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Molecular evidence of Chlamydophila pneumoniae infection in reptiles in Argentina
Evidencia molecular de la infección por Chlamydophila pneumoniae en reptiles de Argentina
María C. Frutos
Corresponding author
mariaceliafrutos@gmail.com

Corresponding author.
, Marina S. Monetti, Viviana E. Ré, Cecilia G. Cuffini
Instituto de Virología “Dr. J. M. Vanella”, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Maximum likelihood tree for the <span class="elsevierStyleItalic">rpoB</span> gene &#40;441 nt&#41; constructed using GTR&#43;G as model of nucleotide substitution&#44; with parameters suggested by ModelTest 3&#46;7 &#40;PhyML software&#41;&#46; Sequences belonging to this study are initiated by ARG PK&#46; Numbers above branches&#58; bootstrap values over 2000 bootstrap pseudo replicates&#46; Only bootstrap values &#62;50&#37; are shown at nodes&#46; <span class="elsevierStyleItalic">C&#46; abortus</span> S26&#47;3 is used as out-group&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> LPCOLN&#58; isolated from a koala&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> WBB&#58; isolated from a bandicoot&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> TWAR 183&#44; CWL029&#44; AR39&#44; J138&#58; isolated from humans&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 01&#58; isolated from a pig&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 02&#58; isolated from cattle&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> C1&#58; isolated from a sheep&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 6BC&#58; isolated from a parakeet&#46; <span class="elsevierStyleItalic">C&#46; felis</span> Fe&#47;C&#8211;56&#58; isolated from a cat&#46; <span class="elsevierStyleItalic">C&#46; caviae</span> GPIC&#58; isolated from a guinea pig&#46; <span class="elsevierStyleItalic">C&#46; pecorum</span> E58&#58; isolated from cattle&#46; <span class="elsevierStyleItalic">C&#46; muridarum</span> Nigg&#58; isolated from a mouse&#46; <span class="elsevierStyleItalic">C&#46; trachomatis</span> L2c&#58; isolated from humans&#46; <span class="elsevierStyleItalic">C&#46; abortus</span> S26&#47;3&#58; isolated from a sheep&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Chlamydia pneumoniae</span> is a widespread pathogen responsible for upper and lower respiratory tract infections&#44; in addition to a wide range of human and animal diseases<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a>&#46; The range of hosts known to be infected by <span class="elsevierStyleItalic">C&#46; pneumoniae</span> has expanded to several species of reptiles&#44; such as puff adders &#40;<span class="elsevierStyleItalic">Bitis arietans</span>&#41;&#44; flap-necked chameleons &#40;<span class="elsevierStyleItalic">Chameleo dilepis</span>&#41;&#44; green turtles &#40;<span class="elsevierStyleItalic">Chelonia mydas</span>&#41;&#44; Nile crocodiles &#40;<span class="elsevierStyleItalic">Crocodylus niloticus</span>&#41;&#44; green iguanas &#40;<span class="elsevierStyleItalic">Iguana iguana</span>&#41; and Burmese pythons &#40;<span class="elsevierStyleItalic">Python molurus bivittatus</span>&#41;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;3</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a>&#46; Lesions are varied and include histiocytic granulomas &#40;puff adders&#41;&#44; granulomatous inflammation &#40;flap necked chameleons&#41;&#44; necrotizing enteritis &#40;green iguanas&#41;&#44; necrotizing myocarditis &#40;green turtles&#41;&#44; and proliferative pneumonia &#40;Burmese pythons&#41;7&#46; However&#44; in humans&#44; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> infections range from asymptomatic to severe respiratory diseases&#44; including pneumonia&#46; Previous studies have reported seroprevalence values of 50&#37; by the age of 20 years and 80&#37; in the elderly<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a>&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Genome characterization of the <span class="elsevierStyleItalic">C&#46; pneumoniae</span> sequence detected in Australian reptiles and amphibians showed 99&#37; homology with the human sequence&#44; revealing their potential role in the zoonotic transmission from reptiles to humans11&#46; Recently&#44; at a Recreation Center in Cordoba province&#44; a specimen of reticulated python &#40;<span class="elsevierStyleItalic">Python reticulata</span>&#41; presented symptoms compatible with proliferative pneumonia&#44; which led to the development of this investigation&#46; The aim of this study was to describe the presence of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> in several species of reptiles in C&#243;rdoba and in their caregivers&#44; and to evaluate the presence of specific antibodies against <span class="elsevierStyleItalic">C&#46; pneumoniae</span> in the personnel&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">We analyzed 27 cloacal swab samples from 19 reptiles at a recreational area using a specific nested-PCR for <span class="elsevierStyleItalic">C&#46; pneumoniae</span><a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a>&#46; In May 2011&#44; we obtained 1 cloacal swab from the reticulated python with symptoms compatible with proliferative pneumonia and 18 samples of reptiles living together&#46; In