Advertisement

Paracoccidioidomycosis in Animals and Humans

  • Sandra de Moraes Gimenes Bosco
  • Eduardo Bagagli
Chapter

Abstract

Paracoccidioidomycosis (PCM) is the most important systemic mycosis in Latin American countries, especially in Brazil, Colombia, Venezuela, and Argentina. The disease is caused by Paracoccidioides brasiliensis and P. lutzii, which are dimorphic fungi belonging to the Ajellomycetaceae. The disease is relatively common in humans, but poorly known in animals. The finding that nine-banded armadillos (Dasypus novemcinctus) are naturally infected by P. brasiliensis, systematically recovered from their tissues, has opened up new opportunities to better comprehend the fungus’ eco-epidemiology. Armadillos are ancient South American mammals belonging to the order Xenarthra, which also comprises anteaters and sloths. The fungus was detected by nested PCR and histopathology in the anteater Myrmecophaga tridactyla and in the two-toed sloth Choloepus didactylus, respectively. The pathogen was also detected by molecular assays in different species of wild road-killed animals originating from PCM-endemic areas. In domestic animals, asymptomatic PCM infection has been detected by intradermal tests and serological surveys, e.g., in dogs, cats, sheep, horses, cattle, pigs, and chickens. Naturally acquired PCM disease was reported in three dogs with generalized lymphadenomegaly and hepatosplenomegaly. Certainly, PCM has been underdiagnosed in animals. Veterinarians should always keep this fungal infection in mind when dealing with animals from regions endemic/enzootic for PCM.

Keywords

Paracoccidioides Paracoccidioidomycosis Systemic mycosis Endemic Enzootic Dogs Armadillos Xenarthra 

References

  1. Almeida F (1930) Estudos comparativos do granuloma coccidioidico nos Estados Unidos e no Brasil. Novo gênero para o parasito brasileiro. An Fac Med Sao Paulo 5:125–142Google Scholar
  2. Arantes TD, Theodoro RC, Macoris SADG, Bagagli E (2013) Detection of Paracoccidioides spp. in environmental aerosol samples. Med Mycol 51:83–92CrossRefPubMedGoogle Scholar
  3. Bagagli E, Bosco SMG (2008) Armadillos and dimorphic pathogenic fungi: ecological and evolutionary aspects. In: Lowghry WJ, Viscaino SF (eds) The biology of the Xenarthra. University Press of Florida, Gainesville, pp 103–110Google Scholar
  4. Bagagli E, Sano A, Coelho KI et al (1998) Isolation of Paracoccidioides brasiliensis from armadillos (Dasypus noveminctus) captured in an endemic area of paracoccidioidomycosis. Am J Trop Med Hyg 58:505–512CrossRefPubMedGoogle Scholar
  5. Bagagli E, Franco M, Bosco SDM et al (2003) High frequency of Paracoccidioides brasiliensis infection in armadillos (Dasypus novemcinctus): an ecological study. Med Mycol 41:217–223CrossRefPubMedGoogle Scholar
  6. Bagagli E, Arantes T, Theodoro R (2012) Paracoccidioides brasiliensis: ecology and evolution. Mycoses 55:54–55Google Scholar
  7. Batista J, de Camargo ZP, Fernandes GF et al (2010) Is the geographical origin of a Paracoccidioides brasiliensis isolate important for antigen production for regional diagnosis of paracoccidioidomycosis? Mycoses 53:176–180.  https://doi.org/10.1111/j.1439-0507.2008.01687.x CrossRefPubMedGoogle Scholar
