Mycopathologia

, Volume 182, Issue 3–4, pp 425–434 | Cite as

Paracoccidioides brasiliensis-associated dermatitis and lymphadenitis in a dog

  • Selwyn Arlington Headley
  • Lucienne Garcia Pretto-Giordano
  • Giovana Wingeter Di Santis
  • Lucas Alécio Gomes
  • Rafaela Macagnan
  • Daniela Farias da Nóbrega
  • Katherine Moura Leite
  • Brígida Kussumoto de Alcântara
  • Eiko Nakagawa Itano
  • Amauri Alcindo Alfieri
  • Mario Augusto Ono
Article

Abstract

Paracoccidioidomycosis (PCM) is an endemic disease of humans from Latin America that is caused by Paracoccidioides brasiliensis and P. lutzii, with most cases of PCM in domestic animals being associated with P. brasiliensis. This study presents the clinical, cytological, mycological, serological, and molecular findings associated with P. brasiliensis in a dog from Southern Brazil. Fine needle biopsies were collected from the skin and several lymph nodes of a 5-year-old female Labrador dog that had enlargement of most superficial lymph nodes. Cytology of the skin and lymph nodes revealed pyogranulomatous dermatitis and lymphadenitis associated with fine-necked, budding fungal structures consistent with the Paracoccidioides genus of organisms; mycological culture derived from the lymph node aspirate demonstrated similar budding structures. Serological assays using exoantigens obtained from the fungal culture demonstrated that the fungal organisms derived from the lymph node were antigenically similar to P. brasiliensis by immunodiffusion and Western blot. A PCR assay, using the fungal culture as input, amplified a partial segment of the internal transcribed spacer 1 and 2 regions of P. brasiliensis; direct sequencing and phylogenetic analyses confirmed the PCR product as P. brasiliensis. The combined cytological, mycological, serological, and molecular findings confirmed a diagnosis of fungal dermatitis and lymphadenitis due to P. brasiliensis in this dog. This case represents the third description of clinical PCM in dogs and the first confirmation of mycotic dermatitis associated with P. brasiliensis in this species. The participation of dogs in the possible dissemination of PCM is reviewed, and it is proposed that dogs are probable accidental hosts in the epidemiological cycle associated with P. brasiliensis.

Keywords

Canine paracoccidioidomycosis Fungal dermatitis Cytological diagnosis Epidemiology 

Notes

Acknowledgments

Selwyn A. Headley, Amauri A. Alfieri, and Mario Augusto Ono are recipients of the National Council for Scientific and Technological Development (CNPq; Brazil) fellowships and grants. The authors thank the owners of this dog for the usage during this investigation. We express sincere appreciation and gratitude to Mrs Eliana Celia Pereira, technician Laboratory of Animal Mycology, Universidade Estadual de Londrina, for the preparation of the fungal culture used during this investigation.

