Next Article in Journal
Substrate-Induced Response in Biogas Process Performance and Microbial Community Relates Back to Inoculum Source
Next Article in Special Issue
The Protean Acremonium. A. sclerotigenum/egyptiacum: Revision, Food Contaminant, and Human Disease
Previous Article in Journal
The Interaction of the Gut Microbiota with the Mucus Barrier in Health and Disease in Human
Previous Article in Special Issue
Human Pathogenic Paecilomyces from Food
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Opportunistic Water-Borne Human Pathogenic Filamentous Fungi Unreported from Food

1
Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia
2
Department of Environmental Health, National Institute of Health Doutor Ricardo Jorge, Av. Padre Cruz, 1649-016 Lisboa, Portugal
*
Author to whom correspondence should be addressed.
Microorganisms 2018, 6(3), 79; https://doi.org/10.3390/microorganisms6030079
Received: 14 June 2018 / Revised: 2 August 2018 / Accepted: 2 August 2018 / Published: 3 August 2018

Abstract

:
Clean drinking water and sanitation are fundamental human rights recognized by the United Nations (UN) General Assembly and the Human Rights Council in 2010 (Resolution 64/292). In modern societies, water is not related only to drinking, it is also widely used for personal and home hygiene, and leisure. Ongoing human population and subsequent environmental stressors challenge the current standards on safe drinking and recreational water, requiring regular updating. Also, a changing Earth and its increasingly frequent extreme weather events and climatic changes underpin the necessity to adjust regulation to a risk-based approach. Although fungi were never introduced to water quality regulations, the incidence of fungal infections worldwide is growing, and changes in antimicrobial resistance patterns are taking place. The presence of fungi in different types of water has been thoroughly investigated during the past 30 years only in Europe, and more than 400 different species were reported from ground-, surface-, and tap-water. The most frequently reported fungi, however, were not waterborne, but are frequently related to soil, air, and food. This review focuses on waterborne filamentous fungi, unreported from food, that offer a pathogenic potential.

1. Water in Natural and Anthropogenic Environments

Fresh water, one of our essential needs, is valuable not only for drinking, but also as one of the driving forces for the development of humankind [1]. As such, it must be accessible and safe, especially in overpopulated areas, where pollution occurs more frequently [2]. Fresh water may be divided depending on the location, flow, and anthropogenic influence into different types: groundwater, surface water (streams, rivers, lakes), and tap-water [1,3,4]. Influenced by specific physio-chemical characteristics, their microbial populations differ [4]. The most important natural and anthropogenic abiotic and biotic factors influencing microbial presence in different water sources, include location of the main water source, water flow, ion composition, presence of organic matter, pollution rate, and water cleaning processes (Table 1) [1,3]. The latter are particularly important to maintain safe drinking and recreational water, preventing outbreaks of (mainly) gastrointestinal illnesses or irritation due to chemicals [2]. Chemical and microbiological parameters are listed in regulations covering quality of different water sources depending on water usage [1]. In Europe, the main documents regulating water quality are the Drinking Water Directive (98/83/CE), the Directive 2009/54/EC on mineral water and spring water, and Council Directive 76/160/EEC for bathing water. Whilst these documents successfully control and prevent the spreading of gastrointestinal illnesses (mainly attributed to bacteria and viruses), they leave out monitoring of causative agents of opportunistic fungal infections [1]. Only in Europe, over the last 30 years, more than 400 different fungal species have been reported from groundwater, surface water, and drinking water; among which 46 were classified as Biosafety Level 2 [1].
However, the majority of reported fungal species were not related exclusively to water, but they can be found also in air, soil, and food [1,5]. Food-related opportunistic filamentous fungi, isolated also from water, included those from the genera Acremonium, Alternaria, Aspergillus, Chaetomium, Fusarium, Mucor, Lichtheimia, Paecilomyces, Penicillium, Phoma, Scopulariopsis, and Trichoderma [1,5]. Paterson and Lima (2017) discussed their presence on food, and their medical relevance, in detail [5]. The present paper thus focuses only on opportunistic filamentous fungi related to water, and not reported from food [5].

2. Water-Related Filamentous Fungi as Causative Agents of Opportunistic Infections

Different types of water carry diverse fungal biota, but some species are more likely connected to the specific water type. For instance, surface water sources harbor fungi that are mainly associated with plants and their debris, and causative agents of plant diseases, such as representatives from Botrytis and Cylindrocarpon [1,3]. Similarly, melanised fungi from Aureobasidium, Exophiala, and Rhinocladiella are mainly associated with groundwater [1,6]. Knowing the origin of waterborne opportunistic fungi is of a great importance for health risk assessments. Reports related to fungal diseases are numerous, primarily due to the increasing number of transitory and serious immune alterations, particularly among people who spend a long time in hospital or other healthcare facilities [7,8]. Reports include allergies, opportunistic infections and intoxications [7,8]. Skin-related diseases, however, are the most common outcome of fungal infections, with an estimated number of patients on a global scale of over one billion [9]. Infections with filamentous fungi from water may occur in different ways—via exposure during sport and recreation, drinking, and personal and home hygiene, including aerosol intake from breathing during showering [1].
The present work focuses on reports on filamentous fungi with opportunistic potential isolated from water during the last five years. The most abundant waterborne filamentous fungi belong to the phylum Ascomycota, followed by species from the phylum Mucoromycota. Basidiomycota phylum does not contain exclusively waterborne species of filamentous fungi [10].

