Open access peer-reviewed chapter

High Incidence of an Emerging Opportunistic Pathogen Candida parapsilosis in Water-Related Domestic Environments

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Jerneja Zupančič, Monika Novak Babič and Nina Gunde-Cimerman

Submitted: May 23rd, 2018 Reviewed: September 4th, 2018 Published: November 5th, 2018

DOI: 10.5772/intechopen.81313

From the Edited Volume

Fungal Infection

Edited by Érico Silva de Loreto and Juliana Simoni Moraes Tondolo

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Abstract

Candidiasis is one of the common fungal opportunistic infections, usually associated with diverse Candida species. Candida albicans, C. glabrata complex, C. parapsilosis complex, C. tropicalis and C. auris are often identified in affected patients. Candida parapsilosis sensu stricto is an emerging cause of hospital-acquired Candida infections, predominantly in Southern Europe, South America and Asia. Home environment is a less known source of infection despite frequent isolation of C. parapsilosis from kitchen surfaces and household appliances such as dishwashers, washing machines and refrigerators. C. parapsilosis is one of the first colonisers of novel dishwashers and a member of stable fungal communities on rubber seals worldwide in concentrations up to 102 CFU/cm2. It colonises also drawers for detergents in washing machines and drainage channels in refrigerators. Tap water and groundwater act as vector for entrance of C. parapsilosis in the indoor environments. Within C. parapsilosis, four clinically relevant phenotypes can be distinguished. Experimental data on the prevalence of C. parapsilosis isolates phenotypes, obtained from indoor environments, will be presented. Smooth phenotype prevails in dishwashers and washing machines, while crepe and crater dominate in water. In conclusion, the ability to colonise diverse environments and accordingly switch phenotypes defines C. parapsilosis as a versatile, domestic environment-related opportunistic pathogen.

Keywords

  • emerging opportunistic pathogen
  • water
  • household appliances
  • phenotype occurrence in domestic environments

1. Introduction

Yeast Candida parapsilosis sensu stricto (Ascomycota, Saccharomycetes, Saccharomycetales, Debaryomycetaceae) is the most commonly isolated species from C. parapsilosis complex, followed by its closest relative C. orthopsilosis and C. metapsilosis [1]. Its primary natural habitat remains undefined to date although it was recently reported from different fresh water sources [2, 3, 4] as well as from pine trees [5]. On the other hand, the presence of C. parapsilosis in relation to humans is well documented [1, 6]. The species is one of the asymptomatic colonisers of gastrointestinal and reproductive tract of most healthy humans [6]. In addition, it is commonly found on the skin and nails [1, 6]. Thus, the carriage and transfer of C. parapsilosis via hands of healthcare workers to patients have been for long recognised as a cause of opportunistic infections in hospitals [7]. The significance and prevalence of the yeast in clinical settings and samples dramatically increased during the past two decades, which ranks it among emerging opportunistic human pathogens [8]. C. parapsilosis is globally one of the most frequent non-albicans Candida (NAC) species causing a broad spectrum of infections from superficial to invasive candidiasis, including vulvovaginal infections, nosocomial bloodstream infections, pericarditis, endocarditis, endophthalmitis and sepsis [1, 9, 10, 11, 12]. Individuals at the highest risk for severe infection include neonates and patients in intensive care units [8]. Infections with C. parapsilosis are often related to contaminated catheters, due to its remarkable ability to produce biofilms on plastic and silicone surfaces of catheter instruments [6, 8, 13]. Ability for successful biofilm formation was linked with observed phenotypic differences of C. parapsilosis strains [14]. Among four described phenotypes (smooth, crepe, crater and concentric), the yeastlike smooth phenotype reportedly formed less biofilm in comparison to the entirely filamentous concentric phenotype [14].

In our study we focused on little known phenotypic diversity of C. parapsilosis strains, isolated from clinical material in comparison to those isolated from human-made indoor environments, particularly related to tap water and household appliances, such as washing machines, dishwashers and refrigerators. In addition, we discuss the ability for biofilm formation among tested strains and possible sources of infection originating from the household environment.

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2. Daily home-related activities pose an overlooked infection risk

The risk for infection caused by C. parapsilosis is reportedly the highest in hospitals and healthcare facilities, as C. parapsilosis is commonly transferred via hands of healthcare workers [1, 7]. However, recent discoveries reveal domestic environments as sites where people are exposed to this emerging pathogen on a daily basis. Exposure points include water and hygiene-related activities, cooking area and household appliances, like dishwashers, washing machines and refrigerators. C. parapsilosis was isolated in high frequencies from these areas, pointing towards its preference for indoor environment [4, 15, 16, 17, 18].

