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

  • Selwyn Arlington HeadleyEmail author
  • Mariana de Mello Zanim Michelazzo
  • Bruno Elias
  • Nayara Emily Viana
  • Yuri Lima Pereira
  • Lucienne Garcia Pretto-Giordano
  • Jhonata Fragoso da Silva
  • Felipe Eduardo Scardovelli da Silva
  • Laurival Antonio Vilas-Boas
  • Karina Keller Marques da Costa Flaiban
  • Amauri Alcindo Alfieri
  • Lucas Alécio Gomes
Veterinary Microbiology - Research Paper


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.


Choroid plexitis Cladosporiosis Dematiaceous fungi Diagnostic pathology Dog Pleocytosis Thromboembolism Ventriculitis 



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.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. 1.
    Brandt ME, Warnock DW (2003) Epidemiology, clinical manifestations, and therapy of infections caused by dematiaceous fungi. J Chemother 15(sup2):36–47CrossRefGoogle Scholar
  2. 2.
    Wong EH, Revankar SG (2016) Dematiaceous molds. Infect Dis Clin N Am 30(1):165–178CrossRefGoogle Scholar
  3. 3.
    Revankar SG, Sutton DA (2010) Melanized fungi in human disease. Clin Microbiol Rev 23(4):884–928CrossRefGoogle Scholar
  4. 4.
    Seyedmousavi S, Guillot J, de Hoog GS (2013) Phaeohyphomycoses, emerging opportunistic diseases in animals. Clin Microbiol Rev 26(1):19–35CrossRefGoogle Scholar
  5. 5.
    Revankar SG, Sutton DA, Rinaldi MG (2004) Primary central nervous system phaeohyphomycosis: a review of 101 cases. Clin Infect Dis 38(2):206–216CrossRefGoogle Scholar
  6. 6.
    Revankar SG, Patterson JE, Sutton DA, Pullen R, Rinaldi MG (2002) Disseminated phaeohyphomycosis: review of an emerging mycosis. Clin Infect Dis 34(4):467–476CrossRefGoogle Scholar
  7. 7.
    Dillehay DL, Ribas JL, Newton JC Jr, Kwapien RP (1987) Cerebral phaeohyphomycosis in two dogs and a cat. Vet Pathol 24(2):192–194CrossRefGoogle Scholar
  8. 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):59–63CrossRefGoogle Scholar
  9. 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):754–757CrossRefGoogle Scholar
  10. 10.
    Uchôa ICP, Santos JRS, APd S et al (2012) Feo-hifomicose sistêmica em cão. Cienc Rural 42:670–674CrossRefGoogle Scholar
  11. 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 15:28–32CrossRefGoogle Scholar
  12. 12.
    Spano M, Zuliani D, Peano A, Bertazzolo W (2018) Cladosporium cladosporioides-complex infection in a mixed-breed dog. Vet Clin Pathol 47(1):150–153CrossRefGoogle Scholar
  13. 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):70–72CrossRefGoogle Scholar
  14. 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):50–53CrossRefGoogle Scholar
  15. 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):295–297CrossRefGoogle Scholar
  16. 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):194–197CrossRefGoogle Scholar
  17. 17.
    Coles BM, Stevens DR, Hunter RL (1978) Equine nodular dermatitis associated with Alternaria tenuis infection. Vet Pathol 15(6):779–780CrossRefGoogle Scholar
  18. 18.
    Genovese LM, Whitbread TJ, Campbell CK (2001) Cutaneous nodular phaeohyphomycosis in five horses associated with Alternaria alternata infection. Vet Rec 148(2):55–56CrossRefGoogle Scholar
  19. 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):3047–3053CrossRefGoogle Scholar
  20. 20.
    Haligur M, Ozmen O, Dorrestein GM (2010) Fatal systemic cladosporiosis in a merino sheep flock. Mycopathologia. 170(6):411–415CrossRefGoogle Scholar
  21. 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):123–128CrossRefGoogle Scholar
  22. 22.
    Schroeder H, Jardine JE, Davis V (1994) Systemic phaeohyphomycosis caused by Xylohypha bantiana in a dog. J S Afr Vet Assoc 65(4):175–178Google Scholar
  23. 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):165–187CrossRefGoogle Scholar
  24. 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):724–727CrossRefGoogle Scholar
  25. 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 315–322Google Scholar
  26. 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):1323–1330Google Scholar
  27. 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):61–66CrossRefGoogle Scholar
  28. 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):13477CrossRefGoogle Scholar
  29. 29.
