Next Article in Journal
Bone Marrow Iron Stores Are Not Associated with Increased Risk for Invasive Fungal Infections in Patients with Newly Diagnosed Acute Leukemia or Myelodysplastic Syndrome in Transformation: Is There a Relationship?
Next Article in Special Issue
Aspergillus terreus Antibody Serosurveillance in Tyrol: A Population-Based, Cross-Sectional Study of a Healthy Population
Previous Article in Journal
Recent Advancements in Pathogenic Mechanisms, Applications and Strategies for Entomopathogenic Fungi in Mosquito Biocontrol
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JoF
Volume 9
Issue 7
10.3390/jof9070747
jof-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Rare Yeasts in Latin America: Uncommon Yet Meaningful

by
Óscar Gil
1,†,
Juan Camilo Hernández-Pabón
1,†,
Bryan Tabares
1,2,
Carlos Lugo-Sánchez
1 and
Carolina Firacative
3,*
1
Group MICROS Research Incubator, School of Medicine and Health Sciences, Universidad de Rosario, Bogota 111221, Colombia
2
Unidad de Extensión Hospitalaria, Hospital Universitario Mayor Méderi, Bogota 111411, Colombia
3
Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad de Rosario, Bogota 111221, Colombia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Fungi 2023, 9(7), 747; https://doi.org/10.3390/jof9070747
Submission received: 30 May 2023 / Revised: 20 June 2023 / Accepted: 28 June 2023 / Published: 14 July 2023
(This article belongs to the Special Issue Rare Fungal Infectious Agents)
Browse Figures
Review Reports Versions Notes

Abstract

:
Systemic infections caused by rare yeasts are increasing given the rise in immunocompromised or seriously ill patients. Even though globally, the clinical significance of these emerging opportunistic yeasts is increasingly being recognized, less is known about the epidemiology of rare yeasts in Latin America. This review collects, analyzes, and contributes demographic and clinical data from 495 cases of infection caused by rare yeasts in the region. Among all cases, 32 species of rare yeasts, distributed in 12 genera, have been reported in 8 Latin American countries, with Trichosporon asahii (49.5%), Rhodotorula mucilaginosa (11.1%), and Saccharomyces cerevisiae (7.8%) the most common species found. Patients were mostly male (58.3%), from neonates to 84 years of age. Statistically, surgery and antibiotic use were associated with higher rates of Trichosporon infections, while central venous catheter, leukemia, and cancer were associated with higher rates of Rhodotorula infections. From all cases, fungemia was the predominant diagnosis (50.3%). Patients were mostly treated with amphotericin B (58.7%). Crude mortality was 40.8%, with a higher risk of death from fungemia and T. asahii infections. Culture was the main diagnostic methodology. Antifungal resistance to one or more drugs was reported in various species of rare yeasts.

1. Introduction

The increasing incidence of severely ill and immunocompromised patients is leading to the rise in invasive fungal infections caused by rare yeasts, which comprise non-Candida and non-Cryptococcus species [1,2]. Even though these microorganisms are not rare per se, as they abound in the human microbiome, the environment, and food, they are called rare as they hardly ever cause disease in humans, mostly because of their low pathogenicity [3]. Patients at risk include those in supportive and intensive care, people with cancer or hematological malignancies, solid organ and stem cell transplant recipients, patients on active treatment with high-dose corticosteroids, among others [4]. Hence, the weakened immune status of the host is a crucial determinant of the severity of the disease these rare yeasts cause, which in many cases results in high mortality rates, particularly in patients with disseminated infection [4,5]. The outcome for these infections is also determined by the etiologic agent, since various species of rare yeasts, including nonpathogenic, are characterized by intrinsic or acquired resistance to one or more commonly used antifungal drugs, which reduces treatment options and worsens the prognosis [6,7].
Although rare yeast pathogens cause less than 2% of cases of fungemia and invasive infections, as reported by various surveillance studies from different geographic regions, these yeasts are typically encountered in health care-associated settings [8,9,10]. This scenario leads to longer hospital stays as well as additional therapies, which significantly increases patient morbidity and mortality. Together, this represents a great financial impact on hospital resources, outweighing the burden of the underlying diseases alone and hampering medical advancements [11,12]. Moreover, the identification of rare yeasts remains a challenge and the diagnosis depends on a high degree of suspicion. As such, many infections caused by these infrequent pathogens are still misdiagnosed or have late diagnosis, leading to inadequate treatment and, therefore, poorer outcomes [4].
Globally, the importance of rare yeasts as emerging opportunistic human pathogens is increasingly being recognized; thus, clinical guidelines for their diagnosis and management are already available [1,6]. However, less is known about the infections that are caused by species of rare yeasts in Latin America and knowledge about distinctive epidemiological traits of these pathogens in the region is scarce and insufficient. Therefore, this review aims to collect and analyze the demographic and clinical characteristics of a large set of patients affected by rare yeasts from Latin American countries. The information herein presented adds to local data that can be useful for identifying patients at the highest risk of developing severe infections caused by rare yeasts and puts together data on antifungal susceptibility testing of these species, which can guide choosing antifungal therapy that results in better outcomes. In addition, this review seeks to raise awareness of the significance of these mycoses, a growing global public health problem, and of the importance of reporting clinical cases and surveys on rare yeasts in the region to increase our understanding of these life-threatening pathogens. Regional epidemiological studies, surveys, and data collections are essential to inform local differences in the prevalence of medically important fungi, as well as to highlight diagnostic and management priorities.

2. Materials and Methods

2.1. Data Collection

A literature search comprising studies published until March 2022 was undertaken, focusing on case reports and surveys of rare yeasts causing infection in Latin American countries. Rare yeasts were defined as non-candidal and non-cryptococcal species, according to the European Confederation for Medical Mycology (ECMM), the International Society for Human and Animal Mycology (ISHAM), and the American Society for Microbiology (ASM) and include the yeasts that are most well described in clinical settings [1]. Publications in English, Spanish, and Portuguese from PubMed, SciELO, and Google databases were included. The literature search was based on the keywords “invasive”, “infection”, “case”, “report”, in combination with the names of the genera Geotrichum (Dipodascus or Galactomyces), Kodamaea (Pichia), Magnusiomyces, Malassezia (Pityrosporum), Pseudozyma (Moesziomyces or Dirkmeia), Rhodotorula (Cystobasidium), Saccharomyces, Saprochaete, Sporobolomyces, and Trichosporon, and each of the 21 countries from Latin America, namely, Argentina, Bolivia, Brazil, Chile, Colombia, Costa Rica, Cuba, Dominican Republic, Ecuador, El Salvador, Guatemala, Haiti, Honduras, Mexico, Nicaragua, Panama, Paraguay, Peru, Puerto Rico, Uruguay, and Venezuela. Additional fungal names were used in the search, where taxonomic changes had occurred or synonyms were in use [1,3].
All cases of fungemia and other invasive fungal infections, as defined by the European Organization for Research and Treatment of Cancer and the Mycoses Study Group [13], as well as cases of urinary tract infections and catheter-related infections, were included when stated. In immunocompromised patients or those with other underlying conditions, cases of oral infection, vaginal infection, and folliculitis were included, as they represent distinct cases. Superficial fungal infections of the skin, nails, hair, and mucosal surfaces were not included in this review. Epidemiological data of patients with rare yeast infections, including age, sex, risk factors, or underlying conditions, treatment, and outcome, together with data on the site of the body affected, the diagnostic methods utilized, and antifungal susceptibility testing of the yeasts were collected when available.

2.2. Statistical Analysis

Data are shown as numbers and percentages. For quantitative variables, median and range are shown. A multivariate logistic regression was performed to assess the relation between the genera of the etiological agent and the variables, (i) type of infection caused and (ii) risk factor or underlying condition of affected patients. A multivariate logistic regression was performed, in addition, to assess the relation between outcome and the explanatory variables, (i) age, (ii) sex, (iii) type of infection, and (iv) species of the etiological agent. Data were checked for multicollinearity with the Belsley–Kuh–Welsch technique. Heteroskedasticity and normality of residuals were assessed, respectively, by the White test and the Shapiro–Wilk test. Adjusted odds ratio (OR) and 95% confidence interval (CI) are presented. The association between outcome and the explanatory variables, (i) risk factor or underlying condition, (ii) type of infection, (ii) treatment, and iv) genera of the etiological agent, was tested with the Chi-squared test. The alpha risk was set to 5% (α = 0.05). Statistical analysis was performed with the online platform EasyMedStat (version 3.9; www.easymedstat.com (accessed on 18 May 2023)) and the software GraphPad Prism version 9. The population of each Latin American country, to calculate the number of cases of rare yeast infections per million residents per country, was obtained from www.worldometers.info (accessed on 2 May 2023) [1,14].

3. Results

3.1. Species of Rare Yeasts

To date, 96 publications reporting 495 cases of infections caused by rare yeasts have been published in Latin America. From the cases, dating back to 1997 [15,16,17,18], 288 (58.2%) were reported from Brazil, followed by Argentina with 110 cases (22.2%), Mexico with 63 (12.7%), Venezuela with 12 (2.4%), Chile with 11 (2.2%), Colombia with 8 (1.6%), Cuba with 2 (0.4%), and Guatemala with 1 case (0.2%). Cases of severe infections caused by rare yeasts from Bolivia, Costa Rica, Dominican Republic, Ecuador, El Salvador, Haiti, Honduras, Nicaragua, Panama, Paraguay, Peru, Puerto Rico, and Uruguay have not been reported until now (Figure 1).
From the species of rare yeasts, 396 (80%) were identified to the species level, accounting for 32 species, distributed in 12 genera: Geotrichum candidum [19,20,21], Kloeckera apiculata (Hanseniaspora uvarum) [17], Kodamaea ohmeri [22,23,24,25], Magnusiomyces capitatus (Geotrichum capitatum, Saprochaete capitata, Blastoschizomyces capitatus) [26,27,28,29,30], Malassezia furfur [18,31,32,33,34,35], Malassezia pachydermatis [36], Malassezia sympodialis [34,37,38], Millerozyma farinosa (Pichia farinosa) [39], Pichia angusta (Hansenula polymorpha) [40], Pichia anomala (Wickerhamomyces anomalus) [40,41], Pseudozyma aphidis [42,43], Rhodotorula dairenensis [44], Rhodotorula glutinis [15,34,39,45,46], Rhodotorula minuta (Cystobasidium minutum) [44,47], Rhodotorula mucilaginosa (Rhodotorula rubra) [40,44,46,48,49,50,51,52,53], Rhodotorula toruloides [44], Saccharomyces cerevisiae [18,21,54,55,56,57,58,59,60,61,62,63,64,65], Saprochaete clavata (Geotrichum clavatum) [66], Trichosporon asahii [40,49,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93], Trichosporon asteroides [76,91], Trichosporon beigelii [17,18], Trichosporon coremiiforme [71,76,94], Trichosporon cutaneum [95], Trichosporon dermatis [71,76], Trichosporon faecale [71,91], Trichosporon figueirae [18], Trichosporon inkin [16,67,71,74,79,91,96,97,98,99,100,101], Trichosporon japonicum, Trichosporon jirovecii [71], Trichosporon montevideense [79], Trichosporon mucoides [23,57,102,103], and Trichosporon ovoides [71].
In the remaining 99 cases (20%), species identification was not possible; however, the genera, Geotrichum [18,30], Malassezia [104,105,106], Rhodotorula [21,46,107,108,109], Saccharomyces [109], or Trichosporon [21,39,62,79,91,109,110], were identified.
Among the 396 cases in which the genus and species were identified, T. asahii was the most common species found, with 196 reports (49.5%), followed by R. mucilaginosa with 44 cases (11.1%), S. cerevisiae with 31 cases (7.8%), M. furfur and T. inkin with 20 cases each (5.1%), G. candidum with 14 cases (3.5%), and T. asteroides with 11 cases (2.8%). The other 25 species, accounting for 15.2% of cases, were reported with less than 10 cases each (Figure 2). From the 32 species reported in Latin America, 22 were identified in Brazil, 20 in Argentina, 6 in Mexico, 5 each in Chile and Colombia, 2 in Cuba, and 1 each in Venezuela and Guatemala. While T. asahii was reported in Argentina, Brazil, Chile, Colombia, Guatemala, and Mexico, R. mucilaginosa was reported only in Brazil, Chile, and Colombia and S. cerevisiae only in Argentina, Brazil, and Chile.

3.2. Clinical Characteristics of Patients

Documented demographic and clinical characteristics of patients with infections caused by rare yeasts in Latin America are summarized in Table 1. From the patients with data on sex, 144 (58.3%) were men and 103 (41.7%) were women. From the 179 patients with data on age, cases were described from neonates to 84-year-old patients, with an average age of 34.7 years and median 39.5 years. Neonates included 10 newborns with less than 24 h of life and 5 infants between 9 and 22 days of age.
In 312 cases, underlying conditions or risk factors were documented, with leukemia, central venous catheter (CVC), cancer, surgery, and antibiotic use the most commonly reported among patients (Table 1). While some patients presented two or more underlying conditions or risk factors, most patients (70%) had only one. In multivariate analysis, surgery (OR:12.11; CI: 2.57–57.02, p = 0.0016) and antibiotic use (OR: 168.57; CI: 5.52–5149.53; p = 0.0033) were associated with higher rates of Trichosporon infections. In addition, CVC (OR: 4.51; CI: 1.74–11.68, p = 0.0019), leukemia (OR:4.76; CI: 2.63–8.63], p < 0.0001), and cancer (OR: 5.41; CI: 2.56–11.45; p < 0.0001) were associated with higher rates of Rhodotorula infections. No other association was found between underlying conditions or risk factors and the etiological agent.
From all 495 cases, fungemia alone accounted for 249 cases (50.3%), followed by 86 cases (17.4%) of other invasive infections and 81 cases (16.4%) of urinary tract infection. The remaining 79 cases (16%) were distributed among other various infections, including abscesses, folliculitis, endophthalmitis, and oral, oropharyngeal, and vaginal infections. With respect to the etiological agent, both Trichosporon and Rhodotorula infections were more likely to be fungemia (OR: 2.28; CI: 1.57–3.31 and OR: 0.061; CI: 0.029–0.13, respectively, with p < 0.001), while cases of Geotrichum (OR: 8.63; CI: 1.96–37.94; p < 0.001) and other genera (OR: 2.09; CI: 1.09–4.01; p = 0.035) were more likely to be infections other than fungemia, invasive infection, or urinary tract infection.
Treatment was reported in 213 patients. Of those, 130 (61.3%) received monotherapy either with amphotericin B (29.2%), fluconazole (19.3%), voriconazole (11.3%), or itraconazole (1.4%). In 62 patients (29.2%), combined therapy, mainly amphotericin B plus an azole drug, was reported. Five (2.4%) patients received treatment, but this was not specified. Fifteen (7.1%) patients were reported not to have received any antifungal treatment.
The outcome for the patients was reported in 277 cases. Of those, 164 (59.2%) survived and 113 (40.8%) died. Multivariate analysis revealed that per every year of life, patients were 1.02 times more likely to die. Additionally, patients who died were 13.6 years older than those who survived (p < 0.001) (Table 2). Patients’ sex was not associated with the outcome. In Table 2, reference levels, defined automatically by the statistical program, serve as “baseline” values for a given variable, and helps comparing the data generated.
Among patients with data on the outcome, there was a statistically significant higher risk to die of fungemia than of other infections (OR: 23.59; CI: 3.1–179.78; p = 0.00229) and T. asahii infections were found more likely to cause death than infections caused by other species of rare yeasts (OR: 11.28; CI: 5.61–22.66; p < 0.0001). Univariate analysis revealed that patients with leukemia, corticosteroid use, bacteremia and mechanical ventilation were also statistically more likely to die than patients with other risk factors or underlying conditions, while patients with surgery were more likely to survive (Table 3). Generally, fungemia and invasive infection as well as infections caused by species of the genus Trichosporon were found more likely to cause death, while patients with infections caused by species of the genera Rhodotorula and Geotrichum were more likely to survive. The outcome was not associated with the treatment received.

3.3. Diagnosis

In 487 out of the 495 patients from Latin America with infections caused by rare yeasts, the method used for diagnosis was specified. Of these, cultures from diverse biological samples, including blood, respiratory tract samples, urine, abdominal/thoracic fluids, and biopsies, among others, were done in most cases (95.9%). Biochemical identification, following culture, was performed in 190 cases (39.3%), using automated systems based on carbohydrate and other compound assimilation tests (e.g., Vitek, the API 20C, and the ID 32C yeast identification systems from bioMérieux, Inc. (Marcy-l’Étoile, France)). Molecular identification was performed in 201 cases (41.4%); 90 from cultures and 111 directly from patients’ specimens. Molecular techniques included sequencing of the internal transcribed spacer (ITS) region, the D1/D2 region, and other species-specific genes, as well as genotyping of the isolates to further characterize certain species. Microscopic examination was performed in 77 cases (15.8%), 58 following culture and 19 by observing fungal elements directly in clinical samples. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) was used for species identification in 28 cases (5.8%), when the pure culture of the yeasts was available. Of these yeasts identified by MALDI-TOF MS, 17 were R. mucilaginosa, 10 were other species of Rhodotorula, and 1 was T. inkin.

3.4. Antifungal Susceptibility

The susceptibility to commonly used antifungal drugs was determined in 164 (33.1%) isolates of rare yeast from Latin America. In 79 (48.2%) of them, the antifungal susceptibility testing was based on the European Committee on Antimicrobial Susceptibility Testing-Subcommittee on Antifungal Susceptibility Testing (EUCAST-AFST) method E.Def.7.2. In 70 isolates (42.7%), the microdilution method in RPMI broth, according to the M27-A3 guideline of the Clinical and Laboratory Standards Institute (CLSI) [111], was used. Other methodologies, such as E-test strips (bioMerieux, Inc., Marcy-l’Étoile, France), disk diffusion in accordance with the CLSI protocol M44-A2, the Vitek-2 Compact system (bioMerieux, Inc., Marcy-l’Étoile France), and Fungifast®® AFG (ELITech Microbiology, Puteaux, France), were reported in the remaining 15 isolates (9.1%).
From the isolates with antifungal susceptibility data, 129 (78.7%) belonged to the genus Trichosporon, followed by 18 (11%) Saccharomyces isolates, 5 (3%) of Rhodotorula, and 12 (7.3%) of other genera. Even though minimum inhibitory concentrations (MIC) data for one or more antifungal drugs were reported for all isolates, interpretation for susceptibility or resistance could not always be established. Nevertheless, resistance to fluconazole was reported in 27 (16.5%) isolates; 10 of them were T. asahii, 3 each of S. cerevisiae and Trichosporon sp., 2 each of R. mucilaginosa and Rhodotorula sp., and 1 each of G. candidum, K. ohmeri, M. capitatus, M. sympodialis, R. glutinis, and T. inkin. Resistance to 5-fluorocytocine was reported in 25 isolates, of which, 19 were T. asahii (76%), 5 were S. cerevisiae (20%), and 1 were T. inkin (4%). Resistance to amphotericin B was reported in 17 isolates of T. asahii, 2 of Trichosporon spp., and 1 each of M. sympodialis and T. inkin. Itraconazole resistance was reported in two isolates of T. asahii and one each of R. mucilaginosa and R. glutinis, while only two isolates of T. asahii were reported as voriconazole resistant. Concomitant resistance to amphotericin B and fluconazole was reported in two isolates each of T. asahii and Trichosporon spp., and one isolate of M. sympodialis. Four isolates of T. asahii were additionally concomitantly resistant to 5-fluorocytocine and two other isolates of T. asahii were, in addition, resistant to itraconazole and voriconazole, making them pan-drug resistant. Concomitant resistance to fluconazole and itraconazole was reported in one isolate each of R. mucilaginosa and R. glutinis and concomitant resistance to amphotericin B and 5-fluorocytocine was found in seven isolates of T. asahii.

4. Discussion

In the growing population of patients receiving medical interventions and those with a weakened immune system, infections caused by rare yeasts have emerged as an important health concern, given that these infections are usually associated with significant morbidity and high mortality rates [1,6]. The first difficulty when fighting these emerging infectious pathogens is that little is known about their modes of transmission, how to best diagnose them, and how to treat them, particularly when it is unknown if they present resistance or reduced susceptibility to certain antifungal drugs. By analyzing 495 cases of rare yeast infections from 8 Latin American countries, this review is contributing to an increase in our knowledge on the demographic and clinical characteristics of patients at risk as well as on the diagnostic methodologies and antifungal susceptibility of the etiological agents.
Similar to the global epidemiology of rare yeast infections [1,2], T. asahii and R. mucilaginosa were found to be the two most common species of rare yeasts isolated from clinical specimens in Latin America. However, in this region, infections caused by Saccharomyces, Malassezia, other species of Trichosporon and Rhodotorula, and G. candidum prevail over cases by Kodamea, which is the third most common genus of rare yeast causing invasive infections in hospitalized patients worldwide. In Latin American countries, Kodamea species could be misidentified as Candida species, due to their phenotypic resemblance and because molecular diagnostic methods, which are required for proper identification, are not always available [3].
Notably, this review complements the epidemiology of non-Candida and non-Cryptococcus invasive infections in Latin America and the world by adding data on reports of rare yeast species that were not included in the latest guidelines [1]. Specifically, the isolation of M. capitatus (S. capitata) in Argentina, R. mucilaginosa in Colombia, G. candidum and R. glutinis in Mexico, and Malassezia species in Argentina, Brazil, Colombia, Mexico, and Venezuela. In addition, we include for the first time the reports on the isolation of M. farinosa, P. angusta, P. anomala, R. dairenensis, and R. toruloides from human samples in Brazil [39,40,41,44] and K. apiculata in Cuba [17]. This last species being rarely recovered from clinical samples [112,113]. Here, we also confirm that Sporobolomyces species have not been reported in Latin America.
As previously reported in global surveys [4,6], rare yeast infections in Latin America also occur similarly among male and female patients of all ages. However, considering the outcome, our review revealed that patient at an older age are less likely to survive, probably because aging is associated with declining immunity and increased vulnerability to other malignancies [114,115]. The prevalence and outcome of rare yeast infections in Latin America varied as well depending on the risk factors of patients and the etiological agent, even though there are slight differences compared to the global epidemiology of these infections. While hematologic malignancies and neutropenia are considered classical risk factors for invasive Trichosporon infection [2,116,117], in Latin America, surgery and antibiotic use prevail among patients affected by species of this genus. Conversely, CVC, leukemia, and cancer were associated with higher rates of Rhodotorula infections, which agrees with the typical risk factors for this genus [5,46]. Mortality associated with invasive infections caused by T. asahii is generally higher than that of Candida infections [117,118]. In Latin America, about 80% of patients affected by T. asahii died. In addition, a larger proportion of patients with corticosteroid use (78.9%), bacteremia (63.6%), and leukemia (61.5%) died compared to patients with other risk factors. The recognition of the underlying conditions and etiological agent is, therefore, very important, as outcomes for patients are often worse because of them [5].
Rare yeasts most commonly cause fungemia, as found in this study. Nevertheless, non-blood stream infections (BSI) caused by these pathogens accounted for almost half the cases, including catheter-related infection, urinary tract infection, pneumonia, peritonitis, meningoencephalitis, and endocarditis. As reported in the literature, Trichosporon and Rhodotorula invasive infections, particularly by T. asahii and R. mucilaginosa, are more likely to be fungemia [2,5,11,46,117], while other genera can cause diverse clinical manifestations, such as Geotrichum causing pulmonary infection or Saccharomyces causing oral infection [30,60,119,120].
Although the outcome for patients in Latin America was not associated with the treatment they received, it is important to consider the therapeutic options when fighting rare opportunistic infections. In the hospital setting, prophylactic antifungal therapy is mostly prescribed upon suspicion of candidemia, with echinocandins being the first option for Candida species [121]. In fact, the use of echinocandins is strongly recommended in patients with a high risk of serious sepsis or septic shock, due to their demonstrated efficacy and broad spectrum of action [122]. However, this family of antifungals is ineffective in the treatment of species that present natural or intrinsic resistance, including the basidiomycetes Trichosporon, Rhodotorula, and Malassezia [48,120,123] that are the most common genera of rare yeasts affecting critically ill patients. This explains why patients receiving caspofungin as empirical treatment are susceptible to breakthrough infections and why after diagnosis, amphotericin B and fluconazole are the most common antifungal therapy.
Apart from the intrinsic resistance to echinocandins of Trichosporon and Rhodotorula, some isolates of these two genera, mainly T. asahii isolates, have been reported in Latin America to be resistant to fluconazole, itraconazole, 5-fluorocytocine, and amphotericin B, separately or concomitantly. This clearly leaves physicians with an even smaller arsenal of therapeutic options against these pathogens. Moreover, while voriconazole exhibits the best in vitro activity against T. asahii clinical isolates and resistance is uncommon [97,124], our study found that in Latin American countries, this triazole is not considered as first-line therapy. Fluconazole resistance has also been identified in M. sympodialis and ascomycetes yeasts such as S. cerevisiae, G. candidum, K. ohmeri, and M. capitatus from Latin America. In Europe, S. cerevisiae and G. candidum, particularly, have been reported to be resistant to many current antifungals including echinocandins [125]. Together, these findings highlight the importance of identifying the genus and species of the etiological agents and applying antifungal susceptibility testing on all rare yeasts. In Latin America, antifungal susceptibility was determined in less than a third of the isolates. In addition, it is necessary to further investigate whether in vitro results are predictors of the clinical response to antifungal therapy.
Regarding the diagnosis of rare yeast infections, we show that in Latin American countries, culture is the preferred and most accessible approach that can be utilized to identify the etiological agents. Globally, cultures from clinical samples remain the gold standard for the diagnosis of fungal infections, allowing, moreover, for susceptibility testing [1,126]. However, a final and accurate identification by biochemical, proteomic, and molecular methods is generally limited to commercial platforms that are usually directed toward the identification of common rather than rare fungi. This is why the use of MALDI-TOF MS to identify non-Candida and non-Cryptococcus yeast species has been found to be considerably less suitable, given the absence of reference spectra for other genera [127]. In Latin America, particularly, this technique has only been used to identify Rhodotorula species. Microscopy and histopathology, utilizing fungal-specific stains, can be suggestive and aids the diagnosis, but these approaches depend on the skills and experience of laboratory personnel and cannot be used alone [6]. In Latin America, more advanced diagnostic approaches and methodologies, both culture- and non-culture-based, are still needed to meet the requirements to diagnose fungal infections caused by rare yeasts, especially considering that many countries lack sufficient resources for testing.
It is important to note as well that several species of rare yeasts are medically important in Latin America, even though cases of severe infections have not been reported in many countries. S. cerevisiae, Rhodotorula sp., and T. cutaneum were found as part of the vaginal yeast flora, some of them causing vulvovaginitis, in pregnant women living in Peru [128]. Trichosporon and Rhodotorula species have been reported as causing vaginosis in Venezuela [129]. Malassezia species have also been reported in cases of pityriasis versicolor in infants under one year of age in Dominican Republic [130] and M. globosa, M. furfur, M. sympodialis, and Malassezia slooffiae causing pityriasis versicolor in more than 100 patients from 1 month to 63 years of age in Paraguay [131]. In Puerto Rico, Malassezia and Saccharomyces were found in the fungal cervicovaginal biota in women with human papillomavirus (HPV) infection [132]. Trichosporon species causing invasive and superficial infections and Saccharomyces causing fungemia following probiotic ingestion have been associated with overall mortality in Brazil [124,133]. These reports highlight the importance of increasing awareness among physicians and laboratory personnel for better diagnosing rare yeast infections, especially in the early stages of infection, which is essential to avoid further complications.

5. Conclusions

The epidemiology of rare yeast infections differs between regions, countries, and even between institutions. Not only is the distribution of these pathogens in the environment or in the human microbiota different, but also the number and spectrum of susceptible patients and the availability of diagnostic tools, which causes species of rare yeasts to be misidentified and the prevalence of their infections to be underestimated. Because of the significant medical impact of these yeasts, timely diagnosis and accurate patient care are essential. That, in turn, relies on recognizing disease patterns and having access to appropriate therapeutic options. During the last decade, the array of rare yeasts that are being recognized as human opportunistic pathogens has expanded, because of the advances in health care and improved diagnostic techniques. However, regardless of this progress, some species of rare yeasts are still difficult to identify by phenotypic methods and many species show important resistance profiles to commonly used antifungals. Clinicians and microbiologists must, therefore, be aware of and stay alert for the appearance of these emerging pathogens as they can lead to serious complications that aggravate the underlying diseases of patients at risk and negatively impact patient care. Epidemiological surveillance is key to obtaining a true picture of the burden of rare yeast infections and to identify local unmet needs, which ultimately will be needed to optimize the clinical management of patients.

Author Contributions

Conceptualization, Ó.G., J.C.H.-P., B.T., C.F.; methodology, Ó.G., J.C.H.-P., B.T., C.L.-S.; software, C.F.; validation, C.F.; formal analysis, C.F.; investigation, C.F.; resources, C.F.; data curation, C.F.; writing—original draft preparation, O.G, C.F.; writing—review and editing, Ó.G., J.C.H.-P., B.T., C.L.-S., C.F.; supervision, C.F.; project administration, C.F.; funding acquisition, C.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Centro de Investigaciones de Méderi—CIMED, grant number B-024-2021.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data supporting this review are from previously reported studies and datasets, which have been properly cited. The processed data are available from the corresponding author upon request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Chen, S.C.; Perfect, J.; Colombo, A.L.; Cornely, O.A.; Groll, A.H.; Seidel, D.; Albus, K.; de Almedia, J.N., Jr.; Garcia-Effron, G.; Gilroy, N.; et al. Global guideline for the diagnosis and management of rare yeast infections: An initiative of the ECMM in cooperation with ISHAM and ASM. Lancet Infect. Dis. 2021, 21, e375–e386. [Google Scholar] [CrossRef]
  2. Miceli, M.H.; Diaz, J.A.; Lee, S.A. Emerging opportunistic yeast infections. Lancet Infect. Dis. 2011, 11, 142–151. [Google Scholar] [CrossRef] [PubMed]
  3. de Hoog, G.S.; Guarro, J.; Gené, J.; Ahmed, S.A.; Al-Hatmi, A.M.S.; Figueras, M.J.; Vitale, R.G. Atlas of Clinical Fungi the Ultimate Benchtool for Diagnostics, 4th ed.; Centraalbureau voor Schimmlcultures/Universitat Rovira i Virgili: Reus, Spain, 2020. [Google Scholar]
  4. Byrne, D.D.; Reboli, A.C. Rare yeast infections: Risk factors, clinical manifestations, treatment, and special considerations. Curr. Clin. Micro. Rpt. 2017, 4, 218–231. [Google Scholar] [CrossRef]
  5. Chitasombat, M.N.; Kofteridis, D.P.; Jiang, Y.; Tarrand, J.; Lewis, R.E.; Kontoyiannis, D.P. Rare opportunistic (non-Candida, non-Cryptococcus) yeast bloodstream infections in patients with cancer. J. Infect. 2012, 64, 68–75. [Google Scholar] [CrossRef] [Green Version]
  6. Arendrup, M.C.; Boekhout, T.; Akova, M.; Meis, J.F.; Cornely, O.A.; Lortholary, O.; European Society of Clinical, M.; Infectious Diseases Fungal Infection Study, G.; European Confederation of Medical, M. ESCMID and ECMM joint clinical guidelines for the diagnosis and management of rare invasive yeast infections. Clin. Microbiol. Infect. 2014, 20 (Suppl. S3), 76–98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Perez-Hansen, A.; Lass-Florl, C.; Lackner, M.; Rare Yeast Study, G. Antifungal susceptibility profiles of rare ascomycetous yeasts. J. Antimicrob. Chemother. 2019, 74, 2649–2656. [Google Scholar] [CrossRef]
  8. Arendrup, M.C.; Dzajic, E.; Jensen, R.H.; Johansen, H.K.; Kjaeldgaard, P.; Knudsen, J.D.; Kristensen, L.; Leitz, C.; Lemming, L.E.; Nielsen, L.; et al. Epidemiological changes with potential implication for antifungal prescription recommendations for fungaemia: Data from a nationwide fungaemia surveillance programme. Clin. Microbiol. Infect. 2013, 19, E343–E353. [Google Scholar] [CrossRef] [Green Version]
  9. Fernandez-Ruiz, M.; Guinea, J.; Puig-Asensio, M.; Zaragoza, O.; Almirante, B.; Cuenca-Estrella, M.; Aguado, J.M.; Project, C.; Geih, G.; Reipi. Fungemia due to rare opportunistic yeasts: Data from a population-based surveillance in Spain. Med. Mycol. 2017, 55, 125–136. [Google Scholar] [CrossRef] [Green Version]
  10. Lin, S.Y.; Lu, P.L.; Tan, B.H.; Chakrabarti, A.; Wu, U.I.; Yang, J.H.; Patel, A.K.; Li, R.Y.; Watcharananan, S.P.; Liu, Z.; et al. The epidemiology of non-Candida yeast isolated from blood: The Asia Surveillance Study. Mycoses 2019, 62, 112–120. [Google Scholar] [CrossRef] [Green Version]
  11. Skiada, A.; Pavleas, I.; Drogari-Apiranthitou, M. Rare fungal infectious agents: A lurking enemy. F1000Res 2017, 6, 1917. [Google Scholar] [CrossRef] [Green Version]
  12. Firacative, C. Invasive fungal disease in humans: Are we aware of the real impact? Mem. Inst. Oswaldo Cruz 2020, 115, e200430. [Google Scholar] [CrossRef]
  13. Donnelly, J.P.; Chen, S.C.; Kauffman, C.A.; Steinbach, W.J.; Baddley, J.W.; Verweij, P.E.; Clancy, C.J.; Wingard, J.R.; Lockhart, S.R.; Groll, A.H.; et al. Revision and Update of the Consensus Definitions of Invasive Fungal Disease From the European Organization for Research and Treatment of Cancer and the Mycoses Study Group Education and Research Consortium. Clin. Infect. Dis. 2019, 71, 1367–1376. [Google Scholar] [CrossRef] [Green Version]
  14. Worldometer. Countries in the World by Population. Available online: https://www.worldometers.info/world-population/population-by-country/ (accessed on 2 May 2023).
  15. Colombo, A.L.; Dantas, L.S.; Abramczyk, M.L.; Cypriano, M.; Fischman, O.; Iazzetti, A.V.; Petrilli, A.S.; Selijan, M.P. Rhodotorula glutinis fungemia: A case report and literature review. Braz. J. Infect. Dis. 1997, 1, 204–207. [Google Scholar] [PubMed]
  16. Lopes, J.O.; Alves, S.H.; Klock, C.; Oliveira, L.T.; Dal Forno, N.R. Trichosporon inkin peritonitis during continuous ambulatory peritoneal dialysis with bibliography review. Mycopathologia 1997, 139, 15–18. [Google Scholar] [CrossRef]
  17. Martinez Machin, G.; Perurena Lancha, M.; Nunez Carvajal, J.; Fernandez Andreu, C.M.; Bandera Tirado, F. Isolation, identification, and typing of yeasts from HIV-positive patients with oral candidiasis. Rev. Cubana Med. Trop. 1997, 49, 174–180. [Google Scholar]
  18. Rodero, L.; Boutureira, M.; Demkura, H.; Burkett, A.; Fernandez, C.; Losso, M.; Jauregui Rueda, H.; Monticelli, A.; Vitale, R.; Canteros, C.; et al. Yeast infections: Causative agents and their antifungal resistance in hospitalized pediatric patients and HIV-positive adults. Rev. Argent. Microbiol. 1997, 29, 7–15. [Google Scholar] [PubMed]
  19. Bonifaz, A.; Vazquez-Gonzalez, D.; Macias, B.; Paredes-Farrera, F.; Hernandez, M.A.; Araiza, J.; Ponce, R.M. Oral geotrichosis: Report of 12 cases. J. Oral Sci. 2010, 52, 477–483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Hernandez-Hernandez, F.; Cordova-Martinez, E.; Manzano-Gayosso, P.; Lopez-Alvarez, R.; Bazan-Mora, E.; Lopez-Martinez, R. Frequency of mycosis in immunosuppressed patients at a regional hospital of Mexico City. Salud Publica Mex. 2003, 45, 455–460. [Google Scholar]
  21. Cordoba, S.; Vivot, W.; Bosco-Borgeat, M.E.; Taverna, C.; Szusz, W.; Murisengo, O.; Isla, G.; Davel, G.; Red Nacional De Laboratorios De Micología. Species distribution and susceptibility profile of yeasts isolated from blood cultures: Results of a multicenter active laboratory-based surveillance study in Argentina. Rev. Argent. Microbiol. 2011, 43, 176–185. [Google Scholar] [CrossRef]
  22. De Barros, J.D.; Do Nascimento, S.M.; De Araujo, F.J.; Braz Rde, F.; Andrade, V.S.; Theelen, B.; Boekhout, T.; Illnait-Zaragozi, M.T.; Gouveia, M.N.; Fernandes, M.C.; et al. Kodamaea (Pichia) ohmeri fungemia in a pediatric patient admitted in a public hospital. Med. Mycol. 2009, 47, 775–779. [Google Scholar] [CrossRef] [Green Version]
  23. Junqueira, J.C.; Vilela, S.F.; Rossoni, R.D.; Barbosa, J.O.; Costa, A.C.; Rasteiro, V.M.; Suleiman, J.M.; Jorge, A.O. Oral colonization by yeasts in HIV-positive patients in Brazil. Rev. Inst. Med. Trop. Sao Paulo 2012, 54, 17–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Alvarado Socarras, J.; Rojas Torres, J.P.; Vargas Soler, J.A.; Guerrero, C. Kodamaea ohmeri infection in a newborn with a mediastinal mass. Arch. Argent. Pediatr. 2016, 114, e319–e322. [Google Scholar] [CrossRef]
  25. Vivas, R.; Beltran, C.; Munera, M.I.; Trujillo, M.; Restrepo, A.; Garces, C. Fungemia due to Kodamaea ohmeri in a young infant and review of the literature. Med. Mycol. Case Rep. 2016, 13, 5–8. [Google Scholar] [CrossRef] [PubMed]
  26. Lafayette, T.C.; Oliveira, L.T.; Landell, M.; Valente, P.; Alves, S.H.; Pereira, W.V. Dipodascus capitatus (Geotrichum capitatum): Fatal systemic infection on patient with acute myeloid leukemia. Rev. Soc. Bras. Med. Trop. 2011, 44, 648–650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Parahym, A.M.; Rolim Neto, P.J.; da Silva, C.M.; Domingos Ide, F.; Goncalves, S.S.; Leite, E.P.; de Morais, V.L.; Macedo, D.P.; de Lima Neto, R.G.; Neves, R.P. Invasive infection due to Saprochaete capitata in a young patient with hematological malignancies. Braz. J. Microbiol. 2015, 46, 527–530. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Radich, R.J.; Alvarez, Z.C.; Valenzuela, R.A.; Castillo, H.F.; Moraga, V.F.; Castillo, A.J. Role of surgery in Saprochaete capitata (S. capitata) sepsis in a patient with acute myeloid leukemia. Rev. Med. Chil. 2017, 145, 1067–1071. [Google Scholar] [CrossRef]
  29. Garcia-Melendo, C.; Cubiro, X.; Lopez-Sanchez, C.; Turienzo, M.; Mozos, A.; Puig, L. Saprochaete capitata disseminated infection presenting as macular rash after haematopoietic stem cell transplantation. J. Eur. Acad. Dermatol. Venereol. 2020, 34, e748–e750. [Google Scholar] [CrossRef]
  30. Palacios-Reyes, D.; Yamazaki-Nakashimada, M.A.; Castano-Jaramillo, L.; Roman-Montes, C.M.; Gonzalez-Lara, M.F.; Scheffler-Mendoza, S.; Costta-Michuy, A.; Bustamante, J.; Blancas-Galicia, L. Pulmonary geotrichosis in chronic granulomatous disease. J. Investig. Allergol. Clin. Immunol. 2021, 32, 306–308. [Google Scholar] [CrossRef]
  31. Archer-Dubon, C.; Icaza-Chivez, M.E.; Orozco-Topete, R.; Reyes, E.; Baez-Martinez, R.; Ponce de Leon, S. An epidemic outbreak of Malassezia folliculitis in three adult patients in an intensive care unit: A previously unrecognized nosocomial infection. Int. J. Dermatol. 1999, 38, 453–456. [Google Scholar] [CrossRef]
  32. Alves, E.V.; Martins, J.E.; Ribeiro, E.B.; Sotto, M.N. Pityrosporum folliculitis: Renal transplantation case report. J. Dermatol. 2000, 27, 49–51. [Google Scholar] [CrossRef]
  33. Cermeno, J.R.; Hernandez, I.; Godoy, G.; Cabello, I.; Cermeno, J.J.; Orellan, Y.; Blanco, Y. Mycoses at Hospital Universitario “Ruiz y Paez”, Ciudad Bolivar, Venezuela, 2002. Investig. Clin. 2005, 46, 37–42. [Google Scholar]
  34. Giusiano, G.; Mangiaterra, M.; Saito, V.G.; Rojas, F.; Gomez, V.; Diaz, M.C. Etiology of fungaemia and catheter colonisation in Argentinean paediatric patients. Mycoses 2006, 49, 49–54. [Google Scholar] [CrossRef] [PubMed]
  35. Peres, F.L.X.; Bonamigo, R.R.; Bottega, G.B.; Staub, F.L.; Cartell, A.S.; Bakos, R.M. Pityrosporum folliculitis in critically ill COVID-19 patients. J. Eur. Acad. Dermatol. Venereol. 2022, 36, e186–e188. [Google Scholar] [CrossRef]
  36. Mestroni, S.C.; Verna, J.A.; Smolkin, A.; Bava, A.J. Etiological factors of fungemia in the Hospital San Martin in La Plata. Rev. Argent. Microbiol. 2003, 35, 106–109. [Google Scholar] [PubMed]
  37. Aguirre, C.; Euliarte, C.; Finquelievich, J.; Sosa Mde, L.; Giusiano, G. Fungemia and interstitial lung compromise caused by Malassezia sympodialis in a pediatric patient. Rev. Iberoam. Micol. 2015, 32, 118–121. [Google Scholar] [CrossRef]
  38. Galvis-Marín, J.C.; Giraldo-Ospina, B.; Martínez-Ríos, J.B.; Echeverri-Peláez, S. Fungemia por Malassezia sympodialis en una Unidad de Cuidados Intensivos Neonatal de Colombia. Infectio 2021, 25, 130–134. [Google Scholar] [CrossRef]
  39. Magalhaes, Y.C.; Bomfim, M.R.; Melonio, L.C.; Ribeiro, P.C.; Cosme, L.M.; Rhoden, C.R.; Marques, S.G. Clinical significance of the isolation of Candida species from hospitalized patients. Braz. J. Microbiol. 2015, 46, 117–123. [Google Scholar] [CrossRef] [Green Version]
  40. Batista, G.C.; Krebs, V.L.; Ruiz, L.S.; Auler, M.E.; Hahn, R.C.; Paula, C.R. Oral colonization: A possible source for candidemia in low-weight neonates. J. Mycol. Med. 2014, 24, 81–86. [Google Scholar] [CrossRef]
  41. Paula, C.R.; Krebs, V.L.; Auler, M.E.; Ruiz, L.S.; Matsumoto, F.E.; Silva, E.H.; Diniz, E.M.; Vaz, F.A. Nosocomial infection in newborns by Pichia anomala in a Brazilian intensive care unit. Med. Mycol. 2006, 44, 479–484. [Google Scholar] [CrossRef] [Green Version]
  42. Orecchini, L.A.; Olmos, E.; Taverna, C.G.; Murisengo, O.A.; Szuzs, W.; Vivot, W.; Cordoba, S.; Bosco-Borgeat, M.E.; Montanaro, P.C. First case of fungemia due to Pseudozyma aphidis in a pediatric patient with osteosarcoma in Latin America. J. Clin. Microbiol. 2015, 53, 3691–3694. [Google Scholar] [CrossRef] [Green Version]
  43. Parahym, A.M.; da Silva, C.M.; Domingos Ide, F.; Goncalves, S.S.; Rodrigues Mde, M.; de Morais, V.L.; Neves, R.P. Pulmonary infection due to Pseudozyma aphidis in a patient with Burkitt lymphoma: First case report. Diagn. Microbiol. Infect. Dis. 2013, 75, 104–106. [Google Scholar] [CrossRef] [Green Version]
  44. Brito-Santos, F.; Figueiredo-Carvalho, M.H.G.; Coelho, R.A.; de Oliveira, J.C.A.; Monteiro, R.V.; da Silva Chaves, A.L.; Almeida-Paes, R. Molecular identification and antifungal susceptibility testing of Pucciniomycotina red yeast clinical isolates from Rio de Janeiro, Brazil. Braz. J. Microbiol. 2020, 51, 95–98. [Google Scholar] [CrossRef]
  45. Gaytan-Martinez, J.; Mateos-Garcia, E.; Sanchez-Cortes, E.; Gonzalez-Llaven, J.; Casanova-Cardiel, L.J.; Fuentes-Allen, J.L. Microbiological findings in febrile neutropenia. Arch. Med. Res. 2000, 31, 388–392. [Google Scholar] [CrossRef]
  46. Potenza, L.; Chitasombat, M.N.; Klimko, N.; Bettelli, F.; Dragonetti, G.; Del Principe, M.I.; Nucci, M.; Busca, A.; Fracchiolla, N.; Sciume, M.; et al. Rhodotorula infection in haematological patient: Risk factors and outcome. Mycoses 2019, 62, 223–229. [Google Scholar] [CrossRef] [PubMed]
  47. Inacio, C.P.; Diniz, M.V.; Araujo, P.S.R.; Barros, M.S.; Andrade, M.C.L.; Lima-Neto, R.G.; Macedo, D.P.C.; Neves, R.P. Bloodstream infection of a cancer patient by Cystobasidium minutum: A case report and literature review. Mycopathologia 2020, 185, 395–398. [Google Scholar] [CrossRef] [PubMed]
  48. Lunardi, L.W.; Aquino, V.R.; Zimerman, R.A.; Goldani, L.Z. Epidemiology and outcome of Rhodotorula fungemia in a tertiary care hospital. Clin. Infect. Dis. 2006, 43, e60–e63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Pereira, G.H.; Muller, P.R.; Szeszs, M.W.; Levin, A.S.; Melhem, M.S. Five-year evaluation of bloodstream yeast infections in a tertiary hospital: The predominance of non-C. albicans Candida species. Med. Mycol. 2010, 48, 839–842. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Verdugo, F.J.; Briones, E.; Porte, L.; Amaro, J.; Fica, A. Peritonitis fúngica por Rhodotorula mucilaginosa en una paciente en diálisis peritoneal automatizada: Revisión de la literatura. Rev. Chil. Infectología 2016, 33, 222–225. [Google Scholar] [CrossRef]
  51. Cabral, A.M.; da Siveira Rioja, S.; Brito-Santos, F.; Peres da Silva, J.R.; MacDowell, M.L.; Melhem, M.S.C.; Mattos-Guaraldi, A.L.; Hirata Junior, R.; Damasco, P.V. Endocarditis due to Rhodotorula mucilaginosa in a kidney transplanted patient: Case report and review of medical literature. JMM Case Rep. 2017, 4, e005119. [Google Scholar] [CrossRef] [Green Version]
  52. Chaparro, M.; Estupiñán, M.; Camacho, G.; Uribe, G. Infección por Rhodotorula mucilaginosa en trasplante alogénico de progenitores hematopoyéticos, reporte de un caso. Casos Clínicos 2018, 5, 55–57. [Google Scholar] [CrossRef]
  53. Pereira, L.C.; Correia, A.F.; da Silva, Z.D.L.; de Resende, C.N.; Brandao, F.; Almeida, R.M.; de Medeiros Nobrega, Y.K. Vulvovaginal candidiasis and current perspectives: New risk factors and laboratory diagnosis by using MALDI TOF for identifying species in primary infection and recurrence. Eur. J. Clin. Microbiol. Infect. Dis. 2021, 40, 1681–1693. [Google Scholar] [CrossRef] [PubMed]
  54. Ruiz-Esquide, F.; Diaz, M.C.; Wu, E.; Silva, V. Verrucous endocarditis secondary to Saccharomyces cerevisiae. A case report. Rev. Med. Chil. 2002, 130, 1165–1169. [Google Scholar] [CrossRef] [PubMed]
  55. Riquelme, A.J.; Calvo, M.A.; Guzman, A.M.; Depix, M.S.; Garcia, P.; Perez, C.; Arrese, M.; Labarca, J.A. Saccharomyces cerevisiae fungemia after Saccharomyces boulardii treatment in immunocompromised patients. J. Clin. Gastroenterol. 2003, 36, 41–43. [Google Scholar] [CrossRef]
  56. Buscemi, L.; Arechavala, A.; Negroni, R. Study of acute vulvovaginitis in sexually active adult women, with special reference to candidosis, in patients of the Francisco J. Muniz Infectious Diseases Hospital. Rev. Iberoam. Micol. 2004, 21, 177–181. [Google Scholar]
  57. Silva, V.; Diaz, M.C.; Febre, N.; Chilean Invasive Fungal Infections, G. Invasive fungal infections in Chile: A multicenter study of fungal prevalence and susceptibility during a 1-year period. Med. Mycol. 2004, 42, 333–339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Kliemann, D.A.; Antonello, V.S.; Severo, L.C.; Pasqualotto, A.C. Saccharomyces cerevisiae oesophagitis in a patient with oesophageal carcinoma. J. Infect. Dev. Ctries. 2011, 5, 493–495. [Google Scholar] [CrossRef] [Green Version]
  59. Bulacio, L.; Paz, M.; Ramadan, S.; Ramos, L.; Pairoba, C.; Sortino, M.; Escovich, L.; Lopez, C. Oral infections caused by yeasts in patients with head and neck cancer undergoing radiotherapy. Identification of the yeasts and evaluation of their antifungal susceptibility. J. Mycol. Med. 2012, 22, 348–353. [Google Scholar] [CrossRef]
  60. Souza Goebel, C.; de Mattos Oliveira, F.; Severo, L.C. Saccharomyces cerevisiae infections. Rev. Iberoam. Micol. 2013, 30, 205–208. [Google Scholar] [CrossRef]
  61. Gamarra, S.; Morano, S.; Dudiuk, C.; Mancilla, E.; Nardin, M.E.; de Los Angeles Mendez, E.; Garcia-Effron, G. Epidemiology and antifungal susceptibilities of yeasts causing vulvovaginitis in a teaching hospital. Mycopathologia 2014, 178, 251–258. [Google Scholar] [CrossRef] [PubMed]
  62. Guimaraes, L.F.; Halpern, M.; de Lemos, A.S.; de Gouvea, E.F.; Goncalves, R.T.; da Rosa Santos, M.A.; Nucci, M.; Santoro-Lopes, G. Invasive fungal disease in renal transplant recipients at a Brazilian center: Local epidemiology matters. Transplant. Proc. 2016, 48, 2306–2309. [Google Scholar] [CrossRef] [PubMed]
  63. Appel-da-Silva, M.C.; Narvaez, G.A.; Perez, L.R.R.; Drehmer, L.; Lewgoy, J. Saccharomyces cerevisiae var. boulardii fungemia following probiotic treatment. Med. Mycol. Case Rep. 2017, 18, 15–17. [Google Scholar] [CrossRef] [PubMed]
  64. Landaburu, M.F.; Lopez Daneri, G.A.; Relloso, S.; Zarlenga, L.J.; Vinante, M.A.; Mujica, M.T. Fungemia following Saccharomyces cerevisiae var. boulardii probiotic treatment in an elderly patient. Rev. Argent. Microbiol. 2020, 52, 27–30. [Google Scholar] [CrossRef]
  65. Pinto, G.; Lima, L.; Pedra, T.; Assumpcao, A.; Morgado, S.; Mascarenhas, L. Bloodstream infection by Saccharomyces cerevisiae in a COVID-19 patient receiving probiotic supplementation in the ICU in Brazil. Access Microbiol. 2021, 3, 000250. [Google Scholar] [CrossRef] [PubMed]
  66. de Almeida, J.N.J.; Sztajnbok, J.; da Silva, A.R.J.; Vieira, V.A.; Galastri, A.L.; Bissoli, L.; Litvinov, N.; Del Negro, G.M.; Motta, A.L.; Rossi, F.; et al. Rapid identification of moulds and arthroconidial yeasts from positive blood cultures by MALDI-TOF mass spectrometry. Med. Mycol. 2016, 54, 885–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Moretti-Branchini, M.L.; Fukushima, K.; Schreiber, A.Z.; Nishimura, K.; Papaiordanou, P.M.; Trabasso, P.; Tanaka, R.; Miyaji, M. Trichosporon species infection in bone marrow transplanted patients. Diagn. Microbiol. Infect. Dis. 2001, 39, 161–164. [Google Scholar] [CrossRef]
  68. Silva, V.; Zepeda, G.; Alvareda, D. Nosocomial urinary infection due to Trichosporon asahii. First two cases in Chile. Rev. Iberoam. Micol. 2003, 20, 21–23. [Google Scholar]
  69. Abdala, E.; Lopes, R.I.; Chaves, C.N.; Heins-Vaccari, E.M.; Shikanai-Yasuda, M.A. Trichosporon asahii fatal infection in a non-neutropenic patient after orthotopic liver transplantation. Transpl. Infect. Dis. 2005, 7, 162–165. [Google Scholar] [CrossRef]
  70. Chan-Tack, K.M. Fatal Trichosporon asahii septicemia in a Guatemalan farmer with acute lymphoblastic leukemia. South Med. J. 2005, 98, 954–955. [Google Scholar] [CrossRef]
  71. Rodriguez-Tudela, J.L.; Diaz-Guerra, T.M.; Mellado, E.; Cano, V.; Tapia, C.; Perkins, A.; Gomez-Lopez, A.; Rodero, L.; Cuenca-Estrella, M. Susceptibility patterns and molecular identification of Trichosporon species. Antimicrob. Agents Chemother. 2005, 49, 4026–4034. [Google Scholar] [CrossRef] [Green Version]
  72. Rodrigues Gda, S.; de Faria, R.R.; Guazzelli, L.S.; Oliveira Fde, M.; Severo, L.C. Nosocomial infection due to Trichosporon asahii: Clinical revision of 22 cases. Rev. Iberoam. Micol. 2006, 23, 85–89. [Google Scholar] [CrossRef]
  73. Rodriguez-Tudela, J.L.; Gomez-Lopez, A.; Alastruey-Izquierdo, A.; Mellado, E.; Bernal-Martinez, L.; Cuenca-Estrella, M. Genotype distribution of clinical isolates of Trichosporon asahii based on sequencing of intergenic spacer 1. Diagn. Microbiol. Infect. Dis. 2007, 58, 435–440. [Google Scholar] [CrossRef] [PubMed]
  74. Araujo Ribeiro, M.; Alastruey-Izquierdo, A.; Gomez-Lopez, A.; Rodriguez-Tudela, J.L.; Cuenca-Estrella, M. Molecular identification and susceptibility testing of Trichosporon isolates from a Brazilian hospital. Rev. Iberoam. Micol. 2008, 25, 221–225. [Google Scholar] [CrossRef] [PubMed]
  75. Biasoli, M.S.; Carlson, D.; Chiganer, G.J.; Parodi, R.; Greca, A.; Tosello, M.E.; Luque, A.G.; Montero, A. Systemic infection caused by Trichosporon asahii in a patient with liver transplant. Med. Mycol. 2008, 46, 719–723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Chagas-Neto, T.C.; Chaves, G.M.; Melo, A.S.; Colombo, A.L. Bloodstream infections due to Trichosporon spp.: Species distribution, Trichosporon asahii genotypes determined on the basis of ribosomal DNA intergenic spacer 1 sequencing, and antifungal susceptibility testing. J. Clin. Microbiol. 2009, 47, 1074–1081. [Google Scholar] [CrossRef] [Green Version]
  77. Pontes, Z.B.; Silva, A.D.; Lima Ede, O.; Guerra Mde, H.; Oliveira, N.M.; Carvalho Mde, F.; Guerra, F.S. Otomycosis: A retrospective study. Braz. J. Otorhinolaryngol. 2009, 75, 367–370. [Google Scholar] [CrossRef]
  78. Menezes, E.A.; Marinho, J.A.; Angelo, M.R.; Cunha Mda, C.; Cunha, F.A.; Vasconcelos Junior, A.A. Isolation and antifungal susceptibility testing of Trichosporon asahii in Ceara, Brazil. Rev. Inst. Med. Trop. Sao Paulo 2012, 54, 1–3. [Google Scholar] [CrossRef] [Green Version]
  79. Taverna, C.G.; Cordoba, S.; Murisengo, O.A.; Vivot, W.; Davel, G.; Bosco-Borgeat, M.E. Molecular identification, genotyping, and antifungal susceptibility testing of clinically relevant Trichosporon species from Argentina. Med. Mycol. 2014, 52, 356–366. [Google Scholar] [CrossRef] [Green Version]
  80. Corzo-Leon, D.E.; Satlin, M.J.; Soave, R.; Shore, T.B.; Schuetz, A.N.; Jacobs, S.E.; Walsh, T.J. Epidemiology and outcomes of invasive fungal infections in allogeneic haematopoietic stem cell transplant recipients in the era of antifungal prophylaxis: A single-centre study with focus on emerging pathogens. Mycoses 2015, 58, 325–336. [Google Scholar] [CrossRef]
  81. Montoya, A.M.; Sanchez Gonzalez, A.; Palma-Nicolas, J.P.; Gomez-Trevino, A.; Gonzalez, J.G.; Gonzalez, G.M. Genotyping, extracellular compounds, and antifungal susceptibility testing of Trichosporon asahii isolated from Mexican patients. Med. Mycol. 2015, 53, 505–511. [Google Scholar] [CrossRef] [Green Version]
  82. Almeida, A.A.; Crispim Bdo, A.; Grisolia, A.B.; Svidzinski, T.I.; Ortolani, L.G.; Oliveira, K.M. Genotype, antifungal susceptibility, and biofilm formation of Trichosporon asahii isolated from the urine of hospitalized patients. Rev. Argent. Microbiol. 2016, 48, 62–66. [Google Scholar] [CrossRef] [Green Version]
  83. Alzate-Atehortua, M.V.; Garzón, J.; Valderrama, S.; Zhong, A. Tricosporonosis en un paciente con leucemia aguda. Acta Colomb. Cuid. Intensivo 2016, 17, 68–75. [Google Scholar] [CrossRef]
  84. Bastidas, A.R.; Pantoja, J.A.; Munar, M.A.; Giraldo, L.F.; Yurgaki, J. Bronquiolitis respiratoria y neumonía descamativa asociada a fungemia por Trichosporon asahii en inmunocompetente: A propósito de un caso. Revista Med. 2016, 24, 89–101. [Google Scholar] [CrossRef] [Green Version]
  85. Escarra, F.; Lema, J.; Caracciolo, B.; Carnovale, S.; Alvarez, V.; Tramonti, N.; Guarracino, F.; Teresa Rosanova, M. Trichosporon asahii sepsis associated with urinary catheter in a pediatric burn unit: 2 case reports. Arch. Argent. Pediatr. 2017, 115, e311–e314. [Google Scholar] [CrossRef] [PubMed]
  86. Montoya, A.M.; Elizondo-Zertuche, M.; Trevino-Rangel, R.J.; Becerril-Garcia, M.; Gonzalez, G.M. Biofilm formation and antifungal susceptibility of Trichosporon asahii isolates from Mexican patients. Rev. Iberoam. Micol. 2018, 35, 22–26. [Google Scholar] [CrossRef]
  87. Cardenas-de la Garza, J.A.; Ancer-Arellano, J.; Cuellar-Barboza, A.; Saenz-Ibarra, B.; Ocampo-Garza, S.S.; Barboza-Quintana, O.; Gallardo-Rocha, A.; Vera-Cabrera, L.; Ocampo-Candiani, J.; Welsh, O. Disseminated Trichosporon asahii infection in a patient with acute myeloid leukemia. J. Dermatol. 2019, 46, e128–e129. [Google Scholar] [CrossRef]
  88. Alvarez Duarte, E.; Salas, V. In vitro activity of isavuconazole against clinically isolated yeasts from Chile. Braz J. Microbiol. 2020, 51, 1801–1805. [Google Scholar] [CrossRef]
  89. Ramirez, I.; Moncada, D. Fatal disseminated infection by Trichosporon asahii under voriconazole therapy in a patient with acute myeloid leukemia: A review of breakthrough infections by Trichosporon spp. Mycopathologia 2020, 185, 377–388. [Google Scholar] [CrossRef]
  90. Nobrega de Almeida, J., Jr.; Moreno, L.; Francisco, E.C.; Noronha Marques, G.; Mendes, A.V.; Barberino, M.G.; Colombo, A.L. Trichosporon asahii superinfections in critically ill COVID-19 patients overexposed to antimicrobials and corticosteroids. Mycoses 2021, 64, 817–822. [Google Scholar] [CrossRef]
  91. Nobrega de Almeida, J.; Francisco, E.C.; Holguin Ruiz, A.; Cuellar, L.E.; Rodrigues Aquino, V.; Verena Mendes, A.; Queiroz-Telles, F.; Santos, D.W.; Guimaraes, T.; Maranhao Chaves, G.; et al. Epidemiology, clinical aspects, outcomes and prognostic factors associated with Trichosporon fungaemia: Results of an international multicentre study carried out at 23 medical centres. J. Antimicrob. Chemother. 2021, 76, 1907–1915. [Google Scholar] [CrossRef]
  92. Robles-Tenorio, A.; Rivas-Lopez, R.A.; Bonifaz, A.; Tarango-Martinez, V.M. Disseminated mucocutaneous trichosporonosis in a patient with histiocytic sarcoma. An. Bras. Dermatol. 2021, 96, 595–597. [Google Scholar] [CrossRef]
  93. Segrelles-Calvo, G.; Araujo, G.R.S.; Llopis-Pastor, E.; Frases, S. Trichosporon asahii as cause of nosocomial pneumonia in patient with COVID-19: A triple co-infection. Arch. Bronconeumol. 2021, 57, 46–48. [Google Scholar] [CrossRef] [PubMed]
  94. Monzani, V.; Cordoba, S.; Vivot, M.; Arias, B.; Vivot, W.; Szusz, W.; Castellaro, P.; Appendino, A.; Taverna, C.G. A case report of catheter-related bloodstream infection due to Trichosporon coremiiforme in a patient with secondary neutropenia to HIV. J. Mycol. Med. 2020, 30, 100916. [Google Scholar] [CrossRef]
  95. Giusiano, G.E.; Mangiaterra, M.; Rojas, F.; Gomez, V. Yeasts species distribution in neonatal intensive care units in northeast Argentina. Mycoses 2004, 47, 300–303. [Google Scholar] [CrossRef] [PubMed]
  96. Macedo, D.P.; de Oliveira, N.T.; da Silva, V.K.; de Almeida Farias, A.M.; de Lima Neto, R.G.; Wilheim, A.B.; de Oliveira, P.C.; Pedi, N.; de Andrade, S.L.; Neves, R.P. Trichosporon inkin esophagitis: An uncommon disease in a patient with pulmonary cancer. Mycopathologia 2011, 171, 279–283. [Google Scholar] [CrossRef] [PubMed]
  97. Almeida Junior, J.N.; Song, A.T.; Campos, S.V.; Strabelli, T.M.; Del Negro, G.M.; Figueiredo, D.S.; Motta, A.L.; Rossi, F.; Guitard, J.; Benard, G.; et al. Invasive Trichosporon infection in solid organ transplant patients: A report of two cases identified using IGS1 ribosomal DNA sequencing and a review of the literature. Transpl. Infect. Dis. 2014, 16, 135–140. [Google Scholar] [CrossRef] [PubMed]
  98. Nobrega de Almeida Junior, J.; Buccheri de Oliveira, R.; Duarte, A.; Lopes Motta, A.; Rossi, F.; Sachiko Yamamoto de Figueiredo, D.; Barbaro Del Negro, G.M.; Aoki, V.; Wakisaka Maruta, C.; Giuli Santi, C.; et al. Trichosporon inkin as an emergent pathogen in patients with severe pemphigus. JAMA Dermatol. 2015, 151, 642–645. [Google Scholar] [CrossRef]
  99. Milan, E.P.; Silva-Rocha, W.P.; de Almeida, J.J.S.; Fernandes, T.U.G.; de Araujo Prudente, A.L.; de Azevedo, M.F.; Francisco, E.C.; de Azevedo Melo, A.S.; Colombo, A.L.; Chaves, G.M. Trichosporon inkin meningitis in Northeast Brazil: First case report and review of the literature. BMC Infect. Dis. 2018, 18, 470. [Google Scholar] [CrossRef] [Green Version]
  100. Santos, F.A.; Leite-Andrade, M.C.; Vasconcelos, M.A.; Alves, A.I.; Buonafina-Paz, M.D.; Araujo-Neto, L.N.; Macedo, D.P.; Neves, R.P. Trichosporon inkin fungemia case report: Clinical and laboratory management. Future Microbiol. 2022, 17, 81–87. [Google Scholar] [CrossRef]
  101. Burgo, F.J.; Mengelle, D.E.; Abraham, A.; Kremer, G.; Autorino, C.M. Periprosthetic fungal infection of a hip caused by Trichosporon inkin. Arthroplast. Today 2018, 4, 24–26. [Google Scholar] [CrossRef] [Green Version]
  102. García, L.; Osorio, G.F. Trichosporon mucoides infección en paciente inmunocompetente. Colomb. Med. 2008, 39, 185–188. [Google Scholar]
  103. Mendez-Tovar, L.J.; Rodriguez-Sanchez, J.F.; Manzano-Gayosso, P.; Hernandez-Hernandez, F.; Blancas-Valencia, J.M.; Silva-Gonzalez, I. Esophageal candidiasis in patients from a specialty hospital. Rev. Med. Inst. Mex. Seguro. Soc. 2019, 57, 74–81. [Google Scholar] [PubMed]
  104. Marin-Hernandez, E.; Mejia-Mancera, C.G.; Quijada-Henderson, M.A.; Valero-Gomez, A. Atypical folliculitis caused by Malassezia spp. in immunosuppressed patients. Bol. Med. Hosp. Infant. Mex. 2022, 79, 62–68. [Google Scholar] [CrossRef] [PubMed]
  105. Messina, F.; Romero, M.; Marin, E.; Depardo, R.; Negroni, R.; Arechavala, A.; Masini, D.; Corti, M.; Walker, L.; Santiso, G. Clinical problems in medical mycology: Problem number 53. Rev. Iberoam. Micol. 2019, 36, 93–95. [Google Scholar] [CrossRef] [PubMed]
  106. Rodriguez-Carreon, A.A.; Arenas-Guzman, R.; Fonte-Avalos, V.; Gutierrez-Mendoza, D.; Vega-Memije, M.E.; Dominguez-Cherit, J. Confluent and reticulated Gougerot-Carteaud papillomatosis: A case report of an excellent response to minocycline. Gac. Med. Mex. 2008, 144, 67–70. [Google Scholar] [PubMed]
  107. Pasqualotto, G.C.; Copetti, F.A.; Meneses, C.F.; Machado, A.R.; Brunetto, A.L. Infection by Rhodotorula sp. in children receiving treatment for malignant diseases. J. Pediatr. Hematol. Oncol. 2005, 27, 232–233. [Google Scholar] [CrossRef]
  108. De Almeida, G.M.; Costa, S.F.; Melhem, M.; Motta, A.L.; Szeszs, M.W.; Miyashita, F.; Pierrotti, L.C.; Rossi, F.; Burattini, M.N. Rhodotorula spp. isolated from blood cultures: Clinical and microbiological aspects. Med. Mycol. 2008, 46, 547–556. [Google Scholar] [CrossRef] [Green Version]
  109. Lopez Moral, L.; Tiraboschi, I.N.; Schijman, M.; Bianchi, M.; Guelfand, L.; Cataldi, S.; integrantes de la Red de Micología de la Ciudad de Buenos Aires. Fungemia in hospitals of the city of Buenos Aires, Argentina. Rev. Iberoam. Micol. 2012, 29, 144–149. [Google Scholar] [CrossRef]
  110. Pereira, D.N.; Nader, S.S.; Nader, P.; Martins, P.G.; Furlan, S.P.; Hentges, C.R. Disseminated Trichosporon spp. infection in preterm newborns: A case report. J. Pediatr. (Rio J.) 2009, 85, 459–461. [Google Scholar] [CrossRef]
  111. CLSI. Performance Standards for Antifungal Susceptibility Testing of Yeasts. In CLSI Supplement M27M44S, 3rd ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2022. [Google Scholar]
  112. Garcia-Martos, P.; Hernandez-Molina, J.M.; Galan, F.; Ruiz-Henestrosa, J.R.; Garcia-Agudo, R.; Palomo, M.J.; Mira, J. Isolation of Hanseniaspora uvarum (Kloeckera apiculata) in humans. Mycopathologia 1998, 144, 73–75. [Google Scholar] [CrossRef]
  113. Cendejas-Bueno, E.; Gomez-Lopez, A.; Mellado, E.; Rodriguez-Tudela, J.L.; Cuenca-Estrella, M. Identification of pathogenic rare yeast species in clinical samples: Comparison between phenotypical and molecular methods. J. Clin. Microbiol. 2010, 48, 1895–1899. [Google Scholar] [CrossRef] [Green Version]
  114. Montecino-Rodriguez, E.; Berent-Maoz, B.; Dorshkind, K. Causes, consequences, and reversal of immune system aging. J. Clin. Investig. 2013, 123, 958–965. [Google Scholar] [CrossRef] [Green Version]
  115. Weyand, C.M.; Goronzy, J.J. Aging of the Immune System. Mechanisms and Therapeutic Targets. Ann. Am. Thorac. Soc. 2016, 13 (Suppl. S5), S422–S428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Castano, G.; Yarrarapu, S.N.S.; Mada, P.K. Trichosporonosis; StatPearls: Treasure Island, FL, USA, 2023. [Google Scholar]
  117. Kourti, M.; Roilides, E. Invasive Trichosporonosis in Neonates and Pediatric Patients with Malignancies or Hematologic Disorders. Pathogens 2022, 11, 242. [Google Scholar] [CrossRef] [PubMed]
  118. Suzuki, K.; Nakase, K.; Kyo, T.; Kohara, T.; Sugawara, Y.; Shibazaki, T.; Oka, K.; Tsukada, T.; Katayama, N. Fatal Trichosporon fungemia in patients with hematologic malignancies. Eur. J. Haematol. 2010, 84, 441–447. [Google Scholar] [CrossRef]
  119. Enache-Angoulvant, A.; Hennequin, C. Invasive Saccharomyces infection: A comprehensive review. Clin. Infect. Dis. 2005, 41, 1559–1568. [Google Scholar] [CrossRef] [PubMed]
  120. Vazquez-Gonzalez, D.; Perusquia-Ortiz, A.M.; Hundeiker, M.; Bonifaz, A. Opportunistic yeast infections: Candidiasis, cryptococcosis, trichosporonosis and geotrichosis. J. Dtsch. Dermatol. Ges. 2013, 11, 381–393. [Google Scholar] [CrossRef] [Green Version]
  121. Pappas, P.G.; Kauffman, C.A.; Andes, D.R.; Clancy, C.J.; Marr, K.A.; Ostrosky-Zeichner, L.; Reboli, A.C.; Schuster, M.G.; Vazquez, J.A.; Walsh, T.J.; et al. Clinical practice guideline for the management of candidiasis: 2016 update by the Infectious Diseases Society of America. Clin. Infect. Dis. 2016, 62, e1–e50. [Google Scholar] [CrossRef] [Green Version]
  122. Cornely, O.A.; Bassetti, M.; Calandra, T.; Garbino, J.; Kullberg, B.J.; Lortholary, O.; Meersseman, W.; Akova, M.; Arendrup, M.C.; Arikan-Akdagli, S.; et al. ESCMID * guideline for the diagnosis and management of Candida diseases 2012: Non-neutropenic adult patients. Clin. Microbiol. Infect. 2012, 18 (Suppl. S7), 19–37. [Google Scholar] [CrossRef] [Green Version]
  123. Denning, D.W. Echinocandin antifungal drugs. Lancet 2003, 362, 1142–1151. [Google Scholar] [CrossRef]
  124. Francisco, E.C.; de Almeida Junior, J.N.; de Queiroz Telles, F.; Aquino, V.R.; Mendes, A.V.A.; de Andrade Barberino, M.G.M.; de Tarso, O.C.P.; Guimaraes, T.; Hahn, R.C.; Padovan, A.C.B.; et al. Species distribution and antifungal susceptibility of 358 Trichosporon clinical isolates collected in 24 medical centres. Clin. Microbiol. Infect. 2019, 25, 909.e1–909.e5. [Google Scholar] [CrossRef]
  125. Lass-Florl, C.; Mayr, A.; Perkhofer, S.; Hinterberger, G.; Hausdorfer, J.; Speth, C.; Fille, M. Activities of antifungal agents against yeasts and filamentous fungi: Assessment according to the methodology of the European Committee on Antimicrobial Susceptibility Testing. Antimicrob. Agents. Chemother. 2008, 52, 3637–3641. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  126. Kozel, T.R.; Wickes, B. Fungal diagnostics. Cold Spring Harb. Perspect. Med. 2014, 4, a019299. [Google Scholar] [CrossRef] [PubMed]
  127. Buchan, B.W.; Ledeboer, N.A. Advances in identification of clinical yeast isolates by use of matrix-assisted laser desorption ionization-time of flight mass spectrometry. J. Clin. Microbiol. 2013, 51, 1359–1366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  128. Vidotto, V.; Guevara Ochoa, L.; Ponce, L.M.; Tello, G.M.; Prada, G.R.; Bruatto, M. Vaginal yeast flora of pregnant women in the Cusco region of Peru. Mycoses 1992, 35, 229–234. [Google Scholar] [CrossRef] [PubMed]
  129. Llovera Suárez, V.; Perurena Lancha, M.R. Identificación de levaduras de exudados vaginales: Características clínicas asociadas a la candidiasis. Rev. Cubana Med. Trop. 2004, 56, 21–25. [Google Scholar]
  130. Isa-Isa, R.; Cruz, A.C.; Arenas, R.; Duarte, Y.; Linares, C.M.; Bogaert, H. Pityriasis versicolor in infants under one year of age. A report of 92 cases. Rev. Iberoam. Micol. 2001, 18, 109–112. [Google Scholar]
  131. Farina-Gonzalez, N.; Acosta, R.; Samudio, M.; Adama, A.; Bolla, L.; Figueredo, L.; Giusiano, G. Malassezia species causative of pityriasis versicolor in Paraguay. Rev. Chilena Infectol. 2019, 36, 742–749. [Google Scholar] [CrossRef]
  132. Godoy-Vitorino, F.; Romaguera, J.; Zhao, C.; Vargas-Robles, D.; Ortiz-Morales, G.; Vazquez-Sanchez, F.; Sanchez-Vazquez, M.; de la Garza-Casillas, M.; Martinez-Ferrer, M.; White, J.R.; et al. Cervicovaginal fungi and bacteria associated with cervical intraepithelial neoplasia and high-risk human papillomavirus infections in a hispanic population. Front. Microbiol. 2018, 9, 2533. [Google Scholar] [CrossRef] [Green Version]
  133. Costa, R.L.; Moreira, J.; Lorenzo, A.; Lamas, C.C. Infectious complications following probiotic ingestion: A potentially underestimated problem? A systematic review of reports and case series. BMC Complement. Altern. Med. 2018, 18, 329. [Google Scholar] [CrossRef] [Green Version]
Jof 09 00747 g001 550
Figure 1. Number of cases of rare yeast infections, per million inhabitants, reported in eight Latin American countries between 1997 and 2022.
Figure 1. Number of cases of rare yeast infections, per million inhabitants, reported in eight Latin American countries between 1997 and 2022.
Jof 09 00747 g001
Jof 09 00747 g002 550
Figure 2. Distribution of species of rare yeasts reported to cause infection in Latin America.
Figure 2. Distribution of species of rare yeasts reported to cause infection in Latin America.
Jof 09 00747 g002
Table
Table 1. Demographic and clinical characteristics of patients from Latin America diagnosed with infections caused by rare yeasts.
Table 1. Demographic and clinical characteristics of patients from Latin America diagnosed with infections caused by rare yeasts.
Characteristic of PatientsNumber (%)
Sex (n = 247)
Male144 (58.3)
Female103 (41.7)
Underlying condition (n = 312)
Leukemia78 (25.0)
Central venous catheter58 (18.6)
Cancer48 (15.4)
Surgery36 (11.5)
Antibiotic use28 (9.0)
Mechanical ventilation 26 (8.3)
Solid organ transplantation23 (7.4)
Corticosteroid use21 (6.7)
Diabetes mellitus21 (6.7)
Human immunodeficiency virus17 (5.4)
Chemotherapy14 (4.5)
Hematopoietic stem cell transplant14 (4.5)
Urinary catheter14 (4.5)
COVID-199 (2.9)
Premature birth9 (2.9)
Other110 (35.3)
Diagnosis (n = 495)
Fungemia249 (50.3)
Invasive infection86 (17.4)
Urinary tract infection81 (16.4)
Other infections79 (16.0)
Treatment 1 (n = 213)
Amphotericin B125 (58.7)
Fluconazole65 (30.5)
Voriconazole40 (18.8)
Others19 (8.9)
None15 (7.0)
Outcome (n = 277)
Alive164 (59.2)
Dead113 (40.8)
1 Usage of the antifungal alone or in combination.
Table
Table 2. Multivariate analysis of characteristics associated with death among patients from Latin America diagnosed with infections caused by rare yeasts (n = 277).
Table 2. Multivariate analysis of characteristics associated with death among patients from Latin America diagnosed with infections caused by rare yeasts (n = 277).
Survived
n = 164		Died
n = 113		OR (95% CI)p-Value
SexMale63 (22.7%)39 (14.1%)0.792 [0.425–1.48]0.463
Female52 (18.8%)25 (9.0%)Reference
Missing data49 (17.7%)49 (17.7%)
AgeWith data101 (36.5%)57 (20.6%)--
Missing data63 (22.7%)56 (20.2%)--
Average in years (SD)30.38 (±23.37)43.94 (±25.18)-<0.001
Risk for each 1-unit increase1.02 [1.01–1.04]0.0013
DiagnosisFungemia78 (28.2%)92 (33.2%)23.59 [3.1–179.78]0.00229
Invasive infection56 (20.2%)12 (4.3%)4.36 [0.533–35.75]0.17
Urinary tract infection10 (3.6%)8 (2.9%)16 [1.75–146.31]0.0141
Other20 (7.2%)1 (0.4%)Reference
Species/
Genus		T. asahii21 (7.6%)74 (26.7%)11.28 [5.61–22.66]<0.0001
R. mucilaginosa17 (6.1%)10 (3.6%)2 [0.784–5.1]0.147
Rhodotorula27 (9.7%)5 (1.8%)0.593 [0.202–1.74]0.342
Trichosporon35 (12.6%)4 (1.4%)0.366 [0.116–1.15]0.0864
Other64 (23.1%)20 (7.2%)Reference
1 Folliculitis, oral and oropharyngeal infections.
Table
Table 3. Univariate analysis of characteristics associated with death among patients from Latin America diagnosed with infections caused by rare yeasts (n = 277).
Table 3. Univariate analysis of characteristics associated with death among patients from Latin America diagnosed with infections caused by rare yeasts (n = 277).
Survived
n = 164		Died
n = 113		OR (95% CI)p-Value
Underlying
condition		Leukemia30483.92 [1.65–9.33]0.00204
CVC35220.754 [0.317–1.8]0.524
Cancer32151.33 [0.521–3.4]0.55
Surgery3050.262 [0.0842–0.814]0.0206
Mechanical ventilation 8166.32 [0.887–45.04]0.0657
Antibiotic use9140.398 [0.0356–4.45]0.455
SOT1270.993 [0.306–3.22]0.991
Corticosteroid use4159.01 [1.55–52.29]0.0143
Diabetes mellitus1280.878 [0.251–3.07]0.838
Chemotherapy770.511 [0.124–2.1]0.352
HSCT1130.203 [0.0411–1.01]0.0511
Urinary catheter570.555 [0.0576–5.36]0.611
Bacteremia476.58 [1.54–28.04]0.0108
Other54330.946 [0.444–2.02]0.885
DiagnosisFungemia78924.77 [2.71–8.4]<0.001
Invasive infection56120.23 [0.12; 0.46]<0.001
Urinary tract infection1081.17 [0.45; 3.05]0.807
TreatmentAmphotericin B71541.19 [0.735–1.94]0.475
Fluconazole47280.841 [0.481–1.47]0.544
Voriconazole22181.19 [0.593–2.38]0.628
GenusTrichosporon79863.39 [1.99–5.76]<0.001
Rhodotorula51160.37 [0.2–0.7]0.003
Geotrichum1510.088 [0.011–0.68]0.003
Saccharomyces950.79 [0.26–2.43]0.785
CVC: Central venous catheter; SOT: Solid organ transplantation; HSCT: Hematopoietic stem cell transplant.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Gil, Ó.; Hernández-Pabón, J.C.; Tabares, B.; Lugo-Sánchez, C.; Firacative, C. Rare Yeasts in Latin America: Uncommon Yet Meaningful. J. Fungi 2023, 9, 747. https://doi.org/10.3390/jof9070747

AMA Style

Gil Ó, Hernández-Pabón JC, Tabares B, Lugo-Sánchez C, Firacative C. Rare Yeasts in Latin America: Uncommon Yet Meaningful. Journal of Fungi. 2023; 9(7):747. https://doi.org/10.3390/jof9070747

Chicago/Turabian Style

Gil, Óscar, Juan Camilo Hernández-Pabón, Bryan Tabares, Carlos Lugo-Sánchez, and Carolina Firacative. 2023. "Rare Yeasts in Latin America: Uncommon Yet Meaningful" Journal of Fungi 9, no. 7: 747. https://doi.org/10.3390/jof9070747

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop