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Disseminated melanized fungal infection due to Cladosporium halotolerans in a dog coinfected with canine adenovirus-1 and canine parvovirus-2

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Abstract

This report presents the pathologic findings associated with disseminated infection due to Cladosporium halotolerans in a dog that was simultaneously infected with canine adenovirus-1 (CAdV-1) and canine parvovirus-2 (CPV-2). A 12-year-old, mixed breed dog, with a clinical history of neurological manifestations was submitted for routine autopsy due to poor prognosis. The principal pathologic findings were mycotic necrotizing nephritis, hepatitis, and splenitis with embolic dissemination to the brain resulting in mycotic necrotizing meningoencephalitis, ventriculitis, choroid plexitis, and obstructive hydrocephalus associated with intralesional and intravascular septate pigmented fungi. PCR and sequencing of the ITS region of fungi revealed that the intralesional fungal organisms had 82% nucleotide identity with members of the Cladosporium sphaerospermum complex of organisms. However, a PCR assay and sequencing of the beta tubulin gene confirmed that the organism identified in this dog had 100% nucleotide sequence identity with C. halotolerans. Using immunohistochemistry, intralesional antigens of CAdV-1 were identified within the epithelial cells of the liver and lungs; there was positive immunolabeling for CPV-2 antigens in degenerated cardiomyocytes. These findings confirmed the active participation of C. halotolerans in the development of disseminated cladosporiosis in this dog and represent a rare occurrence of concomitant infection with CAdV-1 and CPV-2.

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References

  1. Brandt ME, Warnock DW (2003) Epidemiology, clinical manifestations, and therapy of infections caused by dematiaceous fungi. J Chemother 15(sup2):36–47

    Article  PubMed  Google Scholar 

  2. Wong EH, Revankar SG (2016) Dematiaceous molds. Infect Dis Clin N Am 30(1):165–178

    Article  Google Scholar 

  3. Revankar SG, Sutton DA (2010) Melanized fungi in human disease. Clin Microbiol Rev 23(4):884–928

    Article  PubMed  PubMed Central  Google Scholar 

  4. Seyedmousavi S, Guillot J, de Hoog GS (2013) Phaeohyphomycoses, emerging opportunistic diseases in animals. Clin Microbiol Rev 26(1):19–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Revankar SG, Sutton DA, Rinaldi MG (2004) Primary central nervous system phaeohyphomycosis: a review of 101 cases. Clin Infect Dis 38(2):206–216

    Article  PubMed  Google Scholar 

  6. Revankar SG, Patterson JE, Sutton DA, Pullen R, Rinaldi MG (2002) Disseminated phaeohyphomycosis: review of an emerging mycosis. Clin Infect Dis 34(4):467–476

    Article  PubMed  Google Scholar 

  7. Dillehay DL, Ribas JL, Newton JC Jr, Kwapien RP (1987) Cerebral phaeohyphomycosis in two dogs and a cat. Vet Pathol 24(2):192–194

    Article  CAS  PubMed  Google Scholar 

  8. Poutahidis T, Angelopoulou K, Karamanavi E, Polizopoulou ZS, Doulberis M, Latsari M, Kaldrymidou E (2009) Mycotic encephalitis and nephritis in a dog due to infection with Cladosporium cladosporioides. J Comp Pathol 140(1):59–63

    Article  CAS  PubMed  Google Scholar 

  9. Giri DK, Sims WP, Sura R, Cooper JJ, Gavrilov BK, Mansell J (2011) Cerebral and renal phaeohyphomycosis in a dog infected with Bipolaris species. Vet Pathol 48(3):754–757

    Article  CAS  PubMed  Google Scholar 

  10. Uchôa ICP, Santos JRS, APd S et al (2012) Feo-hifomicose sistêmica em cão. Cienc Rural 42:670–674

    Article  Google Scholar 

  11. Rothenburg LS, Snider TA, Wilson A, Confer AW, Ramachandran A, Mani R, Rizzi T, Nafe L (2017) Disseminated phaeohyphomycosis in a dog. Med Mycol Case Rep 15:28–32

    Article  PubMed  PubMed Central  Google Scholar 

  12. Spano M, Zuliani D, Peano A, Bertazzolo W (2018) Cladosporium cladosporioides-complex infection in a mixed-breed dog. Vet Clin Pathol 47(1):150–153

    Article  PubMed  Google Scholar 

  13. Bouljihad M, Lindeman CJ, Hayden DW (2002) Pyogranulomatous meningoencephalitis associated with dematiaceous fungal (Cladophialophora bantiana) infection in a domestic cat. J Vet Diagn Investig 14(1):70–72

