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The Black Yeast Exophiala Dermatitidis and Other Selected Opportunistic Human Fungal Pathogens Spread from Dishwashers to Kitchens

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The Black Yeast Exophiala Dermatitidis and Other Selected Opportunistic Human Fungal Pathogens Spread from Dishwashers to Kitchens RESEARCH ARTICLE The Black Yeast Exophiala dermatitidis and Other Selected Opportunistic Human Fungal Pathogens Spread from Dishwashers to Kitchens Jerneja Zupančič1, Monika Novak Babič1, Polona Zalar1, Nina Gunde-Cimerman1,2* 1 Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia, 2 Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP), Ljubljana, Slovenia * [email protected] Abstract OPEN ACCESS We investigated the diversity and distribution of fungi in nine different sites inside 30 resi- dential dishwashers. In total, 503 fungal strains were isolated, which belong to 10 genera Citation: Zupančič J, Novak Babič M, Zalar P, Gunde-Cimerman N (2016) The Black Yeast and 84 species. Irrespective of the sampled site, 83% of the dishwashers were positive for Exophiala dermatitidis and Other Selected fungi. The most frequent opportunistic pathogenic species were Exophiala dermatitidis, Opportunistic Human Fungal Pathogens Spread from Candida parapsilosis sensu stricto, Exophiala phaeomuriformis, Fusarium dimerum, and Dishwashers to Kitchens. PLoS ONE 11(2): the Saprochaete/Magnusiomyces clade. The black yeast E. dermatitidis was detected in e0148166. doi:10.1371/journal.pone.0148166 47% of the dishwashers, primarily at the dishwasher rubber seals, at up to 106 CFU/cm2; Editor: Joy Sturtevant, Louisiana State University, the other fungi detected were in the range of 102 to 105 CFU/cm2. The other most heavily UNITED STATES contaminated dishwasher sites were side nozzles, doors and drains. Only F. dimerum was Received: June 18, 2015 isolated from washed dishes, while dishwasher waste water contained E. dermatitidis, Exo- Accepted: January 13, 2016 phiala oligosperma and Sarocladium killiense. Plumbing systems supplying water to house- Published: February 11, 2016 hold appliances represent the most probable route for contamination of dishwashers, as the Copyright: © 2016 Zupančič et al. This is an open fungi that represented the core dishwasher mycobiota were also detected in the tap water. access article distributed under the terms of the Hot aerosols from dishwashers contained the human opportunistic yeast C. parapsilosis, Creative Commons Attribution License, which permits Rhodotorula mucilaginosa and E. dermatitidis (as well as common air-borne genera such unrestricted use, distribution, and reproduction in any as Aspergillus, Penicillium, Trichoderma and Cladosporium). Comparison of fungal contam- medium, provided the original author and source are credited. ination of kitchens without and with dishwashers revealed that virtually all were contami- nated with fungi. In both cases, the most contaminated sites were the kitchen drain and the Data Availability Statement: All relevant data are within the paper. dish drying rack. The most important difference was higher prevalence of black yeasts (E. dermatitidis in particular) in kitchens with dishwashers. In kitchens without dishwashers, C. Funding: The authors acknowledge the financial support received from: Ministry of Higher Education, parapsilosis strongly prevailed with negligible occurrence of E. dermatitidis. F. dimerum Science and Technology of the Republic of Slovenia was isolated only from kitchens with dishwashers, while Saprochaete/Magnusiomyces iso- in corporation with Slovenia Research Agency, as a lates were only found within dishwashers. We conclude that dishwashers represent a reser- Young Researcher grant (JZ) (no. 382228-1/2013); voir of enriched opportunistic pathogenic species that can spread from the dishwasher into Ministry of Higher Education, Science and Technology and the University of Ljubljana via the the indoor biome. “Innovative scheme for co-financing of doctoral studies”, Contract No. 1244 (MNB); Slovenian Research Agency through the Infrastructural Centre PLOS ONE | DOI:10.1371/journal.pone.0148166 February 11, 2016 1/29 Fungi in Dishwasher and Kitchen Environment Mycosmo, MRIC UL and the grant P2-0103 (PZ); Introduction Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP); Over the last two decades, the incidence of fungal infections of humans has increased at an European Commission, via the grants ICT-2013- alarming rate, which already today presents a major challenge to health care systems. This corre- 612944 MAESTRA and ICT-2013-604102 HBP lates with the increased average age, the large number of people with treatable chronic diseases, (NGC). the growing population of immunocompromised individuals, and the practices of intensive che- Competing Interests: The authors report no motherapy and use of immunosuppressive