Advertisement

Paracoccidioidomycosis ceti (Lacaziosis/Lobomycosis) in Dolphins

  • Raquel Vilela
  • Leonel Mendoza
Chapter

Abstract

Infections caused by the fungal pathogen Lacazia loboi were first reported in 1931 by Jorge de Oliveira Lobo in a human with granulomatous skin lesions in Pernambuco, Brazil. Early histopathological and serological analyses found morphological similarities and cross-reactive antigens with Paracoccidioides brasiliensis. In 1971, veterinarians working with dolphins in Florida, USA, reported granulomatous skin lesions in a dolphin, similar to that in human lacaziosis. Based on histopathological findings, L. loboi was initially believed to be also the etiologic agent of cutaneous disease in dolphins. Ever since, cutaneous granulomas have been reported in different dolphin species around the coast of Asia, Europe, and North and South America. Recently, using molecular biology approaches, some investigators stated that the DNA sequences extracted from cases of cutaneous granulomas in dolphins were closely related to those of P. brasiliensis. This chapter deals with the history, taxonomy, and other features of L. loboi in humans and the unculturable P. brasiliensis var. ceti type affecting the skin of dolphins.

Keywords

Lacazia loboi Paracoccidioides brasiliensis Paracoccidioides brasiliensis var. ceti Paracoccidioidomycosis ceti Dolphins 

References

  1. Almeida FP, Lacaz CDS (1948–1949) Blastomicose “tipo Jorge Lobo”. An Fac Med Sao Paulo 24:5–37Google Scholar
  2. Arju R, Kothadia JP, Kaminski M, Abraham S, Giashuddin S (2014) Jorge Lobo’s disease: a case of keloidal blastomycosis (lobomycosis) in a nonendemic area. Ther Adv Infect Dis 2:91–96CrossRefPubMedPubMedCentralGoogle Scholar
  3. Azulay RD, Carneiro JA, Da Graça M, Cunha S, Reis LT (1976) Keloidal blastomycosis (Lobo’s disease) with lymphatic involvement: a case report. Int J Dermatol 15:40–42CrossRefPubMedGoogle Scholar
  4. Baruzzi RG, Castro RM, D’Andretta C Jr, Carvalhal S, Ramos OL, Pontes PL (1973) Occurrence of Lobo’s blastomycosis among “Caiabi,” Brazilian Indians. Int J Dermatol 12:95–99CrossRefPubMedGoogle Scholar
  5. Baruzzi RG, Marcopito LF, Michalany NS, Livianu J, Pintoe NR (1981) Early diagnosis and prompt treatment by surgery in Jorge Lobo’s disease (keloidal blastomycosis). Mycopathologia 74:51–54CrossRefPubMedGoogle Scholar
  6. Belone AFF, Madeira S, Rosa PS, Opromolla DVA (2001) Experimental reproduction of the Jorge Lobo’s disease in BALB/c mice inoculated with Lacazia loboi obtained from a previously infected mouse. Mycopathologia 155:191–194CrossRefGoogle Scholar
  7. Bermudez L, Van Bressem MF, Reyes-Jaimes O, Sayegh AJ, Paniz-Mondolfi AE (2009) Lobomycosis in man and lobomycosis-like disease in bottlenose dolphin, Venezuela. Emerg Infect Dis 15:1301–1303CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bessesen BL, Oviedo L, Burdett Hart L, Herra-Miranda D, Pacheco-Polanco JD, Baker L, Saborío-Rodriguez G, Bermúdez-Villapol L, Acevedo-Gutiérrez A (2014) Lacaziosis-like disease among bottlenose dolphins Tursiops truncatus photographed in Golfo Dulce, Costa Rica. Dis Aquat Org 107:173–180CrossRefPubMedGoogle Scholar
