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Disease of Aquatic Organisms 128:73 Vol. 128: 73–79, 2018 DISEASES OF AQUATIC ORGANISMS Published March 22 https://doi.org/10.3354/dao03207 Dis Aquat Org NOTE Pulmonary and systemic fungal infections in an Atlantic spotted dolphin and a Bryde’s whale, Brazil Kátia R Groch1,*, Josué Díaz-Delgado1,2, Carlos Sacristán1, Denyiélim E. Oliveira3, Gabriela Souza3, Angélica M. Sánchez-Sarmiento1, Samira Costa-Silva1, Juliana Marigo1, Pedro V. Castilho3, Marta J. Cremer4, Aline Rodrigues Hoffmann2, Fernando Esperón5, José L. Catão-Dias1 1Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, SP 05508-270, Brazil 2Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77845, USA 3Departamento de Engenharia de Pesca, Universidade do Estado de Santa Catarina, Bairro Progresso, Laguna, SC 88.790-000, Brazil 4Laboratório de Nectologia, Universidade da Região de Joinville, UNIVILLE, São Francisco do Sul, SC 89240-000, Brazil 5Grupo de Epidemiología y Sanidad Ambiental, Centro de Investigación en Sanidad Animal (INIA-CISA), Valdeolmos, Madrid 28130, Spain ABSTRACT: We report the gross and microscopic findings and molecular identification of 2 cases of hyphate fungal infection in cetaceans from Brazil. The first case involved an adult male Atlantic spotted dolphin Stenella frontalis with localized pulmonary disease characterized by pyogranulo- matous and necrotizing bronchopneumonia with intralesional hyphae. The second case involved an adult male Bryde’s whale Balaenoptera edeni with orchitis, periorchitis, mesenteric lym- phadenitis and pyogranulomatous bronchopneumonia with intralesional hyphae. PCR analysis from the dolphin’s lung yielded Aspergillus fumigatus, and the fungus from the whale’s mesen- teric lymph node showed the greatest identity to Nanniziopsis obscura and Stagonosporopsis cucurbitacearum These cases represent the first reports of pulmonary aspergillosis by A. fumiga- tus in an Atlantic spotted dolphin and systemic mycosis by a possibly novel Onygenales in marine mammals. KEY WORDS: Marine mammal · Balaenoptera edeni · Stenella frontalis · Cetacean pathology · Fungal infection · Mycosis · Onygenales · Nannizziopsiaceae · Aspergillus Resale or republication not permitted without written consent of the publisher INTRODUCTION due to potential systemic involvement. Several fungi have been associated with superficial colo- Fungal infections are a relatively minor cause of nization and with cutaneous, subcutaneous and morbidity and mortality in free-ranging cetaceans deep infection (localized or disseminated) in ceta - when compared to viral and bacterial ailments; ceans (Reidarson et al. 2001). Occasionally, despite however, in captivity, mycosis incidence is higher isolation of potentially pathogenic fungi from and pharmacological treatment is often required bodily surfaces, mucocutaneous junctions, excreted *Corresponding author: [email protected] © Inter-Research 2018 · www.int-res.com 74 Dis Aquat Org 128: 73–79, 2018 products and internal mucosae, there is no evi- MATERIALS AND METHODS dence of clinical disease (Reidarson et al. 2001). Given their low transmissibility, mycoses are fre- A 1.79 m long, adult male Atlantic spotted dol- quently endemic. phin (Case 1) in poor nutritional status and mod - Most reported mycosis cases in cetaceans involve erate auto lysis was found stranded dead in La - the skin, the lungs and the central nervous system guna, Santa Catarina state (SC) (Brazil; 28° 28’ S, (CNS). Regardless of the primary infection site, 48° 45’ W), on 19 October 2016. A 13.12 m long, fungemia and dissemination are relatively common adult male Bryde’s whale (Case 2) in apparent sequelae (Reidarson et al. 2001, Abdo et al. 2012). good nutritional status and moderate autolysis was Although some fungi are known to act as primary found stranded dead in São Francisco do Sul, SC pathogens in cetaceans, e.g. Blastomyces dermati- (Brazil; 26° 13’ S, 48° 29’ W), on 23 June 2014. A tidis, Coccidioides immitis and Histoplasma capsula- standard necropsy was performed in both cases. tum (Reidarson et al. 2001, Miller et al. 2002), most Representative tissue samples from Case 1 (heart, fungal infections are regarded as opportunistic (Rei- lung, trachea, mediastinal and tracheobronchial darson et al. 2001, Mouton et al. 2015). The latter are lymph nodes, diaphragm, tongue, stomach, intes- often associated with inconspicuous or demonstrable tine, liver, kidney, urinary bladder, spleen, pancreas, immunosuppressive pathogens, such as cetacean testicle, epididymis, skin, rectus abdominis and morbillivirus (CeMV) (Domingo et al. 1992) and her- longissimus dorsi) and Case 2 (aorta, heart, lung, pesvirus (Abdo et al. 2012), xenobiotics (e.g. persist- baleen, tongue, gastric compartments, small and ent organic pollutants, inorganic compounds such as large intestine, mesenteric lymph nodes, testicle, heavy metals) (Mouton et al. 2015) and malnutrition optic nerve, skin, rectus abdominis and longissimus (Dagleish et al. 2008). dorsi) were collected and fixed in 10% neutral Fungi of varying medical importance in cetaceans buffered formalin. All these tissues were processed may include class Zygomycetes, e.g. Mucor sp. routinely and embedded in paraffin, and 5 µm sec- (Naota et al. 2009), Rhizomucor pusillus (Reidarson et tions were stained with hematoxylin and eosin al. 2001), Cunninghamella bertholletiae, Saksenaea (H&E) for microscopic analysis. Selected tissue sec- vasiformis and Apophysomyces elegans (Reidarson tions were also stained with Grocott and Gomori et al. 2001, Robeck & Dalton 2002); class Saccharo- methenamine silver (GMS), periodic acid-Schiff mycetes, e.g. Candida spp., mainly C. albicans (Rei- (PAS), Gram/Twort and Masson’s trichrome stains darson et al. 2001); class Eurotiomycetes, e.g. Asper - to better characterize the microscopic findings. gillus spp., mainly A. fumigatus, Cladophialophora For molecular analysis of fungi, frozen tissues in- bantiana, H. capsulatum (Reidarson et al. 2001), cluding lung (Cases 1 and 2) and mesenteric lymph Paraccocidioides brasiliensis (Lacazia loboi) (Vilela et node (Case 2), were selected. Briefly, the DNA was al. 2016), Coccidioides immitis, B. dermatitides and extracted from frozen tissues with a DNeasy Blood Trichophyton sp. (Reidarson et al. 2001); class Sor- & Tissue kit (Qiagen). A pan-polymerase chain re - dariomycetes, e.g. Fusarium spp. and Sporothrix action (pan-PCR) to amplify the internal transcribed schenckii (Reidarson et al. 2001); and class Tremel- spacer regions 1 and 2 (ITS-1 and ITS-2), including lomycetes, e.g. Cryptococcus neoformans var. neo- part of the 18S rRNA, the 5.8S rRNA and the formans and gattii (Reidarson et al. 2001, Miller et al. 26S rRNA genes, was performed (White et al. 1990, 2002) and Trichosporon pullulans (Reidarson et al. Gardes & Bruns 1993). After electrophoresis in 2001). 1.5% agarose gels, positive samples were identified Most descriptions of fungal infection in cetaceans through direct sequencing. Sequences were aligned have involved odontocetes; they are rarely reported on MEGA6, primer se quences were removed, and in mysticetes (Best & McCully 1979, McAloose et al. BLAST searches (www. ncbi. nlm. nih. gov/ blast/ Blast. 2016). This study describes the gross and microscopic cgi) of the edited sequences were performed. findings and molecular identification of 2 cases of MEGA6 was selected to establish the identity of the hyphate fungal infection involving an Atlantic spot- sequenced material based on the p-distance be- ted dolphin Stenella frontalis and a Bryde’s whale tween the obtained se quences and the closest se - Balaenoptera edeni from Brazil. These cases repre- quences available in GenBank. Additionally, forma- sent the first reports of pulmonary aspergillosis by lin-fixed paraffin-em bedded (FFPE) tissue sections A. fumigatus in an Atlantic spotted dolphin and from the lung, peritesticular mass and mesenteric systemic mycosis by a possibly novel Onygenales lymph node from case 2 were used for a panfungal in marine mammals. PCR targeting the ITS1 region, followed by sequen- Groch et al.: Fungal infections in Atlantic dolphin and whale 75 cing (Meason-Smith et al. 2017). Given potential bronchial/bronchiolar obliteration, chondritis, chron- immunosuppressive effects on host and occasional dronecrosis and chondrolysis with intralesional non- reports linking CeMV with fungal coinfections, con- pigmented hyphae (Fig. 1B). Hyphae were 3−10 µm ventional PCR analysis for CeMV was performed. (in width) × 7−15 µm (in length), displayed an arboriz- RNA was ex tracted from frozen tissue samples ing growth pattern with progressive dicho tomous (Case 1: lung, kidney; Case 2: lung and mesenteric acute-angle branching, regular septation and paral- lymph node) by using TRIzol Reagent (Life Tech- lel, faded-to-hyalinized walls (Fig. 1Bi). Rarely, in nologies) according to the manufacturer’s instruc- areas of mycelial growth, hyphae were tangled, bul- tions. Reverse transcription PCR was performed tar- bous and distorted. Arteritis and phlebitis with fun- geting a conserved fragment of the phosphoprotein gal angioinvasion, vascular thrombosis and ischemic gene following a previously described method (Bar- infarction were also noted. Varying degrees of fibro- rett et al. 1993). sis surrounded these inflammatory foci. In the tra- cheobronchial and mediastinal lymph nodes there was marked, diffuse
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