2.1. Filamentous Opportunistic Fungi with Possible Groundwater Origin

Groundwater is rarely directly associated with fungal diseases, due to its restricted public access, but it serves as a vector for fungal cells and spores during the preparation of groundwater-derived tap-water. The presence of fungi in groundwater can thus affect the tap-water quality and this poses a health risk during tap-water-related activities [1,6,11,12] (Table 2). As reported by Novak Babič et al. (2017), groundwater derived tap-water will more likely harbor species from Verticillium and different melanised fungi. Among them, fungi from Cyphellophora (former members of Phialophora) and Exophiala were the most commonly encountered [1] (Table 2). All currently known species within Verticillium (Plectosphaerellaceae) are opportunistic or true plant pathogens, and despite being commonly detected in water, they do not present a significant health risk for humans [13]. Melanised fungi from Cyphellophora (Cyphellophoraceae) have a more diverse ecology. They have been linked to humid indoor niches, swimming facilities, but also to plant and human diseases. They mainly cause surface infections of skin and nails [14,15] (Table 2). Yet, Exophiala (Herpotrichiellaceae) includes many water-related opportunistic pathogens, most of them classified under Biosafety Level 2 [8,15]. Recent literature reported on the presence of E. castellanii, E. dermatitidis, E. jeanselmei, E. oligosperma, E. phaeomuriformis and E. spinifera mainly from groundwater and groundwater derived tap-water, pointing towards groundwater as a possible source of these black fungi [6,12,16,17] (Table 2). Exophiala are associated with diverse spectra of opportunistic diseases such as otitis, keratitis, phaeohyphomycosis, and respiratory, cutaneous, and subcutaneous infections. Although rare, disseminated, systemic, and cerebral infections can be fatal [8].

2.2. Filamentous Opportunistic Fungi with Possible Origin from Surface Water

Surface water include streams, rivers, and lakes that can be used for preparation of drinking water, but they may also serve recreational purposes [26,40,41]. During recreational activities, people are exposed to fungi via direct skin contact and through inhalation of aerosols [1]. The latest literature links surface water with the presence of ascomycetous species of Cylindrocarpon, Microsporum, Phialemonium, Rhinocladiella, and fungi from subphylum Mucoromycotina (Table 2) [19,26,35]. Cylindrocarpon (Nectriaceae) species are closely related to Fusarium and Nectria, and are causative agents of plant and trees diseases [42]. Human-related infections were rarely reported and they usually occur after trauma. They include mycetoma, cutaneous infections, and keratitis [8]. Species of Phialemonium (Cephalothecaceae) are commonly found in air, soil, and polluted or industrial water [43], but have also been detected in drinking water (Table 2). Their presence in tap-water could have a surface water origin. They are opportunistic pathogens, reported to cause endocarditis, keratitis, and peritonitis, respiratory, subcutaneous, and systemic infections [8]. Also close relatives of Exophiala, black filamentous fungi Rhinocladiella (Herpotrichiellaceae) were isolated from both groundwater and surface water, and they are one of the common contaminants of drinking water [6,12,17,26,33] (Table 2). They can cause chromoblastomycosis and cutaneous infections, particularly in tropical and sub-tropical regions [8]. Surface water can be a possible vector for the transmission of dermatophytes Microsporum (Arthrodermataceae) [27,28,29]. Microsporum species are causative agents of different tineas (Table 2) and they are highly transmittable between animal hosts and people [8]. The highest degree of infections has been reported for children under the age of nine [8]. Also, Cunninghamella (Cunninghamellaceae), Rhizopus (Rhizopodaceae), and Rhizomucor (Lichtheimiaceae) species, classified in subphylum Mucoromycotina, are commonly associated with surface water (Table 2), due to their ability to degrade plants and debris [44]. Although members of these genera can additionally cause diseases in insects, they may colonize also other animals and humans. According to the revised taxonomy, fungi causing mucormycosis are classified in the phylum Mucoromycota, and subphylum Mucoromycotina. Representative taxa within Rhizopus, Mucor, Lichtheimia (formerly Absidia), Cunninghamella, Rhizomucor, and Saksenaea constitute those that are identified as causative agents of the majority of cases of mucormycosis [45]. Approximately half of all mucormycosis cases are caused by Rhizopus spp. [46]. Mucormycoses in humans are limited to severely immuno-compromised people, those with diabetes mellitus, or those after experiencing trauma [44]. Clinical manifestations include disseminated, cutaneous, subcutaneous, respiratory, and rhinocerebral infections (Table 2) [8].
One of the most serious fungal infections of the lungs and brain that may afflict patients follows exposure by near–drowning events due to inhalation of contaminated water [47,48]. The most common fungi associated with near-drowning syndrome belong to the Scedosporium apiospermum complex (Microascaceae), including fungi Pseudallescheria and its anamorph Scedosporium [21]. The disease develops slowly, and only after several weeks or months do cerebral abscesses or pulmonary infection appear, often with a fatal outcome [47,48]. Fungi from Scedosporium apiospermum complex were also related to otitis, subcutaneous, and disseminated infections (Table 2) [8]. Another accidental exposure to fungi originating from surface water can occur after natural disasters, like floods. Stachybotrys chartarum and S. ramosus (Stachybotryaceae) are particularly associated with sick building syndrome, often developed in such instances [19,34]. Due to the high number of spores on water-damaged buildings [36,37], long term exposure to species from Stachybotrys may lead to respiratory and cutaneous infections, hemorrhage, irritation, and allergies [8,36].