  9. Borelli D (1962) Lobomicosis experimental. Derm Venez 3:72–82Google Scholar
  10. Borelli D (1968) Lobomicosis: nomenclatura de agente (revisión critica). Med Cutanea 3(2):151–156Google Scholar
  11. Bossart GD, Schaefer AM, McCulloch S, Goldstein J, Fair PSA, Reif JS (2015) Mucocutaneous lesions in free-ranging Atlantic bottlenose dolphins Tursiops truncates from the southeastern USA. Dis Aquat Org 115:175–184CrossRefPubMedGoogle Scholar
  12. Burns RA, Roy JS, Woods C, Padhye AA, Warnock DW (2000) Report of the first human case of lobomycosis in the United States. J Clin Microbiol 38:1283–1285PubMedPubMedCentralGoogle Scholar
  13. Bustamante B, Seas C, Salomon M, Bravo F (2013) Lobomycosis successfully treated with posaconazole. Am J Trop Med Hyg 88:1207–1208CrossRefPubMedPubMedCentralGoogle Scholar
  14. Caldwell DK, Caldwell MC, Woodard JC, Ajello L, Kaplan W, McClure HM (1975) Lobomycosis as a disease of the Atlantic bottle-nosed dolphin (Tursiops truncatus Montagu, 1821). Am J Trop Med Hyg 24:105–114CrossRefPubMedGoogle Scholar
  15. Camargo ZP, Baruzzi RG, Maeda SM, Floriano MC (1998) Antigenic relationship between Loboa loboi and Paracoccidioides brasiliensis as shown by serological methods. Med Mycol 36:413–417CrossRefPubMedGoogle Scholar
  16. Cardoso de Brito A, Quaresma JAS (2007) Lacaziosis (Jorge Lobo’s disease): review and update. An Bras Dermatol 82:461–474CrossRefGoogle Scholar
  17. Carneiro FP, Maia LB, Moraes MA, deMagalhaes AV, Vianna LM (2009) Lobomycosis: diagnosis and management of relapsed and multifocal lesions. Diagn Microbiol Infect Dis 65:62–64CrossRefPubMedGoogle Scholar
  18. Costa PF (2015) Isolation and in vitro cultivation of the etiologic agent of Jorge Lobo: morphology physiology and complete genome of Candida loboi sp. nov. PhD. Thesis, Universidade Federal do ParaGoogle Scholar
  19. Cucé LC, Wroclawski EL, Sampaio SA (1980) Treatment of paracoccidioidomycosis, candidiasis, chromomycosis, lobomycosis, and mycetoma with ketoconazole. Int J Dermatol 19:405–408CrossRefPubMedGoogle Scholar
  20. Daura-Jorge FG, Simões-Lopes PC (2011) Lobomycosis-like disease in wild bottlenose dolphins Tursiops truncatus of Laguna, southern Brazil: monitoring of a progressive case. Dis Aquat Org 93:163–170CrossRefPubMedGoogle Scholar
  21. De Moura JF, Hauser-Davis RA, Lemos L, Emin-Lima R, Siciliano S (2014) Guiana dolphins (Sotalia guianensis) as marine ecosystem sentinels: ecotoxicology and emerging diseases. Rev Environ Contam Toxicol 228:1–29PubMedGoogle Scholar
  22. De Vries GA, Laarman JJ (1973) A case of Lobo’s disease in the dolphin Sotalia guianensis. Aquat Mamm 1:26–33Google Scholar
  23. Dudok van Heel WH (1977) Successful treatment in a case of lobomycosis (Lobo’s disease) in Tursiops truncatus (Mont) at Dolfinarium, Harderwijk. Aquat Mamm 5:8–15Google Scholar
