Original article
Prevalence and antibiotic susceptibility of coagulase-negative Staphylococcus species from bovine subclinical mastitis in dairy herds in the central region of Argentina
Prevalencia y sensibilidad a antibióticos de especies de estafilococos coagulasa negativos provenientes de mastitis subclínica en bovinos de tambos de la región central de Argentina
Claudia G. Raspantia,
, Cesar C. Bonettob, Claudina Vissioc,d, Matías S. Pellegrinoa,d, Elina B. Reinosoa,d, Silvana A. Diesera,d, Cristina I. Bognia, Alejandro J. Larriestrac, Liliana M. Odiernoa
Corresponding author
a Departamento de Microbiología e Inmunología, Facultad de Ciencias Exactas,Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Ruta 36 km 601 (X5806JRA), Río Cuarto, Córdoba, Argentina
b Laboratorio de Diagnóstico Veterinario – Calidad de Leche – Nutrición Animal, CP 436 Parajón Ortiz (X5900KBJ), Villa María, Córdoba, Argentina
c Departamento de Patología Animal, Facultad de Agronomía y Medicina Veterinaria, Universidad Nacional de Río Cuarto, Ruta 36 km 601 (X5806JRA), Río Cuarto, Córdoba, Argentina
d Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
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(B) Electrophoresis on 1% agarose gel of the <span class="elsevierStyleItalic">hwp1</span> PCR using individual DNAs (from the DNA pool displayed in lane 3 – (A)). Lane M, 100<span class="elsevierStyleHsp" style=""></span>bp size marker. Lane 1, <span class="elsevierStyleItalic">C. albicans</span> control strain (ATCC 90028). Lane 2, <span class="elsevierStyleItalic">C. dubliniensis</span> control strain (NCPF 3949). Lane 3, <span class="elsevierStyleItalic">C. africana</span> (Strain LMDM 678). 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"apellidos" => "Odierno" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Departamento de Microbiología e Inmunología, Facultad de Ciencias Exactas,Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Ruta 36 km 601 (X5806JRA), Río Cuarto, Córdoba, Argentina" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Laboratorio de Diagnóstico Veterinario – Calidad de Leche – Nutrición Animal, CP 436 Parajón Ortiz (X5900KBJ), Villa María, Córdoba, Argentina" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Departamento de Patología Animal, Facultad de Agronomía y Medicina Veterinaria, Universidad Nacional de Río Cuarto, Ruta 36 km 601 (X5806JRA), Río Cuarto, Córdoba, Argentina" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina" "etiqueta" => "d" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Prevalencia y sensibilidad a antibióticos de especies de estafilococos coagulasa negativos provenientes de mastitis subclínica en bovinos de tambos de la región central de Argentina" ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Bovine mastitis is one of the most costly and complex diseases of the dairy industry<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">3,9</span></a>. The complexity is reflected in the numerous causative pathogens, the variety and magnitude of the physiological responses to these pathogens and the variation in efficacy of control measures for different causative organisms<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">4,7,17,18,23,32</span></a>. Coagulase-negative staphylococci (CNS) have been traditionally considered minor pathogens. However, their importance has increased because they have become the most frequently isolated group of species from bovine milk in many areas around the world<a class="elsevierStyleCrossRefs" href="#bib0275"><span class="elsevierStyleSup">16,29,33</span></a>. CNS usually cause subclinical mastitis (SCM), resulting in an increase in the somatic cell count (SCC) and a decrease in milk quality with the resulting economic losses that this implies<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">30</span></a>. The understanding and control of CNS mastitis are complicated by the heterogeneity of this group of bacteria. So far, based on Jean Euzéby's List of Procaryotic names with Standing in Nomenclature (<a id="intr0005" class="elsevierStyleInterRef" href="http://www.bacterio.net/s/staphylococcus.html">http://www.bacterio.net/s/staphylococcus.html</a>), the genus <span class="elsevierStyleItalic">Staphylococcus</span> contains 47 species and 24 subspecies. Even though, the prevalence of CNS species varies among the studies; six species have been reported to be commonly involved in intramammary infections (IMI)<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">20,30</span></a>. Recently, it has been found that CNS speciation based on the biochemical profile is not accurate enough for bovine CNS identification<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">26</span></a>. Hence, molecular methods have become an important diagnostic tool to improve CNS species differentiation<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">5,15,39</span></a>. CNS tend to be more resistant to antibiotics than <span class="elsevierStyleItalic">Staphylococcus aureus</span> and easily develop multiresistance<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">2,27,32</span></a>. In addition, limited information is available regarding differences in antimicrobial susceptibility among CNS species identified by genotyping<a class="elsevierStyleCrossRefs" href="#bib0330"><span class="elsevierStyleSup">27,38</span></a>. As yet, nothing has been reported about the prevalence and susceptibility antibiotics of CNS species of dairy cows in Argentina. Recently, a research conducted in our laboratory<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">8</span></a> showed that CNS represent the most prevalent bacterial group of minor pathogens isolated from the subclinical infection of dairy cows in Córdoba province, Argentina. The aim of the present study was to determine the prevalence and antibiotic resistance profiles of CNS species isolated from bovine subclinical mastitis in 51 dairy herds in the central region of Argentina.