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Canine sporotrichosis: polyphasic taxonomy and antifungal susceptibility profiles of Sporothrix species in an endemic area in Brazil

  • Veterinary Microbiology - Research Paper
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Abstract

Sporotrichosis, a mycosis caused by pathogenic species of the genus Sporothrix, affects diverse species of mammals. Until 2007, Sporothrix schenckii was considered the unique etiologic agent of sporotrichosis. Canine sporotrichosis is a poorly reported disease, and the majority of cases are from Rio de Janeiro, Brazil. There are scarce studies on the characterization of canine isolates of Sporothrix schenckii complex, as well as few antifungal susceptibility data available. The aim of this study was to characterize the clinical isolates of Sporothrix from dogs from Brazil at species level and evaluate their antifungal susceptibility profile. Polyphasic taxonomy was used to characterization at species level (morphological, phenotypical characteristics, and molecular identification). Antifungal susceptibility profiles (amphotericin B, itraconazole, ketoconazole, posaconazole, and terbinafine) were determined using the Clinical and Laboratory Standards Institute broth microdilution method (M38-A2). According to phenotypic identification and molecular analysis, 46 isolates included in this study were identified as S. brasiliensis and one as S. schenckii. Amphotericin B presented the highest minimum inhibitory concentration values, and the other drugs showed effective in vitro antifungal activity. This is the first report of S. schenckii in dogs from Brazil, since S. brasiliensis is the only species that has been described in canine isolates from Rio de Janeiro to date. Nevertheless, no differences were observed in the antifungal susceptibility profiles between the S. brasiliensis and S. schenckii isolates, and it is important to continuously study new canine clinical isolates from Rio de Janeiro, Brazil.

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References

  1. Pereira SA, Gremiao ID, Kitada AA, Boechat JS, Viana PG, Schubach TM (2014) The epidemiological scenario of feline sporotrichosis in Rio de Janeiro, State of Rio de Janeiro, Brazil. Rev Soc Bras Med Trop 47:392–393

    PubMed  Google Scholar 

  2. Rodrigues AM, Hoog GS, de Camargo ZP (2014) Genotyping species of the Sporothrix schenckii complex by PCR-RFLP of calmodulin. Diagn Microbiol Infect Dis 78:383–387

    CAS  PubMed  Google Scholar 

  3. Pereira SA, Gremião IDF, Menezes RC (2015) Sporotrichosis in animals: zoonotic transmission. In: Sporotrichosis - new developments and future prospects, 1st edn. Springer, Suíça, pp 83–102

    Google Scholar 

  4. Cafarchia C, Sasaneli M, Lia RP, Caprariis D, Guillot J, Otranto D (2007) Lymphocutaneous and nasal sporotrichosis in a dog from Southern Italy: case report. Mycopathologia 163:75–79

    PubMed  Google Scholar 

  5. Crothers SL, White SD, Ihrke PJ, Affolter VK (2009) Sporotrichosis: a retrospective evaluation of 23 cases seen in northern California (1987-2007). Vet Dermatol 20:249–259

    PubMed  Google Scholar 

  6. Schubach TM, Schubach A, Okamoto T et al (2006) Canine sporotrichosis in Rio de Janeiro, Brazil: clinical presentation, laboratory diagnosis and therapeutic response in 44 cases (1998-2003). Med Mycol 44:87–92

    PubMed  Google Scholar 

  7. Mascarenhas MB, Lopes NL, Pinto TG, Costa TS, Peixoto AP, Ramadinha RR, Fernandes JI (2018) Canine sporotrichosis: report of 15 advanced cases. Pesqui Vet Bras 38:477–481

    Google Scholar 

  8. Viana PG, Figueiredo ABF, Gremião IDF, de Miranda LHM, da Silva Antonio IM, Boechat JS, de Sá Machado AC, de Oliveira MME, Pereira SA (2018) Successful treatment of canine sporotrichosis with terbinafine: case reports and literature review. Mycopathologia 183:471–478