    Article  Google Scholar 

  14. Elies L, Balandraud V, Boulouha L, Crespeau F, Guillot J (2003) Fatal systemic phaeohyphomycosis in a cat due to Cladophialophora bantiana. J Vet Med A Physiol Pathol Clin Med 50(1):50–53

    Article  CAS  PubMed  Google Scholar 

  15. Simmons JK, McManamon R, Rech RR, Phillips AE, Howerth EW (2010) Pathology in practice. Necrotizing pyogranulomatous meningoencephalitis with intralesional fungal hyphae, consistent with Cladophialophora bantiana. J Am Vet Med Assoc 236(3):295–297

    Article  PubMed  Google Scholar 

  16. Evans N, Gunew M, Marshall R, Martin P, Barrs V (2011) Focal pulmonary granuloma caused by Cladophialophora bantiana in a domestic short haired cat. Med Mycol 49(2):194–197

    Article  PubMed  Google Scholar 

  17. Coles BM, Stevens DR, Hunter RL (1978) Equine nodular dermatitis associated with Alternaria tenuis infection. Vet Pathol 15(6):779–780

    Article  CAS  PubMed  Google Scholar 

  18. Genovese LM, Whitbread TJ, Campbell CK (2001) Cutaneous nodular phaeohyphomycosis in five horses associated with Alternaria alternata infection. Vet Rec 148(2):55–56

    Article  CAS  PubMed  Google Scholar 

  19. Rantala M, Attia S, Koukila-Kahkola P et al (2015) Cladophialophora bantiana as an emerging pathogen in animals: case report of equine endometritis and review of the literature. J Clin Microbiol 53(9):3047–3053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Haligur M, Ozmen O, Dorrestein GM (2010) Fatal systemic cladosporiosis in a merino sheep flock. Mycopathologia. 170(6):411–415

    Article  PubMed  Google Scholar 

  21. Domiciano IG, Domit C, Trigo CC, de Alcântara BK, Headley SA, Bracarense APFRL (2014) Phaeohyphomycoses in a free-ranging loggerhead turtle (Caretta caretta) from Southern Brazil. Mycopathologia. 178(1–2):123–128

    Article  PubMed  Google Scholar 

  22. Schroeder H, Jardine JE, Davis V (1994) Systemic phaeohyphomycosis caused by Xylohypha bantiana in a dog. J S Afr Vet Assoc 65(4):175–178

    CAS  PubMed  Google Scholar 

  23. Seyedmousavi S, Bosco SMG, de Hoog S, Ebel F, Elad D, Gomes RR, Jacobsen ID, Jensen HE, Martel A, Mignon B, Pasmans F, Piecková E, Rodrigues AM, Singh K, Vicente VA, Wibbelt G, Wiederhold NP, Guillot J (2018) Fungal infections in animals: a patchwork of different situations. Med Mycol 56(suppl_1):165–187

    Article  PubMed  Google Scholar 

  24. Coldrick O, Brannon CL, Kydd DM, Pierce-Roberts G, Borman AM, Torrance AG (2007) Fungal pyelonephritis due to Cladophialophora bantiana in a cat. Vet Rec. 161(21):724–727

    Article  CAS  PubMed  Google Scholar 

  25. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  26. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61(4):1323–1330

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Headley SA, Pretto-Giordano LG, Lima SC, Suhett WG, Pereira AHT, Freitas LA, Suphoronski SA, Oliveira TES, Alfieri AF, Pereira EC, Vilas-Boas LA, Alfieri AA (2017) Pneumonia due to Talaromyces marneffei in a dog from southern Brazil with concomitant canine distemper virus infection. J Comp Pathol 157(1):61–66

    Article  CAS  PubMed  Google Scholar 

  28. Headley SA, Oliveira TES, Pereira AHT, Moreira JR, Michelazzo MMZ, Pires BG, Marutani VHB, Xavier AAC, di Santis GW, Garcia JL, Alfieri AA (2018) Canine morbillivirus (canine distemper virus) with concomitant canine adenovirus, canine parvovirus-2, and Neospora caninum in puppies: a retrospective immunohistochemical study. Sci Rep 8(1):13477

    Article  PubMed  PubMed Central  Google Scholar 

  29. Headley SA, Graça DL (2000) Canine distemper: epidemiological findings of 250 cases. Braz J Vet Res Anim Sci 37:136–140