Compliance with Ethical Standards

Conflict of interest

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

  1. 1.
    Teixeira Mde M, Theodoro RC, Oliveira FF, Machado GC, Hahn RC, Bagagli E, et al. Paracoccidioides lutzii sp. nov.: biological and clinical implications. Med Mycol. 2014;52(1):19–28.PubMedGoogle Scholar
  2. 2.
    Teixeira MM, Theodoro RC, Nino-Vega G, Bagagli E, Felipe MSS. Paracoccidioides species complex: ecology, phylogeny, sexual reproduction, and virulence. PLoS Pathog. 2014;10(10):e1004397.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bocca AL, Amaral AC, Teixeira MM, Sato PK, Shikanai-Yasuda MA, Soares Felipe MS. Paracoccidioidomycosis: eco-epidemiology, taxonomy and clinical and therapeutic issues. Future Microbiol. 2013;8(9):1177–91.CrossRefPubMedGoogle Scholar
  4. 4.
    Shikanai-Yasuda MA, Telles Filho F, Mendes RP, Colombo AL, Moretti ML. Group of Consultants on the Guidelines in Paracoccidioidomycosis. Rev Soc Bras Med Trop. 2006;39:297–310.Google Scholar
  5. 5.
    Fontana FF, dos Santos CT, Esteves FM, Rocha A, Fernandes GF, do Amaral CC, et al. Seroepidemiological survey of paracoccidioidomycosis infection among urban and rural dogs from Uberaba, Minas Gerais, Brazil. Mycopathologia. 2010;169(3):159–65.CrossRefPubMedGoogle Scholar
  6. 6.
    Ono MA, Bracarense AP, Morais HS, Trapp SM, Belitardo DR, Camargo ZP. Canine paracoccidioidomycosis: a seroepidemiologic study. Med Mycol. 2001;39(3):277–82.CrossRefPubMedGoogle Scholar
  7. 7.
    Silveira LH, Domingos IH, Kouchi K, Itano EN, Silva EA, Landgraf VO, et al. Serological detection of antibodies against Paracoccidioides brasiliensis in dogs with leishmaniasis. Mycopathologia. 2006;162(5):325–9.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Oliveira GG, Belitardo DR, Balarin MR, Freire RL, Camargo ZP, Ono MA. Serological survey of paracoccidioidomycosis in cats. Mycopathologia. 2013;176(3–4):299–302.CrossRefPubMedGoogle Scholar
  9. 9.
    Oliveira GG, Navarro IT, Freire RL, Belitardo DR, Silveira LH, Camargo ZP, et al. Serological survey of paracoccidioidomycosis in sheep. Mycopathologia. 2012;173(1):63–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Oliveira GG, Silveira LH, Itano EN, Soares RM, Freire RL, Watanabe MA, et al. Serological evidence of Paracoccidioides brasiliensis infection in chickens from Parana and Mato Grosso do Sul States, Brazil. Mycopathologia. 2011;171(3):197–202.CrossRefPubMedGoogle Scholar
  11. 11.
    Silveira LH, Paes RC, Medeiros EV, Itano EN, Camargo ZP, Ono MA. Occurrence of antibodies to Paracoccidioides brasiliensis in dairy cattle from Mato Grosso do Sul, Brazil. Mycopathologia. 2008;165(6):367–71.CrossRefPubMedGoogle Scholar
  12. 12.
    Belitardo DR, Calefi AS, Borges IK, de Oliveira GG, Sbeghen MR, Itano EN, et al. Detection of antibodies against Paracoccidioides brasiliensis in free-range domestic pigs (Sus scrofa). Mycopathologia. 2014;177(1–2):91–5.CrossRefPubMedGoogle Scholar
  13. 13.
    Corte AC, Svoboda WK, Navarro IT, Freire RL, Malanski LS, Shiozawa MM, et al. Paracoccidioidomycosis in wild monkeys from Parana State, Brazil. Mycopathologia. 2007;164(5):225–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Belitardo DR, Calefi AS, Sbeghen MR, de Oliveira GG, Watanabe MA, de Camargo ZP, et al. Paracoccidioides brasiliensis infection in domestic rabbits (Oryctolagus cuniculus). Mycoses. 2014;57(4):222–7.CrossRefPubMedGoogle Scholar
  15. 15.
    Fernandes GF, Deps P, Tomimori-Yamashita J, Camargo ZP. IgM and IgG antibody response to Paracoccidioides brasiliensis in naturally infected wild armadillos (Dasypus novemcinctus). Med Mycol. 2004;42(4):363–8.CrossRefPubMedGoogle Scholar
