type="bibr" rid="CR38">38</xref>], while all others showed up to 99% similarity to sequences from foxes and dogs from all over the world (East Asia, India, Europe, North Africa and South America). All sequences are deposited in GenBank and are available under accession numbers KP216410–KP216494. The presence of <italic>Anaplasma</italic> spp., <italic>Bartonella</italic> spp., ‘<italic>Candidatus</italic> N. mikurensis’, <italic>E. canis</italic>, <italic>Rickettsia</italic> spp. and blood filaroid nematodes was not detected in our samples.</p></sec><sec id="Sec8" sec-type="discussion"><title>Discussion</title><p>This study for the first time reports the occurrence of <italic>B. canis</italic>, <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> parasites in red foxes from Bosnia and Herzegovina. The piroplasm <italic>B.</italic> cf. <italic>microti</italic> was molecularly confirmed in 38/119 (31.9%) animals from all six surveyed regions, with the highest prevalence (66.6%) detected in Herzegovina. The observed prevalence of infection was higher than that previously found in Croatia (5%; [<xref ref-type="bibr" rid="CR3">3</xref>]), Italy (0.98%; [<xref ref-type="bibr" rid="CR7">7</xref>]), Poland (0.7%; [<xref ref-type="bibr" rid="CR4">4</xref>]) and Spain (14%; [<xref ref-type="bibr" rid="CR30">30</xref>]). Higher prevalence was reported in foxes from Austria (50%; [<xref ref-type="bibr" rid="CR29">29</xref>]), Germany (46.4%; [<xref ref-type="bibr" rid="CR9">9</xref>]) and Portugal (69.2%; [<xref ref-type="bibr" rid="CR6">6</xref>]). Differences between prevalence levels reported among studies may occur due to different tissues sampled or assay used, but also due to geographical distributions of the tick vectors [<xref ref-type="bibr" rid="CR6">6</xref>]. <italic>Ixodes hexagonus</italic> was suspected to be the main vector responsible for transmission of <italic>B.</italic> cf. <italic>microti</italic> [<xref ref-type="bibr" rid="CR50">50</xref>], but recently it was molecularly detected in <italic>I. ricinus</italic>, <italic>I. canisuga</italic> and <italic>R. sanguineus</italic> as well [<xref ref-type="bibr" rid="CR9">9</xref>,<xref ref-type="bibr" rid="CR51">51</xref>]. However, the vector competence of these tick species is not confirmed yet and the presence of the piroplasm DNA in the ticks may represent blood engorged from an infected animal host [<xref ref-type="bibr" rid="CR6">6</xref>,<xref ref-type="bibr" rid="CR9">9</xref>]. The fact that infected foxes were discovered in all studied areas, and that the occurrence of <italic>I. hexagonus</italic> was observed only in the western part of Bosnia [<xref ref-type="bibr" rid="CR52">52</xref>], supports the hypothesis about the existence of another vector species other than <italic>I. hexagonus</italic>. Moreover, <italic>B. canis</italic> was detected in one fox (0.8%) originating from North Bosnia. This finding was completely unexpected, since <italic>B. canis</italic> has been molecularly confirmed only in a single fox from Portugal so far [<xref ref-type="bibr" rid="CR6">6</xref>], suggesting that foxes are not suitable hosts for these canine blood parasites; they were probably transmitted accidentally by ticks which fed on infected dogs.</p><p>In this study, <italic>H. canis</italic> was the most frequently detected parasite, with a prevalence of 38.6% (46/119). Infected foxes were present in almost all sampled regions, except in the region of Herzegovina. This finding is intriguing because <italic>R. sanguineus</italic> is present in Herzegovina [<xref ref-type="bibr" rid="CR52">52</xref>] and very small sample size obtained from this area (n = 6) may be the reason for the absence of <italic>H. canis</italic>. However, <italic>H. canis</italic> was also observed in areas lacking <italic>R. sanguineus</italic> [<xref ref-type="bibr" rid="CR29">29</xref>,<xref ref-type="bibr" rid="CR37">37</xref>,<xref ref-type="bibr" rid="CR53">53</xref>]. Among studies using DNA from spleen or blood samples for PCRs, the prevalence of infections with <italic>H. canis</italic> in red foxes ranged from 8% in Hungary to 75.6% in Portugal [<xref ref-type="bibr" rid="CR3">3</xref>,<xref ref-type="bibr" rid="CR4">4</xref>,<xref ref-type="bibr" rid="CR10">10</xref>,<xref ref-type="bibr" rid="CR11">11</xref>,<xref