2.1 Water as a vector for transmission of Candida parapsilosis into household environment

In a modern society, microbiologically safe and potable water is not only one of the essential human rights but also remains one of the biggest concerns for the future [19]. Despite well-established water cleaning procedures, both, filamentous fungi and yeasts, are widely present in water intended for human consumption [19]. Except Swedish legislation, fungal parameters are not included in the present directives, and the lack of monitoring leaves out opportunistic and emerging fungal pathogens [19]. During the last 10 years, different water sources were identified as vectors for C. parapsilosis. Raw natural water, contaminated with C. parapsilosis, included streams [2], rivers [3], and groundwater [4]. Its presence positively correlated with the occurrence of dry season [3], the presence of middle-hard water type and nitrates [4, 18, 20]. Due to its ability to withstand filtration and chlorination process [21], C. parapsilosis is one of the building blocks in biofilms within municipal water systems, with the number of yeast cells in a range of 3.1–4.6 CFU/cm2 [22]. Consequently, C. parapsilosis is regularly present in tap water at consumers’ points, where it was isolated from 11 to 50% of samples [4, 17, 21, 23, 24]. Taps need thus to be taken into consideration as one of the important exposure points in households, where people may become infected with C. parapsilosis via drinking, food preparation and personal hygiene, like showering and bathing [19, 25].

2.2 Kitchens without dishwashers more likely host Candida parapsilosis

In every household, preparation and consumption of food cause dirty dishes, which can be cleaned manually or in a dishwasher. During the cleaning of kitchen utensils, the prewashing and washing steps are usually carried out using sponges in order to remove food residues. In due course, some food residues could adhere to the sponges and, together with retained humidity, tender a positive environment for growth and survival of pathogenic bacteria [26] and yeasts [27], including C. parapsilosis. From a microbiological point of view, kitchen surfaces are one of the most contaminated environments of our homes [17, 28, 29, 30]. Kitchen surfaces are not aseptic, but with proper cleaning, microorganisms may be reduced to the level that is generally recognised as safe. The most probable entryways of C. parapsilosis into domestic kitchen are water [4, 17] and human skin [15]. Adams et al. [15] reported that the highest incidence of C. parapsilosis is on the skin of the inhabitants (40%) and kitchen drains (25%) but the same yeast has a very low settle index on windowsills in kitchens (up to 2%). Zupančič et al. [17] reported the presence of C. parapsilosis on kitchen surfaces in high frequencies (up to 77% of tested kitchen surfaces were populated with C. parapsilosis). However, fungal diversity and occurrence varied considerably between kitchens containing dishwasher and kitchens without. The most significant difference was the presence of C. parapsilosis, which strongly dominated kitchens using handwashing only. The most contaminated sites in these kitchens were drain (43%), followed by dish drying rack and sink in the same occurrence (36%). Settlement index of C. parapsilosis on rubber seal in kitchen drain and kitchen counter did not exceed 25% [17].

2.3 Candida parapsilosis is the first coloniser of new dishwashers

In modern societies, dishwashers are a permanent utility in kitchens facilitating residents’ daily tasks. Washing in a dishwasher is usually carried out at high temperatures of 55–65°C, followed by a shorter hot water rinse cycle (~85°C) and the use of alkaline detergents. The mechanical power of water jets cleans the vessels [31]. The dishwashers do not disinfect the dishes, but reduce the number of microorganisms to a level that is considered safe [32]. The number of bacteria on the vessels is partly reduced due to high pH and temperature [33]. Recent studies have shown that under these unfavourable conditions, such as high temperature, wet and dry periods, high and low pH, presence of high concentrations of salt (NaCl) and water shearing forces, a certain group of microorganisms—polyextremotolerant ones—are enriched [34]. These unfavourable circumstances can defy also the opportunistic pathogenic species like C. parapsilosis [17], which seems to be one of the first colonisers of new dishwashers [20], providing a biotic surface for the construction of mixed bacterial-fungal biofilms [35]. C. parapsilosis forms together with Exophiala dermatitidis, Exophiala phaeomuriformis, Rhodotorula mucilaginosa, Aureobasidium melanogenum, Bisifusarium dimerum (formerly Fusarium dimerum), Fusarium oxysporum and Saprochaete clavata, a stable microbiota of dishwasher rubber seals worldwide [17, 34, 36, 37]. It is globally present on rubber seals of dishwashers [34, 36] with settlement up to 102 CFU/cm2 [17]. It can be found in high frequencies also on dishwasher doors and walls. Drains, cutlery racks and side nozzles are less exposed [17]. Higher dishwasher frequency of use (7–14 times per week) and connection to tap water system with moderately hard tap water hardness (1.5–2 mmol/l CaCO3) significantly affect the incidence of C. parapsilosis [20]. C. parapsilosis can be released from dishwashers via waste water, cleaned vessels and hot aerosols, formed at the end of the washing cycle [17].