  16. 16.
    Albano APN, Klafke GB, Brandolt TM, Da Hora VP, Nogueira CEW, Xavier MO, et al. Seroepidemiology of Paracoccidioides brasiliensis infection in horses from Rio Grande do Sul, Brazil. Braz J Microbiol. 2015;46(2):513–7.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Corte AC, Itano EN, Freire RL, de Camargo ZP, Ono MA. Detection of antibodies to Paracoccidioides brasiliensis in horses from northern region of Paraná State. Semin-Cienc Agrar. 2009;30(2):441–6.CrossRefGoogle Scholar
  18. 18.
    Ferreira JB, Navarro IT, Freire RL, Oliveira GG, Omori AM, Belitardo DR, et al. Evaluation of Paracoccidioides brasiliensis infection in dairy goats. Mycopathologia. 2013;176(1–2):95–9.CrossRefPubMedGoogle Scholar
  19. 19.
    Bagagli E, Sano A, Coelho KI, Alquati S, Miyaji M, de Camargo ZP, et al. Isolation of Paracoccidioides brasiliensis from armadillos (Dasypus novemcinctus) captured in an endemic area of paracoccidioidomycosis. Am J Trop Med Hyg. 1998;58(4):505–12.PubMedGoogle Scholar
  20. 20.
    Silva-Vergara ML, Martinez R, Camargo ZP, Malta MH, Maffei CM, Chadu JB. Isolation of Paracoccidioides brasiliensis from armadillos (Dasypus novemcinctus) in an area where the fungus was recently isolated from soil. Med Mycol. 2000;38(3):193–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Vergara ML, Martinez R. Role of the armadillo Dasypus novemcinctus in the epidemiology of paracoccidioidomycosis. Mycopathologia. 1998;144(3):131–3.CrossRefPubMedGoogle Scholar
  22. 22.
    Bagagli E, Franco M, Bosco Sde M, Hebeler-Barbosa F, Trinca LA, Montenegro MR. High frequency of Paracoccidioides brasiliensis infection in armadillos (Dasypus novemcinctus): an ecological study. Med Mycol. 2003;41(3):217–23.CrossRefPubMedGoogle Scholar
  23. 23.
    Corredor GG, Peralta LA, Castano JH, Zuluaga JS, Henao B, Arango M, et al. The naked-tailed armadillo Cabassous centralis (Miller 1899): a new host to Paracoccidioides brasiliensis. Molecular identification of the isolate. Med Mycol. 2005;43(3):275–80.CrossRefPubMedGoogle Scholar
  24. 24.
    Bagagli E, Bosco SM, Theodoro RC, Franco M. Phylogenetic and evolutionary aspects of Paracoccidioides brasiliensis reveal a long coexistence with animal hosts that explain several biological features of the pathogen. Infect Genet Evol. 2006;6(5):344–51.CrossRefPubMedGoogle Scholar
  25. 25.
    Neves LN, Petroni TF, Fedatto PF, Ono MA. Paracoccidioidomycosis in wild and domestic animals. Semin-Cienc Agrar. 2006;27(3):481–8.CrossRefGoogle Scholar
  26. 26.
    Ono MA, Kishima MO, Itano EN, Bracarense AP, Camargo ZP. Experimental paracoccidioidomycosis in dogs. Med Mycol. 2003;41(3):265–8.CrossRefPubMedGoogle Scholar
  27. 27.
    Mós EN, Fava Netto C. Contribuição ao estudo da paracoccidiodomicose. I. Possível papel epidemiológico dos cães. Estudo sorológico e anatomo-patológico. Rev Inst Med Trop São Paulo. 1974;16(3):154–9.Google Scholar
  28. 28.
    Eisele RC, Juliani LC, Belitardo DR, Itano EN, Estevao D, Bracarense AP, et al. Immune response in dogs experimentally infected with Paracoccidioides brasiliensis. Med Mycol. 2004;42(6):549–53.CrossRefPubMedGoogle Scholar
  29. 29.
    Teles AJ, Klafke GB, Cabana AL, Albano AP, Xavier MO, Meireles MC. Serological investigation into Paracoccidioides brasiliensis infection in dogs from Southern Rio Grande do Sul, Brazil. Mycopathologia. 2016;181(3–4):323–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Canteros CE, Madariaga MJ, Lee W, Rivas MC, Davel G, Iachini R. Endemic fungal pathogens in a rural setting of Argentina: seroepidemiological study in dogs. Rev Iberoam Micol. 2010;27(1):14–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Corte AC, Gennari SM, Labruna MB, Camargo LMA, Itano EN, Freire RL, et al. Paracoccidioides brasiliensis infection in dogs from Western Brazilian Amazon. Pesq Vet Bras. 2012;32:649–52.CrossRefGoogle Scholar