    PubMed  Google Scholar 

  9. Barros MB, Almeida-Paes R, Schubach AO (2011) Sporothrix schenckii and sporotrichosis. Clin Microbiol Rev 24:633–654

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Silva MB, Costa MM, Torres CC et al (2012) Esporotricose urbana: epidemia negligenciada no Rio de Janeiro, Brasil. Cad Saúde Pública 28:1867–1880

    PubMed  Google Scholar 

  11. Freitas DF, Valle AC, da Silva MB et al (2014) Sporotrichosis: an emerging neglected opportunistic infection in HIV-infected patients in Rio de Janeiro, Brazil. PLoS Negl Trop Dis 8:e3110

    PubMed  PubMed Central  Google Scholar 

  12. Gremião IDF, Miranda LHM, Reis EG, Rodrigues AM, Pereira SA (2017) Zoonotic epidemic of sporotrichosis: cat to human transmission. PLoS Pathog 13:e1006077

    PubMed  PubMed Central  Google Scholar 

  13. Rosser E, Dunstan R (2006) Sporotrichosis. Infectious diseases of the dog and cat, 3rd edn. Saunders Elsevier, Philadelphia

    Google Scholar 

  14. Barros MB, Schubach AO, do Valle AC et al (2004) Cat-transmitted sporotrichosis epidemic in Rio de Janeiro, Brazil: description of a series of cases. Clin Infect Dis 38:529–535

    PubMed  Google Scholar 

  15. Schubach A, Barros MB, Wanke B (2008) Epidemic sporotrichosis. Curr Opin Infect Dis 21:129–133

    PubMed  Google Scholar 

  16. Sykes JE, Torres SM, Armstrong PJ, Lindeman CJ (2001) Itraconazole for treatment of sporotrichosis in a dog residing on a Christmas tree far. J Am Vet Med Assoc 218:1440–1443

    CAS  PubMed  Google Scholar 

  17. Scott D, Miller W (1996) Doenças fúngicas da pele. Dermatologia de pequenos animais. Interlivros Edições Ltda, Rio de Janeiro, pp 301–369

    Google Scholar 

  18. Marimon R, Gene J, Cano J, Trilles L, Lazera M, Guarro J (2006) Molecular phylogeny of Sporothrix schenckii. J Clin Microbiol 44:3251–3256

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Marimon R, Cano J, Gene J, Sutton DA, Kawasaki M, Guarro J (2007) Sporothrix brasiliensis, S. globosa, and S. mexicana, three new Sporothrix species of clinical interest. J Clin Microbiol 45:3198–3206

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Marimon R, Gene J, Cano J, Guarro J (2008) Sporothrix luriei: a rare fungus from clinical origin. Med Mycol 46:621–625

    PubMed  Google Scholar 

  21. Romeo O, Scordino F, Criseo G (2011) New insight into molecular phylogeny and epidemiology of Sporothrix schenckii species complex based on calmodulin-encoding gene analysis of Italian isolates. Mycopathologia 172:179–186

    PubMed  Google Scholar 

  22. Oliveira MM, Almeida-Paes R, Muniz MM, Gutierrez-Galhardo MC, Zancope-Oliveira RM (2011) Phenotypic and molecular identification of Sporothrix isolates from an epidemic area of sporotrichosis in Brazil. Mycopathologia 172:257–267

    PubMed  Google Scholar 

  23. Rodrigues AM, Choappa RC, Fernandes GF, De Hoog GS, Camargo ZP (2016) Sporothrix chilensis sp. nov. (Ascomycota: Ophiostomatales), a soil-borne agent of human sporotrichosis with mild-pathogenic potential to mammals. Fungal Biol 120:246–264

  24. Rodrigues AM, de Hoog GS, de Camargo ZP (2016) Sporothrix species causing outbreaks in animals and humans driven by animal-animal transmission. PLoS Pathog 12:e1005638

    PubMed  PubMed Central  Google Scholar 

  25. Lopes-Bezerra LM, Mora-Montes HM, Zhang Y, Nino-Vega G, Rodrigues AM, de Camargo ZP, de Hoog S (2018) Sporotrichosis between 1898 and 2017: the evolution of knowledge on a changeable disease and on emerging etiological agents. Med Mycol 56:S126–S143

