Current Fungal Infection Reports

, Volume 9, Issue 4, pp 238–245 | Cite as

Epidemiological Aspects of Sporotrichosis Epidemic in Brazil

  • Maria Clara Gutierrez-Galhardo
  • Dayvison Francis Saraiva Freitas
  • Antonio Carlos Francesconi do Valle
  • Rodrigo Almeida-Paes
  • Manoel Marques Evangelista de Oliveira
  • Rosely Maria Zancopé-Oliveira
Fungal Infections of Skin and Subcutaneous Tissue (A Bonifaz, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Fungal Infections of Skin and Subcutaneous Tissue

Abstract

Generally, in Brazil, the transmission of sporotrichosis is by traumatic inoculation of fungi with the handling of organic matter. However, since the late 1990s, sporotrichosis in the great metropolitan area of Rio de Janeiro has become an urban endemic/epidemic zoonotic phenomenon, with transmission from infected cats to humans. Middle-aged housewives are the most affected population, particularly from deprived social strata. With the consolidation of the epidemic, vulnerable groups have been affected and the most striking group is people with HIV infection because of the superimposed burdens of both infections. Other states in Brazil have also presented zoonotic cases, however, with smaller dimensions. Sporothrix brasiliensis is the primary species involved in this hyperendemic. We believe that the combination of susceptible hosts, a virulent infecting species, and the absence of an effective public health structure are some of the possible associated factors that resulted in this catastrophe.

Keywords

Brazil Rio de Janeiro Epidemiology Transmission Zoonosis Cat Hyperendemic Soil Sporotrichosis Urban area HIV infection HIV/AIDS epidemic Opportunistic infection Notifiable disease Deprived social strata Pet Molecular epidemiology Sporothrix schenckii S. schenckii complex S. brasiliensis S. globosa S. mexicana T3B fingerprinting Calmodulin gene MALDI-TOF MS 

Notes

Acknowledgments

This work was supported by Programa Estratégico de Pesquisa em Saúde (PAPES) VI – Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)/Fundação Oswaldo Cruz (Fiocruz) [grant proc. 407693/2012-2]. RMZ-O was supported in part by CNPq [304976/2013-0].

