Genetic diversity of Mycoplasma hyopneumoniae in Mendoza province

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Torres Higuera, Sabrina Del C. Jiménez Velásquez, José L. Rodríguez Bautista, Rocio E. Patiño Burbano" "autores" => array:4 [ 0 => array:2 [ "nombre" => "Ligia D." "apellidos" => "Torres Higuera" ] 1 => array:2 [ "nombre" => "Sabrina Del C." "apellidos" => "Jiménez Velásquez" ] 2 => array:2 [ "nombre" => "José L." "apellidos" => "Rodríguez Bautista" ] 3 => array:2 [ "nombre" => "Rocio E." 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Thirteen clusters (I to XIII) were identified at a similarity cutoff of 85%." ] ] ] "textoCompleto" => "IntroductionMycoplasma hyopneumoniae is the primary agent involved in porcine enzootic pneumonia (EP) M. hyopneumoniae infections are highly prevalent in almost all swine-producing areas, causing significant economic losses to the pig industry worldwide<a class="elsevierStyleCrossRef" href="#bib0220">21</a>.In Argentina, pig production is mainly concentrated in Santa Fe, Buenos Aires and Córdoba. provinces. EP is highly prevalent both, in indoor and outdoor systems in Argentina<a class="elsevierStyleCrossRef" href="#bib0140">5</a>. However, there is a lack of information about prevalence and other epidemiological aspects of EP in other provinces in which pig production is less developed, as in Mendoza province.Different genetic types of M. hyopneumoniae have been identified in herds from Córdoba, Santa Fe and San Luis provinces<a class="elsevierStyleCrossRefs" href="#bib0175">12,18,20</a>; however they have never been reported in Mendoza. Thus, the objective of this study (n=100) was to assess the genetic diversity of M. hyopneumoniae circulating in herds from the province of Mendoza.Material and methodsThe study was performed according to the international guidelines of the Council for International Organizations of Medical Sciences (CIOMS).Herds and study designA cross-sectional study was carried out in an abattoir by collecting 20 broncho-alveolar lavage (BAL) specimens recovered from pigs from each of the five herds under study. Herds were located in different districts of Mendoza province. The main characteristics of the herds such as the kind of system and size (number of sows), among others are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Sample processing and M. hyopneumoniae typingDNA from LBA specimens was extracted using DNAzol (Thermo Fisher Scientific, Argentina) according to the manufacturer's instructions. For M. hyopneumoniae detection 100 samples were analyzed by a nested-PCR<a class="elsevierStyleCrossRef" href="#bib0120">1</a>, considered as the screening technique.In order to type M. hyopneumoniae, P97 R1, P97 R1A and P146 R3 loci were analyzed only in those specimens that were positive (48) to the nPCR screening mentioned above. Tandem repeat motives of P97 R1, P97 R1A and P146 R3 were amplified by a nested PCR (nPCR) format previously described<a class="elsevierStyleCrossRef" href="#bib0180">13</a>. After amplification, amplicons were purified (Puriprep-GP Kit, Inbio Highway, Argentina), quantified and sequenced (ABI 3130xl; Applied Biosystems, US) using the primers reported by Vranckx et al.<a class="elsevierStyleCrossRef" href="#bib0225">22</a>, for P97 and by Mayor et al.<a class="elsevierStyleCrossRef" href="#bib0160">9</a>, for P146. The number of tandem repeats was determined by analyzing the sequences with BioEdit 7.1.3.0 software<a class="elsevierStyleCrossRef" href="#bib0150">7</a>. For further analysis, only those specimens which were positive for both loci were considered.Data analysisA dendrogram based on the categorical values of the number of tandem repeats was constructed with the FAMD 1.20 software<a class="elsevierStyleCrossRef" href="#bib0190">15</a> using the Dice similarity coefficient and the unweighted pair group method with arithmetic means (UPGMA). The number of tandem repeats from the 232, J, 7448, PMS and 7422 reference M. hyopneumoniae strains<a class="elsevierStyleCrossRef" href="#bib0130">3</a> was included.The Simpson's index of diversity of the combined variable-number of tandem repeat (VNTR) regions (P97 R1, P97 R1A and P146 R3) was calculated by using the Hunter-Gaston diversity index – HDGI<a class="elsevierStyleCrossRef" href="#bib0155">8</a>.ResultsM. hyopneumoniae was detected by nPCR in all the herds in 48% (48/100) of the specimens. For P97, 27 specimens were positive and could be further sequenced and typed. Nested-PCR for P146 R3 showed more sensitivity, amplifying all processed BAL specimens. Thus, 27/48 (56%) of the specimens could be typed for both loci. The remaining specimens (n=21) could be typed only for P146 R3 and were not included in the analysis. Eight MLVA types were identified: 8-3-16 (n=11), all of them obtained from herd B, 8-4-16 (n=5) from herds A and C, 6-4-15 (n=4) from herd D, 8-5-17 (n=3) from herd E, and the less frequent types: 8-4-14 (n=1), 8-5-14 (n=1), 8-4-17 (n=1), 9-3-17 (n=1) from herds A, C and E, respectively (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). The numbers of tandem repeats of the analyzed loci for M. hyopneumoniae reference strains were: 13-1-21 (strain 232), 9-3-18 (strain J), 10-4-44 (strain 7448), 15-1-19 (strain PMS) and 12-3-40 (strain 7422).