Brief report
COVID-19 associated with disseminated histoplasmosis in a kidney transplant patient
COVID-19 asociado a histoplasmosis diseminada en un paciente trasplantado renal
Ivana Maldonadoa,
, María Elisa Elisiria, Liliana Fernández-Canigiaa, Ana Victoria Sánchezc, Liana Lópezc, Adriana I. Toranzod, Cecilia López-Joffred, Sol González-Fragab, Cristina Elena Canterosd
Corresponding author
a Microbiología, Laboratorio Central-Hospital Alemán, Buenos Aires, Argentina
b Biología Molecular, Laboratorio Central – Hospital Alemán, Buenos Aires, Argentina
c Servicio de Infectología- Hospital Alemán, Buenos Aires, Argentina
d Departamento Micología, Laboratorio Nacional de Referencia en Micología Médica-INEI-ANLIS “Dr. Carlos G. Malbrán”, Buenos Aires, Argentina
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"ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "es" => array:13 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Informe breve</span>" "titulo" => "Calidad microbiológica de la carne picada y detección de patógenos en muestras ambientales de carnicerías de la ciudad de Tandil, provincia de Buenos Aires, Argentina" "tienePdf" => "es" "tieneTextoCompleto" => "es" "tieneResumen" => array:3 [ 0 => "es" 1 => "es" 2 => "en" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "215" "paginaFinal" => "219" ] ] "titulosAlternativos" => array:1 [ "en" => array:1 [ "titulo" => "Microbiological quality of fresh ground beef and detection of pathogens in environmental samples taken from butcher shops in the city of Tandil, Buenos Aires Province, Argentina" ] ] "contieneResumen" => array:2 [ "es" => true "en" => true ] "contieneTextoCompleto" => array:1 [ "es" => true ] "contienePdf" => array:1 [ "es" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "María Julia Ruiz, Nora Lia Padola, Gerardo Leotta, Rocío Colello, Juan Passucci, Edgardo Rodríguez, Daniel Fernández Fellenz, Alejandra Krüger, Marcelo Sanz, Elida Elichiribehety, Analía Inés Etcheverría" "autores" => array:11 [ 0 => array:2 [ "nombre" => "María Julia" "apellidos" => "Ruiz" ] 1 => array:2 [ "nombre" => "Nora Lia" "apellidos" => "Padola" ] 2 => array:2 [ "nombre" => "Gerardo" "apellidos" => "Leotta" ] 3 => array:2 [ "nombre" => "Rocío" "apellidos" => "Colello" ] 4 => array:2 [ "nombre" => "Juan" "apellidos" => "Passucci" ] 5 => array:2 [ "nombre" => "Edgardo" "apellidos" => "Rodríguez" ] 6 => array:2 [ "nombre" => "Daniel" "apellidos" => "Fernández Fellenz" ] 7 => array:2 [ "nombre" => "Alejandra" "apellidos" => "Krüger" ] 8 => array:2 [ "nombre" => "Marcelo" "apellidos" => "Sanz" ] 9 => array:2 [ "nombre" => "Elida" "apellidos" => "Elichiribehety" ] 10 => array:2 [ "nombre" => "Analía Inés" "apellidos" => "Etcheverría" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">•</span><p id="par0005" class="elsevierStylePara elsevierViewall">Se observó riesgo bajo y buenas condiciones higiénico-sanitarias en carnicerías.</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">•</span><p id="par0010" class="elsevierStylePara elsevierViewall">El 75,0% de las muestras no cumplió con los parámetros microbiológicos.</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">•</span><p id="par0015" class="elsevierStylePara elsevierViewall">Se sugiere identificar desvíos e implementar mejoras continuas.</p></li></ul></p></span>" ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754121000754?idApp=UINPBA00004N" "url" => "/03257541/0000005400000003/v1_202209300808/S0325754121000754/v1_202209300808/es/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S0325754121000377" "issn" => "03257541" "doi" => "10.1016/j.ram.2021.02.004" "estado" => "S300" "fechaPublicacion" => "2022-07-01" "aid" => "447" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2022;54:203-8" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "es" => array:14 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">INFORME BREVE</span>" "titulo" => "<span class="elsevierStyleItalic">Trichophyton benhamiae</span>, un dermatofito zoofílico emergente en Argentina con reservorio en cobayos: descripción de 7<span class="elsevierStyleHsp" style=""></span> casos en un hospital de la Ciudad Autónoma de Buenos Aires" "tienePdf" => "es" "tieneTextoCompleto" => "es" "tieneResumen" => array:3 [ 0 => "es" 1 => "es" 2 => "en" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "203" "paginaFinal" => "208" ] ] "titulosAlternativos" => array:1 [ "en" => array:1 [ "titulo" => "<span class="elsevierStyleItalic">Trichophyton benhamiae</span>, an emergent zoonotic pathogen in Argentina associated with Guinea pigs: Description of 7<span class="elsevierStyleHsp" style=""></span>cases in Buenos Aires" ] ] "contieneResumen" => array:2 [ "es" => true "en" => true ] "contieneTextoCompleto" => array:1 [ "es" => true ] "contienePdf" => array:1 [ "es" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figura 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2352 "Ancho" => 2508 "Tamanyo" => 515400 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">A) Examen directo de las escamas obtenidas por raspado de la lesión con KOH al 40% con tinta Parker® azul-negra permanente (400×). B) Aspecto macroscópico de <span class="elsevierStyleItalic">Trichophyton benhamiae</span>. Cultivo primario de escamas de lesión con desarrollo en agar Sabouraud y agar selectivo y diferencial para dermatofitos (DTM). C) Subcultivo en placa de agar Sabouraud, micelio velloso blanco con pigmento amarillo. D. Micromorfología de <span class="elsevierStyleItalic">T. benhamiae</span> en disgregado con azul de lactofenol (400×). Microconidios globosos ovales o claviformes que se originan lateralmente y se disponen formando racimos.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Ivana Maldonado, María Elisa Elisiri, Marina Monaco, Alejandra Hevia, Margarita Larralde, Bárbara Fox, Nicolás Refojo, Ricardo Iachini, Andrea Santos Muñoz, Rita Leitner, Paula Luna, Lucrecia Meirama, Eugenia Abad, Neri Ruiz Diaz, Julián Fernández, Liliana Fernández-Canigia" "autores" => array:16 [ 0 => array:2 [ "nombre" => "Ivana" "apellidos" => "Maldonado" ] 1 => array:2 [ "nombre" => "María Elisa" "apellidos" => "Elisiri" ] 2 => array:2 [ "nombre" => "Marina" "apellidos" => "Monaco" ] 3 => array:2 [ "nombre" => "Alejandra" "apellidos" => "Hevia" ] 4 => array:2 [ "nombre" => "Margarita" "apellidos" => "Larralde" ] 5 => array:2 [ "nombre" => "Bárbara" "apellidos" => "Fox" ] 6 => array:2 [ "nombre" => "Nicolás" "apellidos" => "Refojo" ] 7 => array:2 [ "nombre" => "Ricardo" "apellidos" => "Iachini" ] 8 => array:2 [ "nombre" => "Andrea" "apellidos" => "Santos Muñoz" ] 9 => array:2 [ "nombre" => "Rita" "apellidos" => "Leitner" ] 10 => array:2 [ "nombre" => "Paula" "apellidos" => "Luna" ] 11 => array:2 [ "nombre" => "Lucrecia" "apellidos" => "Meirama" ] 12 => array:2 [ "nombre" => "Eugenia" "apellidos" => "Abad" ] 13 => array:2 [ "nombre" => "Neri" "apellidos" => "Ruiz Diaz" ] 14 => array:2 [ "nombre" => "Julián" "apellidos" => "Fernández" ] 15 => array:2 [ "nombre" => "Liliana" "apellidos" => "Fernández-Canigia" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">–</span><p id="par0005" class="elsevierStylePara elsevierViewall">Primera descripción en Argentina de dermatofitosis por <span class="elsevierStyleItalic">Trichophyton benhamiae</span>.</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">–</span><p id="par0010" class="elsevierStylePara elsevierViewall">El reservorio de <span class="elsevierStyleItalic">T. benhamiae</span> fueron los cobayos.</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">–</span><p id="par0015" class="elsevierStylePara elsevierViewall">Las lesiones por este dermatofito en niños suelen ser inflamatorias.</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">–</span><p id="par0020" class="elsevierStylePara elsevierViewall">El diagnóstico de certeza se debe realizar por proteómica o genómica.</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">–</span><p id="par0025" class="elsevierStylePara elsevierViewall">La mayoría de los casos requirieron tratamiento antifúngico sistémico.</p></li></ul></p></span>" ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754121000377?idApp=UINPBA00004N" "url" => "/03257541/0000005400000003/v1_202209300808/S0325754121000377/v1_202209300808/es/main.assets" ] "en" => array:21 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Brief report</span>" "titulo" => "COVID-19 associated with disseminated histoplasmosis in a kidney transplant patient" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "209" "paginaFinal" => "214" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Ivana Maldonado, María Elisa Elisiri, Liliana Fernández-Canigia, Ana Victoria Sánchez, Liana López, Adriana I. Toranzo, Cecilia López-Joffre, Sol González-Fraga, Cristina Elena Canteros" "autores" => array:9 [ 0 => array:4 [ "nombre" => "Ivana" "apellidos" => "Maldonado" "email" => array:1 [ 0 => "ivanam27@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" => "María Elisa" "apellidos" => "Elisiri" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "Liliana" "apellidos" => "Fernández-Canigia" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "Ana Victoria" "apellidos" => "Sánchez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 4 => array:3 [ "nombre" => "Liana" "apellidos" => "López" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 5 => array:3 [ "nombre" => "Adriana I." "apellidos" => "Toranzo" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] ] 6 => array:3 [ "nombre" => "Cecilia" "apellidos" => "López-Joffre" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] ] 7 => array:3 [ "nombre" => "Sol" "apellidos" => "González-Fraga" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 8 => array:3 [ "nombre" => "Cristina Elena" "apellidos" => "Canteros" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Microbiología, Laboratorio Central-Hospital Alemán, Buenos Aires, Argentina" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Biología Molecular, Laboratorio Central – Hospital Alemán, Buenos Aires, Argentina" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Servicio de Infectología- Hospital Alemán, Buenos Aires, Argentina" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Departamento Micología, Laboratorio Nacional de Referencia en Micología Médica-INEI-ANLIS “Dr. Carlos G. Malbrán”, Buenos Aires, Argentina" "etiqueta" => "d" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "COVID-19 asociado a histoplasmosis diseminada en un paciente trasplantado renal" ] ] "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" => 3448 "Ancho" => 2500 "Tamanyo" => 447324 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Timeline of symptom onset, chest CT, laboratory data, and treatment.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0020" class="elsevierStylePara elsevierViewall">Histoplasmosis is an endemic systemic mycosis caused by the <span class="elsevierStyleItalic">Histoplasma capsulatum</span> species complex divided into eight geographic clades (phylogenetic species): Nam1, Nam 2, LamA, LamB, Australian, The Netherlands (Indonesian?); Eurasian and African<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a>. In Argentina, the median estimated prevalence of previous exposure to <span class="elsevierStyleItalic">H. capsulatum</span> in the general population ranged from 30 to 40%<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">1</span></a>. Histoplasmosis is the fourth systemic mycosis diagnosed in Argentina, and its estimated incidence based on laboratory data is 0.45/100<span class="elsevierStyleHsp" style=""></span>000<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a>. The risk of developing diverse mycoses is increased in kidney transplant recipients, although the incidence rate of histoplasmosis is low (0.16 per 100 person years) in the post-transplant period, even in endemic areas<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">2,13</span></a>. Currently, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been associated with individuals with chronic comorbidities, such as solid organ transplant recipients, and various opportunistic mycoses have been described as a coinfection<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a>. In this study, we report a case of disseminated histoplasmosis with cutaneous involvement, and SARS-CoV-2 coinfection in a renal transplant recipient in Argentina. The Hospital Aleman of Buenos Aires city approved this retrospective case report, and all procedures performed were in accordance with the ethical standards of the institution.</p><p id="par0025" class="elsevierStylePara elsevierViewall">A 57-year-old man, living in San Miguel County, Buenos Aires Province, who had a kidney transplant with cadaveric donor in 2014, was admitted to the emergency department on April 24, 2020, with odynophagia and a history of cough and expectoration for 15 days (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). He had been receiving immunosuppressive maintenance therapy including everolimus, mycophenolate mofetil, and meprednisone. The chest computed tomography (CT) image showed diffusely distributed multiple bilateral centrilobular opacities, and a tree-in-bud pattern in both lobes (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>a).