Abstract
Urinary tract infections (UTIs) caused by Trichosporon are a significant concern for hospitalized patients and those with weakened immune systems. This narrative review study aims to provide a comprehensive overview of UTIs caused by Trichosporon, including its frequency, risk factors, laboratory diagnostic aspects, drug resistance, and the importance of accurate identification in clinical settings. A search of international databases was conducted to identify relevant studies, and it was found that Trichosporon asahii, specifically the G1 type, is the predominant causative agent of UTIs among various Trichosporon species. Prolonged hospitalization and immunosuppressive drug use were identified as significant risk factors for this fungal infection. Conventional methods for laboratory identification are commonly used. Still, rapid and accurate tools such as Matrix-Assisted Laser Desorption-Ionisation-Time of Flight Mass Spectrometry (MALDI-TOF MS) and DNA sequencing can improve the diagnostic process. Against all T. asahii isolates for which this triazole, polyene, and echinocandin were tested, voriconazole demonstrated the most potent in vitro activity, while amphotericin B had high MIC values and echinocandins had inherent resistance. This review provides valuable insights into the clinical significance and management of UTIs caused by Trichosporon.
Key Words: Microbial sensitivity test, Cutaneotrichosporon, Trichosporon, Urinary Tract Infections
Introduction
A urinary tract infection (UTI) is an umbrella term used to describe infections affecting any part of the urinary tract. This includes infections of the bladder, urethra, kidneys, and other associated structures (1). There are an estimated 130 to 175 million cases of UTIs that occur globally (2). In hospital-acquired infections, the occurrence of UTIs was evaluated and found to be 12.9% in the United States, 19.6% in Europe, and 24% in developing nations (3). Urologists must not underestimate the importance of urinary tract infections (UTIs), considering their significant increase in occurrence in recent decades. The elevated frequency of UTIs, as well as the associated morbidity and mortality, signifies a critical challenge, particularly in developing countries (4). The occurrence of UTIs is strongly influenced by age and gender (5). During the year 2019, the age-standardized mortality rate (ASMR) attributable to UTIs stood at 3.13 per 100,000 individuals (6). UTIs are known to negatively affect patients' quality of life and impose a substantial clinical and economic burden. UTIs caused by bacteria and yeasts are a prevalent form of infection that is observed globally (7). UTIs caused by yeasts are predominantly instigated by Candida species, followed by Trichosporon species and other fungi may also be responsible for such infections (8–10). Trichosporon species are causative agents of surface infections such as white piedra, affecting hair at diverse anatomical sites (11–13). These species have also been gaining recognition as opportunistic pathogens that can result in invasive diseases (Trichosporonosis), particularly in patients with weakened immune systems (14,15). The outlook for patients suffering from invasive trichosporonosis is a matter of great concern, as various studies have reported crude mortality rates ranging from 42% to 87% (16,17). In a recent taxonomic review, 20 distinct species were identified within the genus through analysis of IGS1 rDNA sequences (18). Within the group of 20 distinct species, Trichosporon asahii, T. asteroides, T. inkin, T. ovoides, and T. faecale have been reported to cause infections in humans. The primary culprit responsible for invasive trichosporonosis, an emerging infectious disease and UTIs is T. asahii (19–21). Based on the revised taxonomic scheme introduced in 2015, T. cutaneum, T. dermatis, T. jirovecii, and T. mucoides have undergone reclassification and are now classified under the genus Cutaneotrichosporon. Cutaneotrichosporon species are frequently encountered in both human and animal sources, including clinical specimens, and certain strains have been linked to opportunistic infections (18). UTIs caused by T. asahii are atypical invasive infections and have been infrequently reported in medical literature. These infections are typically observed in hospitalized patients (21). In a study conducted by Sabharwal in 2010, it was observed that T. asahii was the predominant fungus in patients with UTIs who also had diabetes (22). The prevalence of medically significant species like Trichosporon spp. that are infrequently encountered has risen in recent years due to various reasons. These include the higher incidence of degenerative and cancerous diseases, greater exposure of patients to immunosuppressive drugs, chemotherapy, and broad-spectrum antibiotics, and increased use of invasive medical procedures like urinary or intravenous catheters, endoscopic forceps, and arteriovenous grafts (14,16,17,23–26). A considerable number of cases of breakthrough trichosporonosis have been frequently observed in immunocompromised patients, particularly following the use of ineffective antifungal therapies such as amphotericin B, echinocandins, and, less commonly, triazoles (16). Trichosporon is a newly emerging infection that has been increasingly observed in invasive forms, which is alarming. This fungus exhibits inherent resistance to conventional antifungal treatments, rendering it even more severe. Appropriate and timely diagnosis and management are vital in managing this infection effectively (15). T. asahii is an emerging opportunistic infection and the predominant pathogenic fungus within its genus, causing urinary tract infections in individuals with weakened immune systems (27,28). Although these cases are rarely documented in scientific literature, more information is needed to understand the risk factors, potential complications, and susceptibility of different species to antifungal drugs.
The identification of T. asahii in urine culture specimens from hospitalized patients is a therapeutic challenge due to the absence of clearly defined and specific guidelines for clinical interpretation and treatment (16). Moreover, the testing for antifungal susceptibility lacks standardization, and there is an absence of interpretive epidemiological cut-off values for minimal inhibitory concentrations that can differentiate non-wild type Trichosporon isolates (29). Due to the lack of comprehensive research on the frequency of urinary tract infections caused by Trichosporon, a review of all Trichosporons isolated from the urine of patients around the world during the last four decades will be conducted in this study. By analyzing patient demographics, geographical location, and other contributing factors, patterns and trends can be identified, precise statistics on the prevalence of these infections can be obtained, major risk factors can be identified, and the susceptibility of various Trichosporon species to commonly used antifungal drugs can be evaluated based on global research findings.
Materials and methods
For this narrative review, a thorough electronic search was performed on international databases to collect pertinent studies published before May 16, 2023. The search was conducted on reputable platforms such as PubMed, Scopus, Google Scholar, and Web of Science. Several specific search terms, such as "urinary tract infection", "urinary tract infections", "UTI", "urine", "funguria", "Trichosporon" and "Cutaneotrichosporon" were utilized in various combinations during each database search.
Results
Study Selection
The study collected a total of 729 articles from designated databases, which were then subjected to a deduplication process. This resulted in 492 unique articles that were considered suitable for further scrutiny and analysis. The study excluded articles written in languages other than English, as well as review papers, case reports, conference proceedings, letters, books, editorials, and notes. The main objective was to focus exclusively on original research articles for the purpose of analysis. Following a thorough examination of the titles and abstracts of the 492 remaining original papers, 46 articles were chosen to advance into the primary phase of the study.
Study Characteristics
This narrative review analyzed 46 articles. These findings are summarized in Table 1 and cover a 33-year period from 1989 to 2022 (Table 1). Asia has been the site of 45.65% of the studies, while America accounts for 30.43%. Following these regions in terms of frequency of study are Europe and Africa. A majority of research studies (60.8%) were carried out in the period starting from 2010 and continuing until the present time.
