Email updates

Keep up to date with the latest news and content from JOMT and BioMed Central.

Open Access Research

Cryptococcus spp isolated from dust microhabitat in Brazilian libraries

Diniz P Leite, Janaina V R S Amadio, Evelin R Martins, Sara A A Simões, Ana Caroline A Yamamoto, Fábio A Leal-Santos, Doracilde T Takahara and Rosane C Hahn*

Author Affiliations

Medicine Faculty, Mycology laboratory, Federal University of Mato Grosso, Fernando Correa da Costa Avenue, 2367, Boa Esperança - Cuiabá/MT, Brazil

For all author emails, please log on.

Journal of Occupational Medicine and Toxicology 2012, 7:11  doi:10.1186/1745-6673-7-11


The electronic version of this article is the complete one and can be found online at: http://www.occup-med.com/content/7/1/11


Received:24 October 2011
Accepted:16 April 2012
Published:8 June 2012

© 2012 Leite et al.; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

The Cryptococcus spp is currently composed of encapsulated yeasts of cosmopolitan distribution, including the etiological agents of cryptococcosis. The fungus are found mainly in substrates of animal and plant origin. Human infection occurs through inhalation of spores present in the environment.

Methods

Eighty-four swab collections were performed on dust found on books in three libraries in the city of Cuiabá, state of Mato Grosso, Brazil. The material was seeded in Sabouraud agar and then observed for characteristics compatible with colonies with a creamy to mucous aspect; the material was then isolated in birdseed (Niger) agar and cultivated at a temperature of 37°C for 5 to 7 days. Identification of isolated colonies was performed by microscopic observation in fresh preparations dyed with India ink, additional tests performed on CGB (L-canavanine glycine bromothymol blue), urea broth, and carbohydrate assimilation tests (auxanogram).

Results

Of the 84 samples collected from book dust, 18 (21.4%) were positive for Cryptococcus spp totalizing 41 UFC’s. The most frequently isolated species was C. gattii 15 (36.6%); followed by C. terreus, 12 (29.3%); C. luteolus 4 (9.8%); C. neoformans, and C. uniguttulatus 3 (7.3%), and C. albidus and C. humiculus with 2 (4.6%) of the isolates.

Conclusion

The high biodiversity of the yeasts of the Cryptococcus genus, isolated from different environmental sources in urban areas of Brazil suggests the possibility of individuals whose immune systems have been compromised or even healthy individuals coming into sources of fungal propagules on a daily bases throughout their lives. This study demonstrates the acquisition possible of cryptococcosis infection from dust in libraries.

Keywords:
Cryptococcus spp; Dust; Libraries; Air; Habitat

Background

Since moving to Cryptococcus spp was first isolated, over 113 years ago, many studies have been conducted on the subject. However, many clinical-epidemiological and ecological aspects are still unknown, especially in Brazil. Regarding the epidemiology of the agent, there is a wide variety of species distributed in different countries and in different regions of the same country [1], and there are also many areas which are yet to be researched in regard to the interaction of the agent with its human host [2].

thumbnailFigure 1. Presence of Cryptococcus spp in 84 samples taken from the dust substrate of three libraries of Cuiabá, MT.

Yeasts of the Cryptococcus genus have a peculiar type of geographic distribution, considering their species. A high incidence of Cryptococcus neoformans is found in European countries and in North America; whereas Cryptococcus gattii is found predominantly in tropical and subtropical regions. This peculiar geographic distribution is a significant factor in the study of the natural habitat of Cryptococcus, as a possible source of contagion for susceptible individuals [3].

Five serotypes are currently recognized for this fungus (A, B, C, D, and AD). The distinction between different serotypes is based on the immunologic reaction to the antiserum produced against different polysaccharide compositions that constitute the yeast capsule. The AD serotype was classified as a diploid hybrid of A and D serotypes [1]. Recent DNA polymorphism studies using AFLP (amplified fragment length polymorphism). Demonstrated that the genetic differences between varieties were enough to classify them as two distinct species: Cryptococcus neoformans and Cryptococcus gattii [4-7].

The distribution of the yeasts of the genus Cryptococcus in nature is very large and is associated especially to decomposing vegetables, fruits, and bird droppings, particularly pigeon droppings [8]. The species C. neoformans is commonly isolated from bird excreta, urban pigeons (Columba livia) being considered the main source of this species [9,10]; C. gattii has been isolated mainly from samples of eucalyptus (Eucalyptus camaldulensis, E. tereticornis, and E. gomphocephala)[11-15] and other trees in Brazil [16-19].

In many situations, reports of cryptococcosis have been associated to pigeon droppings as the source of the infection. However, epidemiological analyses showed that patients who are in contact with pigeons are subjected to a high risk of infection [9,10]. The main problem is that C. neoformans remains viable for many years in dry pigeon droppings, which become a reservoir for infectious particles accumulated by alveolar deposition. These yeasts are currently present in urban areas and associated with urban birds and their habitats, which are adapted to buildings, such as pigeons, and birds that live in parks, commercial establishments, and homes, such as parakeets and canaries [20-22].

