Trichosporon spp.: an emerging fungal pathogen

array:18 ["pii" => "X1665579614283703" "issn" => "16655796" "estado" => "S300" "fechaPublicacion" => "2014-01-01" "documento" => "article" "licencia" => "http://www.elsevier.com/open-access/userlicense/1.0/" "subdocumento" => "fla" "cita" => "Medicina Universitaria. 2014;16:37-43" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 4755 "formatos" => array:3 [ "EPUB" => 46 "HTML" => 4021 "PDF" => 688 ] ] "itemAnterior" => array:15 [ "pii" => "X1665579614283699" "issn" => "16655796" "estado" => "S300" "fechaPublicacion" => "2014-01-01" "documento" => "article" "licencia" => "http://www.elsevier.com/open-access/userlicense/1.0/" "subdocumento" => "fla" "cita" => "Medicina Universitaria. 2014;16:28-36" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 2423 "formatos" => array:3 [ "EPUB" => 45 "HTML" => 1789 "PDF" => 589 ] ] "en" => array:11 [ "idiomaDefecto" => true "titulo" => "Mild cognitive impairment" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "28" "paginaFinal" => "36" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig1" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "304v16n62-90328369fig1.jpg" "Alto" => 1362 "Ancho" => 1712 "Tamanyo" => 185466 ] ] "descripcion" => array:1 [ "en" => "Histopathologic changes in the brain and its clinical correlation." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "J. Isordia-Martínez, F. Gongora-Rivera, H. Leal-Bailey, X. Ortiz-Jiménez" "autores" => array:4 [ 0 => array:2 [ "Iniciales" => "J." "apellidos" => "Isordia-Martínez" ] 1 => array:2 [ "Iniciales" => "F." "apellidos" => "Gongora-Rivera" ] 2 => array:2 [ "Iniciales" => "H." "apellidos" => "Leal-Bailey" ] 3 => array:2 [ "Iniciales" => "X." "apellidos" => "Ortiz-Jiménez" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/X1665579614283699?idApp=UINPBA00004N" "url" => "/16655796/0000001600000062/v0_201607061506/X1665579614283699/v0_201607061508/en/main.assets" ] "en" => array:13 [ "idiomaDefecto" => true "titulo" => "Trichosporon spp.: an emerging fungal pathogen" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "37" "paginaFinal" => "43" ] ] "autores" => array:1 [ 0 => array:3 [ "autoresLista" => "A. M. Montoya, G. M. González" "autores" => array:2 [ 0 => array:3 [ "Iniciales" => "A. M." "apellidos" => "Montoya" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "affa" ] ] ] 1 => array:3 [ "Iniciales" => "G. M." "apellidos" => "González" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "affa" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:3 [ "entidad" => "Department of Microbiology, Faculty of Medicine, Universidad Autónoma de Nuevo León, Monterrey, N. L., Mexico " "etiqueta" => "a" "identificador" => "affa" ] ] ] ] "textoCompleto" => "Introduction Trichosporon spp. was first described by Beigel in 1865 as the agent responsible for a benign hair infection called white piedra (meaning "stone" in Spanish). Beigel classified the microorganism as algae and placed it in the genus Pleurococcus. It wasn't until 1890 when Behrend identified the microorganism causing white piedra as a fungus which he called Trichosporon ovoides.1 Although generally associated with this superficial infection, Trichosporon spp. has gained importance as one of the most opportunistic systemic infections since the first case of invasive trichosporonosis involving the brain, reported in 1970.2Trichosporon spp. Trichosporon spp. belongs to the phylum Basidiomycota. It is a yeast-like fungus macroscopically characterized by forming radially symmetrical colonies; these colonies may be white or yellowish, with a smooth texture, creamy, cerebriform, powdery or moist. Microscopically, Trichosporon spp. forms hyaline septate hyphae, with abundant arthroconidia and blastoconidia, and in some cases presents appressoria. Regarding physiological tests, they assimilate several carbohydrates and other carbon sources, yet they do not possess fermentation capabilities. A major characteristic of the Trichosporon spp. genus is their ability to hydrolize urea.1,3-5 In 1902 Vuillemin grouped the species described for this genus under the Trichosporon beigelii denomination, a practice that remained until the late 90's.5,6 Nevertheless, posterior classifications at morphological, biochemical, and molecular levels provided evidence of the existence of more than one species in the genus. Approximately 50 species of the genus Trichosporon have been characterized, 16 of which are associated with diseases in humans. Guého et al. (1994) typified species that had displayed a major adaptation to the human body: T. asahii, T. asteroides, T. cutaneum, T. inkin, T. mucoides and T. ovoides. These 6 species, reclassified from the Trichosporon beigelii taxon, remain the most relevant clinical species to date.7Virulence factors There is little information regarding virulence factors produced by this microorganism. Hemolysins, proteases, and lipases allow protein degradation and destabilization of the membranes of the host cell, increasing fungus pathogenicity. Dað and Cerikçioðlu analyzed the production of proteases, phospholipases, and esterases of 48 T. asahii clinical isolates, and did not detect protease nor phospholipase activity in any of the isolates analyzed; however, all the evaluated strains displayed esterase activity.8 Similarly, Sun et al. evaluated protease, phospholipase, and hemolysine production in 23 T. asahii clinical isolates, and observed no protease nor phospholipase activity, yet 100% of isolates showed hemolysin activity. This activity, however, varied for the different T. asahii genotypes identified.9 It is important to underline that there are no reports about the production of lytic enzymes for Trichosporon non-asahii species. Phenotypic switching is a fast and reversible change of colonial morphology and/or microscopic features. These changes may occur as a response to different environmental stimuli such as oxidative stress or lack of nutrients, or intrinsic factors such as a mutation in the deoxyribonucleic acid (DNA) repair systems.10 When phenotypic switching occur in vivo, they involve modifications in the expression of virulence factors, or alterations in the microorganism-host cell interactions, thus provoking an increment in the pathogenicity and evasion of the immune response, as observed in Candida albicans and Cryptococcus neoformans.11-13 Lee et al., reported phenotypic switching in vitro for the first time for T. beigelii. The isolated microorganism, recovered from a patient with a systemic infection, was capable of producing two different morphologies when cultivated at 30°C. Such morphotypes were accompanied by their respective structural microscopic changes. Thus, a rough, cerebriform, moist colony with irregular edges was accompanied microscopically by hyphae while a second powder morphotype, with a more regular topography and borders, showed microscopically a greater proportion of arthroconidia or blastoconidia.4 The phenotypic switching was also reported in vivo by Karashima et al., who performed experiments involving repetitive inoculation of T. asahii in mice. They observed macro- and microscopic morphological differences when comparing the fungi before being inoculated and the same fungi recovered after 3 repetitive passages in 8-week-old ICR mice. Similar to the results obtained by Lee et al., Karashima observed that the rugged colony was accompanied microscopically by a greater proportion of hyphae, while a powdery colony was accompanied by a greater amount of conidia.14 In the same paper, Karashima et al. reported the production of a cell wall component similar to the glucuronoxylomannan (GXM) of C. neoformans. They observed that a larger amount of GXM was present in the recovered microorganism after repeated inoculations in mice. GXM has been proposed to offer C. neoformans protection against phagocytosis by neutrophils and monocytes.14 Another factor providing protection to the fungus is the formation of biofilms. Some microorganisms have the ability to produce an extracellular matrix, formed by polysaccharides, proteins, and DNA, which allow conglomeration of cells and their adherence to both organic and inorganic surfaces.15 Due to the association of invasive infections to the use of catheters and similar devices, the microorganism's ability to adhere itself and form a biofilm could play a very important role in the pathogenesis during trichosporonosis. In 2006, Di Bonaventura et al. assessed the biofilm growth kinetics in vitro for some clinical isolates of T. asahii. They found that T. asahii cells were capable of quickly adhering to polystyrene after incubation for 30 minutes, displaying a low metabolic activity during the first 4 hours. The biofilm's complexity increased after 6 to 8 hours of incubation, period during which it was possible to observe a monolayer formed by filamentous structures. At 72 hours, the cells showed both yeast-like and filamentous structures embedded in an extracellular matrix, forming a mature biofilm ranging from 20 to 40 μm in thickness. Biofilm formation was accompanied by a consequent increase in the resistance to voriconazole (up to 16,000 times more compared to planktonic cells).16 That same year, Dað and Cerikçioðlu reported a moderate to weak production of biofilms in 58% of the clinically isolated T. asahii species that were analyzed.8Associated infections Table 1 summarizes the main clinical manifestations and risk factors in infections caused by Trichosporon spp.<img alt="Table 1 Infections caused by Trichosporon spp., main clinical manifestations and risk factors." src="304v16n62-90328370fig1.jpg"></img>White piedra White piedra is an infection in which white nodules are formed due to the aggregation of conidia around the hair shaft. These nodules are soft, whitish, have a defined border, and measure approximately between 1 and 3 mm of diameter. White piedra mainly affects capital hair; however, the infection may present itself in the hair of armpits, pubis, and in a lesser degree moustaches and beards. It is a chronic and asymptomatic disease. It is a superficial infection in which fungi remain in contact with the cuticle, without invading neither the hair medulla, scalp, nor skin.3 White piedra is a cosmopolitan and exogenous mycosis occurring more frequently in tropical and temperate climates. Humidity and poor hygiene are among the risk factors for the attainment of this pathology. Women and children are the groups mainly affected by capital white piedra.17,18 Most cases of genital white piedra, second in incidence, involve males between 15 and 44 years of age.19,20T. asahii, T. inkin, T. cutaneum, T. mucoides, and T. ovoides have all been associated with white piedra, T. ovoides being the one with the highest incidence.1,21Trichosporonosis When Trichosporon spp. develops as an invasive infection, the disease is known as trichosporonosis. This infection has a mortality rate between 50% and 80%,22 and it is the second or third cause of fungemia in immunocompromised patients just after Candida spp.23-25 Trichosporonosis is considered an endogenous disease because the microorganism is commonly found as a part of the flora in the gastrointestinal tract, lungs, and skin.1,3 These opportunistic systemic infections have gained clinical importance due to their growing prevalence in certain groups of patients. Neutropenia is the main risk factor. A relationship between trichosporonosis and having undergone an invasive clinical procedure (e.g., probes and catheters) has been established as well. Kontoyannis et al. (2004) evaluated risk factors associated with the infection caused by Trichosporon spp. in 17 cancer patients. They observed that out of the 10 patients who displayed fungemia, 41% developed trichosporonosis subsequent to the use of catheters. The underlying disease in most patients was acute leukemia, and in 65% of the cases neutropenia was observed. Some patients had received chemotherapy (76%) or high doses of corticosteroids (89%) 1 month prior to the trichosporonosis diagnosis.26 Girmenia et al. (2005) performed a retrospective study including 287 cases of trichosporonosis worldwide. They found that 62.8% of the patients had suffered from a hematologic disease previous to the trichosporonosis diagnosis. Acute leukemia had the highest incidence (68%). Other conditions of risk associated with the development of trichosporonosis were solid tumors, transplants, peritoneal dialysis, and human immunodeficiency virus.27 Ruan et al. (2009), based on a study of 19 cases of invasive trichosporonosis, reported the use of central catheters as the main risk factor (90%).22 Suzuki et al. (2010) analyzed 33 patients with hematological diseases; the results were similar to the ones previously reported: acute leukemia (82%) and neutropenia (85%) were the main risk factors for trichosporonosis. Moreover, it was observed that most patients were undergoing chemotherapy when diagnosed with this mycosis.28 The main trichosporonosis manifestations are fever and fungemia. However, tissue invasion may develop. Cases of inflammation and abscesses in different organs and tissues (heart, brain, liver, spleen, esophagus, urinary tract, joints, peritoneum) have been reported. T. asahii, T. asteroides, T. cutaneum, T. inkin and T. mucoides are the 5 most common species associated with trichosporonosis cases.9,22,29-32 Tissue invasion and damage There are reports using murine models for evaluating tissue damage in invassive infections by Trichosporon spp.. Mice require cyclophosphamide-induced immunosuppression prior to high doses of fungi inoculation, which emulates the neutropenia in patients who develop trichosporonosis. Studies in animal survival have proven that the establishment of the infection is dose dependent. However, both the inoculum size causing mortality and time elapsed until tissue invasion is detected vary in different reports. Gokaslan and Anaissie determined that an inoculum of ≥ 2 x 107 colony forming units (CFU) causes 100% mortality and invasion of organs in immunosupressed mice 6 days after infection.34 On the other hand, Hospenthal et al. reported that an inoculum of ≥ 7 x 106 CFU caused 100% mortality with tissue invasion 6 hours after infection.35 These models were developed with infection by T. beigelii, therefore the observed differences in infectivity and progress of the disease could be a result of an induced infection by an unidentified species of the genus Trichosporon. Yamagata et al. utilized an inoculum of 3 x 106 CFU of T. asahii in a model in which mice were immunosuppressed at week 1, showing a significant difference compared to the animals which were not immunosup-pressed or those receiving a second cyclophosphamide dose at week 3 (20% of mortality). They concluded that the first 3 weeks are critical for the development of systemic trichosporonosis by T. asahii.29 Fungi presence in the affected organs is generalized. Persistence of the microorganism in kidneys of immunosuppressed mice as well as of immunocompetent ones has been reported. In animal groups where mortality is induced via inoculation of lethal doses, the initial inoculum has been recovered as much as 36-fold from brain, heart and kidney. A resolution of the infection in re-immunosuppressed animals has not been observed. The presence of Trichosporon spp. has been confirmed by molecular methods, even when the cell count is under the detection limits.29,34,35 Hyphae and conidia have been observed in different proportions depending on the organ and the stage of infection. Yeast-like structures are often found in earlier stages, while hyphae and arthroconidia are present in later stages of the infection. Predominance of yeast-like structures in the lungs of the infected animals has been reported.35 One of the most prevalent signs of invasive trichosporonosis is the granulomatous inflammation reported in lungs, liver, lymph nodes, and spleen in immunosuppressed and immunecompetent mice, as well as a fungal invasion of the blood vessels' lumen or periphery.34-36 Other findings include kidney, spleen, lung, and heart hyperemia. Tubular edema, focal parenchymal destruction, cortical tubular necrosis, and chronic inflammation with fibrosis have been observed in the kidneys of mice surviving infection. In the liver, hepatic sinus dilation and congestion have been reported, as well as degeneration and necrosis of some hepatocytes and proliferation of Kupffer cells. Splenic sinuses dilation and splenomegaly have also been observed. In lungs, edema, hemorrhage, and alveolar ectasia have been described. In the heart, evidence of hemorrhage and cardiomyocytes necrosis have been reported. 34-37 Onychomycosis In the last few years, cases of onychomycosis associated with infections caused by Trichosporon spp. have increased. Around the world, this genus is the agent responsible for 1.3% to 10% of onychomycosis cases, being T. asahii, T. mucoides, and T. inkin the most frequently involved microorganisms.38-40 There have been discrepancies between cases reported in Mexico and other countries. In a study performed in pediatric patients from a rural area, Archer-Dubon et al. isolated T. cutaneum in 42% of the patients with onychomycosis and athlete's foot, a percentage higher than the estimated for infections by dermatophytes and Candida spp., microorganisms typically responsible for foot infections.41Laboratory diagnosis Clinical laboratory diagnosis varies in cases of superficial and systemic infections. In the case of white piedra, the hair sample is submerged in a potassium hydroxide solution for observation under the microscope of the nodules formed by the aggregated spores around the hair shaft, which allows differential diagnosis of other parasitizations such as pediculosis or trichomycosis. Similarly, onychomycosis diagnosis requires the nail scrape to be submerged in potassium hydroxide for microscopic observation of conidia and hyphae. In both cases, precise etiologic diagnosis requires a culture. Trichosporonosis diagnosis is made routinely by the recovery of fungi from blood and/or biopsies.3 Cultures obtained from diverse clinical samples are used for identifying the etiologic agent through its microscopic morphology by confirming the presence of the 3 characteristic structures of the genus Trichosporon: hyphae, arthrocondia, and blastocondia. The biochemical profile may be obtained by auxanography, which evaluates the ability to assimilate different sources of carbon. However, the complete biochemical characterization of species of the genus Trichosporon is based on the assimilation of approximately 50 carbon compounds and requires anywhere between 5 and 15 days for the readings; consequently, it is not practical to carry out this battery of tests for the precise identification of pathogenic species. There are commercial methods which systematize the application of assimilation tests and reduce the required identification time. The API 20C AUX system by bioMérieux is a commercial micromethod, which has turned into the most used in clinical laboratories. This system evaluates the assimilation ability of 19 carbohydrates and allows identification within a timeframe of 24 to 72 hours of incubation. However, a limitation of this test is that it only allows the identification of 3 species of the genus: T. asahii, T. inkin, and T. mucoides. This last characteristic prevents its generalized use. Different molecular methods have been developed as fast and effective alternatives for the precise identification of many pathogens at the species level. Ribosomal DNA is widely used in the systematic identification of microorganisms. Molecular identification of fungi is typically performed by sequencing of the internal transcribed spacer (ITS) region. One of the inconveniences of this region is the fact that it is highly homologous between the different species in the genus Trichosporon; therefore, the analysis of other genes or regions with higher heterology is needed in order to obtain a more accurate identification. Sugita et al. analyzed 84 strains corresponding to 25 species of the genus Trichosporon to evaluate the efficacy of sequencing the ITS region and the intergenic spacer 1 (IGS1) region for the precise identification at a species level. They found a higher heterology between IGS1 regions in comparison to ITS. This makes the IGS1 sequencing analysis superior compared to ITS for the differentiation between species of the genus. In addition, this method allows genotypification.42 A growing number of reports reveal the effectiveness of molecular methods in the identification of this microorganism. These publications show the lack of specificity of the conventional identification methods based in morphologic and biochemical criteria.43-46Treatment Superficial infections caused by Trichosporon spp. may be treated with galenic solutions such as 1% mercuric chloride, 1% iodine solution, and 30% salicylic acid. They may be treated with topical antifungals, mainly imidazoles like econazole, isoconazole, miconazole, and ketoconazole. In patients with white piedra, the trimming or shaving of parasitized hairs or affected areas prior to topical treatment is recommended.1,3,17 Management of deep infections has been a bigger challenge. Trichosporon spp. has displayed variable resistance to the most common antifungal treatments; consequently, there is no optimal treatment for trichosporonosis cases.In vitro susceptibility Trichosporon spp. was first reported as an amphotericin B-resistant pathogen by Walsh et al. in 1990, after evaluating 2 T. beigelii isolates obtained from patients with systemic infections.47 Since its taxonomic revision, several studies have assessed the efficacy of different antifungals against the species of the genus, mainly T. asahii. It is important to mention that to this day there is not an established method to determine in vitro susceptibility of species belonging to the genus Trichosporon. The most widely used protocol is an adaptation of the method used for Candida spp. and C. neoformans described in documents M27 and M44 of the Clinical and Laboratory Standards Institute. One of the most evaluated antifungals has been amphotericin B (AMB). This is a polyenic derivate that destabilizes the fungal cytoplasmic membrane; it is the treatment of choice for systemic infections. The resistance of Trichosporon spp. to AMB has been reported. T. asahii consistently exhibits a MIC of ≥ 2 μg/mL (Minimal Inhibitory Concentration, which prevents visible growth of 90% of isolates).22,44,48,49 There are similar MICs for other clinical isolates including T. asteroides, T. cutaneum, and T. ovoides.22 Rodríguez-Tudela et al. (2005), contrary to the previous study, reported low MICs for T. cutaneum (0.25-0.5 μg/ml) and T. ovoides (0.37 μg/ml). T. mucoides showed great variability regarding susceptibility to AMB, with MICs ranging between 0.015 and 16.0 μg/ml.44T. inkin is the species which has displayed greater in vitro susceptibility to the inhibitory activity of AMB, with MICs from 0.14 to 1.0 μg/ml.44,48 Triazolic compounds are inhibitors of the ergosterol synthesis, the main component of the fungal cytoplasmic membrane. In addition, they interact with enzymes at a mitochondrial level causing the accumulation of free radicals inside the cell and provoking the inhibition of fungal growth. Triazolics include fluconazole (FLC), voriconazole (VRC), itraconazole (ITR), and posaconazole (POS). These agents have displayed better in vitro activity against Trichosporon spp., with relatively low MICs for T. asahii (FLC 1.27 to ≤ 10.3 μg/ml, ITR ≤ 1.4 μg/ml, POS 0.25 μg/ml), T. asteroides (FLC 0.8 μg/ml, ITR 0.06 μg/ml), T. inkin (FLC ≤ 4 μg/ml, ITR ≤ 1 μg/ml), T. cutaneum (FLC ≤ 32 μg/ml, ITR ≤ 1 μg/ ml), and T. ovoides (FLC 1.74 μg/ml, ITR 0.1 μg/ml).22,44,48,49 Voriconazole is particularly effective for fungal inhibition in vitro, with MICs of ≤ 0.28 μg/ml for the 6 more frequently isolated Trichosporon species causing human pathology.44,49 Terbinafine (TER) is a synthetic antifungal derived from allylamines that inhibits ergosterol synthesis. TER requires high concentrations in order to inhibit T. asahii (12.6 μg/ ml), as opposed to the inhibition of T. cutaneum o T. inkin (1 μg/ml).48 5-Flucytosine (5-FC) is an inhibitor of the synthesis of nucleic acids; it interacts with the fungal RNA disrupting the synthesis of proteins. 5-FC has shown poor antifungal activity against the most clinically relevant species, with MICs ≥ 2 μg/ml and reaching concentrations of up to 128 μg/ml for T. mucoides.9,22,44,49 Caspofungin (CAS) is an echinocandin that inhibits the synthesis of the fungal cell wall. CAS MICs are high for T. asahii (≥ 4 μg/ml) and T. asteroides (16 μg/ml).49,50 Immunotherapy Since neutropenia is the main condition associated with the development of trichosporonosis, the use of cytokines has been considered for the treatment of these infections. Some of the factors used are the granulocytes colony stimulating factors (G-CSF), which increase polymorphonuclear cell count, and the granulocytes-macrophages colony stimulating factors (GM-CSF), which activate monocytes and macrophages functions. Muranka et al. (1997) used a murine model with disseminated T. asahii trichosporonosis for the evaluation of G-CSF and GM-CSF as therapy against systemic infection. They observed that the use of G-CSF prior to fungal infection increased the survival in mice from 25% to 100%, decreasing the fungal load and tissue damage in affected organs, with the most notable improvement in the lungs. The increase in neutrophils by GM-CSF was lower than the one caused by G-CSF, so the use of GM-CSF therapy did not generate any major improvements in animals. In the same study, they observed an increase of tumor necrosis factor alpha (TNF-α) in bronchoalveolar lavage fluid in mice infected with lethal doses of T. asahii and treated with GMCSF compared to non-immunosuppressed animals or animals treated with G-CSF. In addition, a negative correlation between TNF-α production and the presence of leukocytes in peripheral blood was observed, decreasing as mice recuperated from the neutropenia. Anti-TNF-α therapy did not favor infection resolution. The investigators concluded that neutrophil count was the most critical factor in the development of trichosporonosis; however, other factors, such as TNF-α in lung, played an important role in the resolution of the infection.51 Similarly, the use of macrophages colony stimulating factor (M-CSF) has been evaluated as an activator of phagocytosis in a trichosporonosis murine model with T. asahii. M-CSF increased fungicidal activity in mononuclear cells, with a notable increase in survival and a decrease in fungal load. In addition, an increase in TNF-α in lungs and plasma in animals treated with M-CSF was noticeable. Different from the results reported by Muranaka et al., anti-TNF-α treatment did increase survival in mice. Results showed how M-CSF exponentially increased fungal activity by mononuclear phagocytes, helped partly by the production of TNF-α.52 Similar results regarding the effect of G-CSF, GM-CSG, and M-CSF on leukocytes and their role in trichosporonosis resolution were reported by Roilides et al. (2002).53 Conclusion Vast distribution, antifungal resistance, and an increase in the number of patients presenting risk factors have made relevant the study of species belonging to the genus Trichosporon as opportunistic fungal agents relevant. High mortality rates in patients with systemic infections as well as a lack of an optimal treatment generate the need to increase the knowledge of this particular pathogen, in a way that allows us to understand its virulence mechanisms, and consequently, to obtain the necessary tools for the development of effective therapies against these microorganisms.Conflicts of interest The authors have no conflicts of interest to declare.Funding No financial support was provided.<hr></hr> Received: September 2013; Accepted: December 2013 * Corresponding author: Department of Microbiology, Faculty of Medicine, Universidad Autónoma de Nuevo León, Monterrey, N. L., Mexico. E-mail address: <a href="mailto:alexandra.montoya@aol.com" class="elsevierStyleCrossRefs">alexandra.montoya@aol.com</a> (A. M. Montoya)." 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The present paper is a review on the virulence factors, associated infections, and in vitro susceptibility of the species with the highest incidence as pathogenic agents in humans." ] ] "multimedia" => array:2 [ 0 => array:8 [ "identificador" => "tbl1" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:1 [ "tablaImagen" => array:1 [ 0 => array:4 [ "imagenFichero" => "304v16n62-90328370fig1.jpg" "imagenAlto" => 925 "imagenAncho" => 2108 "imagenTamanyo" => 222111 ] ] ] ] ] "descripcion" => array:1 [ "en" => "Infections caused by Trichosporon spp., main clinical manifestations and risk factors." ] ] 1 => array:7 [ "identificador" => "tbl2" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "descripcion" => array:1 [ "en" => "Infections caused by Trichosporon spp., main clinical manifestations and risk factors." ] ] ] "bibliografia" => array:2 [ "titulo" => "Bibliography" "seccion" => array:1 [ 0 => array:1 [ "bibliografiaReferencia" => array:53 [ 0 => array:3 [ "identificador" => "bib1" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Current knowledge of Trichosporon spp. and trichosporonosis. 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A. M.. Montoyaa, G. M.. Gonzáleza

a Department of Microbiology, Faculty of Medicine, Universidad Autónoma de Nuevo León, Monterrey, N. L., Mexico

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    "titulo" => "<span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46;&#58;</span> an emerging fungal pathogen"
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    "textoCompleto" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">Introduction </span></p><p class="elsevierStylePara"><span class="elsevierStyleItalic">Trichosporon </span>spp&#46; was first described by Beigel in 1865 as the agent responsible for a benign hair infection called white <span class="elsevierStyleItalic">piedra</span> &#40;meaning &#34;stone&#34; in Spanish&#41;&#46; Beigel classified the microorganism as algae and placed it in the genus <span class="elsevierStyleItalic">Pleurococcus&#46;</span> It wasn&#39;t until 1890 when Behrend identified the microorganism causing white <span class="elsevierStyleItalic">piedra</span> as a fungus which he called <span class="elsevierStyleItalic">Trichosporon ovoides&#46;</span><span class="elsevierStyleSup">1</span> Although generally associated with this superficial infection&#44; <span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46;</span> has gained importance as one of the most opportunistic systemic infections since the first case of invasive trichosporonosis involving the brain&#44; reported in 1970&#46;<span class="elsevierStyleSup">2</span></p><p class="elsevierStylePara"><span class="elsevierStyleItalic"><span class="elsevierStyleBold">Trichosporon</span></span><span class="elsevierStyleBold"> spp&#46; </span></p><p class="elsevierStylePara"><span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46;</span> belongs to the phylum Basidiomycota&#46; It is a yeast-like fungus macroscopically characterized by forming radially symmetrical colonies&#59; these colonies may be white or yellowish&#44; with a smooth texture&#44; creamy&#44; cerebriform&#44; powdery or moist&#46; Microscopically&#44; <span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46;</span> forms hyaline septate hyphae&#44; with abundant arthroconidia and blastoconidia&#44; and in some cases presents appressoria&#46; Regarding physiological tests&#44; they assimilate several carbohydrates and other carbon sources&#44; yet they do not possess fermentation capabilities&#46; A major characteristic of the <span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46;</span> genus is their ability to hydrolize urea&#46;<span class="elsevierStyleSup">1&#44;3-5</span></p><p class="elsevierStylePara"> In 1902 Vuillemin grouped the species described for this genus under the <span class="elsevierStyleItalic">Trichosporon beigelii</span> denomination&#44; a practice that remained until the late 90&#39;s&#46;<span class="elsevierStyleSup">5&#44;6</span> Nevertheless&#44; posterior classifications at morphological&#44; biochemical&#44; and molecular levels provided evidence of the existence of more than one species in the genus&#46;</p><p class="elsevierStylePara"> Approximately 50 species of the genus <span class="elsevierStyleItalic">Trichosporon</span> have been characterized<span class="elsevierStyleItalic">&#44; </span>16 of which are associated with diseases in humans&#46; Gu&#233;ho et al&#46; &#40;1994&#41; typified species that had displayed a major adaptation to the human body&#58; <span class="elsevierStyleItalic">T&#46; asahii&#44; T&#46; asteroides&#44; T&#46; cutaneum&#44; T&#46; inkin&#44; T&#46; mucoides </span>and <span class="elsevierStyleItalic">T&#46; ovoides</span>&#46; These 6 species&#44; reclassified from the <span class="elsevierStyleItalic">Trichosporon beigelii </span>taxon<span class="elsevierStyleItalic">&#44;</span> remain the most relevant clinical species to date&#46;<span class="elsevierStyleSup">7</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Virulence factors </span></p><p class="elsevierStylePara"> There is little information regarding virulence factors produced by this microorganism&#46;</p><p class="elsevierStylePara"> Hemolysins&#44; proteases&#44; and lipases allow protein degradation and destabilization of the membranes of the host cell&#44; increasing fungus pathogenicity&#46; Da&#240; and Cerik&#231;io&#240;lu analyzed the production of proteases&#44; phospholipases&#44; and esterases of 48 <span class="elsevierStyleItalic">T&#46; asahii</span> clinical isolates&#44; and did not detect protease nor phospholipase activity in any of the isolates analyzed&#59; however&#44; all the evaluated strains displayed esterase activity&#46;<span class="elsevierStyleSup">8</span> Similarly&#44; Sun et al&#46; evaluated protease&#44; phospholipase&#44; and hemolysine production in 23 <span class="elsevierStyleItalic">T&#46; asahii</span> clinical isolates&#44; and observed no protease nor phospholipase activity&#44; yet 100&#37; of isolates showed hemolysin activity&#46; This activity&#44; however&#44; varied for the different <span class="elsevierStyleItalic">T&#46; asahii</span> genotypes identified&#46;<span class="elsevierStyleSup">9</span> It is important to underline that there are no reports about the production of lytic enzymes for <span class="elsevierStyleItalic">Trichosporon </span>non<span class="elsevierStyleItalic">-asahii </span>species<span class="elsevierStyleItalic">&#46; </span></p><p class="elsevierStylePara"> Phenotypic switching is a fast and reversible change of colonial morphology and&#47;or microscopic features&#46; These changes may occur as a response to different environmental stimuli such as oxidative stress or lack of nutrients&#44; or intrinsic factors such as a mutation in the deoxyribonucleic acid &#40;DNA&#41; repair systems&#46;<span class="elsevierStyleSup">10</span> When phenotypic switching occur <span class="elsevierStyleItalic">in vivo</span>&#44; they involve modifications in the expression of virulence factors&#44; or alterations in the microorganism-host cell interactions&#44; thus provoking an increment in the pathogenicity and evasion of the immune response&#44; as observed in <span class="elsevierStyleItalic">Candida albicans</span> and <span class="elsevierStyleItalic">Cryptococcus neoformans</span>&#46;<span class="elsevierStyleSup">11-13</span> Lee et al&#46;&#44; reported phenotypic switching <span class="elsevierStyleItalic">in vitro</span> for the first time for <span class="elsevierStyleItalic">T&#46; beigelii</span>&#46; The isolated microorganism&#44; recovered from a patient with a systemic infection&#44; was capable of producing two different morphologies when cultivated at 30&#176;C&#46; Such morphotypes were accompanied by their respective structural microscopic changes&#46; Thus&#44; a rough&#44; cerebriform&#44; moist colony with irregular edges was accompanied microscopically by hyphae while a second powder morphotype&#44; with a more regular topography and borders&#44; showed microscopically a greater proportion of arthroconidia or blastoconidia&#46;<span class="elsevierStyleSup">4</span> The phenotypic switching was also reported <span class="elsevierStyleItalic">in vivo</span> by Karashima et al&#46;&#44; who performed experiments involving repetitive inoculation of <span class="elsevierStyleItalic">T&#46; asahii</span> in mice&#46; They observed macro- and microscopic morphological differences when comparing the fungi before being inoculated and the same fungi recovered after 3 repetitive passages in 8-week-old ICR mice&#46; Similar to the results obtained by Lee et al&#46;&#44; Karashima observed that the rugged colony was accompanied microscopically by a greater proportion of hyphae&#44; while a powdery colony was accompanied by a greater amount of conidia&#46;<span class="elsevierStyleSup">14</span></p><p class="elsevierStylePara"> In the same paper&#44; Karashima et al&#46; reported the production of a cell wall component similar to the glucuronoxylomannan &#40;GXM&#41; of <span class="elsevierStyleItalic">C&#46; neoformans&#46;</span> They observed that a larger amount of GXM was present in the recovered microorganism after repeated inoculations in mice&#46; GXM has been proposed to offer <span class="elsevierStyleItalic">C&#46; neoformans </span>protection against phagocytosis by neutrophils and monocytes&#46;<span class="elsevierStyleSup">14</span></p><p class="elsevierStylePara"> Another factor providing protection to the fungus is the formation of biofilms&#46; Some microorganisms have the ability to produce an extracellular matrix&#44; formed by polysaccharides&#44; proteins&#44; and DNA&#44; which allow conglomeration of cells and their adherence to both organic and inorganic surfaces&#46;<span class="elsevierStyleSup">15</span> Due to the association of invasive infections to the use of catheters and similar devices&#44; the microorganism&#39;s ability to adhere itself and form a biofilm could play a very important role in the pathogenesis during trichosporonosis&#46; In 2006&#44; Di Bonaventura et al&#46; assessed the biofilm growth kinetics <span class="elsevierStyleItalic">in vitro</span> for some clinical isolates of <span class="elsevierStyleItalic">T&#46; asahii&#46; </span>They found that <span class="elsevierStyleItalic">T&#46; asahii</span> cells were capable of quickly adhering to polystyrene after incubation for 30 minutes&#44; displaying a low metabolic activity during the first 4 hours&#46; The biofilm&#39;s complexity increased after 6 to 8 hours of incubation&#44; period during which it was possible to observe a monolayer formed by filamentous structures&#46; At 72 hours&#44; the cells showed both yeast-like and filamentous structures embedded in an extracellular matrix&#44; forming a mature biofilm ranging from 20 to 40 &#956;m in thickness&#46; Biofilm formation was accompanied by a consequent increase in the resistance to voriconazole &#40;up to 16&#44;000 times more compared to planktonic cells&#41;&#46;<span class="elsevierStyleSup">16 </span>That same year&#44; Da&#240; and Cerik&#231;io&#240;lu reported a moderate to weak production of biofilms in 58&#37; of the clinically isolated <span class="elsevierStyleItalic">T&#46; asahii</span> species that were analyzed&#46;8</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Associated infections </span></p><p class="elsevierStylePara"> Table 1 summarizes the main clinical manifestations and risk factors in infections caused by <span class="elsevierStyleItalic">Trichosporon </span>spp&#46;</p><p class="elsevierStylePara"><img alt="Table 1 Infections caused by Trichosporon spp&#46;&#44; main clinical manifestations and risk factors&#46;" src="304v16n62-90328370fig1.jpg"></img></p><p class="elsevierStylePara"><span class="elsevierStyleBold">White </span><span class="elsevierStyleItalic"><span class="elsevierStyleBold">piedra </span></span></p><p class="elsevierStylePara"> White <span class="elsevierStyleItalic">piedra</span> is an infection in which white nodules are formed due to the aggregation of conidia around the hair shaft&#46; These nodules are soft&#44; whitish&#44; have a defined border&#44; and measure approximately between 1 and 3 mm of diameter&#46; White <span class="elsevierStyleItalic">piedra</span> mainly affects capital hair&#59; however&#44; the infection may present itself in the hair of armpits&#44; pubis&#44; and in a lesser degree moustaches and beards&#46; It is a chronic and asymptomatic disease&#46; It is a superficial infection in which fungi remain in contact with the cuticle&#44; without invading neither the hair medulla&#44; scalp&#44; nor skin&#46;<span class="elsevierStyleSup">3</span></p><p class="elsevierStylePara"> White <span class="elsevierStyleItalic">piedra</span> is a cosmopolitan and exogenous mycosis occurring more frequently in tropical and temperate climates&#46; Humidity and poor hygiene are among the risk factors for the attainment of this pathology&#46; Women and children are the groups mainly affected by capital white <span class="elsevierStyleItalic">piedra</span>&#46;<span class="elsevierStyleSup">17&#44;18</span></p><p class="elsevierStylePara"> Most cases of genital white <span class="elsevierStyleItalic">piedra</span>&#44; second in incidence&#44; involve males between 15 and 44 years of age&#46;<span class="elsevierStyleSup">19&#44;20</span><span class="elsevierStyleItalic">T&#46; asahii&#44; T&#46; inkin&#44; T&#46; cutaneum&#44; T&#46; mucoides&#44; </span>and <span class="elsevierStyleItalic">T&#46; ovoides </span>have all been associated with white <span class="elsevierStyleItalic">piedra</span>&#44; <span class="elsevierStyleItalic">T&#46; ovoides</span> being the one with the highest incidence&#46;<span class="elsevierStyleSup">1&#44;21</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Trichosporonosis </span></p><p class="elsevierStylePara"> When <span class="elsevierStyleItalic">Trichosporon spp&#46;</span> develops as an invasive infection&#44; the disease is known as trichosporonosis&#46; This infection has a mortality rate between 50&#37; and 80&#37;&#44;<span class="elsevierStyleSup">22</span> and it is the second or third cause of fungemia in immunocompromised patients just after <span class="elsevierStyleItalic">Candida </span>spp<span class="elsevierStyleItalic">&#46;</span><span class="elsevierStyleSup">23-25</span> Trichosporonosis is considered an endogenous disease because the microorganism is commonly found as a part of the flora in the gastrointestinal tract&#44; lungs&#44; and skin&#46;<span class="elsevierStyleSup">1&#44;3</span></p><p class="elsevierStylePara"> These opportunistic systemic infections have gained clinical importance due to their growing prevalence in certain groups of patients&#46; Neutropenia is the main risk factor&#46; A relationship between trichosporonosis and having undergone an invasive clinical procedure &#40;<span class="elsevierStyleItalic">e&#46;g&#46;</span>&#44; probes and catheters&#41; has been established as well&#46;</p><p class="elsevierStylePara"> Kontoyannis et al&#46; &#40;2004&#41; evaluated risk factors associated with the infection caused by <span class="elsevierStyleItalic">Trichosporon spp&#46;</span> in 17 cancer patients&#46; They observed that out of the 10 patients who displayed fungemia&#44; 41&#37; developed trichosporonosis subsequent to the use of catheters&#46; The underlying disease in most patients was acute leukemia&#44; and in 65&#37; of the cases neutropenia was observed&#46; Some patients had received chemotherapy &#40;76&#37;&#41; or high doses of corticosteroids &#40;89&#37;&#41; 1 month prior to the trichosporonosis diagnosis&#46;<span class="elsevierStyleSup">26</span> Girmenia et al&#46; &#40;2005&#41; performed a retrospective study including 287 cases of trichosporonosis worldwide&#46; They found that 62&#46;8&#37; of the patients had suffered from a hematologic disease previous to the trichosporonosis diagnosis&#46; Acute leukemia had the highest incidence &#40;68&#37;&#41;&#46; Other conditions of risk associated with the development of trichosporonosis were solid tumors&#44; transplants&#44; peritoneal dialysis&#44; and human immunodeficiency virus&#46;<span class="elsevierStyleSup">27</span> Ruan et al&#46; &#40;2009&#41;&#44; based on a study of 19 cases of invasive trichosporonosis&#44; reported the use of central catheters as the main risk factor &#40;90&#37;&#41;&#46;<span class="elsevierStyleSup">22</span> Suzuki et al&#46; &#40;2010&#41; analyzed 33 patients with hematological diseases&#59; the results were similar to the ones previously reported&#58; acute leukemia &#40;82&#37;&#41; and neutropenia &#40;85&#37;&#41; were the main risk factors for trichosporonosis&#46; Moreover&#44; it was observed that most patients were undergoing chemotherapy when diagnosed with this mycosis&#46;<span class="elsevierStyleSup">28 </span></p><p class="elsevierStylePara"> The main trichosporonosis manifestations are fever and fungemia&#46; However&#44; tissue invasion may develop&#46; Cases of inflammation and abscesses in different organs and tissues &#40;heart&#44; brain&#44; liver&#44; spleen&#44; esophagus&#44; urinary tract&#44; joints&#44; peritoneum&#41; have been reported&#46; <span class="elsevierStyleItalic">T&#46; asahii&#44; T&#46; asteroides&#44; T&#46; cutaneum&#44; T&#46; inkin </span>and <span class="elsevierStyleItalic">T&#46; mucoides </span>are the 5 most common species associated with trichosporonosis cases&#46;<span class="elsevierStyleSup">9&#44;22&#44;29-32 </span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Tissue invasion and damage </span></p><p class="elsevierStylePara"> There are reports using murine models for evaluating tissue damage in invassive infections by <span class="elsevierStyleItalic">Trichosporon</span> spp&#46;&#46; Mice require cyclophosphamide-induced immunosuppression prior to high doses of fungi inoculation&#44; which emulates the neutropenia in patients who develop trichosporonosis&#46;</p><p class="elsevierStylePara"> Studies in animal survival have proven that the establishment of the infection is dose dependent&#46; However&#44; both the inoculum size causing mortality and time elapsed until tissue invasion is detected vary in different reports&#46; Gokaslan and Anaissie determined that an inoculum of &#8805; 2 x 10<span class="elsevierStyleSup">7 </span>colony forming units &#40;CFU&#41; causes 100&#37; mortality and invasion of organs in immunosupressed mice 6 days after infection&#46;<span class="elsevierStyleSup">34</span> On the other hand&#44; Hospenthal et al&#46; reported that an inoculum of &#8805; 7 x 10<span class="elsevierStyleSup">6 </span>CFU caused 100&#37; mortality with tissue invasion 6 hours after infection&#46;<span class="elsevierStyleSup">35</span> These models were developed with infection by <span class="elsevierStyleItalic">T&#46; beigelii</span>&#44; therefore the observed differences in infectivity and progress of the disease could be a result of an induced infection by an unidentified species of the genus <span class="elsevierStyleItalic">Trichosporon</span>&#46; Yamagata et al&#46; utilized an inoculum of 3 x 10<span class="elsevierStyleSup">6</span> CFU of <span class="elsevierStyleItalic">T&#46; asahii</span> in a model in which mice were immunosuppressed at week 1&#44; showing a significant difference compared to the animals which were not immunosup-pressed or those receiving a second cyclophosphamide dose at week 3 &#40;20&#37; of mortality&#41;&#46; They concluded that the first 3 weeks are critical for the development of systemic trichosporonosis by T&#46; <span class="elsevierStyleItalic">asahii&#46;</span><span class="elsevierStyleSup">29</span></p><p class="elsevierStylePara"> Fungi presence in the affected organs is generalized&#46; Persistence of the microorganism in kidneys of immunosuppressed mice as well as of immunocompetent ones has been reported&#46; In animal groups where mortality is induced via inoculation of lethal doses&#44; the initial inoculum has been recovered as much as 36-fold from brain&#44; heart and kidney&#46; A resolution of the infection in re-immunosuppressed animals has not been observed&#46; The presence of Trichosporon spp&#46; has been confirmed by molecular methods&#44; even when the cell count is under the detection limits&#46;<span class="elsevierStyleSup">29&#44;34&#44;35</span></p><p class="elsevierStylePara"> Hyphae and conidia have been observed in different proportions depending on the organ and the stage of infection&#46; Yeast-like structures are often found in earlier stages&#44; while hyphae and arthroconidia are present in later stages of the infection&#46; Predominance of yeast-like structures in the lungs of the infected animals has been reported&#46;<span class="elsevierStyleSup">35</span></p><p class="elsevierStylePara"> One of the most prevalent signs of invasive trichosporonosis is the granulomatous inflammation reported in lungs&#44; liver&#44; lymph nodes&#44; and spleen in immunosuppressed and immunecompetent mice&#44; as well as a fungal invasion of the blood vessels&#39; lumen or periphery&#46;<span class="elsevierStyleSup">34-36</span></p><p class="elsevierStylePara"> Other findings include kidney&#44; spleen&#44; lung&#44; and heart hyperemia&#46; Tubular edema&#44; focal parenchymal destruction&#44; cortical tubular necrosis&#44; and chronic inflammation with fibrosis have been observed in the kidneys of mice surviving infection&#46; In the liver&#44; hepatic sinus dilation and congestion have been reported&#44; as well as degeneration and necrosis of some hepatocytes and proliferation of Kupffer cells&#46; Splenic sinuses dilation and splenomegaly have also been observed&#46; In lungs&#44; edema&#44; hemorrhage&#44; and alveolar ectasia have been described&#46; In the heart&#44; evidence of hemorrhage and cardiomyocytes necrosis have been reported&#46;<span class="elsevierStyleSup"> 34-37 </span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Onychomycosis </span></p><p class="elsevierStylePara"> In the last few years&#44; cases of onychomycosis associated with infections caused by <span class="elsevierStyleItalic">Trichosporon </span>spp&#46; have increased&#46; Around the world&#44; this genus is the agent responsible for 1&#46;3&#37; to 10&#37; of onychomycosis cases&#44; being <span class="elsevierStyleItalic">T&#46; asahii&#44; T&#46; mucoides&#44; </span>and <span class="elsevierStyleItalic">T&#46; inkin</span> the most frequently involved microorganisms&#46;<span class="elsevierStyleSup">38-40</span> There have been discrepancies between cases reported in Mexico and other countries&#46; In a study performed in pediatric patients from a rural area&#44; Archer-Dubon et al&#46; isolated T&#46; cutaneum in 42&#37; of the patients with onychomycosis and athlete&#39;s foot&#44; a percentage higher than the estimated for infections by dermatophytes and Candida spp&#46;&#44; microorganisms typically responsible for foot infections&#46;<span class="elsevierStyleSup">41</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Laboratory diagnosis </span></p><p class="elsevierStylePara"> Clinical laboratory diagnosis varies in cases of superficial and systemic infections&#46; In the case of white <span class="elsevierStyleItalic">piedra</span>&#44; the hair sample is submerged in a potassium hydroxide solution for observation under the microscope of the nodules formed by the aggregated spores around the hair shaft&#44; which allows differential diagnosis of other parasitizations such as pediculosis or trichomycosis&#46; Similarly&#44; onychomycosis diagnosis requires the nail scrape to be submerged in potassium hydroxide for microscopic observation of conidia and hyphae&#46; In both cases&#44; precise etiologic diagnosis requires a culture&#46; Trichosporonosis diagnosis is made routinely by the recovery of fungi from blood and&#47;or biopsies&#46;<span class="elsevierStyleSup">3</span></p><p class="elsevierStylePara"> Cultures obtained from diverse clinical samples are used for identifying the etiologic agent through its microscopic morphology by confirming the presence of the 3 characteristic structures of the genus <span class="elsevierStyleItalic">Trichosporon&#58;</span> hyphae&#44; arthrocondia&#44; and blastocondia&#46; The biochemical profile may be obtained by auxanography&#44; which evaluates the ability to assimilate different sources of carbon&#46; However&#44; the complete biochemical characterization of species of the genus<span class="elsevierStyleItalic"> Trichosporon </span>is based on the assimilation of approximately 50 carbon compounds and requires anywhere between 5 and 15 days for the readings&#59; consequently&#44; it is not practical to carry out this battery of tests for the precise identification of pathogenic species&#46; There are commercial methods which systematize the application of assimilation tests and reduce the required identification time&#46; The API 20C AUX system by bioM&#233;rieux is a commercial micromethod&#44; which has turned into the most used in clinical laboratories&#46; This system evaluates the assimilation ability of 19 carbohydrates and allows identification within a timeframe of 24 to 72 hours of incubation&#46; However&#44; a limitation of this test is that it only allows the identification of 3 species of the genus&#58; <span