<elsevierMultimedia ident="tbl0010"></elsevierMultimedia>At a similarity cutoff of 85%, 13 clusters were observed – I to XIII – (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Most local genotypes were more related to other local genotypes than to the reference strains, with two exceptions (reference strain 7448 and local variant 64). Reference strain 7448 was more closely related to the local strains than to other reference strains. On the other hand, genetic variant 64 (obtained from herd E) was closely related to the reference strains than to the other native genotypes. Only one genetic variant of the agent was found in herd B (grouped into Cluster VII). This genotype was exclusively found in this herd. The same situation was observed in herd D (one genetic variant exclusively found in this herd, grouped into Cluster II). In herd A, three different genetic variants were observed, grouped in Clusters IV, V (variants exclusively found in this herd) and VIII (together with genotypes found in herd C). In herd C, two different variants were found. One genetic variant was exclusively found in this herd (Cluster III). The other variant corresponds to a genotype also found in herd A and grouped into Cluster VIII. Two different genotypes were observed in herd E. These genotypes were exclusively found in this herd and grouped into clusters VI and XI. All reference strains clustered into different groups (I, IX, X XII and XIII) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>The number of tandem repeats for each locus and their combination are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>. Simpson's index of diversity was D=0.789.DiscussionThe circulation of different genetic types of M. hyopneumoniae in Mendoza province was demonstrated using a P97-P146 MLVA scheme. Since no molecular marker has been able to discriminate between high and low virulence M. hyopneumoniae strains, knowing the circulation of the different genotypes is important for the development of control strategies against EP. M. hyopneumoniae genetic diversity has been reported around the world at regional and herd level, between related and unrelated herds<a class="elsevierStyleCrossRefs" href="#bib0145">6,9,10,14,16,17,19</a>.The 2-loci (3-tandem repeat regions) MLVA profiles detected in this study can only be compared to the profiles reported by few studies, since neither these two loci were analyzed nor the number of repeat units present was determined in most reports. In this regard, some P97 R1 and P146 R3 MLVA types found here, were similar to those reported by Dos Santos et al. 6, in specimens from US and Spain. However, they did not consider the P97 R1A region, whose analysis increased the polymorphism. In Argentina, only one study used a similar MLVA Scheme<a class="elsevierStyleCrossRef" href="#bib0175">12</a>.The discriminatory power was lower than the one reported by Dos Santos et al.<a class="elsevierStyleCrossRef" href="#bib0145">6</a>, mainly due to the number of processed specimens. It is worth mentioning that if the R1A region of P97 had not been included into the analysis, it would have obtained 5 MLVA types with a discriminatory power of 0.62 (data not shown).Some studies reported the repeat number only for the P146 R3 motif, and they found similar polyserine repeats in some European countries<a class="elsevierStyleCrossRefs" href="#bib0160">9,14</a>. Moreover, other studies reported the diversity of this gene, and some of them included P97, but did not determine the number of repeats<a class="elsevierStyleCrossRefs" href="#bib0125">2,4,10,11,22</a>.In Argentina there are previous reports about genetic diversity of this pathogen. However, none of the previous studies analyzed P97 R1<a class="elsevierStyleCrossRef" href="#bib0205">18</a>,20. With regard to P146 R3, similar polyserine repeat motives were found in herds from Santa Fé, Córdoba, San Luis and in pigs from abroad<a class="elsevierStyleCrossRef" href="#bib0205">18</a>.From the dendrogram analysis, it can be inferred that, in general, the genotypes from Mendoza province were more related to other native genotypes than to the reference strains. This observation agrees with a previous study in which the genetic difference between local M. hyopneumoniae types and bacterin strains was found<a class="elsevierStyleCrossRef" href="#bib0215">20</a>. More in-depth studies are necessary to determine the implications of such differences.Only one genetic variant of the pathogen was found in herd B, being exclusive of this herd. The same situation was observed in herd D. These variants could represent well established M. hyopneumoniae strains and adapted to the conditions found in these herds, which agrees with previous results that showed persistence of mainly one distinct M. hyopneumoniae type within animals of the same herd<a class="elsevierStyleCrossRef" href="#bib0230">23</a>. However, the circulation of other less frequent types of the agent into the farms cannot be excluded. Different genetic variants were found in herds A, C and E. Such diversity observed in these herds could be explained by the access of different genetic types through replacement animals, wild pigs, personnel, fomites or airborne transmission. Regrettably, this information was not taken into account in this study.As we previously proposed<a class="elsevierStyleCrossRef" href="#bib0175">12</a> and considering the difficulty in comparing the results from different studies, we consider that the use of a standardized nomenclature for MLVA loci and alleles of M. hyopneumoniae is highly needed. Furthermore, the development of an online database including MLVA profiles for this pathogen would be of great help to share results within the scientific community.To the best of our knowledge, this is the first report about diversity of M. hyopneumoniae in Mendoza province. Results obtained in this work allow drawing a better picture of the genetic diversity of this pathogen in several provinces of Argentina. This is important to understand some epidemiological aspects of EP and to develop strategies to control the disease.FundingThis study was financially supported in part by PICT 0442/2015 FONCyT-ANPCyT-MinCyT, República Argentina, PPI 2016-2018, 188/2016-UNRC and Dirección Provincial de Ganadería, Ministerio de Economía, Infraestructura y Energía, Gobierno de Mendoza.Conflict of interestThe authors declare that they have no conflicts of interest." 