|Year : 2019 | Volume
| Issue : 4 | Page : 536-541
Epidemiology and Antifungal Susceptibility of Infections Caused by Trichosporon Species: An Emerging Non-Candida and Non-Cryptococcus Yeast Worldwide
Sukhwinder Singh1, Malini Rajinder Capoor1, Swati Varshney1, Dipendra Kumar Gupta2, Pradeep Kumar Verma3, V Ramesh4
1 Department of Microbiology, VMMC and Safdarjung Hospital, New Delhi, India
2 Department of ICU, VMMC and Safdarjung Hospital, New Delhi, India
3 Department of Haematology, VMMC and Safdarjung Hospital, New Delhi, India
4 Department of Dermatology, VMMC and Safdarjung Hospital, New Delhi, India
|Date of Submission||17-Apr-2019|
|Date of Acceptance||02-Jan-2020|
|Date of Web Publication||18-May-2020|
Malini Rajinder Capoor
Department of Microbiology, VMMC and Safdarjung Hospital, New Delhi - 110 029
Source of Support: None, Conflict of Interest: None
Introduction: Over the past four decades, there has been an increase in the number of fatal opportunistic invasive trichosporonosis cases especially in immunocompromised hosts. Objective: The objective of the study is to evaluate the epidemiological, clinical details and antifungal susceptibility pattern of the patients with Trichosporon infections. Materials and Methods: Twenty-four clinical isolates of Trichosporon species isolated from blood, samples, pleural fluid and nail were included in this study, over a period of 12 years (2005–2016) in a tertiary hospital in North India. The isolates were characterised phenotypically and few representative isolates were sequenced also. The minimum inhibitory concentration (MIC) was determined as per Clinical and Laboratory Standards Institute, 2012. Results: Trichosporon spp. from blood culture (57.78%), nail (37.5%) and pleural fluid (4.17%). On phenotypic tests, 79.16% of the isolates were Trichosporon asahii, followed by Trichosporon dermatis (8.33%), Trichosporon japonicum (4.17%), Trichosporon ovoides (4.17%) and Trichosporon mucoides (4.17%). The MIC range of Trichosporon species from invasive infections were fluconazole (0.06–256 μg/ml), amphotericin B (0.125–16 μg/ml), voriconazole (0.0616–8 μg/ml), posaconazole (0.0616–32 μg/ml) and caspofungin (8–32 μg/ml). The isolates from superficial infection were resistant to fluconazole (0.06–256 μg/ml) and itraconazole (0.125–32 μg/ml), all were susceptible to ketoconazole and while only two were resistant to voriconazole (0.25–4 μg/ml). Conclusion: T. asahii was the most common isolate. Disseminated trichosporonosis is being increasingly reported worldwide including India and represents a challenge for both diagnosis and species identification. Prognosis is limited, and antifungal regimens containing triazoles appear to be the best therapeutic approach. In addition, accurate identification, removal of central venous lines and voriconazole-based treatment along with control of underlying conditions were associated with favourable outcomes.
Keywords: Invasive trichosporonosis, minimum inhibitory concentration, Trichosporon asahii, Trichosporon species, voriconazole
|How to cite this article:|
Singh S, Capoor MR, Varshney S, Gupta DK, Verma PK, Ramesh V. Epidemiology and Antifungal Susceptibility of Infections Caused by Trichosporon Species: An Emerging Non-Candida and Non-Cryptococcus Yeast Worldwide. Indian J Med Microbiol 2019;37:536-41
|How to cite this URL:|
Singh S, Capoor MR, Varshney S, Gupta DK, Verma PK, Ramesh V. Epidemiology and Antifungal Susceptibility of Infections Caused by Trichosporon Species: An Emerging Non-Candida and Non-Cryptococcus Yeast Worldwide. Indian J Med Microbiol [serial online] 2019 [cited 2020 Sep 30];37:536-41. Available from: http://www.ijmm.org/text.asp?2019/37/4/536/284511
| ~ Introduction|| |
Trichosporon species belong to the genus of basidiomycetous yeast. They are widely found in nature such as soil, decomposing wood, rivers, lakes, bird droppings, pigeons, cattle and many other environmental sources. In humans, they are found to be a part of flora of gastrointestinal tract and oral cavity. They transiently colonise the respiratory tract and the skin.
With the development of molecular techniques to identify the many Trichosporon species, a new nomenclature had been proposed. Recently, Colmbo et al. described 50 species of Trichosporon, including 16 species which are of clinical importance. More than 10 Trichosporon species are able to cause infections in human and the most common species is Trichosporon asahii. The main susceptible population is patients with cancer (more in acute myeloid leukaemia), neutropenia, central venous line and chronic antibiotic use. More than 60% of infections occur as breakthrough infections. The most common clinical presentation is fungaemia (>70%), pneumonia and skin lesions which causes mortality of about 50%–70%.
Trichosporon species were initially known to cause superficial infection such as white piedra in which the distal hair had irregular nodules. They were also known to cause onychomycosis and tinea pedis. However, now, it is the second-most common cause of disseminated yeast infections in humans after Candida.
Over the past four decades, there had been an increase in the number of fatal opportunistic invasive trichosporonosis cases, especially in immunocompromised hosts. These hosts include patients with haematological malignant diseases,, peritoneal dialysis, solid tumours and occasionally those with no apparent immune impairment.Trichosporon fungaemia, including catheter-related fungaemia, is the main type of this opportunistic infection which accounts for 58.8%–74.7% of the infections. However, Trichosporon fungaemia is often neglected and often clinically misdiagnosed as other types of yeast fungaemia, especially candidemia.
Amongst the new species, T. asahii and Trichosporon mucoides are associated with severe life-threatening infections while others are associated with superficial infections.T. asahii is the most prevalent species causing disseminated trichosporonosis and has high mortality rate despite treatment.
Identification to species level is crucial for epidemiological and therapeutic purposes. The phenotypic methods for the identification of the different species of Trichosporon are inadequate and time-consuming. Therefore, sequence-based identification is more reliable but are however, only available at referral laboratories.,,,
Invasive trichosporonosis has been described in detail by the European Organization for Research and Treatment of Cancer/Invasive Fungal Infection Cooperative Group and the National Institute of Allergy and Infectious Disease Mycoses Study Group.
Globally there have only been isolated case reports, case series or review of cases of Trichosporon infections.,,,,, Reports of systemic studies on the epidemiology and antifungal susceptibility for such infections from India are scarce. This study was carried out to evaluate the epidemiological and clinical details and antifungal susceptibility of the patients with Trichosporon infections in New Delhi, India.
| ~ Materials and Methods|| |
All the Trichosporon isolates were included in the study period irrespective of the samples to get a full spectrum of Trichosporon infections. Episodes that met the criteria for proven invasive trichosporonosis were chosen for the study (2005–2016) under invasive infections.
All 24 isolated were stocked in duplicate in yeast extract peptone dextrose medium plus 20% glycerol at −80°C and all 24 were revived by subculturing on yeast extract peptone dextrose medium. These isolates were characterised phenotypically according to the colony morphology on sabouraud's dextrose agar (SDA), the microscopic morphology on cornmeal agar (CMA), sugar assimilation, urease production, growth in the presence of cycloheximide, thermotolerance at 42°C and latex agglutination with cryptococcal antigen, as described in the previous study and as per De Hoog et al. The assimilation profile tested were glucose, maltose, sucrose, lactose, galactose, trehalose, rhamnose, melibiose, raffinose, ribose, xylose, L-arabinose and inositol. Growth was positive in basic sugars and rhamnose, L-arabinose, 0.1% cycloheximide, growth at 37°C and xylose, rhamnose were variable for T. asahii. Isolates with positive growth in rhamnose, L-arabinose, melibiose, raffinose, ribose, xylose, inositol, 0.1% cycloheximide, growth at 37°C were identified as Trichosporon cutaneum. T. mucoides had mucoid growth but the assimilation profile was inconclusive.
The identification of Trichosporon species by conventional methods and antifungal susceptibility was done for patient care as soon as the sample revealed growth. These were stocked for further identification by sequencing.
The antifungal susceptibility testing was performed by micro-broth dilution technique as per the clinical and laboratory standards institute document M27-A3 and A2 which are currently standardised for Candida species and Cryptococcus neoformans. The minimum inhibitory concentrations (MICs) was determined for amphotericin B (Hi-Media, Mumbai, India), voriconazole (Sigma Aldrich, Bengaluru, India), posaconazole (Sigma Aldrich, Bengaluru, India) fluconazole (Hi-Media, Mumbai, India) and caspofungin (Sigma Aldrich, Bengaluru, India) for isolates causing invasive trichosporonosis. For the isolates causing superficial infection, MICs for ketoconazole (Hi-Media, Mumbai, India), fluconazole (Hi-Media, Mumbai, India), itraconazole (Hi-Media, Mumbai, India) and voriconazole (Sigma Aldrich, Bengaluru, India) were tested. The test was performed in a 96 well micro-titre plate using (RPMI) Roswell Park Memorial Institute Medium as the medium. The strains of Candida parapsilosis ATCC 22019 and Candida krusei ATCC 6258 were used for quality control.
'Proven invasive trichosporonosis' was defined as those cases presenting with at least one of the following criteria:
- Blood cultures/CSF, sterile site sample yielding Trichosporon species in patients with temporally related clinical signs and symptoms of infection
- Biopsy specimens that were culture positive and present histopathological evidence of fungal elements compatible with Trichosporon species.
'Probable invasive trichosporonosis' was defined as those cases presenting with all of the following criteria:
- Presence of at least one host factor (therapy with an immunosuppressive drug, neutropenia or persisting fever despite therapy with appropriate broad-spectrum antibiotics)
- One microbiological criterion (culture or presence of fungal elements compatible with Trichosporon in non-sterile site) and
- One major clinical criterion (imaging or cytobiochemical findings) consistent with infection.
Further, Trichosporon fungaemia was defined as the isolation of at least one Trichosporon species in blood culture, and in a patient with a clinical syndrome was consistent with infection.
| ~ Results|| |
During the study which ranged for over 12 years, a total of 24 Trichosporon species were isolated.
The various samples from which Trichosporon species were isolated were blood (14/24, 57.78%), nail (9/24, 37.5%) and pleural fluid (1/24, 4.17%). Proven invasive trichosporonosis was documented in 62.5% and superficial trichosporonosis in 37.5% of cases. It was observed that during the first 8 years, only four invasive Trichosporon infections (ITIs) were observed. In the past 4 years, eleven ITIs were observed.
Based on the aforementioned phenotypic tests it was observed that 19 of the 24 isolates (79.16%) were T. asahii, followed by Trichosporon dermatis (2/24, 8.33%), Trichosporon japonicum (1/24, 4.17%), Trichosporon ovoides (1/24, 4.17%) and T. mucoides (1/24, 4.17%). Only the representative isolate were sent for sequencing to confirm the identification. The following isolates were reconfirmed on sequencing also: 4 Trichosporon ashaii (IL-574 NCPF-940036, ILK-774, IL-97 NCPF-44003, IL-774), 2 T. dermatis (ILK-99), 1 T. mucoides, 1 T. japonicum (accession No AF444473), 1 T. ovoides (S4-2/9478) were confirmed by ITS sequencing at reference centre at Post Graduate Institute of Medical Education and Research, Chandigarh, India. Amongst the strains sequenced only T. asahii and T. dematis could be identified by phenotypic test with some variable sugars in the former. T. mucoides though the phenotypic tests were inconclusive of species, but mucoid growth was seen.
Invasive trichosporonosis was most commonly caused by T. asahii (14/15, 93.3%) followed by T. mucoides (6.7%). Moreover, superficial trichosporonosis was caused by mostly by T. asahii (6/9, 66.7%) followed by T. dermatis (2/9, 22.2%) and T. ovoides (1/9, 11.1%).
The risk factors for invasive trichosporonosis were febrile neutropenia (86.7%), antibiotic use (86.7%), prophylactic/empirical antifungal therapy (53.3%), central venous catheter (53.3%), chemotherapy (60%), prolonged intensive care unit (ICU) stay (6.6%), renal agenesis (6.6%). Out of 15 patients of invasive trichosporonosis mortality was observed in two patients (renal agenesis, acute myeloid leukaemia with febrile neutropenia). It was observed that in the patients who survived invasive trichosporonosis removal of catheter lines, voriconazole therapy and control of underlying disease was done.
The MIC range of Trichosporon species from invasive infections were fluconazole (0.06–256 μg/ml), amphotericin B (0.125–16 μg/ml), voriconazole (0.0616–4 μg/ml), posaconazole (0.0616–32 μg/ml), caspofungin (8–32 μg/ml). Amongst the invasive trichosporonosis, it was observed that posaconazole MIC90 was 1 μg/ml and MIC50 was 0.25 μg/ml and voriconazole MIC90 was 2 μg/ml and MIC50 was 0.125 μg/ml. While in non-invasive trichosporonosis, it was further observed that voriconazole MIC90 was 4 μg/ml and MIC50 was 0.25 μg/ml. MICs of Trichosporon species against antifungals are depicted in [Table 1] and [Table 2]. Trichosporon species other than T. asahii, were observed to have had low MIC values to the azoles group of antifungals. Furthermore, all invasive isolates were observed to be resistantin vitro to all echinocandins and also most strains exhibited relatively high MIC values against amphotericin B, fluconazole and itraconazole.
|Table 1: Minimum inhibitory concentration of Trichosporon spp. isolated from cases of invasive trichosporonosis|
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|Table 2: Minimum inhibitory concentration of Trichosporon spp. isolated from cases of noninvasive trichosporonosis|
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All the Trichosporon isolates from superficial infection were resistant to fluconazole (0.06–256 μg/ml) and itraconazole (0.125–32 μg/ml), all were susceptible to ketoconazole and while only two were resistant to voriconazole (0.25–4 μg/ml).
| ~ Discussion|| |
With the increasing population of organ and marrow transplant recipients, persons with HIV infections, and other immune-compromised patients, along with increasing risk factors such as invasive surgical procedures, use of prosthetic materials and intensive chemotherapy, there is a rise of fungal opportunistic infections in the past few decades.
Trichosporonosis is the second most common disseminated yeast infection in humans after Candida. This was also observed in this study. However, its diagnosis is likely to be missed, particularly in developing countries, because of lack of awareness and lack of knowledge of the salient diagnostic features of this pathogen.
Trichosporon species are identified by their hyphae, pseudohyphae, arthroconidia and blastoconidia formation. On SDA, it grows as cream-colored cerebriform yeast. These colony features are often confused with Candida species. In addition to this, it is difficult to differentiate histologically between invasive trichosporonosis and invasive candidiasis. The presence of arthroconidia is the major microscopic feature that differentiates Trichosporon from Candida and some biochemical tests can be used to strengthen the diagnosis. Furthermore, newer stains such as periodic acid-methenamine-silver stain have been found to be the best to discriminate fungal elements of Trichosporon. Trichosporon species share antigens with Cryptococcus and Aspergillus and it has been reported that cross-reaction for the cryptococcal antigen and/or galactomannan antigen kits have been demonstrated. This property of cross-reactivity for cryptococcal antigen could be used in early diagnosis of trichosporonosis in a resource-limited setting. Thus, a false positivity with these tests is also a method of identification although, the sensitivity and specificity of this approach have not been defined.,
However, in this study majority of the strains (15) were identified by conventional methods such as cultural characteristics in SDA, resistance to cycloheximide, CMA micromorphology, urease test, sugar assimilation and a false positive cryptococcal latex agglutination test.
Furthermore, the lack of phenotypic tests to correctly identify the strains of Trichosporon can hamper in the understanding of their epidemiological and clinical importance. Therefore molecular methods are required to accurately identify these species by targeting the conserved regions (D1/D2) and the variable region (ITS and IGS1). Unfortunately, these are very costly, require expertise and are available in reference laboratories only. It was noted on comparative analysis of the nucleotide sequences that the variation is higher in IGS1 region (ranged in size from 195 bp to 704 bp; located between 26S and 5S rDNA) as compared to ITS region thus the former can identify most of the newer or recently described species of Trichosporon.
This was also observed in a recent study.
As per the observations made in this study, it is recommended that the routine isolation, identification and antifungal susceptibility testing of the Trichosporon isolates may be done by conventional methods and the representative isolates may be further sent to a referral centre for confirmation by sequencing. Though accurate identification of Trichosporon species is done by molecular methods such as sequencing cost constraints precludes its routine use. The identification of Trichosporon species to the genus level and antifungal susceptibility testing is the mainstay in diagnosis and patient management as was done in the study.
Furthermore, newer methods like luminex xMAP technology which is a novel flow cytometry technique which has a potential for the detection of medically important species of fungi, and the use of proteomics in the form of matrix-assisted laser desorption ionisation-time of flight have come up as newer methods for the identification of Trichosporon species. Nonetheless, these are available only in a few referral centers.
Since 1982, many authors have been trying to reclassify this group of organisms. A notable contribution was by Sugita et al., who in 1995 proposed a new classification including 17 species and furthermore in 2002 and 2004 proposed 25 and 36 Trichosporon species respectively. In the new classification, the previously named Trichosporon beigelii, the main pathogen that causes Trichosporon diseases, now consists of six species (T. asahii, T. cutaneum, Trichosporon inkin, Trichosporon asteroides, T. mucoides and T. ovoides). Recently T. japonicum, which was first isolated from the air in Japan, was recently reported to cause infection in humans. While the other clinically important species, Trichosporon capitatum, had been classified as Blastoschizomyces capitatus which is a different species altogether.
In this study, it was observed that T. asahii was the most common isolate which was similar to the findings in other studies and case reports., Despite T. asahii remains the most common species associated with invasive trichosporonosis, other species found causing infection were T. dermatis, T. japonicum, T. ovoides and T. mucoides.
In various other studies, it was observed that the most important risk factor for Trichosporon infections were hematological malignancies, neutropenia and immunosuppression due to cancer therapy. However, in this study, it was observed that the previous use of antimicrobials, concomitant bacteraemia, neutropenia (underlying condition), central venous catheter (yielding Trichosporon growth) were the most important risk factors observed, of which few were also observed by Liao et al. where it was reported that 84.05% and 25% of the patients with Trichosporon fungaemia had a history of antimicrobial use and bacterial bloodstream co-infection respectively. It was observed that Trichosporon spp. caused colonisation in central line catheter leading to ITIs; therefore removal of catheter may improve the outcome of the Trichosporon infection along with voriconazole therapy and control of the underlying immunosuppressive condition. There was the isolation of Trichosporon species in both central line and peripheral line sample. It was observed that in the patients who survived invasive trichosporonosis removal of catheter lines, voriconazole therapy and control of underlying disease was done.
Ruan et al. also observed that 63% of the patients with invasive trichosporonosis had received antibiotic therapy. Other risk factors seen in single patients were renal agenesis and prolonged ICU stay.,
The mortality observed in the current study was 33.3% which is less as compared to other studies which observed 42%–80% mortality. This is attributable to various risk factors in our study as compared to other studies wherein hematological malignancies were the predominant risk factors.,,
Based on the MIC of the various antifungal agents that was performed in this study, it was observed that posaconazole and voriconazole had the best antifungal susceptibility as the MIC90 was 1 and 2 μg/ml respectively, and can, therefore, be used for the invasive cases. While in the superficial cases, voriconazole had the best antifungal susceptibility with MIC90 of 4 μg/ml. Most strains exhibited relatively high MIC values against amphotericin B, fluconazole, itraconazole and these findings were similar to those in other studies. It is well documented that echinocandins are observed to be resistant in all Trichosporon isolates which is in concordance with this study in which all the isolates of Trichosporon species over 12 years were observed to be resistant to caspofungin.
Although these studies provide data on thein vitro andin vivo activities of antifungal drugs against clinically relevant species of the genus they are still too limited in number to establish guidelines for the treatment of Trichosporon infections. Therefore, despite the increasing relevance of this pathogen in contemporary medicine, the treatment of patients with Trichosporon infections still remains a challenge. There have been some studies in which despite thein vitro susceptibility of the drug, the patient did not respond to it. This resistance in such cases can be explained to be due to the formation of a biofilm by the pathogen. Furthermore, as there are no MIC interpretative criteria available for Trichosporon species, the interpretative criteria for Candida species were used as a reference for purposes of comparison as was done in this study.
| ~ Conclusion|| |
Disseminated trichosporonosis has been increasingly reported worldwide and represents a challenge for both diagnosis and species identification. Substantial number of patients are not treated and better understanding of the risk factors of invasive trichosporonosis is needed. Prognosis is limited, and antifungal regimens containing triazoles appear to be the best therapeutic approach. In addition, accurate genus identification, proper diagnosis, discouraging misuse of antibiotics, removal of central venous lines and voriconazole-based treatment along with control of underlying conditions should be considered to optimise clinical outcome. Further large scale, multicentric studies are warranted to know the geographic-specific genotypes distribution and antifungal susceptibility of Trichosporon species as these have important epidemiological and therapeutic implications.
The authors would like to thank Prof. Dr. Arunaloke Chakrabarti and Prof. Dr. MR Shivaprakash, PGIMER, Chandigarh for confirming the isolates by sequencing.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2]