  8. Belitardo DR, Calefi AS, Borges IK et al (2014a) Detection of antibodies against Paracoccidioides brasiliensis in free-range domestic pigs (Sus scrofa). Mycopathologia 177:91–95.  https://doi.org/10.1007/s11046-013-9724-2 CrossRefPubMedGoogle Scholar
  9. Belitardo DR, Calefi AS, Sbeghen MR et al (2014b) Paracoccidioides brasiliensis infection in domestic rabbits (Oryctolagus cuniculus). Mycoses 57:222–227.  https://doi.org/10.1111/myc.12146 CrossRefPubMedGoogle Scholar
  10. Bellissimo-Rodrigues F, Machado AA, Martinez R (2011) Paracoccidioidomycosis epidemiological features of a 1,000-cases series from a hyperendemic area on the southeast of Brazil. Am J Trop Med Hyg 85:546–550.  https://doi.org/10.4269/ajtmh.2011.11-0084 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bocca AL, Amaral AC, Teixeira MM et al (2013) Paracoccidioidomycosis: eco-epidemiology, taxonomy and clinical and therapeutic issues. Future Microbiol 8:1177–1191.  https://doi.org/10.2217/fmb.13.68 CrossRefPubMedGoogle Scholar
  12. Brummer E, Castaneda E, Restrepo A (1993) Paracoccidioidomycosis: an update. Clin Microbiol Rev 6:89–117CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cadavid D, Restrepo A (1993) Factors associated with Paracoccidiodes brasiliensis infection among permanent residents of three endemic areas in Colombia. Epidemiol Infect 111:121–133CrossRefPubMedPubMedCentralGoogle Scholar
  14. Canteros CE, Madariaga MJ, Lee W et al (2010) Endemic fungal pathogens in a rural setting of Argentina: seroepidemiological study in dogs. Rev Iberoam Micol 27:14–19.  https://doi.org/10.1016/j.riam.2009.11.002 CrossRefPubMedGoogle Scholar
  15. Cazzo E, Ferrer JAP, Chaim EA (2015) Obstructive jaundice secondary to paracoccidioidomycosis. Trop Gastroenterol 36:46–47CrossRefPubMedGoogle Scholar
  16. Coelho KIR, Defaveri J, Rezkallah-Iwasso MT, Peraçoli MTS (1994) Experimental paracoccidioidomycosis. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 87–107Google Scholar
  17. Corredor GG, Castaño JH, Peralta LA et al (1999) Isolation of Paracoccidioides brasiliensis from the nine-banded armadillo Dasypus novemcinctus, in an endemic area for paracoccidioidomycosis in Colombia. Rev Iberoam Micol 16:216–220PubMedGoogle Scholar
  18. Corredor GG, Peralta LA, Castaño JH et al (2005) The naked-tailed armadillo Cabassous centralis (Miller 1899): a new host to Paracoccidioides brasiliensis. Molecular identification of the isolate. Med Mycol 43:275–280CrossRefPubMedGoogle Scholar
  19. Corte AC, Svoboda WK, Navarro IT et al (2007) Paracoccidioidomycosis in wild monkeys from Paraná state, Brazil. Mycopathologia 164:225–228.  https://doi.org/10.1007/s11046-007-9059-y CrossRefPubMedGoogle Scholar
  20. Costa EO, Fava Netto C (1978) Contribution to the epidemiology of paracoccidioidomycosis and histoplasmosis in the state of Sáo Paulo, Brazil. Paracoccidioidin and histoplasmin intradermic tests in domestic animals. Sabouraudia 16:93–101CrossRefPubMedGoogle Scholar
  21. Costa EO, Netto CF, Rodrigues A, Brito T (1978) Bovine experimental paracoccidioidomycosis intradermic test standardization. Sabouraudia 16:103–113CrossRefPubMedGoogle Scholar
  22. Costa EO, Diniz LS, Netto CF (1995a) The prevalence of positive intradermal reactions to paracoccidioidin in domestic and wild animals in São Paulo, Brazil. Vet Res Commun 19:127–130CrossRefPubMedGoogle Scholar
  23. Costa EO, Diniz LS, Netto CF et al (1995b) Delayed hypersensitivity test with paracoccidioidin in captive Latin American wild mammals. J Med Vet Mycol 33:39–42CrossRefPubMedGoogle Scholar