2.4 The use of softeners increases the likelihood of Candida parapsilosis settlement inside washing machines

Knowledge on washing machines’ microbiomes is relevant particularly in hospitals and other healthcare facilities due to the possible transfer of pathogenic microorganisms between clothes being washed at the same time [38, 39]. Washing cycles at elevated temperatures may prevent cross-contamination lowering the number of microorganisms, but recent energy-saving trends promote washing with biodegradable detergents and usage of eco-programmes with temperatures of washing not exceeding 40°C [16]. These features favour microbial growth and propagation, resulting in persistent odour of textiles and elevated risk for infections [39, 40]. The main worries remain the bacteria of the genera Pseudomonas and Staphylococcus, together with dermatophyte fungi [38]. However, recent studies conducted globally reported C. parapsilosis as one of the most common fungi in washing machines, colonising 8–25% of sampled machines [16, 18, 41]. It was isolated mainly from biofilms at water-entry points, drawers for detergent and softener and rubber seals [16, 18, 41]. Its presence in washing machines positively correlated with the regular use of commercial softeners and washing temperatures ≤40°C [16]. Forty-eight percent of tested C. parapsilosis strains from washing machines showed a remarkable ability of biofilm formation, while none of the tested strains grew on 0.1% cycloheximide [18].

2.5 Candida parapsilosis colonises refrigerators’ rubber and moist parts

Primarily basidiomycetous yeasts but to a lesser extent also ascomycetous yeasts have been reported from extremely cold natural environments, including C. parapsilosis [42]. Extremely cold environments are also present indoors, in the form of refrigerators and freezers. Until date, there are no reports of yeasts, isolated from freezers, and few are reporting their isolation from refrigerators. Yeasts have been isolated from plastic refrigerator vegetable compartments, rubber seals, walls and water dispensers [43, 44]. Candida species have been isolated most frequently, with Pichia kudriavzevii prevailing in refrigerator air [45]. Our preliminary results showed the presence of C. parapsilosis on the shelves and in drainage channel of domestic refrigerators.

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3. Phenotypic diversity of Candida parapsilosis in domestic environments

Phenotypic diversity of C. parapsilosis was first described by Enger et al. [46] who identified five different phenotypes originating from one isolate (crepe, concentric, snowball, rough and smooth) [46]. They were later reidentified into four groups, crepe, concentric, smooth and crater, with a described ability to switch from one phenotype into another [14]. Phenotypic differences of the strains were linked with micromorphological features, growth rate and the ability to form biofilm [14]. The yeast cells of smooth phenotype grow most rapidly but form less biofilm in comparison to the crepe or crater phenotype. On the other hand, concentric phenotype produces entirely filamentous cells and forms biofilm most successfully (Table 1) [14].

3.1 Smooth phenotype of Candida parapsilosis prevails in domestic environment

One-hundred and eighty-four strains of C. parapsilosis sensu lato, deposited in Ex Culture Collection of the Infrastructural Centre Mycosmo, MRIC UL, Slovenia: http://www.ex-genebank.com/, at the Department of Biology, Biotechnical Faculty, University of Ljubljana, were included in the present study. Tested strains originated from clinical material (N = 7), groundwater (N = 2) and domestic environment, like tap water (N = 23), bathrooms (N = 14), washing machines (N = 16), kitchens (N = 22), dishwashers (N = 96) and refrigerators (N = 4). All strains were plated onto malt extract agar and incubated at 30°C for 4 weeks. Phenotypic diversity of the strains (Figure 1) was evaluated weekly (Table 2).

Figure 1.

C. parapsilosis phenotypes in domestic environment. (A) Crepe phenotype, (B) concentric phenotype, (C) crater phenotype and (D) smooth phenotype.

Phenotype propertiesPhenotypes
CrepeCraterConcentricSmooth
MicromorphologyPseudohyphaeElongated, yeastlikeWide, pseudohyphaeSmall, yeastlike
Chitin distributionCell wallCell wall, bud neckCell wall, bud neckBud scar
Growth rateMediumMediumLowHigh
Biofilm formation abilityMediumMediumHighLow

Table 1.

The main differences between four phenotypic groups of C. parapsilosis according to Laffey and Butler (2005) [14].