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However, there is a lack of information about prevalence and other epidemiological aspects of EP in Mendoza province. A multiple Locus variable-number tandem repeat analysis (MLVA) targeting P97 R1, P97 R1A and P146 R3 loci was used to assess the genetic diversity of M. hyopneumoniae from clinical specimens recovered from pigs from five herds located in different districts of Mendoza province. M. hyopneumoniae could be typed from 27 bronchoalveolar lavages (BAL) specimens, and eight different MLVA types were identified. This is the first report about diversity of M. hyopneumoniae in Mendoza. Results obtained in this work allow drawing a better picture of the genetic diversity of this pathogen in Argentina." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "En Argentina, la neumonía enzoótica porcina (NEP) es altamente prevalente y se han identificado diferentes tipos genéticos de Mycoplasma hyopneumoniae. Sin embargo, se carece de información acerca de la prevalencia de NEP y de otros aspectos epidemiológicos de esta entidad en la provincia de Mendoza. En esta investigación se usó un análisis multilocus de regiones repetidas en tándem (MLVA) de los loci P97 R1, P97 R1A y P146 R3 para evaluar la diversidad genética de M. hyopneumoniae a partir de muestras clínicas de cerdos de cinco granjas localizadas en diferentes distritos de la provincia de Mendoza. M. hyopneumoniae pudo ser tipificado a partir de 27 muestras de lavado broncoalveolar (LBA) y se identificaron 8 diferentes MLVA-tipos. Este es el primer informe acerca de la diversidad genética de M. hyopneumoniae en Mendoza. Los resultados obtenidos permiten describir de manera más acabada la diversidad genética de este agente en nuestro país." ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1734 "Ancho" => 2083 "Tamanyo" => 148599 ] ] "descripcion" => array:1 [ "en" => "Dendrogram constructed with FAMD 1.20 software 15 using Dice similarity coefficient and unweighted pair group method with arithmetic means (UPGMA). Thirteen clusters (I to XIII) were identified at a similarity cutoff of 85%." ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "ID: identification.EP: enzootic pneumonia.BAL: bronchoalveolar lavage." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">ID herd \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Main characteristics \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">nPCR Positives/sampled (%) from BAL specimens \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Indoor, one-site, 120-sow, commercial farrow-to-finish farm located in Rivadavia. Vaccination against EP was practiced. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7/20 (35%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Indoor, one-site, 110-sow, commercial farrow-to-finish farm located in San Rafael. Vaccination against EP was practiced. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18/20 (90%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Indoor, one-site, 100-sow, commercial farrow-to-finish farm located in San Carlos. Vaccination against EP was practiced. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4/20 (20%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Indoor, one-site, 300-sow, commercial farrow-to-finish farm located in Guaymallén. Vaccination against EP was practiced. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13/20 (65%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">E \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Outdoor, one site, 300-sow, commercial farrow-to-finish farm located in General Alvear. No vaccination against EP was practiced. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6/20 (30%) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2120351.png" ] ] ] ] "descripcion" => array:1 [ "en" => "ID of the herds, kind of production system (indoor, outdoor), size (number of sows), localization and status of vaccination against EP. Number of PCR positives out of samples (percentage) for M. hyopneumoniae detection from BAL specimens, according to the herd" ] ] 2 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Herd \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Number of typed/positives to nPCR screening \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">MLVA types (VNTR P97 R1-P97 R1A-P146 R3) \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="3" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">A</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="3" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5/7 (71%)</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-4-14 (n=1) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-5-14 (n=1) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-4-16 (n=3) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11/18 (66%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-3-16 (n=11) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3/4 (75%)</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-4-16 (n=2) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-4-17 (n=1) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4/13 (30%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6-4-15 (n=4) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">E</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4/6 (50%)</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8-5-17 (n=3) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9-3-17 (n=1) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2120352.