Table 1.
The detailed information presented in the 46 included studies.
| Row | Year of Publication | Country | No. of Positive Yeast Cultures | Frequency% | Isolates Distribution | Diagnostic Methods | Sex | MeanAge(Years) | Risk Factors | Reference [Number] |
|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 2022 | Thailand | * | * | T. asahii (51)T. inkin (1)Trichosporon spp. (1) | MALDI-TOFDNA-Sequencing (IGS1)Conventional | NA | NA | Hospitalization (53) | (30) |
| 2 | 2021 | Turkey | 1442 | 6.9% | T. asahii (100) | MALDI-TOF MS | M (68)F (32) | 69.94 | ICU (82) | (31) |
| 3 | 2021 | Brazil | * | * | T. asahii (157) | DNA-sequencing (IGS1) | NA | NA | NA | (32) |
| 4 | 2021 | India | * | * | Trichosporon spp. (15) | VITEK MS | NA | NA | NA | (33) |
| 5 | 2020 | Iran | 7 | 14.3% | T. asahii (1) | DNA-sequencing (ITS) | M (1) | 67 | Kidney transplantation (1) | (34) |
| 6 | 2019 | India | 11 | 18.2% | Trichosporon spp. (2) | Conventional | NA | NA | Burn patients (2) | (35) |
| 7 | 2019 | Egypt | 41 | 4.9% | C. mucoides (2) | VITEK 2 | NA | NA | Cancer (2) | (36) |
| 8 | 2019 | Mexico | 51 | 15.7% | T. beigelii (8) | VITEKConventional | NA | NA | NA | (37) |
| 9 | 2019 | Iran | 135 | 3% | T. asahii (4) | DNA-sequencing (ITS) |
M (1)F (3) | 41.5 | Diabetes Mellitus (3)Renal Failure (1) Hospitalization (3) |
(38) |
| 10 | 2018 | Mexico | * | * | T. asahii (33) | API 20CDNA-Sequencing (IGS1)Conventional | NA | NA | NA | (39) |
| 11 | 2018 | Taiwan | 508 | 0.6% | T. asahii (3) | NA | NA | NA | NA | (40) |
| 12 | 2018 | Turkey | * | * | T. asahii (68) | MALDI-TOF MSVITEK MSDNA-sequencing (IGS1) Conventional |
M (43)F (25) | 65 | Hospitalization (68)ICU (63%)Urology ward (14%)Nephrology ward (12%) Oncology ward (5%) Hematology clinic (4%) Neurology ward (2%)Chronic disease (68)Urinary Catheter (51) |
(41) |
| 13 | 2018 | Spain | 155 | 0.6% | T. asahii (1) | MALDI-TOFAPI 32CConventional | NA | Over 80 Years Old | Hospitalization (1) Above 80 years (1) | (42) |
| 14 | 2017 | Korea | 14 | 14.3% | T. asahii (2) | VITEK 2 Conventional | NA | NA | NA | (43) |
| 15 | 2017 | Taiwan | 19 | 5.3% | Trichosporon spp. (1) | Conventional | NA | NA | Hospitalization (1)Urinary Catheter (1) | (44) |
| 16 | 2016 | Brazil | * | * | T. asahii (9) | DNA-sequencing (IGS1) | NA | NA | NA | (45) |
| 17 | 2015 | Brazil | 54 | 3.7% | Trichosporon spp. (2) | VITEK 2Conventional | NA | NA | NA | (46) |
| 18 | 2015 | Egypt | 23 | 8.7% | T. beigelii (2) | Conventional | NA | 25-85years old | Urinary Catheter (2)Bladder cancer (2) | (47) |
| 19 | 2014 | India | 123 | 3.3% | Trichosporon spp. (4) | Conventional | NA | NA | NA | (48) |
| 20 | 2014 | Brazil | * | * | T. asahii (20) | DNA-sequencing (IGS1) | NA | NA | NA | (49) |
| 21 | 2014 | Korea | 159 | 5.0% | Trichosporon spp. (8) | Conventional | NA | Over 18 Years Old | Urinary Catheter (8) | (50) |
| 22 | 2014 | Argentina | * | * |
T. asahii (9) Trichosporon spp. (1) |
DNA-sequencing (IGS1, ITS, D1/D2) | NA | NA | Hospitalization (10) | (51) |
| 23 | 2014 | Spain | * | * | T. asahii (32) | VITEK 2 DNA-sequencing (IGS, ITS) | M (26)F (6) | 85 | Urine drainage bag (32)Hospitalization (32) Antibiotic therapy (32) Pneumonia (12) Sepsis (8) Kidney diseases (6) Cancer (1) ICU (1) |
(52) |
| 24 | 2014 | India | 337 | 2.1% | Trichosporon spp. (7) | VITEK 2 | NA | NA | Chronic liver disease (7)Urinary Catheter (7) | (53) |
| 25 | 2012 | China | * | * | T. asahii (23) | VITEK 2DNA-sequencing (IGS1, ITS) | M (17)F (6) | 80 | ICU (23)Systemic antibiotics (14) Urinary Catheter (14) Diabetes mellitus (8)High blood pressure (7) Heart failure (5)Chronic Diseases (2) | (54) |
| 26 | 2012 | Taiwan | * | * |
T. asahii (8) T. montevideense (2)C. dermatis (1)C. cutaneum (1)T. japonicum (1) |
DNA-sequencing (ITS, D1/D2)API 32C VITEK | NA | NA | NA | (55) |
| 27 | 2011 | Korea | 93 | 1.1% | T. asahii (1) | VITEK 2 | NA | NA | Burn patients (1) Urinary Catheter (1) | (56) |
| 28 | 2011 | Brazil | 27 | 3.7% | T. beigelii (1) | VITEK 2 | NA | NA | Urinary Catheter (1)Hospitalization (1) | (57) |
| 29 | 2010 | Turkey | * | * | T. asahii (23) | API 20CRep-PCR | M (10)F (5) | 44 | Hospitalization (15) Urinary Catheter (15) | (58) |
| 30 | 2009 | Poland | * | * | T. asahii (22) | ATB Expression | NA | NA | Kidney transplantation (21) Simultaneous pancreas Kidney transplantation (1) |
(59) |
| 31 | 2009 | Taiwan | * | * | T. asahii (9)C. dermatis (1)T. montevideense (1) | DNA-sequencing (IGS1)API 32CConventional | NA | NA | Hospitalization (11) | (25) |
| 32 | 2009 | Qatar | * | * |
T. asahii (6) T. faecale (1) |
DNA-sequence (LSU, ITS) VITEK 2API 32CConventional | M (5)F (2) | 47.1 | Pyuria (7)Hematuria (1) | (60) |
| 33 | 2009 | Poland | 12 | 8.3% | Trichosporon spp. (1) | API 32C Conventional |
NA | NA | hematological malignancies (1) | (61) |
| 34 | 2009 | Turkey | 28 | 3.6% | Trichosporon spp. (1) | Conventional | NA | NA | ICU (1) | (62) |
| 35 | 2008 | Brazil | * | * | T. asahii (8) | API 20CConventional | NA | NA | ICU (8) | (63) |
| 36 | 2008 | Brazil | * | * | T. asahii (3) | DNA-sequencing (IGS1, ITS) | NA | NA | Hospitalization (3) | (64) |
| 37 | 2007 | India | 145 | 5.5% | T. beigelii (8) | Conventional | NA | NA | Hospitalization (8) | (65) |
| 38 | 2007 | Brazil | 100 | 3% | T. asahii (3) | Conventional | NA | 0-7years old | Hospitalization (3)Candiduria (3) | (66) |
| 39 | 2005 | Kuwait | * | * | T. asahii (19) | VITEK 2DNA-sequencing (ITS) | NA | NA | Cancer (4)Kidney failure (1)Kidney transplantation (1)Severe burns (1)Hemi-colectomy (1)Low birth weight (1) | (67) |
| 40 | 2005 | Spain and Argentina | * | * |
T. asahii (2) C. jirovecii (1) |
DNA-sequencing (IGS1, ITS)Conventional | NA | NA | Hospitalization (3) | (68) |
| 41 | 2000 | Canada | * | * | T. beigelii (11) | Conventional | M (8)F (3) | 42 | Immunosuppressive drugs (11) Kidney transplantation (11)broad-spectrum antibiotics (6) Urinary Catheter (5) |
(69) |
| 42 | 1993 | Japan | 39 | 10.2% | Trichosporon spp. (4) | Conventional | NA | NA | NA | (70) |
| 43 | 1992 | India | 9 | 11.1% | C. cutaneum (1) | Conventional | NA | NA | Acute leukemia patients (1) | (71) |
| 44 | 1992 | Saudi Arabia | 302 | 0.3% | T. beigelii (1) | API 20CConventional | NA | NA | Hospitalization (1) | (72) |
| 45 | 1989 | USA | * | * | T. beigelii (15) | VITEK | M (11)F (4) | 18-85years old | Hospitalization (15) Urinary Catheter (15) | (73) |