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Species identification of CNS isolates by PCR-RFLP analysis of a <span class="elsevierStyleItalic">groEL</span> gene sequence</span><p id="par0010" class="elsevierStylePara elsevierViewall">In this study, we included 219 (49.6%) CNS randomly selected isolates from a total of 441 isolates in pure cultures from composite milk samples with a SCC ≥200<span class="elsevierStyleHsp" style=""></span>000<span class="elsevierStyleHsp" style=""></span>cells/ml in a previous study<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">8</span></a>. The isolates were obtained from a previous cross-sectional study conducted on a sample randomly selected from 51 dairy farms located in Córdoba province, Argentina, with a herd size of around 100 and 250 cows<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">37</span></a>. The intramammary therapy of clinical cases was administered in 96.1% of the herds. Antibiotics used for dry cow therapy were applied to all cows in 58.8% of herds for at least one year. Among the milking hygienic practices, udder cleaning before milking was implemented in 94.1% of herds, whereas other practices such as using individual paper towels and, pre- and post-test dipping were not or were less frequently applied. On average, 45 lactating cows in each herd were sampled by the same investigator. In total, 2296 composite milk samples were collected. A volume of 0.01<span class="elsevierStyleHsp" style=""></span>ml of milk was streaked on trypticase soy agar plates (Sigma–Aldrich, USA) containing 5% sheep blood and incubated at 37<span class="elsevierStyleHsp" style=""></span>°C; plates were examined for growth at 24 and 48<span class="elsevierStyleHsp" style=""></span>h. A mammary gland was considered infected by CNS when growth of ≥500<span class="elsevierStyleHsp" style=""></span>CFU/ml of a particular organism and only one colony type on the plate were isolated<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">8</span></a>. Genomic DNA was extracted from all isolates and all type strains according to Aires-de-Sousa et al.<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">1</span></a>. PCR-RFLP analysis of a partial <span class="elsevierStyleItalic">groEL</span> gene sequence was performed as described by Santos et al.<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">25</span></a>. The CNS isolates were genotyped at species level as follows: (1) the presence of a DNA fragment (approximately 550<span class="elsevierStyleHsp" style=""></span>bp) obtained by PCR of the partial <span class="elsevierStyleItalic">groEL</span> gene sequence was identified, (2) the banding patterns obtained after digestion by <span class="elsevierStyleItalic">Alu</span>I restriction enzyme of the <span class="elsevierStyleItalic">groEL</span> gene of type strains were determined, (3) these patterns were compared with the known sequences from the NCBI GenBank database, using the NEB cutter program (version 2.0)<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">36</span></a>, (4) those CNS isolates with the same pattern of reference or type-T strains were assigned to a specific species. To differentiate <span class="elsevierStyleItalic">S. chromogenes</span> from <span class="elsevierStyleItalic">S. hyicus</span> and <span class="elsevierStyleItalic">S. capitis</span>, PCR products amplified from reference and type-T strains and/or IMI isolates were digested with <span class="elsevierStyleItalic">Hind</span>III and <span class="elsevierStyleItalic">Pvu</span>II<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">25</span></a>. The following reference and type-T strains were included in this study: <span class="elsevierStyleItalic">S. aureus</span> ATCC 29740, <span class="elsevierStyleItalic">S. capitis</span> subsp. <span class="elsevierStyleItalic">capitis</span> ATCC 35661, <span class="elsevierStyleItalic">S. caprae</span> ATCC 35538<span class="elsevierStyleSup">T</span>, <span class="elsevierStyleItalic">S. chromogenes</span> ATCC 43764<span class="elsevierStyleSup">T</span>, <span class="elsevierStyleItalic">S. epidermidis</span> ATCC 12228, <span class="elsevierStyleItalic">S. haemolyticus</span> ATCC 29970<span class="elsevierStyleSup">T</span>, <span class="elsevierStyleItalic">S. hyicus</span> ATCC 11249<span class="elsevierStyleSup">T</span>, <span class="elsevierStyleItalic">S. saprophyticus</span> ATCC 49453, <span class="elsevierStyleItalic">S. sciuri</span> subsp. <span class="elsevierStyleItalic">sciuri</span> ATCC 29060, <span class="elsevierStyleItalic">S. sciuri</span> subsp. <span class="elsevierStyleItalic">carnaticus</span> ATCC700058<span class="elsevierStyleSup">T</span>, <span class="elsevierStyleItalic">S. simulans</span> ATCC 11631, <span class="elsevierStyleItalic">S. warneri</span> ATCC 49454, <span class="elsevierStyleItalic">S. xylosus</span> ATCC 29971<span class="elsevierStyleSup">T</span>.