2.3. Filamentous Opportunistic Fungi from Tap Water Colonise Water-Related Indoor Niches and Recreational Facilities

In spite of well-established water cleaning processes, fungi originating from groundwater or surface water enter water distribution systems and form stable biofilms on different pipe materials [49]. Case reports about fungal contamination of tap-water and biofilm establishment in hospitals and other healthcare facilities have been published. Fungal propagation, biofilm formation, and consequent infections were common at dental, hemodialysis, pediatric, and intensive care units [50,51,52,53].
There is little data on the health effect of fungi after drinking contaminated water [1]. However, modern society uses substantial amounts of tap-water for showering, bathing, cooking, and cleaning [1,54]; most frequently performed with household appliances, such as washing machines and dishwashers. They represent novel niches for propagation of waterborne fungi, particularly polyextremotolerant species Exophiala dermatitidis and E. phaeomuriformis, and these should be taken into consideration for risk assessment linked to fungal diseases [15,17,55]. Together with the above-mentioned fungi, Phialophora (Herpotrichiellaceae) and Ochroconis (Sympoventuriaceae) were recently linked to nutrient-poor tap-water [30,31] and indoor wet niches, such as bathrooms and washing machines [15,55]. Some species within Phialophora and Ochroconis were reported as causative agents of cutaneous and subcutaneous infections (Table 2) [8].
Tap water is used for recreational purposes in swimming pools, jacuzzies, baths, and saunas [22]. Despite the addition of chlorine-based chemicals, a variety of waterborne fungi were isolated [22,56]. The most common diseases reported to develop after visits to recreational public facilities, are Tineas and other cutaneous infections. Tineas are commonly caused by dermatophytes Trichophyton (Arthrodermataceae). Trichophyton mentagrophytes, T. schoenleinii, T. tonsurans, T. verrucosum, and T. violaceum, amongst others, were recently isolated from tap-water, and are related to swimming pools (Table 2) [8,22,27,35].

3. Conclusions

Due to the expanding human population, safe drinking and recreational waters remains one of the most important present and future goals. Although fungi are not mentioned in the present regulations that define water quality, they are constantly isolated from water microbial communities. Reported waterborne filamentous fungi that are associated with opportunistic infections belonged to 12 families and 16 genera from the phyla Ascomycota and Mucoromycota. Human opportunistic fungi, sometimes also linked to plants and insect diseases, were more likely isolated from surface water, while melanised fungi dominated groundwater and groundwater-derived tap-water. Water-borne filamentous fungi were commonly reported to be causative agents of cutaneous, subcutaneous, and respiratory infections among people with transitory and serious immune alterations. Case reports were mainly related to immuno-compromised people who were held in hospitals. In the future, the incidence of fungal infections could be minimized with the inclusion of fungal parameters in water monitoring.

Funding

Infrastructural center Mycosmo MRIC UL, the Culture Collection of Extremophilic Fungi (Ex): Research Programme P1-0170, The Ministry of Higher Education, Science and Technology of the Republic of Slovenia; Young Researcher grant: 382228-1/2013.

