Abstract
Cryptococcosis is one of the major life-threatening opportunistic/systemic fungal diseases of worldwide occurrence, which can be asymptomatic or establish pneumonia and meningoencephalitis mainly in immunosuppressed patients, caused by the Cryptococcus neoformans and C. gattii species complexes. Acquisition is by inhaling fungal propagules from avian droppings, tree hollows and decaying wood, and the association of the molecular types with geographic origin, virulence and antifungal resistance have epidemiological importance. Since data on cryptococcosis in Alagoas are limited, we sought to determine the molecular types of etiological agents collected from clinical and environmental sources. We evaluated 21 isolates previously collected from cerebrospinal fluid and from environment sources (pigeon droppings and tree hollows) in Maceió-Alagoas (Brazil). Restriction fragment length polymorphism of URA5 gene was performed to characterize among the eight standard molecular types (VNI-VNIV and VGI-VGIV). Among isolates, 66.67% (14) were assigned to C. neoformans VNI – 12 of them (12/14) recovered from liquor and 2 from a tree hollow (2/14). One isolate from pigeon droppings (4.76%) corresponded to C. neoformans VNIV, while five strains from tree hollows and one from pigeon droppings (6, 28.57%) to C. gattii VGII. VNI-type was present in clinical and environmental samples and most C. neoformans infections were observed in HIV-positive patients, while types VNIV and VGII were prevalent in environmental sources in Alagoas. This is the first molecular characterization of Cryptococcus spp. in Alagoas, our study provides additional information on the ecoepidemiology of Cryptococcus spp. in Brazil, contributing to a closer view of the endemic species.
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References
May RC, Stone NRH, Wiesner DL et al (2016) Cryptococcus: from environmental saprophyte to global pathogen. Nat Rev Microbiol 14:106–117. https://doi.org/10.1038/nrmicro.2015.6
Lin X, Heitman J (2006) The Biology of the Cryptococcus neoformans Species Complex. Annu Rev Microbiol 60:69–105. https://doi.org/10.1146/annurev.micro.60.080805.142102
Maziarz EK, Perfect JR (2016) Cryptococcosis. Infect Dis Clin North Am 30:179–206. https://doi.org/10.1016/j.idc.2015.10.006
Cogliati M, Patrizia P, Vincenzo C et al (2020) Cryptococcus neoformans species complex isolates living in a tree micro-ecosystem. Fungal Ecol 44. https://doi.org/10.1016/j.funeco.2019.100889
Rajasingham R, Govender NP, Jordan A et al (2022) The global burden of HIV-associated cryptococcal infection in adults in 2020: a modelling analysis. Lancet Infect Dis 22:1748–1755. https://doi.org/10.1016/S1473-3099(22)00499-6
Henao-Martínez AF, Chastain DB, Franco-Paredes C (2018) Treatment of cryptococcosis in non-HIV immunocompromised patients. Curr Opin Infect Dis 31:278–285. https://doi.org/10.1097/QCO.0000000000000458
Wanderlei Silva DM, de Albuquerque Maranhao FC (2015) Current status of the Diagnostic and Genomics of Cryptococcus neoformans/C. Gattii Species Complex. Fungal Genomics Biol 05:2–5. https://doi.org/10.4172/2165-8056.1000e118
World Health Organization (2022) WHO fungal priority pathogens list to guide research, development and public health action. WHO
Meyer W, Aanensen DM, Boekhout T et al (2009) Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol 47:561–570. https://doi.org/10.1080/13693780902953886
Cogliati M, Desnos-Ollivier M, McCormick-Smith I et al (2019) Genotypes and population genetics of neoformans and gattii species complexes in Europe and the mediterranean area. Fungal Genet Biol 129:16–29. https://doi.org/10.1016/j.fgb.2019.04.001