ref-type="bibr" rid="CR29">29</xref>-<xref ref-type="bibr" rid="CR31">31</xref>,<xref ref-type="bibr" rid="CR36">36</xref>,<xref ref-type="bibr" rid="CR37">37</xref>]. The fact that there was no significant difference in the prevalence between the age groups of the host in our study might indicate that foxes were infected at a young age by vertical intrauterine transmission or by vectors as already suggested [<xref ref-type="bibr" rid="CR10">10</xref>]. Since we had only 7 juveniles in our dataset, we cannot clearly confirm or reject the hypothesis of intrauterine transmission. But even though the age and sex groups were not statistically different, the samples represent not confounding data. Interestingly, the infection rate of females was significantly higher, which suggests that females have an important role in the maintaining and spreading of infection. It has been suggested that there is a difference in parasite burden between males and females and between parasitic taxa due to differences such as hormone level or innate immune response [<xref ref-type="bibr" rid="CR54">54</xref>,<xref ref-type="bibr" rid="CR55">55</xref>]. However, for <italic>H. canis</italic> the differences of the parasite load between females and males has not been explained, yet.</p><p>In dogs, infections with <italic>B.</italic> cf<italic>. microti</italic> and <italic>H. canis</italic> usually cause disorders that affect spleen, lymph nodes, bone marrow and kidneys, resulting in anemia, azotemia, fever, lethargy, cachexia or even death [<xref ref-type="bibr" rid="CR25">25</xref>-<xref ref-type="bibr" rid="CR28">28</xref>,<xref ref-type="bibr" rid="CR35">35</xref>]. During necropsies it was noticed that all examined foxes, except for seven with sarcoptic mange (5.8%), were in a good body condition. This might indicate a low pathogenicity of these pathogens in this wild canid species, as already suggested [<xref ref-type="bibr" rid="CR9">9</xref>]. All sequences obtained from red foxes in this study had a high homology to the ones previously reported from different canid species and different locations, which indicates a wide circulation of these pathogens without obvious geographical and host-related division patterns [<xref ref-type="bibr" rid="CR31">31</xref>].</p><p>Although several studies suggest that red foxes can serve as reservoir hosts for various vector-borne bacteria [<xref ref-type="bibr" rid="CR12">12</xref>-<xref ref-type="bibr" rid="CR18">18</xref>], their presence could not be confirmed in this study. Regarding filaroid nematodes, <italic>D. immitis</italic> and <italic>D. repens</italic> were reported in dogs from Bosnia and Herzegovina [<xref ref-type="bibr" rid="CR43">43</xref>], confirming that this area is suitable for the transmission of these parasites, but they also were not detected in foxes by PCR or necropsy. Since the present data does not allow the occurrence of bacteria and filaroid nematodes in foxes from Bosnia and Herzegovina to be completely excluded, monitoring and further analysis are necessary to elucidate the potential role of red foxes in their epidemiology.</p></sec><sec id="Sec9" sec-type="conclusions"><title>Conclusion</title><p>The relatively high prevalence and widespread distribution of <italic>B.</italic> cf. <italic>microti</italic> and <italic>H. canis</italic> among the red fox population of Bosnia and Herzegovina support the existence of a sylvatic cycle and reinforce the assumption that foxes might be a possible reservoir and vector of infection to dogs and other canids. Moreover, data presented in this study should improve awareness among veterinarians and alert them to include infections caused by these two pathogens in the differential diagnosis of canine babesiosis.</p></sec></body><back><fn-group><fn><p><bold>Competing interests</bold></p><p>The authors declare that they have no competing interests.</p></fn><fn><p><bold>Authors’ contributions</bold></p><p>AH and GGD conceived and designed the study; AH performed PCRs and drafted the manuscript; AA collected the samples; HPF performed sequence analyses; JH designed the primers and performed sequence analyses; WWP provided assistance in the lab and performed PCRs; GGD performed the statistical analysis and revised the manuscript. 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