Acknowledgments

Authors thank to The Ministry of Higher Education, Science and Technology of the Republic of Slovenia and Infrastructural Center Mycosmo MRIC UL, the Culture Collection of Extremophilic Fungi (Ex) for supporting the work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Novak Babič, M.; Gunde-Cimerman, N.; Vargha, M.; Tischner, Z.; Magyar, D.; Veríssimo, C.; Sabino, R.; Viegas, C.; Meyer, W.; Brandão, J. Fungal Contaminants in Drinking Water Regulation? A Tale of Ecology, Exposure, Purification and Clinical Relevance. Int. J. Environ. Res. Public Health 2017, 14, 636. [Google Scholar] [CrossRef]
  2. Gray, F.N. Pathogen control in drinking water. In Microbiology of Waterborne Diseases, 2nd ed.; Percival, L.S., Yates, V.M., Eds.; Elsevier: Oxford, UK, 2014; Volume 1, pp. 537–570. [Google Scholar]
  3. DEFRA (Department for Environment, Food & Rural Affairs). A Review of Fungi in Drinking Water and the Implications for Human Health, 1st ed.; BIO Intelligence Service: Paris, France, 2011; p. 107.
  4. Wurzbacher, C.; Kerr, J.; Grossart, H.-P. Aquatic fungi. In The Dynamical Processes of Biodiversity: Case Studies of Evolution and Spatial Distribution, 1st ed.; Grillo, O., Venora, G., Eds.; InTech: Rijeka, Croatia, 2011; Volume 1, pp. 227–258. [Google Scholar]
  5. Paterson, R.R.M.; Lima, N. Filamentous Fungal Human Pathogens from Food Emphasising Aspergillus, Fusarium and Mucor. Microorganisms 2017, 5, 44. [Google Scholar] [CrossRef] [PubMed]
  6. Heinrichs, G.; Hübner, I.; Schmidt, K.C.; de Hoog, G.S.; Haase, G. Analysis of black fungal biofilms occurring at domestic water taps (II): Potential routes of entry. Mycopathologia 2013, 175, 399–412. [Google Scholar] [CrossRef] [PubMed]
  7. Anaissie, E.J.; Stratton, S.L.; Dignani, M.C.; Lee, C.K.; Summerbell, R.C.; Rex, J.H.; Monson, T.P.; Walsh, T.J. Pathogenic molds (including Aspergillus species) in hospital water distribution systems: A 3-year prospective study and clinical implications for patients with hematologic malignancies. Blood 2003, 101, 2542–2546. [Google Scholar] [CrossRef] [PubMed]
  8. De Hoog, G.S.; Guarro, J.; Gené, J.; Figueras, M.J. Atlas of Clinical Fungi; Electronic Version 4.0; Centraalbureau voor Schimmelcultures: Utrecht, The Netherlands, 2014; Available online: http://www.clinicalfungi.org/ (accessed on 24 May 2018).
  9. Vos, T.; Flaxman, A.D.; Naghavi, M.; Lozano, R.; Michaud, C.; Ezzati, M.; Shibuya, K.; Salomon, J.A.; Abdalla, S.; Aboyans, V.; et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: A systematic analysis of the Global Burden of disease study 2010. Lancet 2012, 380, 2163–2196. [Google Scholar] [CrossRef]
  10. Zhao, R.-L.; Li, G.-J.; Sánchez-Ramírez, S.; Stata, M.; Yang, Z.-L.; Wu, G.; Dai, Y.-C.; He, S.-H.; Cui, B.-K.; Zhou, J.-L.; et al. A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective. Fungal Divers. 2017, 84, 43–74. [Google Scholar] [CrossRef]
  11. Biedunkiewicz, A.; Kowalska, K.; Schulz, Ł.; Stojek, K.; Dynowska, M.; Ejdys, E.; Sucharzewska, E.; Kubiak, D. Mycological monitoring of selected aquatic ecosystems in the context of epidemiological hazards. Drinking water. Ann. Parasitol. 2014, 60, 191–198. [Google Scholar] [PubMed]
  12. 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 Ecol. 2016, 20, 30–39. [Google Scholar] [CrossRef]
  13. Shi-Kunne, X.; Faino, L.; van den Berg, G.C.M.; Thomma, B.P.H.J.; Seidl, M.F. Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss. Environ. Microbiol. 2018, 20, 1362–1373. [Google Scholar] [CrossRef] [PubMed][Green Version]
  14. Feng, P.; Lu, Q.; Najafzadeh, M.J.; Gerrits van den Ende, A.H.; Sun, J.; Li, R.; Xi, L.; Vicente, V.A.; Lai, W.; Lu, C.; et al. Cyphellophora and its relatives in Phialophora: Biodiversity and possible role in human infection. Fungal Divers. 2014, 65, 17–45. [Google Scholar] [CrossRef]