| 46 | 1966 | USA | 179 | 1.1% | C. cutaneum (2) | Conventional | F (2) | NA | NA | (74) |
* Trichosporon and cutaneotrichosporon were the sole microorganisms identified in the urine samples within the statistical population of these studies.
A restricted number of studies have specifically explored UTIs attributed to Trichosporon. Nevertheless, this narrative review encompasses a number of original investigations that documented the identification of Trichosporon isolates derived from urine samples.
Risk Factors
Individuals afflicted with various types of cancer, receiving chemotherapy treatment, displaying neutropenia, experiencing severe burns or cystic fibrosis, or diagnosed with advanced kidney failure, as well as those with compromised immune systems, are more susceptible to the development of severe trichosporonosis (75–77). In a 2015 study, it was discovered that UTIs caused by Trichosporon had an occurrence rate of 6% within the intensive care unit (ICU) over two years. Furthermore, these infections were found to be associated with a significant mortality rate of 20% (9). Based on the findings of the studies, hospitalization, utilization of urinary catheters, receipt of organ transplants, and administration of antibiotic therapy are identified as the prevalent risk factors for urinary trichosporonosis.
Diagnosis
Yeast-like colonies are obtained through culturing on sabouraud dextrose agar. These colonies exhibit a cream-colored appearance, which may eventually transition to a yellowish-grey hue. The colonies possess significant wrinkling, with the center appearing heaped and folded. Additionally, they tend to adhere to and cause cracking of the agar surface. The process of diagnosing the condition is complicated as it involves identifying a yeast-like organism in a clinical sample (78). The use of direct examination is not always helpful for making a conclusive diagnosis since it does not commonly exhibit arthroconidia and has histological similarities with Candida. Nevertheless, this organism can be differentiated from Candida through its thinner hyphae and pseudohyphae and its slight staining with Gomori methenamine silver (GMS) stain (79). The intergenic spacer 1 (IGS1) region of the gene is an essential factor in the precise and distinct identification of different Trichosporon species (80,81). During a research investigation analyzing 45 clinical isolates and three reference isolates of Trichosporon species, assessments that focused on both the internal transcribed spacer (ITS) region and the intergenic spacer 1 (IGS1) region successfully distinguished all 48 isolates (80). The molecular identification of Trichosporon species in clinical samples obtained from Indian patients has been accomplished using the IGS1 region (82). In a reverse line blot (RLB) hybridization and rolling circle amplification (RCA)-based assay, accurate identification of Trichosporon species was achieved utilizing species-specific probes directed towards the ITS region and the D1/D2 domain. This technique exhibited 100% specificity in identifying the species when compared to DNA sequencing results from the ITS region, D1/D2 domain of the 28S rRNA gene, and IGS1 region (81). Successful management of invasive trichosporonosis infections is contingent on the diagnostic method's sensitivity and timeliness.
Identification Method and Species Distribution
After conducting a statistical analysis of several studies, it has been observed that 170 cases out of 4013 instances of yeast urinary tract infections are linked with diverse Trichosporon species. These species have been identified to be responsible for causing such infections, thus indicating the high occurrence and significance of UTIs caused by Trichosporon-related strains. Because there is a scarcity of literature examining urinary tract infections caused by Trichosporon, no temporal boundaries were imposed during the search process. Nevertheless, certain investigations focused solely on candiduria or other microbial urinary infections, which meant that Trichosporon was only identified at the level of genus and not down to the specific species. Furthermore, some studies had limited access to precise identification tools, leading them to limit their identification of Trichosporon to the genus level. Over time, multiple methods have been utilized to identify Trichosporon at the genus or species level. In the past, identification techniques were primarily limited to morphology, microscopic and macroscopic examination, and different sugar fermentation tests. Over time, the progress in microbial identification techniques used in research and medical labs has led to the implementation of advanced methods like VITEK 2, MALDI-TOF MS, and DNA sequencing for better identification of various Trichosporon species. These techniques have greatly improved the accuracy of identification. Having analyzed and consolidated the statistical data reported in multiple studies, our findings indicate that T. asahii is the predominant type of Trichosporon detected from urine, with T. beigelii, Cutaneotrichosporon cutaneum (formerly named T. cutaneum), and C. mucoides (formerly named T. mucoides) following in descending order (Chart 1) (31,34-38,40,42-44,46-48,50,53,56,57,61,62,65,66,70 -72,74).
Fig 1.
The variability of distinct Trichosporon/Cutaneotrichosporon species obtained from urine across 25 investigations.
Genotype of T. asahii
To identify the genotype of T. asahii isolates obtained from urine, a total of nine studies were conducted. The results revealed that more than 69% of the T. asahii isolates belonged to genotype type I (G1) while genotypes G3 and G7 were found to be the subsequent most common genotypes (Chart 2) (30,32,39,41,45,51,52,54,64).
Antifungal Susceptibility Patterns:
In vitro antifungal susceptibility testing (AFST) was performed on T. asahii isolates obtained from urine during studies published before May 16, 2023. The isolates were tested for susceptibility to amphotericin B, 5-flucytosine, 6 triazole, and 3 echinocandin using the broth dilution method according to Clinical and Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines, Epsilometer Test (E-test), and the VITEK 2 system. The results are summarized in Table 2 (20,30,31,45,49,52,58,63,64).
Table 2.
The summary of all data reporting antifungal susceptibility patterns of T. asahii isolated from urine during studies published before May 16, 2023 (studies without raw data of MIC are not included).
| MethodIncubation time | No. of isolates with available data | Antifungal agent | (MIC) values (μg/mL) | ||
|---|---|---|---|---|---|
| MIC range | MIC50 | MIC90 | |||
| CLSI M2748-h | 345 | AMB | 0.062- ≥ 16 | 2 | 4 |
| 345 | FCZ | 0.25- ≥ 64 | 2 | 8 | |
| 328 | VCZ | ≤ 0.015 -2 | 0.062 | 0.125 | |
| 257 | PSZ | 0.015-2 | 0.25 | 1 | |
| 137 | ITZ | 0.015-8 | 0.25 | 0.5 | |
| 100 | ISZ | ≤ 0.008-2 | 0.12 | 0.25 | |
| 100 | MYC | >8 | >8 | >8 | |
| 8 | 5FC | 16-32 | 16 | 32 | |
| E-test48-h | 55 | AMB | 0.062- ≥ 32 | 2 | 8 |
| 55 | FCZ | 0.25-64 | 4 | 16 | |
| 55 | ITZ | 0.032-32 | 0.5 | 4 | |
| 32 | VCZ | 0.008-0.75 | 0.062 | 0.125 | |
| 32 | CAS | ≥16 | ≥16 | ≥16 | |
| 32 | 5FC | ≥32 | ≥32 | ≥32 | |
| EUCAST EDef 7.148-h | 35 | AMB | 0.5- 8 | 1 | 2 |
| 35 | FCZ | 2-32 | 8 | 8 | |
| 35 | ITZ | 0.125-1 | 0.5 | 1 | |
| 35 | VCZ | 0.125-1 | 0.25 | 1 | |
| 35 | CAS | ≥16 | ≥16 | ≥16 | |
| 35 | 5FC | 2-64 | 8 | 16 | |
| 3 | PSZ | 0.125-0.25-0.5 | * | * | |
| 3 | MYC | 16 | * | * | |
| 3 | ANF | 16 | * | * | |
| 3 | RAV | 0.125-0.5-4 | * | * | |
| VITEK 2 system | 32 | AMB | ≤0.25-2 | 0.5 | 1.0 |
| 32 | FCZ | 2.0-16.0 | 2.0 | 8.0 | |
| 32 | VCZ | ≤0.12-1.0 | 0.1 | 0.3 | |
| 32 | CAS | ≥4.0 | ≥4.0 | ≥4.0 | |
| 32 | 5FC | ≤1.0-8.0 | 4.0 | 8.0 | |
MIC: Minimum Inhibitory Concentration, AMB: Amphotericin B, FCZ: Fluconazole, VCZ: Voriconazole, PSZ: Posaconazole, ITZ: Itraconazole, ISZ: Isavuconazole, MYC: Micafungin, 5FC: 5-Fluorocytosine CAS: Caspofungin, ANF: Anidulafungin, RAV: Ravuconazole
Fig 2.
The diversity of distinct T. asahii genotypes across a given population.
Typically, Trichosporon infections are treated with triazole antifungal agents and amphotericin B (16). Based on growth evaluation conducted at 48 hours, it was found that the majority of strains had a MIC90 value equal to or greater than 1 µg/mL for amphotericin B. Previous investigations have indicated that amphotericin B demonstrates insufficient fungicidal activity and restricted in vivo efficacy, with evidence of in vitro resistance (83). In vitro studies comparing the MIC values of various azole antifungal agents, such as voriconazole, itraconazole, posaconazole, isavuconazole, ravuconazole and fluconazole, were conducted. Results indicated that triazole antifungal agents demonstrated similar and low MIC values at 48 hours, whereas fluconazole displayed higher MIC values compared to other azole agents. Among the triazole drugs, voriconazole showed the best in vitro activity against clinical isolates of T. asahii and is considered as the first-line therapy, particularly for hematological patients. The MIC results revealed that all the strains tested had MIC values exceeding 4 mg/L for the echinocandins drug. Furthermore, Trichosporon species showed innate resistance to echinocandins and were found to be unaffected by this class of drugs (17). 5-Flucytosine, a drug commonly used to treat fungal infections, is ineffective against Trichosporon. Nevertheless, certain studies indicate that administering a combination of 5-flucytosine and amphotericin B can lead to favorable outcomes in the treatment of trichosporonosis (84). The findings propose that the concomitant administration of echinocandin and amphotericin B may exhibit synergistic antifungal properties (85). Previous studies have indicated that the broth dilution method and the VITEK 2 system reveal comparable results for the susceptibility testing of amphotericin B, 5-flucytosine, fluconazole, voriconazole, and caspofungin with no discrepancies exceeding a two-dilution difference in MIC50 and MIC90 (86). The E-test is a feasible method for routine laboratory use; however, its results have been found to deviate from previous findings particularly in the case of 5-flucytosine and itraconazole, which appear to be anomalous. Lemes et al. have also reported significant inconsistencies between the E-test and CLSI methodologies regarding 5-flucytosine and itraconazole (87).
Conclusion
Trichosporon species infections, primarily arising from endogenous microbial populations, present a heightened threat to individuals with weakened immune systems or those confined to ICUs. This increased risk can be attributed to factors such as microbial translocation across the gastrointestinal mucosa and the presence of indwelling catheters.
Various factors, including patient age, length of hospital stay, pre-existing medical conditions, invasive medical procedures, immune status, and other variables, play a role in determining the occurrence and severity of invasive fungal infections (IFIs) such as Trichosporonosis.
The traditional methods used to identify fungi based on their physiological and morphological characteristics are not only time-consuming but also often inadequate. However, the introduction of molecular techniques such as polymerase chain reaction (PCR) with species-specific primers has revolutionized fungal infection diagnosis by providing a simpler, more specific, and faster approach. These molecular methods offer high sensitivity and specificity, enabling the differentiation of closely related species with precision and accuracy.
Due to a scarcity of studies concurrently investigating the drug sensitivity and genotypic frequency of Trichosporon isolates derived from urine specimens, our ability to explore the correlation between drug sensitivity and genotype was hindered. While certain studies solely examined the drug sensitivity of Trichosporon isolates acquired from urine, and other studies focused on determining the prevalence of diverse genotypes of T. asahii obtained from similar urine samples, there exists a notable dearth of research encompassing both aspects together. Consequently, we were unable to elucidate the association between drug sensitivity and genotype in this context.