Compliance with Ethics Guidelines

Conflict of Interest

The authors declare that they have no conflict of interest

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Lutz A, Splendore A. Sobre uma mycose observada em homens e ratos. Rev Med S Paulo. 1907;21:433–50.Google Scholar
  2. 2.
    Donadel KW, Reinoso YD, Oliveira JC, Azulay RD. Esporotricose: revisão. An Bras Dermatol. 1993;68(1):45–52.Google Scholar
  3. 3.
    Freitas DC, Migliano MF, Esporotricose Z-NL. Observação de caso espontâneo em gato doméstico (F. catus). Rev Fac Med Vet S Paulo. 1956;5:601–4.CrossRefGoogle Scholar
  4. 4.
    Rosa AC, Scroferneker ML, Vettorato R, Gervini RL, Vettorato G, Weber A. Epidemiology of sporotrichosis: a study of 304 cases in Brazil. J Am Acad Dermatol. 2005;52(3 Pt 1):451–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Sampaio SAP, Lacaz CS, Almeida F. Clinical aspects of sporotrichosis in São Paulo—analysis of 235 cases. Rev Hosp Clin Fac Med S Paulo. 1954;9:391–402.Google Scholar
  6. 6.
    Larsson CE, Goncalves Mde A, Araujo VC, Dagli ML, Correa B, Fava NC. Esporotricose felina: aspectos clínicos e zoonóticos. Rev Inst Med Trop Sao Paulo. 1989;31(5):351–8.PubMedGoogle Scholar
  7. 7.
    Marques SA, Franco SRVS, Camargo RMP, Dias LDF, Haddad-Júnior V, Fabris VE. Esporotricose do gato doméstico (Felis catus): transmissão humana. Rev Inst Med Trop Sao Paulo. 1993;35(4):327–30.CrossRefPubMedGoogle Scholar
  8. 8.
    Alves SH, Boettcher CS, Oliveira DC, Tronco-Alves GR, Sgaria MA, Thadeu P, et al. Sporothrix schenckii associated with armadillo hunting in Southern Brazil: epidemiological and antifungal susceptibility profiles. Rev Soc Bras Med Trop. 2010;43(5):523–5.CrossRefPubMedGoogle Scholar
  9. 9.
    Alchorne M, Paschoalick R, Carrete C, Fernandes K, Jacinto R. Inquérito epidemiológico com esporotriquina em Mogi das Cruzes – SP. An Bras Dermatol. 1990;65(5a):45S–8S.Google Scholar
  10. 10.
    Lima LB, Pereira Jr AC. Esporotricose - Inquérito epidemiológico. Importância como doença profissional. An Bras Dermatol. 1981;56(4):243–8.Google Scholar
  11. 11.
    Helm MAF, Berman C. The clinical, therapeutic and epidemiological features of the sporotrichosis infection on the mines. In: Proceedings of the Transvaal Mine Medical Officers’ Association. Sporotrichosis Infection on Mines of the Witwatersrand. Johannesburg: The Transvaal Chamber of Mines. 1947;p. 59–74.Google Scholar
  12. 12.
    CDC. Epidemiologic notes and reports multistate outbreak of sporotrichosis in seedling handlers. MMWR. 1988;37(42):652–3.Google Scholar
  13. 13.
    Dooley DP, Bostic PS, Beckius ML. Spook house sporotrichosis: a point-source outbreak of sporotrichosis associated with hay bale props in a Halloween haunted-house. Arch Intern Med. 1997;157:1885–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Feeney KT, Arthur IH, Whittle AJ, Altman SA, Speers DJ. Outbreak of sporotrichosis. Western Australia Emerg Infect Dis. 2007;13:1228–31.CrossRefPubMedGoogle Scholar
  15. 15.
    Pappas PG, Tellez I, Deep AE, Nolasco D, Holgado W, Bustamante B. Sporotrichosis in Peru: description of an area of hyperendemicity. Clin Infect Dis. 2000;30:65–70.CrossRefPubMedGoogle Scholar
  16. 16.
    Verma S, Verma GK, Singh G, Kanga A, Shanker V, Singh D, et al. Sporotrichosis in Sub-Himalayan India. PLoS Negl Trop Dis. 2012;6(6):e1673.PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    Bonifaz A, Araiza J, Pérez-Mejía A, Ochoa LA, Toriello C. Intradermal test with sporotrichin in a community in the Sierra Norte de Puebla. Dermatol Rev Mex. 2013;57:428–32 [in Spanish].Google Scholar
