Case and Research Letters
Interaction between Pseudomonas aeruginosa and Dermatophyte Fungi: Repercussions on the Clinical Course and Microbiological Diagnosis of Tinea Pedis
Interacción de Pseudomonas aeruginosa y hongos dermatofitos: repercusión en el curso clínico y en el diagnóstico microbiológico de la tinea pedis
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Aspiroz, C. Toyas, P. Robres, Y. Gilaberte" "autores" => array:4 [ 0 => array:3 [ "nombre" => "C." "apellidos" => "Aspiroz" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "C." "apellidos" => "Toyas" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "P." "apellidos" => "Robres" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 3 => array:4 [ "nombre" => "Y." "apellidos" => "Gilaberte" "email" => array:2 [ 0 => "ygilaberte@salud.aragon.es" 1 => "ygilaberte@gmail.com" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Servicio de Microbiología, Hospital Royo Villanova, Zaragoza, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Servicio de Medicina Interna, Hospital Royo Villanova, Zaragoza, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Servicio de Dermatología, Hospital San Jorge, Huesca, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Instituto Aragonés de Ciencias de la Salud, Zaragoza, Spain" "etiqueta" => "d" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Interacción de <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> y hongos dermatofitos: repercusión en el curso clínico y en el diagnóstico microbiológico de la <span class="elsevierStyleItalic">tinea pedis</span>" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 750 "Ancho" => 1000 "Tamanyo" => 143111 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Intense erythema and maceration, with peripheral peeling in the fourth interdigital space.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Simultaneous skin infection by <span class="elsevierStyleItalic">Pseudomonas</span> and fungi is underdiagnosed. In the context of a complex case of this pathology, we reflect on the interaction between these 2 infectious agents, the mutual influences they exert, and how this circumstance can affect the clinical course and microbiological diagnosis.</p><p id="par0010" class="elsevierStylePara elsevierViewall">We present the case of a 55<span class="elsevierStyleHsp" style=""></span>-year-old man who consulted for cellulitis of the right lower limb with marked systemic repercussions, requiring hospital admission. Physical examination revealed intense erythema of both feet, with desquamation and exudation, particularly in the lateral interdigital spaces, compatible with tinea pedis (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>), and subungual hyperkeratosis of the nail of the great toes of both feet. Wood light did not elicit fluorescence, allowing us to exclude erythrasma.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a></p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">Routine laboratory tests and a basic study of immunity were normal. Samples taken for microbiology repeatedly grew <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> and other gram-negative bacilli that varied in the different cultures performed (<span class="elsevierStyleItalic">Proteus mirabilis, Escherichia coli</span>, and <span class="elsevierStyleItalic">Morganella morganii</span>). Direct examination of both nails with potassium hydroxide (KOH) showed distorted hyphae, but dermatophytes were not isolated in any of the specific cultures for fungi of the sole of the foot and affected nails. Based on the antibiogram, the patient received treatment with ciprofloxacin for 10 days, leading to an improvement and hospital discharge. During follow-up, the clinical suspicion of interdigital tinea pedis increased, though dermatophytes were not isolated in any of the 3 cultures performed, which always included samples from the sole of the foot and the affected nails. In a fourth culture, performed after complete disappearance of <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span>, the sample from the fourth interdigital space showed growth of <span class="elsevierStyleItalic">Trichopyton rubrum</span> and abundant yeasts (<span class="elsevierStyleItalic">Candida albicans</span> and <span class="elsevierStyleItalic">Candida guilliermondii</span>) were also isolated. The patient was treated with terbinafine, 250<span class="elsevierStyleHsp" style=""></span>mg/d, for 28 days, leading to clinical and microbiological cure.</p><p id="par0020" class="elsevierStylePara elsevierViewall">Tinea pedis, particularly the interdigital form, is the most common fungal infection.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a> The warm, moist, and protected anatomic environment predisposes to the proliferation of fungi and gram-negative bacteria. Overgrowth of the normal flora of these spaces provokes maceration, peeling, and the appearance of fissures.</p><p id="par0025" class="elsevierStylePara elsevierViewall">Intertrigo of the foot is usually caused by dermatophytes and yeasts and less commonly by bacteria. Polymicrobial infections are of particular importance, especially when <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> is involved, as management can be complex, due both to the aggressiveness of the infection, which can produce potentially severe conditions such as cellulitis, and to therapeutic difficulties, because of a high frequency of antimicrobial resistence.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">3</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">A major problem with these polymicrobial infections arises from interactions between the different species involved: the presence of fungi in the lesions appears to favor colonization by <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span>,<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">4,5</span></a> and bacterial overgrowth associated with interdigital infections of the foot can have a fungistatic or fungicidal effect. It has been shown that <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> is able to inhibit both yeasts <span class="elsevierStyleItalic">(C. albicans)</span><a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">6,7</span></a> and filamentous fungi (<span class="elsevierStyleItalic">Aspergillus fumigatus</span>, <span class="elsevierStyleItalic">Fusarium</span> species) in vitro.<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2,7,8</span></a> Furthermore, this inhibition can occur with various species of <span class="elsevierStyleItalic">Pseudomonas</span>, such as <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> or <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">clororaphis</span>, but not with other bacteria, and the effect occurs specifically with the dermatophytes most frequently isolated in tinea pedis, such as <span class="elsevierStyleItalic">Trichophyton.</span><a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2,5,6,9</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">Returning to our patient, we created a simple in vitro model of the interaction between <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> and <span class="elsevierStyleItalic">T.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">rubrum</span>. We observed that the dermatophyte did not grow after inoculation into a culture of <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), a finding previously reported by other authors.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a></p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">In conclusion, in patients with interdigital tinea pedis that is clinically extensive, intractable, or that recurs after treatment, we must consider possible reasons for diagnostic failure. These may be clinical, when the presence of bacteria is not considered in the diagnosis of tinea pedis, leading to inefficacy of an exclusively antifungal treatment, or<span class="elsevierStyleHsp" style=""></span>microbiological, when the presence of bacteria is not sought or when overgrowth of <span class="elsevierStyleItalic">P.</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">aeruginosa</span> is not contemplated as a possible cause of falsely negative dermatophyte culture. The application of a diagnostic protocol that includes systematic use of Wood light for the diagnosis of erythrasma (not forgetting possible mixed fungal infection)<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> and taking samples to search both for fungi (particulary dermatophytes, but also yeasts) and for bacteria (especially gram-negative bacteria, including <span class="elsevierStyleItalic">Pseudomonas</span>), could help to define the microbiological etiology of the intertrigo and contribute to a reduction in diagnostic failure that will inevitably lead to inadequate treatment (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Finally, it must not be forgotten that, if all these investigations are negative or inconclusive, a biopsy will help to diagnose noninfectious diseases, such as inverse psoriasis or Bowen Disease.<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">10</span></a></p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Aspiroz C, Toyas C, Robres P, Gilaberte Y. Interacción de <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> y hongos dermatofitos: repercusión en el curso clínico y en el diagnóstico microbiológico de la <span class="elsevierStyleItalic">tinea pedis</span>. Actas Dermosifiliogr. 2016;107:80–82.</p>" ] ] "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" => 750 "Ancho" => 1000 "Tamanyo" => 143111 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Intense erythema and maceration, with peripheral peeling in the fourth interdigital space.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 961 "Ancho" => 1000 "Tamanyo" => 148523 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Sabouraud dextrose agar with chloramphenicol inoculated with <span class="elsevierStyleItalic">Trichophyton rubrum</span> with and without previous seeding with <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span>. Incubation for 12 days at 28<span class="elsevierStyleHsp" style=""></span>°C.</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2753 "Ancho" => 3253 "Tamanyo" => 410291 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Diagnostic algorithm for intertrigo of the foot.</p> <p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Other local measures include the application of topical antiseptics, the use of nonocclusive footwear and adequate drying of the affected area after showering or bathing. In addition, antifungal powders should be applied to the footwear to eliminate fungal spores that could provoke reinfection. When taking samples for culture of fungi or bacteria, no topical antifungal or antibiotic agents should have been used for at least 15<span class="elsevierStyleHsp" style=""></span>days before sampling; in the case of systemic treatments, this period may need to be extended, as some agents remain in the stratum corneum for longer. KOH indicates direct examination with potassium hydroxide.</p> <p id="spar0025" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleSup">a</span> When there is a high clinical suspicion of tinea pedis, empirical treatment with antifungal agents can be started before biopsy, even if direct examination and culture are negative, considering the possibility of a false negative.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Eritrasma interdigital: datos clínicos, epidemiológicos y microbiológicos" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "M.L1 Morales-Trujillo" 1 => "R. Arenas" 2 => "S. 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"fecha" => "2014" "volumen" => "24" "paginaInicial" => "185" "paginaFinal" => "192" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24746721" "web" => "Medline" ] ] ] ] ] ] ] ] 6 => array:3 [ "identificador" => "bib0085" "etiqueta" => "7" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "<span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> pyocyanin and 1-hydroxyphenazine inhibit fungal growth" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "J.R. Kerr" 1 => "G.W. Taylor" 2 => "A. Rutman" 3 => "N. Høiby" 4 => "P.J. Cole" 5 => "R. Wilson" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "J Clin Pathol." 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Available at: http://emedicine.medscape.com/article/1087691-workup" ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack278590" "titulo" => "Acknowledgments" "texto" => "<p id="par0045" class="elsevierStylePara elsevierViewall">We would like to thank Dr. Luis Charlez of the Dermatology Department of Hospital Royo Villanova in Saragossa, for his contribution to the diagnosis, treatment, and management of this case.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/15782190/0000010700000001/v2_201704190205/S1578219015003248/v2_201704190205/en/main.assets" "Apartado" => array:4 [ "identificador" => "6157" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Case and Research Letters" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/15782190/0000010700000001/v2_201704190205/S1578219015003248/v2_201704190205/en/main.pdf?idApp=UINPBA000044&text.app=https://actasdermo.org/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1578219015003248?idApp=UINPBA000044" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 16 | 10 | 26 |
| 2024 October | 108 | 62 | 170 |
| 2024 September | 92 | 47 | 139 |
| 2024 August | 120 | 60 | 180 |
| 2024 July | 130 | 49 | 179 |
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| 2024 May | 125 | 40 | 165 |
| 2024 April | 115 | 31 | 146 |
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| 2023 December | 159 | 28 | 187 |
| 2023 November | 171 | 31 | 202 |
| 2023 October | 95 | 34 | 129 |
| 2023 September | 113 | 35 | 148 |
| 2023 August | 70 | 18 | 88 |
| 2023 July | 109 | 27 | 136 |
| 2023 June | 76 | 23 | 99 |
| 2023 May | 96 | 27 | 123 |
| 2023 April | 86 | 26 | 112 |
| 2023 March | 90 | 17 | 107 |
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| 2023 January | 65 | 34 | 99 |
| 2022 December | 72 | 43 | 115 |
| 2022 November | 53 | 27 | 80 |
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| 2022 August | 88 | 48 | 136 |
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| 2022 May | 70 | 36 | 106 |
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| 2021 May | 40 | 31 | 71 |
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| 2020 December | 55 | 18 | 73 |
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| 2020 October | 27 | 19 | 46 |
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| 2020 July | 28 | 15 | 43 |
| 2020 June | 54 | 43 | 97 |
| 2020 May | 34 | 35 | 69 |
| 2020 April | 36 | 22 | 58 |
| 2020 March | 28 | 22 | 50 |
| 2020 February | 4 | 0 | 4 |
| 2020 January | 4 | 0 | 4 |
| 2019 December | 4 | 1 | 5 |
| 2019 November | 4 | 0 | 4 |
| 2019 October | 0 | 3 | 3 |
| 2019 August | 4 | 0 | 4 |
| 2019 July | 4 | 0 | 4 |
| 2019 June | 4 | 0 | 4 |
| 2019 May | 6 | 0 | 6 |
| 2019 April | 8 | 2 | 10 |
| 2019 March | 3 | 4 | 7 |
| 2019 January | 7 | 0 | 7 |
| 2018 December | 1 | 0 | 1 |
| 2018 November | 2 | 0 | 2 |
| 2018 October | 3 | 0 | 3 |
| 2018 September | 5 | 0 | 5 |
| 2018 March | 1 | 0 | 1 |
| 2018 February | 33 | 2 | 35 |
| 2018 January | 45 | 14 | 59 |
| 2017 December | 49 | 11 | 60 |
| 2017 November | 47 | 7 | 54 |
| 2017 October | 32 | 8 | 40 |
| 2017 September | 25 | 4 | 29 |
| 2017 August | 33 | 5 | 38 |
| 2017 July | 36 | 6 | 42 |
| 2017 June | 36 | 12 | 48 |
| 2017 May | 28 | 6 | 34 |
| 2017 April | 26 | 5 | 31 |
| 2017 March | 23 | 7 | 30 |
| 2017 February | 26 | 8 | 34 |
| 2017 January | 20 | 7 | 27 |
| 2016 December | 40 | 16 | 56 |
| 2016 November | 45 | 17 | 62 |
| 2016 October | 32 | 33 | 65 |
| 2016 September | 0 | 6 | 6 |
| 2016 August | 0 | 1 | 1 |
| 2016 July | 1 | 1 | 2 |
| 2016 June | 0 | 7 | 7 |
| 2016 May | 0 | 3 | 3 |
| 2016 April | 0 | 2 | 2 |
| 2016 February | 0 | 5 | 5 |
| 2016 January | 0 | 2 | 2 |
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