  24. Eichelmann K, González González SE, Salas-Alanis JC, Ocampo-Candiani J (2013) Leprosy. An update: definition, pathogenesis, classification, diagnosis, and treatment. Actas Dermosifiliogr 104:554–563CrossRefPubMedGoogle Scholar
  25. Elsayed S, Kuhn SM, Barber D, Church DL, Adams S, Kasper R (2004) Human case of lobomycosis. Emerg Infect Dis 10:715–718CrossRefPubMedPubMedCentralGoogle Scholar
  26. Esperon F, García-Párraga D, Bellière EN, Sánchez-Vizcaíno JM (2012) Molecular diagnosis of lobomycosis-like disease in a bottlenose dolphin in captivity. Med Mycol 50:106–109CrossRefPubMedGoogle Scholar
  27. Fischer M, Chrusciak-Talhari A, Reinel D, Talhari S (2002) Successful treatment with clofazimine and itraconazole in a 46 year old patient after 32 years duration of disease. Hautarzt 53:677–681CrossRefPubMedGoogle Scholar
  28. Fonseca FO, Area LAE (1940) Contribuição para o conhecimento das granulomatoses blastomycoides: o agente etiológico da doença de Jorge Lobo. Rev Med Cirurg Brasil 48:147–158Google Scholar
  29. Fonseca OJM, Lacaz CDS (1971) Estudo de culturas isoladas de blastomicose queloidiforme (doença de Jorge Lobo). Denominação ao seu agente etiològico. Rev Inst Med Trop São Paulo 13:225–251PubMedGoogle Scholar
  30. Francesconi VA, Klein AP, Santos APBG, Ramasawmy R, Francesconi F (2014) Lobomycosis: epidemiology, clinical presentation, and management options. Ther Clin Risk Manag 10:851–860CrossRefPubMedPubMedCentralGoogle Scholar
  31. Furtado JS, De Brito T, Freymuller E (1967) Structure and reproduction of Paracoccidioides loboi. Mycologia 59:286–294CrossRefGoogle Scholar
  32. Goihman-Yahr M, Cabello de Brito I, Bastardo de Albornoz MC, Pereira MHDGJ, de Roman A, Martin BS, Molina T (1989) Functions of polymorphonuclear leukocytes and individuality of Jorge Lobo’s disease: absence of the specific leukocyte digestive defect against Paracoccidioides brasiliensis. Mycoses 32:603–608CrossRefPubMedGoogle Scholar
  33. Haubold EM, Cooper CR Jr, Wen JW, McGinnis MR, Cowan DF (2000) Comparative morphology of Lacazia loboi (syn. Loboa loboi) in dolphins and humans. Med Mycol 38:9–14CrossRefPubMedGoogle Scholar
  34. Herr RA, Tarcha EJ, Taborda PR, Taylor JW, Ajello L, Mendoza L (2001) Phylogenetic analysis of Lacazia loboi places this previously uncharacterized pathogen within the dimorphic Onygenales. J Clin Microbiol 39(1):309–314CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kiszka J, Van Bressem MF, Pusineri C (2009) Lobomycosis-like disease and other skin conditions in indo-Pacific bottlenose dolphins Tursiops aduncus from the Indian Ocean. Dis Aquat Org 84:151–157CrossRefPubMedGoogle Scholar
  36. Lacaz CDS (1996) Paracoccidioides loboi (Fonseca Filho et Arêa Leão, 1940) Almeida et Lacaz, 1948–1949. Description of the fungus in Latin. Rev Inst Med Trop São Paulo 38(3):229–231CrossRefGoogle Scholar
  37. Lacaz CDS, Baruzzi RG, Rosa MDCB (1986) Doença de Jorge Lobo. IPSIS Editora SA, São Paulo, pp 1–92Google Scholar
  38. Landman G, Velludo MA, Lopes JA, Mendes E (1988) Crossed-antigenicity between the etiologic agents of lobomycosis and paraccocidioidomycosis evidenced by an immunoenzymatic method (PAP). Allergol Immunopathol 16:215–218Google Scholar