  18. 18.
    Itoh M, Okamoto S, Kariya H. Survey of 200 cases of sporotrichosis. Dermatologica. 1986;172:209–13.CrossRefPubMedGoogle Scholar
  19. 19.
    Song Y, Li SS, Zhong SX, Liu YY, Yao L, Huo SS. Report of 457 sporotrichosis cases from Jilin province, northeast China, a serious endemic region. J Eur Acad Dermatol Venereol. 2013;27(3):313–8.CrossRefPubMedGoogle Scholar
  20. 20.
    Vidal G, Rodriguez-de-Kopp N. Sporotrichosis: clinical, therapeutic and epidemiologic overview. Arch Argent Dermatol. 1993;63:221–34 [in Spanish].Google Scholar
  21. 21.
    Conti-Diaz IA. Epidemiology of sporotrichosis in Latin America. Mycopathologia. 1989;108:113–16.PubMedGoogle Scholar
  22. 22.
    Kano R, Okubo M, Siew HH, Kamata H, Hasegawa A. Molecular typing of Sporothrix schenckii isolates from cats in Malaysia. Mycoses. 2015;58(4):220–4.CrossRefPubMedGoogle Scholar
  23. 23.
    Barros MB, Schubach Ade O, do Valle AC, Gutierrez Galhardo MC, Conceicao-Silva F, Schubach TM, et al. Cat-transmitted sporotrichosis epidemic in Rio de Janeiro, Brazil: description of a series of cases. Clin Infect Dis. 2004;38(4):529–35.CrossRefPubMedGoogle Scholar
  24. 24.
    Freitas DF, do Valle AC, Almeida-Paes R, Bastos FI, Galhardo MC. Zoonotic sporotrichosis in Rio de Janeiro, Brazil: a protracted epidemic yet to be curbed. Clin Infect Dis. 2010;50(3):453.CrossRefPubMedGoogle Scholar
  25. 25.•
    Silva MB, Costa MM, Torres CC, Galhardo MC, Valle AC, Magalhaes Mde A, et al. Esporotricose urbana: uma epidemia negligenciada no Rio de Janeiro, Brasil. Cad Saude Publica. 2012;28(10):1867–80. Geoprocessing of sporotrichosis cases in Rio de Janeiro, showing the sporotrichosis belt corresponding to poverty areas.CrossRefPubMedGoogle Scholar
  26. 26.•
    Chakrabarti A, Bonifaz A, Gutierrez-Galhardo MC, Mochizuki T, Li S. Global epidemiology of sporotrichosis. Med Mycol. 2015;53(1):3–14. One of the most comprehensive reviews on the epidemiology of sporotrichosis in the world.CrossRefPubMedGoogle Scholar
  27. 27.•
    Almeida-Paes R, de Oliveira MM, Freitas DF, do Valle AC, Zancope-Oliveira RM, Gutierrez-Galhardo MC. Sporotrichosis in Rio de Janeiro, Brazil: Sporothrix brasiliensis is associated with atypical clinical presentations. PLoS Negl Trop Dis. 2014;8(9):e3094. Association of S. brasiliensis with both classic and unusual cases of sporotrichosis in the endemic area of Rio de Janeiro, Brazil.PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Ferreira CP, do Valle AC, Freitas DF, Reis R, Galhardo MC. Pregnancy during a sporotrichosis epidemic in Rio de Janeiro, Brazil. Int J Gynaecol Obstetrics. 2012;117(3):294–5.CrossRefGoogle Scholar
  29. 29.
    Freitas DF, Lima IA, Curi CL, Jordao L, Zancope-Oliveira RM, do Valle AC, et al. Acute dacryocystitis: another clinical manifestation of sporotrichosis. Mem Inst Oswaldo Cruz. 2014;109(2):262–4.PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.•
    Freitas DF, Valle AC, da Silva MB, Campos DP, Lyra MR, de Souza RV, et al. Sporotrichosis: an emerging neglected opportunistic infection in HIV-infected patients in Rio de Janeiro, Brazil. PLoS Negl Trop Dis. 2014;8(8):e3110. Sporotrichosis associated with zoonotic transmission in Rio de Janeiro, Brazil, also affects HIV-infected individuals. HIV infection aggravates sporotrichosis, with a higher incidence of severe disseminated cases and a higher number of hospitalizations and deaths.PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Cruz LCH. Complexo Sporothrix schenckii. Revisão de parte da literatura e considerações sobre o diagnóstico e a epidemiologia. Vet e Zootec. 2013;20:8–28.Google Scholar