Environment
Clinical materialGroundwaterTap waterBathroomWashing machineKitchenDishwasherRefrigerator
PhenotypesCrepeEXF-10095; EXF-10098; EXF-10192; EXF-10193;EXF-8460; EXF-8247EXF-8404; EXF-8405; EXF-8452; EXF-9873; EXF-10048EXF-12615;
EXF-12765
EXF-6337;
EXF-8239
EXF-9920
EXF-9924
EXF-9925
EXF-9954
EXF-9574
EXF-8850; EXF-8854; EXF-8862; EXF-8907; EXF-8908; EXF-8909; EXF-8931; EXF-9096; EXF-9103; EXF-9105; EXF-9108; EXF-9112; EXF-9113; EXF-9190; EXF-9193; EXF-9207; EXF-9220; EXF-9251; EXF-9259; EXF-9311; EXF-9354; EXF-9355; EXF-9384; EXF-9386; EXF-9490; EXF-9491EXF-9596
CraterEXF-10096EXF-9872; EXF-10133; EXF-10144; EXF-10179; EXF-10240; EXF-9623; EXF-9693EXF-12671; EXF-9692EXF-9915
EXF-9960
EXF-12806
EXF-8892; EXF-8901; EXF-8905; EXF-8914; EXF-9081; EXF-9092; EXF-9106; EXF-9110; EXF-9330; EXF-9334
ConcentricEXF-10099EXF-5670; EXF-8411; EXF-8248EXF-6998EXF-6334EXF-9941;
EXF-9952;
EXF-9953; EXF-10087; EXF-8104
EXF-6078; EXF-8903; EXF-8937; EXF-8938; EXF-9045; EXF-9048; EXF-9099; EXF-9260; EXF-9280; EXF-9281; EXF-9283; EXF-9326; EXF-9342; EXF-9361; EXF-9389; EXF-9475; EXF-9496
SmoothEXF-10097EXF-8406; EXF-9899;
EXF-10058;
EXF-10067;
EXF-10174;
EXF-9691;
EXF-9694;
EXF-9697
EXF-6342; EXF-6356;
EXF-7001;
EXF-12776;
EXF-9696;
EXF-8101;
EXF-8146;
EXF-8149
EXF-5667; EXF-5730;
EXF-5731; EXF-8288;
EXF-8289; EXF-8290;
EXF-8296; EXF-9781;
EXF-9782; EXF-6335;
EXF-6336; EXF-6338;
EXF-8399
EXF-9907; EXF-9916;
EXF-9928; EXF-9944;
EXF-9955; EXF-9956
EXF-8111; EXF-9556
EXF-9557
EXF-8251; EXF-5540; EXF-5545; EXF-5547; EXF-5659; EXF-5717; EXF-5722; EXF-5723; EXF-5726; EXF-5728; EXF-6088; EXF-6102; EXF-6112; EXF-6120; EXF-6126; EXF-8849; EXF-8866; EXF-8867; EXF-8894; EXF-8919; EXF-9052; EXF-9054; EXF-9088; EXF-9095; EXF-9102; EXF-9200; EXF-9203; EXF-9206; EXF-9224; EXF-9275; EXF-9278; EXF-9340; EXF-9364; EXF-9370; EXF-9371; EXF-9395; EXF-9504; EXF-9509; EXF-9514; EXF-9535; EXF-9537; EXF-9769; EXF-9211EXF-11755;
EXF-12203;
EXF-12266

Table 2.

Phenotypic diversity of C. parapsilosis sensu stricto strains. EXF refers to culture collection strain designation.

Identification of yeasts from the C. parapsilosis complex can often be false or incorrect, since the species C. parapsilosis, C. metapsilosis and C. orthopsilosis are genetically very similar. Commercially available reagents currently do not allow accurate distinction within the C. parapsilosis complex [47]. One of the methods used for genetic differentiation between the complex species is also the analysis of the restriction polymorphism of the secondary alcohol dehydrogenase (SADH) gene [48]. After DNA extraction, identification based on the whole internal transcribed spacer (ITS) region and partial 28S rDNA, D1/D2 domains, was performed. All tested strains were checked for accurate identification of C. parapsilosis species complex by RFLP analyses of the SADH gene fragment. SADH amplicons obtained with the primer set S1F and S1R [49] were digested with the restriction enzyme BanI. All tested strains belonged to C. parapsilosis sensu stricto group.

Obtained results showed differences between abundance of phenotypes in clinical strains in comparison to the environmental strains (Figure 2). The prevalent phenotype among clinical strains was crepe (57.1%), while the others were evenly distributed (14.3%). The results are similar to already reported by Laffey and Butler [14]. Among environmental strains, the crepe phenotype was the only one observed in strains isolated from groundwater (2/2). It was represented in a lesser extent in household appliances, with the highest incidence on kitchen surfaces (22.7%) and in dishwashers (27.1%), and the lowest in washing machines (12.5%).