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Antibiotic susceptibility testing</span><p id="par0015" class="elsevierStylePara elsevierViewall">The broth microdilution method was used to carry out <span class="elsevierStyleItalic">in vitro</span> antimicrobial susceptibility testing according to Clinical Laboratory Standards Institute guidelines (CLSI)<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">6</span></a> document M31-A3. Custom-made microtiter plate panels were used (Trek Diagnostic Systems, Magellan Biosciences, UK-USA) (Sensititre-TREK). The antimicrobial agents and dilution ranges tested for each agent were as follows: penicillin (0.06–8<span class="elsevierStyleHsp" style=""></span>μg/ml), oxacillin (0.25–4<span class="elsevierStyleHsp" style=""></span>μg/ml), erythromycin (0.25–4<span class="elsevierStyleHsp" style=""></span>μg/ml), tetracycline (2–16<span class="elsevierStyleHsp" style=""></span>μg/ml) and clindamycin (0.5–2<span class="elsevierStyleHsp" style=""></span>μg/ml). <span class="elsevierStyleItalic">S. aureus</span> strain ATCC 29213 was included in each assay as a control. The minimum inhibitory concentrations (MICs) results were evaluated based on veterinary interpretive criteria of the CLSI<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">6</span></a>, with resistance breakpoints of 0.25<span class="elsevierStyleHsp" style=""></span>μg/ml for penicillin, 0.5<span class="elsevierStyleHsp" style=""></span>μg/ml for oxacillin, 1<span class="elsevierStyleHsp" style=""></span>μg/ml for erythromycin and 8<span class="elsevierStyleHsp" style=""></span>μg/ml for tetracycline. Clindamycin is not licensed for the treatment of bovine mastitis; therefore, no approved breakpoints are available for the classification of bovine staphylococcal isolates from mastitis cases as susceptible or resistant. The MIC value required to inhibit 90% of the isolates tested was defined as MIC<span class="elsevierStyleInf">90</span>. Isolates were categorized as susceptible or resistant, with intermediates classified as resistant. Isolates with a MIC for oxacillin >0.5<span class="elsevierStyleHsp" style=""></span>μg/ml were additionally examined for the presence of the <span class="elsevierStyleItalic">mecA</span> gene by PCR as proposed by Mo and Wang<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">14</span></a>.</p></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Results</span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Distribution of CNS species</span><p id="par0020" class="elsevierStylePara elsevierViewall">Two hundred and nineteen CNS isolates from cows with SCM were identified to the species level by PCR-RFLP of the <span class="elsevierStyleItalic">groEL</span> gene. The distribution of different species among identified CNS is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>, where <span class="elsevierStyleItalic">S. chromogenes</span> and <span class="elsevierStyleItalic">S. haemolyticus</span> were the predominant species. A minimum of three different CNS species were present in 41.2% of the herds. <span class="elsevierStyleItalic">S. chromogenes</span> was isolated in 86.3% of all farms, whereas <span class="elsevierStyleItalic">S. haemolyticus</span> was isolated in 66.7% of them (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Antibiotic susceptibility</span><p id="par0025" class="elsevierStylePara elsevierViewall">In the present study 219 CNS isolated from cows with SCM and identified by genotyping were evaluated for susceptibility to five antimicrobials (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). Penicillin was used as the representative of penicillinase-labile penicillins and is the most frequently used in Argentina for bovine mastitis treatment. One hundred and thirteen strains (51.6%) of the 219 strains were resistant to penicillin; The MIC<span class="elsevierStyleInf">90</span> value for this antibiotic was higher than 8<span class="elsevierStyleHsp" style=""></span>μg/ml, well above the recommended breakpoint. Thirty (13.7%) of all CNS isolates tested were resistant to oxacillin; the MIC<span class="elsevierStyleInf">90</span> value for this antibiotic was 0.5<span class="elsevierStyleHsp" style=""></span>μg/ml. Resistance to oxacillin was attributed to the presence of the <span class="elsevierStyleItalic">mecA</span> gene in 2 of 12 (16.7%) of the oxacillin-resistant isolates with a MIC >0.5<span class="elsevierStyleHsp" style=""></span>μg/ml. Moderate resistance to erythromycin and tetracycline was detected among CNS isolates, 29.2% and 30.1%, respectively. In our study, the MIC<span class="elsevierStyleInf">90</span> values of erythromycin and tetracycline for CNS were more than one or two dilution steps higher than those of the recommended breakpoint, respectively. <a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a> shows phenotypic resistance profiles of CNS obtained from bovine SCM. Of 219 CNS isolates, 56 (25.6%) were phenotypically susceptible to all antimicrobial agents tested. Eighty-five (38.8%) isolates expressed resistance to a single compound, and 11 isolates (5%) expressed resistance to 2 related compounds (β-lactams antimicrobial agents) and 67 (30.6%) isolates expressed resistance to compounds belonging to different antimicrobial classes. In <span class="elsevierStyleItalic">S. chromogenes</span> and <span