drugs [1,2,3]. Although Candida albicans and Asper- conflicts of interest. The authors alone are gillus spp. are the most frequently encountered human opportunistic fungal pathogens, non- responsible for the content and the writing of the albicans Candida spp. (e.g., Candida glabrata, Candida krusei, Candida parapsilosis, Candida manuscript. dubliniensis) and different Fusarium spp. are also increasing in importance as emerging fungal pathogens. Indeed, 80% of all human fungal infections are caused by members of the Fusarium solani species complex (FSSC) and the Fusarium oxysporum species complex (FOSC) [1–4]. Humans are exposed to fungi outdoors and indoors. As people spend more than 80% of their time indoors on average [5], many studies have examined the relationships between hous- ing conditions and air-borne fungi, and how these relate to respiratory symptoms, such as asthma and fungal-related allergies [6–9]. Much less is known about potential risks associated with the presence of fungi in water-related parts of households such as bathrooms [10–12] and kitchens [13–15]. The few studies on the distribution of fungi in residential kitchens have focussed on contamination with outdoor air-borne fungi [16–18], and on contamination of bathrooms and kitchen sinks by fungal biofilms in plumbing systems [13–15,19]. There have been reports of increased frequency and relative abundance of Fusarium spp. and Exophiala spp. taxa, which are known for their thermo tolerance, acid tolerance, oligotro- phicity, and ability to metabolize surfactants [10–12]. Recent studies have showed that fungi also invade extreme kitchen environments, such as dishwashers [20,21]. Conditions inside dishwashers not only enable selected fungal species to survive, but also promote the selective enrichment of particular polyextremotolerant fungi that can tolerate low and high pH, temper- atures up to 60°C or 80°C, occasional dehydration and high organic loads, high concentrations of NaCl, and mechanical stress due to water ejectors. The human opportunistic pathogenic black yeast Exophiala dermatitidis and Exophiala phaeomuriformis have been detected in 35% of dishwashers examined around the world [20]. Other opportunistic pathogenic species that are consistently present are C. parapsilosis sensu stricto, Aureobasidium melanogenoum, Fusar- ium dimerum and Magnusiomyces capitatus [20,21]. Fungi that inhabit dishwashers may be released into the kitchen via aerosols and waste water, and by direct contact between contaminated surfaces and hands. Thus, dishwashers are possible sources of fungal contamination and subsequently infections. An especially endangered group are immunocompromised patients with cystic fibrosis, who are often infected with Aspergillus fumigatus, C. albicans, C. glabrata, C. parapsilosis, E. dermatitidis and Fusarium spp. [22–26]. Dishwashers have been investigated to date only for the presence of fungi on rubber seals [20, 21], while their distribution inside the dishwashers and their transfer into the kitchen envi- ronment has not been investigated. In the present study, we focussed on the presence of human opportunistic fungi in 9 locations within 30 randomly chosen household dishwashers and in the tap-water system connected to these dishwashers. Additionally, we examined the spread of these fungi into the kitchen via waste water, hot dishwasher aerosols, and contact with different surfaces and dishwasher-washed dishes. Materials and Methods Sampling In the autumn of 2013, 30 randomly selected dishwashers used in residential kitchens in seven Slovenian cities were sampled (Ljubljana, Velenje, Žalec, Celje, Mislinja, Sežana, and Portorož). PLOS ONE | DOI:10.1371/journal.pone.0148166 February 11, 2016 2/29 Fungi in Dishwasher and Kitchen Environment The dishwasher age (length of use) was from 1 year to 8 years, they were produced by four dif- ferent manufacturers, and they had different frequencies of use (i.e., from once a week, to twice per day) and cleaning processes (e.g., chemical, mechanical). Nine user-accessible sites inside each dishwasher were sampled: rubber seal, door, interior side wall, cutlery rack, detergent dis- penser, rinse-aid dispenser, dishwasher drain, side nozzle, and upper and lower sprinklers (Fig 1). The internal parts of a single dishwasher that are difficult to access by the user but are in contact with water were also sampled: the water inlet tube, temperature sensor, water purity sensor, circulation pump, waste water pump, ion exchanger, hydraulic tank, and waste-water Fig 1. Sampling sites in the dishwashers (A-H) and the prevailing taxa on the primary isolation plates (A.1-H.1) cultured from the particular dishwashers sampling sites swab samples. On rubber seal (A) and detergent dispenser (B) E. dermatitidis genotype A (A.1, B.1, respectively); on rinse-aid dispenser (C) E. dermatitidis
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