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Number of typed samples out of positives to nPCR screening samples (percentage) and MLVA types (number of tandem repeats for P97 R1, P97 R1A and P146 R3) according to the herd" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:23 [ 0 => array:3 [ "identificador" => "bib0120" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Applications of a nested-polymerase chain reaction assay to detect Mycoplasma hyopneumoniae from nasal swabs" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "M. 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Diversidad genética de Mycoplasma hyopneumoniae en la provincia de Mendoza

Camila Sosaa, Ariel Bloisb, Fernando Ibáñezc,d, Pablo Tamiozzoa,

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ptamiozzo@ayv.unrc.edu.ar

Corresponding author.

a Departamento de Patología Animal, Facultad de Agronomía y Veterinaria, Universidad Nacional de Río Cuarto, Córdoba, Argentina

b Dirección Provincial de Ganadería, Ministerio de Economía, Infraestructura y Energía, Gobierno de Mendoza, Mendoza, Argentina

c Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Córdoba, Argentina

d CONICET, Argentina

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    "titulo" => "Genetic diversity of <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> in Mendoza province"
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        "titulo" => "Diversidad gen&#233;tica de <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> en la provincia de Mendoza"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Dendrogram constructed with FAMD 1&#46;20 software 15 using Dice similarity coefficient and unweighted pair group method with arithmetic means &#40;UPGMA&#41;&#46; Thirteen clusters &#40;I to XIII&#41; were identified at a similarity cutoff of 85&#37;&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> is the primary agent involved in porcine enzootic pneumonia &#40;EP&#41; <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> infections are highly prevalent in almost all swine-producing areas&#44; causing significant economic losses to the pig industry worldwide<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">21</span></a>&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">In Argentina&#44; pig production is mainly concentrated in Santa Fe&#44; Buenos Aires and C&#243;rdoba&#46; provinces&#46; EP is highly prevalent both&#44; in indoor and outdoor systems in Argentina<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">5</span></a>&#46; However&#44; there is a lack of information about prevalence and other epidemiological aspects of EP in other provinces in which pig production is less developed&#44; as in Mendoza province&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Different genetic types of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> have been identified in herds from C&#243;rdoba&#44; Santa Fe and San Luis provinces<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">12&#44;18&#44;20</span></a>&#59; however they have never been reported in Mendoza&#46; Thus&#44; the objective of this study &#40;n&#61;100&#41; was to assess the genetic diversity of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> circulating in herds from the province of Mendoza&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Material and methods</span><p id="par0020" class="elsevierStylePara elsevierViewall">The study was performed according to the international guidelines of the Council for International Organizations of Medical Sciences &#40;CIOMS&#41;&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Herds and study design</span><p id="par0025" class="elsevierStylePara elsevierViewall">A cross-sectional study was carried out in an abattoir by collecting 20 broncho-alveolar lavage &#40;BAL&#41; specimens recovered from pigs from each of the five herds under study&#46; Herds were located in different districts of Mendoza province&#46; The main characteristics of the herds such as the kind of system and size &#40;number of sows&#41;&#44; among others are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Sample processing and M&#46; hyopneumoniae typing</span><p id="par0030" class="elsevierStylePara elsevierViewall">DNA from LBA specimens was extracted using DNAzol &#40;Thermo Fisher Scientific&#44; Argentina&#41; according to the manufacturer&#39;s instructions&#46; For <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> detection 100 samples were analyzed by a nested-PCR<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">1</span></a>&#44; considered as the screening technique&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">In order to type <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span>&#44; P97 R1&#44; P97 R1A and P146 R3 loci were analyzed only in those specimens that were positive &#40;48&#41; to the nPCR screening mentioned above&#46; Tandem repeat motives of P97 R1&#44; P97 R1A and P146 R3 were amplified by a nested PCR &#40;nPCR&#41; format previously described<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">13</span></a>&#46; After amplification&#44; amplicons