class="elsevierStyleItalic">S. haemolyticus</span>, the most prevalent isolated CNS species, a large proportion of the strains investigated were resistant to penicillin, 45.1% and 58.6%, respectively. Although resistance to oxacillin was lower than that found in other 2 resistant species to the same antibiotic, the number of isolates of these species was too low to draw conclusions. For <span class="elsevierStyleItalic">S. warneri</span>, the third most common CNS species, the proportion of resistant isolates to penicillin was less common than in other species and no resistance to oxacillin was observed. Finally, in <span class="elsevierStyleItalic">S. xylosus</span>, penicillin resistance was the most common among the species tested. For other species, <span class="elsevierStyleItalic">S. xylosus</span>, <span class="elsevierStyleItalic">S. epidermidis</span> and <span class="elsevierStyleItalic">S. hyicus</span>, the number of resistant isolates was too low to be analyzed. The percentage of resistant <span class="elsevierStyleItalic">S. haemolyticus</span> strains to two or more non-related antimicrobials was higher than that observed in <span class="elsevierStyleItalic">S. chromogenes</span>, 42.8% and 24.5%, respectively.</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Discussion</span><p id="par0030" class="elsevierStylePara elsevierViewall">Genotypic methods have shown to have higher specificity and sensitivity<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">39</span></a> than other methods for discriminating among species, resulting in a better alternative for the identification of CNS isolates. A number of PCR amplicon sequencing-based methods for the identification of CNS have been reported<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">5,26,30</span></a>. Amplified fragment length polymorphism (AFLP)<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">20,31</span></a> and PCR-restriction fragment length polymorphism (RFLP) applied to the <span class="elsevierStyleItalic">groEL</span> or <span class="elsevierStyleItalic">gap</span> genes have been used to identify CNS isolated from bovine milk<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">15,25</span></a>. The discrepancy observed in the distribution of CNS species identified by genotyping causing SCM in different countries, might be due to differences in experimental design<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">10,20,30,31,35,38</span></a> however, <span class="elsevierStyleItalic">S. chromogenes</span> was one of the most prevalent species both in this work and in previous studies carried out in other countries such as Finland, Sweden, Belgium, Canada and Brazil, ranging between 23.3% and 78.8% of CNS isolates. To our knowledge, only Piessens <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">20</span></a> revealed that <span class="elsevierStyleItalic">S. haemolyticus</span> was the second most prevalent CNS species as in our study causing 27.6% of cases. Special attention should be given to both species, considering that the udder was found to be their main reservoir<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">20</span></a>.</p><p id="par0035" class="elsevierStylePara elsevierViewall">In our study, a minimum of three different species of CNS were present in 41.2% of the herds. <span class="elsevierStyleItalic">S. chromogenes</span> and <span class="elsevierStyleItalic">S. haemolyticus</span> were isolated in most of the farms. This is in line with other studies, where these species have been isolated from all analyzed herds<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">20,30</span></a>. Although the reasons for the increased prevalence of some CNS species are not known, these might be attributed to the ability of each species to adapt to the mammary gland<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">10,20</span></a> or to the different management patterns of mastitis control schemes<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">30</span></a>.</p><p id="par0040" class="elsevierStylePara elsevierViewall">One limitation to the present study is the fact that we cannot be sure that the CNS were isolated from the diseased quarter since other non-infectious factors could cause an inflammatory response. However, CNS in pure culture allow to ensure that they are the only etiological agents causing subclinical mastitis.</p><p id="par0045" class="elsevierStylePara elsevierViewall">The direct comparison of studies on antimicrobial susceptibility of CNS is often difficult mainly because of the use of different methodologies and breakpoints for testing susceptibility. A great variability has been reported in the MIC<span class="elsevierStyleInf">90</span> values for penicillin in CNS, ranging from 0.12<span class="elsevierStyleHsp" style=""></span>μg/ml to 32<span class="elsevierStyleHsp" style=""></span>μg/ml<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">2,11,12,19,22,24,34</span></a>. The MIC<span class="elsevierStyleInf">90</span> value for penicillin found in our study was well above the recommended breakpoint (CLSI, 2008). Moreover, the penicillin resistance percentage was higher than that described by Gentilini <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">11</span></a> in Argentina and those reported in other countries such as Uruguay<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">12</span></a>, The