The Cryptococcus genus is composed of approximately 34 species of yeast which reproduce asexually by budding and can be identified by: starch hydrolysis, assimilation of inositol, production of urease, non fermentation of sugars, and sensitivity to cycloheximide [23,24].

Studies to identify, isolate, and monitor the incidence of specific fungus species in different habitats still need to be conducted, since the literature reports urban environmental sources and plant substrates as the main environments harboring Cryptococcus spp, emphasizing sources associated to the exposure to pigeons and tree hollows in urban centers. In the study of cryptococcosis and its etiologic agents it is important to be aware of and extensively monitor reservoirs and sources of infection [8]. Therefore, these parameters guide epidemiological data for the implementation of prevention programs and effective therapies [25]. This study represents the first Brazilian report on the association between this fungus and dust found in libraries.

Materials and methods

Eighty-four samples were collected inside three libraries (A, B, and C) and analyzed, in the city of Cuiabá, state of Mato Grosso, Brazil. The study was authorized by the people in charge of the libraries. The dust was collected with sterile swabs and placed in 20% sterile saline solution, and later transported to the mycology investigation laboratory of the Federal University of Mato Grosso for isolation and identification of the fungal microorganisms.

The colonies selected from the seeded plates (primary colonies) were re-isolated and diluted in 2.0 ml sterile water solution with chloramphenicol; they were later seeded on Sabouraud medium with chloramphenicol and incubated for 5 to 7 days at 37°C. After growth, the colonies were identified by morpho-physiological tests.

The macroscopic analysis of the colonies suggestive of Cryptococcus spp was conducted by observing the shiny, smooth aspect of the surface, with a creamy to mucous consistency, and a white to beige coloration. The micromorphology of the colonies was analyzed through microculture (Ridell technique). The isolates were submitted to a urease test and microscopic analysis with India ink to visualize the capsule [26].

The colonies were seeded in birdseed agar (Staib agar), which is recommended to verify phenoloxidase activity of the most studied pathogenic species nowadays, Cryptococcus neoformans and Cryptococcus gattii [9]. C. neoformans and C. gattii are the only yeasts of this kind capable of synthesizing melanin through the conversion of hydroxybenzoic substrates by phenoloxidase activity [27]. After passage through birdseed agar, the possible colonies which showed a coffee-brown coloration characteristic of C. neoformans and C. gattii were seeded in CGB medium (L-canavanine glycine bromothymol blue) for species identification [27].

For the biochemical tests, auxanogram technique was used, in which the assimilation of eleven carbon sources (dextrose, lactose, maltose, sucrose, inositol, galactose, cellobiose, dulcitol, melibiose, trehalose, and raffinose) and two nitrogen sources (peptone and potassium nitrate) [27] was used to differentiate, identify, and confirm at the species level.

Results and discussion

Brazilian scientific literature on cryptococcosis has had a significant contribution in directing and explaining facts related to the agent of this disease. The habitat of yeasts of the genus Cryptococcus, especially C. neoformans, are found in the environment, principally in soil made up of decomposing plant material and bird and bat droppings found in both urban and rural areas in Brazil [1,9,10,20,22,28]. However, other studies have shed more light on the ecology of the cryptococcosis agent in Brazil, demonstrating that the yeast is associated not only with pigeons or Eucalyptus spp trees, but also with other tree species, as reported by Lazéra et al. [16-19] (and fellow authors), Fortes et al. [29] and Baltazar and Ribeiro [30].

In this study, the identification of seven different species of Cryptococcus yeasts, isolated from the dust found on books, indicates that dust is a possible biotope for isolating this type of microorganism (Figure 1). Forty-one colonies were isolated distributed through all three libraries and in two of the libraries, the presence of encapsulated yeast was detected in these environments. Cryptococcus gattii was the species most frequently identified, totaling 15 (36.6%) isolates; followed by C. terreus with 12 (29.3%) isolates and C. luteolus with 4 (9.8%) isolates. The other species detected were C. neoformans and C. uniguttulatus represented by 3 (7.3%) isolates each, and by C. albidus and C. humiculus with 2 (4.6%) isolates each, which presented the smallest percentiles (Table 1).

Table 1. Presence ofCryptococcusspp in 84 samples taken from the dust substrate of three libraries of Cuiabá, MT

Table 1. Frequency of colonies of isolates of yeasts species of the genus Cryptococcus from dust collected in three libraries in Cuiabá, MT, Brazil.

