Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates

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As human pathogens, several species of yeasts, mainly of the genus Candida and other closely related genera, are responsible for a great number of life-threatening infections. The occurrence of yeasts in cheeses, including pathogenic species, has been largely studied, yet the antifungal susceptibility of these microorganisms is rarely reported. Here, we identified the species and determined the antifungal susceptibility profile of 45 yeast Candida isolates recovered from artisanal cheeses from 20 cities in Boyacá, Colombia. Among the species, Pichia fermentans (28.9%) prevailed, followed by Pichia kudriavzevii (24.4%), Kluyveromyces marxianus (22.2%), Clavispora lusitaniae (11.1%), Candida inconspicua (6.7%) Candida parapsilosis (4.4%) and Meyerozyma guillermondii (2.2%). Notably, all seven species have been globally reported, to a greater or lesser extent, to cause fungemia and other invasive infections with high mortality rates. Remarkably, together with the intrinsically resistant P. kudriavzevii, most isolates of P. fermentans, C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Our findings highlight the importance of exploring the ecological niches of pathogenic yeasts, together with their antifungal susceptibility, considering that the emergence of resistance in non-commensal opportunistic pathogens poses a serious threat to public health." } { "@context": "http://schema.org", "@type": "BreadcrumbList", "itemListElement": [ { "@type": "ListItem", "position": "1", "item": { "@id": "https://f1000research.com/", "name": "Home" } }, { "@type": "ListItem", "position": "2", "item": { "@id": "https://f1000research.com/browse/articles", "name": "Browse" } }, { "@type": "ListItem", "position": "3", "item": { "@id": "https://f1000research.com/articles/13-789", "name": "Occurrence of pathogenic yeastspecies in artisanal cheeses from Boyacá,..." } } ] } Home Browse Occurrence of pathogenic yeastspecies in artisanal cheeses from Boyacá,... ALL Metrics - Views Downloads Get PDF Get XML Cite How to cite this article Sánchez Quitian ZA, Pérez Rozo GM and Firacative C. Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.12688/f1000research.152447.3 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. Close Copy Citation Details Export Export Citation Sciwheel EndNote Ref. Manager Bibtex ProCite Sente EXPORT Select a format first Track Share ▬ ✚ Brief Report Revised Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] Zilpa Adriana Sánchez Quitian https://orcid.org/0000-0003-3520-6976 1 , Guisell Mariana Pérez Rozo https://orcid.org/0009-0003-2680-578X 2 , Carolina Firacative https://orcid.org/0000-0001-7547-5172 3 Zilpa Adriana Sánchez Quitian https://orcid.org/0000-0003-3520-6976 1 , Guisell Mariana Pérez Rozo https://orcid.org/0009-0003-2680-578X 2 , Carolina Firacative https://orcid.org/0000-0001-7547-5172 3 PUBLISHED 04 Oct 2024 Author details Author details 1 Grupo de Investigación Núcleo, Facultad de Ciencias e Ingeniería, Departamento de Biología y Microbiología, Universidad de Boyacá, Tunja, Boyacá, Colombia 2 Programa de Bacteriología y Laboratorio Clínico, Facultad de Ciencias de la Salud, Universidad de Boyaca, Tunja, Boyacá, Colombia 3 Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia Zilpa Adriana Sánchez Quitian Roles: Conceptualization, Data Curation, Funding Acquisition, Investigation, Methodology, Resources, Supervision, Writing – Original Draft Preparation, Writing – Review & Editing Guisell Mariana Pérez Rozo Roles: Methodology, Writing – Review & Editing Carolina Firacative Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Methodology, Resources, Software, Writing – Original Draft Preparation, Writing – Review & Editing OPEN PEER REVIEW DETAILS REVIEWER STATUS Abstract Yeasts are widely known for their application in food production, but also because of their clinical significance. As human pathogens, several species of yeasts, mainly of the genus Candida and other closely related genera, are responsible for a great number of life-threatening infections. The occurrence of yeasts in cheeses, including pathogenic species, has been largely studied, yet the antifungal susceptibility of these microorganisms is rarely reported. Here, we identified the species and determined the antifungal susceptibility profile of 45 yeast Candida isolates recovered from artisanal cheeses from 20 cities in Boyacá, Colombia. Among the species, Pichia fermentans (28.9%) prevailed, followed by Pichia kudriavzevii (24.4%), Kluyveromyces marxianus (22.2%), Clavispora lusitaniae (11.1%), Candida inconspicua (6.7%) Candida parapsilosis (4.4%) and Meyerozyma guillermondii (2.2%). Notably, all seven species have been globally reported, to a greater or lesser extent, to cause fungemia and other invasive infections with high mortality rates. Remarkably, together with the intrinsically resistant P. kudriavzevii , most isolates of P. fermentans, C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Our findings highlight the importance of exploring the ecological niches of pathogenic yeasts, together with their antifungal susceptibility, considering that the emergence of resistance in non-commensal opportunistic pathogens poses a serious threat to public health. READ ALL READ LESS Keywords Antifungal, Antimicrobial resistance, Artisanal cheeses, Pathogenic yeasts, fluconazole Corresponding Author(s) Carolina Firacative ( [email protected] ) Close Corresponding author: Carolina Firacative Competing interests: No competing interests were disclosed. Grant information: This study was subsidized by funds from Universidad de Boyacá to Z.A.S.Q. and Universidad del Rosario to C.F. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2024 Sánchez Quitian ZA et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. How to cite: Sánchez Quitian ZA, Pérez Rozo GM and Firacative C. Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.12688/f1000research.152447.3 ) First published: 11 Jul 2024, 13 :789 ( https://doi.org/10.12688/f1000research.152447.1 ) Latest published: 04 Oct 2024, 13 :789 ( https://doi.org/10.12688/f1000research.152447.3 ) Revised Amendments from Version 2 The journal did not update the abstract and keywords of version 2, so these are revised here. The journal did not update the abstract and keywords of version 2, so these are revised here. See the authors' detailed response to the review by Anastasia Spiliopoulou See the authors' detailed response to the review by Maria Helena Figueiredo-Carvalho and Rowena Coelho READ REVIEWER RESPONSES Introduction The importance of yeasts is highlighted by their application in food production, as these fungi play a vital role in fermentation ( Maicas 2020 ). However, the clinical significance of yeasts has also been clearly established, considering that these microorganisms, as human pathogens, are able to cause life-threatening infections, particularly among older patients and those with an underlying serious condition associated with medical interventions, comorbidities or immunosuppression ( Firacative 2020 ). Moreover, as antifungal resistance emerges in several species of colonizing and environmental yeasts, management and treatment challenges for the infections that they cause also appear, which represents an even major problem to public health ( Fisher et al. 2022 ). Among the most prominent disease-causing fungi are the ascomycetous yeasts of the genus Candida , together with species of closely related genera formerly grouped in the “ Candida ” clade ( Kidd et al. 2023 ), which are responsible for the majority of cases of invasive fungal infection in hospital settings in the world, with some species having acquired or intrinsic resistance to commonly used antifungal drugs ( Bongomin et al. 2017 ; Lamoth et al. 2018 ). Given that several species of yeasts are frequently found not only in raw milk but also in surfaces and material related with cheese production, handling and manufacturing, the occurrence of these microorganisms in artisanal cheeses is broadly known ( Minervini et al. 2001 ; Mounier et al. 2006 ). In addition, the implications of the presence of a particular species of yeasts in these dairy products have been widely investigated, since some species can positively contribute to the characteristic taste and flavour of cheeses, while other species can spoil the product, causing off-flavours, softening, and bad odours, among others undesirable signs of spoilage ( Minervini et al. 2001 ; Suzzi et al. 2003 ; Fadda et al. 2004 ; Bintsis 2021 ). Interestingly, from the diverse assortment of yeast species that can be present in artisanal cheeses, not only species of Candida and closely related genera have been found, but also of the genera Geotrichum , Rhodotorula , Saccharomyces and Trichosporon , which, albeit uncommon, are increasingly causing severe disease in humans ( Bintsis 2021 ; Chen et al. 2021 ; Gil et al. 2023 ). While the instances of invasive yeast infections potentially acquired from food exposure and consumption are infrequent, these may be progressively observed, given that several emerging pathogenic yeasts species are commonly recovered from various environmental sources, including food, rather than from the normal mycobiota of humans ( Cooper Jr. 2010 ; Benedict et al. 2016 ). In Candida bloodstream infections (BSI), particularly, the gut has been suggested as the main source of endogenous acquisition, and although atypical Candida species are not usually part of the gastrointestinal mycobiota, these yeasts could be transient members of the gut, acquired during feeding ( Nucci Marcio and Anaissie 2001 ; Auchtung et al. 2018 ). As the number of patients at-risk for fungal infections increases, there is a concurrent dramatic upsurge in the number of known opportunistic fungal species that are able to cause disease. Therefore, studies like ours addressed to explore part of the wide diversity of ecological niches of human pathogenic yeasts are helpful to provide further insights into the distribution and expansion of these microorganisms. Moreover, to our knowledge, this is the first study establishing not only the occurrence but also the antifungal susceptibility of clinically relevant Candida species and closely related species recovered from artisanal cheeses, with the identification of resistant isolates, mainly to fluconazole. Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Pichia fermentans (formerly Candida lambica ), Pichia kudriavzevii (formerly Candida krusei ), Kluyveromyces marxianus (formerly Candida kefyr ), Clavispora lusitaniae (formerly Candida lusitaniae ), Candida inconspicua, Candida parapsilosis and Meyerozyma guilliermondii (formerly Candida guilliermondii ) ( Kidd et al. 2023 ). Of notice, C. parapsilosis and P. kudriavzevii are in the high and medium priority group, respectively, of the recently issued World Health Organization (WHO) fungal priority pathogens list ( WHO 2022 ). Methods Isolates Forty-five isolates of yeast species previously recovered from 29 artisanal cheeses in 20 cities in Boyacá, Colombia ( Figure 1 ) and belonging to the Collection of Fungi and Microorganisms of Universidad de Boyacá (UBCHM), were studied. A unique isolate of a yeast species was recovered from 15 cheeses, while two different isolates were recovered from 12 cheeses and three different isolates from two cheeses. Isolates were identified by matrix-assisted laser desorption/ionization time-off-flight (MALDI-TOF) mass spectrometry using the MALDI Biotyper ® (Bruker Daltonics Inc., Germany). Figure 1. Distribution of pathogenic yeast species recovered from artisanal cheeses in Boyacá, Colombia. Isolates were kept at -80 °C in 2 ml of 10% ultra-pure glycerol (Thermo Fisher Scientific, catalogue number 15514011) and were cultured in Sabouraud dextrose agar (SDA) (BD DIFCO, catalogue number 210950) at 35 °C for 24 h prior to the experiments. Antifungal susceptibility testing The colorimetric broth microdilution test, Sensititre ® YeastOne ® (Thermo Fisher Scientific, catalogue number YO9), was used to determine the susceptibility of the isolates to anidulafungin (AND), micafungin (MCF), caspofungin (CAS), 5-fluorocytosine (5FC), posaconazole (PCZ), voriconazole (VOR), itraconazole (ITZ), fluconazole (FCZ) and amphotericin B (AMB), which are lyophilized in each plate, following the manufacturer’s instructions. In brief, each isolate was grown on SDA for 24 h at 35 °C. Subsequently, a yeast inoculum was prepared, per isolate, in 5 ml of sterile water and adjusted to the 0.5 McFarland standard (1-5 × 10 6 cells/ml). From this cell suspension, 20 μl were mixed thoroughly with 11 ml of YeastOne ® inoculum broth (Thermo Fisher Scientific, catalogue number Y3462) to obtain a final concentration of 1.8-9 × 10 3 cells/ml. From the last suspension, 100 μl were served into each well of a Sensititre ® YeastOne ® plate. Plates were sealed and incubated at 35 °C for 24 h. Minimum inhibitory concentration (MIC) values were defined as the lowest concentration of each antifungal that prevented the development of a pink or fuchsia colour, this is, the first blue well (no growth) for amphotericin B, or the first purple well (growth inhibition) or blue well (no growth) for echinocandins, 5-fluorocytosine and azoles ( Espinel-Ingroff et al. 1999 ). The quality control strains of Candida krusei ATCC ® 6258 and Candida parapsilosis ATCC ® 22019 were used following the M27M44S guideline of the Clinical and Laboratory Standards Institute (CLSI) ( CLSI 2022 ). Susceptible or resistant isolates to certain antifungal drug were identified, when available, with the clinical breakpoints per species of Candida and per drug, as established by the CLSI and other studies on the antifungal susceptibility of rare yeasts ( Borman et al. 2019 ; CLSI 2022 ). Per species of yeast with five or more isolates, and per antifungal drug, the frequency of MIC values was determined and the geometric mean MIC was calculated. Using the Mann–Whitney test, the differences in MIC values between species were established, per antifungal drug, with the software GraphPad Prism 9 ( https://www.graphpad.com/ , La Jolla, CA, USA). p -values <0.05 were considered statistically significant. Results P. fermentans prevails among the species of yeasts recovered from artisanal cheeses Among the 45 isolates included in this study, seven species of Candida and other closely related genera were identified. From these, P. fermentans was the most common species, with 13 (28.9%) isolates, followed by P. kudriavzevii with 11 (24.4%), K. marxianus with 10 (22.2%), C. lusitaniae with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and M. guilliermondii with one (2.2%) isolate. From 10 cheeses with two isolates and the two cheeses with three isolates, two different species of yeasts were identified. The occurrence of the species did not differ depending on the city. Even though all seven species recovered from artisanal cheeses have been reported as human pathogens, C. parapsilosis, P. kudriavzevii and M. guilliermondii are of major clinical relevance, as they are responsible for larger proportions of cases of candidemia and other forms of invasive candidiasis in different countries around the world ( Table 1 ). To a lesser extent, C. lusitaniae , K. marxianus , C. inconspicua and P. fermentans have been identified causing invasive fungal infection in humans. Table 1. Ecological characteristic and estimated percentage causing invasive candidiasis of yeast species recovered from artisanal cheeses. Current name Previous name n (%) Ecology Percentage Pichia fermentans Candida lambica 13 (28.9%) Widely distributed in nature and often found in foods and fruit juice, as well as being associated with humans and animals. Infrequent Pichia kudriavzevii 1 Candida krusei 11 (24.4%) Widely distributed in nature often occurring in soil, on fruits and in various natural fermentations. 2.5–2.7% Kluyveromyces marxianus Candida kefyr 10 (22.2%) Mostly isolated from foods and beverages, especially dairy products, but also from decaying plant tissue and associated insects. 0.16% Clavispora lusitaniae Candida lusitaniae 5 (11.1%) The ecological niche is ill-defined. Recovered from necrotic cactus tissue and reported as the most abundant species in leaves from agave for tequila production. 1.1% Candida inconspicua None 3 (6.7%) A significant component of the yeast community in various cheeses. 0.049% Candida parapsilosis 2 None 2 (4.4%) Poorly understood. The species has been recovered sporadically from a variety of substrates and localities. 13–26.5%. Meyerozyma guilliermondii Candida guilliermondii 1 (2.2%) Widely distributed in nature. Recovered from insect frass, flowers, fruits and other food products. Opportunistic pathogen of animals. 0.79–6.5% 1 Medium and 2 high priority in the World Health Organization fungal priority pathogens list ( WHO 2022 ). Resistance to fluconazole was identified in various species of yeasts recovered from artisanal cheeses The majority of yeasts isolates from this study were susceptible to the echinocandins tested, to most azoles and to amphotericin B, according to the CLSI breakpoints and other studies ( Borman et al. 2019 ; CLSI 2022 ) ( Table 2 ). However, 12 isolates (92.3%) of P. fermentans , the most common species recovered, 10 (90.9%) of P. kudriavzevii , two (66.7%) of C. inconspicua and two (100%) of C. parapsilosis were resistant (R) to fluconazole (MIC ≥16 μg/ml) ( Figure 1 ). In addition, the 10 fluconazole resistant isolates of P. kudriavzevii had concomitantly decreased susceptibility to 5-fluorocytosine (MIC ≥8 μg/ml). Intermediate susceptibility to 5-fluorocytosine (MIC = 16 μg/ml) was as well identified in one (10%) isolate of K. marxianus ( Pfaller et al. 2002 ). Notably, fluconazole resistant isolates were identified in 16 (80%) of the 20 studied cities in Boyacá. Table 2. Distribution, per species and antifungal, of the minimum inhibitory concentration (MIC) values of yeasts isolates. No. of isolates at MIC value (μg/ml) 1 Antifungal 2 Species n GM 3 0.0078 0.0156 0.0313 0.0625 0.125 0.25 0.5 1 2 4 8 16 32 64 128 AND P. fermentans 13 0.02663 7 4 1 1 P. kudriavzevii 11 0.04858 5 5 1 K. marxianus 10 0.03125 4 2 4 C. lusitaniae 5 0.05441 1 4 C. inconspicua 3 - 3 C. parapsilosis 2 - 1 1 M. guilliermondii 1 - 1 MCF P. fermentans 13 0.04303 1 7 4 1 P. kudriavzevii 11 0.09715 1 4 4 2 K. marxianus 10 0.04123 1 7 1 1 C. lusitaniae 5 0.05441 1 4 C. inconspicua 3 - 1 2 C. parapsilosis 2 - 1 1 M. guilliermondii 1 - 1 CAS P. fermentans 13 0.06953 4 4 4 1 P. kudriavzevii 11 0.1943 1 2 8 K. marxianus 10 0.02062 1 5 3 1 C. lusitaniae 5 0.07179 4 1 C. inconspicua 3 - 3 C. parapsilosis 2 - 2 M. guilliermondii 1 - 1 5FC P. fermentans 13 0.5274 2 1 3 4 1 2 P. kudriavzevii 11 8 1 9 1 K. marxianus 10 0.134 7 1 1 1 C. lusitaniae 5 0.2872 3 1 1 C. inconspicua 3 - 1 1 1 C. parapsilosis 2 - 1 1 M. guilliermondii 1 - 1 PCZ P. fermentans 13 0.202 1 1 3 3 5 P. kudriavzevii 11 0.151 1 5 4 1 K. marxianus 10 0.01675 3 3 4 C. lusitaniae 5 0.0136 2 2 1 C. inconspicua 3 - 1 2 C. parapsilosis 2 - 2 M. guilliermondii 1 - 1 VOR P. fermentans 13 0.2781 2 2 4 2 3 P. kudriavzevii 11 0.3426 1 1 2 6 1 K. marxianus 10 0.007813 10 C. lusitaniae 5 0.001184 2 3 C. inconspicua 3 - 2 1 C. parapsilosis 2 - 2 M. guilliermondii 1 - 1 ITZ P. fermentans 13 0.101 1 1 3 4 4 P. kudriavzevii 11 0.1331 1 2 3 4 1 K. marxianus 10 0.02368 6 2 2 C. lusitaniae 5 0.03125 1 3 1 C. inconspicua 3 - 1 2 C. parapsilosis 2 - 2 M. guilliermondii 1 - 1 FCZ P. fermentans 13 37.55 1 1 6 4 1 P. kudriavzevii 11 26.49 1 2 5 3 K. marxianus 10 0.1539 7 3 C. lusitaniae 5 0.3789 2 3 C. inconspicua 3 - 1 1 1 C. parapsilosis 2 - 2 M. guilliermondii 1 - 1 AMB P. fermentans 13 0.1816 8 3 2 P. kudriavzevii 11 0.2663 6 2 3 K. marxianus 10 0.1768 8 1 1 C. lusitaniae 5 0.1436 4 1 C. inconspicua 3 - 2 1 C. parapsilosis 2 - 1 1 M. guilliermondii 1 - 1 1 The modal MIC for each distribution is underlined. Resistant isolates are in bold. 2 AND: anidulafungin; MCF: Micafungin; CAS: caspofungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; VOR: Voriconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: Amphotericin-B. 3 GM: Geometric mean in μg/ml calculated with five or more isolates. When comparing the geometric mean MIC among P. fermentans , P. kudriavzevii , K. marxianus and C. lusitaniae , per antifungal tested ( Table 2 ), it was possible to establish that P. kudriavzevii was less susceptible to caspofungin, micafungin and 5-fluorocytosine than P. fermentans , K. marxianus and C. lusitaniae ( p < 0.05). Additionally, both P. fermentans and P. kudriavzevii were less susceptible to anidulafungin and all azoles than K. marxianus and C. lusitaniae ( p < 0.05). The susceptibility of the studied isolates to amphotericin B did not differ depending on these four species of yeasts, with all studied isolates being susceptible to this polyene. Discussion The identification of nonclinical reservoirs of human pathogenic yeasts is of upmost importance, since these might serve as a source of transmission and dissemination of invasive disease. In fact, the full contribution of the environmental reservoirs of Candida species and closely related yeasts to the well documented shifting epidemiology of candidiasis worldwide, remains largely uncharacterized ( Lamoth et al. 2018 ). Here, we not only describe the occurrence of pathogenic yeast species from artisanal cheeses, but we also report the identification of about 60% of the isolates with resistance to fluconazole, some of them with concomitant reduced susceptibility to 5-fluorocytosine. In our study, P. fermenetans (formerly C. lambica ) was recovered in almost a third of samples, which is not surprising as this species was firstly isolated from butter milk in The Netherlands and since, it has been commonly encountered in different dairy products such as hard and white-brined cheeses as well as in fermented food ( Kurtzman et al. 2011 ; Bintsis 2021 ). Even though there have been very few cases of human disease by P. fermentans , this yeast has been able to cause fungemia, which is one of the most severe manifestations of invasive candidiasis, with high mortality rates ( Pfaller and Diekema 2004 ; Vervaeke et al. 2008 ; Noni et al. 2020 ). Moreover, the resistance to fluconazole that characterises the isolates of this species, which agrees with our findings, could hinder treatment and lead to an inappropriate management, hence to a poor prognosis in patients with these infections ( Borman et al. 2019 ). P. kudriavzevii (formerly C. krusei ), which has emerged in the last years as a significant opportunistic pathogen affecting patients with hematologic malignancies and transplant recipients worldwide ( Pfaller et al. 2008 ; Jamiu et al. 2021 ), was also commonly found in artisanal cheeses, as reported previously ( Wanderley et al. 2013 ; Banjara et al. 2015 ). In Colombia, P. kudriavzevii is the fifth most common yeast species causing BSI, accounting for about 2.2% of all cases, as occurring worldwide ( Pfaller and Diekema 2004 ; Cortes et al. 2020 ). Importantly, P. kudriavzevii has intrinsic resistance to fluconazole, as found in our isolates, reduced susceptibility to 5-fluorocytosine and is rapidly developing acquired resistance to other antifungal drugs, making it a multidrug-resistant pathogen, very difficult to treat ( Pfaller et al. 2002 , 2008 ). Another emerging pathogen causing BSI in patients with blood cancer is K. marxianus (formerly C. kefyr ) ( Reuter et al. 2005 ; Dufresne et al. 2014 ), which accounted for about 23% of isolates recovered from our artisanal cheeses. In a global study of candidemia, K. marxianus was the nineth most prevalent species of yeasts, causing 0.16% of all cases ( Pfaller and Diekema 2004 ), and its incidence was suggested to be influenced by exogenous exposure to yogurt and other milk products ( Dufresne et al. 2014 ). Even though the ecology of this yeast is not fully understood, K. marxianus has been occasionally recovered from blue-veined cheeses and other dairy foods, as well as from fruits, plant material and even plastic devices ( Kurtzman et al. 2011 ; Dufresne et al. 2014 ; Bintsis 2021 ). While resistance to antifungals is not common in K. marxianus , we report an isolate with intermediate susceptibility to 5-fluorocytosine, which emphasises the importance of monitoring the emergence of antifungal resistance in uncommon species ( Pfaller et al. 2002 ). Recovered from semi-hard, white brined and other cheeses, as well as from agave leaves ( Wanderley et al. 2013 ; Bintsis 2021 ), Clavispora lusitaniae (formerly Candida lusitaniae ) was the fourth most common species recovered in our study. Known for its low susceptibility to fluconazole and amphotericin B, and its ability to acquire antifungal drug resistance within days of treatment, this species has been recognized as a human pathogen for more than four decades ( Scott et al. 2023 ; Angiolella et al. 2024 ). In fact, in a global surveillance, C. lusitaniae accounted for about 1.1% of all the cases of candidemia, affecting mainly immunocompromised patients with underlying malignancies ( Pfaller and Diekema 2004 ). Commonly recovered from lactic products, including milk, cheeses, or butter ( Minervini et al. 2001 ; Suzzi et al. 2003 ; Bintsis 2021 ), C. inconspicua is a species that has been rarely recovered from clinical samples. Accounting for less than 0.05% of all cases of candidemia globally ( Pfaller and Diekema 2004 ), this yeast, together with other rare yeast species, shared the traits of being the cause of invasive infections and having high MIC values to fluconazole and azole derivatives ( Perez-Hansen et al. 2019 ), which difficult management. While C. parapsilosis has been isolated from cheeses and milk products ( Suzzi et al. 2003 ; Wanderley et al. 2013 ; Banjara et al. 2015 ; Fröhlich-Wyder et al. 2019 ), as reported herein, its relevance lies in the role of this species in healthcare. In Australia, Malaysia, and many countries of Europe and Latin America, including Colombia, C. parapsilosis is the second most important opportunistic pathogenic yeast, after Candida albicans , associated with intrahospital transmission, targeting neonates, immunosuppressed and patients with indwelling catheters ( Pfaller and Diekema 2004 ; Nucci et al. 2013 ; Pappas et al. 2018 ; Arendrup et al. 2023 ; Hernández-Pabón et al. 2024 ). Remarkably, fluconazole and voriconazole cross-resistance has been described in C. parapsilosis , therefore, affected patients should be treated ideally with an echinocandin, which many times are unavailable in resource-limited countries ( Cornely et al. 2012 ). Together with P. kudriavzevii , which was placed in the medium priority group, C. parapsilosis is in the high priority group of the WHO fungal priority pathogens list, highlighting the need to focus attention on the perceived public health importance of these species ( WHO 2022 ). M. guilliermondii (formerly C. guilliermondii ), which is most often associated with onychomycosis, is the fourth most frequent species causing invasive fungal infection in critically ill patients in Argentina, Honduras and Venezuela, fifth in Colombia ( Nucci et al. 2013 ) and the seventh cause of BSI by Candida species globally ( Pfaller and Diekema 2004 ). Unfortunately, resistance to amphotericin B, fluconazole and itraconazole, associated with treatment failure, and reduced susceptibility to several other classes of antifungals have been reported in M. guilliermondii isolates ( Pfaller et al. 2006 ). Although no specific clinical or environmental sources for infection have been identified, M. guilliermondii may be transmitted from patient to patient in the hospital, particularly among those with intravascular foreign bodies ( Pfaller et al. 2006 ). The emergence of uncommon, yet resistant, pathogenic Candida and other yeast species could be due to the selective pressure caused for a larger use of azole derivatives, particularly fluconazole, not only as antifungal prophylaxis but also as empirical therapeutics ( Pfaller and Diekema 2004 ). Given its low cost and low toxicity, fluconazole remains one of the most commonly prescribed antifungal drugs against candidemia and candidiasis ( Cornely et al. 2012 ). Moreover, the use of azoles as fungicides in agriculture, which can contribute to the appearance of antifungal-resistance in nature, is widely documented ( CDC 2019 ). The rise of species that are in addition resistant to other class of antifungals, including polyenes, flucytosine and echinocandins, makes these microorganisms multidrug-resistant, as it is the case of P. kudriavzevii , C. lusitaniae , and M. guilliermondii , among the yeast species reported here, which further increases the risk for human health. Therefore, early detection, including the identification of environmental sources and exogenous exposure, as well as accurate species identification, are crucial to contribute to infection control. Our study provides important data on the occurrence of pathogenic Candida and closely related species recovered from artisanal cheeses and on the antifungal susceptibility of these, which until now is rather limited. Data availability Underlying data is deposited in Figshare: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates. Doi: https://doi.org/10.6084/m9.figshare.26093389 ( Sánchez-Quitian et al. 2024 ). This project contains the following underlying data: - Raw Data.xlsx (antifungal susceptibility testing (AST) data for each isolate and per species with characteristics of each isolate). - Figure 1 (Map with the isolates). 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Comments on this article Comments (0) Version 3 VERSION 3 PUBLISHED 11 Jul 2024 ADD YOUR COMMENT Comment Author details Author details 1 Grupo de Investigación Núcleo, Facultad de Ciencias e Ingeniería, Departamento de Biología y Microbiología, Universidad de Boyacá, Tunja, Boyacá, Colombia 2 Programa de Bacteriología y Laboratorio Clínico, Facultad de Ciencias de la Salud, Universidad de Boyaca, Tunja, Boyacá, Colombia 3 Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia Zilpa Adriana Sánchez Quitian Roles: Conceptualization, Data Curation, Funding Acquisition, Investigation, Methodology, Resources, Supervision, Writing – Original Draft Preparation, Writing – Review & Editing Guisell Mariana Pérez Rozo Roles: Methodology, Writing – Review & Editing Carolina Firacative Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Methodology, Resources, Software, Writing – Original Draft Preparation, Writing – Review & Editing Competing interests No competing interests were disclosed. Grant information This study was subsidized by funds from Universidad de Boyacá to Z.A.S.Q. and Universidad del Rosario to C.F. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Article Versions (3) version 3 Revised Published: 04 Oct 2024, 13:789 https://doi.org/10.12688/f1000research.152447.3 version 2 Revised Published: 26 Sep 2024, 13:789 https://doi.org/10.12688/f1000research.152447.2 version 1 Published: 11 Jul 2024, 13:789 https://doi.org/10.12688/f1000research.152447.1 Copyright © 2024 Sánchez Quitian ZA et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Download Export To Sciwheel Bibtex EndNote ProCite Ref. Manager (RIS) Sente metrics Views Downloads F1000Research - - PubMed Central info_outline Data from PMC are received and updated monthly. - - Citations open_in_new 0 open_in_new 0 open_in_new SEE MORE DETAILS CITE how to cite this article Sánchez Quitian ZA, Pérez Rozo GM and Firacative C. Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.12688/f1000research.152447.3 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS track receive updates on this article Track an article to receive email alerts on any updates to this article. TRACK THIS ARTICLE Share Open Peer Review Current Reviewer Status: ? Key to Reviewer Statuses VIEW HIDE Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Version 3 VERSION 3 PUBLISHED 04 Oct 2024 Revised Views 0 Cite How to cite this report: Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172814.r329206 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v3#referee-response-329206 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 22 Oct 2024 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil Approved VIEWS 0 https://doi.org/10.5256/f1000research.172814.r329206 I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the ... Continue reading READ ALL I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. Competing Interests: No competing interests were disclosed. Reviewer Expertise: Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172814.r329206 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v3#referee-response-329206 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Respond or Comment COMMENT ON THIS REPORT Version 2 VERSION 2 PUBLISHED 26 Sep 2024 Revised Views 0 Cite How to cite this report: Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172175.r327176 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v2#referee-response-327176 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 28 Sep 2024 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil Approved with Reservations VIEWS 0 https://doi.org/10.5256/f1000research.172175.r327176 It's still not adequate. The suggested modifications need to be made ... Continue reading READ ALL It's still not adequate. The suggested modifications need to be made throughout the entire text, from the abstract and keywords to the discussion. Competing Interests: No competing interests were disclosed. Reviewer Expertise: Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however we have significant reservations, as outlined above. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172175.r327176 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v2#referee-response-327176 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Respond or Comment COMMENT ON THIS REPORT Version 1 VERSION 1 PUBLISHED 11 Jul 2024 Views 0 Cite How to cite this report: Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316497 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316497 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 16 Sep 2024 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil Approved with Reservations VIEWS 0 https://doi.org/10.5256/f1000research.167210.r316497 I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some ... Continue reading READ ALL I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Is the work clearly and accurately presented and does it cite the current literature? Partly Is the study design appropriate and is the work technically sound? Yes Are sufficient details of methods and analysis provided to allow replication by others? Yes If applicable, is the statistical analysis and its interpretation appropriate? I cannot comment. A qualified statistician is required. Are all the source data underlying the results available to ensure full reproducibility? Yes Are the conclusions drawn adequately supported by the results? Yes References 1. Kidd SE, Abdolrasouli A, Hagen F: Fungal Nomenclature: Managing Change is the Name of the Game. Open Forum Infect Dis . 2023; 10 (1): ofac559 PubMed Abstract | Publisher Full Text Competing Interests: No competing interests were disclosed. Reviewer Expertise: Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however we have significant reservations, as outlined above. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Figueiredo-Carvalho MH and Coelho R. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316497 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316497 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Author Response 26 Sep 2024 Carolina Firacative , Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia 26 Sep 2024 Author Response Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including ... Continue reading Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Answer : thanks to the reviewer for the time to read and evaluate the manuscript and for each of the valuable comments and suggestions. In the revised manuscript and along with this point-by-point response, we aimed to address all issues mentioned by the reviewer. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Answer : following the reviewer’s suggestion, the title was changed. Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Answer : thanks for the suggestion. We did not remove the name of the species; however, we modified the text to highlight that P. kudriavzevii is intrinsically resistant to FCZ. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Answer : following the reviewer’s suggestion, a keyword was changed. Instead of “ Candida ” we now include “Pathogenic yeasts” Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Answer : following the reviewer’s suggestion, we mention now the priority groups of C. parapsilosis and P. kudrizvzeveii . Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Answer : we followed the reviewer’s suggestion and changed “ Candida ” for “yeasts”. Also, through the text. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Answer : thanks to the reviewer for this question. AST was not conducted in duplicate as we followed carefully the manufacturer’s instructions and considered that the colorimetric method is comparable to the CLSI reference method for testing the susceptibility of Candida species, as reported several times. In addition, quality control was ensured by testing the CLSI-recommended quality control strains C. parapsilosis ATCC 22019 and C. krusei ATCC 6258, in each batch of the YeastOne plates. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Answer : thanks to the reviewer for noticing this. Even though P. kudrizvzeveii has been long recognized as intrinsically resistant to FCZ, we revised the definition of this term in the CLSI manual: “IR is defined as inherent or innate (not acquired) antimicrobial resistance, which is reflected in wild-type antimicrobial patterns of all OR ALMOST ALL representative of a species”. In addition, there are a few publications reporting that some isolates of P. kudrizvzeveii can still have a low MIC to this azole, so not always 100% of the isolates of the species are resistant. Badiee et al 2017 reported ranges of MIC values from 2 to >64 μg/ml, Hrabovsky et al. 2017, ranges from 2 to 256 μg/ml, in a review of Pfaller et al 2006, ranges from 4 to >64 μg/ml and Kaur et al 2020 reported resistance in only 40.5% of the isolates, among other publications. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Answer : the change was done accordingly. Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Answer : the changes were done accordingly in the text, table 2 and figure. Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Answer : thanks to the reviewer for the suggestion. However, we consider that the references are adequate. We added a new reference regarding the nomenclature of Candida . Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Answer : thanks to the reviewer for the time to read and evaluate the manuscript and for each of the valuable comments and suggestions. In the revised manuscript and along with this point-by-point response, we aimed to address all issues mentioned by the reviewer. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Answer : following the reviewer’s suggestion, the title was changed. Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Answer : thanks for the suggestion. We did not remove the name of the species; however, we modified the text to highlight that P. kudriavzevii is intrinsically resistant to FCZ. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Answer : following the reviewer’s suggestion, a keyword was changed. Instead of “ Candida ” we now include “Pathogenic yeasts” Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Answer : following the reviewer’s suggestion, we mention now the priority groups of C. parapsilosis and P. kudrizvzeveii . Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Answer : we followed the reviewer’s suggestion and changed “ Candida ” for “yeasts”. Also, through the text. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Answer : thanks to the reviewer for this question. AST was not conducted in duplicate as we followed carefully the manufacturer’s instructions and considered that the colorimetric method is comparable to the CLSI reference method for testing the susceptibility of Candida species, as reported several times. In addition, quality control was ensured by testing the CLSI-recommended quality control strains C. parapsilosis ATCC 22019 and C. krusei ATCC 6258, in each batch of the YeastOne plates. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Answer : thanks to the reviewer for noticing this. Even though P. kudrizvzeveii has been long recognized as intrinsically resistant to FCZ, we revised the definition of this term in the CLSI manual: “IR is defined as inherent or innate (not acquired) antimicrobial resistance, which is reflected in wild-type antimicrobial patterns of all OR ALMOST ALL representative of a species”. In addition, there are a few publications reporting that some isolates of P. kudrizvzeveii can still have a low MIC to this azole, so not always 100% of the isolates of the species are resistant. Badiee et al 2017 reported ranges of MIC values from 2 to >64 μg/ml, Hrabovsky et al. 2017, ranges from 2 to 256 μg/ml, in a review of Pfaller et al 2006, ranges from 4 to >64 μg/ml and Kaur et al 2020 reported resistance in only 40.5% of the isolates, among other publications. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Answer : the change was done accordingly. Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Answer : the changes were done accordingly in the text, table 2 and figure. Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Answer : thanks to the reviewer for the suggestion. However, we consider that the references are adequate. We added a new reference regarding the nomenclature of Candida . Competing Interests: No competing interests were disclosed. Close Report a concern Respond or Comment COMMENTS ON THIS REPORT Author Response 26 Sep 2024 Carolina Firacative , Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia 26 Sep 2024 Author Response Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including ... Continue reading Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Answer : thanks to the reviewer for the time to read and evaluate the manuscript and for each of the valuable comments and suggestions. In the revised manuscript and along with this point-by-point response, we aimed to address all issues mentioned by the reviewer. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Answer : following the reviewer’s suggestion, the title was changed. Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Answer : thanks for the suggestion. We did not remove the name of the species; however, we modified the text to highlight that P. kudriavzevii is intrinsically resistant to FCZ. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Answer : following the reviewer’s suggestion, a keyword was changed. Instead of “ Candida ” we now include “Pathogenic yeasts” Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Answer : following the reviewer’s suggestion, we mention now the priority groups of C. parapsilosis and P. kudrizvzeveii . Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Answer : we followed the reviewer’s suggestion and changed “ Candida ” for “yeasts”. Also, through the text. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Answer : thanks to the reviewer for this question. AST was not conducted in duplicate as we followed carefully the manufacturer’s instructions and considered that the colorimetric method is comparable to the CLSI reference method for testing the susceptibility of Candida species, as reported several times. In addition, quality control was ensured by testing the CLSI-recommended quality control strains C. parapsilosis ATCC 22019 and C. krusei ATCC 6258, in each batch of the YeastOne plates. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Answer : thanks to the reviewer for noticing this. Even though P. kudrizvzeveii has been long recognized as intrinsically resistant to FCZ, we revised the definition of this term in the CLSI manual: “IR is defined as inherent or innate (not acquired) antimicrobial resistance, which is reflected in wild-type antimicrobial patterns of all OR ALMOST ALL representative of a species”. In addition, there are a few publications reporting that some isolates of P. kudrizvzeveii can still have a low MIC to this azole, so not always 100% of the isolates of the species are resistant. Badiee et al 2017 reported ranges of MIC values from 2 to >64 μg/ml, Hrabovsky et al. 2017, ranges from 2 to 256 μg/ml, in a review of Pfaller et al 2006, ranges from 4 to >64 μg/ml and Kaur et al 2020 reported resistance in only 40.5% of the isolates, among other publications. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Answer : the change was done accordingly. Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Answer : the changes were done accordingly in the text, table 2 and figure. Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Answer : thanks to the reviewer for the suggestion. However, we consider that the references are adequate. We added a new reference regarding the nomenclature of Candida . Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Answer : thanks to the reviewer for the time to read and evaluate the manuscript and for each of the valuable comments and suggestions. In the revised manuscript and along with this point-by-point response, we aimed to address all issues mentioned by the reviewer. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Answer : following the reviewer’s suggestion, the title was changed. Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Answer : thanks for the suggestion. We did not remove the name of the species; however, we modified the text to highlight that P. kudriavzevii is intrinsically resistant to FCZ. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Answer : following the reviewer’s suggestion, a keyword was changed. Instead of “ Candida ” we now include “Pathogenic yeasts” Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Answer : following the reviewer’s suggestion, we mention now the priority groups of C. parapsilosis and P. kudrizvzeveii . Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Answer : we followed the reviewer’s suggestion and changed “ Candida ” for “yeasts”. Also, through the text. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Answer : thanks to the reviewer for this question. AST was not conducted in duplicate as we followed carefully the manufacturer’s instructions and considered that the colorimetric method is comparable to the CLSI reference method for testing the susceptibility of Candida species, as reported several times. In addition, quality control was ensured by testing the CLSI-recommended quality control strains C. parapsilosis ATCC 22019 and C. krusei ATCC 6258, in each batch of the YeastOne plates. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Answer : thanks to the reviewer for noticing this. Even though P. kudrizvzeveii has been long recognized as intrinsically resistant to FCZ, we revised the definition of this term in the CLSI manual: “IR is defined as inherent or innate (not acquired) antimicrobial resistance, which is reflected in wild-type antimicrobial patterns of all OR ALMOST ALL representative of a species”. In addition, there are a few publications reporting that some isolates of P. kudrizvzeveii can still have a low MIC to this azole, so not always 100% of the isolates of the species are resistant. Badiee et al 2017 reported ranges of MIC values from 2 to >64 μg/ml, Hrabovsky et al. 2017, ranges from 2 to 256 μg/ml, in a review of Pfaller et al 2006, ranges from 4 to >64 μg/ml and Kaur et al 2020 reported resistance in only 40.5% of the isolates, among other publications. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Answer : the change was done accordingly. Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Answer : the changes were done accordingly in the text, table 2 and figure. Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Answer : thanks to the reviewer for the suggestion. However, we consider that the references are adequate. We added a new reference regarding the nomenclature of Candida . Competing Interests: No competing interests were disclosed. Close Report a concern COMMENT ON THIS REPORT Views 0 Cite How to cite this report: Spiliopoulou A. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316495 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316495 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 29 Aug 2024 Anastasia Spiliopoulou , University General Hospital of Patras, Patras, Greece; Department of Microbiology, University of Patras, Patras, Greece Approved VIEWS 0 https://doi.org/10.5256/f1000research.167210.r316495 In this manuscript, authors have studied the presence of Candida isolates in artisanal cheeses produced in Boyaca, Colombia. Their findings are quite interesting as they isolated species such as Candida parapsilosis and C. krusei , that are quite commonly isolated in invasive ... Continue reading READ ALL In this manuscript, authors have studied the presence of Candida isolates in artisanal cheeses produced in Boyaca, Colombia. Their findings are quite interesting as they isolated species such as Candida parapsilosis and C. krusei , that are quite commonly isolated in invasive Candida human infections as well as other species, such as C. kefyr , C. guillermondii , C. lusitaniae etc that are more uncommonly encountered. It is well known that in many cases the source of candidiasis is the intestinal and colonization of certain Candida spp has been associated with invasive infections in certain patient groups. Moreover, antifungal resistance has spread in livestock farming, a finding that raises great concern. All these aspects are nicely presented and discussed in this work. Is the work clearly and accurately presented and does it cite the current literature? Yes Is the study design appropriate and is the work technically sound? Yes Are sufficient details of methods and analysis provided to allow replication by others? Yes If applicable, is the statistical analysis and its interpretation appropriate? Not applicable Are all the source data underlying the results available to ensure full reproducibility? No source data required Are the conclusions drawn adequately supported by the results? Yes Competing Interests: No competing interests were disclosed. Reviewer Expertise: Medical microbiology, Mycology, Antimicrobial resistance, Host-pathogen interactions I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Spiliopoulou A. Reviewer Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316495 ) The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316495 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Author Response 30 Aug 2024 Carolina Firacative , Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia 30 Aug 2024 Author Response Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Competing Interests: No competing interests were disclosed. Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Competing Interests: No competing interests were disclosed. Close Report a concern Respond or Comment COMMENTS ON THIS REPORT Author Response 30 Aug 2024 Carolina Firacative , Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia 30 Aug 2024 Author Response Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Competing Interests: No competing interests were disclosed. Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. Competing Interests: No competing interests were disclosed. Close Report a concern COMMENT ON THIS REPORT Comments on this article Comments (0) Version 3 VERSION 3 PUBLISHED 11 Jul 2024 ADD YOUR COMMENT Comment keyboard_arrow_left keyboard_arrow_right Open Peer Review Reviewer Status info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Reviewer Reports Invited Reviewers 1 2 Version 3 (revision) 04 Oct 24 read Version 2 (revision) 26 Sep 24 read Version 1 11 Jul 24 read read Anastasia Spiliopoulou , University General Hospital of Patras, Patras, Greece; University of Patras, Patras, Greece Maria Helena Figueiredo-Carvalho , Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Brazil Rowena Coelho , Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Brazil Comments on this article All Comments (0) Add a comment Sign up for content alerts Sign Up You are now signed up to receive this alert Browse by related subjects keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 22 Oct 2024 | for Version 3 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (0) Approved info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. Competing Interests No competing interests were disclosed. Reviewer Expertise Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. reply Respond to this report Responses (0) Figueiredo-Carvalho MH and Coelho R. Peer Review Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172814.r329206) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/13-789/v3#referee-response-329206 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 28 Sep 2024 | for Version 2 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (0) Approved With Reservations info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions It's still not adequate. The suggested modifications need to be made throughout the entire text, from the abstract and keywords to the discussion. Competing Interests No competing interests were disclosed. Reviewer Expertise Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however we have significant reservations, as outlined above. reply Respond to this report Responses (0) Figueiredo-Carvalho MH and Coelho R. Peer Review Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.172175.r327176) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/13-789/v2#referee-response-327176 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 16 Sep 2024 | for Version 1 Maria Helena Figueiredo-Carvalho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto Nacional de Infectologia Evandro Chagas (INI)/Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil Rowena Coelho , Laboratório de Micologia, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz., Instituto acional de Infectologia Evandro Chagas, Rio de Janeiro, Rio de Janeiro, Brazil 0 Views copyright © 2024 Figueiredo-Carvalho M et al. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (1) Approved With Reservations info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Is the work clearly and accurately presented and does it cite the current literature? Partly Is the study design appropriate and is the work technically sound? Yes Are sufficient details of methods and analysis provided to allow replication by others? Yes If applicable, is the statistical analysis and its interpretation appropriate? I cannot comment. A qualified statistician is required. Are all the source data underlying the results available to ensure full reproducibility? Yes Are the conclusions drawn adequately supported by the results? Yes References 1. Kidd SE, Abdolrasouli A, Hagen F: Fungal Nomenclature: Managing Change is the Name of the Game. Open Forum Infect Dis . 2023; 10 (1): ofac559 PubMed Abstract | Publisher Full Text Competing Interests No competing interests were disclosed. Reviewer Expertise Medical mycology We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however we have significant reservations, as outlined above. reply Respond to this report Responses (1) Author Response 26 Sep 2024 Carolina Firacative, Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia Reviewer 2. I have reviewed the manuscript submitted by Sánchez Quitian ZA, Pérez Rozo GM, and Firacative C which evaluated the occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. The manuscript was written clearly and objectively. However, some modifications are necessary. Answer : thanks to the reviewer for the time to read and evaluate the manuscript and for each of the valuable comments and suggestions. In the revised manuscript and along with this point-by-point response, we aimed to address all issues mentioned by the reviewer. Title Occurrence of pathogenic Candida species in artisanal cheeses from Boyacá, Colombia, including fluconazole-resistant isolates. Suggest Yeast Answer : following the reviewer’s suggestion, the title was changed. Abstract …Remarkably, most isolates of C. lambica C. krusei , C. inconspicua and C. parapsilosis were resistant to fluconazole, one of the most common drugs to treat candidiasis. Suggest Remove the species C. krusei . This species is intrinsically resistant to fluconazole. Answer : thanks for the suggestion. We did not remove the name of the species; however, we modified the text to highlight that P. kudriavzevii is intrinsically resistant to FCZ. Review all yeast species nomenclature. Kidd SE., 2023 [Ref-1] or MycoBank Current name Pichia fermentan s Previous name Candida lambica Pichia kudriavzevii ( Candida krusei )…. Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. Keywords antifungal, antimicrobial resistance, artisanal cheeses, Candida, fluconazole. Suggest Yeast species or Candida, Pichia, Meyrozyma, Clavispora, Kluyveromyces Answer : following the reviewer’s suggestion, a keyword was changed. Instead of “ Candida ” we now include “Pathogenic yeasts” Introduction: … Our study contributes to the little information regarding the epidemiology, ecology and antifungal susceptibility profiles of Candida lambica, Candida krusei, Candida kefyr, Candida lusitaniae, Candida inconspicua, Candida parapsilosis and Candida guillermondii , two of which are part of the recently issued World Health Organization (WHO) fungal priority pathogens list (WHO 2022). Suggest Candida parapsilosis and Pichia kudrizvzeveii ( Candida krusei ) hight and media priority group, respectively. Answer : following the reviewer’s suggestion, we mention now the priority groups of C. parapsilosis and P. kudrizvzeveii . Methods Isolates Figure 1. Distribution of pathogenic Candida species recovered from artisanal cheeses in Boyacá, Colombia. Suggest Distribution of pathogenic Yeast species recovered from artisanal cheeses in Boyacá, Colombia. Answer : we followed the reviewer’s suggestion and changed “ Candida ” for “yeasts”. Also, through the text. Antifungal susceptibility testing Was the antifungal test conducted in duplicate? Resistant isolates were found. Answer : thanks to the reviewer for this question. AST was not conducted in duplicate as we followed carefully the manufacturer’s instructions and considered that the colorimetric method is comparable to the CLSI reference method for testing the susceptibility of Candida species, as reported several times. In addition, quality control was ensured by testing the CLSI-recommended quality control strains C. parapsilosis ATCC 22019 and C. krusei ATCC 6258, in each batch of the YeastOne plates. Pichia kudrizvzeveii ( Candida krusei ) is intrinsically resistant to fluconazole. However, in your study, one isolate was sensitive. Answer : thanks to the reviewer for noticing this. Even though P. kudrizvzeveii has been long recognized as intrinsically resistant to FCZ, we revised the definition of this term in the CLSI manual: “IR is defined as inherent or innate (not acquired) antimicrobial resistance, which is reflected in wild-type antimicrobial patterns of all OR ALMOST ALL representative of a species”. In addition, there are a few publications reporting that some isolates of P. kudrizvzeveii can still have a low MIC to this azole, so not always 100% of the isolates of the species are resistant. Badiee et al 2017 reported ranges of MIC values from 2 to >64 μg/ml, Hrabovsky et al. 2017, ranges from 2 to 256 μg/ml, in a review of Pfaller et al 2006, ranges from 4 to >64 μg/ml and Kaur et al 2020 reported resistance in only 40.5% of the isolates, among other publications. Results …Among the 45 isolates included in this study, seven species of Candida were identified. From these, C. lambica (Pichia fermentans) was the most common species, with 13 (28.9%) isolates, followed by C. krusei ( Pichia kudriavzevii ) with 11 (24.4%), C. kefyr ( Kluyveromyces marxianus ) with 10 (22.2%), C. lusitaniae (Clavispora lusitaniae) with five (11.1%), C. inconspicua with three (6.7%), C. parapsilosis with two (4.4%) and C. guillermondii (Meyerozyma guilliermondii) with one (2.2%)… Suggest current name (previous name) Answer : thanks for the suggestion. We changed the names of all species through the text, keeping the current name according to Kidd et al. 2023. This reference is now included. The previous names are also mentioned in the introduction, table 1 and discussion. …To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing disease in humans. Suggest To a lesser extent, C. lusitaniae, C. kefyr, C. inconspicua and C. lambica have been identified causing invasive fungal infection in humans Answer : the change was done accordingly. Table 2 AND: anidulafungin; MF: Micafungin; CAS: caspofungin; FC: 5-fluorocytosine; PZ: Posaconazole; VOR: Voriconazole; IZ: Itraconazole; FZ: Fluconazole; AB: Amphotericin-B. Suggest MCF: Micafungin; 5FC: 5-fluorocytosine; PCZ: Posaconazole; ITZ: Itraconazole; FCZ: Fluconazole; AMB: amphotericin B Answer : the changes were done accordingly in the text, table 2 and figure. Discussion Update the references. In the discussion, the cited references are very outdated. I suggest using more up-to-date references on the species identified in this study. Answer : thanks to the reviewer for the suggestion. However, we consider that the references are adequate. We added a new reference regarding the nomenclature of Candida . View more View less Competing Interests No competing interests were disclosed. reply Respond Report a concern Figueiredo-Carvalho MH and Coelho R. Peer Review Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316497) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316497 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2024 Spiliopoulou A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 29 Aug 2024 | for Version 1 Anastasia Spiliopoulou , University General Hospital of Patras, Patras, Greece; Department of Microbiology, University of Patras, Patras, Greece 0 Views copyright © 2024 Spiliopoulou A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (1) Approved info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions In this manuscript, authors have studied the presence of Candida isolates in artisanal cheeses produced in Boyaca, Colombia. Their findings are quite interesting as they isolated species such as Candida parapsilosis and C. krusei , that are quite commonly isolated in invasive Candida human infections as well as other species, such as C. kefyr , C. guillermondii , C. lusitaniae etc that are more uncommonly encountered. It is well known that in many cases the source of candidiasis is the intestinal and colonization of certain Candida spp has been associated with invasive infections in certain patient groups. Moreover, antifungal resistance has spread in livestock farming, a finding that raises great concern. All these aspects are nicely presented and discussed in this work. Is the work clearly and accurately presented and does it cite the current literature? Yes Is the study design appropriate and is the work technically sound? Yes Are sufficient details of methods and analysis provided to allow replication by others? Yes If applicable, is the statistical analysis and its interpretation appropriate? Not applicable Are all the source data underlying the results available to ensure full reproducibility? No source data required Are the conclusions drawn adequately supported by the results? Yes Competing Interests No competing interests were disclosed. Reviewer Expertise Medical microbiology, Mycology, Antimicrobial resistance, Host-pathogen interactions I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. reply Respond to this report Responses (1) Author Response 30 Aug 2024 Carolina Firacative, Studies in Translational Microbiology and Emerging Diseases (MICROS) Research Group, School of Medicine and Health Sciences, Universidad del Rosario, Bogota, Colombia Thanks to the reviewer for the time to read and evaluate our manuscript and for each of the valuable comments. View more View less Competing Interests No competing interests were disclosed. reply Respond Report a concern Spiliopoulou A. Peer Review Report For: Occurrence of pathogenic yeast species in artisanal cheeses from Boyacá, Colombia, including fluconazole resistant isolates [version 3; peer review: 2 approved] . F1000Research 2024, 13 :789 ( https://doi.org/10.5256/f1000research.167210.r316495) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/13-789/v1#referee-response-316495 Alongside their report, reviewers assign a status to the article: Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. 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