Accurate identification of Trichosporon species is crucial to administer appropriate and effective treatment. This is because different species of Trichosporon exhibit varying levels of susceptibility to antifungal medications. Additionally, timely diagnosis and prompt initiation of treatment are of utmost importance for patients affected by trichosporonosis. Based on the existing data, it appears that the sensitivity of Trichosporon strains obtained from urine samples towards antifungal agents is subject to variation, which can be attributed to both the species and the type of drug utilized in the analysis. However, additional investigations are warranted to comprehensively elucidate the drug susceptibility patterns of Trichosporon strains isolated from urinary sources. Furthermore, it is worth noting that T. asahii, a specific species within the Trichosporon genus, demonstrates high resistance to the antifungal drug amphotericin B.
The isolation of various Trichosporon species from urine, specifically in immunocompromised patients and ICU admissions, necessitates comprehensive research efforts. These studies aim to achieve multiple objectives, including investigating the prevalence of Trichosporon infections in urine samples, employing molecular and sequence-based methods for identifying Trichosporon species, gathering accurate epidemiological data, and performing antifungal susceptibility testing for commonly used antifungal drugs. Such efforts can provide a clear, precise, and broader understanding of the management and treatment of this infection.
Acknowledgments
None.
Data Availability
There is no additional data separate from available in cited references.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sector.
Conflict of Interest
The authors declared no conflict of interest.
Ethics Approval:
Not applicable
References
- 1.Tan CW, Chlebicki MP. Urinary tract infections in adults. Singapore Med J. 2016;57(9):485–90. doi: 10.11622/smedj.2016153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Nitzan O, Elias M, Chazan B, Saliba W. Urinary tract infections in patients with type 2 diabetes mellitus: review of prevalence, diagnosis, and management. Diabetes Metab Syndr Obes. 2015;8:129–36. doi: 10.2147/DMSO.S51792. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Tandogdu Z, Wagenlehner FM. Global epidemiology of urinary tract infections. Curr Opin Infect Dis. 2016;29(1):73–9. doi: 10.1097/QCO.0000000000000228. [DOI] [PubMed] [Google Scholar]
- 4.Shiralizadeh S, Taghizadeh S, Asgharzadeh M, Shokouhi B, Gholizadeh P, Rahbar M, et al. Urinary tract infections: raising problem in developing countries. Rev Res Med Microbiol. 2018;29(4):159–65. [Google Scholar]
- 5.Schmiemann G, Kniehl E, Gebhardt K, Matejczyk MM, Hummers-Pradier E. The diagnosis of urinary tract infection: a systematic review. Dtsch Arztebl Int. 2010 ;107(21):361–7. doi: 10.3238/arztebl.2010.0361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Zhu C, Wang DQ, Zi H, Huang Q, Gu JM, Li LY, et al. Epidemiological trends of urinary tract infections, urolithiasis and benign prostatic hyperplasia in 203 countries and territories from 1990 to 2019. Mil Med Res. 2021;8(1):64 . doi: 10.1186/s40779-021-00359-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Öztürk R, Murt A. Epidemiology of urological infections: a global burden. World J Urol. 2020;38(11):2669–2679. doi: 10.1007/s00345-019-03071-4. [DOI] [PubMed] [Google Scholar]
- 8.Sobel JD, Vazquez JA. Fungal infections of the urinary tract. World J Urol. 1999;17(6):410–4. doi: 10.1007/s003450050167. [DOI] [PubMed] [Google Scholar]
- 9.Mattede Md, Piras C, Mattede KD, Ferrari AT, Baldotto LS, Assbu MS. Urinary tract infections due to Trichosporon spp in severely ill patients in an intensive care unit. Rev Bras Ter Intensiva. 2015;27(3):247–51. doi: 10.5935/0103-507X.20150045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Fagundes Júnior AA, Carvalho RT, Focaccia R, Fernandez JG, Araújo HB, Strabelli TM, et al. Emergência de infecção por Trichosporon asahii em pacientes portadores de insuficiência cardíaca em unidade de terapia intensiva cardiológica: relato de caso e revisão da literatura. Rev Bras Ter Intensiva. 2008;20(1):106–9. [PubMed] [Google Scholar]
- 11.Sellami A, Sellami H, Trabelsi H, Makni F, Néji S, Cheikhrouhou F, et al. Fongémie fatale à Trichosporon asahii: À propos des deux premiers cas à Sfax (Tunisie) J Mycol Med. 2010;20(2):133–5. [Google Scholar]
- 12.Servonnet A, Bourgault M, Trueba F, Sarret D, Nicand E. Infection invasive à Trichosporon asahii. Ann Biol Clin. 2010;68(3):363–6. doi: 10.1684/abc.2010.0444. [DOI] [PubMed] [Google Scholar]
- 13.Lacroix C, De Feuilhade Chauvin M. Infections dues à Trichosporon spp et à Geotrichum sp. EMC- Maladies Infectieuses. 2005;2(2):97–104. [Google Scholar]
- 14.Darier J, Simon C. Nouvelle pratique dermatologique. J Am Med Assoc. 1939;112(16):1630. [Google Scholar]
- 15.Mehta V, Nayyar C, Gulati N, Singla N, Rai S, Chandar J. A Comprehensive Review of Trichosporon spp : An Invasive and Emerging Fungus. Cureus. 2021;13(8):e17345. doi: 10.7759/cureus.17345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Colombo AL, Padovan AC, Chaves GM. Current knowledge of Trichosporon spp and Trichosporonosis. Clin Microbiol Rev. 2011;24(4):682–700. doi: 10.1128/CMR.00003-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.de Almeida Júnior JN, Hennequin C. Invasive Trichosporon Infection: a Systematic Review on a Re-emerging Fungal Pathogen. Front Microbiol. 2016;7:1629. doi: 10.3389/fmicb.2016.01629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Liu XZ, Wang QM, Göker M, Groenewald M, Kachalkin AV, Lumbsch HT, et al. Towards an integrated phylogenetic classification of the Tremellomycetes. Stud Mycol. 2015;81(1):85–147. doi: 10.1016/j.simyco.2015.12.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Guo LN, Yu SY, Hsueh PR, Al-Hatmi AMS, Meis JF, Hagen F, et al. Invasive Infections Due to Trichosporon: Species Distribution, Genotyping, and Antifungal Susceptibilities from a Multicenter Study in China. J Clin Microbiol. 2019;57(2):e01505–18. doi: 10.1128/JCM.01505-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Francisco EC, de Almeida Junior JN, de Queiroz Telles F, Aquino VR, Mendes AVA, de Andrade Barberino MGM, et al. Species distribution and antifungal susceptibility of 358 Trichosporon clinical isolates collected in 24 medical centres. Clin Microbiol Infect. 2019;25(7):909.e1–909. doi: 10.1016/j.cmi.2019.03.026. [DOI] [PubMed] [Google Scholar]
- 21.Khan ID, Sahni AK, Basu A, Haleem S. Trichosporon asahii urinary tract infection in immunocompetent patients. Med J Armed Forces India. 2015;71(4):373–6. doi: 10.1016/j.mjafi.2014.08.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Sabharwal ER. Successful management of Trichosporon asahii urinary tract infection with fluconazole in a diabetic patient. Indian J Pathol Microbiol. 2010;53(2):387–8. doi: 10.4103/0377-4929.64320. [DOI] [PubMed] [Google Scholar]
- 23.Sugita T, Ichikawa T, Matsukura M, Sueda M, Takashima M, Ikeda R, et al. Genetic diversity and biochemical characteristics of Trichosporon asahii isolated from clinical specimens, houses of patients with summer-type-hypersensitivity pneumonitis, and environmental materials. J Clin Microbiol. 2001;39(7):2405–11. doi: 10.1128/JCM.39.7.2405-2411.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Kontoyiannis DP, Torres HA, Chagua M, Hachem R, Tarrand JJ, Bodey GP, et al. Trichosporonosis in a tertiary care cancer center: risk factors, changing spectrum and determinants of outcome. Scand J Infect Dis. 2004;36(8):564–9. doi: 10.1080/00365540410017563. [DOI] [PubMed] [Google Scholar]
- 25.Ruan SY, Chien JY, Hsueh PR. Invasive trichosporonosis caused by Trichosporon asahii and other unusual Trichosporon species at a medical center in Taiwan. Clin Infect Dis. 2009;49(1):e11–7. doi: 10.1086/599614. [DOI] [PubMed] [Google Scholar]
- 26.Silva V, Zepeda G, Alvarado D. Infección urinaria nosocomial por Trichosporon asahii Primeros dos casos en Chile. Rev Iberoam Micol. 2003;20(1):21–3. [PubMed] [Google Scholar]
- 27.Cronyn V, Howard J, Chiang L, Le L, Tims-Cook Z, Gertz AM. Trichosporon asahii Urinary Tract Infection in a Patient with Severe COVID-19. Case Rep Infect Dis. 2021;2021(1):6841393. doi: 10.1155/2021/6841393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Li H, Guo M, Wang C, Li Y, Fernandez AM, Ferraro TN, et al. Epidemiological study of Trichosporon asahii infections over the past 23 years. Epidemiol Infect. 2020;148:e169. doi: 10.1017/S0950268820001624. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Arastehfar A, de Almeida Júnior JN, Perlin DS, Ilkit M, Boekhout T, Colombo AL. Multidrug-resistant Trichosporon species: underestimated fungal pathogens posing imminent threats in clinical settings. Crit Rev Microbiol. 2021;47(6):679–98. doi: 10.1080/1040841X.2021.1921695. [DOI] [PubMed] [Google Scholar]
- 30.Wongsuk T, Boonsilp S, Pumeesat P, Homkaew A, Sangsri T, Chongtrakool P. Genotyping, antifungal susceptibility testing and biofilm formation of Trichosporon sp isolated from urine samples in a University Hospital in Bangkok, Thailand. Acta Microbiol Immunol Hung. 2022;69(3):247–257. doi: 10.1556/030.2022.01797. [DOI] [PubMed] [Google Scholar]
- 31.Turan D, Barış A, Özakkaş F, Dinçer ŞD, Aksaray S. Investigation of Antifungal Susceptibility of Trichosporon Asahii Isolated From Urine Samples. Med J Bakirkoy. 2021;17(2):130–4. [Google Scholar]
- 32.Francisco EC, de Almeida Junior JN, Queiroz-Telles F, Aquino VR, Mendes AVA, de Oliveira Silva M, et al. Correlation of Trichosporon asahii Genotypes with Anatomical Sites and Antifungal Susceptibility Profiles: Data Analyses from 284 Isolates Collected in the Last 22 Years across 24 Medical Centers. Antimicrob Agents Chemother. 2021;65(3):e01104–20. doi: 10.1128/AAC.01104-20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Mehta V, Chander J, Gulati N, Singla N, Vasdeva H, Sardana R, et al. Epidemiological profile and antifungal susceptibility pattern of Trichosporon species in a tertiary care hospital in Chandigarh, India. Curr Med Mycol. 2021;7(1):19–24. doi: 10.18502/cmm.7.1.6179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Zarei F, Hashemi SJ, Salehi M, Mahmoudi S, Zibafar E, Ahmadinejad Z, et al. Molecular characterization of fungi causing colonization and infection in organ transplant recipients: A one-year prospective study. Curr Med Mycol. 2020;6(1):30–35. doi: 10.18502/cmm.6.1.2505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.R E, Princess I, Vadala R, Kumar S, Ramakrishnan N, Krishnan G. Microbiological Profile of Infections in a Tertiary Care Burns Unit. Indian J Crit Care Med. 2019;23(9):405–410. doi: 10.5005/jp-journals-10071-23234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.El-Mashad NB, Aal AM, Elewa AM, Elshaer MY. Nosocomial yeast infections among cancer patients in Egypt: species distribution and antifungal susceptibility profile. Jundishapur J Microbiol. 2019;12(2):82421. [Google Scholar]
- 37.Sierra-Díaz E, Hernández-Ríos CJ, Bravo-Cuellar A. Antibiotic resistance: Microbiological profile of urinary tract infections in Mexico. Cir Cir. 2019;87(2):176–182. doi: 10.24875/CIRU.18000494. [DOI] [PubMed] [Google Scholar]
- 38.Taei M, Chadeganipour M, Mohammadi R. An alarming rise of non-albicans Candida species and uncommon yeasts in the clinical samples; a combination of various molecular techniques for identification of etiologic agents. BMC Res Notes. 2019;12(1):779 . doi: 10.1186/s13104-019-4811-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Montoya AM, Elizondo-Zertuche M, Treviño-Rangel RJ, Becerril-García M, González GM. Biofilm formation and antifungal susceptibility of Trichosporon asahii isolates from Mexican patients. Rev Iberoam Micol. 2018;35(1):22–26. doi: 10.1016/j.riam.2017.02.008. [DOI] [PubMed] [Google Scholar]
- 40.Yang YL, Chu WL, Lin CC, Zhou ZL, Chen PN, Lo HJ. Mixed yeast infections in Taiwan. Med Mycol. 2018;56(6):770–773. doi: 10.1093/mmy/myx094. [DOI] [PubMed] [Google Scholar]
- 41.Hazirolan G, Koçak N, Karagöz A. Sequence-based identification, genotyping and virulence factors of Trichosporon asahii strains isolated from urine samples of hospitalized patients (2011-2016) J Mycol Med. 2018;28(3):452–456. doi: 10.1016/j.mycmed.2018.06.006. [DOI] [PubMed] [Google Scholar]
- 42.García-Agudo L, Rodríguez-Iglesias M, Carranza-González R. Nosocomial Candiduria in the Elderly: Microbiological Diagnosis. Mycopathologia. 2018;183(3):591–596. doi: 10.1007/s11046-017-0232-7. [DOI] [PubMed] [Google Scholar]
- 43.Kim SH, Song SA, Urm SH, Kook JK, Kim HR, Yong D, et al. Evaluation of the Cobas u 701 microscopy analyser compared with urine culture in screening for urinary tract infection. J Med Microbiol. 2017;66(8):1110–1113. doi: 10.1099/jmm.0.000553. [DOI] [PubMed] [Google Scholar]
- 44.Lai CC, Lee CM, Chiang HT, Hung CT, Chen YC, Su LH, et al. Infection Control Society of Taiwan Implementation of a national bundle care program to reduce catheter-associated urinary tract infection in high-risk units of hospitals in Taiwan. J Microbiol Immunol Infect. 2017;50(4):464–470. doi: 10.1016/j.jmii.2017.01.006. [DOI] [PubMed] [Google Scholar]
- 45.Almeida AA, Crispim Bdo A, Grisolia AB, Svidzinski TI, Ortolani LG, Oliveira KM. Genotype, antifungal susceptibility, and biofilm formation of Trichosporon asahii isolated from the urine of hospitalized patients. Rev Argent Microbiol. 2016;48(1):62–6. doi: 10.1016/j.ram.2015.11.005. [DOI] [PubMed] [Google Scholar]
- 46.Magalhães YC, Bomfim MR, Melônio LC, Ribeiro PC, Cosme LM, Rhoden CR, et al. Clinical significance of the isolation of Candida species from hospitalized patients. Braz J Microbiol. 2015;46(1):117–23. doi: 10.1590/S1517-838246120120296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Farrag HA, A-Karam El-Din A, Mohamed El-Sayed ZG, Abdel-Latifissa S, Kamal MM. Microbial colonization of irradiated pathogenic yeast to catheter surfaces: Relationship between adherence, cell surface hydrophobicity, biofilm formation and antifungal susceptibility A scanning electron microscope analysis. Int J Radiat Biol. 2015;91(6):519–27. doi: 10.3109/09553002.2015.1021959. [DOI] [PubMed] [Google Scholar]
- 48.Sulaiman SP, Singh R, Mandal J. Fungal profile of funguria cases at a tertiary care hospital in southern India. Indian J Med Res. 2014;140(4):556–9. [PMC free article] [PubMed] [Google Scholar]
- 49.Iturrieta-González IA, Padovan AC, Bizerra FC, Hahn RC, Colombo AL. Multiple species of Trichosporon produce biofilms highly resistant to triazoles and amphotericin B. PLoS One. 2014;9(10):e109553. doi: 10.1371/journal.pone.0109553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Oh WS, Hur JA, Kim ES, Park KH, Choi HK, Moon C, et al. Factors associated with specific uropathogens in catheter-associated urinary tract infection: developing a clinical prediction model. J Int Med Res. 2014;42(6):1335–47. doi: 10.1177/0300060514543035. [DOI] [PubMed] [Google Scholar]
- 51.Taverna CG, Córdoba S, Murisengo OA, Vivot W, Davel G, Bosco-Borgeat ME. Molecular identification, genotyping, and antifungal susceptibility testing of clinically relevant Trichosporon species from Argentina. Med Mycol. 2014;52(4):356–66. doi: 10.1093/mmy/myt029. [DOI] [PubMed] [Google Scholar]
- 52.Treviño M, García-Riestra C, Areses P, García X, Navarro D, Suárez FJ, et al. Emerging Trichosporon asahii in elderly patients: epidemiological and molecular analysis by the DiversiLab system. Eur J Clin Microbiol Infect Dis. 2014;33(9):1497–503. doi: 10.1007/s10096-014-2099-6. [DOI] [PubMed] [Google Scholar]
- 53.Rathor N, Khillan V, Sarin SK. Nosocomial candiduria in chronic liver disease patients at a hepatobilliary center. Indian J Crit Care Med. 2014;18(4):234–7. doi: 10.4103/0972-5229.130575. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Sun W, Su J, Xu S, Yan D. Trichosporon asahii causing nosocomial urinary tract infections in intensive care unit patients: genotypes, virulence factors and antifungal susceptibility testing. J Med Microbiol. 2012;61(12):1750–7. doi: 10.1099/jmm.0.049817-0. [DOI] [PubMed] [Google Scholar]
- 55.Tsai MS, Yang YL, Wang AH, Wang LS, Lu DC, Liou CH, et al. Susceptibilities to amphotericin B, fluconazole and voriconazole of Trichosporon clinical isolates. Mycopathologia. 2012;174(2):121–30. doi: 10.1007/s11046-012-9525-z. [DOI] [PubMed] [Google Scholar]
- 56.Kim J, Kim DS, Lee YS, Choi NG. Fungal urinary tract infection in burn patients with long-term foley catheterization. Korean J Urol. 2011;52(9):626–31. doi: 10.4111/kju.2011.52.9.626. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Marra AR, Sampaio Camargo TZ, Gonçalves P, Sogayar AM, Moura DF Jr, Guastelli LR, et al. Preventing catheter-associated urinary tract infection in the zero-tolerance era. Am J Infect Control. 2011;39(10):817–22. doi: 10.1016/j.ajic.2011.01.013. [DOI] [PubMed] [Google Scholar]
- 58.Karahan ZC, Koyuncu E, Dolapci I, Akan ÖA, Can F, Tekeli A. Genotyping of Trichosporon asahii strains isolated from urinary tract infections in a Turkish university hospital. Turkish J Med Sci. 2010;40(3):485–93. [Google Scholar]
- 59.Netsvyetayeva I, Swoboda-Kopeć E, Paczek L, Fiedor P, Sikora M, Jaworska-Zaremba M, et al. Trichosporon asahii as a prospective pathogen in solid organ transplant recipients. Mycoses. 2009;52(3):263–5. doi: 10.1111/j.1439-0507.2008.01590.x. [DOI] [PubMed] [Google Scholar]
- 60.Taj-Aldeen SJ, Al-Ansari N, El Shafei S, Meis JF, Curfs-Breuker I, Theelen B, et al. Molecular identification and susceptibility of Trichosporon species isolated from clinical specimens in Qatar: isolation of Trichosporon dohaense Taj-Aldeen, Meis & Boekhout sp nov. J Clin Microbiol. 2009;47(6):1791–9. doi: 10.1128/JCM.02222-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Nawrot U, Nowicka J, Kuliczkowski K. Evaluation of Mycobiota in Patients with Hematological Malignancies in One− Day Examination. Adv Clin Exp Med. 2009;18(1):55–62. [Google Scholar]
- 62.Eryüksel E, Ergönül Ö, Olgun Ș, Odabașı Z, Korten V, Çelİkel T. Risk factors for mortality in fungal infections. Turkiye Klin J Med Sci. 2009;29(1):99–103. [Google Scholar]
- 63.de Oliveira Silva RB, Fusco-Almeida AM, Matsumoto MT, Baeza LC, Benaducci T, Mendes-Giannini MJ. Genetic diversity and antifungal susceptibility testing of Trichosporon asahii isolated of Intensive Care Units patients. Braz J Microbiol. 2008;39(3):585–92. doi: 10.1590/S1517-838220080003000033. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Araujo Ribeiro M, Alastruey-Izquierdo A, Gomez-Lopez A, Rodriguez-Tudela JL, Cuenca-Estrella M. Molecular identification and susceptibility testing of Trichosporon isolates from a Brazilian hospital. Rev Iberoam Micol. 2008;25(4):221–5. [PubMed] [Google Scholar]
- 65.Paul N, Mathai E, Abraham OC, Michael JS, Mathai D. Factors associated with candiduria and related mortality. J Infect. 2007;55(5):450–5. doi: 10.1016/j.jinf.2007.06.010. [DOI] [PubMed] [Google Scholar]
- 66.da Silva EH, Ruiz Lda S, Matsumoto FE, Auler ME, Giudice MC, Moreira D, et al. Candiduria in a public hospital of São Paulo (1999-2004): characteristics of the yeast isolates. Rev Inst Med Trop Sao Paulo. 2007;49(6):349–53. doi: 10.1590/s0036-46652007000600003. [DOI] [PubMed] [Google Scholar]
- 67.Ahmad S, Al-Mahmeed M, Khan ZU. Characterization of Trichosporon species isolated from clinical specimens in Kuwait. J Med Microbiol. 2005;54(7):639–46. doi: 10.1099/jmm.0.45972-0. [DOI] [PubMed] [Google Scholar]
- 68.Rodriguez-Tudela JL, Diaz-Guerra TM, Mellado E, Cano V, Tapia C, Perkins A, et al. Susceptibility patterns and molecular identification of Trichosporon species. Antimicrob Agents Chemother. 2005;49(10):4026–34. doi: 10.1128/AAC.49.10.4026-4034.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.Lussier N, Laverdière M, Delorme J, Weiss K, Dandavino R. Trichosporon beigelii funguria in renal transplant recipients. Clin Infect Dis. 2000;31(5):1299–301. doi: 10.1086/317463. [DOI] [PubMed] [Google Scholar]
- 70.Matsumoto T, Haraoka M, Kubo S, Takahashi K, Tanaka M, Ogata N, et al. Beta-D-glucan concentrations detected by Toxicolor and Endospecy tests in the urine of patients with urinary fungal infections. Urol Res. 1993;21(2):117–20. doi: 10.1007/BF01788829. [DOI] [PubMed] [Google Scholar]
- 71.Rajendran C, Basu TK, Baby A, Kumari S, Verghese T. Incidence and significance of opportunistic fungi in leukemia patients in India. Mycopathologia. 1992;119(2):83–7. doi: 10.1007/BF00443938. [DOI] [PubMed] [Google Scholar]
- 72.Al-Hedaithy SS. The medically important yeasts present in clinical specimens. Ann Saudi Med. 1992;12(1):57–62. doi: 10.5144/0256-4947.1992.57. [DOI] [PubMed] [Google Scholar]
- 73.Stone J, Manasse R. Pseudoepidemic of urinary tract infections due to Trichosporon beigelii. Infect Control Hosp Epidemiol. 1989;10(7):312–5. doi: 10.1086/646034. [DOI] [PubMed] [Google Scholar]
- 74.Ahearn DG, Jannach JR, Roth FJ Jr. Speciation and densities of yeasts in human urine specimens. Sabouraudia. 1966;5(2):110–9. doi: 10.1080/00362176785190201. [DOI] [PubMed] [Google Scholar]
- 75.Tamayo Lomas L, Domínguez-Gil González M, Martín Luengo AI, Eiros Bouza JM, Piqueras Pérez JM. Infección nosocomial por Trichosporon asahii en un paciente quemado crítico [Nosocomial infection due to Trichosporon asahii in a critical burned patient] Rev Iberoam Micol. 2015;32(4):257–60. doi: 10.1016/j.riam.2014.07.005. [DOI] [PubMed] [Google Scholar]
- 76.Heslop OD, Nyi Nyi MP, Abbott SP, Rainford LE, Castle DM, Coard KC. Disseminated trichosporonosis in a burn patient: meningitis and cerebral abscess due to Trichosporon asahii. J Clin Microbiol. 2011;49(12):4405–8. doi: 10.1128/JCM.05028-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Shah AV, McColley SA, Weil D, Zheng X. Trichosporon mycotoxinivorans infection in patients with cystic fibrosis. J Clin Microbiol. 2014;52(6):2242–4. doi: 10.1128/JCM.03309-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Chander J. Oxford Textbook of Medical Mycology. New Delhi: Jaypee Publishers; 2018. pp. 1– 905. [Google Scholar]
- 79.Kourti M, Roilides E. Invasive Trichosporonosis in Neonates and Pediatric Patients with Malignancies or Hematologic Disorders. Pathogens. 2022;11(2):242. doi: 10.3390/pathogens11020242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Guo LN, Xiao M, Kong F, Chen SC, Wang H, Sorrell TC, et al. Three-locus identification, genotyping, and antifungal susceptibilities of medically important Trichosporon species from China. J Clin Microbiol. 2011;49(11):3805–11. doi: 10.1128/JCM.00937-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Xiao M, Guo LN, Kong F, Wang H, Sorrell TC, Li RY, et al. Practical identification of eight medically important Trichosporon species by reverse line blot hybridization (RLB) assay and rolling circle amplification (RCA) Med Mycol. 2013;51(3):300–8. doi: 10.3109/13693786.2012.723223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82.Parashar A, Rastogi V, Prakash H, Rudramurthy SM. P441 Molecular identification, genotyping, and antifungal susceptibility of Trichosporon species isolated from clinical samples of patients at various parts of the Indian subcontinent. Med Mycol. 2022;60(Suppl 1):myac072P441. [Google Scholar]
- 83.Walsh TJ, Melcher GP, Rinaldi MG, Lecciones J, McGough DA, Kelly P, et al. Trichosporon beigelii, an emerging pathogen resistant to amphotericin B. J Clin Microbiol. 1990;28(7):1616–22. doi: 10.1128/jcm.28.7.1616-1622.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Girmenia C, Pagano L, Martino B, D'Antonio D, Fanci R, Specchia G, et al. Invasive infections caused by Trichosporon species and Geotrichum capitatum in patients with hematological malignancies: a retrospective multicenter study from Italy and review of the literature. J Clin Microbiol. 2005;43(4):1818–28. doi: 10.1128/JCM.43.4.1818-1828.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 85.Bassetti M, Bisio F, Di Biagio A, Pierri I, Balocco M, Soro O, et al. Trichosporon asahii infection treated with caspofungin combined with liposomal amphotericin B. J Antimicrob Chemother. 2004;54(2):575–7. doi: 10.1093/jac/dkh337. [DOI] [PubMed] [Google Scholar]
- 86.Cejudo MA, Gallego AG, Lacasa EC, Aller AI, Romero A, García JP, et al. Evaluation of the VITEK 2 system to test the susceptibility of Candida spp Trichosporon asahii and Cryptococcus neoformans to amphotericin B, flucytosine, fluconazole and voriconazole: a comparison with the M27-A3 reference method. Med Mycol. 2010;48(5):710–9. doi: 10.3109/13693780903473343. [DOI] [PubMed] [Google Scholar]
- 87.Lemes RM, Lyon JP, Moreira LM, de Resende MA. Antifungal susceptibility profile of Trichosporon isolates: correlation between CLSI and etest methodologies. Braz J Microbiol. 2010;41(2):310–5. doi: 10.1590/S1517-83822010000200008. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
There is no additional data separate from available in cited references.