    Article  Google Scholar 

  30. Headley SA, Amude AM, Alfieri AF, Bracarense APRFL, Alfieri AA (2012) Epidemiological features and the neuropathological manifestations of canine distemper virus-induced infections in Brazil: a review. Semina Cienc Agrar 33(5):1945–1978

    Article  Google Scholar 

  31. Headley SA, Alfieri AA, Fritzen JT et al (2013) Concomitant canine distemper, infectious canine hepatitis, canine parvoviral enteritis, canine infectious tracheobronchitis, and toxoplasmosis in a puppy. J Vet Diagn Investig 25(1):129–135

    Article  Google Scholar 

  32. Guarner J, Brandt ME (2011) Histopathologic diagnosis of fungal infections in the 21st century. Clin Microbiol Rev 24(2):247–280

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sandoval-Denis M, Gene J, Sutton DA et al (2016) New species of Cladosporium associated with human and animal infections. Persoonia. 36:281–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sandoval-Denis M, Sutton DA, Martin-Vicente A, Cano-Lira JF, Wiederhold N, Guarro J, Gené J (2015) Cladosporium species recovered from clinical samples in the United States. J Clin Microbiol 53(9):2990–3000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bentley RT, Taylor AR, Thomovsky SA (2018) Fungal infections of the central nervous system in small animals: clinical features, diagnosis, and management. Vet Clin North Am Small Anim Pract 48(1):63–83

    Article  PubMed  Google Scholar 

  37. Bentley RT, Reese MJ, Heng HG, Lin TL, Shimonohara N, Fauber A (2013) Ependymal and periventricular magnetic resonance imaging changes in four dogs with central nervous system blastomycosis. Vet Radiol Ultrasound 54(5):489–496

    Article  PubMed  Google Scholar 

  38. Egelund GB, Ertner G, Kristensen LK et al (2017) Cerebrospinal fluid pleocytosis in infectious and noninfectious central nervous system disease: a retrospective cohort study. Medicine 96(18):e6686

    Article  Google Scholar 

  39. Rakich PM, Latimer KS (2003) Cytology. In: Latimer KS, Mahaffey EA, Prasse KW (eds) Duncan and Prasse’s Veterinary Laboratory Medicine: Clinical Pathology. Iowa State Press, Ames, pp 304–330

    Google Scholar 

  40. Garg N, Devi I, Vajramani G, Nagarathna S, Sampath S, Chandramouli BA, Chandramuki A, Shankar SK (2007) Central nervous system cladosporiosis: an account of ten culture-proven cases. Neurol India 55(3):282–288

    Article  PubMed  Google Scholar 

  41. Sharma RR, Pawar SJ, Lad SD, Mishra GP, Netalkar AS, Rege S (2012) Chapter 149 - fungal infections of the central nervous system. In: Quiñones-Hinojosa A (ed) Schmidek and sweet operative neurosurgical techniques, 6th edn. W.B. Saunders, Philadelphia, pp 1691–1732

    Chapter  Google Scholar 

  42. Suri P, Chhina DK, Kaushal V, Kaushal RK, Singh J (2014) Cerebral phaeohyphomycosis due to Cladophialophora bantiana – a case report and review of literature from India. J Clin Diagn Res 8(4):DD01–DD05

    PubMed  PubMed Central  Google Scholar 

  43. Colombo AC, Rodrigues ML (2015) Fungal colonization of the brain: anatomopathological aspects of neurological cryptococcosis. An Acad Bras Cienc 87(2 Suppl):1293–1309

    Article  PubMed  Google Scholar 

  44. Gaunt MC, Taylor SM, Kerr ME (2009) Central nervous system blastomycosis in a dog. Can Vet J 50(9):959–962

    PubMed  PubMed Central  Google Scholar 

  45. Riet-Correa F, Krockenberger M, Dantas AF, Oliveira DM (2011) Bovine cryptococcal meningoencephalitis. J Vet Diagn Investig 23(5):1056–1060

    Article  Google Scholar 

  46. Headley SA, Pimentel LA, Michelazzo MZ, Toma HS, Pretto-Giordano LG, Marcasso RA, Amude AM, Oliveira TE, Santos MD, Krockenberger M (2019) Pathological, histochemical and immunohistochemical findings associated with caprine pulmonary and encephalitic cryptococcosis. J Vet Diagn Investig 31(1):69–73

  47. Curtis B, Hollinger C, Lim A, Kiupel M (2017) Embolic mycotic encephalitis in a cow following Mortierella wolfii infection of a surgery site. J Vet Diagn Investig 29(5):725–728