    CAS  Google Scholar 

  26. Moussa TAA, Kadasa NMS, Al Zahrani HS et al (2017) Origin and distribution of Sporothrix globosa causing sapronoses in Asia. J Med Microbiol 66:560–569

    PubMed  Google Scholar 

  27. Oliveira MM, Almeida-Paes R, Muniz MM, Barros MBL, Gutierrez-Galhardo MC, Zancope-Oliveira RM (2010) Sporotrichosis caused by Sporothrix globosa in Rio de Janeiro, Brazil: case report. Mycopathologia 169:359–363

    PubMed  Google Scholar 

  28. Rodrigues AM, Teixeira MM, Hoog GS et al (2013) Phylogenetic analysis reveals a high prevalence of Sporothrix brasiliensis in feline sporotrichosis outbreaks. PLoS Negl Trop Dis 7:e2281

    PubMed  PubMed Central  Google Scholar 

  29. Kano R, Okubo M, Siew HH, Kamata H, Hasegawa A (2015) Molecular typing of Sporothrix schenckii isolates from cats in Malaysia. Mycoses 58:220–224

    CAS  PubMed  Google Scholar 

  30. Han HS, Kano R, Chen C, Noli C (2017) Comparison of two in vitro antifungal sensitivity tests and monitoring during therapy of Sporothrix schenckii sensu stricto in Malaysian cats. Vet Dermatol 28:156–e32

    PubMed  Google Scholar 

  31. Siew HH (2017) The current status of feline sporotrichosis in Malaysia. Med Mycol J 58E:E107–E113

    Google Scholar 

  32. Boechat JS, Oliveira MME, Almeida-Paes R, Gremião IDF, Machado ACS, Oliveira RVC, Figueiredo ABF, Rabello VBS, Silva KBL, Zancopé-Oliveira RM, Schubach TMP, Pereira SA (2018) Feline sporotrichosis: associations between clinical-epidemiological profiles and phenotypic-genotypic characteristics of the etiological agents in the Rio de Janeiro epizootic area. Mem Inst Oswaldo Cruz 113:185–196

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Arrillaga-Moncrieff I, Capilla J, Mayayo E, Marimon R, Marine M, Genis J, Cano J, Guarro J (2009) Different virulence levels of the species of Sporothrix in a murine model. Clin Microbiol Infect 15:651–655

    CAS  PubMed  Google Scholar 

  34. Oliveira DC, Lopes PG, Spader TB et al (2011) Antifungal susceptibilities of Sporothrix albicans, S. brasiliensis, and S. luriei of the S. schenckii complex identified in Brazil. J Clin Microbiol 49:3047–3049

    PubMed  PubMed Central  Google Scholar 

  35. Silva-Vergara ML, Camargo ZP, Silva PF et al (2012) Disseminated Sporothrix brasiliensis infection with endocardial and ocular involvement in an HIV-infected patient. Am J Trop Med Hyg 86:477–480

    PubMed  PubMed Central  Google Scholar 

  36. Córdoba S, Isla G, Szusz W et al (2018) Molecular identification and susceptibility profile of Sporothrix schenckii sensu lato isolated in Argentina. Mycoses 61:1–8

  37. Macêdo-Sales PA, Souto SRL, Destefani CA et al (2018) Domestic feline contribution in the transmission of Sporothrix in Rio de Janeiro State, Brazil: a comparison between infected and non-infected populations. BMC Vet Res 14:1–10

    Google Scholar 

  38. Souza EW, Borba CM, Pereira SA et al (2018) Clinical features, fungal load, coinfections, histological skin changes, and itraconazole treatment response of cats with sporotrichosis caused by Sporothrix brasiliensis. Sci Rep 8:9074

    PubMed  PubMed Central  Google Scholar 

  39. Etchecopaz AN, Lanza N, Toscanini MA, Devoto TB, Pola SJ, Daneri GL, Iovannitti CA, Cuestas ML (2019) Sporotrichosis caused by Sporothrix brasiliensis in Argentina: case report, molecular identification and in vitro susceptibility pattern to antifungal drugs. J Mycol Med 30:100908. https://doi.org/10.1016/j.mycmed.2019.100908