    Headley SA, Graça DL (2000) Canine distemper: epidemiological findings of 250 cases. Braz J Vet Res Anim Sci 37:136–140CrossRefGoogle Scholar
  30. 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):1945–1978CrossRefGoogle Scholar
  31. 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):129–135CrossRefGoogle Scholar
  32. 32.
    Guarner J, Brandt ME (2011) Histopathologic diagnosis of fungal infections in the 21st century. Clin Microbiol Rev 24(2):247–280CrossRefGoogle Scholar
  33. 33.
    Sandoval-Denis M, Gene J, Sutton DA et al (2016) New species of Cladosporium associated with human and animal infections. Persoonia. 36:281–298CrossRefGoogle Scholar
  34. 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):2990–3000CrossRefGoogle Scholar
  35. 35.
    Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401CrossRefGoogle Scholar
  36. 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):63–83CrossRefGoogle Scholar
  37. 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):489–496CrossRefGoogle Scholar
  38. 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):e6686CrossRefGoogle Scholar
  39. 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 304–330Google Scholar
  40. 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):282–288CrossRefGoogle Scholar
  41. 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 1691–1732CrossRefGoogle Scholar
  42. 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–DD05Google Scholar
  43. 43.
    Colombo AC, Rodrigues ML (2015) Fungal colonization of the brain: anatomopathological aspects of neurological cryptococcosis. An Acad Bras Cienc 87(2 Suppl):1293–1309CrossRefGoogle Scholar
  44. 44.
    Gaunt MC, Taylor SM, Kerr ME (2009) Central nervous system blastomycosis in a dog. Can Vet J 50(9):959–962Google Scholar
  45. 45.
    Riet-Correa F, Krockenberger M, Dantas AF, Oliveira DM (2011) Bovine cryptococcal meningoencephalitis. J Vet Diagn Investig 23(5):1056–1060CrossRefGoogle Scholar
  46. 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):69–73Google Scholar
  47. 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):725–728CrossRefGoogle Scholar
  48. 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 9:80CrossRefGoogle Scholar
  49. 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):273–276Google Scholar
  50. 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):117–122CrossRefGoogle Scholar
  51. 51.
    Habibi A, Safaiefarahani B (2018) Indoor damp surfaces harbor molds with clinical significance. Curr Med Mycol 4(3):1–9Google Scholar
  52. 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):7–14CrossRefGoogle Scholar
  53. 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):2055116916677935Google Scholar
  54. 54.
    (2017) Chapter 12 - Parvoviridae. In: MacLachlan NJ, Dubovi EJ (ed) Fenner’s Veterinary Virology, 5th edn. Boston, Academic, pp 245–257Google Scholar
  55. 55.
    Revankar SG (2007) Dematiaceous fungi. Mycoses. 50(2):91–101CrossRefGoogle Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Selwyn Arlington Headley
    • 1
    • 2
    Email author
  • Mariana de Mello Zanim Michelazzo
    • 1
  • Bruno Elias
    • 3
  • Nayara Emily Viana
    • 1
  • Yuri Lima Pereira
    • 4
  • Lucienne Garcia Pretto-Giordano
    • 5
  • Jhonata Fragoso da Silva
    • 6
  • Felipe Eduardo Scardovelli da Silva
    • 6
  • Laurival Antonio Vilas-Boas
    • 6
  • Karina Keller Marques da Costa Flaiban
    • 4
  • Amauri Alcindo Alfieri
    • 7
  • Lucas Alécio Gomes
    • 3
  1. 1.Laboratory of Animal Pathology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  2. 2.Tissue Processing Unit, Multi-User Animal Health Laboratory, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  3. 3.Small Animal Internal Medicine, Department of Veterinary ClinicsUniversidade Estadual de LondrinaLondrinaBrazil
  4. 4.Laboratory of Clinical Pathology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  5. 5.Laboratory of Mycology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  6. 6.Laboratory of Genetics and Bacterial Taxonomy, Department of General BiologyUniversidade Estadual de LondrinaLondrinaBrazil
  7. 7.Molecular Biology Unit, Multi-User Animal Health Laboratory, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil

Personalised recommendations