  32. 32.
    Mós EN, Fava Netto C, Saliba AM, Brito T. Contribuição ao estudo da paracoccidiodomicose. II. Infecção experimental do cão. Rev Inst Med Trop São Paulo. 1974;16(4):232–7.PubMedGoogle Scholar
  33. 33.
    Ricci G, Mota FT, Wakamatsu A, Serafim RC, Borra RC, Franco M. Canine paracoccidioidomycosis. Med Mycol. 2004;42(4):379–83.CrossRefPubMedGoogle Scholar
  34. 34.
    Farias MR, Condas LA, Ribeiro MG, Bosco Sde M, Muro MD, Werner J, et al. Paracoccidioidomycosis in a dog: case report of generalized lymphadenomegaly. Mycopathologia. 2011;172(2):147–52.CrossRefPubMedGoogle Scholar
  35. 35.
    White T, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990. p. 315–22.Google Scholar
  36. 36.
    Headley SA, Di Santis GW, de Alcantara BK, Costa TC, da Silva EO, Pretto-Giordano LG, et al. Cryptococcus gattii-induced infections in dogs from Southern Brazil. Mycopathologia. 2015;180(3–4):265–75.CrossRefPubMedGoogle Scholar
  37. 37.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 1999;41:95–8.Google Scholar
  39. 39.
    Camargo Z, Unterkircher C, Campoy SP, Travassos LR. Production of Paracoccidioides brasiliensis exoantigens for immunodiffusion tests. J Clin Microbiol. 1988;26(10):2147–51.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Brummer E, Castaneda E, Restrepo A. Paracoccidioidomycosis: an update. Clin Microbiol Rev. 1993;6(2):89–117.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Reiss E, Shadomy HJ, Lyon GM. Fundamental medical mycology. Hoboken: Wiley; 2012.Google Scholar
  42. 42.
    Ramos-e-Silva M, Saraiva LES. Paracoccidioidomycosis. Dermatol Clin. 2008;26(2):257–69.CrossRefPubMedGoogle Scholar
  43. 43.
    Bellissimo-Rodrigues F, Bollela VR, Da Fonseca BA, Martinez R. Endemic paracoccidioidomycosis: relationship between clinical presentation and patients’ demographic features. Med Mycol. 2013;51(3):313–8.CrossRefPubMedGoogle Scholar
  44. 44.
    Teles FR, Martins ML. Laboratorial diagnosis of paracoccidioidomycosis and new insights for the future of fungal diagnosis. Talanta. 2011;85(5):2254–64.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Selwyn Arlington Headley
    • 1
    • 2
  • Lucienne Garcia Pretto-Giordano
    • 3
  • Giovana Wingeter Di Santis
    • 1
    • 2
  • Lucas Alécio Gomes
    • 4
  • Rafaela Macagnan
    • 8
  • Daniela Farias da Nóbrega
    • 1
  • Katherine Moura Leite
    • 4
  • Brígida Kussumoto de Alcântara
    • 6
  • Eiko Nakagawa Itano
    • 7
  • Amauri Alcindo Alfieri
    • 6
    • 8
  • Mario Augusto Ono
    • 5
  1. 1.Laboratory of Animal Pathology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  2. 2.Multi-User Animal Health Laboratory, Organic Tissue Processing Unit, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  3. 3.Laboratory of Mycology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  4. 4.Small Animal Internal Medicine, Department of Veterinary ClinicsUniversidade Estadual de LondrinaLondrinaBrazil
  5. 5.Laboratory of Applied Immunology, Department of Pathological SciencesUniversidade Estadual de LondrinaLondrinaBrazil
  6. 6.Laboratory of Molecular Biology, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil
  7. 7.Laboratory of Applied Immunology, Department of Pathological SciencesUniversidade Estadual de LondrinaLondrinaBrazil
  8. 8.Multi-User Animal Health Laboratory, Molecular Biology Unit, Department of Veterinary Preventive MedicineUniversidade Estadual de LondrinaLondrinaBrazil

Personalised recommendations