  24. Coutinho ZF, da Silva D, Lazera M et al (2002) Paracoccidioidomycosis mortality in Brazil (1980–1995). Cad Saúde Pública 18:1441–1454CrossRefPubMedGoogle Scholar
  25. Coutinho ZF, Wanke B, Travassos C et al (2015) Hospital morbidity due to paracoccidioidomycosis in Brazil (1998–2006). Trop Med Int Health 20:673–680.  https://doi.org/10.1111/tmi.12472 CrossRefPubMedGoogle Scholar
  26. de Castro LF, Ferreira MC, da Silva RM et al (2013) Characterization of the immune response in human paracoccidioidomycosis. J Infect 67:470–485.  https://doi.org/10.1016/j.jinf.2013.07.019 CrossRefPubMedGoogle Scholar
  27. de Oliveira GG, Belitardo DR, Balarin MRS et al (2013) Serological survey of paracoccidioidomycosis in cats. Mycopathologia 176:299–302.  https://doi.org/10.1007/s11046-013-9681-9 CrossRefPubMedGoogle Scholar
  28. Del Negro G, Lacaz CS, Zamith VA, Siqueira AM (1994) General clinical aspects: polar forms of Paracoccidioidomycosis, the disease in childhood. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 225–232Google Scholar
  29. Do Valle AC, Guimaraes MR, Cuba J et al (1993) Recovery of adrenal function after treatment of paracoccidioidomycosis. Am J Trop Med Hyg 48:626–629CrossRefPubMedGoogle Scholar
  30. Dukik K, Muñoz JF, Jiang Y, Feng P et al (2017) Novel taxa of thermally dimorphic systemic pathogens in the Ajellomycetaceae (Onygenales). Mycoses 60(5):296–309.  https://doi.org/10.1111/myc.12601 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Eisele RC, Juliani LC, Belitardo DR et al (2004) Immune response in dogs experimentally infected with Paracoccidioides brasiliensis. Med Mycol 42:549–553CrossRefPubMedGoogle Scholar
  32. Faiçal S, Borri ML, Hauache OM, Ajzen S (1996) Addison’s disease caused by Paracoccidioides brasiliensis: diagnosis by needle aspiration biopsy of the adrenal gland. AJR Am J Roentgenol 166:461–462.  https://doi.org/10.2214/ajr.166.2.8553971 CrossRefPubMedGoogle Scholar
  33. Farias MR, Condas LAZ, Ribeiro MG et al (2011) Paracoccidioidomycosis in a dog: case report of generalized lymphadenomegaly. Mycopathologia 172:147–152CrossRefPubMedGoogle Scholar
  34. Ferreira JB, Navarro IT, Freire RL et al (2013) Evaluation of Paracoccidioides brasiliensis infection in dairy goats. Mycopathologia 176:95–99.  https://doi.org/10.1007/s11046-013-9644-1 CrossRefPubMedGoogle Scholar
  35. Fontana FF, dos Santos CTB, Esteves FM et al (2010) Seroepidemiological survey of paracoccidioidomycosis infection among urban and rural dogs from Uberaba, Minas Gerais, Brazil. Mycopathologia 169:159–165.  https://doi.org/10.1007/s11046-009-9241-5 CrossRefPubMedGoogle Scholar
  36. Franco M, Montenegro MR, Mendes RP et al (1987) Paracoccidioidomycosis: a recently proposed classification of its clinical forms. Rev Soc Bras Med Trop 20:129–132CrossRefPubMedGoogle Scholar
  37. Franco M, Peracoli MT, Soares A et al (1993) Host-parasite relationship in paracoccidioidomycosis. Curr Top Med Mycol 5:115–149PubMedGoogle Scholar
  38. Franco MV, Goes AM, Koury MC (1997) Model of in vitro granulomatous hypersensitivity in human paracoccidioidomycosis. Mycopathologia 137:129–136CrossRefPubMedGoogle Scholar
  39. Franco M, Bagagli E, Scapolio S, Lacaz CDS (2000) A critical analysis of isolation of Paracoccidioides brasiliensis from soil. Med Mycol 38:185–191CrossRefPubMedGoogle Scholar
  40. Gegembauer G, Araujo LM, Pereira EF et al (2014) Serology of paracoccidioidomycosis due to Paracoccidioides lutzii. PLoS Negl Trop Dis 8:e2986.  https://doi.org/10.1371/journal.pntd.0002986 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Goldani LZ, Sugar AM (1995) Paracoccidioidomycosis and AIDS: an overview. Clin Infect Dis 21:1275–1281CrossRefPubMedGoogle Scholar
  42. Gonzalez JF, Montiel NA, Maass RL (2010) First report on the diagnosis and treatment of encephalic and urinary paracoccidioidomycosis in a cat. J Feline Med Surg 12:659–662.  https://doi.org/10.1016/j.jfms.2010.03.016 CrossRefPubMedGoogle Scholar
  43. Headley SA, Pretto-Giordano LG, Di Santis GW, Gomes LA, Macagnan R, da Nóbrega DF, Leite KM, de Alcântara BK, Itano EN, Alfieri AA, Ono MA (2017) Paracoccidioides brasiliensis-associated dermatitis and lymphadenitis in a dog. Mycopathologia 182(3–4):425–434CrossRefPubMedGoogle Scholar
  44. Herr RA, Tarcha EJ, Taborda PR et al (2001) Phylogenetic analysis of Lacazia loboi places this previously uncharacterized pathogen within the dimorphic Onygenales. J Clin Microbiol 39:309–314.  https://doi.org/10.1128/JCM.39.1.309-314.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kuria JN, Gathogo SM (2013) Concomitant fungal and Mycobacterium bovis infections in beef cattle in Kenya. Onderstepoort J Vet Res 80(1):585.  https://doi.org/10.4102/ojvr.v80i1.585 CrossRefPubMedGoogle Scholar
  46. Lutz A (1908) Uma mycose pseudococcidica localisada na bocca e observada no Brasil. Contribuição ao conhecimento das hyphoblastomycoses americanas. Brasil Méd 22:121–124Google Scholar
  47. Martinez R (2015) Epidemiology of paracoccidioidomycosis. Rev Inst Med Trop São Paulo 57(Suppl 19):11–20.  https://doi.org/10.1590/S0036-46652015000700004 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Martinez R, Moya MJ (1992) The relationship between paracoccidioidomycosis and alcoholism. Rev Saúde Pública 26:12–16CrossRefPubMedGoogle Scholar
  49. Matute DR, McEwen JG, Puccia R et al (2006a) Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol Biol Evol 23:65–73.  https://doi.org/10.1093/molbev/msj008 CrossRefPubMedGoogle Scholar
  50. Matute DR, Sepulveda VE, Quesada LM et al (2006b) Microsatellite analysis of three phylogenetic species of Paracoccidioides brasiliensis. J Clin Microbiol 44:2153–2157.  https://doi.org/10.1128/JCM.02540-05 CrossRefPubMedPubMedCentralGoogle Scholar
  51. McEwen JG, Bedoya V, Patiño MM et al (1987) Experimental murine paracoccidiodomycosis induced by the inhalation of conidia. J Med Vet Mycol 25:165–175CrossRefPubMedGoogle Scholar
  52. Mendes RP (1994) The gamut of clinical manifestations. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 233–257Google Scholar
  53. Mendes JF, Klafke GB, Albano APN, Cabana AL, Teles AJ, Camargo ZP, Xavier MO, Meireles MCA (2017) Paracoccidioidomycosis infection in domestic and wild mammals by Paracoccidioides lutzii. Mycoses 60:402–406CrossRefPubMedGoogle Scholar
  54. Montenegro MR, Franco MF (1994) Pathology. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 131–150Google Scholar
  55. Mós EDN, Netto CF (1974) Contribution to the study of paracoccidioidomycosis. I. Possible epidemiological role of dogs. Serological and anatomo-pathological study. Rev Inst Med Trop São Paulo 16:154–159Google Scholar