  39. Lane EP, de Wet M, Thompson P, Siebert U, Wohlsein P, Plön S (2014) A systemic health assessment of Indian Ocean bottlenose (Tursiops aduncus) and Indo-Pacific humpback (Sousa plumbea) dolphins accidentally caught in shark nets off the KwaZulu-Natal coast, South Africa. PLoS One 9:1–13Google Scholar
  40. Lawrence DN, Ajello L (1986) Lobomycosis in western Brazil: report of a clinical trial with ketoconazole. Am J Trop Med Hyg 35:162–166CrossRefPubMedGoogle Scholar
  41. Lobo JO (1931) Um caso de blastomicose produzido por uma espécie nova, encontrada em Recife. Rev Med Pernamb 1:763–765Google Scholar
  42. Machado PA (1972) Polimorfismo das lesões dermatológicas na blastomicose de Jorge Lobo entre os índios Caiabi. Acta Amaz 2:93–97CrossRefGoogle Scholar
  43. Madeira S, Opromolla DVA, Belone ADFF (2000) Inoculation of BALB/C mice with Lacazia loboi. Rev Inst Med Trop São Paulo 42:239–243CrossRefPubMedGoogle Scholar
  44. Mendes E, Michalany N, Mendes NF (1986) Comparison of the cell walls of Paracoccidioides loboi and Paracoccidioides brasiliensis by using polysaccharide-binding dyes. Int J Tissue React 6:229–231Google Scholar
  45. Mendoza L, Belone AF, Vilela R, Rehtanz M, Bossart GD, Reif JS, Fair PA, Durden WN, St. Leger J, Travassos LR, Rosa PS (2008) Use of sera from humans and dolphins with lacaziosis and sera from experimentally infected mice for western blot analyses of Lacazia loboi antigens. Clin Vaccine Immunol 15:164–167CrossRefPubMedGoogle Scholar
  46. Migaki G, Valerio MG, Irvine B, Garner FM (1971) Lobo’s disease in an Atlantic bottle-nosed dolphin. J Am Vet Med Assoc 159:578–582PubMedGoogle Scholar
  47. Minakawa T, Ueda K, Tanaka M, Tanaka N, Kuwamura M, Izawa T, Konno T, Yamate J, Itano EN, Sano A, Wada S (2016) Detection of multiple budding yeast cells and partial sequence of 43-Kda glycoprotein coding gene of Paracoccidioides brasiliensis from a case of lacaziosis in a female Pacific white-sided dolphin (Lagenorhyncus obliquidens). Mycopathologia 181:523–529CrossRefPubMedGoogle Scholar
  48. Miranda MF, Silva AJ (2005) Vinyl adhesive tape also effective for direct microscopy diagnosis of chromomycosis, lobomycosis, and paracoccidioidomycosis. Diagn Microbiol Infect Dis 52:39–43CrossRefPubMedGoogle Scholar
  49. Murdoch ME, Mazzoil M, McCulloch S, Bechdel S, O'Corry-Crowe G, Bossart GD, Reif JS (2010) Lacaziosis in bottlenose dolphins Tursiops truncatus along the coastal Atlantic Ocean, Florida, USA. Dis Aquat Organ 92:69–73CrossRefPubMedGoogle Scholar
  50. Norton SA (2006) Dolphin-to-human transmission of lobomycosis? J Am Acad Dermatol 55:723–724CrossRefPubMedGoogle Scholar
  51. Opromolla DVA, Belone AFF, Taborda PR, Taborda VBA (2000) Clinic-pathological correlation in 40 cases of lobomycosis. An Bras Dermatol 75:425–434Google Scholar
  52. Opromolla DV, Belone AF, Taborda PR, Rosa PS (2003) Lymph node involvement in Jorge Lobo’s disease: report of two cases. Int J Dermatol 42:938–941CrossRefPubMedGoogle Scholar
