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Piedraia hortae: biofilm formation and its importance in the pathogenesis of Piedra nigra (black piedra)
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"identificador" => "aff0015" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Postgraduation in Health and Behavior, Universidade Católica de Pelotas" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Dermatology, Universidade Federal de Pelotas, Pelotas, RS, Brazil" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Sector of Mycology, Laboratório Ary Costa, Pelotas, RS, Brazil" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig0030" "etiqueta" => "Fig. 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr6.jpeg" "Alto" => 1532 "Ancho" => 1005 "Tamanyo" => 182489 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0030" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">SEM ‒ adhered and parallel hyphae (×2,000 and ×4,500).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Piedra nigra</span> is a well-known disease,<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> which, together with <span class="elsevierStyleItalic">Piedra alba</span> (white piedra), constitutes a group of two similar diseases, also called trichomycosis<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> or ectotrichomycosis,<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> in which nodules appear on the hair shafts, dark or white respectively, without epidermal involvement.</p><p id="par0010" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Piedra alba</span> is a condition resulting from the colonization of some species of the genus <span class="elsevierStyleItalic">Trichosporon</span>, such as <span class="elsevierStyleItalic">T. cutaneum</span>, <span class="elsevierStyleItalic">T. ovoides</span> and <span class="elsevierStyleItalic">T. inkin</span>, occurring on the hair shafts of the beard, armpits and pubis, with scalp hair less affected, varying from white to light brownish coloration. The genus <span class="elsevierStyleItalic">Trichosporon</span> includes filamentous fungi that can form complex biofilms.</p><p id="par0015" class="elsevierStylePara elsevierViewall">Historically, <span class="elsevierStyleItalic">Piedra nigra</span> was described by Paulo Horta,<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> who discussed in the original publication <span class="elsevierStyleItalic">Piedra nostras</span> from Europe and <span class="elsevierStyleItalic">Piedra colombica</span> from South America, both caused by non-pigmented fungi, also called nodular trichomycosis or trichosporia, as the genus <span class="elsevierStyleItalic">Trichosporum</span> had already been coined (in the spelling used at that time).</p><p id="par0020" class="elsevierStylePara elsevierViewall">In that publication, he described cases of two young male students<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> from Bahia different in clinical appearance, with dark nodules (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A), as well as the fungal colonies obtained from them. Morphologically, the examination of the agent also showed differences, without the formation of yeast-like coccoid structures described for the <span class="elsevierStyleItalic">Piedra alba</span> agent. The hyphae, in addition to pigment, showed round dilations (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B), chlamydospores, as well as ascospores (observed inside a saccular structure) at different evolution stages (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Piedra nigra</span> is endemic to South America,<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5–7</span></a> and some indigenous populations show a prevalence of up to 50%, with cases also being described in Asia,<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">8,9</span></a> commonly affecting the scalp.</p><p id="par0030" class="elsevierStylePara elsevierViewall">Scanning electron microscopy (SEM) with a Jeol microscope, JSM ‒ 6610LV at CEME-SUL (microscopy center of the southern region, of the Universidade Federal do Rio Grande) was used to examine a colony of <span class="elsevierStyleItalic">P. hortae</span> obtained from the mycolibrary of Instituto de Medicina Tropical de São Paulo, lineage 499, with the aim of describing its ultrastructure.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Results</span><p id="par0035" class="elsevierStylePara elsevierViewall">The colony has a typical blackish appearance (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>A). Examination of the microculture with optical microscopy demonstrates hyphae with typical dilations (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>B), as shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B. Ascospores (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>C) were also observed on optical microscopy, showing a structure similar to drawing 10 in <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">It is noteworthy that, in the potassium hydroxide test, part of the colonies do not dissolve, forming brownish clumps, which are difficult to focus and examine due to their thickness (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>B).</p><p id="par0045" class="elsevierStylePara elsevierViewall">With scanning electron microscopy on low magnification, two distinct aspects of the colony can be identified, a compact area and a filamentous one (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">Examination of the filamentous area demonstrates dilations in the hyphae, as seen under optical microscopy (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>). Detailed examination of them also shows that they are adhered by a thin reticular substance (<a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a>). A recurring finding is the adhesion between the fungal filaments in a parallel distribution (<a class="elsevierStyleCrossRef" href="#fig0030">Fig. 6</a>). On high magnification, the micro-fibrillar substance adhering the hyphae to each other becomes very evident (<a class="elsevierStyleCrossRefs" href="#fig0035">Figs. 7 and 8</a>).</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="fig0030"></elsevierMultimedia><elsevierMultimedia ident="fig0035"></elsevierMultimedia><elsevierMultimedia ident="fig0040"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Examination of the compact area shows the hyphae embedded in the reticular matrix forming a biofilm (<a class="elsevierStyleCrossRef" href="#fig0045">Fig. 9</a>), and the colony looks well adhered. On high magnification, it can be observed that the hyphae are inside this fibrillar matrix (<a class="elsevierStyleCrossRef" href="#fig0050">Fig. 10</a>), which has the same appearance as the extracellular matrix that adheres the hyphae to each other in the filamentous area.</p><elsevierMultimedia ident="fig0045"></elsevierMultimedia><elsevierMultimedia ident="fig0050"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Discussion</span><p id="par0060" class="elsevierStylePara elsevierViewall">No reports were found about the ultrastructural examination of <span class="elsevierStyleItalic">P. hortae</span> colonies, only of the disease nodules; in these reports, a cementing extracellular substance<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10,11</span></a> is mentioned, as forming the nodules on the hair shafts, together with hyphae and spores.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The present findings demonstrate that the fungal structures produce a substance secreted into the extracellular environment, with a microfibrillar appearance, which adheres the hyphae to each other, and in some areas, perhaps older areas of the colony, causes great compaction, embedding these structures and forming a biofilm. Ascospores were not found, as only the surface of samples is examined using this technique and ascospores are found inside the colony or nodule of the <span class="elsevierStyleItalic">piedra</span>.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">This fibrillar network is what may provide resistance and configuration to <span class="elsevierStyleItalic">Piedra</span> nodules, allowing them to occur in the partly hostile environment of the hair shafts, possibly also acting as a factor for hair adhesion in disease dissemination. Corroborating this formation of resistant structures, upon direct examination with optical microscopy, there is some difficulty in dissolving the colonies, which appear as brownish clumps, as seen in figure 2B.</p><p id="par0075" class="elsevierStylePara elsevierViewall">The term biofilm was first used in the 1970s, despite being an old observation by microbiologists. It describes a polymeric extracellular matrix with embedded etiological agents, having a protective function against ultraviolet radiation, extreme temperatures and pH, salinity, and pressure that are harmful to bacteria, as well as being involved in antibiotic resistance.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> They can be formed by polysaccharides, proteins, or fats,<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> and with the morphological analysis technique used here, it is not possible to establish the composition of the documented matrix.</p><p id="par0080" class="elsevierStylePara elsevierViewall">Fungi can also produce biofilms, which has already been demonstrated in species that cause onychomycosis such as <span class="elsevierStyleItalic">Trichophyton rubrum</span> and <span class="elsevierStyleItalic">T. mentagrophytes</span>.<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13,14</span></a> In a publication, slight adhesion between the hyphae was described in <span class="elsevierStyleItalic">T. mentagrophytes</span> colonies using SEM,<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> a lighter finding than the one reported herein for <span class="elsevierStyleItalic">P. hortae</span>.</p><p id="par0085" class="elsevierStylePara elsevierViewall">Regarding the <span class="elsevierStyleItalic">Piedras</span>, the formation of biofilms has already been described in several species of Trichosporon,<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">16,17</span></a> and interspecies variation has been found, allowing them to be classified as weak or strong producers of biofilms. Possibly, strains with low biofilm production do not cause <span class="elsevierStyleItalic">Piedra alba</span>.</p><p id="par0090" class="elsevierStylePara elsevierViewall">The ultrastructural findings of the <span class="elsevierStyleItalic">Piedraia hortae</span> colony demonstrate that the formation of biofilm by the extracellular matrix secreted by the hyphae may be crucial in the pathogenesis of <span class="elsevierStyleItalic">Piedra nigra</span>.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Financial support</span><p id="par0095" class="elsevierStylePara elsevierViewall">None declared.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Authors' contributions</span><p id="par0100" class="elsevierStylePara elsevierViewall">Hiram Larangeira de Almeida Jr.: Approval of the final version of the manuscript; design and planning of the study; drafting and editing of the manuscript; collection, analysis and interpretation of data; effective participation in research orientation; intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the literature; critical review of the manuscript.</p><p id="par0105" class="elsevierStylePara elsevierViewall">Thales de Moura Assis: Approval of the final version of the manuscript; design and planning of the study; drafting and editing of the manuscript; collection, analysis and interpretation of data; intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the literature; critical review of the manuscript.</p><p id="par0110" class="elsevierStylePara elsevierViewall">Eduardo Camargo Faria: Approval of the final version of the manuscript; design and planning of the study; drafting and editing of the manuscript; collection, analysis and interpretation of data; intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the literature; critical review of the manuscript.</p><p id="par0115" class="elsevierStylePara elsevierViewall">Luiz Roberto Kramer Costa: Approval of the final version of the manuscript; design and planning of the study, drafting and editing of the manuscript; collection, analysis and interpretation of data; intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the literature; critical review of the manuscript.</p><p id="par0120" class="elsevierStylePara elsevierViewall">Berenice Marques Ibaldo: Approval of the final version of the manuscript; design and planning of the study; drafting and editing of the manuscript; collection, analysis and interpretation of data; intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the literature; critical review of the manuscript.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflicts of interest</span><p id="par0125" class="elsevierStylePara elsevierViewall">None declared.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres2281413" "titulo" => "Abstract" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Objective" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Study limitations" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1897732" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 3 => array:2 [ "identificador" => "sec0010" "titulo" => "Results" ] 4 => array:2 [ "identificador" => "sec0015" "titulo" => "Discussion" ] 5 => array:2 [ "identificador" => "sec0020" "titulo" => "Financial support" ] 6 => array:2 [ "identificador" => "sec0025" "titulo" => "Authors' contributions" ] 7 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflicts of interest" ] 8 => array:2 [ "identificador" => "xack783752" "titulo" => "Acknowledgments" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2023-11-14" "fechaAceptado" => "2023-12-17" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1897732" "palabras" => array:4 [ 0 => "Biofilms" 1 => "Microscopy" 2 => "Electron" 3 => "Piedraia hortae" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Little is known about the ultrastructure of <span class="elsevierStyleItalic">Piedraia hortae</span>.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Objective</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">To examine a <span class="elsevierStyleItalic">P. hortae</span> colony with scanning electron microscopy and investigate possible contributions to its the pathogenesis of black piedra.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">On low magnifications, two distinct aspects of the colony are identified, a compact area and a filamentous area. Analysis of the filamentous area demonstrates hyphae adhered by a thin reticular substance. A recurring finding is the adhesion between the fungal filaments in parallel. On high magnifications, the microfibrillar substance adhering the hyphae to each other becomes very evident. Examination of the compact area shows the hyphae embedded in the reticular matrix forming a biofilm and the colony well adhered. On high magnification, it can be observed that the hyphae are within this fibrillar matrix, which has the same appearance as the filamentous substance that adheres the hyphae to each other.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Study limitations</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Only one strain was examined.</p></span> <span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conclusions</span><p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">The formation of biofilm with fungal structures and reticulated extracellular substance is important in the pathogenesis of black piedra.</p></span>" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Objective" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Study limitations" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Study conducted at the Universidade Católica de Pelotas, Pelotas, RS, Brazil.</p>" ] ] "multimedia" => array:10 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1562 "Ancho" => 2925 "Tamanyo" => 637027 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Drawings from the original 1911 publication. (A) Dark nodules on the hair shaft and the formation of ascospores (8 to 18). (B) Microscopic appearance of the etiological agent with hyphae, which show round dilations (arrows).</p>" ] ] 1 => array:8 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1085 "Ancho" => 1505 "Tamanyo" => 207758 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">(A) Blackish appearance of the colony. (B) Optical microscopy – dilated hyphae (arrows); in the upper right corner, one can see the brownish area of the colony, which was not dissolved. (C) Optical microscopy ‒ initial ascospore (arrow).</p>" ] ] 2 => array:8 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 761 "Ancho" => 1005 "Tamanyo" => 148445 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Scanning electron microscopy (SEM) - low magnification viewing the colony with filamentous area on the right and compact area on the left (×300).</p>" ] ] 3 => array:8 [ "identificador" => "fig0020" "etiqueta" => "Fig. 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 761 "Ancho" => 1005 "Tamanyo" => 85954 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0020" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">SEM ‒ detail of a dilated hyphae (arrow), similar to those seen under optical microscopy (×8,000).</p>" ] ] 4 => array:8 [ "identificador" => "fig0025" "etiqueta" => "Fig. 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 761 "Ancho" => 1005 "Tamanyo" => 107603 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0025" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">SEM – hyphae covered with microfibrillar extracellular matrix (×3,500).</p>" ] ] 5 => array:8 [ "identificador" => "fig0030" "etiqueta" => "Fig. 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr6.jpeg" "Alto" => 1532 "Ancho" => 1005 "Tamanyo" => 182489 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0030" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">SEM ‒ adhered and parallel hyphae (×2,000 and ×4,500).</p>" ] ] 6 => array:8 [ "identificador" => "fig0035" "etiqueta" => "Fig. 7" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr7.jpeg" "Alto" => 746 "Ancho" => 1005 "Tamanyo" => 127751 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0035" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">SEM ‒ high magnification, showing in detail hyphae adhered by the reticular matrix (×7.000).</p>" ] ] 7 => array:8 [ "identificador" => "fig0040" "etiqueta" => "Fig. 8" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr8.jpeg" "Alto" => 746 "Ancho" => 1005 "Tamanyo" => 101075 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0040" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">SEM ‒ high magnification with detail of the adhesion and parallel arrangement of hyphae (×11.000).</p>" ] ] 8 => array:8 [ "identificador" => "fig0045" "etiqueta" => "Fig. 9" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr9.jpeg" "Alto" => 746 "Ancho" => 1005 "Tamanyo" => 120755 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0045" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">SEM – low magnification in the compact area, showing fungal structures embedded in dense extracellular matrix (×1.000).</p>" ] ] 9 => array:8 [ "identificador" => "fig0050" "etiqueta" => "Fig. 10" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr10.jpeg" "Alto" => 1242 "Ancho" => 1675 "Tamanyo" => 256661 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0050" "detalle" => "Fig. 1" "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">SEM – high magnification in the compact area, depicting hyphae (H) embedded in microfibrillar matrix (×5.000).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:17 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ 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