Netherlands<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">27</span></a>, USA<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">22</span></a> and Sweden<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">2</span></a>. In the last decade, Gentilini <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">11</span></a> reported methicillin resistance among CNS isolated from bovine mastitis in our country. Since continuous surveillance is needed for the early detection of this kind of resistance, oxacillin has been used in this study to test susceptibility to methicillin. The MIC<span class="elsevierStyleInf">90</span> value for oxacillin was similar to those reported by different authors<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">11–13,24,28</span></a>. The percentage of resistant strains found was higher than that reported by other authors<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">2,11–13</span></a>, and similar to that reported in studies from Finland, Germany, USA, Sweden and The Netherlands<a class="elsevierStyleCrossRefs" href="#bib0290"><span class="elsevierStyleSup">19,21,22,27,28</span></a>. The variability in the MIC<span class="elsevierStyleInf">90</span> values of the antimicrobial activity of penicillin and oxacillin against CNS highlights the relevance of determining β-lactams susceptibility patterns for this bacterial group. Macrolides are frequently used in Argentina for bovine mastitis treatment, since high concentrations in milk are obtained following parenteral administration. Although erythromycin was evaluated as representative of this group, tylosin is used in the therapy. Tetracycline was included in this study for epidemiological purposes as representative of tetracyclines; however, they are not recommended for mastitis treatment in Argentina because of the risk of an extended residue presence in milk. The MIC<span class="elsevierStyleInf">90</span> value for erythromycin and tetracycline was higher than that observed by several authors in Argentina, Finland, Germany, Sweden and USA<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">2,11,13,19,21,28</span></a>. Although clindamycin is not used in the treatment of bovine mastitis, the determination of the MIC for this antibiotic was conducted in order to test susceptibility to lincomycin; however, specific interpretative breakpoints are defined for pirlimicyn<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">6</span></a>. Susceptibility to pirlimycin could not be inferred from clindamycin results because some mechanism (enzymatic modification) does not exhibit cross-resistance. The MIC<span class="elsevierStyleInf">90</span> value for clindamycin obtained in this study was similar to that previously described by Gentilini <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">11</span></a> in our country and higher than that reported by other investigators in different countries<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">2,13,19,21</span></a>. The proportion of CNS resistant to a single compound or two related compounds obtained in our study was found to be similar to that described by Sampimon <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">27</span></a><span class="elsevierStyleItalic">S</span>. <span class="elsevierStyleItalic">haemolyticus</span> and <span class="elsevierStyleItalic">S. chromogenes</span> were the most frequent resistant species; therefore, it would also be hypothesized that they should be more “at risk” of developing antibiotic resistance or acquiring resistance determinants. Conversely, the absence or lower percentages of resistant isolates to multiple drugs for both species were found by Sampimon <span class="elsevierStyleItalic">et al.</span><a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">27</span></a> We conclude that CNS species from bovine subclinical mastitis differ in prevalence and antimicrobial resistance profiles, which may have implications for treatment and management decisions when CNS are the predominant bacterial group on dairy farms.</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Ethical disclosures</span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Protection of human and animal subjects</span><p id="par0050" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study.</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Confidentiality of data</span><p id="par0055" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article.</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Right to privacy and informed consent</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article.</p></span></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflict of interest</span><p id="par0065" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres620821" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec635104" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres620820" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec635105" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Species identification of CNS isolates by PCR-RFLP analysis of a groEL gene sequence" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Antibiotic susceptibility testing" ] ] ] 6 => array:3 [ "identificador" => "sec0025" "titulo" => "Results" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Distribution of CNS species" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Antibiotic susceptibility" ] ] ] 7 => array:2 [ "identificador" => "sec0040" "titulo" => "Discussion" ] 8 => array:3 [ "identificador" => "sec0045" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0050" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0055" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0060" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0065" "titulo" => "Conflict of interest" ] 10 => array:2 [ "identificador" => "xack209306" "titulo" => "Acknowledgements" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-05-27" "fechaAceptado" => "2015-12-03" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec635104" "palabras" => array:4 [ 0 => "Subclinical mastitis" 1 => "Bovines" 2 => "Coagulase-negative staphylococci species" 3 => "Antimicrobial resistance" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec635105" "palabras" => array:4 [ 0 => "Mastitis subclínica" 1 => "Bovinos" 2 => "Especies de estafilococos coagulasa negativos" 3 => "Resistencia a antimicrobianos" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Coagulase-negative staphylococci (CNS) are a common cause of bovine subclinical mastitis (SCM). The prevalence of CNS species causing SCM identified by genotyping varies among countries. Overall, the antimicrobial resistance in this group of organisms is increasing worldwide; however, little information exists about a CNS species resistant to antibiotics. The aim of the present study was to genotypically characterize CNS at species level and to determine the prevalence and antibiotic resistance profiles of CNS species isolated from bovine SCM in 51 dairy herds located in the central region of the province of Cordoba, Argentina. In this study, we identified 219 CNS isolates at species level by PCR-restriction fragment length polymorphism of the <span class="elsevierStyleItalic">groEL</span> gene. <span class="elsevierStyleItalic">Staphylococcus chromogenes</span> (46.6%) and <span class="elsevierStyleItalic">Staphylococcus haemolyticus</span> (32%) were the most prevalent species. A minimum of three different CNS species were present in 41.2% of the herds. <span class="elsevierStyleItalic">S. chromogenes</span> was isolated from most of the herds (86.3%), whereas <span class="elsevierStyleItalic">S. haemolyticus</span> was isolated from 66.7% of them. The broth microdilution method was used to test <span class="elsevierStyleItalic">in vitro</span> antimicrobial susceptibility. Resistance to a single compound or two related compounds was expressed in 43.8% of the isolates. <span class="elsevierStyleItalic">S. chromogenes</span> and <span class="elsevierStyleItalic">S. haemolyticus</span> showed a very high proportion of isolates resistant to penicillin. Resistance to two or more non-related antimicrobials was found in 30.6% of all CNS. <span class="elsevierStyleItalic">S. haemolyticus</span> exhibited a higher frequency of resistance to two or more non-related antimicrobials than <span class="elsevierStyleItalic">S. chromogenes</span>.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Los estafilococos coagulasa negativos (ECN) son una causa frecuente de mastitis subclínica (MSC) en bovinos. La prevalencia de especies de ECN causantes de MSC identificadas por métodos genotípicos varía entre países. La resistencia antimicrobiana en este grupo de organismos se está incrementando en el mundo; sin embargo, existe poca información acerca de las especies de ECN resistentes a antibióticos. Los objetivos del presente estudio fueron caracterizar genotípicamente los ECN a nivel de especie y determinar la prevalencia y los perfiles de resistencia a antibióticos de las especies de ECN aisladas de MSC en bovinos de 51 rodeos situados en la provincia de Córdoba, Argentina. Mediante polimorfismos de los fragmentos de restricción del gen <span class="elsevierStyleItalic">groEL</span> identificamos 219 aislamientos de ECN a nivel de especie. <span class="elsevierStyleItalic">Staphylococcus chromogenes</span> (46,6%) y <span class="elsevierStyleItalic">Staphylococcus haemolyticus</span> (32%) fueron las especies más prevalentes. Un mínimo de 3 especies diferentes de ECN estuvieron presentes en el 41,2% de los tambos. <span class="elsevierStyleItalic">S. chromogenes</span> fue aislado en la mayoría de los tambos (86,3%), mientras que <span class="elsevierStyleItalic">S. haemolyticus</span> fue aislado en el 66,7% de aquellos. Para el análisis de sensibilidad a los antimicrobianos <span class="elsevierStyleItalic">in vitro</span> se usó el método de microdilución en caldo. La resistencia a un único compuesto o a 2 compuestos relacionados fue expresada en el 43,8% de los aislamientos. <span class="elsevierStyleItalic">S. chromogenes</span> y <span class="elsevierStyleItalic">S. haemolyticus</span> mostraron una muy elevada proporción de aislamientos resistentes a penicilina. La resistencia a 2 o más antimicrobianos no relacionados fue hallada en el 30,6% de los ECN. <span class="elsevierStyleItalic">S. haemolyticus</span> exhibió una frecuencia de resistencia a 2 o más antimicrobianos no relacionados más elevada que <span class="elsevierStyleItalic">S. chromogenes</span>.