Scientific letter
Emergence of multidrug-resistant Haemophilus parainfluenzae in genital specimens: Importance of culture and antimicrobial susceptibility surveillance
Emergencia de Haemophilus parainfluenzae multiresistente en muestras genitales: importancia del cultivo y vigilancia de sensibilidad antimicrobiana
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Eugenia Portillo Bordonabe, Alberto Gil Setas, Carmen Ezpeleta Baquedano" "autores" => array:4 [ 0 => array:4 [ "nombre" => "Irati" "apellidos" => "Arregui Garcia" "email" => array:1 [ 0 => "iratiarreguig@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "M. Eugenia" "apellidos" => "Portillo Bordonabe" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Alberto" "apellidos" => "Gil Setas" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Carmen" "apellidos" => "Ezpeleta Baquedano" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Microbiología Clínica, Hospital Universitario de Navarra, Pamplona, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Instituto de Investigación Sanitaria de Navarra (IdisNA), Pamplona, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Emergencia de <span class="elsevierStyleItalic">Haemophilus parainfluenzae</span> multiresistente en muestras genitales: importancia del cultivo y vigilancia de sensibilidad antimicrobiana" ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Haemophilus parainfluenzae</span> is a Gram-negative coccobacillus of the microbiota of the upper respiratory tract. Evidence has recently been found of its role as a pathogen causing non-gonococcal urethritis (NGU), although the pathogenicity is difficult to assess, as it can also be isolated in asymptomatic patients or along with other pathogens.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,2</span></a> The emergence of multidrug resistant (MDR) strains of <span class="elsevierStyleItalic">H. parainfluenzae</span> has recently been documented in different countries in Europe.<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3–6</span></a> As the empirical treatment for urethritis is a third-generation cephalosporin with or without a macrolide, these drugs would not be effective against MDR <span class="elsevierStyleItalic">H. parainfluenzae</span>.</p><p id="par0010" class="elsevierStylePara elsevierViewall">We present the isolates of <span class="elsevierStyleItalic">H. parainfluenzae</span> obtained from genital samples analysed at Hospital Universitario de Navarra from 2016 to March 2022.</p><p id="par0015" class="elsevierStylePara elsevierViewall">The isolates were identified using MALDI-TOF (Bruker Daltonik, Germany) and the antibiogram was performed using the disc-plate method on Haemophilus Test Medium agar (Becton Dickinson, United States) with 24<span class="elsevierStyleHsp" style=""></span>h incubation at 37°C in an atmosphere with 5% of CO<span class="elsevierStyleInf">2</span>, studying the sensitivity to ampicillin, amoxicillin/clavulanic acid, cefuroxime, cefotaxime, nalidixic acid, ciprofloxacin and cotrimoxazole. We followed the cut-off points established by EUCAST in 2021.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Beta-lactamase activity was studied using a nitrocefin disc (cefinase, BD, USA) and/or molecular detection of TEM/ROB enzymes. An MDR strain was defined as resistant to three or more classes of antibiotics.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">During the study period, 443 isolates of <span class="elsevierStyleItalic">H. parainfluenzae</span> were obtained from genital samples, with or without clinical significance. The mean age of the patients was 34 years (SD: 13 years), and 345 (77.8%) were male.</p><p id="par0025" class="elsevierStylePara elsevierViewall">In the susceptibility study, 13 (2.2%) MDR strains were identified, all in males with a mean age of 32 (SD: 5 years). <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> shows how MDR <span class="elsevierStyleItalic">H. parainfluenzae</span> has evolved in Navarra.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">We found a significant increase in resistance, from not isolating any resistant strains to having 18% MDR strains in seven years. All MDR <span class="elsevierStyleItalic">H. parainfluenzae</span> strains were resistant to ampicillin, amoxicillin/clavulanic acid and cefuroxime. One strain also showed resistance to quinolones, five strains to cotrimoxazole, and five were resistant to all the antibiotics studied. Two types of resistance mechanisms to beta-lactams have been described in this genus: a) enzymatic hydrolysis by TEM-type beta-lactamases, or less frequently ROB-types, a phenotype known as beta-lactamase-positive ampicillin-resistant (BLPAR); and b) resistance due to modifications in penicillin-binding proteins (PBP), beta-lactamase-negative ampicillin-resistant (BLNAR) phenotype.