Figure 2.

Prevalence of C. parapsilosis phenotype in indoor environments and among clinical isolates. Prevailing indoor phenotype of C. parapsilosis is the smooth one; crepe phenotype is a predominant phenotype in clinical isolates.

C. parapsilosis strains isolated from groundwater-derived tap water mostly formed smooth (34.8%) or crater (30.4%) phenotypes, followed by crepe (21.7%) and concentric (13.0%) phenotype. Tap water serves as a vector for fungi entering water-related niches in households [4], where environmental pressure leads to the selection of the most tolerant strains [17], even on the phenotypic level. Room interior and household appliances that are usually present in these rooms (bathroom and washing machine, kitchen and dishwasher) show similar phenotype distribution (Figure 3). In addition, co-occurrence of different phenotypes from the same sampling spot was observed. Smooth phenotype was positively selected in all appliances, washing machine, refrigerator and dishwasher, with 81.3, 75.0 and 44.8%, respectively. Slightly positive selection was observed also for concentric phenotype in kitchens (22.7%) and inside dishwashers (17.7%) in comparison to bathrooms (7.1%) and washing machines (6.3%). On the other hand, negative selection was observed for crater phenotype, which was among all tested habitats most commonly found in tap water (30.4%), but its presence was low on kitchen (13.6%) and bathroom (14.3%) surfaces, with total absence in washing machines and refrigerators.

Figure 3.

Distribution of C. parapsilosis phenotypes in indoor environments. In clinical strains, crepe phenotype was prevailing, while in household appliances, such as washing machines, dishwashers and refrigerators, the predominant phenotype was smooth. Crepe phenotype was present to a lesser extent.

Survival of microorganisms invading household niches is higher due to biofilm formation [17]. Next-generation sequencing of dishwasher biofilm community and further usage of several statistical models showed that Candida (C. parapsilosis) is one of the first colonisers of rubber seals in dishwashers [20].

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4. Conclusions

C. parapsilosis is a commonly known opportunistic pathogen, particularly in a connection with hospital care, as a natural coloniser of health workers’ hands and skin. Superficial or invasive infections usually occur via catheters, due to yeast’s biofilm formation ability. Recent studies revealed human-made indoor environments as a previously unrecognised hot spot of their occurrence. This completely new aspect enables many possible routes for infection with this emerging opportunistic pathogen. C. parapsilosis is commonly present in tap water, bathrooms, washing machines, kitchens surfaces, dishwashers and refrigerators. While tap water carried all four phenotypes of the species, with a slight preference for the crater phenotype, selection inside household appliances clearly promoted the smooth phenotype. In accordance, the smooth phenotype showed the most abundant biofilm formation on polystyrene. On the other hand, tested clinical strains mainly formed the crepe phenotype, which was isolated also from all sampled indoor niches, with the highest incidence in kitchens, dishwashers and refrigerators. In the future, household environments where people maintain and prepare food and personal hygiene should be taken into consideration as possible routes for infection with C. parapsilosis.

4.1 Objectives

There are four different phenotypes of C. parapsilosis strains, smooth, crepe, crater and concentric. As C. parapsilosis is commonly present in domestic environment, we were interested in occurrence and prevalence of these phenotypes in different indoor environments.

4.2 Experimental methods used

All tested strains, stored in deep frozen stock (−80°C), were inoculated with a loop on malt extract agar plates (MEA) and incubated for 4 weeks at 30°C. Phenotype check-up was made after 1, 2, 3 and 4 weeks of incubation. Results of C. parapsilosis phenotype occurrence after 4 weeks are presented in Table 2.

4.2.1 Extraction and molecular characterisation of DNA

Pure fungal cultures were revived from deep frozen stock of EX culture collection by inoculation on a fresh malt extract agar medium. After 3 days of incubation at 30°C, the DNA was extracted using PrepMan Ultra reagent (Applied Biosystems), according to the manufacturer instructions.

Identification was based on amplification and sequencing of the large subunit ribosomal DNA sequences (LSU; partial 28S rDNA, D1/D2 domains), using the NL1 and NL4 primer set [50]. A fragment of the rDNA including internal transcribed spacer (ITS) region 1, 5.8S rDNA and ITS2 was also amplified and sequenced for identification, using the ITS5 and ITS4 primer set [51]. The ITS and LSU nucleotide sequences were determined by direct PCR sequencing, performed by Microsynth AG, Switzerland. BigDye terminator cycle sequencing kits were used in the sequence reactions (Applied Biosystems, Foster City, CA, USA). The sequences were obtained using an ABI Prism 3700 Big Dye Sequencer (Applied Biosystems). The sequences were assembled using FinchTV 1.4 (Geospiza, PerkinElmer, Inc.) and automatically and manually aligned using the Molecular Evolutionary Genetics Analysis (MEGA) software, version 6.06 [52]. The assembled DNA sequences were examined using the BLAST software of the National Center for Biotechnology Information (NCBI) database and were compared to the appropriate sequences of the reference and type strains. All strains, included into this research, were sequenced as C. parapsilosis sensu lato.

4.2.2 Determination of Candida parapsilosis species complex

Amplification of SADH gene was performed using S1F and S1R primer set according to [49]. After the final amplification, PCR products were treated with restriction enzyme BanI (BshNI) (Thermo Fisher Scientific™, USA) according to the manufacturer instructions. After restriction the obtained fragments were checked on 1% agarose gel (Sigma-Aldrich) for 20 minutes at 120 V. The expected fragment length for Candida metapsilosis was 400 bp, for Candida orthopsilosis was 700 bp and for Candida parapsilosis was 550 bp [49]. After restriction profile, all tested strains were determined as Candida parapsilosis sensu stricto.

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Acknowledgments

Infrastructural centre Mycosmo MRIC UL, the Culture Collection of Extremophilic Fungi (Ex) and Research Programme P1-0170 supported the work. The authors would like to thank also Dr. Tadeja Matos, MD, who provided clinical strains for the study, and Daša Janeš, Mag. Biochem., for helping with the identification of the strains.

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Conflict of interest

Authors declare no conflict of interest.

References

  1. 1. de Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of Clinical Fungi, Electronic Version 4.0. Utrecht: Centraalbureau voor Schimmelcultures; 2014. http://www.clinicalfungi.org/
  2. 2. Ayanbimpe MG, Abbah EV, Ior AC. Yeasts and yeast-like fungal contaminants of water used for domestic purposes in Jos, Nigeria. Microbiological Research. 2012;3:99-102
  3. 3. Medeiros OA, Missagia SB, Brandão RL, Callisto M, Barbosa ARF, Rosa AC. Water quality and diversity of yeasts from tropical lakes and rivers from the Rio Doce basin in Southeastern Brazil. Brazilian Journal of Microbiology. 2012;43(4):1582-1594
  4. 4. Novak Babič M, Zalar P, Ženko B, Džeroski S, Gunde-Cimerman N. Yeasts and yeast-like fungi in tap water and groundwater, and their transmission to household appliances. Fungal Ecology. 2016;20:30-39
  5. 5. Maganti H, Bartfai D, Xu J. Ecological structuring of yeasts associated with trees around Hamilton, Ontario, Canada. FEMS Yeast Research. 2012;12:9-19
  6. 6. Suhr MJ. Characterization and investigation of fungi inhabiting the gastrointestinal tract of healthy and diseased humans [thesis]. Lincoln: University of Nebraska; 2015
  7. 7. Huang YC, Lin TY, Leu HS, Wu JL, Chang HY. Yeast carriage on hands of hospital personnel working in intensive care units. The Journal of Hospital Infection. 1998;39:47-51
  8. 8. Trofa D, Gácser A, Nosanchuk JD. Candida parapsilosis, an emerging fungal pathogen. Clinical Microbiology Reviews. 2008;21(4):606-625. DOI: 10.1128/CMR.00013-08
  9. 9. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: A persistent public health problem. Clinical Microbiology Reviews. 2007;20(1):133-163
  10. 10. Laal Kargar M, Fooladi-Rad S, Mohammad Davoodi M, Khalilzadeh S, Hassanzad M, Mayahi S, et al. Fungal colonization in patients with cystic fibrosis. Journal of Mazandaran University of Medical Sciences. 2013;22(2):204-218
  11. 11. Bassetti M, Merelli M, Righi E, Diaz-Martin A, Rosello EM, Luzzati R, et al. Epidemiology, species distribution, antifungal susceptibility, and outcome of candidemia across five sites in Italy and Spain. Journal of Clinical Microbiology. 2013;51(12):4167-4172
  12. 12. Nucci M, Queiroz-Telles F, Alvarado-Matute T, Tiraboschi IN, Cortes J, Zurita J, et al. Epidemiology of candidemia in Latin America: A laboratory-based survey. PLoS One. 2013;8(3):e59373. DOI: 10.1371/journal.pone.0059373
  13. 13. Pires HR, dos Santos MJ, Zaia EJ, Gomes Martins HC, Mendes-Giannini SJM. Candida parapsilosis complex water isolates from a haemodialysis unit: Biofilm production and in vitro evaluation of the use of clinical antifungals. Memórias do Instituto Oswaldo Cruz. 2011;106(6):646-654
  14. 14. Laffey SF, Butler G. Phenotype switching affects biofilm formation by Candida parapsilosis. Microbiologica. 2005;151:1073-1081
