Case Report
Cutaneous protothecosis in kidney transplant recipient
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=> 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" => "Jane" "apellidos" => "Tomimori" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "Marilia Marufuji" "apellidos" => "Ogawa" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Department of Dermatology, Universidade Federal de São Paulo, São Paulo, SP, Brazil" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Pathology, Universidade Federal de São Paulo, São Paulo, SP, Brazil" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 907 "Ancho" => 1207 "Tamanyo" => 139923 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Presence of sporangia grouped within the cytoplasm of macrophages (Hematoxylin & eosin, x400).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Protothecosis is an uncommon infection caused by the aclorophyllated algae of the genus <span class="elsevierStyleItalic">Prototheca</span>. Five species are known, two of which affect humans: <span class="elsevierStyleItalic">P. zopfii</span> and <span class="elsevierStyleItalic">P. wickerhamii</span>, the latter being the most common.</p><p id="par0010" class="elsevierStylePara elsevierViewall">The first case of human infection was described in 1964 as a cutaneous ulcer located on the foot of a rice grower in Sierra Leone.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> A little more than 200 cases have been reported worldwide, with 10 in Brazil.<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2–4</span></a> We report a new case of protothetosis that occurred in a renal transplant recipient (RTR) in Brazil.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Case report</span><p id="par0015" class="elsevierStylePara elsevierViewall">A 60-year-old male patient, a skin phototype IV, born in Caetité-BA and moved to São Paulo-SP 35 years ago, reported a nodular lesion 6 months ago on the right leg (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>), with no history of previous trauma. Regarding his personal history, the patient was RTR 15 years ago, due to arterial hypertension, and had been treated for multiple previous squamous cell carcinomas. He had already used cyclosporin and azathioprine. At the time of the infection, the patient had been using prednisone 5<span class="elsevierStyleHsp" style=""></span>mg/day and sirolimus 1<span class="elsevierStyleHsp" style=""></span>mg/day for 5 years.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">The initial diagnostic hypothesis was subcutaneous mycosis and the patient was referred for complete lesion excision. The material was sent for histopathological analysis and granulomatous inflammatory process was observed with suppuration and sporangia grouped within the cytoplasm of the macrophages (<a class="elsevierStyleCrossRefs" href="#fig0010">Figs. 2 and 3</a>). The sporangia were stained by Period Acid-Schiff (PAS) and Grocott, and presented a morula appearance (<a class="elsevierStyleCrossRefs" href="#fig0020">Figs. 4 and 5</a>). Part of the skin fragment was sent for mycological examination and fungal culture, with no growth of agents.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">In the postoperative period, the surgical wound was allowed to heal by secondary intention and was initially performed with compressive cotton dressing, then dressed daily with topical mupirocin for 3 weeks, and silver nitrate 10% until complete healing. The patient was treated with fluconazole 150<span class="elsevierStyleHsp" style=""></span>mg/day for a period of 3 months, until complete healing of the lesion.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Discussion</span><p id="par0030" class="elsevierStylePara elsevierViewall">The algae of the genus <span class="elsevierStyleItalic">Prototheca</span> do not present chloroplasts, organelles that contain the chlorophyll pigment, so they do not have the capacity to perform photosynthesis. They need a heterotrophic source of nutrients, such as organic carbon and nitrogen, and the skin is the most frequently affected organ.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Prototheca spp.</span> is widely distributed throughout the world. Algae are found in soil, in the decomposition of plants, in water, and in certain food items. They also exist as a saprophyte organism in the human skin, nails and respiratory and digestive tracts.<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">1,6</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Prototheca spp</span>. resists chlorine treatment, sewage treatment and intestinal digestion. This contributes to its persistence in sewage, dissemination by domestic animals and permanence in the environment. It is also resistant to milk pasteurization, representing a problem for the consumption of dairy products.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Human protothecosis is rare, but the incidence is higher in immunocompromised patients (local or systemic corticosteroids, immunobiologicals,<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">7</span></a> hematologic malignancies or cancer, diabetes mellitus, AIDS, solid organ and bone marrow transplant recipients, alcoholism or autoimmune disease). In the literature, only 219 cases of human protothecosis have been described worldwide, of which 11 were reported in Brazil,<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">1,4</span></a> including this one. Among the cases of human protothecosis, there are only 15 reports of cases in solid organ receptors,<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">4,7,8</span></a> 9 in renal transplant recipients and 1 in liver/kidney transplantation. In Brazil, it is the first case described in a renal transplant recipient.</p><p id="par0050" class="elsevierStylePara elsevierViewall">The pathogenesis of protothecosis is unknown. In most cases, the source of the infection is exogenous contact with contaminated soil or water, commonly occurring after traumatic inoculation. These infections were also described as complications after surgery.</p><p id="par0055" class="elsevierStylePara elsevierViewall">In man, protothecosis is caused mainly by <span class="elsevierStyleItalic">P. wickerhamii</span> and manifests itself in three forms: cutaneous, articular and systemic, with an acute or chronic course. The cutaneous form is the most observed. Lesions have a slow evolution and variable appearance: plaques, papules, nodules, ulcerations and eczematous eruptions. The most common presentations are vesiculobullous lesion and ulceration.<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">9</span></a> In the present case, the patient presented a nodular lesion, reminiscent of the phaeohyphomycosis, a mycosis by dematiaceous fungi described in the recipients of solid organ transplantation.</p><p id="par0060" class="elsevierStylePara elsevierViewall">In histopathological examination, there is a granulomatous inflammatory infiltrate, consisting of lymphocytes, macrophages, giant cells and neutrophils. In staining with PAS or Grocott, we can observe sporangia internally containing sporangiospores, which may be inside macrophages or free in the exudate. Sporangia are surrounded by a capsule that can vary from 7 to 30<span class="elsevierStyleHsp" style=""></span>μm; <span class="elsevierStyleItalic">P. zopfii</span> tends to be larger (7–30<span class="elsevierStyleHsp" style=""></span>μm) than <span class="elsevierStyleItalic">P. wickerhamii</span> (3–15<span class="elsevierStyleHsp" style=""></span>μm).<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a> A feature of <span class="elsevierStyleItalic">P. wickerhamii</span> is to exhibit sporangiospores with a rounded central endospore, and this characteristic has been described as morula-like, daisy-like or raspberry-like.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a> In the histopathological examination of the our patient, sporangiospores were better evidenced with PAS and Grocott staining, so routine screening with special staining for nodular or nodule-cystic lesions in transplant recipients should be included.</p><p id="par0065" class="elsevierStylePara elsevierViewall">There is currently no definite treatment for <span class="elsevierStyleItalic">Prototheca spp</span>. due to the rarity of the disease. Amphotericin B appears to be effective in cases of disseminated infection.<a class="elsevierStyleCrossRefs" href="#bib0075"><span class="elsevierStyleSup">5,8</span></a> Azole antifungals are also used, although their efficacy is variable.<a class="elsevierStyleCrossRefs" href="#bib0075"><span class="elsevierStyleSup">5,10</span></a> Our patient had a good therapeutic response with surgical treatment and oral fluconazole, evolving with adequate healing and there was no relapse after 4 years of follow-up.</p><p id="par0070" class="elsevierStylePara elsevierViewall">In conclusion, nodular or nodule-cystic lesions in transplant recipients should be biopsied to screen for infectious agents using special stains (PAS, Grocott, Fite-Faraco). Culturing for fungi and mycobacteria is also recommended. The lesion of protothecosis should be completely excised and healing left by secondary intention. Complementing surgical treatment with azole derivatives is highly recommended.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Financial support</span><p id="par0075" class="elsevierStylePara elsevierViewall">None declared.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Authors’ contributions</span><p id="par0080" class="elsevierStylePara elsevierViewall">Valeria Romero Godofredo: Statistical analysis; approval of the final version of the manuscript; conception and planning of the study; elaboration and writing of the manuscript; obtaining, analysis, and interpretation of the 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="par0085" class="elsevierStylePara elsevierViewall">Milvia Maria Simões e Silva Enokihara: Intellectual participation in the propaedeutic and/or therapeutic conduct of the studied cases; critical review of the manuscript.</p><p id="par0090" class="elsevierStylePara elsevierViewall">Jane Tomimori: Obtaining, analysis, and interpretation of the 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="par0095" class="elsevierStylePara elsevierViewall">Marilia Marufuji Ogawa: Approval of the final version of the manuscript; conception and planning of the study; 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></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Conflicts of interest</span><p id="par0100" class="elsevierStylePara elsevierViewall">None declared.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres1327249" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1223478" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 3 => array:2 [ "identificador" => "sec0010" "titulo" => "Case report" ] 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:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2019-06-06" "fechaAceptado" => "2019-08-04" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1223478" "palabras" => array:3 [ 0 => "Harmful algal proliferation" 1 => "Opportunistic infections" 2 => "<span class="elsevierStyleItalic">Skin diseases, infectious</span>" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Protothecosis is a rare condition caused by the aclorophylated algae of the genus <span class="elsevierStyleItalic">Prototheca</span>. In humans, protothecosis, caused mainly by <span class="elsevierStyleItalic">P. wickerhamii</span>, manifests itself in three forms: cutaneous, articular and systemic. It can occur in both immunocompetent and immunosuppressed individuals, being much more common in the latter. We present a new case of protothecosis in Brazil in a kidney transplant recipient.</p></span>" ] ] "NotaPie" => array:2 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">How to cite this article: Godofredo VR, Enokihara MMSS, Tomimori J, Ogawa MM. Cutaneous protothecosis in kidney transplant recipient. An Bras Dermatol. 2020;95:210–3.</p>" ] 1 => array:2 [ "etiqueta" => "☆☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Study conducted at the Universidade Federal de São Paulo, São Paulo, SP, Brazil.</p>" ] ] "multimedia" => array:5 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1973 "Ancho" => 1207 "Tamanyo" => 301427 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Erythematous nodule in the distal third of the right leg.</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" => 906 "Ancho" => 1207 "Tamanyo" => 217956 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Presence of a granulomatous inflammatory process with suppuration. In the middle, the sporangia (Hematoxylin & eosin, x40).</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" => 907 "Ancho" => 1207 "Tamanyo" => 139923 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Presence of sporangia grouped within the cytoplasm of macrophages (Hematoxylin & eosin, x400).</p>" ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 906 "Ancho" => 1207 "Tamanyo" => 179735 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">The sporangia appear stained by PAS (x400).</p>" ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 906 "Ancho" => 1207 "Tamanyo" => 240160 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">The sporangia appear stained in black by Grocott (x400).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A case of human protothecosis" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "R.R. 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