  56. Mós EN, Netto CF, Saliba AM, de Brito T (1974) Contribution to the study of paracoccidioidomycosis. II. Experimental infection of dogs. Rev Inst Med Trop São Paulo 16:232–237PubMedGoogle Scholar
  57. Moscardi-Bacchi M, Soares A, Mendes R et al (1989) In situ localization of T lymphocyte subsets in human paracoccidioidomycosis. J Med Vet Mycol 27:149–158CrossRefPubMedGoogle Scholar
  58. Mota NG, Rezkallah-Iwasso MT, Peraçoli MT et al (1985) Correlation between cell-mediated immunity and clinical forms of paracoccidioidomycosis. Trans R Soc Trop Med Hyg 79:765–772CrossRefPubMedGoogle Scholar
  59. Mota NG, Peraçoli MT, Mendes RP et al (1988) Mononuclear cell subsets in patients with different clinical forms of paracoccidioidomycosis. J Med Vet Mycol 26:105–111CrossRefPubMedGoogle Scholar
  60. Musatti CC, Peraçoli MTS, Soares AMVC, Rezkallah-Iwasso MT (1994) Cell-mediated immunity in patients with Paracoccidioidomycosis. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 175–186Google Scholar
  61. Naiff RD, Ferreira LC, Barrett TV et al (1986) Enzootic paracoccidioidomycosis in armadillos (Dasypus novemcinctus) in the state of Pará. Rev Inst Med Trop São Paulo 28:19–27CrossRefPubMedGoogle Scholar
  62. Nóbrega JPS, Spina-França A (1994) Neuroparacocidioidomycosis. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 321–330Google Scholar
  63. Oliveira GG, Silveira LH, Itano EN et al (2011) Serological evidence of Paracoccidioides brasiliensis infection in chickens from Paraná and Mato Grosso do Sul states, Brazil. Mycopathologia 171:197–202.  https://doi.org/10.1007/s11046-010-9366-6 CrossRefPubMedGoogle Scholar
  64. Oliveira GG, Navarro IT, Freire RL et al (2012) Serological survey of Paracoccidioidomycosis in sheep. Mycopathologia 173:63–68.  https://doi.org/10.1007/s11046-011-9463-1 CrossRefPubMedGoogle Scholar
  65. Oñate JM, Tobón AM, Restrepo A (2002) Adrenal gland insufficiency secondary to paracoccidioidomycosis. Biomédica 22:280–286CrossRefPubMedGoogle Scholar
  66. Ono MA, Bracarense AP, Morais HS et al (2001) Canine paracoccidioidomycosis: a seroepidemiologic study. Med Mycol 39:277–282CrossRefPubMedGoogle Scholar
  67. Ono MA, Kishima MO, Itano EN et al (2003) Experimental paracoccidioidomycosis in dogs. Med Mycol 41:265–268CrossRefPubMedGoogle Scholar
  68. Paniago AMM, Aguiar JIA, Aguiar ES et al (2003) Paracoccidioidomycosis: a clinical and epidemiological study of 422 cases observed in Mato Grosso do Sul. Rev Soc Bras Med Trop 36:455–459CrossRefPubMedGoogle Scholar
  69. Peraçoli MT, Mota NG, Montenegro MR (1982) Experimental paracoccidioidomycosis in the Syrian hamster. Morphology and correlation of lesions with humoral and cell-mediated immunity. Mycopathologia 79:7–17CrossRefPubMedGoogle Scholar
  70. Peraçoli MTS, Kurokawa CS, Calvi SA et al (2003) Production of pro- and anti-inflammatory cytokines by monocytes from patients with paracoccidioidomycosis. Microbes Infect 5:413–418CrossRefPubMedGoogle Scholar
  71. Restrepo A (1985) The ecology of Paracoccidioides brasiliensis: a puzzle still unsolved. Sabouraudia 23:323–334CrossRefPubMedGoogle Scholar
  72. Restrepo A, Salazar ME, Cano LE et al (1984) Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis. Infect Immun 46:346–353PubMedPubMedCentralGoogle Scholar