</p></span>" ] ] "multimedia" => array:3 [ 0 => 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 [ "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="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Species \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">No. of isolates<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">CNS IMI<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a> (%) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">No. of herds<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Distribution of each CNS species in dairy herds sampled (%) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus chromogenes</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">102 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">46.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">44 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">86.3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus haemolyticus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">70 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">32.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">34 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">66.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus warneri</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">16 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">27.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus xylosus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21.6 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus simulans</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus epidermidis</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.8 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus hyicus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.8 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="5" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Total \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">219 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">51 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1017884.png" ] ] ] "notaPie" => array:3 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Each organisms was isolated from only one cow (composite sample).</p>" ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">IMI: intramammary infections.</p>" ] 2 => array:3 [ "identificador" => "tblfn0015" "etiqueta" => "c" "nota" => "<p class="elsevierStyleNotepara" id="npar0015">Number of dairy herds from which each species was isolated.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Species distribution of coagulase-negative staphylococci (CNS) isolates from bovine subclinical mastitis in 51 Argentinean dairy herds</p>" ] ] 1 => 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:2 [ "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">White fields denote the range of dilutions tested for each substance. MICs above the range are given as the concentration closest to the range. MICs equal to or lower than the lowest concentration tested are given as the lowest tested concentration. Bold vertical lines indicate breakpoints based on veterinary interpretive criteria (CLSI 2008). Numbers in brackets indicate the number of isolates with a MIC in the intermediate resistant range.</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleSup">a</span> Clindamycin is not licensed for the treatment of bovine mastitis. As a consequence, no approved breakpoints are available for the classification of bovine staphylococcal isolates from mastitis cases as susceptible or resistant; NA, not applicable.</p>" "tablatextoimagen" => array:1 [ 0 => array:1 [ "tablaImagen" => array:1 [ 0 => array:4 [ "imagenFichero" => "fx1.jpeg" "imagenAlto" => 1123 "imagenAncho" => 3417 "imagenTamanyo" => 214343 ] ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Proportion of resistant isolates and minimum inhibitory concentration (MIC) distribution for 219 isolated coagulase-negative staphylococci (CNS) from bovine subclinical mastitis</p>" ] ] 2 => array:7 [ "identificador" => "tbl0015" "etiqueta" => "Table 3" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Species \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col">Total \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="10" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Phenotypic resistance to antibiotics<a class="elsevierStyleCrossRef" href="#tblfn0020"><span class="elsevierStyleSup">a</span></a></th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col">0 \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">1</th><th class="td" title="table-head " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">2</th><th class="td" title="table-head " align="left" valign="top" scope="col">>2 \t\t\t\t\t\t\n \t\t\t\t</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">P \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">O \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">E \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">T \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PO \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PT \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PE \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">ET \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus chromogenes</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">102 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">3 POT, 3 POE, 6 PET \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus haemolyticus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">70 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5 POE, 7 PET \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus warneri</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">16 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">1 PET \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus xylosus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">1 POT, 2 POE, 2 PET \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus simulans</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus epidermidis</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2 POT \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus hyicus</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="12" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Total \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">219 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">39 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">32 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1017883.