  15. Wang, X.; Cai, W.; van den Ende, A.H.G.; Zhang, J.; Xie, T.; Xi, L.; Li, X.; Sun, K.; de Hoog, G.S. Indoor wet cells as a habitat for melanized fungi, opportunistic pathogens on humans and other vertebrates. Sci. Rep. 2018, 8, 7685. [Google Scholar] [CrossRef] [PubMed]
  16. Biedunkiewicz, A.; Schulz, Ł. Fungi of the genus Exophiala in tap water-potential etiological factors of phaeohyphomycoses. Med. Mycol. 2012, 19, 23–26. [Google Scholar]
  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. [Google Scholar] [CrossRef] [PubMed]
  18. Patil, V.R.; Borse, B.D. Checklist of freshwater mitosporic fungi of India. Int. J. Bioassays 2015, 4, 4090–4099. [Google Scholar]
  19. Dubey, A.; Kaushal, A. Diversity of Aquatic Hyphomycetes in Different Eco-Climatic Zones of India. IJIR 2017, 3, 1841–1854. [Google Scholar]
  20. Karun, N.C.; Sridhar, K.R.; Ghate, S.D. Aquatic Hyphomycetes in Detritus, Sediment and Water in the Western Ghat Streams. KAVAKA 2016, 47, 107–113. [Google Scholar]
  21. Al-Gabr, H.M.; Zheng, T.; Yu, X. Fungi contamination of drinking water. Rev. Environ. Contam. Toxicol. 2014, 228, 121–139. [Google Scholar] [PubMed]
  22. Ekowati, Y.; van Diepeningen, A.D.; Ferrero, G.; Kennedy, M.D.; de Roda Husman, A.M.; Schets, F.M. Clinically relevant fungi in water and on surfaces in an indoor swimming pool facility. Int. J. Hyg. Environ. Health 2017, 220, 1152–1160. [Google Scholar] [CrossRef] [PubMed]
  23. Fish, K.E.; Osborn, A.M.; Boxall, J. Characterising and understanding the impact of microbial biofilms and the extracellular polymeric substance (EPS) matrix in drinking water distribution systems. Environ. Sci. Water Res. Technol. 2016, 2, 614–630. [Google Scholar] [CrossRef][Green Version]
  24. Novak Babič, M.; Zupančič, J.; Gunde-Cimerman, N.; de Hoog, S.; Zalar, P. Ecology of the Human Opportunistic Black Yeast Exophiala dermatitidis Indicates Preference for Human-Made Habitats. Mycopathologia 2018, 183, 201–212. [Google Scholar] [CrossRef] [PubMed]
  25. Najafzadeh, M.J.; Dolatabadi, S.; Saradeghi Keisari, M.; Naseri, A.; Feng, P.; de Hoog, G.S. Detection and identification of opportunistic Exophiala species using the rolling circle amplification of ribosomal internal transcribed spacers. J. Microbiol. Methods 2013, 94, 338–342. [Google Scholar] [CrossRef] [PubMed]
  26. Madrid, H.; Hernández-Restrepo, M.; Gené, J.; Cano, J.; Guarro, J.; Silva, V. New and interesting chaetothyrialean fungi from Spain. Mycol. Prog. 2016, 15, 1179–1201. [Google Scholar] [CrossRef][Green Version]
  27. Gayatri, T.; Chowdhry, P.N. Study of filamentous fungal flora from polluted river Yamuna water from Delhi catchment areas as a basis to determine water pollution. World J. Pharm. Pharm. Sci. 2017, 6, 534–541. [Google Scholar]
  28. Dolenc-Voljč, M.; Gasparič, J. Human Infections with Microsporum gypseum Complex (Nannizzia gypsea) in Slovenia. Mycopathologia 2017, 182, 1069–1075. [Google Scholar] [CrossRef] [PubMed]
  29. Machido, D.; Yakubu, S.; Ezeonuegbu, B. Composition of Fungal Flora in Raw Refinery Effluent, Effluent Retention Pond and a Treated Effluent Recipient River. J. Appl. Sci. Environ. Manag. 2014, 18, 592–596. [Google Scholar] [CrossRef]
  30. Samerpitak, K.; Gerrits van den Ende, A.H.; Menken, S.B.; de Hoog, G.S. Three New Species of the Genus Ochroconis. Mycopathologia 2015, 180, 7–17. [Google Scholar] [CrossRef] [PubMed]
  31. Samerpitak, K.; Duarte, A.P.M.; Attili-Angelis, D.; Pagnocca, F.C.; Heinrichs, G.; Rijs, A.J.M.M.; Alfjorden, A.; Gerrits van den Ende, A.H.; Menken, S.B.; de Hoog, G.S. A new species of the oligotrophic genus Ochroconis (Sympoventuriaceae). Mycol. Prog. 2015, 14, 6. [Google Scholar] [CrossRef]
  32. De Marchi, R.; Koss, M.; Ziegler, D.; De Respinis, S.; Petrini, O. Fungi in water samples of a full-scale water work. Mycol. Progress 2018, 17, 467–478. [Google Scholar]