  73. Restrepo A, Baumgardner D, Bagagli E et al (2000) Clues to the presence of pathogenic fungi in certain environments. Med Mycol 38:67–77CrossRefPubMedGoogle Scholar
  74. Restrepo A, McEwen JG, Castañeda E (2001) The habitat of Paracoccidioides brasiliensis: how far from solving the riddle? Med Mycol 39:233–241CrossRefPubMedGoogle Scholar
  75. Restrepo-Moreno A (1994) Ecology of Paracoccidioides brasiliensis. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 121–129Google Scholar
  76. Ricci G, Mota FT, Wakamatsu A et al (2004) Canine paracoccidioidomycosis. Med Mycol 42:379–383CrossRefPubMedGoogle Scholar
  77. Richini-Pereira VB, Bosco SDMG, Macoris SDG et al (2008a) Detecção de Paracoccidioides brasiliensis em tatus (Dasypus novemcinctus) provenientes de uma reserva de Cerrado do Instituto Lauro de Souza Lima (Bauru, SP). BEPA Bol Epidemiol Paul 5:4–8Google Scholar
  78. Richini-Pereira VB, Bosco SDMG, Griese J et al (2008b) Molecular detection of Paracoccidioides brasiliensis in road-killed wild animals. Med Mycol 46:35–40CrossRefPubMedGoogle Scholar
  79. Richini-Pereira VB, Bosco SM, Theodoro RC et al (2009) Importance of xenarthrans in the eco-epidemiology of Paracoccidioides brasiliensis. BMC Res Notes 2:228CrossRefPubMedPubMedCentralGoogle Scholar
  80. Salazar ME, Restrepo A, Stevens DA (1988) Inhibition by estrogens of conidium-to-yeast conversion in the fungus Paracoccidioides brasiliensis. Infect Immun 56:711–713PubMedPubMedCentralGoogle Scholar
  81. Santos WA, da Silva BM, Passos ED et al (2003) Association between smoking and paracoccidioidomycosis: a case-control study in the state of Espírito Santo, Brazil. Cad Saúde Pública 19:245–253CrossRefPubMedGoogle Scholar
  82. Sbeghen MR, Zanata TB, Macagnan R et al (2015) Paracoccidioides brasiliensis infection in small wild mammals. Mycopathologia 180:435–440.  https://doi.org/10.1007/s11046-015-9928-8 CrossRefPubMedGoogle Scholar
  83. Shikanai-Yasuda MA, Telles Filho FDQ, Mendes RP et al (2006) Guidelines in paracoccidioidomycosis. Rev Soc Bras Med Trop 39:297–310CrossRefPubMedGoogle Scholar
  84. Silva-Vergara ML, Martinez R, Camargo ZP et al (2000) Isolation of Paracoccidioides brasiliensis from armadillos (Dasypus novemcinctus) in an area where the fungus was recently isolated from soil. Med Mycol 38:193–199CrossRefPubMedGoogle Scholar
  85. Silveira LH, Domingos IH, Kouchi K et al (2006) Serological detection of antibodies against Paracoccidioides brasiliensis in dogs with leishmaniasis. Mycopathologia 162:325–329.  https://doi.org/10.1007/s11046-006-0046-5 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Silveira LH, Paes RCS, Medeiros EV et al (2008) Occurrence of antibodies to Paracoccidioides brasiliensis in dairy cattle from Mato Grosso do Sul, Brazil. Mycopathologia 165:367–371.  https://doi.org/10.1007/s11046-008-9095-2 CrossRefPubMedGoogle Scholar
  87. Singer-Vermes LM, Burger E, Russo M et al (1993) Advances in experimental paracoccidioidomycosis using an isogenic murine model. Arch Med Res 24:239–245PubMedGoogle Scholar
  88. Soares AM, Peraçoli MT, Dos Santos RR (2000) Correlation among immune response, morphogenesis of the granulomatous reaction and spleen lymphoid structure in murine experimental paracoccidioidomycosis. Med Mycol 38:371–377CrossRefPubMedGoogle Scholar