  32. 32.
    Silva EA, Schoendorfer LMP, Gardica NO. Investigation and control of sporotrichosis at the municipality of São Paulo. 1st International Meeting on Sporothrix and Sporotrichosis; Rio de Janeiro, Brazil 2013.Google Scholar
  33. 33.•
    Montenegro H, Rodrigues AM, Dias MA, da Silva EA, Bernardi F, de Camargo ZP. Feline sporotrichosis due to Sporothrix brasiliensis: an emerging animal infection in Sao Paulo, Brazil. BMC Vet Res. 2014;10:269. Description of the recent emergence of feline sporotrichosis and its fast spread in the metropolitan region of São Paulo, Brazil, with an overwhelming occurrence of S. brasiliensis as the etiological agent.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Marques GF, Martins AL, Sousa JM, Brandao LS, Wachholz PA, Masuda PY. Characterization of sporotrichosis cases treated in a dermatologic teaching unit in the state of Sao Paulo - Brazil, 2003–2013. An Bras Dermatol. 2015;90(2):273–5.PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Falqueto A, Bravim Maifrede S, Araujo RM. Unusual clinical presentation of sporotrichosis in three members of one family. Int J Dermatol. 2012;51(4):434–8.CrossRefPubMedGoogle Scholar
  36. 36.•
    Oliveira MM, Maifrede SB, Ribeiro MA, Zancope-Oliveira RM. Molecular identification of Sporothrix species involved in the first familial outbreak of sporotrichosis in the state of Espirito Santo, southeastern Brazil. Mem Inst Oswaldo Cruz. 2013;108(7):936–8. This article reinforced the spread of S. brasiliensis through other Brazilian states rather than Rio de Janeiro.PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Cordeiro FN, Bruno CB, Paula CD, Motta JO. Familial occurrence of zoonotic sporotrichosis. An Bras Dermatol. 2011;86(4 Suppl 1):S121–4.CrossRefPubMedGoogle Scholar
  38. 38.
    Madrid IM, Mendes RS, Prestes C, Neto FMS. Surveillance and control of the human and animal sporotrichosis in the city of Pelotas, Rio Grande do Sul, Brazil. 1st International Meeting on Sporothrix and Sporotrichosis 2013. p. 61.Google Scholar
  39. 39.
    Madrid IM, Mattei A, Martins A, Nobre M, Meireles M. Feline sporotrichosis in the southern region of Rio Grande do Sul, Brazil: clinical, zoonotic and therapeutic aspects. Zoonoses Public Health. 2010;57(2):151–4.CrossRefPubMedGoogle Scholar
  40. 40.
    Sanchotene KO, Bergamaschi MP, Xavier MO. Feline Sporotrichosis in Rio Grande, RS, Brazil. 1st International Meeting on Sporothrix and Sporotrichosis; Rio de Janeiro, Brazil 2013.Google Scholar
  41. 41.
    Rodrigues AM, de Hoog G, Zhang Y, Camargo ZP. Emerging sporotrichosis is driven by clonal and recombinant species. Emerg Microbes Infect. 2014;3(5). e32.Google Scholar
  42. 42.
    Lopes-Bezerra LM, Schubach A, Costa RO. Sporothrix schenckii and sporotrichosis. An Acad Bras Sci. 2006;78(2):293–308.Google Scholar
  43. 43.
    Suzuki K, Kawasaki M, Ishizaki H. Analysis of restriction profiles of mitochondrial DNA from Sporothrix schenckii and related fungi. Mycopathologia. 1988;103(3):147–51.CrossRefPubMedGoogle Scholar
  44. 44.
    Takeda Y, Kawasaki M, Ishizaki H. Phylogeny and molecular epidemiology of Sporothrix schenckii in Japan. Mycopathologia. 1991;116(1):9–14.CrossRefPubMedGoogle Scholar
  45. 45.