    Article  PubMed  Google Scholar 

  40. Waller SB, Hoffmann JF, Madrid IM, Picoli T, Cleff MB, Chaves FC, Zanette RA, de Mello JRB, de Faria RO, Meireles MCA (2018) Polar Origanum vulgare (Lamiaceae) extracts with antifungal potential against Sporothrix brasiliensis. Med Mycol 56:225–233

    CAS  PubMed  Google Scholar 

  41. Lopez-Romero E, Reyes-Montes MR, Perez-Torres A et al (2011) Sporothrix schenckii complex and sporotrichosis, an emerging health problem. Future Microbiol 6:85–102

    PubMed  Google Scholar 

  42. Padhye AA, Kaufman L, Durry E, Banerjee CK, Jindal SK, Talwar P, Chakrabarti A (1992) Fatal pulmonary sporotrichosis caused by Sporothrix schenckii var. luriei in India. J Clin Microbiol 30:2492–2494

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Schubach TM, Menezes RC, Wanke B (2012) Sporotrichosis. Infectious diseases of the dog and cats, 4th edn. Elsevier, Missouri

    Google Scholar 

  44. Schreiber AZ (2007) Antifungiograma: Quando solicitar e Como Interpretar. Prática Hospitalar 49:87–91

    Google Scholar 

  45. Kohler LM, Monteiro PC, Hahn RC, Hamdan JS (2004) In vitro susceptibilities of isolates of Sporothrix schenckii to itraconazole and terbinafine. J Clin Microbiol 42:4319–4320

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Rodrigues AM, Hoog GS, Pires DC et al (2014) Genetic diversity and antifungal susceptibility profiles in causative agents of sporotrichosis. BMC Infect Dis 14:219

    PubMed  PubMed Central  Google Scholar 

  47. Stopiglia CDO, Magagnin CM, Castrillón MR et al (2014) Antifungal susceptibilities and identification of species of the Sporothrix schenckii complex isolated in Brazil. Med Mycol 52:56–64

    Google Scholar 

  48. Borba-Santos LP, Rodrigues AM, Gagini TB, Fernandes GF, Castro R, de Camargo ZP, Nucci M, Lopes-Bezerra LM, Ishida K, Rozental S (2015) Susceptibilidade of Sporothrix brasiliensis isolates to amphotericin B, azoles and terbinafine. Med Mycol 53:178–188

    CAS  PubMed  Google Scholar 

  49. Almeida-Paes R, Frases S, Monteiro PCF, Gutierrez-Galhardo MC, Zancopé-Oliveira RM, Nosanchuk JD (2009) Growth conditions influence melanization of Brazilian clinical Sporothrix schenckii isolates. Microbes Infect 11:554–562

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Almeida-Paes R, Oliveira LC, Oliveira MME, Gutierrez-Galhardo MC, Nosanchuk JD, Zancopé-Oliveira RM (2015) Phenotypic characteristic associated with virulence of clinical isolates from Sporothrix complex. Biomed Res Int 2015:212308

  51. Oliveira MME, Franco-Duarte R, Romeo O et al (2015) Evaluation of T3B fingerprinting for identification of clinical and environmental Sporothrix species. FEMS Microbiol Lett 362:1–7

    Google Scholar 

  52. Clinical and Laboratory Standards Institute (CLSI) (2008) Approved standard M38-A2) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, 2nd edn. Clincal and Laboratory Standards Institute, Wayne

    Google Scholar 

  53. Almeida-Paes R, Brito-Santos F, Figueiredo-Carvalho MHG, Machado ACS, Oliveira MME, Pereira SA, Gutierrez-Galhardo MC, Zancopé-Oliveira RM (2017) Minimal inhibitory concentration distributions and epidemiological cutoff values of five antifungal agents against Sporothrix brasiliensis. Mem Inst Oswaldo Cruz 112:376–381

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Brilhante RSM, Rodrigues AM, Sidrim JJC et al (2016) In vitro susceptibility of antifungal drugs against Sporothrix brasiliensis recovered from cats with sporotrichosis in Brazil. Med Mycol 54:275–279