  89. Splendore A (1912) Zimonematosi con localizzazione nella cavita della bocca osservata nel Brasile. Bull Soc Path 5:313–319Google Scholar
  90. Tani EM, Franco M, Peraçoli MT, Montenegro MR (1987) Experimental pulmonary paracoccidioidomycosis in the Syrian hamster: morphology and correlation of lesions with the immune response. J Med Vet Mycol 25:291–300CrossRefPubMedGoogle Scholar
  91. Teixeira MDM, Theodoro RC, Nino-Vega G et al (2014a) Paracoccidioides species complex: ecology, phylogeny, sexual reproduction, and virulence. PLoS Pathog 10:e1004397.  https://doi.org/10.1371/journal.ppat.1004397 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Teixeira MDM, Theodoro RC, Oliveira FFM et al (2014b) Paracoccidioides lutzii sp. nov.: biological and clinical implications. Med Mycol 52:19–28.  https://doi.org/10.3109/13693786.2013.794311 CrossRefGoogle Scholar
  93. Teles AJ, Klafke GB, Cabana ÂL et al (2015) Serological investigation into Paracoccidioides brasiliensis infection in dogs from southern Rio Grande do Sul, Brazil. Mycopathologia 181(3-4):323–328.  https://doi.org/10.1007/s11046-015-9972-4 CrossRefPubMedGoogle Scholar
  94. Theodoro RC, Candeias JMG, Araújo JP et al (2005) Molecular detection of Paracoccidioides brasiliensis in soil. Med Mycol 43:725–729CrossRefPubMedGoogle Scholar
  95. Theodoro RC, Volkmann G, Liu X-Q, Bagagli E (2011) PRP8 intein in Ajellomycetaceae family pathogens: sequence analysis, splicing evaluation and homing endonuclease activity. Fungal Genet Biol 48:80–91.  https://doi.org/10.1016/j.fgb.2010.07.010 CrossRefPubMedGoogle Scholar
  96. Theodoro RC, Teixeira MDM, Felipe MSS et al (2012) Genus Paracoccidioides: species recognition and biogeographic aspects. PLoS One 7:e37694.  https://doi.org/10.1371/journal.pone.0037694 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Trejo-Chávez A, Ramírez-Romero R, Ancer-Rodríguez J et al (2011) Disseminated paracoccidioidomycosis in a southern two-toed sloth (Choloepus didactylus). J Comp Pathol 144:231–234.  https://doi.org/10.1016/j.jcpa.2010.08.012 CrossRefPubMedGoogle Scholar
  98. Turissini DA, Gomez OM, Teixeira MM, Mcewen JG, Matute DR (2017) Species boundaries in the human pathogen Paracoccidioides. Fungal Genet Biol 106:9–25CrossRefPubMedGoogle Scholar
  99. Untereiner WA, Scott JA, Naveau FA et al (2004) The Ajellomycetaceae, a new family of vertebrate-associated Onygenales. Mycologia 96:812–821CrossRefPubMedGoogle Scholar
  100. Vilela R, Rosa PS, Belone AFF et al (2009) Molecular phylogeny of animal pathogen Lacazia loboi inferred from rDNA and DNA coding sequences. Mycol Res 113:851–857.  https://doi.org/10.1016/j.mycres.2009.04.007 CrossRefPubMedGoogle Scholar
  101. Wanke B, Londero AT (1994) Epidemiology and Paracoccidioidomycosis infection. In: Franco M, Lacaz CDS, Restrepo-Moreno A, Negro GD (eds) Paracoccidioidomycosis. CRC Press, Boca Raton, pp 109–119Google Scholar
  102. Weber SAT, Brasolotto A, Rodrigues L et al (2006) Dysphonia and laryngeal sequelae in paracoccidioidomycosis patients: a morphological and phoniatric study. Med Mycol 44:219–225.  https://doi.org/10.1080/13693780500340320 CrossRefPubMedGoogle Scholar
  103. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sandra de Moraes Gimenes Bosco
    • 1
  • Eduardo Bagagli
    • 1
  1. 1.Department of Microbiology and ImmunologyInstitute of Biosciences, UNESPBotucatuBrazil

Personalised recommendations