<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3,9</span></a> In addition, the two mechanisms can coexist in the same strain, also decreasing susceptibility to amoxicillin/clavulanic acid and second-generation cephalosporins. Strains with double resistance mechanism can be detected by positive cefinase test and amoxicillin/clavulanic acid halo diameter ≤12<span class="elsevierStyleHsp" style=""></span>mm.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> In our study, the resistance to beta-lactams of MDR <span class="elsevierStyleItalic">H. parainfluenzae</span> was due in 58.3% to alteration of PBP plus beta-lactamases (66.7% of the cases due to production of TEM) and in 41.7% to PBP alteration only.</p><p id="par0035" class="elsevierStylePara elsevierViewall">In conclusion, as has been reported elsewhere, we have found that in our hospital there has been an increase in MDR <span class="elsevierStyleItalic">H. parainfluenzae</span> in genital samples in recent years, mainly in males aged 30–40.<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4–6</span></a> This increase may be due to the increase in the number of genital samples taken following the opening of the sexually transmitted infection clinic in our department, and the fact that the microorganism is actively looked for in cultures, identifying it and performing a susceptibility study for proper surveillance.</p><p id="par0040" class="elsevierStylePara elsevierViewall">The potential role of <span class="elsevierStyleItalic">H. parainfluenzae</span> in urethritis needs to be taken into account, as empirical treatment in monotherapy with ceftriaxone might not be effective against MDR isolates. Therefore, when a patient has symptoms consistent with urethritis, in addition to starting empirical antibiotic therapy, we have to take samples for culture, identify <span class="elsevierStyleItalic">H. parainfluenzae</span> as the probable cause of NGU and determine the susceptibility profile, in order to closely monitor the emergence of resistant <span class="elsevierStyleItalic">H. parainfluenzae</span> isolates.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "multimedia" => array:1 [ 0 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:1 [ "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">Year \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Total number of isolates \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">MDR isolates \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Percentage of MDR isolates (%) \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">2016 \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">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">0 \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">0 \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">2017 \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">79 \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">1 \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">1.3 \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">2018 \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">84 \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">1 \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">1.2 \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">2019 \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">92 \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">3 \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">3.7 \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">2020 \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">65 \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">0 \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">0 \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">2021 \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">41 \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">5 \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">12.2 \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">First quarter 2022 \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">16 \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">3 \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">18.8 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Number of <span class="elsevierStyleItalic">H. parainfluenzae</span> isolates and MDR strains from genital samples per year of study.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:9 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "<span class="elsevierStyleItalic">Haemophilus parainfluenzae</span> urethritis among homosexual men" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "H. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 6 | 0 | 6 |
| 2024 October | 32 | 11 | 43 |
| 2024 September | 34 | 12 | 46 |
| 2024 August | 27 | 12 | 39 |
| 2024 July | 29 | 8 | 37 |
| 2024 June | 14 | 3 | 17 |
| 2024 May | 16 | 1 | 17 |
| 2024 April | 16 | 64 | 80 |
| 2024 March | 30 | 6 | 36 |
| 2024 February | 27 | 2 | 29 |
| 2024 January | 36 | 4 | 40 |
| 2023 December | 15 | 2 | 17 |
| 2023 November | 11 | 1 | 12 |
| 2023 October | 4 | 2 | 6 |
| 2023 September | 1 | 1 | 2 |
| 2023 June | 2 | 2 | 4 |
| 2023 April | 11 | 0 | 11 |
| 2023 March | 0 | 5 | 5 |
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