class="elsevierStyleItalic">T&#46; asahii&#44; T&#46; inkin&#44; </span>and <span class="elsevierStyleItalic">T&#46; mucoides&#46;</span> This last characteristic prevents its generalized use&#46;</p><p class="elsevierStylePara"> Different molecular methods have been developed as fast and effective alternatives for the precise identification of many pathogens at the species level&#46; Ribosomal DNA is widely used in the systematic identification of microorganisms&#46; Molecular identification of fungi is typically performed by sequencing of the internal transcribed spacer &#40;ITS&#41; region&#46; One of the inconveniences of this region is the fact that it is highly homologous between the different species in the genus <span class="elsevierStyleItalic">Trichosporon</span>&#59; therefore&#44; the analysis of other genes or regions with higher heterology is needed in order to obtain a more accurate identification&#46; Sugita et al&#46; analyzed 84 strains corresponding to 25 species of the genus <span class="elsevierStyleItalic">Trichosporon</span> to evaluate the efficacy of sequencing the ITS region and the intergenic spacer 1 &#40;IGS1&#41; region for the precise identification at a species level&#46; They found a higher heterology between IGS1 regions in comparison to ITS&#46; This makes the IGS1 sequencing analysis superior compared to ITS for the differentiation between species of the genus&#46; In addition&#44; this method allows genotypification&#46;<span class="elsevierStyleSup">42 </span></p><p class="elsevierStylePara"> A growing number of reports reveal the effectiveness of molecular methods in the identification of this microorganism&#46; These publications show the lack of specificity of the conventional identification methods based in morphologic and biochemical criteria&#46;<span class="elsevierStyleSup">43-46</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Treatment </span></p><p class="elsevierStylePara"> Superficial infections caused by <span class="elsevierStyleItalic">Trichosporon </span>spp&#46; may be treated with galenic solutions such as 1&#37; mercuric chloride&#44; 1&#37; iodine solution&#44; and 30&#37; salicylic acid&#46; They may be treated with topical antifungals&#44; mainly imidazoles like econazole&#44; isoconazole&#44; miconazole&#44; and ketoconazole&#46; In patients with white <span class="elsevierStyleItalic">piedra</span>&#44; the trimming or shaving of parasitized hairs or affected areas prior to topical treatment is recommended&#46;<span class="elsevierStyleSup">1&#44;3&#44;17</span></p><p class="elsevierStylePara"> Management of deep infections has been a bigger challenge&#46; <span class="elsevierStyleItalic">Trichosporon </span>spp&#46; has displayed variable resistance to the most common antifungal treatments&#59; consequently&#44; there is no optimal treatment for trichosporonosis cases&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleItalic"><span class="elsevierStyleBold">In vitro</span></span><span class="elsevierStyleBold"> susceptibility </span></p><p class="elsevierStylePara"><span class="elsevierStyleItalic">Trichosporon </span>spp&#46; was first reported as an amphotericin B-resistant pathogen by Walsh et al&#46; in 1990&#44; after evaluating 2 <span class="elsevierStyleItalic">T&#46; beigelii</span> isolates obtained from patients with systemic infections&#46;<span class="elsevierStyleSup">47</span> Since its taxonomic revision&#44; several studies have assessed the efficacy of different antifungals against the species of the genus&#44; mainly <span class="elsevierStyleItalic">T&#46; asahii</span>&#46;</p><p class="elsevierStylePara"> It is important to mention that to this day there is not an established method to determine <span class="elsevierStyleItalic">in vitro</span> susceptibility of species belonging to the genus <span class="elsevierStyleItalic">Trichosporon&#46;</span> The most widely used protocol is an adaptation of the method used for <span class="elsevierStyleItalic">Candida </span>spp&#46; and <span class="elsevierStyleItalic">C&#46; neoformans</span> described in documents M27 and M44 of the Clinical and Laboratory Standards Institute&#46;</p><p class="elsevierStylePara"> One of the most evaluated antifungals has been amphotericin B &#40;AMB&#41;&#46; This is a polyenic derivate that destabilizes the fungal cytoplasmic membrane&#59; it is the treatment of choice for systemic infections&#46; The resistance of Trichosporon spp&#46; to AMB has been reported&#46; <span class="elsevierStyleItalic">T&#46; asahii</span> consistently exhibits a MIC of &#8805; 2 &#956;g&#47;mL &#40;Minimal Inhibitory Concentration&#44; which prevents visible growth of 90&#37; of isolates&#41;&#46;<span class="elsevierStyleSup">22&#44;44&#44;48&#44;49</span> There are similar MICs for other clinical isolates including <span class="elsevierStyleItalic">T&#46; asteroides</span>&#44; <span class="elsevierStyleItalic">T&#46; cutaneum&#44; </span>and <span class="elsevierStyleItalic">T&#46; ovoides&#46;</span><span class="elsevierStyleSup">22 </span>Rodr&#237;guez-Tudela et al&#46; &#40;2005&#41;&#44; contrary to the previous study&#44; reported low MICs for <span class="elsevierStyleItalic">T&#46; cutaneum </span>&#40;0&#46;25-0&#46;5 &#956;g&#47;ml&#41; and <span class="elsevierStyleItalic">T&#46; ovoides </span>&#40;0&#46;37 &#956;g&#47;ml&#41;&#46; <span class="elsevierStyleItalic">T&#46; mucoides showed</span> great variability regarding susceptibility to AMB&#44; with MICs ranging between 0&#46;015 and 16&#46;0 &#956;g&#47;ml&#46;<span class="elsevierStyleSup">44</span><span class="elsevierStyleItalic">T&#46; inkin</span> is the species which has displayed greater <span class="elsevierStyleItalic">in vitro </span>susceptibility to the inhibitory activity of AMB&#44; with MICs from 0&#46;14 to 1&#46;0 &#956;g&#47;ml&#46;<span class="elsevierStyleSup">44&#44;48</span></p><p class="elsevierStylePara"> Triazolic compounds are inhibitors of the ergosterol synthesis&#44; the main component of the fungal cytoplasmic membrane&#46; In addition&#44; they interact with enzymes at a mitochondrial level causing the accumulation of free radicals inside the cell and provoking the inhibition of fungal growth&#46; Triazolics include fluconazole &#40;FLC&#41;&#44; voriconazole &#40;VRC&#41;&#44; itraconazole &#40;ITR&#41;&#44; and posaconazole &#40;POS&#41;&#46; These agents have displayed better <span class="elsevierStyleItalic">in vitro </span>activity against <span class="elsevierStyleItalic">Trichosporon </span>spp&#46;<span class="elsevierStyleItalic">&#44;</span> with relatively low MICs for <span class="elsevierStyleItalic">T&#46; asahii </span>&#40;FLC 1&#46;27 to &#8804; 10&#46;3 &#956;g&#47;ml&#44; ITR &#8804; 1&#46;4 &#956;g&#47;ml&#44; POS 0&#46;25 &#956;g&#47;ml&#41;&#44; <span class="elsevierStyleItalic">T&#46; asteroides </span>&#40;FLC 0&#46;8 &#956;g&#47;ml&#44; ITR 0&#46;06 &#956;g&#47;ml&#41;&#44; <span class="elsevierStyleItalic">T&#46; inkin </span>&#40;FLC &#8804; 4 &#956;g&#47;ml&#44; ITR &#8804; 1 &#956;g&#47;ml&#41;&#44; <span class="elsevierStyleItalic">T&#46; cutaneum </span>&#40;FLC &#8804; 32 &#956;g&#47;ml&#44; ITR &#8804; 1 &#956;g&#47; ml&#41;&#44; and <span class="elsevierStyleItalic">T&#46; ovoides </span>&#40;FLC 1&#46;74 &#956;g&#47;ml&#44; ITR 0&#46;1 &#956;g&#47;ml&#41;&#46;<span class="elsevierStyleSup">22&#44;44&#44;48&#44;49</span></p><p class="elsevierStylePara"> Voriconazole is particularly effective for fungal inhibition <span class="elsevierStyleItalic">in vitro&#44;</span> with MICs of &#8804; 0&#46;28 &#956;g&#47;ml for the 6 more frequently isolated <span class="elsevierStyleItalic">Trichosporon</span> species causing human pathology&#46;44&#44;49</p><p class="elsevierStylePara"> Terbinafine &#40;TER&#41; is a synthetic antifungal derived from allylamines that inhibits ergosterol synthesis&#46; TER requires high concentrations in order to inhibit <span class="elsevierStyleItalic">T&#46; asahii </span>&#40;12&#46;6 &#956;g&#47; ml&#41;&#44; as opposed to the inhibition of <span class="elsevierStyleItalic">T&#46; cutaneum</span> o <span class="elsevierStyleItalic">T&#46; inkin </span>&#40;1 &#956;g&#47;ml&#41;&#46;<span class="elsevierStyleSup">48</span></p><p class="elsevierStylePara"> 5-Flucytosine &#40;5-FC&#41; is an inhibitor of the synthesis of nucleic acids&#59; it interacts with the fungal RNA disrupting the synthesis of proteins&#46; 5-FC has shown poor antifungal activity against the most clinically relevant species&#44; with MICs &#8805; 2 &#956;g&#47;ml and reaching concentrations of up to 128 &#956;g&#47;ml for <span class="elsevierStyleItalic">T&#46; mucoides&#46;</span><span class="elsevierStyleSup">9&#44;22&#44;44&#44;49</span></p><p class="elsevierStylePara"> Caspofungin &#40;CAS&#41; is an echinocandin that inhibits the synthesis of the fungal cell wall&#46; CAS MICs are high for <span class="elsevierStyleItalic">T&#46; asahii </span>&#40;&#8805; 4 &#956;g&#47;ml&#41; and <span class="elsevierStyleItalic">T&#46; asteroides </span>&#40;16 &#956;g&#47;ml&#41;&#46;<span class="elsevierStyleSup">49&#44;50 </span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Immunotherapy </span></p><p class="elsevierStylePara"> Since neutropenia is the main condition associated with the development of trichosporonosis&#44; the use of cytokines has been considered for the treatment of these infections&#46; Some of the factors used are the granulocytes colony stimulating factors &#40;G-CSF&#41;&#44; which increase polymorphonuclear cell count&#44; and the granulocytes-macrophages colony stimulating factors &#40;GM-CSF&#41;&#44; which activate monocytes and macrophages functions&#46; Muranka et al&#46; &#40;1997&#41; used a murine model with disseminated <span class="elsevierStyleItalic">T&#46; asahii </span>trichosporonosis for the evaluation of G-CSF and GM-CSF as therapy against systemic infection&#46; They observed that the use of G-CSF prior to fungal infection increased the survival in mice from 25&#37; to 100&#37;&#44; decreasing the fungal load and tissue damage in affected organs&#44; with the most notable improvement in the lungs&#46; The increase in neutrophils by GM-CSF was lower than the one caused by G-CSF&#44; so the use of GM-CSF therapy did not generate any major improvements in animals&#46; In the same study&#44; they observed an increase of tumor necrosis factor alpha &#40;TNF-&#945;&#41; in bronchoalveolar lavage fluid in mice infected with lethal doses of <span class="elsevierStyleItalic">T&#46; asahii</span> and treated with GMCSF compared to non-immunosuppressed animals or animals treated with G-CSF&#46; In addition&#44; a negative correlation between TNF-&#945; production and the presence of leukocytes in peripheral blood was observed&#44; decreasing as mice recuperated from the neutropenia&#46; Anti-TNF-&#945; therapy did not favor infection resolution&#46; The investigators concluded that neutrophil count was the most critical factor in the development of trichosporonosis&#59; however&#44; other factors&#44; such as TNF-&#945; in lung&#44; played an important role in the resolution of the infection&#46;<span class="elsevierStyleSup">51</span></p><p class="elsevierStylePara"> Similarly&#44; the use of macrophages colony stimulating factor &#40;M-CSF&#41; has been evaluated as an activator of phagocytosis in a trichosporonosis murine model with <span class="elsevierStyleItalic">T&#46; asahii</span>&#46; M-CSF increased fungicidal activity in mononuclear cells&#44; with a notable increase in survival and a decrease in fungal load&#46; In addition&#44; an increase in TNF-&#945; in lungs and plasma in animals treated with M-CSF was noticeable&#46; Different from the results reported by Muranaka et al&#46;&#44; anti-TNF-&#945; treatment did increase survival in mice&#46; Results showed how M-CSF exponentially increased fungal activity by mononuclear phagocytes&#44; helped partly by the production of TNF-&#945;&#46;<span class="elsevierStyleSup">52 </span></p><p class="elsevierStylePara"> Similar results regarding the effect of G-CSF&#44; GM-CSG&#44; and M-CSF on leukocytes and their role in trichosporonosis resolution were reported by Roilides et al&#46; &#40;2002&#41;&#46;<span class="elsevierStyleSup">53 </span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Conclusion </span></p><p class="elsevierStylePara"> Vast distribution&#44; antifungal resistance&#44; and an increase in the number of patients presenting risk factors have made relevant the study of species belonging to the genus <span class="elsevierStyleItalic">Trichosporon </span>as opportunistic fungal agents relevant<span class="elsevierStyleItalic">&#46;</span> High mortality rates in patients with systemic infections as well as a lack of an optimal treatment generate the need to increase the knowledge of this particular pathogen&#44; in a way that allows us to understand its virulence mechanisms&#44; and consequently&#44; to obtain the necessary tools for the development of effective therapies against these microorganisms&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Conflicts of interest </span></p><p class="elsevierStylePara"> The authors have no conflicts of interest to declare&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Funding </span></p><p class="elsevierStylePara"> No financial support was provided&#46;</p><hr></hr><p class="elsevierStylePara"> Received&#58; September 2013&#59; <br></br> Accepted&#58; December 2013</p><p class="elsevierStylePara"> &#42; Corresponding author&#58; <br></br> Department of Microbiology&#44; <br></br> Faculty of Medicine&#44; <span class="elsevierStyleItalic"><br></br> Universidad Aut&#243;noma de Nuevo Le&#243;n</span>&#44; Monterrey&#44; N&#46; L&#46;&#44; Mexico&#46; <span class="elsevierStyleItalic"><br></br> E-mail address</span>&#58; <a href="mailto&#58;alexandra&#46;montoya&#64;aol&#46;com" class="elsevierStyleCrossRefs">alexandra&#46;montoya&#64;aol&#46;com</a> &#40;A&#46; M&#46; Montoya&#41;&#46;</p>"
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        "resumen" => "<p class="elsevierStylePara"> <span class="elsevierStyleItalic">Trichosporon </span>spp<span class="elsevierStyleItalic">&#46; </span>has gained importance as the cases of immunosuppressed patients increase&#46; The genus <span class="elsevierStyleItalic">Trichosporon </span>includes 6 species of clinical relevance that may cause superficial infections&#44; such as white <span class="elsevierStyleItalic">piedra</span> and onychomycosis&#44; or deep and invasive infections with high mortality rates&#46; These microorganisms have a broad geographical distribution and some species are resistant to antifungal drugs <span class="elsevierStyleItalic">in vitro</span>&#46; The present paper is a review on the virulence factors&#44; associated infections&#44; and <span class="elsevierStyleItalic">in vitro </span>susceptibility of the species with the highest incidence as pathogenic agents in humans&#46;</p>"
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Article information

ISSN: 16655796
Original language: English

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Year/Month	Html	Pdf	Total

2024 November	102	5	107
2024 October	826	34	860
2024 September	867	49	916
2024 August	761	31	792
2024 July	780	24	804
2024 June	541	23	564
2024 May	606	29	635
2024 April	831	24	855
2024 March	695	42	737
2024 February	824	33	857
2024 January	1024	24	1048
2023 December	585	61	646
2023 November	666	42	708
2023 October	904	62	966
2023 September	813	40	853
2023 August	430	27	457
2023 July	432	38	470
2023 June	525	57	582
2023 May	615	19	634
2023 April	565	28	593
2023 March	501	28	529
2023 February	357	24	381
2023 January	289	18	307
2022 December	230	25	255
2022 November	454	20	474
2022 October	392	56	448
2022 September	358	32	390
2022 August	337	24	361
2022 July	223	42	265
2022 June	239	28	267
2022 May	303	42	345
2022 April	652	49	701
2022 March	328	42	370
2022 February	247	32	279
2022 January	298	50	348
2021 December	268	48	316
2021 November	335	51	386
2021 October	353	49	402
2021 September	373	40	413
2021 August	419	29	448
2021 July	222	40	262
2021 June	317	27	344
2021 May	222	30	252
2021 April	376	50	426
2021 March	311	27	338
2021 February	223	26	249
2021 January	104	16	120
2020 December	148	21	169
2020 November	225	25	250
2020 October	109	19	128
2020 September	110	36	146
2020 August	149	21	170
2020 July	145	26	171
2020 June	198	23	221
2020 May	166	19	185
2020 April	481	36	517
2020 March	272	20	292
2020 February	197	17	214
2020 January	193	20	213
2019 December	188	41	229
2019 November	166	25	191
2019 October	168	30	198
2019 September	131	18	149
2019 August	96	25	121
2019 July	91	14	105
2019 June	143	27	170
2019 May	256	48	304
2019 April	199	26	225
2019 March	58	12	70
2019 February	85	16	101
2019 January	64	10	74
2018 December	58	8	66
2018 November	72	8	80
2018 October	115	11	126
2018 September	61	19	80
2018 August	62	0	62
2018 July	53	2	55
2018 June	37	4	41
2018 May	50	8	58
2018 April	47	1	48
2018 March	46	1	47
2018 February	28	0	28
2018 January	28	0	28
2017 December	25	0	25
2017 November	12	0	12
2017 October	20	7	27
2017 September	23	3	26
2017 August	18	1	19
2017 July	23	0	23
2017 June	25	0	25
2017 May	22	5	27
2017 April	20	1	21
2017 March	20	24	44
2017 February	35	0	35
2017 January	15	1	16
2016 December	32	1	33
2016 November	37	2	39
2016 October	26	4	30
2016 September	9	1	10
2016 August	12	2	14
2016 July	21	3	24
2016 June	79	14	93
2016 May	56	22	78
2016 April	100	20	120
2016 March	60	16	76
2016 February	45	15	60
2016 January	48	16	64
2015 December	50	14	64
2015 November	57	12	69
2015 October	73	5	78
2015 September	46	11	57
2015 August	45	4	49
2015 July	34	2	36
2015 June	28	3	31
2015 May	40	11	51
2015 April	26	7	33
2015 March	28	7	35
2015 February	13	2	15
2015 January	19	2	21
2014 December	27	12	39
2014 November	21	6	27
2014 October	21	10	31
2014 September	26	8	34
2014 August	34	13	47
2014 July	39	12	51
2014 June	25	8	33

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