    CAS  PubMed  Google Scholar 

  55. Espinel-Ingroff A, Abreu DPB, Almeida-Paes R et al (2017) Multicenter 1 and international study of MIC/MEC distributions for definition of epidemiological cutoff values (ECVs) for species of Sporothrix identified by molecular methods. Antimicrob Agents Chemother 61:1–8

    Google Scholar 

  56. Almeida-Paes R, Oliveira MME, Freitas DF, Francesconi AC, Zancopé-Oliveira RM, Gutierrez-Galhardo MC (2014) Sporotrichosis in Rio de Janeiro, Brazil: Sporothrix brasiliensis is associated with atypical clinical presentations. PLoS Negl Trop Dis 8:e3094

    PubMed  PubMed Central  Google Scholar 

  57. Liu T, Zhang K, Zhou X (2014) Molecular identification of Sporothrix clinical isolates in China. J Zhejiang Univ Sci B 15:100–108

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Montenegro H, Rodrigues AM, Dias MAG, Silva EA, Bernardi F, Camargo ZP (2014) Feline sporotrichosis due to Sporothrix brasiliensis: an emerging animal infection in São Paulo, Brazil. BMC Vet Res 10:269

    PubMed  PubMed Central  Google Scholar 

  59. Miranda LHM, Silva JN, Gremião IDF et al (2018) Monitoring fungal burden and viability of Sporothrix spp. in skin lesions of cats for predicting antifungal treatment response. J Fungi (Basel) 4:92

    Google Scholar 

  60. Oliveira MME, Maifrede SB, Ribeiro MA, Zancopé-Oliveira RM (2013) Molecular identification of Sporothrix species involved in the first familial outbreak of sporotrichosis in the state of Espírito Santo, southeastern Brazil. Mem Inst Oswaldo Cruz 108:936–938

    PubMed  PubMed Central  Google Scholar 

  61. Mahmoudi S, Zaini F, Kordbacheh P, Safara M, Heidari M (2016) Sporothrix schenckii complex in Iran: molecular identification and antifungal susceptibility. Med Mycol 54:593–599

    PubMed  Google Scholar 

  62. Meinerz AR, Nascente OS, Schuch LFD et al (2007) In vitro susceptibility of isolates of Sporothrix schenckii to terbinafine and itraconazole. Rev Soc Bras Med Trop 40:60–62

    PubMed  Google Scholar 

  63. Marimon R, Serena C, Gene J, Cano J, Guarro J (2008) In vitro antifungal susceptibilities of five species of Sporothrix. Antimicrob Agents Chemother 52:732–734

    CAS  PubMed  Google Scholar 

  64. Thomson J, Trott DJ, Malik R, Galgut B, McAllister MM, Nimmo J, Renton D, Kidd SE (2019) An atypical cause of sporotrichosis in a cat. Med Mycol Case Rep 23:72–76

    PubMed  PubMed Central  Google Scholar 

  65. Fernández-Silva F, Capilla J, Mayayo E, Guarro J (2012) Efficacy of posaconazole in murine experimental sporotrichosis. Antimicrob Agents Chemother 56:2273–2277

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors are grateful for access to the Oswaldo Cruz Foundation’s sequencing platform (PDTIS/Fiocruz).

Funding

This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001 and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ (E-26/200.839/2017). SAP was supported in part by Jovem Cientista do Nosso Estado 2016 (JCNE)—FAPERJ (grant no.: E-26/203.303/2016) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant no.: 309657/2016-4). RMZ-O was supported in part by CNPq (grant no.: 304976/2013-0) and FAPERJ (grant no.: E-26/103.157/2011). MMO was supported in part by FAPERJ (grant no.: INST E-26/010.001784/2016, JCNE E-26/203.301/2017).

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Correspondence to Jéssica Sepulveda Boechat.

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The study was approved by the Ethics Committee on Animal Use of the Oswaldo Cruz Foundation (CEUA/Fiocruz; number: LW-17/17).

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Boechat, J.S., Pereira, S.A., de Sá Machado, A.C. et al. Canine sporotrichosis: polyphasic taxonomy and antifungal susceptibility profiles of Sporothrix species in an endemic area in Brazil. Braz J Microbiol 52, 135–143 (2021). https://doi.org/10.1007/s42770-020-00328-8

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