Firacative C, Trilles L, Meyer W (2022) Recent advances in and cryptococcosis. Microorganisms 10:2022–2024. https://doi.org/10.3390/microorganisms10010013
Chen SCA, Meyer W, Sorrell TC (2014) Cryptococcus gattii infections. Clin Microbiol Rev 27:980–1024. https://doi.org/10.1128/CMR.00126-13
Meyer W, Gilgado F, Ngamskulrungroj P et al (2011) Molecular typing of the Cryptococcus neoformans/Cryptococcus gattii species Complex. Cryptococcus: from human pathogen to model yeast. ASM, p 434
Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG (2006) Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. Grubii (serotype A), including a unique population in Botswana. Genetics 172:2223–2238. https://doi.org/10.1534/GENETICS.105.046672
Ferreira-Paim K, Andrade-Silva L, Fonseca FM et al (2017) MLST-Based Population Genetic Analysis in a global context reveals clonality amongst Cryptococcus neoformans var. Grubii VNI isolates from HIV patients in Southeastern Brazil. PLoS Negl Trop Dis 11:e0005223. https://doi.org/10.1371/journal.pntd.0005223
Farrer RA, Chang M, Davis MJ et al (2019) A New Lineage of Cryptococcus gattii (VGV) discovered in the Central Zambezian Miombo Woodlands. MBio 10:1–19. https://doi.org/10.1128/mBio.02306-19
Hagen F, Khayhan K, Theelen B et al (2015) Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol 78:16–48. https://doi.org/10.1016/j.fgb.2015.02.009
Taverna CG, Bosco-Borgeat ME, Mazza M et al (2020) Frequency and geographical distribution of genotypes and mating types of Cryptococcus neoformans and Cryptococcus gattii species complexes in Argentina. Rev Argent Microbiol 52:183–188. https://doi.org/10.1016/J.RAM.2019.07.005
Kwon-Chung KJ, Bennett JE, Wickes BL et al (2017) The case for adopting the species Complex nomenclature for the Etiologic agents of Cryptococcosis. mSphere 2:e00357–e00316. https://doi.org/10.1128/mSphere.00357-16
Hagen F, Lumbsch HT, Arsic Arsenijevic V et al (2017) Importance of resolving Fungal nomenclature: the case of multiple pathogenic species in the Cryptococcus Genus. mSphere 2:1–13. https://doi.org/10.1128/msphere.00238-17
Beardsley J, Dao A, Keighley C et al (2023) What’s New in Cryptococcus gattii: from bench to Bedside and Beyond. J Fungi 9:41. https://doi.org/10.3390/jof9010041
Trilles L, Lazéra M dos, Wanke S B, et al (2008) Regional pattern of the molecular types of Cryptococcus neoformans and Cryptococcus gattii in Brazil. Mem Inst Oswaldo Cruz 103:455–462. https://doi.org/10.1590/S0074-02762008000500008
Firacative C, Meyer W, Castañeda E (2021) Cryptococcus neoformans and Cryptococcus gattii species complexes in latin America: a map of molecular types, genotypic diversity, and antifungal susceptibility as reported by the latin American cryptococcal study group. J Fungi 7. https://doi.org/10.3390/jof7040282
Firacative C, Lizarazo J, Illnait-Zaragozí MT et al (2018) The status of cryptococcosis in Latin America. Mem Inst Oswaldo Cruz 113:1–23. https://doi.org/10.1590/0074-02760170554
Martins LMS, Wanke B, Lazéra M dos S, et al (2011) Genotypes of Cryptococcus neoformans and Cryptococcus gattii as agents of endemic cryptococcosis in Teresina, Piauí (northeastern Brazil). Mem Inst Oswaldo Cruz 106:725–730. https://doi.org/10.1590/S0074-02762011000600012
do Carmo FN, de Camargo Fenley J, Garcia MT et al (2022) Cryptococcus spp. and Cryptococcosis: focusing on the infection in Brazil. Brazilian J Microbiol 53:1321–1337. https://doi.org/10.1007/s42770-022-00744-y
Ferrer C, Colom F, Frasés S et al (2001) Detection and identification of fungal pathogens by PCR and by ITS2 and 5.8S ribosomal DNA typing in ocular infections. J Clin Microbiol 39:2873–2879. https://doi.org/10.1128/JCM.39.8.2873-2879.2001
Júnior JL, Laerte V, Júnior P et al Revista de Medicina e Saúde de Brasília EDITORIAL Implantação da Rede de Criptococose Brasil no Distrito Federal - RCB-DF. Rev Med e Saúde Brasília 4–6
Meyer W, Castañeda A, Jackson S et al (2003) Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg Infect Dis 9:189–195. https://doi.org/10.3201/eid0902.020246
Vélez N, Escandón P (2016) Distribution and association between environmental and clinical isolates of Cryptococcus neoformans in bogotá-Colombia, 2012–2015. Mem Inst Oswaldo Cruz 111:642–648. https://doi.org/10.1590/0074-02760160201
Rajasingham R, Smith RM, Park BJ et al (2017) Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect Dis 17:873–881. https://doi.org/10.1016/S1473-3099(17)30243-8
Aguiar PADF, Pedroso R, dos Sebastião S BA, et al (2017) The epidemiology of cryptococcosis and the characterization of Cryptococcus neoformans isolated in a Brazilian University Hospital. Rev Inst Med Trop Sao Paulo 59:63–69
da Silva LBB, Bock D, Klafke GBB et al (2020) Cryptococcosis in HIV-AIDS patients from Southern Brazil: still a major problem. J Mycol Med 30:101044. https://doi.org/10.1016/j.mycmed.2020.101044
BRASIL. Ministério da Saúde (2020) Boletim Epidemiológico HIV / Aids | 2020. Secr Vigilância em Saúde 1:68
de Sousa Tsujisaki RA, Paniago AMM, da Costa Lima Júnior MS et al (2013) First molecular typing of Cryptococcemia-causing Cryptococcus in Central-West Brazil. Mycopathologia 176:267–272. https://doi.org/10.1007/s11046-013-9676-6
Favalessa OC, de Paula DAJ, Dutra V et al (2014) Molecular typing and in vitro antifungal susceptibility of Cryptococcus spp from patients in Midwest Brazil. J Infect Dev Ctries 8:1037–1043. https://doi.org/10.3855/jidc.4446
Fang W, Fa Z, Liao W (2015) Epidemiology of Cryptococcus and cryptococcosis in China. Fungal Genet Biol 78:7–15. https://doi.org/10.1016/j.fgb.2014.10.017
Mora DJ, Pedrosa AL, Rodrigues V et al (2010) Genotype and mating type distribution within clinical Cryptococcus neoformans and Cryptococcus gattii isolates from patients with cryptococcal meningitis in Uberaba, Minas Gerais, Brazil. Med Mycol 48:561–569. https://doi.org/10.3109/13693780903358317
Nascimento E, Barião PHG, von Kress MR Z, et al (2021) Cryptococcosis by Cryptococcus neoformans/Cryptococcus gattii species complexes in non-HIV-Infected patients in Southeastern Brazil. Rev Soc Bras Med Trop 54:1–7. https://doi.org/10.1590/0037-8682-0169-2021
Oliveira EP, Inácio CP, de Freitas JF et al (2022) Tuberculosis and neurocryptococcosis by Cryptococcus neoformans molecular type VNI in a non-HIV patient: a comorbidities case report. J Med Mycol 32. https://doi.org/10.1016/j.mycmed.2021.101213
Watkins R, King J, Johnston S (2017) Nutritional requirements and their importance for virulence of pathogenic Cryptococcus species. Microorganisms 5:65. https://doi.org/10.3390/microorganisms5040065
Ellis DH, Pfeiffer TJ (1990) Natural habitat of Cryptococcus neoformans var. Gattii. J Clin Microbiol 28:1642–1644. https://doi.org/10.1128/jcm.28.7.1642-1644.1990
Trilles L, Lazéra M, Wanke B et al (2003) Genetic characterization of environmental isolates of the Cryptococcus neoformans species complex from Brazil
Barbosa GG, Trilles L, Wanke B, Lazéra MS (2013) Cryptococcus Gattii VGI and Cryptococcus neoformans VNI Associated with Wood Decay in Ficus Hollow Trees in Rio De Janeiro, Brazil. Br Microbiol Res J 3:106–115
Costa S do, P, Lazéra M dos, Santos S et al (2009) WRRA, First isolation of Cryptococcus gattii molecular type VGII and Cryptococcus neoformans molecular type VNI from environmental sources in the city of Belém, Pará, Brazil. Mem Inst Oswaldo Cruz 104:662–664. https://doi.org/10.1590/S0074-02762009000400023
Nielsen K, De Obaldia AL, Heitman J (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6:949–959. https://doi.org/10.1128/EC.00097-07
Teodoro VLI, Gullo FPPP, Sardi J (2013) de COJ de CO, Environmental isolation, biochemical identification, and antifungal drug susceptibility of Cryptococcus species. Rev Soc Bras Med Trop 46:759–764. https://doi.org/10.1590/0037-8682-0025-2013
Cogliati M (2021) Global warming impact on the expansion of fundamental niche of Cryptococcus gattii VGI in Europe. Environ Microbiol Rep 13:375–383. https://doi.org/10.1111/1758-2229.12945
Kidd SE, Hagen F, Tscharke RL et al (2004) A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci 101:17258–17263. https://doi.org/10.1073/pnas.0402981101
Herkert PF, Hagen F, de Oliveira Salvador GL et al (2016) Molecular characterisation and antifungal susceptibility of clinical Cryptococcus deuterogattii (AFLP6/VGII) isolates from Southern Brazil. Eur J Clin Microbiol Infect Dis 35:1803–1810. https://doi.org/10.1007/s10096-016-2731-8
Gago S, Serrano C, Alastruey-Izquierdo A et al (2017) Molecular identification, antifungal resistance and virulence of Cryptococcus neoformans and Cryptococcus deneoformans isolated in Seville. Spain Mycoses 60:40–50. https://doi.org/10.1111/myc.12543
Cogliati M (2013) Global Molecular Epidemiology of Cryptococcus neoformans and Cryptococcus gattii: an Atlas of the molecular types. Scientifica (Cairo) 2013:1–23. https://doi.org/10.1155/2013/675213
Casadevall A, Freij JB, Hann-Soden C, Taylor J (2017) Continental Drift and Speciation of the Cryptococcus neoformans and Cryptococcus gattii Species Complexes. mSphere 2:e00103-17-6
Cogliati M, Zani A, Rickerts V et al (2016) Multilocus sequence typing analysis reveals that Cryptococcus neoformans var. Neoformans is a recombinant population. Fungal Genet Biol 87:22–29. https://doi.org/10.1016/j.fgb.2016.01.003
Medeiros Ribeiro Â, Silva LKRE, Silveira Schrank I et al (2006) Isolation of Cryptococcus neoformans var. Neoformans serotype D from Eucalypts in South Brazil. Med Mycol 44:707–713. https://doi.org/10.1080/13693780600917209
Araújo Mjaneck, Marinho M (2023) Diversity of potencial pathogenic Cryptococcus species isolated from environment in country side São Paulo state, Brazil. Peer Rev 5:25–41. https://doi.org/10.53660/744.prw1920b
Andrade-Silva LE, Ferreira-Paim K, Ferreira TB et al (2018) Genotypic analysis of clinical and environmental Cryptococcus neoformans isolates from Brazil reveals the presence of VNB isolates and a correlation with biological factors. PLoS ONE 13:e0193237. https://doi.org/10.1371/journal.pone.0193237
Trilles L, Meyer W, Wanke B et al (2012) Correlation of antifungal susceptibility and molecular type within the Cryptococcus neoformans/C. Gattii species complex. Med Mycol 50:328–332. https://doi.org/10.3109/13693786.2011.602126
Grizante Barião PH, Tonani L, Cocio TA et al (2020) Molecular typing, in vitro susceptibility and virulence of Cryptococcus neoformans/Cryptococcus gattii species complex clinical isolates from south-eastern Brazil. Mycoses 63:1341–1351. https://doi.org/10.1111/myc.13174
BRASIL. Ministério da Saúde (2020) Portaria No 264, De 17 De Fevereiro De 2020. Diário Of. da União 17–19
Alves Soares E, Lazera M, dos Wanke S B, et al (2019) Mortality by cryptococcosis in Brazil from 2000 to 2012 a descriptive epidemiological study. PLoS Negl Trop Dis 13:1–17. https://doi.org/10.1371/journal.pntd.0007569
Ribeiro N, de Costa Q, Magalhães MC TFF, et al (2017) Atorvastatin as a promising anticryptococcal agent. Int J Antimicrob Agents 49:695–702. https://doi.org/10.1016/j.ijantimicag.2017.04.005
Giro A (2021) Review on Cryptococcus Disease. J Trop Dis Public Heal 9:1–6
Howard-Jones AR, Sparks R, Pham D et al (2022) Pulmonary cryptococcosis. J Fungi 8:1156. https://doi.org/10.3390/jof8111156
Kaul DR, Vece G, Blumberg E et al (2021) Ten years of donor-derived disease: a report of the disease transmission advisory committee. Am J Transpl 21:689–702. https://doi.org/10.1111/ajt.16178
Revenga F, Paricio JF, Merino FJ et al (2002) Primary cutaneous cryptococcosis in an Immunocompetent host: Case Report and Review of the literature. Dermatology 204:145–149. https://doi.org/10.1159/000051835
Norman SA, Raverty S, Zabek E et al (2011) Maternal–fetal transmission of Cryptococcus gattii in Harbor Porpoise. Emerg Infect Dis 17:304–305. https://doi.org/10.3201/eid1702.101232
Danesi P, Falcaro C, Schmertmann LJ et al (2021) Cryptococcus in wildlife and free-living mammals. J Fungi 7:1–23. https://doi.org/10.3390/jof7010029
Siqueira NP, Favalessa OC, Maruyama FH et al (2022) Domestic birds as source of Cryptococcus deuterogattii (AFLP6/VGII): potential risk for Cryptococcosis. Mycopathologia 187:103–111. https://doi.org/10.1007/s11046-021-00601-w
Sephton-Clark P, McConnell SA, Grossman N et al (2023) Similar evolutionary trajectories in an environmental Cryptococcus neoformans isolate after human and murine infection. Proc Natl Acad Sci 120:2017. https://doi.org/10.1073/pnas.2217111120
Alves GSB, Freire AKL, Bentes A dos S, et al (2016) Molecular typing of environmental Cryptococcus neoformans/C. Gattii species complex isolates from Manaus. Amazonas Brazil Mycoses 59:509–515. https://doi.org/10.1111/myc.12499
Jalene Alves M, Sadalla do Nascimento I, Santana Cruz K et al (2022) Cryptococcosis in HIV/AIDS patients in northern Brazil: clinical aspects, molecular types and isolation of agents from environmental samples associated with patients. Trop Med Int Heal 27:387–396. https://doi.org/10.1111/tmi.13737
dos Santos Bentes A, Wanke B, dos Santos Lazéra M et al (2019) Cryptococcus Gattii VGII isolated from native forest and river in Northern Brazil. Brazilian J Microbiol 50:495–500. https://doi.org/10.1007/s42770-019-00066-6
Brito-Santos F, Barbosa GG, Trilles L et al (2015) Environmental isolation of gattii VGII from indoor dust from typical wooden houses in the deep Amazonas of the Rio Negro basin. PLoS ONE 10:1–11. https://doi.org/10.1371/journal.pone.0115866
Brito-Santos F, Trilles L, Firacative C et al (2020) Indoor dust as a source of virulent strains of the agents of cryptococcosis in the rio negro micro-region of the Brazilian Amazon. Microorganisms 8:1–11. https://doi.org/10.3390/microorganisms8050682
Freire AKL, dos Santos Bentes A, de Lima Sampaio I et al (2012) Molecular characterisation of the causative agents of cryptococcosis in patients of a tertiary healthcare facility in the state of Amazonas-Brazil. Mycoses 55:e145–e150. https://doi.org/10.1111/j.1439-0507.2012.02173.x
Khell Da Silva B, Freire AK, Dos Santos Bentes A et al (2012) Characterization of clinical isolates of the Cryptococcus neoformans-Cryptococcus gattii species complex from the Amazonas State in Brazil. Rev Iberoam Micol 29:40–43. https://doi.org/10.1016/j.riam.2011.05.003
Pinheiro SB, Sousa ES, Cortez ACA et al (2021) Cryptococcal meningitis in non-HIV patients in the State of Amazonas, Northern Brazil. Brazilian J Microbiol 52:279–288. https://doi.org/10.1007/s42770-020-00383-1
Fernando Silva Rocha D, Cruz KS, da Silva Santos CS et al (2018) MLST reveals a clonal population structure for Cryptococcus neoformans molecular type VNI isolates from clinical sources in Amazonas, Northern-Brazil. PLoS ONE 13:1–15. https://doi.org/10.1371/journal.pone.0197841
Matos CS, De Souza Andrade A, Oliveira NS, Barros TF (2012) Microbiological characteristics of clinical isolates of Cryptococcus spp. in Bahia, Brazil: Molecular types and antifungal susceptibilities. Eur J Clin Microbiol Infect Dis 31:1647–1652. https://doi.org/10.1007/s10096-011-1488-3
Ribeiro MA, Ngamskulrungroj P (2008) Molecular characterization of environmental Cryptococcus neoformans isolated in Vitoria, ES, Brazil. Rev Inst Med Trop Sao Paulo 50:315–320. https://doi.org/10.1590/S0036-46652008000600001
Souza LKHH, Souza Junior AH, Costa CR et al (2010) Molecular typing and antifungal susceptibility of clinical and environmental Cryptococcus neoformans species complex isolates in Goiania. Brazil Mycoses 53:62–67. https://doi.org/10.1111/j.1439-0507.2008.01662.x
Anzai MC, Dos Santos Lazéra M, Wanke B et al (2014) Cryptococcus Gattii VGII in a Plathymenia reticulata hollow in Cuiabá, Mato Grosso, Brazil. Mycoses 57:414–418. https://doi.org/10.1111/myc.12177
Maruyama FH, de Paula DAJ, de Menezes I G, et al (2019) Genetic diversity of the Cryptococcus Gattii Species Complex in Mato Grosso State, Brazil. Mycopathologia 184:45–51. https://doi.org/10.1007/s11046-018-0313-2
Nunes J, de O, Tsujisaki RA, de Nunes S, de O M et al (2018) Cryptococcal meningitis epidemiology: 17 years of experience in a state of the Brazilian pantanal. Rev Soc Bras Med Trop 51:485–492. https://doi.org/10.1590/0037-8682-0050-2018
Andrade-Silva L, Ferreira-Paim K, Silva-Vergara ML, Pedrosa AL (2010) Molecular characterization and evaluation of virulence factors of Cryptococcus laurentii and Cryptococcus neoformans strains isolated from external hospital areas. Fungal Biol 114:438–445. https://doi.org/10.1016/j.funbio.2010.03.005
Damasceno-Escoura AH, de Souza ML, de Oliveira Nunes F et al (2019) Epidemiological, clinical and Outcome aspects of patients with Cryptococcosis caused by Cryptococcus gattii from a non-endemic area of Brazil. Mycopathologia 184:65–71. https://doi.org/10.1007/s11046-018-0304-3
Ferreira-Paim K, Andrade-Silva L, Mora DJ et al (2011) Genotyping of Cryptococcus neoformans isolated from captive birds in Uberaba, Minas Gerais, Brazil. https://doi.org/10.1111/j.1439-0507.2010.01901.x. Mycoses 54:
Leão CA, Ferreira-Paim K, Andrade-Silva L et al (2011) Primary cutaneous cryptococcosis caused by Cryptococcus gattii in an immunocompetent host. Med Mycol 49:352–355. https://doi.org/10.3109/13693786.2010.530697
Headley SA, Di Santis GW, de Alcântara BK et al (2015) Cryptococcus Gattii-Induced infections in Dogs from Southern Brazil. Mycopathologia 180:265–275. https://doi.org/10.1007/s11046-015-9901-6
Lugarini C, Goebel CS, Condas LAZ et al (2008) Cryptococcus neoformans isolated from passerine and psittacine bird excreta in the state of Paraná. Brazil Mycopathologia 166:61–69. https://doi.org/10.1007/s11046-008-9122-3
dos Santos WRA, Meyer W, Wanke B et al (2008) Primary endemic cryptococcosis gattii by molecular type VGII in the state of Pará, Brazil. Mem Inst Oswaldo Cruz 103:813–818. https://doi.org/10.1590/S0074-02762008000800012
Brito-Santos F, Reis RS, Coelho RA et al (2019) Cryptococcosis due to Cryptococcus Gattii VGII in Southeast Brazil: the One Health approach revealing a possible role for domestic cats. Med Mycol Case Rep 24:61–64. https://doi.org/10.1016/j.mmcr.2019.04.004
Pinto Junior VL, Pone MV da, Pone S et al (2010) SM, Cryptococcus gattii molecular type VGII as agent of meningitis in a healthy child in Rio de Janeiro, Brazil: report of an autochthonous case. Rev Soc Bras Med Trop 43:746–748. https://doi.org/10.1590/S0037-86822010000600032
Reis RS, Bonna ICF, Antonio IM da S, et al (2021) Cryptococcus neoformans VNII as the Main cause of cryptococcosis in domestic cats from Rio De Janeiro, Brazil. J Fungi 7:980. https://doi.org/10.3390/jof7110980
Vechi HT, Theodoro RC, de Oliveira AL et al (2019) Invasive fungal infection by Cryptococcus neoformans var. Grubii with bone marrow and meningeal involvement in a HIV-infected patient: a case report. BMC Infect Dis 19:1–8. https://doi.org/10.1186/s12879-019-3831-8
Wirth F, Azevedo MI, Goldani LZ (2018) Molecular types of Cryptococcus species isolated from patients with cryptococcal meningitis in a Brazilian tertiary care hospital. Brazilian J Infect Dis 22:495–498. https://doi.org/10.1016/j.bjid.2018.11.002
Dal Pupo HD, Sena BAG, Reis FCG et al (2019) Polysaccharide diversity in VNI isolates of Cryptococcus neoformans from Roraima, Northern Brazil. Fungal Biol 123:699–708. https://doi.org/10.1016/j.funbio.2019.06.003
Cardoso PHM, Baroni FDA, Silva EG et al (2013) Feline Nasal Granuloma due to Cryptoccocus gattii type VGII. Mycopathologia 176:303–307. https://doi.org/10.1007/s11046-013-9686-4
Castro e Silva DMM, Santos DC, CS, Martins MAA et al (2016) First isolation of Cryptococcus neoformans genotype VNI MAT-alpha from wood inside hollow trunks of Hymenaea courbaril. Med Mycol 54:97–102. https://doi.org/10.1093/mmy/myv066
FIGUEIREDO TP, LUCAS RC de CAZZANIGARA et al (2016) Antifungal susceptibility testing and genotyping characterization of cryptococcus neoformans and gattii isolates from hiv-infected patients of Ribeirão Preto, São Paulo, Brazil. Rev Inst Med Trop Sao Paulo 58. https://doi.org/10.1590/S1678-9946201658069
Nascimento E, Vitali LH, Tonani L et al (2016) Refractory and/or relapsing Cryptococcosis Associated with Acquired Immune Deficiency Syndrome: clinical features, genotype, and virulence factors of Cryptococcus spp. Isolates. Am J Trop Med Hyg 94:975–981. https://doi.org/10.4269/ajtmh.15-0595
da Silva EC, Guerra JM, Torres LN et al (2017) Cryptococcus Gattii molecular type VGII infection associated with lung disease in a goat. BMC Vet Res 13:4–9. https://doi.org/10.1186/s12917-017-0950-6
Ponzio V, Chen Y, Rodrigues AM et al (2019) Genotypic diversity and clinical outcome of cryptococcosis in renal transplant recipients in Brazil. Emerg Microbes Infect 8:119–129. https://doi.org/10.1080/22221751.2018.1562849
de Abreu DPB, Machado CH, Makita MT et al (2017) Intestinal Lesion in a dog due to Cryptococcus gattii type VGII and review of published cases of Canine Gastrointestinal Cryptococcosis. Mycopathologia 182:597–602. https://doi.org/10.1007/s11046-016-0100-x
Silva DC, Martins MA, Szeszs MW et al (2012) Susceptibility to antifungal agents and genotypes of Brazilian clinical and environmental Cryptococcus gattii strains. Diagn Microbiol Infect Dis 72:332–339. https://doi.org/10.1016/j.diagmicrobio.2011.11.016
de Sousa HR, de Oliveira GP, Frazão S, de O et al (2022) Faster Cryptococcus Melanization increases virulence in experimental and human cryptococcosis. J Fungi 8. https://doi.org/10.3390/jof8040393
Favalessa OC, Lázera M, dos S, Wanke B et al (2014) Fatal Cryptococcus gattii genotype AFLP6/VGII infection in a HIV-negative patient: case report and a literature review. Mycoses 57:639–643. https://doi.org/10.1111/myc.12210
de Faria Ferreira M, Brito-Santos F, Henrique Nascimento Theodoro P et al (2022) Mixed infection by Cryptococcus neoformans and Cryptococcus gattii and coinfection with paracoccidioidomycosis in PLHIV. Med Mycol Case Rep 35:48–50. https://doi.org/10.1016/j.mmcr.2022.01.006
Lomes NR, De Carvalho Melhem MS, Szeszs MW et al (2016) Cryptococcosis in non-HIV/non-transplant patients: a Brazilian case series. Med Mycol 54:669–676. https://doi.org/10.1093/mmy/myw021
Maciel RA, Ferreira LS, Wirth F et al (2017) Corticosteroids for the management of severe intracranial hypertension in meningoencephalitis caused by Cryptococcus gattii: a case report and review. J Mycol Med 27:109–112. https://doi.org/10.1016/j.mycmed.2016.09.003
Silva LM, Ferreira WA, Filho RAAB et al (2020) New ST623 of Cryptococcus neoformans isolated from a patient with non-hodgkin’s lymphoma in the Brazilian Amazon. Ann Clin Microbiol Antimicrob 19:1–5. https://doi.org/10.1186/s12941-020-00361-3
Nascimento E, Bonifácio da Silva MEN, Martinez R, Von Zeska Kress MR (2014) Primary cutaneous cryptococcosis in an immunocompetent patient due to Cryptococcus Gattii molecular type VGI in Brazil: a case report and review of literature. Mycoses 57:442–447. https://doi.org/10.1111/myc.12176
de Carvalho Santana R, Schiave LA, dos Santos Quaglio AS et al (2017) Fluconazole non-susceptible Cryptococcus neoformans, Relapsing/Refractory cryptococcosis and long-term use of liposomal amphotericin B in an AIDS patient. Mycopathologia 182:855–861. https://doi.org/10.1007/s11046-017-0165-1
Souto ACP, Bonfietti LX, Ferreira-Paim K et al (2016) Population Genetic Analysis reveals a high genetic diversity in the Brazilian Cryptococcus gattii VGII Population and shifts the global origin from the Amazon Rainforest to the semi-arid Desert in the Northeast of Brazil. PLoS Negl Trop Dis 10:e0004885. https://doi.org/10.1371/journal.pntd.0004885
Vilas-Boas AM, Andrade-Silva LE, Ferreira-Paim K et al (2020) High genetic variability of clinical and environmental Cryptococcus gattii isolates from Brazil. Med Mycol 58:1126–1137. https://doi.org/10.1093/mmy/myaa019
Acknowledgements
The authors would like to acknowledge Tamires Y. M. dos Santos, Isabelle R. de O. Queiroz and Madson C. M. Cavalcante for previous sampling and phenotypical identification of the isolates. We thank the Hospital Escola Dr. Hélvio Auto personnel for collecting clinical samples. We also thank Marcia Lazera (INI-Fiocruz) for the kind donation of the standard molecular types of Cryptococcus spp.
Funding
This work was supported by Ministério da Saúde do Brasil; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado de Alagoas (FAPEAL) [grant number 60030000739/2013] and funding scholarship by Universidade Federal de Alagoas (UFAL).
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Douglas Lyra (Investigation; data curation; writing – original draft preparation; writing – review and editing), Denise Wanderlei (Supervision; conceptualization; funding acquisition; methodology; project administration; data curation; writing – review and editing) and Fernanda Maranhão (Supervision; conceptualization; funding acquisition; methodology; project administration; data curation; writing – review and editing).
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This study was approved by the Research Ethics Committee (number 19035713.8.0000.5013) in accordance with the resolution 466/2012 of the National Council of Health from Brazil. Informed consent was obtained from all individuals participants in this study.
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de Holanda Fonseca, D.L., Silva, D.M.W. & de Albuquerque Maranhão, F.C. Molecular characterization of clinical and environmental isolates from the Cryptococcus neoformans/C. Gattii species complexes of Maceió, Alagoas, Brazil. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01313-1
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DOI: https://doi.org/10.1007/s42770-024-01313-1