    Mora-Cabrera M, Alonso RA, Ulloa-Arvizu R, Torres-Guerrero H. Analysis of restriction profiles of mitochondrial DNA from Sporothrix schenckii. Med Mycol. 2001;39(5):439–44.CrossRefPubMedGoogle Scholar
  46. 46.
    Watanabe S, Kawasaki M, Mochizuki T, Ishizaki H. RFLP analysis of the internal transcribed spacer regions of Sporothrix schenckii. Nihon Ishinkin Gakkai Zasshi. 2004;45(3):165–75.CrossRefPubMedGoogle Scholar
  47. 47.
    Gutierrez-Galhardo MC, Zancopé-Oliveira RM, Valle AC, Almeida-Paes R, Tavares PMS, Monzon A, et al. Molecular epidemiology and antifungal susceptibility patterns of Sporothrix schenckii isolates from a cat-transmitted epidemic of sporotrichosis in Rio de Janeiro. Brazil Med Mycol. 2008;46(2):141–51.CrossRefGoogle Scholar
  48. 48.
    Kanbe T, Natsume L, Goto I, Kawasaki M, Mochizuki T, Ishizaki H, et al. Rapid and specific identification of Sporothrix schenckii by PCR targeting the DNA topoisomerase II gene. J Dermatol Sci. 2005;38(2):99–106.CrossRefPubMedGoogle Scholar
  49. 49.
    Neyra E, Fonteyne PA, Swinne D, Fauche F, Bustamante B, Nolard N. Epidemiology of human sporotrichosis investigated by amplified fragment length polymorphism. J Clin Microbiol. 2005;43(3):1348–52.PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    de Meyer EM, de Beer ZW, Summerbell RC, Moharram AM, de Hoog GS, Vismer HF, et al. Taxonomy and phylogeny of new wood- and soil-inhabiting Sporothrix species in the Ophiostoma stenoceras-Sporothrix schenckii complex. Mycologia. 2008;100(4):647–61.CrossRefPubMedGoogle Scholar
  51. 51.
    Marimon R, Cano J, Gene J, Sutton DA, Kawasaki M, Guarro J. Sporothrix brasiliensis, S. globosa, and S. mexicana, three new Sporothrix species of clinical interest. J Clin Microbiol. 2007;45(10):3198–206.PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Marimon R, Gene J, Cano J, Guarro J. Sporothrix luriei: a rare fungus from clinical origin. Med Mycol. 2008;46(6):621–5.CrossRefPubMedGoogle Scholar
  53. 53.
    Cruz-Choappa RM, Vieille-Oyarzo PI, Carvajal-Silva LC. Aislamiento de Sporothrix pallida complex en muestras clínicas y ambientales de Chile. Rev Arg Microbiol. 2014;46(4):311–4.Google Scholar
  54. 54.
    Dias NM, Oliveira MM, Santos C, Zancope-Oliveira RM, Lima N. Sporotrichosis caused by Sporothrix mexicana. Portugal Emerg Infect Dis. 2011;17(10):1975–6.CrossRefPubMedGoogle Scholar
  55. 55.
    Oliveira DC, Lopes PG, Spader TB, Mahl CD, Tronco-Alves GR, Lara VM, et al. Antifungal susceptibilities of Sporothrix albicans, S. brasiliensis, and S. luriei of the S. schenckii complex identified in Brazil. J Clin Microbiol. 2011;49(8):3047–9.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Oliveira MM, Almeida-Paes R, Muniz MM, Barros MBL, Gutierrez-Galhardo MC, Zancope-Oliveira RM. Sporotrichosis caused by Sporothrix globosa in Rio de Janeiro, Brazil: case report. Mycopathologia. 2010;169(5):359–63.CrossRefPubMedGoogle Scholar
  57. 57.
    Rodrigues AM, de Hoog S, Camargo ZP. Emergence of pathogenicity in the Sporothrix schenckii complex. Med Mycol. 2013;51(4):405–12.CrossRefPubMedGoogle Scholar
  58. 58.
    Ishizaki H, Kawasaki M, Anzawa K, Mochizuki T, Chakrabarti A, Ungpakorn R, et al. Mitochondrial DNA analysis of Sporothrix schenckii in India, Thailand, Brazil, Colombia, Guatemala and Mexico. Nihon Ishinkin Gakkai Zasshi. 2009;50(1):19–26.CrossRefPubMedGoogle Scholar
  59. 59.
    Reis RS, Almeida-Paes R, Muniz MM, Tavares PMS, Monteiro PCF, Schubach TMP, et al. Molecular characterisation of Sporothrix schenckii isolates from humans and cats involved in the sporotrichosis epidemic in Rio de Janeiro. Brazil Mem Inst Oswaldo Cruz. 2009;104(5):769–74.CrossRefPubMedGoogle Scholar