were purified &#40;Puriprep-GP Kit&#44; Inbio Highway&#44; Argentina&#41;&#44; quantified and sequenced &#40;ABI 3130xl&#59; Applied Biosystems&#44; US&#41; using the primers reported by Vranckx et al&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">22</span></a>&#44; for P97 and by Mayor et al&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">9</span></a>&#44; for P146&#46; The number of tandem repeats was determined by analyzing the sequences with BioEdit 7&#46;1&#46;3&#46;0 software<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">7</span></a>&#46; For further analysis&#44; only those specimens which were positive for both loci were considered&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Data analysis</span><p id="par0040" class="elsevierStylePara elsevierViewall">A dendrogram based on the categorical values of the number of tandem repeats was constructed with the FAMD 1&#46;20 software<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">15</span></a> using the Dice similarity coefficient and the unweighted pair group method with arithmetic means &#40;UPGMA&#41;&#46; The number of tandem repeats from the 232&#44; J&#44; 7448&#44; PMS and 7422 reference <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> strains<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">3</span></a> was included&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The Simpson&#39;s index of diversity of the combined variable-number of tandem repeat &#40;VNTR&#41; regions &#40;P97 R1&#44; P97 R1A and P146 R3&#41; was calculated by using the Hunter-Gaston diversity index &#8211; HDGI<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">8</span></a>&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> was detected by nPCR in all the herds in 48&#37; &#40;48&#47;100&#41; of the specimens&#46; For P97&#44; 27 specimens were positive and could be further sequenced and typed&#46; Nested-PCR for P146 R3 showed more sensitivity&#44; amplifying all processed BAL specimens&#46; Thus&#44; 27&#47;48 &#40;56&#37;&#41; of the specimens could be typed for both loci&#46; The remaining specimens &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#41; could be typed only for P146 R3 and were not included in the analysis&#46; Eight MLVA types were identified&#58; 8-3-16 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>11&#41;&#44; all of them obtained from herd B&#44; 8-4-16 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41; from herds A and C&#44; 6-4-15 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41; from herd D&#44; 8-5-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41; from herd E&#44; and the less frequent types&#58; 8-4-14 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; 8-5-14 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; 8-4-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; 9-3-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; from herds A&#44; C and E&#44; respectively &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; The numbers of tandem repeats of the analyzed loci for <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> reference strains were&#58; 13-1-21 &#40;strain 232&#41;&#44; 9-3-18 &#40;strain J&#41;&#44; 10-4-44 &#40;strain 7448&#41;&#44; 15-1-19 &#40;strain PMS&#41; and 12-3-40 &#40;strain 7422&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">At a similarity cutoff of 85&#37;&#44; 13 clusters were observed &#8211; I to XIII &#8211; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Most local genotypes were more related to other local genotypes than to the reference strains&#44; with two exceptions &#40;reference strain 7448 and local variant 64&#41;&#46; Reference strain 7448 was more closely related to the local strains than to other reference strains&#46; On the other hand&#44; genetic variant 64 &#40;obtained from herd E&#41; was closely related to the reference strains than to the other native genotypes&#46; Only one genetic variant of the agent was found in herd B &#40;grouped into Cluster VII&#41;&#46; This genotype was exclusively found in this herd&#46; The same situation was observed in herd D &#40;one genetic variant exclusively found in this herd&#44; grouped into Cluster II&#41;&#46; In herd A&#44; three different genetic variants were observed&#44; grouped in Clusters IV&#44; V &#40;variants exclusively found in this herd&#41; and VIII &#40;together with genotypes found in herd C&#41;&#46; In herd C&#44; two different variants were found&#46; One genetic variant was exclusively found in this herd &#40;Cluster III&#41;&#46; The other variant corresponds to a genotype also found in herd A and grouped into Cluster VIII&#46; Two different genotypes were observed in herd E&#46; These genotypes were exclusively found in this herd and grouped into clusters VI and XI&#46; All reference strains clustered into different groups &#40;I&#44; IX&#44; X XII and XIII&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">The number of tandem repeats for each locus and their combination are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; Simpson&#39;s index of diversity was <span class="elsevierStyleItalic">D</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;789&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Discussion</span><p id="par0065" class="elsevierStylePara elsevierViewall">The circulation of different genetic types of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> in Mendoza province was demonstrated using a P97-P146 MLVA scheme&#46; Since no molecular marker has been able to discriminate between high and low virulence <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> strains&#44; knowing the circulation of the different genotypes is important for the development of control strategies against EP&#46; <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> genetic diversity has been reported around the world at regional and herd level&#44; between related and unrelated herds<a class="elsevierStyleCrossRefs" href="#bib0145"><span class="elsevierStyleSup">6&#44;9&#44;10&#44;14&#44;16&#44;17&#44;19</span></a>&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The 2-loci &#40;3-tandem repeat regions&#41; MLVA profiles detected in this study can only be compared to the profiles reported by few studies&#44; since neither these two loci were analyzed nor the number of repeat units present was determined in most reports&#46; In this regard&#44; some P97 R1 and P146 R3 MLVA types found here&#44; were similar to those reported by Dos Santos et al&#46; <span class="elsevierStyleSup">6</span>&#44; in specimens from US and Spain&#46; However&#44; they did not consider the P97 R1A region&#44; whose analysis increased the polymorphism&#46; In Argentina&#44; only one study used a similar MLVA Scheme<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">12</span></a>&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The discriminatory power was lower than the one reported by Dos Santos et al&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">6</span></a>&#44; mainly due to the number of processed specimens&#46; It is worth mentioning that if the R1A region of P97 had not been included into the analysis&#44; it would have obtained 5 MLVA types with a discriminatory power of 0&#46;62 &#40;data not shown&#41;&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Some studies reported the repeat number only for the P146 R3 motif&#44; and they found similar polyserine repeats in some European countries<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">9&#44;14</span></a>&#46; Moreover&#44; other studies reported the diversity of this gene&#44; and some of them included P97&#44; but did not determine the number of repeats<a class="elsevierStyleCrossRefs" href="#bib0125"><span class="elsevierStyleSup">2&#44;4&#44;10&#44;11&#44;22</span></a>&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">In Argentina there are previous reports about genetic diversity of this pathogen&#46; However&#44; none of the previous studies analyzed P97 R1<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleSup">&#44;20</span>&#46; With regard to P146 R3&#44; similar polyserine repeat motives were found in herds from Santa F&#233;&#44; C&#243;rdoba&#44; San Luis and in pigs from abroad<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">18</span></a>&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">From the dendrogram analysis&#44; it can be inferred that&#44; in general&#44; the genotypes from Mendoza province were more related to other native genotypes than to the reference strains&#46; This observation agrees with a previous study in which the genetic difference between local <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> types and bacterin strains was found<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">20</span></a>&#46; More in-depth studies are necessary to determine the implications of such differences&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Only one genetic variant of the pathogen was found in herd B&#44; being exclusive of this herd&#46; The same situation was observed in herd D&#46; These variants could represent well established <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> strains and adapted to the conditions found in these herds&#44; which agrees with previous results that showed persistence of mainly one distinct <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> type within animals of the same herd<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">23</span></a>&#46; However&#44; the circulation of other less frequent types of the agent into the farms cannot be excluded&#46; Different genetic variants were found in herds A&#44; C and E&#46; Such diversity observed in these herds could be explained by the access of different genetic types through replacement animals&#44; wild pigs&#44; personnel&#44; fomites or airborne transmission&#46; Regrettably&#44; this information was not taken into account in this study&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">As we previously proposed<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">12</span></a> and considering the difficulty in comparing the results from different studies&#44; we consider that the use of a standardized nomenclature for MLVA loci and alleles of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> is highly needed&#46; Furthermore&#44; the development of an online database including MLVA profiles for this pathogen would be of great help to share results within the scientific community&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">To the best of our knowledge&#44; this is the first report about diversity of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> in Mendoza province&#46; Results obtained in this work allow drawing a better picture of the genetic diversity of this pathogen in several provinces of Argentina&#46; This is important to understand some epidemiological aspects of EP and to develop strategies to control the disease&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Funding</span><p id="par0110" class="elsevierStylePara elsevierViewall">This study was financially supported in part by PICT 0442&#47;2015 FONCyT-ANPCyT-MinCyT&#44; Rep&#250;blica Argentina&#44; PPI 2016-2018&#44; 188&#47;2016-UNRC and Direcci&#243;n Provincial de Ganader&#237;a&#44; Ministerio de Econom&#237;a&#44; Infraestructura y Energ&#237;a&#44; Gobierno de Mendoza&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflict of interest</span><p id="par0115" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">In Argentina&#44; enzootic pneumonia &#40;EP&#41; is highly prevalent and different genetic types of <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> have been identified&#46; However&#44; there is a lack of information about prevalence and other epidemiological aspects of EP in Mendoza province&#46; A multiple Locus variable-number tandem repeat analysis &#40;MLVA&#41; targeting P97 R1&#44; P97 R1A and P146 R3 loci was used to assess the genetic diversity of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> from clinical specimens recovered from pigs from five herds located in different districts of Mendoza province&#46; <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> could be typed from 27 bronchoalveolar lavages &#40;BAL&#41; specimens&#44; and eight different MLVA types were identified&#46; This is the first report about diversity of <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> in Mendoza&#46; Results obtained in this work allow drawing a better picture of the genetic diversity of this pathogen in Argentina&#46;</p></span>"
      ]
      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">En Argentina&#44; la neumon&#237;a enzo&#243;tica porcina &#40;NEP&#41; es altamente prevalente y se han identificado diferentes tipos gen&#233;ticos de <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span>&#46; Sin embargo&#44; se carece de informaci&#243;n acerca de la prevalencia de NEP y de otros aspectos epidemiol&#243;gicos de esta entidad en la provincia de Mendoza&#46; En esta investigaci&#243;n se us&#243; un an&#225;lisis multilocus de regiones repetidas en t&#225;ndem &#40;MLVA&#41; de los <span class="elsevierStyleItalic">loci</span> P97 R1&#44; P97 R1A y P146 R3 para evaluar la diversidad gen&#233;tica de <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> a partir de muestras cl&#237;nicas de cerdos de cinco granjas localizadas en diferentes distritos de la provincia de Mendoza&#46; <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> pudo ser tipificado a partir de 27 muestras de lavado broncoalveolar &#40;LBA&#41; y se identificaron 8 diferentes MLVA-tipos&#46; Este es el primer informe acerca de la diversidad gen&#233;tica de <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> en Mendoza&#46; Los resultados obtenidos permiten describir de manera m&#225;s acabada la diversidad gen&#233;tica de este agente en nuestro pa&#237;s&#46;</p></span>"
      ]
    ]
    "multimedia" => array:3 [
      0 => array:7 [
        "identificador" => "fig0005"
        "etiqueta" => "Figure 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
            "Alto" => 1734
            "Ancho" => 2083
            "Tamanyo" => 148599
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Dendrogram constructed with FAMD 1&#46;20 software 15 using Dice similarity coefficient and unweighted pair group method with arithmetic means &#40;UPGMA&#41;&#46; Thirteen clusters &#40;I to XIII&#41; were identified at a similarity cutoff of 85&#37;&#46;</p>"
        ]
      ]
      1 => array:8 [
        "identificador" => "tbl0005"
        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at1"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:2 [
          "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">ID&#58; identification&#46;</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">EP&#58; enzootic pneumonia&#46;</p><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">BAL&#58; bronchoalveolar lavage&#46;</p>"
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">ID herd&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Main characteristics&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">nPCR Positives&#47;sampled &#40;&#37;&#41; from BAL specimens&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">A&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Indoor&#44; one-site&#44; 120-sow&#44; commercial farrow-to-finish farm located in Rivadavia&#46; Vaccination against EP was practiced&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7&#47;20 &#40;35&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Indoor&#44; one-site&#44; 110-sow&#44; commercial farrow-to-finish farm located in San Rafael&#46; Vaccination against EP was practiced&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">18&#47;20 &#40;90&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Indoor&#44; one-site&#44; 100-sow&#44; commercial farrow-to-finish farm located in San Carlos&#46; Vaccination against EP was practiced&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#47;20 &#40;20&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">D&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Indoor&#44; one-site&#44; 300-sow&#44; commercial farrow-to-finish farm located in Guaymall&#233;n&#46; Vaccination against EP was practiced&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">13&#47;20 &#40;65&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">E&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Outdoor&#44; one site&#44; 300-sow&#44; commercial farrow-to-finish farm located in General Alvear&#46; No vaccination against EP was practiced&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&#47;20 &#40;30&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab2120351.png"