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0020" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0020">When phenotypic resistance to 0, 1 or 2 compounds was observed, the number of isolates with the specified resistance profile is shown. For isolates with resistance to >2 tested compounds, resistance profiles are shown. E: erythromycin; O: oxacillin; P: penicillin; T: tetracycline.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Phenotypic resistance profiles of coagulase-negative staphylococci (CNS) obtained from bovine subclinical mastitis</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:39 [ 0 => array:3 [ "identificador" => "bib0200" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Characterization of <span class="elsevierStyleItalic">Staphylococcus aureus</span> isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro State, Brazil" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "M. 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Dieser is a recipient of a posdoctoral fellowship from CONICET.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/03257541/0000004800000001/v1_201603250025/S0325754115001662/v1_201603250025/en/main.assets" "Apartado" => array:4 [ "identificador" => "44540" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Agentes antimicrobianos" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/03257541/0000004800000001/v1_201603250025/S0325754115001662/v1_201603250025/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754115001662?idApp=UINPBA00004N" ]
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| 2024 May | 49 | 5 | 54 |
| 2024 April | 67 | 6 | 73 |
| 2024 March | 68 | 9 | 77 |
| 2024 February | 71 | 9 | 80 |
| 2024 January | 61 | 9 | 70 |
| 2023 December | 63 | 17 | 80 |
| 2023 November | 65 | 13 | 78 |
| 2023 October | 98 | 10 | 108 |
| 2023 September | 75 | 11 | 86 |
| 2023 August | 47 | 2 | 49 |
| 2023 July | 32 | 4 | 36 |
| 2023 June | 42 | 9 | 51 |
| 2023 May | 58 | 2 | 60 |
| 2023 April | 57 | 21 | 78 |
| 2023 March | 30 | 6 | 36 |
| 2023 February | 44 | 6 | 50 |
| 2023 January | 26 | 8 | 34 |
| 2022 December | 28 | 11 | 39 |
| 2022 November | 29 | 21 | 50 |
| 2022 October | 21 | 11 | 32 |
| 2022 September | 38 | 9 | 47 |
| 2022 August | 31 | 16 | 47 |
| 2022 July | 35 | 15 | 50 |
| 2022 June | 22 | 10 | 32 |
| 2022 May | 28 | 15 | 43 |
| 2022 April | 29 | 18 | 47 |
| 2022 March | 33 | 17 | 50 |
| 2022 February | 40 | 12 | 52 |
| 2022 January | 40 | 11 | 51 |
| 2021 December | 35 | 17 | 52 |
| 2021 November | 65 | 15 | 80 |
| 2021 October | 45 | 15 | 60 |
| 2021 September | 51 | 19 | 70 |
| 2021 August | 23 | 7 | 30 |
| 2021 July | 28 | 9 | 37 |
| 2021 June | 13 | 9 | 22 |
| 2021 May | 23 | 10 | 33 |
| 2021 April | 47 | 19 | 66 |
| 2021 March | 26 | 9 | 35 |
| 2021 February | 24 | 11 | 35 |
| 2021 January | 17 | 12 | 29 |
| 2020 December | 17 | 8 | 25 |
| 2020 November | 30 | 10 | 40 |
| 2020 October | 22 | 10 | 32 |
| 2020 September | 20 | 12 | 32 |
| 2020 August | 23 | 17 | 40 |
| 2020 July | 34 | 7 | 41 |
| 2020 June | 29 | 13 | 42 |
| 2020 May | 51 | 11 | 62 |
| 2020 April | 14 | 12 | 26 |
| 2020 March | 34 | 18 | 52 |
| 2020 February | 27 | 15 | 42 |
| 2020 January | 27 | 9 | 36 |
| 2019 December | 25 | 10 | 35 |
| 2019 November | 25 | 7 | 32 |
| 2019 October | 31 | 4 | 35 |
| 2019 September | 44 | 5 | 49 |
| 2019 August | 18 | 2 | 20 |
| 2019 July | 41 | 12 | 53 |
| 2019 June | 49 | 23 | 72 |
| 2019 May | 97 | 82 | 179 |
| 2019 April | 58 | 26 | 84 |
| 2019 March | 15 | 6 | 21 |
| 2019 February | 19 | 12 | 31 |
| 2019 January | 13 | 7 | 20 |
| 2018 December | 10 | 3 | 13 |
| 2018 November | 17 | 7 | 24 |
| 2018 October | 34 | 17 | 51 |
| 2018 September | 12 | 5 | 17 |
| 2018 August | 10 | 19 | 29 |
| 2018 July | 11 | 6 | 17 |
| 2018 June | 16 | 1 | 17 |
| 2018 May | 19 | 7 | 26 |
| 2018 April | 22 | 12 | 34 |
| 2018 March | 8 | 10 | 18 |
| 2018 February | 14 | 7 | 21 |
| 2018 January | 19 | 4 | 23 |
| 2017 December | 12 | 6 | 18 |
| 2017 November | 23 | 8 | 31 |
| 2017 October | 9 | 6 | 15 |
| 2017 September | 16 | 14 | 30 |
| 2017 August | 15 | 6 | 21 |
| 2017 July | 17 | 4 | 21 |
| 2017 June | 23 | 18 | 41 |
| 2017 May | 28 | 11 | 39 |
| 2017 April | 26 | 10 | 36 |
| 2017 March | 34 | 58 | 92 |
| 2017 February | 19 | 13 | 32 |
| 2017 January | 22 | 11 | 33 |
| 2016 December | 21 | 7 | 28 |
| 2016 November | 28 | 6 | 34 |
| 2016 October | 38 | 17 | 55 |
| 2016 September | 38 | 14 | 52 |
| 2016 August | 48 | 22 | 70 |
| 2016 July | 53 | 14 | 67 |
| 2016 June | 60 | 53 | 113 |
| 2016 May | 52 | 43 | 95 |
| 2016 April | 35 | 30 | 65 |
| 2016 March | 5 | 3 | 8 |
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