  60. 60.
    Rodrigues AM, de Hoog GS, Camargo ZP. Genotyping species of the Sporothrix schenckii complex by PCR-RFLP of calmodulin. Diagn Microbiol Infect Dis. 2014;78(4):383–7.CrossRefPubMedGoogle Scholar
  61. 61.
    Xun Z, Rodrigues AM, Feng P, de Hoog G. Global ITS diversity in the Sporothrix schenckii complex. Fungal Divers. 2014;66:153–65.Google Scholar
  62. 62.•
    Teixeira MM, Rodrigues AM, Tsui CK, Almeida LG, Van Diepeningen AD, van den Ende BG, et al. Asexual propagation of a virulent clone complex in a human and feline outbreak of sporotrichosis. Eukaryotic Cell. 2015;14(2):158–69. A discussion about differential forms of propagation and genetic variability of the two major species causing sporotrichosis in Brazil.PubMedCentralCrossRefGoogle Scholar
  63. 63.
    Sasaki AA, Fernandes GF, Rodrigues AM, Lima FM, Marini MM, Dos SFL, et al. Chromosomal polymorphism in the Sporothrix schenckii complex. PLoS One. 2014;9(1), e86819.PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Rodrigues AM, de Hoog GS, Pires DC, Brihante RS, Sidrim JJ, Gadelha MF, et al. Genetic diversity and antifungal susceptibility profiles in causative agents of sporotrichosis. BMC Infect Dis. 2014;14:219.PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Rodrigues AM, Teixeira MM, de Hoog GS, Schubach TM, Pereira SA, Fernandes GF, et al. Phylogenetic analysis reveals a high prevalence of Sporothrix brasiliensis in feline sporotrichosis outbreaks. PLoS Negl Trop Dis. 2013;7(6):e2281.PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    Kovarik CL, Neyra E, Bustamante B. Evaluation of cats as the source of endemic sporotrichosis in Peru. Med Mycol. 2008;46(1):53–6.CrossRefPubMedGoogle Scholar
  67. 67.
    Rees RK, Swartzberg JE. Feline-transmitted sporotrichosis: a case study from California. Dermatol Online J. 2011;17(6):2.PubMedGoogle Scholar
  68. 68.
    Oliveira MM, Sampaio P, Almeida-Paes R, Pais C, Gutierrez-Galhardo MC, Zancope-Oliveira RM. Rapid identification of Sporothrix species by T3B fingerprinting. J Clin Microbiol. 2012;50(6):2159–62.PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Oliveira MM, Franco-Duarte R, Romeo O, Pais C, Criseo G, Sampaio P, et al. Evaluation of T3B fingerprinting for identification of clinical and environmental Sporothrix species. FEMS Microbiol Lett. 2015;362(6):fnv027.CrossRefPubMedGoogle Scholar
  70. 70.•
    Oliveira MM, Santos C, Sampaio P, Romeo O, Almeida-Paes R, Pais C, et al. Development and optimization of a new MALDI-TOF protocol for identification of the Sporothrix species complex. Res Microbiol. 2015;166(2):102–10. A presentation of a rapid and reliable tool for Sporothrix spp. identification, with potential application in future epidemiological studies.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Maria Clara Gutierrez-Galhardo
    • 1
  • Dayvison Francis Saraiva Freitas
    • 1
  • Antonio Carlos Francesconi do Valle
    • 1
  • Rodrigo Almeida-Paes
    • 2
  • Manoel Marques Evangelista de Oliveira
    • 2
  • Rosely Maria Zancopé-Oliveira
    • 2
  1. 1.Instituto Nacional de Infectologia Evandro Chagas, FiocruzLaboratório de Pesquisa Clínica em Dermatologia InfecciosaRio de JaneiroBrazil
  2. 2.Instituto Nacional de Infectologia Evandro Chagas, FiocruzLaboratório de MicologiaRio de JaneiroBrazil

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