December 2011&#44; resampling of only 8 of these reptiles could be conducted&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The cotton swabs were placed in 1<span class="elsevierStyleHsp" style=""></span>ml sucrose-phosphateglutamate &#40;SPG&#41; and 200<span class="elsevierStyleHsp" style=""></span>&#956;l was subjected to DNA extraction using the Accuprep Genomic DNA Extraction Kit &#40;BIONEER&#44; Alameda&#44; CA&#44; USA&#41; according to the manufacturer&#39;s instructions&#46; DNA AR39 <span class="elsevierStyleItalic">C&#46; pneumoniae</span> &#40;ATCC53592&#41; was used as positive control&#46; Negative controls &#40;deionized H<span class="elsevierStyleInf">2</span>O instead of template DNA&#41; were included in all PCR reaction sets&#46; First&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;l of DNA extract was used to amplify a fragment of RNA polymerase beta subunit gene &#40;<span class="elsevierStyleItalic">rpoB</span>&#41; using primers HL1 &#40;GTT GTT CAT GAA GGC CTA CT&#41;&#47; HR1 &#40;TGC ATA ACC TAC GGT GTG TT&#41; and N1 &#40;AGT TGA GCA TAT TCG TGA GG&#41;&#47; N2 &#40;TTT ATT TCC GTG TCG TCC AG&#41; as previously described by Mass et al&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Positive samples were sequenced to corroborate the species&#46; For sequence analysis&#44; the nested polymerase chain reaction products were purified with the QIAquick Gel Extraction Kit &#40;Qiagen&#44; Valencia&#44; CA&#44; USA&#41; and subjected to direct nucleotide sequencing reaction in both directions using an ABI automatic sequencer &#40;Applied Biosystems&#44; Foster City&#44; CA&#44; USA&#41;&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> identification was confirmed by phylogenetic analysis&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Human pharyngeal swabs were also analyzed by a nested- PCR of <span class="elsevierStyleItalic">C&#46; pneumoniae</span><a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a>&#46; Furthermore&#44; sera from the 6 healthy caregivers were tested for <span class="elsevierStyleItalic">C&#46; pneumoniae</span> antichlamydial immunoglobulin G &#40;IgG&#41; and IgM using the microimmunofluorescence assay &#40;MIF&#41;&#44; according to the manufacturer&#39;s instructions &#40;Bion Enterprises<span class="elsevierStyleSup">&#174;</span>&#44; France&#41;&#46; In this test&#44; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> elementary bodies were purified by removal of genus-reactive LPS&#46; Since this technique has very low cross-reactivity with other <span class="elsevierStyleItalic">Chlamydophila</span> species&#44; it is recommended for the differential diagnosis of these agents in humans&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">rpoB</span> sequences obtained were submitted to the GenBank &#40;accession numbers are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41; and alignment using the ClustalX program was performed &#40;Conway Institute UCD Dublin&#44; Dublin&#44; Ireland&#41;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a>&#46; The maximum likelihood tree was constructed with the PhyML 3&#46;0 software &#40;Universit&#233; de Montpellier&#44; Montpellier&#44; France&#41;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a>&#46; The model of nucleotide substitution for the data set analyzed was selected according to the Akaike Information Criterion implemented in the ModelTest 3&#46;7 software &#40;Universidad de Vigo&#44; Galicia&#44; Spain&#41;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a>&#46;<a name="p47"></a></p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">Among the cloacal swabs samples of 19 reptiles studied&#44; 11 &#40;57&#46;89&#37;&#41; tested <span class="elsevierStyleItalic">C&#46; pneumoniae</span> positive by nested-PCR &#91;<span class="elsevierStyleItalic">Pythom reticulata</span> &#40;n&#61;2&#41;&#44; <span class="elsevierStyleItalic">Python molurus bivittatus</span> &#40;n&#61;2&#41;&#44; <span class="elsevierStyleItalic">Bothrops alternatus</span> &#40;n&#61;1&#41;&#44; <span class="elsevierStyleItalic">Crotalus atrox</span> &#40;n&#61;1&#41;&#44; <span class="elsevierStyleItalic">Trachemis scripta elegans</span> &#40;n&#61;2&#41;&#59; <span class="elsevierStyleItalic">Phrynops hilaris</span> &#40;n&#61;2&#41;&#59; <span class="elsevierStyleItalic">Micrurus pirracryptus</span> &#40;n&#61;1&#41;&#93;&#46; DNA of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> was not detected in samples from the symptomatic reticulated python&#44; probably because at the time of collection&#44; this reptile was isolated and had already received specific antibiotic treatment&#46; PCR products suitable for sequencing were obtained from 6 reptiles&#46; Sequence analysis confirmed that the amplicons obtained belonged to <span class="elsevierStyleItalic">C&#46; pneumoniae</span> &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; These findings demonstrated that <span class="elsevierStyleItalic">C&#46; pneumoniae</span> is capable of infecting several species of snakes and turtles&#44; broadening the range of reptiles known to be infected by this primarily human pathogen&#46; After confirmation of infection&#44; reptiles were subjected to specific antibiotic treatment&#46; All the caregivers&#8217; pharyngeal swabs tested negative for <span