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">ID of the herds&#44; kind of production system &#40;indoor&#44; outdoor&#41;&#44; size &#40;number of sows&#41;&#44; localization and status of vaccination against EP&#46; Number of PCR positives out of samples &#40;percentage&#41; for <span class="elsevierStyleItalic">M&#46; hyopneumoniae</span> detection from BAL specimens&#44; according to the herd</p>"
        ]
      ]
      2 => array:8 [
        "identificador" => "tbl0010"
        "etiqueta" => "Table 2"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at2"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Herd&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Number of typed&#47;positives to nPCR screening&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">MLVA types &#40;VNTR P97 R1-P97 R1A-P146 R3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="3" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">A</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="3" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5&#47;7 &#40;71&#37;&#41;</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-4-14 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-5-14 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-4-16 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">11&#47;18 &#40;66&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-3-16 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>11&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">C</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&#47;4 &#40;75&#37;&#41;</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-4-16 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-4-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">D&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#47;13 &#40;30&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6-4-15 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">E</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#47;6 &#40;50&#37;&#41;</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8-5-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9-3-17 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab2120352.png"
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        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Number of typed samples out of positives to nPCR screening samples &#40;percentage&#41; and MLVA types &#40;number of tandem repeats for P97 R1&#44; P97 R1A and P146 R3&#41; according to the herd</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:23 [
            0 => array:3 [
              "identificador" => "bib0120"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Applications of a nested-polymerase chain reaction assay to detect <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> from nasal swabs"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "M&#46; Calsamiglia"
                            1 => "C&#46; Pijoan"
                            2 => "A&#46; Trigo"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J Vet Diag Inv"
                        "fecha" => "1999"
                        "volumen" => "1"
                        "paginaInicial" => "246"
                        "paginaFinal" => "251"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0125"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Genetic diversity of <span class="elsevierStyleItalic">Mycoplasma hyopneumoniae</span> isolates of abattoir pigs"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:6 [
                            0 => "A&#46; Charlebois"
                            1 => "C&#46; Marois-Cr&#233;han"
                            2 => "P&#46; H&#233;lie"
                            3 => "C&#46;A&#46; Gagnon"
                            4 => "M&#46; Gottschalk"
                            5 => "M&#46; Archambault"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.vetmic.2013.11.006"
                      "Revista" => array:6 [
                        "tituloSerie" => "Vet Microbiol"
                        "fecha" => "2014"
                        "volumen" => "168"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2018.07.004

The statistics are updated each day

Year/Month	Html	Pdf	Total

2024 October	6	1	7
2024 September	22	6	28
2024 August	20	2	22
2024 July	14	4	18
2024 June	20	4	24
2024 May	15	5	20
2024 April	9	2	11
2024 March	43	3	46
2024 February	15	16	31
2024 January	21	8	29
2023 December	17	9	26
2023 November	21	7	28
2023 October	31	5	36
2023 September	31	2	33
2023 August	29	11	40
2023 July	22	3	25
2023 June	44	8	52
2023 May	73	9	82
2023 April	54	1	55
2023 March	38	5	43
2023 February	36	8	44
2023 January	24	10	34
2022 December	18	7	25
2022 November	30	13	43
2022 October	26	8	34
2022 September	35	16	51
2022 August	26	5	31
2022 July	27	22	49
2022 June	28	12	40
2022 May	30	11	41
2022 April	22	9	31
2022 March	29	15	44
2022 February	26	12	38
2022 January	33	10	43
2021 December	46	15	61
2021 November	47	8	55
2021 October	75	9	84
2021 September	50	22	72
2021 August	56	7	63
2021 July	30	13	43
2021 June	20	6	26
2021 May	21	7	28
2021 April	72	6	78
2021 March	30	12	42
2021 February	18	11	29
2021 January	13	8	21
2020 December	21	6	27
2020 November	12	5	17
2020 October	14	7	21
2020 September	18	7	25
2020 August	23	14	37
2020 July	28	13	41
2020 June	24	12	36
2020 May	10	5	15
2020 April	14	7	21
2020 March	27	6	33
2020 February	19	6	25
2020 January	12	7	19
2019 December	28	5	33
2019 November	41	13	54
2019 October	32	13	45
2019 September	23	20	43

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