  15. 15. Adams RI, Miletto M, Taylor JW, Bruns TD. The diversity and distribution of fungi on residential surfaces. PLoS One. 2013;8(11):e78866. DOI: 10.1371/journal.pone.0078866
  16. 16. Novak Babič M, Zalar P, Ženko B, Schroers HJ, Džeroski S, Gunde-Cimerman N. Candida and Fusarium species known as opportunistic human pathogens from customer-accessible parts of residential washing machines. Fungal Biology. 2015;119:95-113. DOI: 10.1016/j.funbio.2014.10.007
  17. 17. Zupančič J, Novak Babič M, Zalar P, Gunde-Cimerman N. The black yeast Exophiala dermatitidis and other selected opportunistic human fungal pathogens spread from dishwashers to kitchens. PLoS One. 2016;11:e014816
  18. 18. Dögen A, Sav H, Gonca S, Kaplan E, Ilkit M, Novak Babič M, et al. Candida parapsilosis in domestic laundry machines. Medical Mycology. 2017;55(8):813-819
  19. 19. Novak Babič M, Gunde-Cimerman N, Vargha M, Tischner Z, Magyar D, Veríssimo C, et al. Fungal contaminants in drinking water regulation? A tale of ecology, exposure, purification and clinical relevance. International Journal of Environmental Research and Public Health. 2017;14:636. DOI: 10.3390/ijerph14060636
  20. 20. Raghupathi PK, Zupančič J, Brejnrod AD, Jacquiod S, Houf K, Burmølle M, Gunde-Cimerman N, Sørensen SJ. 2018. Microbial diversity and putative opportunistic pathogens in dishwasher biofilm communities. Applied and Environmental Microbiology 84:e02755-17. https://doi.org/10.1128/AEM.02755-17
  21. 21. Shaker KB, Sharif MF. Isolation and identification of some fungi frome Al-Sader water treatment plant, Baghdad, Iraq. Al-Mustansiriyah Journal of Science. 2012;23(5):1-12
  22. 22. Doggett MS. Characterisation of fungal biofilms within a municipal water distribution system. Applied and Environmental Microbiology. 2000;66:1249-1251. DOI: 10.1128/AEM.66.3.1249-1251.2000
  23. 23. Yamaguchi UM, Rampazzo PCR, Yamada-Ogatta FS, Nakamura VC, Ueda-Nakamura T, del Filho DPB. Yeasts and filamentous fungi in bottled mineral water and tap water from municipal supplies. Brazilian Archives of Biology and Technology. 2007;50:1-9
  24. 24. Biedunkiewicz A, Kowalska K, Schulz Ł, Stojek K, Dynowska M, Ejdys E, et al. Mycological monitoring of selected aquatic ecosystems in the context of epidemiological hazards. Drinking water. Annals of Parasitology. 2014;60:191-198
  25. 25. Francesca N, Gagli R, Stucchi C, De Martino S, Moschetti G, Settanni L. Yeasts and moulds contaminants of food ice cubes and their survival in different drinks. Journal of Applied Microbiology. 2017;124:188-196
  26. 26. Mattick K, Durham K, Domingue G, Jørgensen F, Sen M, Schaffner DW, et al. The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. International Journal of Food Microbiology. 2003;85(3):213-226
  27. 27. Wolde T, Bacha K. Microbiological safety of kitchen sponges used in food establishments. International Journal of Food Sciences and Nutrition. 2016;2016:1659784. DOI: 10.1155/2016/1659784
  28. 28. Ojima M, Toshima Y, Koya E, Ara K, Kawai S, Ueda N. Bacterial contamination of Japanese households and related concern about sanitation. International Journal of Environmental Health Research. 2002;12:41-52
  29. 29. Sinclair RG, Gerba CP. Microbial contamination in kitchens and bathrooms of rural Cambodian village households. Letters in Applied Microbiology. 2011;52:144-149
  30. 30. Flores GE, Bates ST, Caporaso JG, Lauber CL, Leff JW, Knight R, et al. Diversity, distribution and sources of bacteria in residential kitchens. Environmental Microbiology. 2013;15:588-596
  31. 31. Ståhl Wernersson E, Johansson E, Håkanson H. Cross-contamination in dishwashers. The Journal of Hospital Infection. 2004;56:312-317
  32. 32. Nicolella C, Casini B, Rossi F, Chericoni A, Pardini G. Thermal sanitizing in a commercial dishwashing machine. Journal of Food Safety. 2011;31:81-90
  33. 33. Jeppsson M, Ståhl Wernersson E, Håkanson H. The effect of silver ions and chlorine on the survival of Staphylococcus aureus and Bacillus cereus in dishwater. Environmental Technology. 2007;28:1419-1427