class="elsevierStyleItalic">C&#46; pneumoniae</span>&#44; excluding active human infection&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0045" class="elsevierStylePara elsevierViewall">In the second visit to the recreational centre in December&#44; all cloacal and pharyngeal swabs analyzed were negative for <span class="elsevierStyleItalic">C&#46; pneumoniae</span>&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">In terms of immune response&#44; IgM antibodies anti-<span class="elsevierStyleItalic">C&#46; pneumoniae</span> were not detected in the caregivers&#8217; sera tested in May&#46; One of the caregivers who maintained sporadic contact with the animals presented IgG titers of 1&#58;512&#46; Three caregivers with periodic contact showed IgG titers of 1&#58;2048&#46; One susceptible caregiver &#91;IgG &#40;&#8722;&#41;&#93; was the only worker who always used protection when handling the animals or cleaning their excreta&#46; In December&#44; the caregiver who used protective equipment remained susceptible while IgG levels remained elevated in the others &#40;1&#58;2048&#41;&#46; The immune status of a new caregiver who had reported pneumonia in September showed high titers of IgG anti-<span class="elsevierStyleItalic">C&#46; pneumoniae</span> &#40;1&#58;4096&#41;&#59; however specific IgM was not detected&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">The presence of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> strains in reptiles is important because this bacterium is a common cause of human pneumonia and bronchitis throughout the world&#59; in addition&#44; it has recently been associated with several chronic diseases&#44; including coronary heart disease&#44; Alzheimer&#39;s disease&#44; and multiple sclerosis<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a>&#46; Although <span class="elsevierStyleItalic">C&#46; pneumoniae</span> DNA or specific IgM was not detected in the caregivers&#44; the detection of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> DNA in the animals demonstrated the circulation of this agent in the recreational park and supports the exacerbated immune response in people handling the reptiles&#44; which suggests a potential zoonotic cycle&#46; Respiratory diseases and excretion of this bacterium in the reptiles were attenuated by specific antibiotic treatment&#46; The implementation of biosecurity measures is essential to prevent transmission&#44; as demonstrated by our results&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">In our study&#44; as well as in other reports in a range of reptiles &#40;snakes&#44; iguanas&#44; chameleons&#41; and amphibians &#40;frogs&#44; turtles&#41;&#44; the relationship of our sequences with other reference data sets of <span class="elsevierStyleItalic">chlamydiae</span> indicates that<a name="p48"></a> although our sequences belonged to the <span class="elsevierStyleItalic">C&#46; pneumoniae</span> branch&#44; they are quite distinct from the human TWAR strain &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a>&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Even though a limited amount of sequences were analyzed&#44; we found that all <span class="elsevierStyleItalic">C&#46; pneumoniae</span> sequences clustered among them and revealed segregation with sequences of human strains&#46; Although transmission among humans is believed to occur from person to person through respiratory secretions<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a>&#44; until more is known about the epidemiology&#44; pathogenicity&#44; and transmission of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> strains recovered from captive and wild populations of cold-blooded animals&#44; their zoonotic potential must be considered&#46; Moreover&#44; because of the increasing ownership of reptiles as pets&#44; caution must be exercised during direct handling of these animals&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Isolation and characterization of reptile <span class="elsevierStyleItalic">C&#46; pneumoniae</span> strains are required to assess their clinical impact and possible zoonotic potential&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Ethical responsibilities</span><p id="par0075" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Protection of human and animal subjects&#46;</span> The authors declare that no experiments were performed on humans or animals for this investigation&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Confidentiality of data</span>&#46; The authors declare that they have followed the protocols of their work centre on the publication of patient data and that all the patients included in the study have received sufficient information and have given their informed consent in writing to participate in that study&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Right to privacy and informed consent&#46;</span> The authors declare that no patient data appears in this article&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conflicts of interest</span><p id="par0090" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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        6 => array:2 [
          "identificador" => "xack214235"
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          "titulo" => "References"
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    "fechaRecibido" => "2013-08-06"
    "fechaAceptado" => "2014-02-14"
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          "clase" => "keyword"
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            0 => "<span class="elsevierStyleItalic">Chlamydophila pneumoniae</span>"
            1 => "Reptiles"
            2 => "Phylogenetic Analysis"
            3 => "Immune Response"
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            0 => "<span class="elsevierStyleItalic">Chlamydophila pneumoniae</span>"
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            2 => "An&#225;lisis filogen&#233;ticos"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">In the central area of Argentina&#44; the epidemiological and molecular characteristics of <span class="elsevierStyleItalic">Chlamydophila pneumoniae</span> infections in reptiles are still unknown&#46; A nested polymerase chain reaction of the <span class="elsevierStyleItalic">rpoB</span> gene was used to detect <span class="elsevierStyleItalic">C&#46; pneumoniae</span> in cloacal swab samples from 19 reptiles at a recreational area&#46; Eleven &#40;57&#46;89&#37;&#41; reptiles were positive&#59; the sequencing and phylogenetic analysis confirmed the presence of this bacterium&#46; Neither <span class="elsevierStyleItalic">C&#46; pneumoniae</span> DNA in the caregivers pharynges nor IgM antibodies anti-<span class="elsevierStyleItalic">C&#46; pneumoniae</span> in their serum samples were detected&#59; however&#44; caregivers presented very high titers of IgG anti<span class="elsevierStyleItalic">-C&#46; pneumoniae&#46;</span> The detection of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> DNA in reptiles demonstrated the circulation of this agent in the recreational area and could be responsible for the exacerbated immune response of the personnel handling the reptiles&#44; which suggests a potential zoonotic cycle&#46; This is the first report of the detection of <span class="elsevierStyleItalic">C&#46; pneumoniae</span> in reptiles in Argentina&#46;</p></span>"
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      "es" => array:2 [
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">En la regi&#243;n central de Argentina&#44; las caracter&#237;sticas epidemiol&#243;gicas y moleculares de las infecciones por <span class="elsevierStyleItalic">Chlamydophila pneumoniae</span> en reptiles son desconocidas&#46; Para detectar <span class="elsevierStyleItalic">C&#46; pneumoniae</span>&#44; se us&#243; la reacci&#243;n en cadena de la polimerasa anidada que amplifica el gen <span class="elsevierStyleItalic">rpoB</span> en muestras de hisopado cloacal de 19 reptiles&#46; Once &#40;57&#44;89 &#37;&#41; reptiles resultaron positivos&#46; La secuenciaci&#243;n y el an&#225;lisis filogen&#233;tico corroboraron la presencia de esta bacteria&#46; No se detect&#243; ADN de <span class="elsevierStyleItalic">C&#46; pneumoniae</span> en la faringe ni IgM anti-<span class="elsevierStyleItalic">C&#46; pneumoniae</span> en el suero de los cuidadores&#59; sin embargo&#44; ellos presentaron t&#237;tulos muy elevados de IgG anti-<span class="elsevierStyleItalic">C&#46; pneumoniae&#46;</span> La detecci&#243;n de ADN de <span class="elsevierStyleItalic">C&#46; pneumoniae</span> en los reptiles demostr&#243;<a name="p46"></a> la circulaci&#243;n de este agente en el centro recreativo donde se realiz&#243; este estudio&#44; lo que podr&#237;a explicar la exacerbada respuesta inmunitaria en los cuidadores&#59; este hallazgo sugiere la presencia de un potencial ciclo zoon&#243;tico&#46; Se reporta aqu&#237; por primera vez la detecci&#243;n de <span class="elsevierStyleItalic">C&#46; pneumoniae</span> en reptiles en Argentina&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Maximum likelihood tree for the <span class="elsevierStyleItalic">rpoB</span> gene &#40;441 nt&#41; constructed using GTR&#43;G as model of nucleotide substitution&#44; with parameters suggested by ModelTest 3&#46;7 &#40;PhyML software&#41;&#46; Sequences belonging to this study are initiated by ARG PK&#46; Numbers above branches&#58; bootstrap values over 2000 bootstrap pseudo replicates&#46; Only bootstrap values &#62;50&#37; are shown at nodes&#46; <span class="elsevierStyleItalic">C&#46; abortus</span> S26&#47;3 is used as out-group&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> LPCOLN&#58; isolated from a koala&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> WBB&#58; isolated from a bandicoot&#46; <span class="elsevierStyleItalic">C&#46; pneumoniae</span> TWAR 183&#44; CWL029&#44; AR39&#44; J138&#58; isolated from humans&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 01&#58; isolated from a pig&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 02&#58; isolated from cattle&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> C1&#58; isolated from a sheep&#46; <span class="elsevierStyleItalic">C&#46; psittaci</span> 6BC&#58; isolated from a parakeet&#46; <span class="elsevierStyleItalic">C&#46; felis</span> Fe&#47;C&#8211;56&#58; isolated from a cat&#46; <span class="elsevierStyleItalic">C&#46; caviae</span> GPIC&#58; isolated from a guinea pig&#46; <span class="elsevierStyleItalic">C&#46; pecorum</span> E58&#58; isolated from cattle&#46; <span class="elsevierStyleItalic">C&#46; muridarum</span> Nigg&#58; isolated from a mouse&#46; <span class="elsevierStyleItalic">C&#46; trachomatis</span> L2c&#58; isolated from humans&#46; <span class="elsevierStyleItalic">C&#46; abortus</span> S26&#47;3&#58; isolated from a sheep&#46;</p>"
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">ARG PK11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bothrops alternatus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Big Yarar&#225;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">ARG PK14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Micrurus pirracryptus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Argentinian<br>Coral Snake&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Lagoon<br>Turttle&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">JX960451&nbsp;\t\t\t\t\t\t\n
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                    0 => array:2 [
                      "titulo" => "<span class="elsevierStyleItalic">Chlamydiae</span> in free-ranging and captive frogs in Switzerland"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "C&#46; Blumer"
                            1 => "D&#46;R&#46; Zimmermann"
                            2 => "R&#46; Weilenmann"
                            3 => "L&#46; Vaughan"
                            4 => "A&#46; Pospischil"
                          ]
                        ]
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                    ]
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                    0 => array:2 [
                      "doi" => "10.1354/vp.44-2-144"
                      "Revista" => array:6 [
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                        "link" => array:1 [
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            1 => array:3 [
              "identificador" => "bib0010"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Molecular evidence to support the expansion of the host range of <span class="elsevierStyleItalic">Chlamydia pneumoniae</span> to include reptiles as well as humans&#44; horses&#44; koalas and amphibians"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:7 [
                            0 => "T&#46; Bodetti"
                            1 => "E&#46; Jacobson"
                            2 => "C&#46; Wan"
                            3 => "L&#46; Hafner"
                            4 => "A&#46; Pospischil"
                            5 => "K&#46; Rose"
                            6 => "P&#46; Timms"
                          ]
                        ]
                      ]
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                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1078/0723-2020-00086"
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                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12086181"
                            "web" => "Medline"
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                    ]
                  ]
                ]
              ]
            ]
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              "identificador" => "bib0015"
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                0 => array:2 [
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                    0 => array:2 [
                      "titulo" => "Isolation of <span class="elsevierStyleItalic">Chlamydophila pneumoniae</span> from atheromas of the carotid artery and their antibiotics susceptibility profile"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:10 [
                            0 => "C&#46; Cuffini"
                            1 => "L&#46; Alberto Guzm&#225;n"
                            2 => "N&#46; Villegas"
                            3 => "C&#46; Eduardo Alonso"
                            4 => "L&#46; Mart&#237;nez-Riera"
                            5 => "M&#46; Rodr&#237;guez-Fermep&#237;n"
                            6 => "A&#46; Carolina Entrocassi"
                            7 => "M&#46; Pilar Adamo"
                            8 => "M&#46; Pedranti"
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                        "fecha" => "2006"
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            3 => array:3 [
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                0 => array:2 [
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                      "titulo" => "Background and current knowledge of <span class="elsevierStyleItalic">Chlamydia pneumoniae</span> and atherosclerosis"
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                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
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                    ]
                  ]
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                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J Infect Dis"
                        "fecha" => "2000"
                        "volumen" => "181"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "A simple&#44; fast&#44; and accurate algorithm to estimate large phylogenies by maximum likelihood"
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                          "etal" => false
                          "autores" => array:2 [
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