  33. Oliveira, H.M.; Santos, C.; Paterson, R.R.; Gusmão, N.B.; Lima, N. Fungi from a Groundwater-Fed Drinking Water Supply System in Brazil. Int. J. Environ. Res. Public Health 2016, 13, 304. [Google Scholar] [CrossRef] [PubMed][Green Version]
  34. Oliveira, B.R.; Crespo, M.T.; San Romão, M.V.; Benoliel, M.J.; Samson, R.A.; Pereira, V.J. New insights concerning the occurrence of fungi in water sources and their potential pathogenicity. Water Res. 2013, 47, 6338–6347. [Google Scholar] [CrossRef] [PubMed]
  35. Schiavano, G.F.; Parlani, L.; Sisti, M.; Sebastianelli, G.; Brandi, G. Occurrence of fungi in dialysis water and dialysate from eight haemodialysis units in central Italy. J. Hosp. Infect. 2014, 6, 194–200. [Google Scholar] [CrossRef] [PubMed]
  36. Ochiai, E.; Kamei, K.; Hiroshima, K.; Watanabe, A.; Hashimoto, Y.; Sato, A.; Ando, A. The Pathogenicity of Stachybotrys chartarum. Nihon Ishinkin Gakkai Zasshi 2005, 46, 109–117. [Google Scholar] [CrossRef] [PubMed]
  37. Hossain, M.A.; Ahmed, M.S.; Ghannoum, M.A. Attributes of Stachybotrys chartarum and its association with human disease. J. Allergy Clin. Immunol. 2004, 113, 200–208. [Google Scholar] [CrossRef] [PubMed]
  38. Mitra, S.; Pramanik, A.; Banerjee, S.; Haldar, S.; Gachhui, R.; Mukherjee, J. Enhanced biotransformation of fluoranthene by intertidally derived Cunninghamella elegans under biofilm-based and niche-mimicking conditions. Appl. Environ. Microbiol. 2013, 79, 7922–7930. [Google Scholar] [CrossRef] [PubMed]
  39. Abdalla, W.G. Isolation and Identification of Water-borne Fungi from Poultry Farms in Khartoum State, Sudan. Sudan J. Vet. Res. 2017, 32, 35–38. [Google Scholar]
  40. Hageskal, G.; Lima, N.; Skaar, I. The study of fungi in drinking water. Mycol. Res. 2009, 113, 165–172. [Google Scholar] [CrossRef] [PubMed][Green Version]
  41. Pereira, V.J.; Fernandes, D.; Carvalho, G.; Benoliel, M.J.; San Romão, M.V.; Barreto Crespo, M.T. Assessment of the presence and dynamics of fungi in drinking water sources using cultural and molecular methods. Water Res. 2010, 44, 4850–4859. [Google Scholar] [CrossRef] [PubMed]
  42. Jankowiak, R.; Stępniewska, H.; Szwagrzyk, J.; Bilański, P.; Gratzer, G. Characterization of Cylindrocarpon-like species associated with litter in the old-growth beech forests of Central Europe. For. Pathol. 2016, 46, 582–594. [Google Scholar] [CrossRef]
  43. Perdomo, H.; García, D.; Gené, J.; Cano, J.; Sutton, D.A.; Summerbell, R.; Guarro, J. Phialemoniopsis, a new genus of Sordariomycetes, and new species of Phialemonium and Lecythophora. Mycologia 2013, 105, 398–421. [Google Scholar] [CrossRef] [PubMed]
  44. Richardson, M. The ecology of the Zygomycetes and its impact on environmental exposure. Clin. Microbiol. Infect. 2009, 15, 2–9. [Google Scholar] [CrossRef] [PubMed]
  45. Spatafora, J.W.; Chang, Y.; Benny, G.L.; Lazarus, K.; Smith, M.E.; Berbee, M.L.; Bonito, G.; Corradi, N.; Grigoriev, I.; Gryganskyi, A.; et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 2016, 108, 1028–1046. [Google Scholar] [CrossRef] [PubMed][Green Version]
  46. Kontoyiannis, P.D. Mucormycosis. In Goldman's Cecil Medicine, 24th ed.; Goldman, L., Schafer, I.A., Arend, P.W., Armitage, O.J., Clemmons, R.D., Drazen, M.J., Griggs, C.R., Landry, W.D., Lewinson, W., Rustgi, K.A., et al., Eds.; Elsevier: Oxford, UK, 2012; Volume 2, pp. 1994–1997. [Google Scholar]
  47. Lackner, M.; de Hoog, G.S.; Verweij, P.E.; Najafzadeh, M.J.; Curfs-Breuker, I.; Klaassen, C.H.; Meis, J.F. Species-specific antifungal susceptibility patterns of Scedosporium and Pseudallescheria species. Antimicrob. Agents Chemother. 2012, 56, 2635–2642. [Google Scholar] [CrossRef] [PubMed]
  48. Signore, S.C.; Dohm, C.P.; Schütze, G.; Bähr, M.; Kermer, P. Scedosporium apiospermum brain abscesses in a patient after near-drowning—A case report with 10-year follow-up and a review of the literature. Med. Mycol. Case Rep. 2017, 17, 17–19. [Google Scholar] [CrossRef] [PubMed]