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Nasopharyngeal swab samples were analyzed by real-time RT-PCR based SARS-CoV-2 detection, and by Multiplex Real-Time PCR using FilmArray® Respiratory Panel 2.0 (BioFire Diagnostics, LLC). The results of RT-PCR and FilmArray were negative.</p><p id="par0035" class="elsevierStylePara elsevierViewall">Sputum and bronchoalveolar lavage (BAL) samples were processed for microbiological studies. Ziehl–Neelsen stained sputum and BAL smears did not show acid-fast bacilli. Direct microscopic examination and Giemsa-staining to detect fungi were also negative. Common bacteria, fungi and mycobacterium cultures were negative.</p><p id="par0040" class="elsevierStylePara elsevierViewall">The clinical diagnostic criteria, CT features and microbiological results suggested bacterial community-acquired pneumonia (CAP), and the patient received empiric antimicrobial (ampicillin/sulbactam combination) plus anti-viral (oseltamivir) treatments. After five days the patient was discharged from hospital and outpatient follow-up was indicated.</p><p id="par0045" class="elsevierStylePara elsevierViewall">Two weeks later, on May 12, the patient returned to the outpatient unit with persistent odynophagia, cough with expectoration, night sweats and subfebrile state. The clinical examination revealed inflammation to the right peri-tonsillar pillar with soft tissue injury, and a painless, heatless non-scaly circular rash in the forearm. Because of the CT images and a suspicion of disseminated tuberculosis, empiric anti-TB therapy was indicated while waiting for the culture results. After 15 days, both oral and skin biopsies were performed on an outpatient basis.</p><p id="par0050" class="elsevierStylePara elsevierViewall">On May 26, the patient presented to the emergency department with dyspnea on mild exertion (class 3), low blood-oxygen saturation (83%), odynophagia and severe dysphagia. He was re-admitted for close monitoring in the transplantation unit. A new chest CT scan showed slight enlargement of the bilateral centrilobular opacities and small consolidations with a pseudonodular appearance on the upper lung lobes (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>b). Clinical examination showed worsening of the oral and left forearm skin lesions (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>a and b). Routine laboratory tests showed a white blood cell count of 3280<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span>, with elevated fibrinogen (609<span class="elsevierStyleHsp" style=""></span>mg/dl) and D-dimer (650 ng/ml) in plasma. In serum, the results showed low albumin (2.50<span class="elsevierStyleHsp" style=""></span>g/dl), elevated lactate dehydrogenase (266<span class="elsevierStyleHsp" style=""></span>UI/l), as well as C-reactive protein (66.8<span class="elsevierStyleHsp" style=""></span>mg/l), and ferritin (1728<span class="elsevierStyleHsp" style=""></span>ng/ml).</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Considering the pandemic situation, new samples of nasopharyngeal swab were collected for the SARS-CoV-2 test and the results of the RT-PCR test were negative for the virus. Biopsies of both lesions were performed for histological and microbiological studies and a new sputum sample was processed for fungus and mycobacterial culture.</p><p id="par0060" class="elsevierStylePara elsevierViewall">The microbiological direct microscopic examination of the oral mucosa smear showed intracellular yeasts measuring 2–5<span class="elsevierStyleHsp" style=""></span>μm in diameter compatible with <span class="elsevierStyleItalic">H. capsulatum</span> on the Giemsa stain. Under direct microscopic examination the skin and sputum samples were negative for fungi and acid-fast bacilli. Coinciding with the previous findings, histopathology showed yeasts compatible with <span class="elsevierStyleItalic">H. caspulatum</span> in the oral mucosa. Urinary antigen detection was positive with a value of 2.1<span class="elsevierStyleHsp" style=""></span>ng/ml using the Histoplasma GM enzyme immunoassay kit (IMMY, Norman, Oklahoma).</p><p id="par0065" class="elsevierStylePara elsevierViewall">The cultures for fungi on SDA at 28<span class="elsevierStyleHsp" style=""></span>°C showed mold in both oral, skin and sputum samples, after 10 and 18 days, respectively. All isolates were identified by their microscopic characteristics and MALDI-TOF MS (matrix-assisted laser desorption/ionization time-of-flight mass spectrometry) as <span class="elsevierStyleItalic">H. capsulatum</span>.</p><p id="par0070" class="elsevierStylePara elsevierViewall">The serum sample, isolates, and Formalin-Fixed Paraffin-Embedded (FFPE) tissue slices of the oral mucosa and skin samples were sent to the National Reference Laboratory for Mycology of Argentina-INEI “Carlos G. Malbrán” – ANLIS for additional tests. Anti-<span class="elsevierStyleItalic">H. capsulatum</span> antibodies were not detected in the serum sample using counterimmunoelectrophoresis and immunodiffusion methods.</p><p id="par0075" class="elsevierStylePara elsevierViewall">In addition, FFPE tissue specimens were analyzed using both PCRs, a nested conventional PCR that amplified a fragment of the HP100 gene and a real time quantitative PCR that amplified the ITS1 fragment<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">4</span></a>. The nested PCR amplified a 220<span class="elsevierStyleHsp" style=""></span>bp fragment specific for <span class="elsevierStyleItalic">H. capsulatum</span> while the quantitative PCR detected 2.2<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">2</span><span class="elsevierStyleHsp" style=""></span>fg<span class="elsevierStyleHsp" style=""></span>DNA/μl in the oral mucosa sample. Neither of the two PCRs detected <span class="elsevierStyleItalic">Histoplasma</span> DNA in the skin samples.</p><p id="par0080" class="elsevierStylePara elsevierViewall">The isolate was analyzed using phylogenetic multi-locus sequence analysis according to Kasuga et al.<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a>, and the fungus was identified as <span class="elsevierStyleItalic">H. capsulatum</span> clade LamB. Gene sequences of <span class="elsevierStyleItalic">H. capsulatum</span> strain (Culture collection DMIc206235) were deposited in GenBank under accession numbers MW027017 (<span class="elsevierStyleItalic">arf</span>) MW027018 (<span class="elsevierStyleItalic">ole</span>), MW027019 (<span class="elsevierStyleItalic">tub1</span>) and MW002769 (<span class="elsevierStyleItalic">H-anti</span>).</p><p id="par0085" class="elsevierStylePara elsevierViewall">After ten days in the hospital, the patient developed fever (38<span class="elsevierStyleHsp" style=""></span>°C), night sweats, malaise and asthenia. Based on the recent diagnosis of disseminated histoplasmosis, treatment with intravenous liposomal amphotericin B (3<span class="elsevierStyleHsp" style=""></span>mg/kg/day) was initiated with daily renal function measurements, while maintaining the TB treatment. A new nasopharyngeal swab was collected for SARS-CoV-2 detection, which was not detectable by RT-PCR.</p><p id="par0090" class="elsevierStylePara elsevierViewall">During his hospital stay, on June 16, due to a worsening of the symptoms, and chest CT findings (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>c), a new nasopharyngeal swab sample for SARS-CoV-2 detection was performed in the context of the COVID-19 pandemic, and viral RNA was detected.</p><p id="par0095" class="elsevierStylePara elsevierViewall">The patient's immunosuppressive regimen was changed, everolimus was discontinued, mycophenolate mofetil was reduced and meprednisone was increased. The patient received convalescent plasma therapy (one unit, title 1:800 IgG), with good clinical evolution, afebrile, hemodynamically stable, eupneic, and without supplemental oxygen requirements.</p><p id="par0100" class="elsevierStylePara elsevierViewall">Two weeks later, liposomal amphotericin B therapy was switched to oral therapy with itraconazole 200<span class="elsevierStyleHsp" style=""></span>mg t.i.d. for three days, and 200<span class="elsevierStyleHsp" style=""></span>mg b.i.d. for one year<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a>.</p><p id="par0105" class="elsevierStylePara elsevierViewall">On July 4, the patient was discharged with favorable evolution, and SARS-CoV-2 RNA was detected in a nasopharyngeal swab sample until July 24.</p><p id="par0110" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a> summarizes the timeline of symptom onset, chest CT, laboratory data, and treatment.</p><p id="par0115" class="elsevierStylePara elsevierViewall">Cases of COVID-19-associated histoplasmosis have already been reported in a patient living with HIV and advanced immunosuppression<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">3,10</span></a>. Here, we are describing a new case of disseminated histoplasmosis with mucocutaneous and lung involvement in a renal transplant patient who acquired SARS-CoV-2 infection probably during hospitalization for his treatment with amphotericin B.</p><p id="par0120" class="elsevierStylePara elsevierViewall">Histoplasmosis is often mistaken for tuberculosis because this condition often shows similar chest CT images in patients with clinical epidemiological criteria. Furthermore, kidney transplant recipients seem to have greater predisposition to acquire tuberculosis<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">9</span></a>. In this case, the patient showed mucocutaneous lesions that led to the diagnosis of histoplasmosis. This mycosis has a low incidence rate in transplant recipients, and respiratory manifestations and cutaneous lesions are the most common<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a>.</p><p id="par0125" class="elsevierStylePara elsevierViewall">Finally, COVID-19 was suspected because, when the patient had already been diagnosed with histoplasmosis, on day 10 of the antifungal therapy, his respiratory symptoms had worsened. A new CT showed progression of abnormalities with unifocal and peripheral lesions in the right lung with a characteristic ground glass pattern compatible with coronavirus disease<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>.</p><p id="par0130" class="elsevierStylePara elsevierViewall">Histoplasmosis has often resulted in allograft loss and overall mortality<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">6</span></a>. Moreover, COVID-19 co-infection may be severe, requiring intensive care admission of kidney transplant recipients due to long-term immunosuppression<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a>. In the case reported here, the patient had a favorable outcome probably because histoplasmosis was rapidly diagnosed and treated. In addition, he was treated early, after the diagnosis of SARS-CoV-2, with convalescent plasma therapy in line with the management of COVID-19 in kidney transplant recipients published by some authors<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">11</span></a>.</p><p id="par0135" class="elsevierStylePara elsevierViewall">The molecular analysis of four genes using MLST identified the isolate as belonging to the LAmB clade, which did not surprise us since this clade is the predominant one in South America and the major clade circulating in Argentina<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a>.</p><p id="par0140" class="elsevierStylePara elsevierViewall">Twenty days after the last discharge, SARS-CoV-2 RNA was detected in a nasopharyngeal swab sample. This coincides with some authors who noted that in immunosuppressed renal transplant recipients SARS-CoV-2 viral shedding could be prolonged<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a>.</p><p id="par0145" class="elsevierStylePara elsevierViewall">The Centers for Disease Control and Prevention (CDC) listed patients requiring immunosuppressive therapy following organ transplantation, as being at high risk for severe SARS-CoV-disease. However, it is known that a low proportion of COVID-19 patients have post fungal co-infections<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a>; in this case, histoplasmosis was prior to the viral infection, and subsequent hospitalizations and discharges could have been the factors influencing the acquisition of COVID-19 infection, in addition to the immunosuppressive status.</p><p id="par0150" class="elsevierStylePara elsevierViewall">In the context of the COVID-19 pandemic it is important to pay attention to endemic mycoses such as histoplasmosis, since they exhibit respiratory symptoms that can be mistaken with viral or bacterial community-acquired pneumonia, and in pulmonary and disseminated histoplasmosis they can resemble other infections such as tuberculosis. To the best of our knowledge, this is the first report in the medical literature of COVID-19 associated with disseminated histoplasmosis in a renal transplant recipient. COVID-19 disease should be considered in patients with histoplasmosis, as well as other endemic mycoses and prolonged immunosuppression, particularly during the pandemic.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conflict of interest</span><p id="par0155" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:8 [ 0 => array:3 [ "identificador" => "xres1777042" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:3 [ "identificador" => "xres1777041" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1560249" "titulo" => "Keywords" ] 3 => array:3 [ "identificador" => "xres1777043" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0015" ] ] ] 4 => array:2 [ "identificador" => "xpalclavsec1560250" "titulo" => "Palabras clave" ] 5 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflict of interest" ] 6 => array:2 [ "identificador" => "xack627965" "titulo" => "Acknowledgments" ] 7 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2021-03-10" "fechaAceptado" => "2021-10-31" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1560249" "palabras" => array:6 [ 0 => "COVID-19" 1 => "Fungal infection" 2 => "<span class="elsevierStyleItalic">Histoplasma capsulatum</span>" 3 => "Renal transplant" 4 => "SARS-CoV-2" 5 => "Argentina" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1560250" "palabras" => array:6 [ 0 => "COVID-19" 1 => "Infección fúngica" 2 => "<span class="elsevierStyleItalic">Histoplasma capsulatum</span>" 3 => "Trasplante renal" 4 => "SARS-CoV-2" 5 => "Argentina" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">•</span><p id="par0005" class="elsevierStylePara elsevierViewall">First report of histoplasmosis and COVID-19 in a renal transplant recipient.</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">•</span><p id="par0010" class="elsevierStylePara elsevierViewall">Rapid diagnosis and correct treatment of clinically suspected histoplasmosis facilitates a positive patient's outcome.</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">•</span><p id="par0015" class="elsevierStylePara elsevierViewall">Histoplasmosis should be suspected as a differential diagnosis in patients with pneumonia in endemic areas.</p></li></ul></p></span>" ] "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We report a case of disseminated histoplasmosis and COVID-19 infection in a renal transplant recipient in Argentina. The patient exhibited respiratory symptoms, and a chest computed tomography scan (CT) showed multiple bilateral centrilobular opacities with a tree-in-bud pattern in both lobes. The patient was initially treated as having bacterial community-acquired pneumonia, and then tuberculosis. A month later, histoplasmosis was diagnosed, and <span class="elsevierStyleItalic">Histoplasma capsulatum</span> LAmB clade was isolated from sputum, skin and oral lesions. The patient was hospitalized and treatment was started with intravenous liposomal amphotericin B. During the course of the antifungal therapy the respiratory symptoms worsened, a new chest CT showed a unilateral lesion with a ground glass appearance and SARS-CoV-2 was detected in a new nasopharyngeal sample. In addition, plasma therapy was administered, and the immunosuppressive regimen was adjusted (everolimus was interrupted, mycophenolate mofetil reduced, and meprednisone increased). Finally, the patient's progress was favorable and was discharged after five days on oral itraconazole treatment for histoplasmosis.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Se presenta un caso de histoplasmosis diseminada e infección por COVID-19 en un paciente trasplantado renal en Argentina. El paciente presentó un cuadro clínico respiratorio, y la tomografía computarizada (TC) de tórax mostró múltiples opacidades centrolobulillares bilaterales con patrón de árbol en brote. El paciente fue tratado inicialmente con antibióticos para agentes causantes de neumonía bacteriana adquirida en la comunidad y luego como tuberculosis. Un mes después se le diagnosticó una histoplasmosis diseminada y el hongo fue aislado del esputo, la piel y la mucosa oral. El hongo fue tipificado molecularmente como <span class="elsevierStyleItalic">Histoplasma capsulatum</span> clado LAmB. El paciente fue hospitalizado y se inició tratamiento con anfotericina B liposomal vía intravenosa. Durante el transcurso de la terapia antifúngica los síntomas respiratorios del paciente empeoraron, una nueva TC de tórax mostró una lesión unilateral con apariencia de vidrio esmerilado y se detectó SARS-CoV-2 en el hisopado nasofaríngeo. El paciente fue tratado con plasmoterapia y se modificó el régimen de inmunosupresión (se interrumpió everolimus, se redujo micofenolato de mofetilo y se incrementó la meprednisona). La evolución del paciente fue favorable y fue dado de alta con tratamiento oral con itraconazol.</p></span>" ] ] "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" => 3448 "Ancho" => 2500 "Tamanyo" => 447324 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Timeline of symptom onset, chest CT, laboratory data, and treatment.</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" => 413 "Ancho" => 1750 "Tamanyo" => 91304 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Evolution of chest computed tomography images. Multiple bilateral centrilobular opacities, with tree-in-bud pattern during first hospitalization. Slight increase of multiple bilateral centrilobular opacities during second hospitalization. Follow-up CT image obtained 10 days later of the third hospitalization shows multifocal peripheral abnormalities (circle) with ground glass pattern involve right lung.</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" => 701 "Ancho" => 1250 "Tamanyo" => 127918 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Mucocutaneous lesions. a. Right peri-tonsillar pillar injury (circle). b. 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Denning" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.3390/jof4020051" "Revista" => array:4 [ "tituloSerie" => "J Fungi (Basel)" "fecha" => "2018" "volumen" => "24" "paginaInicial" => "51" ] ] ] ] ] ] 14 => array:3 [ "identificador" => "bib0150" "etiqueta" => "15" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Coronavirus disease 2019 pneumonia in immunosuppressed renal transplant recipients: a summary of 10 confirmed cases in Wuhan, China" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:19 [ 0 => "L. Zhu" 1 => "N. Gong" 2 => "B. Liu" 3 => "X. Lu" 4 => "D. Chen" 5 => "S. Chen" 6 => "H. Shu" 7 => "K. Ma" 8 => "X. Xu" 9 => "Z. Guo" 10 => "E. Lu" 11 => "D. Chen" 12 => "Q. Ge" 13 => "J. Cai" 14 => "J. Jiang" 15 => "L. Wei" 16 => "W. Zhang" 17 => "G. Chen" 18 => "Z. Chen" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.eururo.2020.03.039" "Revista" => array:6 [ "tituloSerie" => "Eur Urol" "fecha" => "2020" "volumen" => "77" "paginaInicial" => "748" "paginaFinal" => "754" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/32317180" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack627965" "titulo" => "Acknowledgments" "texto" => "<p id="par0160" class="elsevierStylePara elsevierViewall">We thank Liliana Guelfand and Mariana Andreani Hospital Fernández, CABA, Argentina for the Histoplasma urinary antigen detection.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/03257541/0000005400000003/v1_202209300808/S0325754121001218/v1_202209300808/en/main.assets" "Apartado" => array:4 [ "identificador" => "37861" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Microbiología clínica y enfermedades infecciosas" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/03257541/0000005400000003/v1_202209300808/S0325754121001218/v1_202209300808/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754121001218?idApp=UINPBA00004N" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 2 | 0 | 2 |
| 2024 October | 45 | 2 | 47 |
| 2024 September | 60 | 2 | 62 |
| 2024 August | 52 | 9 | 61 |
| 2024 July | 45 | 6 | 51 |
| 2024 June | 41 | 4 | 45 |
| 2024 May | 30 | 3 | 33 |
| 2024 April | 58 | 8 | 66 |
| 2024 March | 77 | 8 | 85 |
| 2024 February | 80 | 8 | 88 |
| 2024 January | 82 | 9 | 91 |
| 2023 December | 103 | 10 | 113 |
| 2023 November | 146 | 15 | 161 |
| 2023 October | 248 | 17 | 265 |
| 2023 September | 151 | 8 | 159 |
| 2023 August | 131 | 14 | 145 |
| 2023 July | 139 | 13 | 152 |
| 2023 June | 99 | 11 | 110 |
| 2023 May | 273 | 18 | 291 |
| 2023 April | 79 | 12 | 91 |
| 2023 March | 37 | 20 | 57 |
| 2023 February | 30 | 16 | 46 |
| 2023 January | 22 | 31 | 53 |
| 2022 December | 40 | 22 | 62 |
| 2022 November | 47 | 10 | 57 |
| 2022 October | 47 | 18 | 65 |
| 2022 September | 35 | 16 | 51 |
| 2022 August | 33 | 18 | 51 |
| 2022 July | 32 | 18 | 50 |
| 2022 June | 35 | 21 | 56 |
| 2022 May | 20 | 10 | 30 |
| 2022 April | 17 | 26 | 43 |
| 2022 March | 21 | 17 | 38 |
| 2022 February | 15 | 14 | 29 |
| 2022 January | 13 | 7 | 20 |
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