    Article  Google Scholar 

  48. Schwerk C, Tenenbaum T, Kim KS, Schroten H (2015) The choroid plexus—a multi-role player during infectious diseases of the CNS. Front Cell Neurosci 9:80

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kovoor JM, Mahadevan A, Narayan JP et al (2002) Cryptococcal choroid plexitis as a mass lesion: MR imaging and histopathologic correlation. AJNR Am J Neuroradiol 23(2):273–276

    PubMed  PubMed Central  Google Scholar 

  50. Graciela Agar CH, Orozco Rosalba V, Macias Ivan C et al (2009) Cryptococcal choroid plexitis an uncommon fungal disease. Case report and review. Can J Neurol Sci 36(1):117–122

    Article  PubMed  Google Scholar 

  51. Habibi A, Safaiefarahani B (2018) Indoor damp surfaces harbor molds with clinical significance. Curr Med Mycol 4(3):1–9

    PubMed  PubMed Central  Google Scholar 

  52. Ascioglu S, Rex JH, de Pauw B, Bennett JE, Bille J, Crokaert F, Denning DW, Donnelly JP, Edwards JE, Erjavec Z, Fiere D, Lortholary O, Maertens J, Meis JF, Patterson TF, Ritter J, Selleslag D, Shah PM, Stevens DA, Walsh TJ, Invasive Fungal Infections Cooperative Group of the European Organization for Research and Treatment of Cancer, Mycoses Study Group of the National Institute of Allergy and Infectious Diseases (2002) Defining opportunistic invasive fungal infections in immunocompromised patients with cancer and hematopoietic stem cell transplants: an international consensus. Clin Infect Dis 34(1):7–14

    Article  CAS  PubMed  Google Scholar 

  53. Russell EB, Gunew MN, Dennis MM, Halliday CL (2016) Cerebral pyogranulomatous encephalitis caused by Cladophialophora bantiana in a 15-week-old domestic shorthair kitten. JFMS Open Rep 2(2):2055116916677935

    PubMed  PubMed Central  Google Scholar 

  54. (2017) Chapter 12 - Parvoviridae. In: MacLachlan NJ, Dubovi EJ (ed) Fenner’s Veterinary Virology, 5th edn. Boston, Academic, pp 245–257

  55. Revankar SG (2007) Dematiaceous fungi. Mycoses. 50(2):91–101

    Article  PubMed  Google Scholar 

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Acknowledgements

Selwyn A. Headley and Amauri A. Alfieri are recipients of the National Council for Scientific and Technological Development (CNPq; Brazil) fellowships and grants. The authors thank the owner of this dog for permission to use this animal during this report and Dr. Kerlei Cristina Medici for the realization of the beta-tubulin PCR assay.

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Authors and Affiliations

  1. Laboratory of Animal Pathology, Department of Veterinary Preventive Medicine, Universidade Estadual de Londrina, Rodovia Celso Garcia Cid, PR 445 Km 380, Campus Universitário, PO Box 10.011, Londrina, Paraná, 86057-970, Brazil

    Selwyn Arlington Headley, Mariana de Mello Zanim Michelazzo & Nayara Emily Viana

  2. Tissue Processing Unit, Multi-User Animal Health Laboratory, Department of Veterinary Preventive Medicine, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Selwyn Arlington Headley

  3. Small Animal Internal Medicine, Department of Veterinary Clinics, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Bruno Elias & Lucas Alécio Gomes

  4. Laboratory of Clinical Pathology, Department of Veterinary Preventive Medicine, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Yuri Lima Pereira & Karina Keller Marques da Costa Flaiban

  5. Laboratory of Mycology, Department of Veterinary Preventive Medicine, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Lucienne Garcia Pretto-Giordano

  6. Laboratory of Genetics and Bacterial Taxonomy, Department of General Biology, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Jhonata Fragoso da Silva, Felipe Eduardo Scardovelli da Silva & Laurival Antonio Vilas-Boas

  7. Molecular Biology Unit, Multi-User Animal Health Laboratory, Department of Veterinary Preventive Medicine, Universidade Estadual de Londrina, Londrina, Paraná, Brazil

    Amauri Alcindo Alfieri

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  1. Selwyn Arlington Headley
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Correspondence to Selwyn Arlington Headley.

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Headley, S.A., de Mello Zanim Michelazzo, M., Elias, B. et al. Disseminated melanized fungal infection due to Cladosporium halotolerans in a dog coinfected with canine adenovirus-1 and canine parvovirus-2. Braz J Microbiol 50, 859–870 (2019). https://doi.org/10.1007/s42770-019-00082-6

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