  53. Paniz-Mondolfi AE, Sander-Hoffmann L (2009) Lobomycosis in inshore and estuarine dolphins. Emerg Infect Dis 15:672–673CrossRefPubMedPubMedCentralGoogle Scholar
  54. Paniz-Mondolfi A, Talhari C, Sander Hoffmann L, Connor DL, Talhari S, Bermudez-Villapol L, Hernadez-Perez M, VanBressem MF (2012) Lobomycosis: an emerging disease in humans and delphinidae. Mycoses 55:298–309CrossRefPubMedGoogle Scholar
  55. Papadavid E, Dalamaga M, Kapniari I, Pantelidaki E, Papageorgiou S, Vassiliki P, Tsirigotis P, Dervenoulas I, Stavrianeas N, Rigopoulos D (2012) Lobomycosis: a case from southeastern Europe and review of the literature. J Dermatol Case Rep 6:65–69CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pecher SA, Croce J, Ferri RG (1979) Study of humoral and cellular immunity in lobomycosis. Allergol Immunopathol (Madr) 7(6):439–444Google Scholar
  57. Puccia R, Travassos LR (1991) 43-kilodalton glycoprotein from Paracoccidioides brasiliensis: immunochemical reactions with sera from patients with paracoccidioidomycosis, histoplasmosis, or Jorge Lobo’s disease. J Clin Microbiol 29:1610–1615PubMedPubMedCentralGoogle Scholar
  58. Reif JS, Mazzoil MS, McCulloch SD, Varela RA, Doldstein JD, Fair PA, Bossart GD (2006) Lobomycosis in Atlantic bottlenose dolphins form the Indian River lagoon, Florida. J Am Vet Med Assoc 228:104–108CrossRefPubMedGoogle Scholar
  59. Reif JS, Peden-Adams MM, Romano TA, Rice CD, Fair PA, Bossart GD (2009) Immune dysfunction in Atlantic bottlenose dolphins (Tursiops truncatus) with lobomycosis. Med Mycol 47:125–135CrossRefPubMedGoogle Scholar
  60. Reif JS, Schaefer AM, Bossart GD (2013) Lobomycosis: risk of zoonotic transmission from dolphins to humans. Vector Borne Zoonotic Dis 13:689–693CrossRefPubMedPubMedCentralGoogle Scholar
  61. Rodriguez-Toro G (1993) Lobomycosis. Int J Dermatol 32:324–332CrossRefPubMedGoogle Scholar
  62. Rosa PS, Soares CT, Belone ADFF, Vilela R, Ura S, Filho MC, Mendoza L (2009) Accidental Jorge Lobo’s disease in a worker dealing with Lacazia loboi infected mice: a case report. J Med Case Rep 3:67–71CrossRefPubMedPubMedCentralGoogle Scholar
  63. Rotstein DS, Burdett LG, McLellan W, Schwacke L, Rwles T, Terio KA, Schultz S, Pabst A (2009) Lobomycosis in offshore bottlenose dolphins (Tursiops truncatus), North Carolina. Emerg Infect Dis 15:588–590CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sacristan C, Réssio RA, Castilho P, Fernandes N, Costa-Silva S, Esperón F, Daura-Jorge FG, Groch KR, Kolesnikovas CK, Marigo J, Ott PH, Oliveira LR, Sánchez-Sarmiento AM, Simões-Lopes PC, Catão-Dias JL (2016) Lacaziosis-like disease in Tursiops truncatus from Brazil: a histopathological and immunohistochemical approach. Dis Aquat Org 117:229–235CrossRefPubMedGoogle Scholar
  65. Saint-Blancard P, Maccari F, Le Guyadec T, Lanternier G, Le Vagueresse R (2000) Lobomycosis: a mycosis seldom observed in metropolitan France. Ann Pathol 20(3):241–244PubMedGoogle Scholar
  66. Sampaio MM, Dias LB (1970) Experimental infection of Jorge Lôbo’s disease in the cheek-pouch of the golden hamster. Rev Inst Med Trop Sao Paulo 12:115–120PubMedGoogle Scholar