In Brazil, this encapsulated yeast has been isolated in several geographical regions: Bahia [20,31]; São Paulo [32,33]; Mato Grosso do Sul [9]; Goiás [34]; Rio de Janeiro [10,16,22] and Rio Grande do Sul [35-37]. In Mato Grosso, the first description of these microorganisms in HIV-positive patients was reported by Favalessa et al. [38]. The authors detected 37 C. neoformans and C. gattii isolates in distinct clinical materials from seropositive and seronegative patients.

The percentage (21.4%) of positive samples in this study (Chart 1) conducted in the city of Cuiabá is noteworthy compared with studies by other authors conducted in other Brazilian cities, when these involved bird droppings as substrates in the research. Soares et al. [39], in a study conducted in the city of Santos, obtained a frequency of 13.9% for pigeon excreta samples positive for C. neoformans. In the city of Goiânia, Kobayashi et al. [34] verified a frequency of 23.2%; while researching in church towers in Rio de Janeiro, Baroni et al. [10] observed that 37.8% of the samples collected showed the presence of encapsulated yeast and in Rio Grande do Sul, Abegg et al. [36] isolated C. neoformans var. grubii in 87% of Psittacidae excreta samples. The percentage presented in this study, conducted in what is considered a closed environment, is in agreement with the data presented in the study by Kobayashi et al. [34], who demonstrated that the presence of the fungus in environmental samples is more representative when such samples are protected from the weather. In Brazil, no reports concerning the ecology of this species were identified exclusively in the presence of library dust. Isolates from 41 colonies of seven species of Cryptococcus spp. identified in the microhabitat of dust shows the importance of knowledge regarding the saprobiotic sources that host the Cryptococcus spp yeasts responsible for important and fatal cases of cryptococcal meningitis in immunosuppressed and immunocompetent individuals [40-42].

In addition to public places, enclosed environments may contain a high density of C. neoformans, as shown in the study conducted by Criseo et al. [43], who reported 26.6% in bird excreta in pet stores and homes. Swinne et al. [44] isolated C. neoformans in domestic dust in Bujumbura (South Africa) in samples collected from homes of patients with cryptococcosis associated with AIDS, making a significant correlation between the existence of pigeons close to the home environment and the probability of contamination of these homes. In a study conducted in different regions of Bangkok, Soogarum et al. [45] demonstrated the presence of C. neoformans in 14 samples of pigeon droppings. Hanasha et al. [46] analyzed 509 samples of columbiform droppings collected from several Jordanian cities and reported 336 samples positive for Cryptococcus spp. However, these studies did not classify these yeasts at the species level. In addition, Passoni et al. [22] isolated basidiomycetous from captive bird droppings, compared with dust from the inside of the home and the) peridomicile. Of the 79 samples of bird droppings collected by these researchers, 12.7% were positive. The authors concluded that the frequency of positive isolates in homes that maintained captive birds was the main factor responsible for the contamination in these homes. In this study, the percentage of isolates of Cryptococcus spp in 84 samples collected with swabs resulted in 18 (21.4%) positive samples (Chart 1).

The environmental source of C. gattii is associated with decomposing eucalyptus material, as well as other plant materials in the process of decomposition. Nowadays, this species is being identified on different trees and in different geographical regions of Brazil, and has already been isolated on native and introduced plant specimens, such as false sicklepod (Senna multijuga), stinking toe (Cassia grandis), Chinese banyan (Ficus microcarpa), Cabori (Miroxilum peruiferum), Sibipiruna (Caesalpinia peltophoroides), and Oiti (Moquilea tomentosa), revealing other natural habitats for this species [16,17,19,28,30,47,48]. While researching trees in the Brazilian Amazon, Fortes et al. [29] reinforced evidence that C. gattii is not associated with one species of tree in particular, but rather to a specific habitat niche formed by the natural decomposition of wood. Recent research has proved this hypothesis, as shown by Randhawa et al. [49], who demonstrated the prevalence of C. gattii (24%) and C. neoformans (26%) in the soil around the base of certain host trees, indicating that the soil is another important ecological niche for these two species of Cryptococcus. More recently, Girish et al. [50] confirmed this hypothesis by isolating C. neoformans from environmental samples on 40 selected trees, taking into consideration decomposing wood and bits of bark of live trees in the Guindy National Park in Chennai, in the southern region of India, with the very first isolation of C. gatti on a species of jambul (Syzygium cumini).

Studies performed in several countries, including samples from plant specimens, have revealed the presence and abundance of C. gattii in a variety of native species in Australia [1,13], Mexico [51], Egypt [52], Portugal [15], Argentina [53], Colombia [54,55], India [49,50,56] and Canada [57-59].

Last year, while investigating plant species on a Caribbean island in Puerto Rico, Loperena-Alvares et al. [60] detected the presence of C. gatti in lesions on succulent plants of the Cactaceae family (Cephalocereus royenii), a type of cactus that is extremely common in the region. More recently, in Colombia, Firacative et al. [61] processed 3,634 samples from trees surrounding the residences of patients afflicted by cryptococcosis caused by C. gatti, isolating a sample of C. gatti serotype B, two samples of C. gatti serotype C and three samples of C. neoformans var. grubii serotype A.

Given these facts, the results obtained in this study suggest that the locations researched may be surrounded by abundant varied tree vegetation (Mangifera indicaCocothrimax spissaCassia fistulaCaesalpinia peltophoroidesEucalyptus camaldulensis), including species of Eucalyptus spp, in which the main spore is represented by basidiospores present in the flowers of this genus of trees that functions as “host tree” for the fungus through a biotrophic association; thus greatly facilitating the dispersion of these spores into the environments analyzed. This fact can be observed in the work of Mahmoud et al. [52] in Egypt, which revealed the presence of C. gatti in samples of flowers of Eucalyptus camaldulensis, and in the study performed by Velagapudi et al. [42], which used acquisition by inhalation as the environmental criteria.

The basidiomycete yeast C. neoformans is well adapted to bird droppings, particularly that of pigeons. The increasing population of birds is becoming an environmental and public health issue in Brazil and the rest of the world. This columbiform species has a habit of living in groups, building its nests high up on buildings, towers, attics and windowsills, among other locations, while it feeds on grains and remnants of food and garbage in public locations [62]. In this study, a large concentration of pigeons (Columba livia domestica) was observed in the urban environments near the locations studied and these birds have access to attics and windowsills that are not sealed. Observation verified that the bird droppings remained on roofs and air-conditioning vents, facilitating the dispersal of dry particles containing fungal spores inside the facilities. In a recent study conducted by Takahara et al. [63], which analyzed samples of pigeon droppings in the city of Cuiabá, state of Mato Grosso, Brazil, collected from several domestic, commercial, and public environments, the presence of strains of C. neoformans was demonstrated in bird droppings.

The meteorological factors of each region, such as temperature, humidity and light exposure, influence and can contribute to obtaining different results [40,64,65]. Granados and Castañeda [65] have demonstrated the prevalence of Cryptococcus species, suggesting that meteorological conditions influenced the presence of this yeast and that C. neoformans is more frequently isolated during wetter seasons on dry droppings. The microclimatic conditions in the city of Cuiabá, Brazil, with an average temperature between 34 and 35°C, a dry winter, and a rainy summer, can favor the development and dispersion of fungi in the environment. The microclimates, (temperature and humidity) identified in these environments are considered to be factors for the presence of these microorganisms in the locations studied. In addition to the relation of these ligninolytic basidiomycetes decomposers of cellulose and other plant materials, the greater frequency of C. gattii (15; 36.6%) in relation to C. neoformans (3; 7.3%) may be directly influenced by temperature, since according to Ishaq et al. [66], C. neoformans does not grow in temperatures above 40°C and is sensitive to direct sunlight. However, in a study performed by Kobayashi et al. [34], the authors affirmed that humidity is another factor that also seems to influence the viability of C. neoformans during collection and possibly on the swab samples, that tends to affect bacterial decomposition, thus altering the pH and probably inhibits the proliferation of the yeast.

Cryptococcosis is generally related to infection by C. neformans and C. gattii and is rarely caused by other species, including C. albidusC. laurentiiC. curvatus and C. uniguttulatus[23]. According to Khawcharoenporn et al. [67], the other species of the genus Cryptococcus are generally considered to be saprophytes. However, in the last few decades, reports have appeared in the literature regarding infections caused by other species, with C. albidus and C. laurentii being responsible for 80% of the cases of cryptococcosis caused by organisms other than C. neoformans and C. gattii. With the increase in the number of patients presenting compromised immune systems and the ample use of immunosuppressant agents, the incidence of fungal infections has increased worldwide, including those caused by emerging Cryptococcus species such as C. albidus and C. laurentii [68]. In this study, the isolation of 15 (36.6%) C. gattii samples; 3 (7.3%) C. neoformans samples, and 2 (4.9%) C. albidus samples (Table 1) demonstrated that the presence of species considered to be potentially pathogenic, as well as emerging species, may reflect the possibility of such species, which are present in a wide variety of substrates, constituting infectious agents for cryptococcosis.

The results obtained in this study indicate evidence of the diversity of the environmental origin of Cryptococcus spp and highlights the substrates favorable to their respective development in the environment. The microbiota analysis of dust from locations where human presence is constant is necessary to implement health surveillance programs to protect the health of workers, as well as preventing possible sources of acquisition of infectious disease-causing organisms, including cryptococcosis.

Abbreviations

KOH, Potassium hydroxide; AFLP, (Amplified fragment length polymorphism); CGB, Medium (L-canavanine glycine bromothymol blue).

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

All authors collected the biological material. DPLJ designed the study, performed and was involved in drafting the manuscript. All authors were involved performed in examination of biological materials, in data analysis and drafting of the papers. RCH participated in revising the manuscript and was the researcher in chief. All authors have read and approved the final manuscript.

References

  1. Nishikawa MM, Lazera MS, Barbosa GG, Trilles L, Balassiano BR, Macedo RCL, Bezerra CCF, Pérez MA, Cardarelli P, Wanke B: Serotyping of 467 Cryptococcus neoformans isolated from clinical and environmental sources in Brazil: analysis of host and regional patterns.

    J Clin Microbiol 2003, 41(1):72-7. OpenURL

  2. Pappalardo MCSM, Melhem MSC: Cryptococcosis: a review of the brazilian experience for the disease.

    Rev Inst Med Trop S Paulo 2003, 45(6):299-305. PubMed Abstract | Publisher Full Text OpenURL

  3. Colom-Valiente MF, Alberdi M, Meseguer I, Torres-Rodriguez JM: Aislamiento de Cryptococcus neoformans em muestras de médio ambiente de Alicante.

    Rev Iberoam Micol 1997, 14:63-64. PubMed Abstract | Publisher Full Text OpenURL

  4. Boekhout T, Theelen B, Diaz M, Fell JW, Hop WC, Abeln EC, Dromer F, Meyer W: Hybrids genotypes in the pathogenic yeast Cryptococcus neoformans.

    Microbiol 2001, 147(4):891-907. OpenURL

  5. Kwon-Chung KJ, Boekhout T, Fell JW, Diaz M: Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. bacillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae).

    Taxon 2002, 51:804-806. Publisher Full Text OpenURL

  6. Gams W: Report of the Committee for fungi: 12.

    Taxon 2005, 54:520-522. Publisher Full Text OpenURL

  7. Kwon-Chung KJ, Varma A: Do major species concepts support one, two or more species within Cryptococcus neoformans?

    FEMS Yeast Res 2006, 6:574-87. PubMed Abstract | Publisher Full Text OpenURL

  8. Nigro NTMRC, Pereira AD, Huggins DW, Lacaz CS: Isolamento de Cryptococcus neoformans de fezes de pombos, do solo e ninhos de pombos.

    Rev Bras Med 1987, 44:6-9. OpenURL

  9. Filiú WFOF, Wanke B, Agüena SM, Vilela VO, Macedo RCL, Lazera MS: Cativeiro de aves como fonte de Crytopcoccus neoformans na cidade de Campo Grande Mato grosso do Sul.

    Brasil Rev Soc Bras Med Trop 2002, 35(6):591-594. Publisher Full Text OpenURL

  10. Baroni FA, Paula CR, SILVA EG, SILVA FC, Rivera ING, Oliveira MTB, Gambale W: Cryptococcus neoformans strains isolated from church towers in Rio de Janeiro city, RJ, Brazil.

    Rev Inst Med Trop S Paulo 2006, 48(2):71-75. PubMed Abstract | Publisher Full Text OpenURL

  11. Ellis DH: Cryptococcus neoformans var. gattii in Australia.

    J Clin Microbiol 1987, 25:430-431. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  12. Pfeiffer TJ, Ellis DH: Environmental isolation of C. neoformans var. gattii, from E. territicornis.

    J Med Vet Mycol 1992, 30:407-408. PubMed Abstract | Publisher Full Text OpenURL

  13. Ellis DH, Pfeiffer TJ: Natural habitat of Cryptococcus neoformans var. gattii.

    J Clin Microbiol 1990, 28(7):1642-44. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  14. Sorrel TC, Ellis D: Ecology of Cryptococcus neoformans.

    Rev Ibveroam Micol 1997, 14:42-43. OpenURL

  15. Bernardo FM, Martin HM, Martin ML: Urban Sources of Cryptococcus spp - Lisbon (Portugal).

    RPCV 2001, 96(539):157-160. OpenURL

  16. Lazera MS, Wanke B, Nishikawa MM: Isolation of both varieties of Cryptococcus neoformans from saprophytic sources in the city of Rio de Janeiro.

    Brazil J Med Vet Mycol 1993, 31:449-454. Publisher Full Text OpenURL

  17. Lazera MS, Pires FDA, Camillo-Coura L, Nishikawa MM, Bezerra CCF, Trilles L, Wanke B: Natural habitat of Cryptococcus neoformans var. gattii in decaying wood forming hollows in living trees.

    J Med Vet Mycol 1996, 34:127-131. PubMed Abstract | Publisher Full Text OpenURL

  18. Lazera MS, Cavalcanti MAS, Thilles L, Nishikawa MM, Wanke B: Cryptococcus neoformans var. gattii: evidence for a natural habitat related to decaying wood in pottery three hollow.

    Med Mycol 1998, 36:119-122. PubMed Abstract OpenURL

  19. Lazera MS, Salmito CMA, Londero AT, Trilles L, Nishikawa MM, Wanke B: Possible primary ecological niche of Cryptococcus neoformans.

    Med Mycol 2000, 38:379-383. PubMed Abstract OpenURL

  20. Silva ME, Paula LA: Isolamento de Cryptococcus neoformans de excrementos e ninhos de pombos (Columba livia) em Salvador, Bahia (Brasil).

    Rev Inst Med Trop S Paulo 1963, 5:9-11. PubMed Abstract OpenURL

  21. Hubalek Z: Distribution of Cryptococcus neoformans in pigeon habitat.

    Folia Parasit 1975, 22:73-179. OpenURL

  22. Passoni LFC, Wanke B, Nishikawa MM, Lazéra MS: Cryptococcus neoformans isolated from human dwellings in Rio de Janeiro, Brazil: an analysis of the domestic environment of AIDS patients with and without cryptococcosis.

    Medical Mycology 1998, 36:305-11. PubMed Abstract OpenURL

  23. Mitchell TG, Perfect JR: Cryptococcosis in the era of AIDS – 100 years after the discovery of Cryptococcus neoformans.

    Clin Microbiol Reviews 1995, 8(4):515-48. OpenURL

  24. Ikeda R, Sugita T, Juacobson ES, Shinoda T: Laccase and Melanization in Clinically Important Cryptococcus species other than Cryptococcus neoformans.

    J Clin Microbiol 2002, 40(4):1214-8. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  25. Horta JA, Staats CC, Casali AK, Ribeiro AM, Schrank IS, Schrank A, Vainstein MH: Epidemiological aspects of clinical and environmental Cryptococcus neoformans isolates in the Brazilian state Rio Grande do Sul.

    Medical Mycology 2002, 40(6):565-71. PubMed Abstract OpenURL

  26. Lacaz CS, Porto E, Martins JEC, Heins-Vaccari EM, Melo NT: Tratado de Micologia Médica. 9th edition. Sarvier, São Paulo; 2002. OpenURL

  27. Kwon-Chung KJ, Bennett JE: Medical Mycology. Lea e Fibiger, Philadelphia; 1992:866 p. OpenURL

  28. Montenegro H, Paula CR: Environmental isolation of Cryptococcus neoformans var. gattii and Cryptococcus neoformans var. neoformans in the city of São Paulo, Brazil.

    Med Mycol 2000, 38:385-390. PubMed Abstract OpenURL

  29. Fortes ST, Lazéra MS, Nishikawa MM, Macedo RC, Wanke B: First isolation of Cryptococcus neoformans var. gattii from a native jungle trees in the Brazilian Amazon rainforest.

    Mycoses 2001, 44:127-40. OpenURL

  30. Baltazar LM, Ribeiro MA: Primeiro isolamento ambiental de Cryptococcus gattii no estado do espírito santo.

    Rev Soc Bras Med Trop 2008, 41(5):449-53. PubMed Abstract | Publisher Full Text OpenURL

  31. Santana LS, Costa MSF, Queiroz LA: Ocorrência de Cryptococcus neoformans (Sanfelice) Vuillemin (1901) em excretas de pombos no perímetro urbano de Salvador, Bahia, Brasil.

    Sitientibus Série Ciências Biológicas 2007, 7(2):170-175. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  32. Silva JO, Capuano DM: Ocorrência de Cryptococcus spp e de parasitas de interesse em saúde pública, nos excretas de pombos na cidade de Ribeirão Preto, São Paulo, Brasil.

    Rev Inst Adolfo Lutz 2008, 67(2):137-141. OpenURL

  33. Rezende C, Munhóz CJM, Almeida GG: Investigação Ambiental de Cryptococcus neoformans na Cidade de Votuporanga. Newslab, São Paulo; 2008:87. PubMed Abstract OpenURL

  34. Kobayashi CCBA, Souza LKH, Fernandes OFL, Brito SCA, Silva AC, Sousa ED, Silva MRR: Characterization of Cryptococcus neoformans isolated from urban environmental sources in Goiania, Goias State, Brazil.

    Rev Ins Med Trop S Paulo 2005, 47(4):203-207. OpenURL

  35. Reolon A, Rodrigues LR, Mezzari A: Prevalência de Cryptococcus neoformans nos pombos urbanos da cidade de Porto Alegre, Rio Grande do Sul.

    J Bras Patol Med Lab 2004, 40(5):293-8. Publisher Full Text OpenURL

  36. Abegg MA, Cella FC, Faganello J, Valent P, Schrank A, Vainstein MH: Cryptococcus neoformans and Cryptococcus gattii isolated from the excreta of Psittaciformes in a Southern Brazilian Zoological Garden.

    Mycopathologia 2006, 161(2):83-91. PubMed Abstract | Publisher Full Text OpenURL

  37. Faria RO, Nascente PS, Meinerz ARM, Cleff MB, Antunes TA, Silveira TA, Silveira ES, Nobre MO, Meireles MCA, Mello JRB: Ocorrência de Cryptococcus neoformans em excretas de pombos na cidade de Pelotas, Estado do Rio Grande do Sul.

    Rev Soc Bras Med Trop 2010, 43(2):198-200. PubMed Abstract | Publisher Full Text OpenURL

  38. Favalessa OC, Ribeiro LC, Tadano T, Fontes CJF, Dias FB, Coelho BPA, Hahn RC: Primeira descrição da caracterização fenotípica e susceptibilidade in vitro a drogas de leveduras do gênero Cryptococcus spp isoladas de pacientes HIV positivos e negativos, Estado de Mato Grosso.

    Rev Soc Bras Med Trop 2009, 42(6):661-665. PubMed Abstract | Publisher Full Text OpenURL

  39. Soares MCB, Paula CR, Dias ALT, Caseiro MM, Costa SOP: Environmental strains of Cryptococcus neoformans var. grubii in the city of Santos, SP, Brazil.

    Rev Inst Med Trop Sao Paulo 2005, 47:31-36. PubMed Abstract | Publisher Full Text OpenURL

  40. Quintero E, Castañeda E, Ruiz A: Environmental distribution of Cryptococcus neoformans in the department of Cundinamarca-Colombia.

    Rev Iberoam Micol 2005, 22(2):93-8. PubMed Abstract | Publisher Full Text OpenURL

  41. Pukkila-Worley R, Mylonakis E: Epidemiology and management of cryptococcal meningitis: developments and challenges.

    Expert Opin Pharmacother 2008, 9(4):551-60. PubMed Abstract | Publisher Full Text OpenURL

  42. Velagapudi R, Hsueh YP, Geunes-Boyer S, Wright JR, Heitman J: Spores as infectious propagules of Cryptococcus neoformans.

    Infect Immun 2009, 77(10):4345-55. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  43. Criseo G, Bolignano MS, De Leo F, Staib F: Evidence of canary droppings as an important reservoir of Cryptococcus neoformans.

    Zentralblatt fuer Bakteriologia 1995, 282(3):244-54. OpenURL

  44. Swinne D, Deppner M, Maniratunga S, Laroche R, Floch JJ, Kadense P: AIDS – Associated Cryptococcosis in Bujunbura, Burundi and Epidemiological Study.

    J Med Vet Mycol 1991, 29:25-30. PubMed Abstract | Publisher Full Text OpenURL

  45. Soogarun S, Wiwanitki V, Palasuwan A, Pradniwat P, Suwansaksri J, Lertlum T, Maungkote T: Detection of Cryptococcus neoformans in bird excreta.

    Southeast Asian J Trop Med Public Health 2006, 37(4):768-70. PubMed Abstract OpenURL

  46. Hamascha AM, Vildiran ST, Gonlum A, Saracli MA, Doganci L: Cryptococcus neoformans varieties from material under the canopies of eucalyptus trees and pigeon dropping samples from four major cities in Jordan.

    Mycopathologia 2002, 158(2):195-9. OpenURL

  47. Restrepo A, Baumgardner DJ, Bagagli E, Cooper CRJr, Mcginnis MR, Lázera MS, Barbosa FH, Bosco FH, Bosco SM, Camargo ZP, Coelho KI, Fortes ST, Franco M, Montenegro MR, Sano A, Wanke B: Clues to the presence of pathogenic fungi in certain environments.

    Med Mycol 200, 38(suppl I):67-77. OpenURL

  48. Reimão JQ, Drummond ED, Terceti MS, Lyon JP, Franco MC, Siqueira AM: Isolation of Cryptococcus neoformans from hollows of living trees in the city of Alfenas, MG, Brasil.

    Mycosis 2007, 50:261-264. Publisher Full Text OpenURL

  49. Randhawa HS, Kowshik T, Chowdhary A, Preeti Sinha K, Kahan ZU, Sun S, Xu J: The expanding host tree species spectrum of Cryptococcus gatti and Cryptococcus neoformans and their isolation from surrounding soil in India.

    Med Mycol 2008, 46:823-33. PubMed Abstract | Publisher Full Text OpenURL

  50. Girish CP, Prabu D, Mitani H, Mikami Y, Menon T: Environmental isolation of Cryptococcus neoformans and Cryptococcus gattii from living trees in Guindy National Park, Chennai, South India.

    Mycoses 2010, 53:262-4. PubMed Abstract | Publisher Full Text OpenURL

  51. Licea BA, Garza DG, Zúñiga MT: Aislamento de Cryptococcus neoformans var. gattii de Eucalyptus tereticornis.

    Rev Iberoam Micol 1996, 13:27-28. OpenURL

  52. Mahmoud YAG: First environmental isolation of Cryptococcus neoformans var. neoformans and var. gattii from the Gharbia Governorate, Egypt.

    Mycopathologia 1999, 148(2):83-86. PubMed Abstract | Publisher Full Text OpenURL

  53. Davel G, Abrant R, Brudny M, Córdoba S, Rodero L, Canteros CE, Perrotta D: Primer aislamiento ambiental de Cryptococcus neoformans var. gattii em Argentina.

    Rev. Arg. Microbiol 2003, 35:110-12. OpenURL

  54. Callejas A, Ordoñez N, Rodrigues MC, Castañeda E: First isolation of Cryptococcus neoformans var. gattii serotype C from the environment in Colombia.

    Med Mycol 1998, 36:341-344. PubMed Abstract OpenURL

  55. Escandón P, Sáchez A, Martínes M, Meyer W, Castañeda E: Molecular epidemiology of clinical and environmental isolates of the Cryptococcus neoformans species complex reveals a high genetic diversity and the presence of the molecular type VGII mating type a in Colombia.

    Fed. Europ. Microbiol. Societies Yeast Res 2006, 6:625-35. OpenURL

  56. Randhawa HS, Kowshik T, Preeti Sinha K, Chowdhary A, Khan ZU, Yan Z, Xu J, Kumar A: Distribution of Cryptococcus gattii and Cryptococcus neoformans in decayed trunk wood of Syzygium cumini trees in north-western India.

    Med Mycology 2006, 44:623-30. Publisher Full Text OpenURL

  57. Kidd SE, Hagen F, Tsharke RL, Hyunh M, Bartlett KH, Fyfe M, Macdougall L, Boekhout T, Kwon-Chung KJ, Meyer W, Rita R: A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada).

    Proc Natl Acad Sci USA 2004, 101(49):17258-63. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  58. Kidd SE, Chow Y, Mak S, Back PJ, Chen H, Hingston OA, Kronstad JW, Bartlett KH: Characterization of environmental sources of the human and animal pathogen Cryptococcus gatti in British Columbia, Canada, and the Pacific Northwest of the United States.

    Appl Environm Microbiol 2007, 73:1433-43. Publisher Full Text OpenURL

  59. Springer DJ, Chaturvedi V: Projecting global occurrence of Cryptococcus gattii.

    Emerg Infect Dis 2010, 16:14-20. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  60. Loperena-Alvarez Y, Ren P, Li X, Bopp DJ, Ruiz A, Chaturvedi V, Rios-Velasques C: Genotypic characterization of environmental isolates of Cryptococcus gattii from Puerto Rico.

    Mycopathologia 2010, 170(4):279-85. PubMed Abstract | Publisher Full Text OpenURL

  61. Firacative C, Torre GR, Rodrigues MC, Escandón P: First environmental isolation of Cryptococcus gattii serotype B, from Cúcuta, Colombia.

    Biomedica 2011, 31:118-23. PubMed Abstract | Publisher Full Text OpenURL

  62. Rosario I, Acosta B, Colom F: La paloma y otras aves como reservorio de Cryptococcus spp.

    Rev Iberoam Micol 2008, 25:13-18. Publisher Full Text OpenURL

  63. Takahara DT: Isolamento e identificação de Cryptococcus neoformans a partir de excretas de pombos provenientes de locais públicos e residênciais de Cuiabá e Várzea Grande – MT. 122 pth edition. (MSc. Dissertation. Faculdade de Ciências Médicas – Universidade Federal de Mato Grosso, Cuiabá/MT; 2011. OpenURL

  64. Granados DP, Castañeda E: Isolation and characterization of Cryptococcus neoformans varieties recovered from natural sources in Bogota, Colombia and study of ecological conditions in the area.

    Microb Ecol 2005, 49:282-90. PubMed Abstract | Publisher Full Text OpenURL

  65. Granados DP, Castañeda E: Influence of climatic conditions on the isolation of members of the Cryptococcus neoformans species complex from tress in Colombia from 1992–2004.

    FEMS Yeast Res 2006, 6(4):636-44. PubMed Abstract | Publisher Full Text OpenURL

  66. Ishaq CM, Bulmer GS, Felton EG: An evaluation of various environmental factors affecting the propagation of Cryptococcus neoformans.

    Mycopathology 1968, 35:81-90. OpenURL

  67. Khawcharoenporn T, Apisarnthanarak A, Muny LM: Non-neoformans cryptococcal infectious: a systematic review.

    Infection 2007, 35:51-7. PubMed Abstract | Publisher Full Text OpenURL

  68. Pedroso RS, Penatti MPA, Maffei CML, Candido RC: Infecções causadas por Cryptococcus albidus e C. laurentii: Implicações Clínicas e Identificação Laboratorial.

    Newslab 2010, 102:96-104. OpenURL