  34. 34. Zalar P, Novak M, de Hoog GS, Gunde-Cimerman N. Dishwashers—A man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biology. 2011;115:997-1007
  35. 35. Zupančič J, Raghupathi PK, Houf K, Burmølle M, Sørensen SJ, Gunde-Cimerman N. Synergistic interactions in microbial biofilms facilitate the establishment of opportunistic pathogenic fungi in household dishwashers. Frontiers in Microbiology. 2018;9:21. DOI: 10.3389/fmicb.2018.00021
  36. 36. Döğen A, Kaplan E, Oksüz Z, Serin MS, Ilkit M, de Hoog GS. Dishwashers are a major source of human opportunistic yeast-like fungi in indoor environments in Mersin, Turkey. Medical Mycology. 2013;5:493-498
  37. 37. Gümral R, Özhak-Baysan B, Tümgör A, Saraçlı MA, Yıldıran ŞT, Ilkit M, et al. Dishwashers provide a selective extreme environment for human-opportunistic yeast-like fungi. Fungal Diversity. 2016;76:1-9
  38. 38. Bloomfield SF, Exner M, Nath KJ, Scott EA, Signorelli C. The Infection Risks Associated with Clothing and Household Linens in Home and Everyday Life Settings, and the Role of Laundry. Home Hygiene & Health. International Scientific Forum on Home Hygiene; 2011. p. 47
  39. 39. Bockmühl PD. Hygiene aspects in domestic laundry. Hygiene + Medizin. 2011;36:280-286
  40. 40. Stapleton K, Hill K, Day K, Perry DJ, Dean RJ. The potential impact of washing machines on laundry malodour generation. Letters in Applied Microbiology. 2013;56:299-306
  41. 41. Nix DI, Frontzek A, Bockmühl PD. Characterization of microbial communities in household washing machines. Tenside, Surfactants, Detergents. 2015;52(6):433-440
  42. 42. Butinar L, Strmole T, Gunde-Cimerman N. Relative incidence of ascomycetous yeasts in arctic coastal environments. Microbial Ecology. 2011;61(4):832-843. DOI: 10.1007/s00248-010-9794-3
  43. 43. NSF. The Public Health and Safety Organization. International Household Germ Study [Internet]. 2013. Available from: https://www.nsf.org/newsroom_pdf/2013_germ_study_FOR-WEB-ONLY.pdf [Accessed: November 21, 2016]
  44. 44. Catellani P, Miotti Scapin R, Alberghini L, Radu IL, Giaccone V. Levels of microbial contamination of domestic refrigerators in Italy. Food Control. 2014;42:257-262
  45. 45. Altunatmaz SS, Issa G, Aydin A. Detection of airborne psychrotrophic bacteria and fungi in food storage refrigerators. Brazilian Journal of Microbiology. 2012;43:1436-1443
  46. 46. Enger L, Joly S, Pujol C, Simonson P, Pfaller M, Soll DR. Cloning and characterization of a complex DNA fingerprinting probe for Candida parapsilosis. Journal of Clinical Microbiology. 2001;39:658-669
  47. 47. Roy B, Meyer SA. Confirmation of the distinct genotype groups within the form species Candida parapsilosis. Journal of Clinical Microbiology. 1998;36:216-218
  48. 48. Tavanti A, Hensgens LA, Ghelardi E, Campa M, Senesi S. Genotyping of Candida orthopsilosis clinical isolates by amplification fragment length polymorphism reveals genetic diversity among independent isolates and strain maintenance within patients. Journal of Clinical Microbiology. 2007;45:1455-1462
  49. 49. Tavanti A, Davidson AD, Gow NA, Maiden MC, Odds FC. Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. Journal of Clinical Microbiology. 2005;43:284-292
  50. 50. Boekhout T, Kurtzman CP. Principles and methods used in yeast classification and an overview of currently accepted yeast genera. In: Wolf K, editor. Non-conventional Yeasts in Biotechnology. Berlin/Heidelberg: Springer; 1996. pp. 1-81
  51. 51. White TJ, Bruns T, Lee S, Taylor WJ. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Ninsky JJ, White TJ, editors. PCR Protocols: A Guide to Methods and Applications. New York: Academic Press, Inc.; 1990. pp. 315-322
  52. 52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. 2013;30:2725-2729

Written By

Jerneja Zupančič, Monika Novak Babič and Nina Gunde-Cimerman

Submitted: May 23rd, 2018 Reviewed: September 4th, 2018 Published: November 5th, 2018