  67. Schaefer AM, Reif JS, Guzmán EA, Bossart GD, Ottuso P, Snyder J, Medalie N, Rosato R, Han S, Fair PA, McCarthy PJ (2016) Toward the identification, characterization and experimental culture of Lacazia loboi from Atlantic bottlenose dolphin (Tursiops truncatus). Med Mycol 54:659–565CrossRefPubMedGoogle Scholar
  68. Silva D (1972) Micose de Lobo. Rev Soc Bras Med Trop 6:85–98CrossRefGoogle Scholar
  69. Silva D, Brito A (1994) Formas clínicas não usuais da micose de Lobo. An Bras Dermatol 69:133–136Google Scholar
  70. Silva ME, Kaplan W, Miranda JL (1968) Antigenic relationships between Paracoccidioides loboi and other pathogenic fungi determined by immunofluorescence. Mycopathol Mycol Appl 36:97–106CrossRefPubMedGoogle Scholar
  71. Symmers WS (1983) A possible case of Lôbo’s disease acquired in Europe from a bottle-nosed dolphin (Tursiops truncatus). Bull Soc Pathol Exot Filiales 76:777–784PubMedGoogle Scholar
  72. Taborda PR, Taborda VA, McGinnis MR (1999a) Lacazia loboi gen. nov, comb. nov, the etiologic agent of lobomycosis. J Clin Microbiol 37:2031–2033PubMedPubMedCentralGoogle Scholar
  73. Taborda VB, Taborda PR, McGinnis MR (1999b) Constitutive melanin in the cell wall of the etiologic agent of Lobo’s disease. Rev Inst Med Trop Sao Paulo 41:9–12CrossRefPubMedGoogle Scholar
  74. Tajima Y, Sasaki K, Kashiwagi N, Yamada TK (2015) A case of stranded Indo-Pacific bottlenose dolphin (Tursiops aduncus) with lobomycosis-like skin lesions in Kinko-wan, Kagoshima, Japan. J Vet Med Sci 77:989–992CrossRefPubMedPubMedCentralGoogle Scholar
  75. Talhari S, Talhari C (2012) Lobomycosis. Clin Dermatol 30:420–424CrossRefPubMedGoogle Scholar
  76. Talhari C, Chrusciak-Talhari A, de Souza JV, Araújo JR, Talhari S (2009) Exfoliative cytology as a rapid diagnostic tool for lobomycosis. Mycoses 52:187–189CrossRefPubMedGoogle Scholar
  77. Tapia A, Torres-Calcindo A, Arosemena R (1978) Keloidal blastomycosis (Lobo’s disease) in Panama. Int J Dermatol 17:572–574CrossRefPubMedGoogle Scholar
  78. Ueda K, Sano A, Yamate J, Nakagawa EI, Kuwamura M, Izawa T, Tanaka M, Hasegawa Y, Chibana H, Izumisawa Y, Miyahara H, Senzo Uchida S (2013) Two cases of Lacaziosis in bottlenose dolphins (Tursiops truncatus) in Japan. Case Rep Vet Med 2013:1–9.  https://doi.org/10.1155/2013/318548CrossRefGoogle Scholar
  79. Van Bressem MF, Santos MC, Oshima JE (2009) Skin diseases in Guiana dolphins (Sotalia guianensis) from the Paranaguá estuary, Brazil: a possible indicator of a compromised marine environment. Mar Environ Res 67:63–68CrossRefPubMedGoogle Scholar
  80. Vidal MS, Palacios SA, de Melo NT, Lacaz CDS (1997) Reactivity of anti-gp43 antibodies from Paracoccidioides brasiliensis antiserum with extracts from cutaneous lesions of Lobo’s disease. Preliminary note. Rev Inst Med Trop Sao Paulo 39:35–37CrossRefPubMedGoogle Scholar
  81. Vilani-Moreno FR, Opromolla DV (1997) Determinação da viabilidade do Paracoccidioides loboi em biópsias de pacientes portadores de doença de Jorge Lobo. Ann Bras Dermatol 72:433–437Google Scholar
  82. Vilani-Moreno FR, Silva LM, Opromolla DV (2004a) Evaluation of the phagocytic activity of peripheral blood monocytes of patients with Jorge Lobo’s disease. Rev Soc Bras Med Trop 37:165–168CrossRefPubMedGoogle Scholar
  83. Vilani-Moreno FR, Lauris JR, Opromolla DV (2004b) Cytokine quantification in the supernatant of mononuclear cell cultures and in blood serum from patients with Jorge Lobo’s disease. Mycopathologia 158:17–24CrossRefPubMedGoogle Scholar
  84. Vilani-Moreno FR, Mozer E, de Sene AM, Ferasçoli MDO, Pereira TC, Miras MG, Souza GHDP, ADFF B (2007) In vitro and in situ activation of the complement system by the fungus Lacazia loboi. Rev Inst Med Trop Sao Paulo 49:97–101CrossRefPubMedGoogle Scholar
  85. Vilani-Moreno FR, Belone Ade F, Lara VS, Venturini J, Lauris JR, Soares CT (2011) Detection of cytokines and nitric oxide synthase in skin lesions of Jorge Lobo’s disease patients. Med Mycol 49(6):643–648PubMedGoogle Scholar
  86. Vilela R, Mendoza L (2015) Lacazia, lagenidium, pythium, and rhinosporidium. In: Jorgenses JH, Pfaller MA, Carrol KC, Funke G, Landry ML, Richerter SS, Warnock DW (eds) Manual of clinical microbiology, 11th edn. ASM Press, Washington, pp 2196–2208CrossRefGoogle Scholar
  87. Vilela R, Mendoza L, Rosa PS, Belone AFF, Madeira S, Opromolla DVA, de Resende MA (2005) Molecular model for studying the uncultivated fungal pathogen Lacazia loboi. J Clin Microbiol 43:3657–3661CrossRefPubMedPubMedCentralGoogle Scholar
  88. Vilela R, Martins JEC, Pereira CN, Melo N, Mendoza L (2007) Molecular study of archival fungal strains isolated from cases of lacaziosis (Jorge Lobo’s disease). Mycoses 50:470–474CrossRefPubMedGoogle Scholar
  89. Vilela R, Rosa PS, Belone AF, Taylor JW, Diório SM, Mendoza L (2009) Molecular phylogeny of animal pathogen Lacazia loboi inferred from rDNA and DNA coding sequences. Mycol Res 113:851–857CrossRefPubMedGoogle Scholar
  90. Vilela R, Bossart GD, St. Leger JA, Dalton LM, Reif JS, Schaefer AM, McCarthy PJ, Fair PA, Mendoza L (2016) Cutaneous granulomas in dolphins caused by novel uncultivated Paracoccidioides brasiliensis. Emerg Infect Dis 22:2097–2103CrossRefGoogle Scholar
  91. Woodard JC (1972) Electron microscope study of lobomycosis (Loboa loboi). Lab Investig 27:606–612PubMedGoogle Scholar
  92. Woods WJ, Belone Ade F, Carneiro LB, Rosa PS (2010) Ten years experience with Jorge Lobo’s disease in the state of acre, Amazon region, Brazil. Rev Inst Med Trop Sao Paulo 52:273–278CrossRefPubMedGoogle Scholar
  93. Xavier MB, Libonati RM, Unger D, Oliveira C, Corbett CE, de Brito AC, Quaresma JA (2008) Macrophage and TGF-beta immunohistochemical expression in Jorge Lobo’s disease. Hum Pathol 39(2):269–274CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of PharmacyFederal University of Minas GeraisBelo HorizonteBrazil
  2. 2.Biomedical Laboratory DiagnosticsMichigan State UniversityEast LansingUSA
  3. 3.Microbiology and Molecular Genetics, Biomedical Laboratory DiagnosticsMichigan State UniversityEast LansingUSA

Personalised recommendations