  49. Siqueira, V.M.; Oliveira, H.M.; Santos, C.; Paterson, R.R.M.; Gusmão, B.N.; Lima, N. Filamentous fungi in drinking water, particularly in relation to biofilm formation. Int. J. Environ. Res. Public Health 2011, 8, 456–469. [Google Scholar] [CrossRef] [PubMed][Green Version]
  50. Kadaifciler, D.G.; Ökten, S.; Sen, B. Mycological contamination in dental unit waterlines in Istanbul, Turkey. Braz. J. Microbiol. 2013, 44, 977–981. [Google Scholar] [CrossRef] [PubMed][Green Version]
  51. Mesquita-Rocha, S.; Godoy-Martinez, P.C.; Gonçalves, S.S.; Urrutia, M.D.; Carlesse, F.; Seber, A.; Silva, M.A.; Petrilli, A.S.; Colombo, A.L. The water supply system as a potential source of fungal infection in paediatric haematopoietic stem cell units. BMC Infect. Dis. 2013, 13, 289. [Google Scholar] [CrossRef] [PubMed][Green Version]
  52. Lisboa, G.M.; Lisboa, Y.R.; Pinheiro, T.M.; Stegun, R.C.; da Silva-Filho, E.A. Microbial diversity in dental unit waterlines. Acta Odontol. Latinoam. 2014, 27, 110–114. [Google Scholar] [PubMed]
  53. Oliveira, V.A.M.A.; de Alencar, R.M.; Santos Porto, J.C.; Fontenele Ramos, I.R.B.; Noleto, I.S.; Santos, T.C.; Mobin, M. Analysis of fungi in aerosols dispersed by high speed pens in dental clinics from Teresina, Piaui, Brazil. Environ. Monit. Assess. 2018, 190, 56. [Google Scholar] [CrossRef] [PubMed]
  54. Moat, J.; Rizoulis, A.; Fox, G.; Upton, M. Domestic shower hose biofilms contain fungal species capable of causing opportunistic infection. J. Water Health 2016, 14, 727–737. [Google Scholar] [CrossRef] [PubMed]
  55. Novak Babič, M.; Zalar, P.; Ženko, B.; Schroers, H.-J.; Džeroski, S.; Gunde-Cimerman, N. Candida and Fusarium species known as opportunistic human pathogens from customer-accessible parts of residential washing machines. Fungal Biol. 2015, 119, 95–113. [Google Scholar] [CrossRef] [PubMed]
  56. Rafiei, A.; Amirrajab, N. Fungal Contamination of Indoor Public Swimming Pools, Ahwaz, South-west of Iran. Iran. J. Public Health 2010, 39, 124–128. [Google Scholar] [PubMed]
Table 1. Natural and anthropogenic biotic and abiotic factors, influencing microbial presence in different water sources.
Table 1. Natural and anthropogenic biotic and abiotic factors, influencing microbial presence in different water sources.
Biotic and Abiotic FactorsWater Source
Natural EnvironmentHuman-Made Environment
GroundwaterRivers & StreamsLakesMineral WaterTap WaterWater from Swimming Facilities
Primary water source locationUndergroundSurfaceSurfaceUnderground/SurfaceUnderground/SurfaceUnderground/Surface
Water flowStableVariableStableStable/VariableVariableStable/Variable
Sun irradiationAbsentPresentPresentAbsent/PresentAbsentAbsent/Present
TemperatureStableVariableVariableStableVariableStable
Ion compositionStableVariableVariableStableStableVariable
pHStableVariableVariableStableStableStable
Organic matter concentrationLowHighHighLow/HighLowLow
Dissolved oxygen concentrationLowLow/HighLowLow/HighHighHigh
Water treatmentAbsentAbsentAbsentAbsent/OzonationAeration
Ultrafiltration
UV-treatment
Ozonation
Chlorination
Additional chlorination
Effect of materials in distribution systemsAbsentAbsentAbsentAbsentPresentPresent
Table 2. Opportunistic waterborne filamentous fungi not reported from food, and their effects on human health.
Table 2. Opportunistic waterborne filamentous fungi not reported from food, and their effects on human health.
Fungal SpeciesBSL *Water TypeEffect on HealthReferences
Phylum Ascomycota
Cylindrocarpon aquaticum1Surface waterNo data[18,19]
Cylindrocarpon sp.1/2Surface waterCutaneous infections
Keratitis
Mycetoma
[8,19,20]
Cyphellophora europaea2Surface water
Tap water
Cutaneous infections[6,8,21]
Cyphellophora oxyspora1Swimming poolCutaneous infections[8,22]
Cyphellophora reptans1Groundwater
Tap water
Superficial infections[6,8,23]
Cyphellophora sessilis1Groundwater
Tap water
No data[6]
Exophiala castellanii2Groundwater
Tap water
Cutaneous infections[6,8,11,16,23]
Exophiala dermatitidis2Glacier water
Mineral water
Groundwater
Tap water
Cerebral infections
Cutaneous infections
Disseminated infections
Keratitis
Otitis
Respiratory infections
Subcutaneous infections
[8,12,17,24]
Exophiala jeanselmei2Tap waterCutaneous infections
Subcutaneous infections
[8,11,16]
Exophiala oligosperma2Groundwater
Surface water
Tap water
Cerebral infections
Cutaneous infections
Onychomycosis
Subcutaneous infections
[6,8,12,25,26]
Exophiala phaeomuriformis2Tap waterCutaneous infections
Endocarditis
Subcutaneous infections
[6,8,12,17]
Exophiala spinifera2Surface water
Tap water
Bottled water
Cutaneous infections
Disseminated infections
Sinusitis
Subcutaneous infections
[8,11,16,21]
Microsporum canis2Surface waterTinea capitis
Tinea corporis
[8,27]
Microsporum gypseum1Surface waterTinea corporis
Tinea faciei
Tinea manus
[27,28]
Microsporum sp.1/2Surface waterDifferent Tineas[8,29]
Ochroconis bacilliformis1Tap waterNo data[30]
Ochroconis constricta1Tap waterNo data[30]
Ochroconis globalis1Tap waterNo data[30,31]
Ochroconis musae1Tap waterCutaneous infections
Subcutaneous infections
[6,8,30]
Ochroconis tshamytschae1Tap waterCutaneous infections
Subcutaneous infections
[8,30,32]
Phialophora bubakii1Tap waterSubcutaneous infections[8,33]
Phialemonium obovatum2Tap waterEndocarditis
Keratitis
Peritonitis
Subcutaneous infections
Systemic infections
[8,33]
Phialemonium sp.1/2Surface water
Tap water
Respiratory infections
Subcutaneous infections
Systemic infections
[8,34,35]
Rhinocladiella aquaspersa2Surface water
Tap water
Chromoblastomycosis[8,26,33]
Rhinocladiella similis2Groundwater
Surface water
Tap water
Cutaneous infections[6,8,12,17,26]
Scedosporium apiospermum complex (including former Pseudallescheria boydii)2Surface water
Tap water
Cerebral infections
Respiratory infections
Subcutaneous infections
Systemic infections
[8,21]
Scedosporium prolificans2Tap waterDisseminated infections
Respiratory infections
Otitis
[8,35]
Stachybotrys chartarum1Surface waterCutaneous infections
Respiratory infections
[19,34,36]
Stachybotrys ramosus1Surface waterCutaneous infections
Respiratory infections
[18,37]
Trichophyton mentagrophytes2Tap water
Swimming pool
Different Tineas[8,22,35]
Trichophyton schoenleinii2Tap waterTinea capitis
Tinea corporis
[8,35]
Trichophyton tonsurans2Surface waterTinea capitis
Tinea corporis
[8,27]
Trichophyton verrucosum2Tap waterOnychomycosis
Tinea barbae
[8,35]
Trichophyton violaceum2Tap waterTinea capitis
Tinea corporis
[8,35]
Verticillium spp.1Groundwater
Tap water
Keratitis[34,35]
Phylum Mucoromycota
Cunninghamella elegans1Surface waterRespiratory infections[8,38]
Cunninghamella sp.1/2Tap waterCutaneous infections
Respiratory infections
Rhinocerebral infections
[8,34]
Rhizopus spp.1Surface waterCutaneous infections
Respiratory infections
Rhinocerebral infections
Subcutaneous infections
[8,21]
Rhizopus stolonifer1Surface waterRhinocerebral infections[8,27]
Rhizomucor spp.1/2Surface water
Tap water
Disseminated infections
Systemic infections
[8,35,39]
* Biosafety Level.

Share and Cite

MDPI and ACS Style

Novak Babič, M.; Zupančič, J.; Brandão, J.; Gunde-Cimerman, N. Opportunistic Water-Borne Human Pathogenic Filamentous Fungi Unreported from Food. Microorganisms 2018, 6, 79. https://doi.org/10.3390/microorganisms6030079

AMA Style

Novak Babič M, Zupančič J, Brandão J, Gunde-Cimerman N. Opportunistic Water-Borne Human Pathogenic Filamentous Fungi Unreported from Food. Microorganisms. 2018; 6(3):79. https://doi.org/10.3390/microorganisms6030079

Chicago/Turabian Style

Novak Babič, Monika, Jerneja Zupančič, João Brandão, and Nina Gunde-Cimerman. 2018. "Opportunistic Water-Borne Human Pathogenic Filamentous Fungi Unreported from Food" Microorganisms 6, no. 3: 79. https://doi.org/10.3390/microorganisms6030079

Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop