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Review

A Repertoire of Clinical Non-Dermatophytes Moulds

by
Estelle Menu
1,2,*,
Quentin Filori
3,
Jean-Charles Dufour
3,4,
Stéphane Ranque
1,2 and
Coralie L’Ollivier
1,2
1
Laboratoire de Parasitologie-Mycologie, IHU Méditerranée Infection, 13385 Marseille, France
2
Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, VITROME: Vecteurs-Infections Tropicales et Méditerra-néennes, Aix Marseille Université, 13385 Marseille, France
3
INSERM, IRD, SESSTIM, Sciences Economiques & Sociales de la Santé & Traitement de l’Information Médicale, ISSPAM, Aix Marseille University, 13385 Marseille, France
4
APHM, Hôpital de la Timone, Service Biostatistique et Technologies de l’Information et de la Communication, 13385 Marseille, France
*
Author to whom correspondence should be addressed.
J. Fungi 2023, 9(4), 433; https://doi.org/10.3390/jof9040433
Submission received: 1 March 2023 / Revised: 24 March 2023 / Accepted: 27 March 2023 / Published: 31 March 2023
Browse Figures
Versions Notes

Abstract

:
Humans are constantly exposed to micromycetes, especially filamentous fungi that are ubiquitous in the environment. In the presence of risk factors, mostly related to an alteration of immunity, the non-dermatophyte fungi can then become opportunistic pathogens, causing superficial, deep or disseminated infections. With new molecular tools applied to medical mycology and revisions in taxonomy, the number of fungi described in humans is rising. Some rare species are emerging, and others more frequent are increasing. The aim of this review is to (i) inventory the filamentous fungi found in humans and (ii) provide details on the anatomical sites where they have been identified and the semiology of infections. Among the 239,890 fungi taxa and corresponding synonyms, if any, retrieved from the Mycobank and NCBI Taxonomy databases, we were able to identify 565 moulds in humans. These filamentous fungi were identified in one or more anatomical sites. From a clinical point of view, this review allows us to realize that some uncommon fungi isolated in non-sterile sites may be involved in invasive infections. It may present a first step in the understanding of the pathogenicity of filamentous fungi and the interpretation of the results obtained with the new molecular diagnostic tools.

1. Introduction

It is estimated that there are between 1.5 and 5 million fungal species on Earth, and about 100,000 species are currently described [1,2]. Of these species, only a few hundred have the capacity to infect humans [3]. Humans are constantly exposed to potential fungal pathogens, as they are part of their normal flora and that of soil, water and air [3]. Moulds are a part of the vast kingdom of fungi alongside yeasts, mushrooms, polypores, plant parasitic rusts and smuts, microsporidia and Pneumocystis. Filamentous fungi are ubiquitous in the environment and can lead to opportunistic diseases presenting as superficial, invasive or disseminated infections. The number of described species is constantly increasing, probably due to the popularisation of DNA-based diagnostic tools, which now allow the distinction between close taxa and the identification of fungi, even in small quantities [1,4]. The taxonomy of fungi is also in constant evolution with the “one fungus, one name” nomenclature and integrative taxonomy approach combining genomics, morphology and ecology [1,5]. In recent years, epidemiological changes in invasive fungal diseases have been observed, new risk factors have emerged, and the number of patients at risk of developing these infections is also increasing [6,7]. Medical mycology is, therefore, a constantly evolving dynamic. Aspergillus, Penicillium, mucorales and dematiaceous fungi are the main filamentous fungi taxa involved in human diseases. Current reviews mainly focused on these taxa [3,8,9]. However, other, rarer species of moulds can emerge in specific infection sites, such as Paecilomyces variotii or Purpureocillium lilacinum in sino-pulmonary fungal infections, and should not be overlooked [10].
In this review, we offer an overview, as of 16 June 2020, of the filamentous fungi identified in humans by culture and nucleotide analyses associated or not with histopathology. We also provide information on the organs where these micromycetes are isolated and on the semiology of the infections. We have chosen to divide our review into two approaches. First, we describe the taxa of interest and indicate their preferred site of infection. We then described which filamentous fungi were involved at each major anatomical site.

2. Materials and Methods

2.1. Systematic Literature Review and Database Creation

First, all fungi names and synonyms were collected on both Mycobank (https://www.mycobank.org/, accessed on 15 November 2019) and NCBI Taxonomy (https://www.ncbi.nlm.nih.gov/taxonomy, accessed on 15 November 2019) that represent the state of the art of taxonomy of microfungi, updated on 15 November 2019. From Mycobank, the downloaded fungi taxon names and synonyms were provided in the worksheet https://www.MycoBank.org/images/MBList.zip accessed on 15 November 2019. From NCBI Taxonomy, the query used was Fungi[subtree] AND species[rank] AND specified[prop]. Python script using the Biopython package [11] was also implemented to fetch synonyms from NCBI Taxonomy. We have aggregated and deduplicated these two fungi name listings in order to obtain a single list of 239,890 fungi taxa and corresponding synonyms, if any (Figure 1). For each fungus name in the list, we used a Python script and Biopython package [11] to query PubMed to find bibliographic references that mention the fungi name or its synonyms associated with the term “human” in the article title (TI), abstract (AB), author-supplied keywords (Other Term (OT)) or the Medical Subject Headings' (MeSH) terms. The syntax of the queries was dynamically built using this pattern (fungi_name_or_synonyms [TIAB] OR fungi_name_or_synonyms[OT] OR fungi_name_or_synonyms[MeSH]) AND (“Human”[TIAB] OR “Human”[OT] OR “Humans”[MeSH]). Based on the query performed on 15 November 2019, 7428 fungi taxa were found with at least one PubMed reference.
An MS Access® database (Access 2013, Microsoft) was set up on 16 June 2020, with these 7428 recorded fungi names. Using this relational database management system, a link for each taxa corresponding to the query described above gave access to the relevant PubMed references and made it possible to study them one by one in order to identify and collect the relevant information.

2.2. Manual Database Incrementation

In the MS Access database (MS Access 2013 TM, Microsoft), each of the 7428 fungi had a record from a page linked to the PubMed-relevant references. For each PubMed reference, an analysis of the title and/or abstract and/or whole paper was performed manually to ensure that it was isolated from humans. This process was time-consuming. Only references present in PubMed before 16 June 2020 were taken into account in order to have the same PubMed content for each fungal species.
After analysis, 6516 fungal taxa that were ultimately not found in humans were excluded. They included fungi of food, therapeutic or environmental interest, or those involved in domesticated animal diseases. Synonyms, when not isolated from humans but associated with a species involved in humans, were also excluded. We focused on non-dermatophytes moulds. In fact, yeasts, microsporidia, dimorphic fungi, dermatophytes and Pneumocystis isolated in humans were also excluded.
We analysed the titles and/or abstracts and/or full paper and/or supplementary data, when available, of 565 moulds fungal names and synonyms isolated in humans to complete information on the anatomical site involved and the semiologies of the associated infection by filling in the PubMed Unique Identifier (PMID) of the publication concerned. Only identifications by direct diagnosis were taken into account, including culture (followed by morphological, Matrix-Assisted Laser Desorption Ionization Time of Flight (MALDI-TOF) mass spectrometry or DNA sequence-based identification) associated or not with histopathological findings and Polymerase Chain Reaction (PCR). Publications reporting a species-level diagnosis based solely on histopathological examination or indirect methods results were excluded. The date of first publication, last publication and the name used was also reported in the software.
The anatomical sites included: systemic (isolated from blood, bone marrow, blood vessels/arteries or lymph nodes), central nervous system (isolated from cerebrospinal fluid or brain biopsy); ophthalmic systems (isolated from ocular samples, such as vitreous humour, corneal scrapings or lacrimal fluid); heart (isolated from cardiac specimens, e.g., valve or pericardial fluid); osteo-articular system (isolated from joint or bone samples); skeletal muscles (isolated from muscles); soft-tissue (isolated from soft-tissue); endocrine glands (isolated from adrenal, pituitary gland or thyroid); skin system (isolated from cutaneous or subcutaneous samples); otorhinolaryngeal sphere (isolated from nasal specimens, including sinuses, and throat specimens, including mouth, tongue, oesophagus, larynx, pharynx or trachea); auditory system (isolated from ear samples); dental (isolated from tooth root, dental pulp or anatomical structures directly in contact with the tooth in case of periodontitis, gingivitis, implant infection or abscess); pulmonary (isolated from the upper respiratory tract, e.g., sputum, lower respiratory tract, bronchoalveolar lavage fluid, lung biopsy, bronchial brushing, bronchoscopic needle aspiration and bronchial aspirate, pleural fluid and mediastinal specimen); breast; urinary tract (isolated from the urinary tract including kidneys, ureters, bladder, urinary meatus and the prostate); genital (isolated from genitalia or related body fluids, both male and female, including penile and urethral samples); digestive system (isolated from stool samples or organs of the digestive system, including peritoneum, intestines, pancreas, spleen, gallbladder or appendix, but excluding the liver); hepatic (liver biopsy); and pregnancy (isolated from the placenta or foetus). When information on the anatomical site was provided, we added a degree of accuracy by specifying anatomical details or semiology of the associated infection (e.g., endophthalmitis for ocular sphere) by filling in the PMIDs. In brief, for each fungus with publications reporting having been identified in humans, the current name and dates of the first and last publications were completed by filling in a list of PMID for each anatomical site and the semiology of the associated infection.

2.3. Data Analysis

The MS Access® database (Access 2013, Microsoft) was converted into two Excel files (Excel 2013, Microsoft). In the first file, the number of PMIDs per taxa was calculated by the anatomical site where the fungi were isolated. In the second, the number of PMIDs per fungus was given for six major fungal categories (i.e., Aspergillus, dematiaceous, Fusarium, mucorales, Penicillium and Pseudallescheria/Scedosporium) according to the infections associated with the isolation of the fungus, as stated by the authors of the article. If more than one case was described in a publication with the same anatomical site, it counted as one publication because of a single PMID.

2.4. Taxonomy

Taxa were organised at the high-level classification into sections or species complexes based on https://www.aspergilluspenicillium.org/ (accessed on 1 September 2022) for Aspergillus spp. [12] and Penicillium spp. [13,14] and relevant publications for Fusarium spp. [15,16]. Mucorales and dematiaceous fungi were classified by genus [17,18].

2.5. Synonyms

We referred to the “current name” in Mycobank to identify the current name and the synonyms. The current name/synonym association was then checked by querying the PubMed database.

2.6. Figures

All figures were produced using the online tool, Wordart (https://wordart.com/). The size of the name of each species was proportional to the number of times it occurred in the database. The genus Aspergillus is represented in red, the dematiaceous fungi in brown, the mucorales in blue, the genus Fusarium in turquoise, the Scedosporium/Lometospora species complex in purple, the genus Penicillium in green and the others in black.

3. Results

3.1. Fungal Location by Focusing on the Predominant Genus

In total, 6913 articles/PMIDs were included. This bibliographical research identified 565 fungal species of 192 genera, which had been reported at least once in humans. The list of theses taxa is detailed in Table 1, with their former and current scientific name, if applicable. Briefly, there were 204 dematiaceous fungi, 81 Aspergillus spp., 25 Penicillium spp., 35 Fusarium spp., 45 mucorales, 14 of to the Scedosporium/Lomentospora complex, and 161 to other mould species distributed in 103 genera. The results obtained for each of these taxa will be presented below. Regarding the publications reporting the isolation of these micromycetes at all anatomical sites (a publication can be counted multiple times due to the possible report of multiple anatomical sites in the same publication), the leading genus was Aspergillus (total: 4401). The Fumigati and Flavi sections were the most recorded into this genus (total: 2671 and 865, respectively). In second place come the dematiaceous fungi (total: 1976), followed by the Scedosporium/Lomentospora complex (total: 1222), mucorales (total: 1089) and Fusarium (total: 713). Penicillium was rarely reported in human infections (total: 163).

3.1.1. Aspergillus

Aspergillus species were the most frequent moulds isolated in human clinical samples. In this repertoire, the 81 Aspergillus species identified at least once in humans belong to 14 sections of the 20 described [19], as follows: Aspergillus, Candidi, Circumdati, Clavati, Cremei, Flavi, Flavipedes, Fumigati, Nidulantes, Nigri, Polypaecilum, Restricti, Terrei and Usti. As reported in the literature, the filamentous fungus mostly isolated from humans is Aspergillus fumigatus [20], followed by Aspergillus flavus, Aspergillus niger and Aspergillus terreus. The lung and respiratory tracts were the most common anatomical sites of infection, with a total of 1180 publications for A. fumigatus, 174 for A. flavus, 102 for A. niger and 81 publications for A. terreus. These fungi are indeed ubiquitous in the environment and are transmitted by the airways [21]. The results will be approached in terms of the Aspergillus section to rule out potential misidentifications related to morphological identification [4]. The anatomical site in the second position and concerning all the sections was the skin system. Cutaneous aspergillosis can be primary and can affect immunocompetent patients or can be secondary in cases of disseminated infection, predominantly in immunosuppressed patients [22,23,24]. The Nigri section has a tropism for the auditory system, with 79 publications, which has already been noted in the literature [25]. Regarding the clinical presentations involving the central nervous system or heart, the Fumigati section was predominantly represented (194 and 118 publications, respectively). The Fumigati, Flavi and Nigri sections had a predominantly ocular involvement, with 140, 93, and 36 publications, respectively.

3.1.2. Fusarium

The genus Fusarium includes at least 200 species, grouped into about ten phylogenetic species complexes [15,16,26]. In this review of the literature, only eight species complexes were found to have been isolated from humans: F. chlamydosporum species complex (FCSC), F. dimerum species complex (FDSC), F. incarnatum–F. equiseti species complex (FIESC), F. oxysporum species complex (FOSC), F. sambucinum species complex (FSAMSC), F. solani species complex (FSSC), F. fujikuroi species complex (FFSC) and Gibberella fujikuroi species complex (GFSC). Interestingly, looking at the Fusarium genus as a whole, three anatomical sites stand out: the ocular system (190 publications), the cutaneous system (233 publications) and systemic involvement (134 publications). This is consistent with the data in the literature reporting superficial cases, mainly keratitis and onychomycosis in immunocompromised or immunocompromised patients and disseminated infections in immunocompromised patients [27,28,29,30]. Species belonging to the FSSC are predominantly represented, which has previously been shown to be the most virulent Fusarium species complex in animal models [31].

3.1.3. Penicillium

The genus Penicillium is ubiquitous in the environment and is rarely involved in human infections. When found in superficial and aerial samples, they are often considered contaminants. In this literature review, only 163 publications reporting the isolation of these hyaline hyphomycetes in humans were found. One species has emerged since the 1990s and mainly affects humans with acquired immunodeficiency syndrome (AIDS): Talaromyces marneffei [32,33], and this is the predominant species within the genus Penicillium representing 54% of the publications (89/164). The members of the genus Penicillium are mostly reported in three anatomical sites: the pulmonary sphere (48 publications), the cutaneous system (23 publications) and systemic involvement (36 publications).

3.1.4. Mucorales

The order of the mucorales (previously Zygomyces) includes the hyaline pauciseptated filamentous fungi group, comprising 13 genera: Mucor, Lichtheimia, Rhizomucor, Rhizopus, Absidia, Syncephalastrum, Cunninghamella, Apophysomyces, Mycocladus, Saksenaea, Actinomucor, Thamnostylum and Thermomucor. All of these are implicated in human infections [34]. In this literature review, Rhizopus was the genus mostly involved in human infections, with Rhizopus oryzae (121 publications) (plus its synonym and current appellation Rhizopus arrhizus (53 publications)) leading the way, followed by Rhizopus microsporus (90 publications). Mucorales can be classified according to the primary route of infection: airborne, direct contact with contaminated devices or by trauma [34,35]. Here, we compare the number of publications reporting isolation in the skin system versus the respiratory system, including from the oto-rhino-laryngological sphere and pulmonary sphere: The genera Apophysomyces (54 versus 26 publications, respectively), Mucor (40 versus 18 publications, respectively) and Saksenaea (45 versus eight publications, respectively) are mostly isolated from the skin system and therefore transmitted by contact; the genera Cunninghamella (12 versus 52 publications, respectively), Rhizopus (75 versus 134 publications, respectively) and Rhizomucor (8 versus 31 publications, respectively) are mostly isolated from the oto-rhino-laryngological sphere and pulmonary system and are, therefore, airborne; finally, Lichtheimia (77 versus 74 publications, respectively) had a less obvious tropism for one or the other of these two systems. The cutaneous or respiratory tropism can be explained by the differences found in the sporangia of these genera [35]. In fact, the wet spores of the Mucor, Apophysomyces and Saksenaea species are probably not primarily dispersed by the air and transmitted by trauma [35,36]. On the contrary, the sporangiospores of Rhizopus and Rhizomucor species are small (less than 4 µm in diameter), dry and therefore easily airborne [37,38]. This morphological hypothesis does not explain everything because, similar to Mucor, Lichteimia have wet spores and yet they are equivalently reported in the lung and skin in this review.

3.1.5. Dematiaceous moulds

Dematiaceous fungi are also known as “black fungi” due to the predominance of melanin in their cell walls, which likely acts as a virulence factor. These darkly pigmented fungi are found on the soil surface, where they live as saprophytes but also sometimes as parasites of plants [39]. This review has highlighted 204 dematiaceous fungi species isolated from humans, belonging to 19 genera: Alternaria, Exophiala, Cladophialophora, Scopulariopsis, Curvularia, Phialemoniopsis, Phialemonium, Exserohilum, Microascus, Bipolaris, Chaetomium, Cladosporium, Ochroconis, Phaeoacremonium, Rhinocladiella, Fonsecaea, Phialophora, Phoma and Madurella. The genus Exophiala is the most represented. Contamination most often takes place through infection of a wound by a telluric strain or during a transcutaneous traumatism by means of a plant [40]. This explains the predominantly cutaneous location found in this review (1043 publications). Among the cutaneous affections, melanised fungi are responsible for chromoblastomycosis, which mainly affect individuals performing soil-related tasks [41], phaeohyphomycosis [42] and eumycotic myetoma [43]. Two synonyms species stand out for their tropism for the central nervous system, Cladiophialophora bantiana and Cladosporium trichoides, for which 51 publications and 30 publications, respectively, were found in this location.

3.1.6. Pseudallescheria/Scedosporium Species Complex (PSC)

Among the PSC, six genera were represented: Allescheria, Lomentospora, Monosporium, Petriellidium, Pseudallescheria and Scedosporium. These fungi are ubiquitous in the environment and can be found in soil, compost and polluted water [44]. Regarding current nomenclature and taxonomy, the Pseudallescheria/Scedosporium species complex includes the three major species isolated from humans: Scedosporium apiospermum, Scedosporium boydii, and Lomentospora prolificans, and four distinct species, namely Scedosporium aurantiacum (29 publications), Scedosporium dehoogii (2 publications), Scedosporium inflatum (86 publications) and Scedosporium minutisporum (1 publication) [45]. By grouping the publications concerning the main species and their synonyms, we find 468 publications reporting the isolation of Scedosporium apiospermum, 275 publications reporting the isolation of Scedosporium boydii and 261 publications concerning the isolation of Lomentospora prolificans in humans. In regard to locations, S. boydii and S. apiospermum are found in all anatomical sites, with a greater prevalence in the pulmonary sphere (72 and 94 publications, respectively) and the cutaneous system (79 and 110 publications, respectively). Scedosporium prolificans is mainly found in the pulmonary sphere (56 publications) and in systemic infections (52 publications).

3.1.7. Others

Among the moulds not classified in the five major genera, some present in the environment stands out for their ability to affect multiple organs, such as the members of the genus Acremonium, with Acremonium strictum (35 publications) and Acremonium kiliense (27 publications) in the lead, members of the genus Paecilomyces, with Paecilomyces variotii (53 publications), and members of the Trichoderma genus, with Trichoderma longibrachiatum in the lead (40 publications). Others have a cutaneous tropism. Hendersonula toruloidea is an opportunistic fungus which is almost exclusively responsible for skin infections (34/35 publications). Onychocola canadensis is found only on the skin system (17 publications) and is mostly responsible for onychomycosis (16 publications). Finally, some rarely reported species were exclusively found in the ocular area, often secondary to trauma, such as Arthrobotrys oligospora (one publication), Beauveria alba (one publication), Carpoligna pleurothecii (one publication), Cephaliophora irregularis (one publication), Cephalosporium niveolanosum (one publication), Colletotrichum coccodes (one publication), Colletotrichum dematium (seven publications), Edenia gomezpompae (one publication), Epicoccum nigrum (one publication), Glomerella cingulate (one publication), Laetisaria arvalis (one publication), Metarhizium robertsii (one publication), Microcyclosporella mali (one publication), Paecilomyces viridis (one publication), Papulaspora equi (one publication), Pestalotiopsis clavispora (one publication), Phaeoisaria clematidis (one publication), Podospora austroamericana (one publication), Pseudopestalotiopsis theae (one publication), Roussoella solani (one publication), Setosphaeria holmii (one publication), Stachybotrys eucylindrospora (one publication), Tintelnotia destructans (one publication) and Tritirachium roseum (one publication).

3.2. Fungal Location by Focusing on the Anatomical Site

Within the 19 anatomical sites, the semiology of infection was detailed for the six major categories of fungi involved in human pathologies (Table 2).

3.2.1. Systemic

Regarding systemic localisation (comprising fungaemia, aortitis, vasculitis, lymph node infection and bone marrow infection), there is a large majority of fungaemias. The genus Aspergillus was predominantly isolated from blood samples, with Aspergillus fumigatus and Aspergillus flavus predominating (Figure 2). It should be noted that the genus Fusarium was in second place with Fusarium solani. Aspergillus is rarely isolated from blood cultures and is usually in the case of infective endocarditis. This predominance of Aspergillus detection in systemic infections is explained by the use of new detection tools, including PCR.

3.2.2. Central Nervous System

Three genera are mostly represented in central nervous system infections: Aspergillus, dematiaceous fungi and Pseudallescheria/Scedosporium species complex (Figure 3). The majority of infections occur as brain abscesses or meningitis. Figure 2 highlights several species of dematiaceous fungi. Exserohilum rostratum has been involved in iatrogenic meningitis outbreaks secondary to the use of contaminated injectable corticosteroids [46,47,48,49,50,51]. Cladophialophora bantiana is a dematiaceous mould that may infect immunocompetent patients (mainly farmers or residents of agricultural regions), whose reservoirs and modes of transmission are still poorly known [52]. Its neurotropism is highlighted by 51 publications concerning the CNS among a total of 84 in this review. Its synonym, Cladosporium trichoides, causes brain abscesses for which we have recovered 30 publications. Both are responsible for 81 publications reporting CNS involvement.

3.2.3. Ocular System

All categories of fungi can cause ocular damage. Indeed, as filamentous fungi are ubiquitous in the environment, this type of infection is frequently observed during injuries with plants. The genera Aspergillus with Aspergillus fumigatus, Aspergillus flavus, Aspergillus terreus and Aspergillus niger and Fusarium with Fusarium solani and Fusarium oxysporum are predominant (Figure 4). In most cases, it can be keratitis (623 publications) or endophthalmitis (240 publications). The most described species that can cause both keratitis and endophthalmitis are Fusarium solani (85 and 21 publications, respectively), Aspergillus fumigatus (63 and 44 publications, respectively), Aspergillus flavus (52 and 16 publications, respectively), Scedosporium apiospermum (35 and 13 publications, respectively), Aspergillus niger (12 and 13 publications, respectively) and Pseudallescheria boydii (10 and 10 publications, respectively). The other species mostly involved in keratitis are Pythium insidiosum (31 publications), Fusarium oxysporum (21 publications), Lasiodiplodia theobromae (11 publications), Alternaria alternata (10 publications) and Colletotrichum gloeosporioides (10 publications). It should be noted that ten species have been found in conjunctival infections: Aspergillus flavus (one), Aspergillus fumigatus (one), Aspergillus niger (four), Cephalosporium niveolanosum (one), Exophiala jeanselmei (one), Fonsecaea pedrosoi (one), Monosporium apiospermum (one), Neocucurbitaria keratinophila (one), Pseudallescheria boydii (one) and Scedosporium apiospermum (one).

3.2.4. Auditory System

The genus Aspergillus is predominantly isolated from the auditory system, with Aspergillus niger in the lead, a member of the Nigri section known for its tropism for the auditory meatus [25]. Aspergillus flavus and Aspergillus fumigatus come in second place (Figure 5). These fungi are responsible for fungal otomycosis in the majority of cases [53]. Interestingly, 29 publications reported the identification of Pseudallescheria/Scedosporium complex in the auditory system, including 18 reporting otomycosis. Scedosporium apiospermum was predominant, with ten publications reporting otomycosis, including two cases of malignant otitis externa [54,55] and one otitis complicated with temporomandibular arthritis [56]. Other species stand out in Figure 4, such as Absidia corymbifera, of which five publications report the involvement in otomycosis, including one case of malignant otitis externa [57] and a few cases of Penicillium otomycosis (six publications).

3.2.5. Oto-Rhino-Laryngeal System

It is not surprising that a majority of aspergillosis rhinosinusitis is recorded (282 publications) (Figure 6). This anatomical site also includes rhino-orbital, rhino-facial and rhino-orbito-cerebral involvement, which explains the strong representation of mucorales (170 publications). Rhizopus oryzae (heterotypic synonym Rhizopus arrhizus) is largely in the majority of the mucorales (38 publications), which is not surprising, given that it is the most common mucorale species worldwide [58]. Rhizopus oryzae is responsible for variable oto-rhino-laryngeal system infections, with a majority of rhino-orbito-cerebral infections (17 publications) followed by rhino-sinusitis (nine publications) and rhino-orbital involvement (seven publications). These rhino-orbito-cerebral lesions can also be caused by Aspergillus fumigatus (16 publications) and two other species of mucorales Rhizopus arrhizus (12 publications) and Apophysomyces elegans (11 publications). One fungus stands out, Conidiobolus coronatus, which is responsible for entomophthoromycosis and rhino-facial infections. C. coronatus is a widely distributed insect pathogenic fungus belonging to the class Zygomycetes and is rarely involved in human pathology. This mycosis is mainly tropical due to its tropism of plant detritus in very humid environments [59].

3.2.6. Pulmonary System

The respiratory system is the anatomical site most affected by fungal infections (4496 publications). It should be noted that no distinction was made between colonisation and allergic bronchopulmonary aspergillosis, which thus includes the respiratory isolation of Aspergillus species. Similar to Aspergilli, moulds are ubiquitous saprophytes in the environment. Their dispersion in the air is possible by the production of volatile spores, which ensures their presence in both indoor and outdoor environments [60,61]. Human contamination thus mainly occurs by inhaling the airborne conidia, with the lungs being the first to be exposed. We, therefore, note a wide variety of moulds responsible for lung damage (Figure 7).

3.2.7. Cardiac Involvement

Cardiac involvement was found among 13% (74/565) of the species described in this repertoire. These species belonged to the major taxa Aspergillus, Penicillium, Fusarium, mucorales, dematiaceous fungi and Scedosporium/Lomentospora complex, as well as the genera Acremonium sp, Arthrographis sp., Conidiobolus sp., Emericella sp., Engyodontium sp., Paecilomyces sp., Purpureocillium sp., Pythium sp., Rasamsonia sp., Thermothelomyces sp. and Trichoderma sp., with Aspergillus fumigatus being the most common species isolated (Figure 8). These infections are, however, rare with species belonging to the genus Penicillium, including only three publications (one endocarditis due to Penicillium chrysogenum [62] and two pericarditis due to P. citrinum and P. rubens [63,64]) being reported. Cardiac involvement was mainly in the form of endocarditis, whether native (105 publications) or on a prosthetic valve or implanted equipment (96 publications). Interestingly, in native valve endocarditis, mitral involvement seems to be the most frequent (41 publications) (Table 3). Pericarditis and myocarditis were described in 37 and 49 publications, respectively.

3.2.8. Digestive System

Concerning the digestive system, the two main diseases are fungal peritonitis (135 publications) and spleen disease (80 publications) (Figure 9). Micromycetes are known to be responsible for peritonitis during peritoneal dialysis between 1% and 3% of cases, which is indeed the situation we found in the majority of this review [162,163]. In this review, 77.8% of the publications reported peritonitis secondary to peritoneal dialysis (105/135). Other risk factors that emerged were prematurity [164,165,166,167,168] and solid organ transplantation, including the kidney [169,170,171,172,173], heart [174], small bowel [175] and liver [176,177]. Seven publications reported peritoneal involvement secondary to dissemination [174,178,179,180,181,182]. The species mostly found were Aspergillus fumigatus (18 publications), Aspergillus niger (9 publications) and Paecilomyces variotii (8 publications).
Invasive bowel infections by Aspergillus and mucorales (14 and 9 publications, respectively) are mainly reported concomitantly with disseminated infection. Invasion of the gastrointestinal tract is rarely described individually [183].
Splenic involvement was, in the majority of cases, secondary to haematogenous dissemination of the pathogen, with the exception of three situations where splenic abscesses were described. One case of a splenic abscess caused by Aureobasidium pullulans in a patient with lymphoma [184] and one caused by Hortaea werneckii in a patient with acute myeloid leukaemia [185] were both diagnosed postmortem. The third case of splenic abscess caused by Paecilomyces variotii was described in a child with chronic granulomatous disease [186].

3.2.9. Liver Involvement

In terms of hepatic involvement (Figure 10), there is great variability in the forms found, including abscesses, hepatitis, ascites and lesions secondary to hematogenous dissemination (Table 2). The genus Aspergillus is mostly represented (41 publications) with a predominance of Aspergillus fumigatus and Aspergillus flavus.

3.2.10. Urinary Tract

In terms of urinary tract involvement (Figure 11), the vast majority of infections are renal (185 publications), with a predominance of the genus Aspergillus (85 publications). These infections may be primary or secondary to the haematogenous dissemination of the fungus.

3.2.11. Osteo-Articular System

Among the osteoarticular diseases, osteomyelitis is the most frequent (266 publications). The second most common form is joint damage (164 publications), which includes arthritis (57 publications), bursitis (one publication), unspecified joint damage (60 publications) and synovitis (46 publications). Spondylodiscitis comes in third place (71 publications). Among the species involved in these infections are species of the genus Aspergillus (Aspergillus fumigatus, Aspergillus flavus and Aspergillus terreus), the Scedosporium/Lomentospora complex (Pseudallescheria boydii, Scedosporium prolificans and Scedosporium apiospermum) and Fusarium solani (Figure 12).

3.2.12. Skin System

Concerning the involvement of the cutaneous system, four affections stand out: superficial cutaneous infection (1195 publications), subcutaneous infection (610 publications), onychomycosis (394 publications) and mycetoma (282 publications). Aspergillus fumigatus is mostly represented (Figure 13) and is mainly responsible for superficial (84 publications) and subcutaneous (37 publications) infections. The subcutaneous infections are mainly due to dematiaceous fungi (338 publications), with Exophiala jeanselmei coming in first position (47 publications). Melanised fungi are responsible for chronic infections, such as chromoblastomycosis, or phaeohyphomycosis, which can evolve towards an invasive character [43]. Eumycotic mycetoma are subcutaneous infections that we have chosen to put aside, mainly due to the species Madurella mycetomatis (67 publications) and Madurella mycetomi (25 publications). Among the agents mainly responsible for onychomycosis, we found Scopulariopsis brevicaulis (50 publications), Hendersonula toruloidea (28 publications), Fusarium oxysporum (22 publications), Scytalidium dimidiatum (20 publications), Aspergillus niger (18 publications) and Fusarium solani (17 publications). These species are responsible for distal and lateral subungual onychomycosis, the most common type of onychomycosis mainly affecting the toenails [187].

3.2.13. Endocrine Glands

Among the endocrine glands, the thyroid is the most frequently affected (66 publications/84). In the majority of cases, the disease is secondary to systemic dissemination of the pathogen, diagnosed postmortem [188]. In fact, infiltration of the thyroid with Aspergillus organisms occurs in approximately 20% of autopsies in patients dying from a disseminated disease [189]. However, a few rare cases of primary thyroid infections have been reported with Aspergillus fumigatus: two cases of thyroid suppuration in lupus patients treated with corticosteroids [190,191], two cases described in HIV patients [192,193] and one case in a child with chronic granulomatous disease [194]. Scedosporium apiospermum was reported to cause multiple thyroid abscesses in a patient with cirrhosis and autoimmune haemolytic anaemia, presenting swelling in the neck [195].

3.2.14. Rarely Involved Anatomical Sites

Dental location: Endodontic infections were rarely found in this review and manifested themselves in the form of root involvement [196,197], granuloma [198,199] or gingival infections [200,201]. No species seemed to have a particular tropism for this sphere.
Genital sphere: Interestingly, the male genital sphere seems to be mostly affected, with 71.4% of the publications (15/21) reporting testicular, epididymal or glans involvement. Only three publications reported vaginitis [202,203,204], two reported labial involvement [190,205] and one tubo-ovarian abscess [206]. No species seemed to have a particular tropism for this sphere.
Breast: A majority of Aspergillus was isolated from this particular site. It should be noted that the Aspergillus glaucus and Aspergillus niger complexes have already been isolated from milk samples [207,208]. Interestingly, four publications reported fungal infections following breast implant surgery, a situation that is not well-known in this field, due to Aspergillus niger [209,210], Paecilomyces variotii [211] and Scedosporium apiospermum [212].
Placental infection: a single case of placental aspergillosis due to Aspergillus niger was found in this literature review [213].

4. Discussion

The aim of this study was to establish as exhaustive a catalogue as possible of filamentous fungi identified in humans by culture and molecular biology, whether or not they were associated with histopathological findings. We found 565 filamentous fungi identified in humans, for which we specified the organs where these fungi had been found and the semiology of the infections. This repertoire thus helps to understand the pathogenic potential of certain fungi and can also alert clinicians that the isolation of certain rare fungi, such as Trichoderma longibrachiatum (from stool specimens), can lead to disseminated infection. One of the limitations of this work, however, is the lack of distinction between colonisation and infection, mainly for fungi isolated from non-sterile sites (i.e., the cutaneous system, pulmonary system, digestive system and ENT sphere). Fungi isolated from sterile sites were considered infections (i.e., the heart, liver and ocular system and CNS). The use of new powerful molecular tools, such as pan-fungal PCR, metagenomic and next-generation sequencing, now means it is possible to detect pathogens even in samples containing extremely low levels of nucleic acids [214,215] and to diagnose mixed infections [216]. However, the application of these tools to medical mycology can lead to interpretation difficulties [217,218,219]. This problem is particularly encountered with filamentous fungi, which are ubiquitous in the environment and for which it is sometimes difficult to distinguish between colonisation, infection and environmental contamination. It is now necessary to go further in our work for each anatomical site in order to distinguish colonisations from infections, in order to help clinicians interpret positive results and to assist with the diagnostic management of patients. Similarly, we did not distinguish between diagnosis by molecular biology and macroscopic identification, although it has been shown that potential errors were found in macroscopic identifications, mostly between close species within a section or species complex [4]. More, even in molecular identification, it was pointed out that 20% of the sequences available in public databases are unreliable [220,221]. We have based our repertoire according to state of the art at the time of reported publications. Therefore, in Table 1, we have chosen to group species by sections, sharing morphological similarities, in order to bypass this limitation.
Finally, one of the limitations of this publication is its temporality. As explained in Section 2, only references present in PubMed before 16 June 2020 were taken into account in order to have the same PubMed content for all fungi species. However, medical mycology is dynamic, and new organisms constantly need to be accounted for by both clinicians and microbiology laboratories [222]. Moreover, with the COVID-19 pandemic, a new risk factor has emerged [223]. Publications reporting the detection of filamentous fungi in humans have multiplied, reporting, for example, the emergence of mucormycosis and COVID-19-associated pulmonary aspergillosis throughout the world [224,225]. It will therefore be necessary to update this data regularly.

Author Contributions

Conceptualization, S.R. and C.L.; methodology, E.M., Q.F. and. J.-C.D.; software, Q.F. and. J.-C.D.; formal analysis, E.M. and C.L.; data curation, E.M.; writing—original draft preparation, E.M., C.L. and J.-C.D.; supervision, S.R. and C.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study did not require ethical approval.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Systematic literature review flowchart.
Figure 1. Systematic literature review flowchart.
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Figure 2. Wordcloud represents the species name involved in systemic infections. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 2. Wordcloud represents the species name involved in systemic infections. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 3. Wordcloud represents the species name isolated in the central nervous system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 3. Wordcloud represents the species name isolated in the central nervous system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 4. Wordcloud represents the species name isolated in the ocular system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 4. Wordcloud represents the species name isolated in the ocular system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 5. Wordcloud represents the species name isolated in the auditory system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 5. Wordcloud represents the species name isolated in the auditory system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 6. Wordcloud represents the species name isolated in the oto-rhino-laryngeal sphere. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 6. Wordcloud represents the species name isolated in the oto-rhino-laryngeal sphere. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 7. Wordcloud represents the species name isolated in the pulmonary system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 7. Wordcloud represents the species name isolated in the pulmonary system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 8. Wordcloud represents the species name isolated in the cardiac system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 8. Wordcloud represents the species name isolated in the cardiac system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 9. Wordcloud represents the species name isolated in the digestive system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 9. Wordcloud represents the species name isolated in the digestive system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 10. Wordcloud represents the species name isolated in the liver. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 10. Wordcloud represents the species name isolated in the liver. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 11. Wordcloud represents the species name isolated in the urinary tract. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 11. Wordcloud represents the species name isolated in the urinary tract. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 12. Wordcloud represents the species name isolated in the osteo-articular system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 12. Wordcloud represents the species name isolated in the osteo-articular system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Figure 13. Wordcloud represents the species name isolated in the skin system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
Figure 13. Wordcloud represents the species name isolated in the skin system. The size of the name of each species is proportional to the number of times it occurs in the repertoire.
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Table
Table 1. Number of publications found by anatomical site and species. In the same publication (PMID), several anatomical sites of isolation could be found.
Table 1. Number of publications found by anatomical site and species. In the same publication (PMID), several anatomical sites of isolation could be found.
NameCurrent NameYear of 1st PublicationYear of Last PublicationSystemicCNSOcularAuditory SystemDental and GumsORL SpherePulmonaryBreastHeartDigestive SystemLiverUrinary TractGenitalOA SystemSkeletal MusclesSoft-TissueSkin SystemEndocrine GlandPlacental InfectionTotal
Aspergillus spp. 18127230019245281674619812541122923321444153514401
Section Aspergillus 11 121 1 2 9
Aspergillus chevalieri 19941994 1 1
Aspergillus cibarius 20142014 1 1
Aspergillus glaucus 19902020 1 121 1 6
Aspergillus ruber 20142014 1 1
Section Candidi 1 1 13 6 12
Aspergillus candidus 19622015 1 1 13 6 12
Section Circumdati 11 12 1 14 11
Aspergillus melleus 20152020 1 1 2
Aspergillus ochraceopetaliformis 20092009 1 1
Aspergillus ochraceus 19872019 1 2 1 1 5
Aspergillus persii 20102010 1 1
Aspergillus sclerotiorum 20042004 1 1
Aspergillus subramanianii 20182018 1 1
Section Clavati 1 11 2 5
Aspergillus clavatus 19862019 1 11 2 5
Section Cremei 11 2
Aspergillus stromatoides 19871987 1 1
Aspergillus wentii 20112011 1 1
Section Flavi 32439347 166190145227331585141044 865
Aspergillus alliaceus 20072010 2 2
Aspergillus caelatus 20192019 1 1
Aspergillus effusus 20192019 1 1
Aspergillus flavus 1956202032418147 16217414421733158514984 823
Aspergillus flavus complex 20062020 3 3 6
Aspergillus minisclerotigenes 20142014 1 1
Aspergillus nomius 20092020 1 3 1 5
Aspergillus oryzae 19762018 23 25 11 14
Aspergillus tamarii 19922020 4 11 5 11
Aspergillus tanneri 20122012 1 1
Section Flavipedes 2 1 3
Aspergillus flavipes 19791999 2 1 3
Section Fumigati 1161941404612931225 1187130737133142116128 2671
Aspergillus felis 20132019 0 14 1 6
Aspergillus fischeri 19731998 2 2
Aspergillus fumigatus 19452022114190 (191)134 (136)4612871180 (1186) 113 (115)6729737131142115627 2590 (2601)
Aspergillus fumigatesAspergillus fumigatus20102020 12 6 2 11
Aspergillus fumigatus complex 20122020011 110 1 1 15
Aspergillus lentulus 20062020 14 14
Aspergillus novofumigatus 20132013 1 1
Aspergillus thermomutatus 199420201 11 1 1 2 7
Aspergillus udagawae 20122017 1 1 2
Aspergillus viridinutans 200920141 1 4 6
Neosartorya aureolaAspergillus aureoluteus (anamorph)20112017 1 1
Neosartorya fischeriAspergillus fischeranus (anamorph)19901997 11 1 211 11 9
Neosartorya hiratsukaeAspergillus hiratsukae (anamorph)20022010 1 1 2 4
Neosartorya laciniosaAspergillus laciniosus (anamorph)20132013 1 1
Neosartorya udagawaeAspergillus udagawae (anamorph)20092011 1 1 2
Section Nidulantes 31210511239134 41142440 155
Aspergillus amoenus 20162016 11 2
Aspergillus creber 20162016 1 1 2
Aspergillus delacroxii 201520151 1 2
Aspergillus hongkongensis 20162016 1 1
Aspergillus nidulans 1963202119 (10)3 (4)2 6 (8)20 (23)111 3 112419 83 (90)
Emericella nidulansAspergillus nidulans19832016 11 23 7
Aspergillus nidulans var. echinulatusAspergillus delacroxii19881988 1 1 2
Aspergillus protuberus 20152019 1 1 1 3
Aspergillus quadrilineatus 19921992 1(1) (4) 1 (6)
Aspergillus tetrazonusAspergillus quadrilineatus20042015 2 2
Emericella quadrilineataAspergillus quadrilineatus20042015 1 2 3
Aspergillus sydowii 198920191 21 12 1 1 7 16
Aspergillus sublatus 20142019 3 3
Aspergillus tabacinus 20162016 1 1
Aspergillus unguis 20162016 1 1
Aspergillus versicolor 19502021 232115 2 1 5 22
Emericella rugulosaAspergillus rugulovalvus20122012 1 1 1 1 4
Section Nigri 17436791331133121214 9 458 1387
Aspergillus aculeatus 19841984 1 1 2
Aspergillus awamori 19922020 1 12 1 5
Aspergillus brasiliensis 20102020 1 1 2
Aspergillus luchuensis 20102010 1 1
Aspergillus niger 1965202014433721281022121014 8 447 (48) 1343 (344)
Aspergillus foetidusAspergillus niger19921992 1 1
Aspergillus niger complex 20022014 1 11 3
Aspergillus tubingensis 200920203 15 27 1 1 6 26
Aspergillus uvarum 20152015 1 1
Aspergillus welwitschiae 20162019 11 1 3
Section Polypaecilum 1 1
Polypaecilum insolitumAspergillus insolitus19721972 1 1
Section Restricti 112 4 32 1 14
Aspergillus conicus 20132013 1 1
Aspergillus gracilis 20192019 1 1
Aspergillus penicillioides 20162018 11 1 11 1 6
Aspergillus restrictus 196019931 3 2 6
Section Terrei 1113151111682 161137 16 353 240
Aspergillus carneus 20162016 1 1
Aspergillus niveus 19842008 1 1 2
Aspergillus terreus 194820211113151011681 161037 16 353 237
Section Usti 121 310 1 1 3 22
Aspergillus calidoustus 20082021111 39 1 1 2 19
Aspergillus granulosus 19952009 1 1 2
Aspergillus pseudodeflectus 20182018 1 1
Unknown Section 1 21 4
Aspergillus amstelodami 19832008 1 1 2
Aspergillus repens 19891989 1 1
Eurotium amstelodami 20162016 1 1
Penicillium spp. 3638511748131121 4 23 163
Section Biverticillata 1 1 1 3
Penicillium piceum 200120061 1 1 3
Section Brevicompacta 11 1 3
Penicillium brevicompactum 19962013 11 1 3
Section Canescentia 3 3
Penicillium nigricans 19922002 3 3
Section Chrysogena 2221 55122 2 24
Penicillium chrysogenum 19742016212(1) 3 (4)3 (4) 12 2 16 (19)
Penicillium notatumPenicillium chrysogenum19782016 1 11 3
Penicillium rubens 20162020 1 1111 5
Section Citrina 51134 1 15
Penicillium citrinum 19762020 4 (5)1(1)34 1 13 (15)
Penicillium implicatumPenicillium citrinum20102010 1 1 2
Section Exilicaulis 1 3 4
Penicillium corylophilum 20022011 2 2
Penicillium decumbens 199019921 1 2
Section Fasciculata 1 1
Penicillium verrucosum 20012001 1 1
Section Lanata-Divaricata 1 1
Penicillium vitalePenicillium simplicissimum19921992 1 1
Section Penicillium 1 11 3
Penicillium digitatum 20132013 1 1
Penicillium expansum 19782000 1 1 2
Section Ramigena 1 1
Penicillium capsulatum 20132013 1 1
Section Robsamsonia 1 1
Penicillium dipodomyicola 20132013 1 1
Section Roquefortorum 1 1
Penicillium roqueforti 20182018 1 1
Section Talaromyces 301 425 521 3 19 90
Talaromyces (Penicillium) marneffei 20152020301 424 521 3 19 89
Talaromyces purpurogenus 20162016 1 1
Section Tachyspermi 1 13 1 1 7
Talaromyces amestolkiae 20162017 2 2
Talaromyces atroroseus 202020201 11 1 1 5
Unclassified into a Section 1 13 1 6
Penicillium lilacinum 19721972 1 1
Penicillium purpurogenum 19981998 1 1
Penicillium rugulosumTalaromyces rugulosus19991999 1 1
Talaromyces eburneus 201020101 1 1 3
Fusarium spp. 134219011344111217414116142331 713
F. chlamydosporum Species Complex (FCSC) 1 1 1 1 1 5
Fusarium chlamydosporum 198520201 1 1 1 1 5
F. dimerum Species Complex (FDSC) 2 7 1 11 14 17
Fusarium dimerum 197220182 6 1 11 14 16
Fusarium penzigii 20162016 1 1
F. incarnatum–F. equiseti Species Complex (FIESC) 1 5 11 1 3 12
Fusarium equiseti 20072007 1 1
Fusarium incarnatum 201420201 4 11 1 3 11
F. oxysporum Species Complex (FOSC) 21224 510 3433 3 53 131
Fusarium oxysporum 1958202121224 510 3433 3 53 131
F. sambucinum Species Complex (FSAMSC) 1 2 3
Fusarium roseumFusarium sambucinum19871987 1 1
Fusarium sporotrichioides 20172017 1 1 2
F. solani Species Complex (FSSC) 81 138 2024169 8110131431 452
Phialophora cyanescensNeocosmospora cyanescens19841993 1 3 4
Cephalosporium falciformeNeocosmospora (fusarium) falciformis19681983 2 2
Fusarium keratoplasticum 201520197 8 21 1 1 9 29
Fusarium lichenicola 20032020 3 2 5
Fusarium metavorans 20182018 1 1
Fusarium petroliphilum 201320196 2 1 3 12
Fusarium proliferatum 198820206 3 32 1 3 114 33
Fusarium pseudensiformeNeocosmospora pseudensiformis20202020 1 1
Fusarium riograndense 20182018 1 1
Fusarium solani 19702020555102 1015158 41712941 311
Fusarium solani complex 200520196118 23 1 14 45
Neocosmospora tonkinensis 20182018 1 1
Neocosmospora vasinfectaFusarium neocosmosporiellum199320081 1 11 1 2 7
F. fujikuroi Species Complex (FFSC) 2 1 2 5
Fusarium musae 201520162 1 2 5
Gibberella fujikuroi Species Complex (GFSC) 26 121166 1312 3 25 87
Fusarium acutatum 20062015 2 2
Fusarium andiyazi 201420141 1
Fusarium moniliforme 197720137 61112 1212 2 11 37
Fusarium napiforme 199320182 2 2 6
Fusarium nygamai 199620153 3
Fusarium ramigenum 20162016 1 1
Fusarium sacchari 200020201 4 1 6
Fusarium subglutinans 20102013 2 2
Fusarium temperatum 20142014 1 1
Fusarium thapsinum 200420041 1
Fusarium verticillioides 1995201811 51 1 1 7 26
Fusarium verticillioides complex 20132013 1 1
Unclassified Into Complex 1 1
Fusarium langsethiae 20152015 1 1
Mucorales 454018130164189126693450625245032114 1089
Absidia 1 2 3
Absidia coerulea 19881988 2 2
Absidia Lichtheimii 19681968 1 1
Actinomucor 1 22 111 1 31 13
Actinomucor elegans 200120201 22 111 1 31 13
Apophysomyces 311 233 15114 791954 141
Apophysomyces elegans 19852020211 193 13112 771241 110
Apophysomyces trapeziformis 201220141 254 12
Apophysomyces variabilis 20112020 4 2 2 29 19
Cunninghamella 104 646 9533 313124 109
Cunninghamella bertholletiae 19792019104 544 9533 313114 105
Cunninghamella blakesleeana 20122012 1 1
Cunninghamella echinulata 20092013 11 1 3
Lichtheimia 141999 2351 9208132439776 276
Lichtheimia corymbifera 198220199 (13)9 (18)4 (8)4 (9) 9 (20)22 (43) 3 (7)9 (14)3 (6)6 (11)1 (2)3 (4)1 (3)3 (9)37 (67)2 (4) 125 (238)
Absidia corymbiferaLichtheimia corymbifera198220154845 1120 45341126292 109
Mycocladus corymbiferaLichtheimia corymbifera20132013 1 1 1 1 4
Lichtheimia hongkongensis 20102010 1 1 1 3
Lichtheimia ornata 20182020 1 1 2
Lichtheimia ramosa 20102019111 18 2522 82 33
Mucor 9121 117 11053122 40 95
Mucor circinelloides 1987201931 24 1 212 7 23
Mucor ellipsoideusMucor ardhlaengiktus20112011 1 1
Mucor hiemalis 19862015 1 4 5
Mucor indicus 199020192 1 1 1751 2 5 25
Mucor irregularis 20112019 1 3 (6)1 12 (21) 17 (29)
Rhizomucor variabilisMucor irregularis20092018 3 9 12
Mucor lusitanicus 19901990 1 1
Mucor mucedo 196620131 1 2
Mucor racemosus 20112015 1 1 2
Mucor ramosissimus 19931993 1 1
Mucor velutinosus 201120183 11 1 6
Rhizomucor 25 1021 347511 82 69
Rhizomucor miehei 19992017 2 011 1 5
Rhizomucor pusillus 1983201725 9 (10)18 (19) 336511 6 (7)2 61 (64)
Mucor pusillusRhizomucor pusillus19521981 11 1 3
Rhizopus 6104 805412219102641375 297
Rhizopus arrhizus 19752020(3)4 (9)(3) 19 (57)8 (29)(1)(2)(4)(4)1 (4)(1)(4)2 (3)3 (7)16 (44) 53 (175)
Rhizopus oryzaeRhizopus arrhizus19552020353 382112443141427 121
Rhizopus delemarRhizopus arrhizus var. delemar20142014 1 1
Rhizopus homothallicus 20102019 24 02 8
Rhizopus microsporus 19882020111 1519 15 (16)4 (5)5 (6)121520 (22) 90 (95)
Rhizopus azygosporusRhizopus microsporus19962005 111 1 4
Rhizopus oligosporusRhizopus microsporus var. oligosporus19891989 1 1
Rhizopus rhizopodiformisRhizopus microsporus var. rhizopodiformis197820081 32 16 13
Rhizopus pusillus 20192019 1 1
Rhizopus schipperae 19991999 1 1 2
Rhizopus stolonifer 199620181 2 3
Saksenaea 22 62 1 1 246451 72
Saksenaea erythrospora 20112018 1 34 8
Saksenaea vasiformis 19762020 12 62 1 1 243411 64
Syncephalastrum 21 3 6 12
Syncephalastrum racemosum 20052020 21 3 6 12
Thamnostylum 1 1
Thamnostylum lucknowense 20122012 1 1
Thermomucor 1 1
Thermomucor indicae-seudaticae 19931993 1 1
Dematiaceous Fungi 6918916017512716632845101417081510436 1976
Alternaria 12161 155 4 2 2 284 134
Alternaria alternata 197620191113 134 3 1 (2) 2 240 (41) 80 (82)
Alternaria tenuisAlternaria alternata19601970 1 1 2
Ulocladium atrumAlternaria atra20062006 1 1
Alternaria chlamydospora 19902001 4 4
Alternaria dennisii 20162016 1 1
Alternaria humicola 19841985 1 1 2
Alternaria infectoria 19982020 11 21 25 30
Alternaria longipes 19951995 1 1
Alternaria malorum 20122013 1 1
Alternaria rosae 20172017 1 1
Alternaria tenuissima 19862020 1 1 8 10
Alternaria triticina 20142014 1 1
Exophiala 2510192294413931111131721 317
Exophiala asiatica 20092009 1 1 2
Exophiala bergeri 20162016 1 1
Exophiala castellanii 19941994 1 1
Exophiala dermatitidis 1984202017561 5381163 11291 97
Exophiala equina 20132013 1 1
Exophiala hongkongensis 20132013 1 1
Exophiala jeanselmei 1981202031 (4)10 213 13 13 (4) 85 (98) 113 (130)
Exophiala mansoniiExophiala jeanselmei var. castellanii19861989 1 2 3
Aureobasidium mansoniExophiala jeanselmei var. castellanii19891998 3 1 4
Phialophora gougerotiiExophiala jeanselmei19671983 6 6
Phialophora jeanselmeiExophiala jeanselmei19641979 4 4
Exophiala lecanii-corni 19942018 5 5
Exophiala moniliae 19811984 2 2
Exophiala oligosperma 200320201 1 12 1 116 23
Exophiala phaeomuriformis 20172018 3 3
Exophiala pisciphila 19911991 1 1
Exophiala polymorpha 20152015 1 1
Exophiala salmonis 20062012 2 2
Exophiala spinifera 198320204 11 1 4 29 40
Exophiala xenobiotica 20092016 1 6 7
Cladophialophora 1922 110 1 7 175 190
Cladophialophora ajelloiCladophialophora carrionii19821982 1 1
Cladophialophora arxii 20092015 1 1 2
Cladophialophora bantiana 19962020151 (92)1 15 (7) 5 (6) 119 (25) 84 (134)
Cladosporium trichoidesCladophialophora bantiana19522020 30 1 6 37
Xylohypha bantianaCladophialophora bantiana19892013 11 1 1 13
Cladophialophora boppii 20092020 1 5 (7) 6 (8)
Taeniolella boppiCladophialophora boppii19831983 2 2
Cladophialophora (Cladosporium) carrionii 19792021 1 1 1 38 41
Cladophialophora devriesii 20062006 1 (3) 1 (3)
Cladosporium devriesiiCladophialophora devriesii19841990 2 2
Cladophialophora saturnica 20092009 1 1
Scopulariopsis 6374 616 7313 1 1802 140
Scopulariopsis acremonium 19982009 1 21 11 1 1 8
Scopulariopsis alboflavescens 20182018 1 1 2
Scopulariopsis brevicaulis 195120206 74 37 51 1 1 172 108
Scopulariopsis brumptii 19752017 2 6 1111 51 18
Scopulariopsis candida 19942015 11 2 4
Curvularia 10201 2611 110 6 229 116
Curvularia australiensis 20152015 1 1
Curvularia borreriae 20132013 1 11 1 4
Curvularia brachyspora 19921997 1 1 2
Curvularia clavata 19992009 1 1 1 3
Curvularia geniculata 19642014 131 11 2 1 10
Drechslera hawaiiensisCurvularia hawaiiensis19731999 2 21 2 7
Curvularia hominis 20182018 1 1
Curvularia inaequalis 20052013 2 1 1 4
Curvularia lunata 19702019 311 136 14 3 220 63
Curvularia pallescens 19771995 1 1 2 4
Curvularia senegalensis 19911999 1 1 1 3
Curvularia spicifera 20172017 (2)(1) 1 (4) (2) (1) (1) 1 (11)
Drechslera spiciferaCurvularia spicifera19751988 21 3 2 1 1 10
Curvularia tuberculata 20192019 11 1 3
Phialemoniopsis 2 2
Phialemoniopsis endophytica 20172017 1 1
Phialemoniopsis hongkongensis 20142014 1 1
Phialemonium 3 1 2 22 1 3 14
Phialemonium dimorphosporumPhialemonium curvatum199319991 1 2
Phialemonium obovatum 198620122 1 2 22 1 2 12
Exserohilum 11010 111 2 14 49
Exserohilum longirostratum 19942006 1 1 2
Exserohilum mcginnisii 19862018 2 1 3
Exserohilum rostratum 198620201107 101 2 13 44
Microascus 11 18 2 8 21
Microascus cinereus 19802013 1 12 1 4 9
Microascus cirrosus 199220181 4 1 3 9
Microascus ennothomasiorum 20192019 1 1
Microascus trigonosporus 20042015 2 2
Bipolaris 58181 22912322 1 152 91
Bipolaris australiensis 19862017113 11 1 2 10
Bipolaris cynodontis 20122015 1 11 2 5
Bipolaris hawaiiensis 19862019 28 52 1 4 22
Bipolaris oryzae 20162016 1 1
Bipolaris papendorfii 20052005 1 1
Bipolaris spicifera 198420154541 15511222 1 72 52
Chaetomium 1421 16 1 16 32
Chaetomium atrobrunneum 19982019 21 1 3 7
Chaetomium brasiliense 20112011 1 1
Chaetomium funicola 20072007 1 1
Chaetomium globosum 19882020111 4 12 19
Chaetomium homopilatumHumicola homopilata19971997 1 1
Chaetomium perlucidum 20032003 1 1 1 3
Cladosporium 144 277 1 17 43
Cladosporium bruhneiCladosporium allicinum19942014 1 1 1 3
Cladosporium castellanii 20052005 1 1
Cladosporium cladosporioides 19752019 13 136 9 23
Cladosporium herbarum 19942012 3 1 4
Cladosporium langeronii 20182018 1 1
Cladosporium macrocarpum 20112011 1 1
Cladosporium oxysporum 19992006 2 2
Cladosporium sphaerospermum 20032019121 1 1 2 8
Ochroconis 121 5 61 16
Ochroconis constricta 20142014(1)(2) (1) (3) 1(1) 1 (9)
Dactylaria constrictaOchroconis constricta19922012121 3 1 8
Ochroconis cordanae 20142014 1 1
Ochroconis mirabilis 20142016 1 2 3
Ochroconis musae 20182018 1 1
Ochroconis olivacea 20142014 1 1
Ochroconis tshawytschae 20122012 1 1
Phaeoacremonium 423 3 1 61129 50
Phaeoacremonium aleophilum 20032011 2 2
Phaeoacremonium fuscum 20152015 1 1
Phaeoacremonium inflatipes 199820141 1 2 4
Phaeoacremonium krajdenii 20062006 1 1
Phaeoacremonium parasiticum (Phialophora parasitica) 19832019322 3 1 51118 36
Phaeoacremonium rubrigenum 19992012 3 3
Phaeoacremonium sphinctrophorum 20162016 1 1
Phaeoacremonium venezuelense 20062012 1 1 2
Rhinocladiella 1512 1 1 8 28
Rhinocladiella aquaspersa 19832019 2 4 6
Rhinocladiella atrovirens 19891989 1 1
Rhinocladiella basitona 20132015 1 1 2
Rhinocladiella mackenziei 20092020 14 1 1 16
Rhinocladiella similis 20172020 3 3
Fonsecaea 1963 46 1 2 1147 180
Fonsecaea monomorpha 20052019 21 10 13
Fonsecaea nubica 20102020 1 14 15
Fonsecaea pedrosoi 197320201752 45 (6) 1 2 1107 (122) 135 (151)
Fonsecaea compactumFonsecaea pedrosoi19831989 2 2
Fonsecaea compactum/compactaFonsecaea pedrosoi19832007 5 5
Hormodendrum pedrosoiFonsecaea pedrosoi19611978 1 2 3
Phialophora pedrosoiFonsecaea pedrosoi19511994 6 6
Fonsecaea pugnacius 20152015 1 1
Phialophora 81 2 11 7 139 60
Phialophora americana 20192019 1 1
Phialophora hoffmannii 19821982 1 1
Phialophora reptans 20112011 1 1
Phialophora richardsiae 19682004 1 1 5 111 19
Phialophora verrucosa 19682019 71 2 1 2 25 38
Phoma 1 1 5 7
Phoma exigua 20062006 1 1
Phoma glomerata 20082008 1 1
Phoma herbarum 20102010 1 (2) 1 (2)
Phoma hibernicaPhoma herbarum19701970 1 1
Phoma minutella 19871987 1 1
Phoma minutisporaWesterdykella minutispora19841984 1 1
Phoma sorghina 19891989 1 1
Madurella 1 21 1 154 94 118
Madurella fahalii 20122014 2 2
Madurella mycetomatis 19852020 1 (2)1 1 13 (15)4 63 (88) 83 (112)
Madurella mycetomiMadurella mycetomatis19562013 2 2 25 29
Madurella pseudomycetomatis 20102020 3 3
Madurella tropicana 20122012 1 1
Other Genus 211642112033 101425 1013200 379
Achaetomium strumarium 20182018 1 1
Acrophialophora fusispora 19832020 35 15 14
Acrophialophora levis 20152019 1 2 1 4
Anthopsis deltoidea 19841984 1 1
Arnium leporinum 19841984 1 1 1 3
Arthrinium arundinis 20172018 4 4
Arthrinium phaeospermum 19891989 1 1
Ascotricha chartarum 19962019 11 2
Aureobasidium melanogenum 20162016 1 1
Aureobasidium proteae 20122012 1 1
Aureobasidium pullulans 1971201911 5 113 6 1 13 41
Cladorrhinum bulbillosum 20112011 1 1
Cochliobolus hawaiiensis 20152015 1 1
Lecythophora hoffmanniiConiochaeta hoffmannii19971997 1 1
Phialophora mutabilisConiochaeta mutabilis19731991 1 2 3
Coniochaeta polymorpha 20132013 1 1
Coniothyrium fuckelii 19871987 1 1
Corynespora cassiicola 19692019 1 8 9
Cyphellophora pluriseptata 19862002 2 2
Pseudomicrodochium fusarioidesCyphellophora fusarioides19911991 1 1
Drechslera dematioidea 20052005 1 1
Drechslera rostrata 19861986 1 1
Dichotomophthoropsis nymphaearum 19901990 1 1
Hormonema dematioides 199019981 1 1 3
Hortaea werneckii 200520191 (1) 1 13 (26) 15 (29)
Cladosporium werneckiiHortaea werneckii19641978 6 6
Exophiala werneckiiHortaea werneckii19802000 1 7 8
Lasiodiplodia theobromae 197620191 12 41 3 21
Lecythophora mutabilis 198520111 4 21 1 9
Leptosphaeria senegalensis 19602006 4 4
Macrophomina phaseolina 20082020 2 1 11 5
Microsphaeropsis arundinis 20042019 25 7
Microsphaeropsis olivacea 19992001 1 1 2
Mycoleptodiscus indicus 19952012 21 3 6
Neoscytalidium dimidiatum 20092019(2)(2)(1) 1 (4)1 (2) 17 (46) 19 (57)
Scytalidium dimidiatumNeoscytalidium dimidiatum19932015221 31 29 38
Neotestudina rosatii 19681982 3 3
Nigrospora oryzae 20142014 1 1
Nigrospora sphaerica 20092020 1 2 3
Oidiodendron cerealis 19691969 1 1
Papulaspora equi 20142020 2 2
Phaeosclera dematioides 19871996 1 3 4
Phomopsis bougainvilleicola 20132013 1 1
Phomopsis longicolla 20112011 1 1
Piedraia hortae 19781997 4 4
Pleurophomopsis lignicola 19952004 1 3 4
Phialophora repensPleurostoma repens19751996 3 3
Pleurostomophora richardsiae 201220191 1 4 6
Pseudochaetosphaeronema larense 19872014 3 3
Pseudochaetosphaeronema martinelli 20152015 1 1
Phoma cavaPyrenochaeta cava19971997 1 1
Pyrenochaeta unguis-hominis 19802020 3 3
Scytalidium cuboideum 20132013 11 2
Scytalidium hyalinum 19772018 1 21 22
Scytalidium lignicola 19832020 1 4 5
Sphaeropsis subglobosa 19911991 1 1
Tetraploa aristata 19902013 1 1 2
Thermomyces lanuginosus 19911991 1 1
Thermothelomyces thermophila 20172017 1 1 11 1 1 1 7
Myceliophthora thermophilaThermothelomyces thermophila1992201121 3 31 1 1 1 13
Ulocladium botrytis 20042010 1 1 2
Ulocladium chartarum 19812003 2 2
Veronaea botryosa 20032018 0 10 10
Verruconis gallopava 20142020(1)1 (7)(1)1 16 (12) (3)(1)(1) (2) 1 (5) 10 (35)
Dactylaria gallopavaVerruconis gallopava19902001 4 2 111 1 10
Ochroconis gallopavaVerruconis gallopava19862018121 4 2 2 3 15
Scedosporium/Lomentospora complex 9812613227173253150351744311042121116 1222
Lomentospora prolificans 201520207 (52)4 (21)4 (17)(2)(1)(11)10 (56) 1 (17)(13)(8)(15) 4 (25)(1)22 (18)(2) 34 (261)
Scedosporium prolificansLomentospora prolificans19932017451713211146 1613815 211 162 227
Scedosporium apiospermum 198120201840 (43)56 (64)15 (16) 25 (27)86 (94)113736 (8)142 (45)11496 (110)3 427 (468)
Monosporium apiospermumScedosporium apiospermum19531993 381 28 2 3 12 39
Polycytella hominisScedosporium apiospermum19872006 2 2
Scedosporium aurantiacum 200520192133 114 2 3 29
Scedosporium boydii 20142020(13)1 (55)2 (44)(5) (29)4 (79) 1 (15)(5)(2)(14)(2)(33) (2)2 (72)(5) 10 (375)
Allescheria boydiiScedosporium boydii19481996 89 217 2 1 4 122 57
Petriellidium boydiiScedosporium boydii197619971761 59 3 1 5 10 48
Pseudallescheria angustaScedosporium boydii20112019 1 1 2
Pseudallescheria boydiiScedosporium boydii198220171239274 2248 95212224 2473 258
Scedosporium dehoogii 20172018 2 2
Scedosporium inflatum 1990201213641 59 51047 52366 86
Pseudallescheria minutisporaScedosporium minutisporum20132013 1 1
Others 66311505 10414022252107116452542 871
Acremonium atrogriseum 20002000 1 1
Acremonium implicatum 20012012 1 1 2
Acremonium potronii 19752015 1 1 2
Acremonium sclerotigenum 201120141 2 3
Albifimbria verrucaria 202020201 1 2
Amesia atrobrunnea 20192019 1 1
Amylomyces rouxii 20182018 1 1
Aphanoascus fulvescens 19701992 3 3
Arachnomyces kanei 20022002 1 1
Arthrobotrys oligospora 19901990 1 1
Arthrographis kalrae 19972020324 33 1 2 3 21
Arthropsis hispanica 20132013 1 1 2
Auxarthron ostraviense 20132013 1 1
Basidiobolus haptosporus 19782020 2 3 1 8 14
Beauveria bassiana 19972016 8 12 2 13
Botryosphaeria dothidea 20202020 2 2
Carpoligna pleurothecii 20102010 1 1
Cephaliophora irregularis 19951995 1 1
Cephalotheca foveolata 20062006 1 1
Ceratocystis adiposa 20142014 1 1
Cercospora apii 19571957 1 1
Chalara ellisii 19991999 1 1
Neurospora sitophilaChrysonilia sitophila (Asexual State)19971997 1 1
Chrysosporium articulatum 20152015 1 1
Chrysosporium georgii 20012001 1 1
Chrysosporium keratinophilum 20172017 1 1
Chrysosporium parvum 197320071 1 7 1 2 12
Chrysosporium tropicum 20072007 1 1
Chrysosporium zonatum 19992016 3 1 4
Colletotrichum coccodes 20152015 1 1
Colletotrichum crassipes 20012001 1 1
Colletotrichum dematium 20042019 7 7
Colletotrichum gloeosporioides 19982020 10 (11) 14 15 (16)
Glomerella cingulataColletotrichum gloeosporioides19831983 1 1
Colletotrichum siamense 20192019 1 1
Colletotrichum truncatum 20112020 3 1 4
Conidiobolus coronatus 1978202131 47 (57)2 1 11 31 60 (70)
Entomophthora coronataConidiobolus coronatus19652006 10 10
Conidiobolus incongruus 198320101 42 111 3 13
Conidiobolus lamprauges 20112011 1 111 4
Coniosporium epidermidis 20082012 3 3
Paecilomyces javanicusCordyceps javanica (Teleomorph)1984198611 2 4
Paecilomyces farinosusCordyceps farinosa19941994 1 1
Thielavia sepedoniumCorynascus sepedonium19901990 1 1
Cryptendoxyla hypophloia 20142014 1 1
Cryptostroma corticale 19621966 2 2
Cylindrocarpon destructans 19912011 2 2
Cylindrocarpon lichenicola 19972012 5 1 1 5 12
Daldinia eschscholtzii 20152015 1 1
Diaporthe phaseolorum 20112019 12 (3) 3 (4)
Phomopsis phaseoliDiaporthe phaseolorum (Teleomorph)20112011 1 1
Didymella microchlamydospora 20192019 1 1
Edenia gomezpompae 20132013 1 1
Emarellia grisea 20162016 1 1
Emarellia paragrisea 20162016 1 1
Emergomyces africanus 201720192 3 5
Emergomyces canadensis 201820181 1 1 3
Emergomyces orientalis 20172017 1 1 2
Emergomyces pasteurianus 201520201 21 5 9
Emmonsia crescens 196420121 117 2 1 22
Engyodontium album 19832016 11 (2) 2 1 5 (6)
Beauveria albaEngyodontium album19841984 1 1
Epicoccum nigrum 19972020 1 2 3
Setosphaeria holmiiExserohilum holmii20182018 1 1
Falciformispora senegalensis 20142014 1 1
Fuscoporia ferrea 20102010 1 1
Geomyces pannorum 20032008 3 3
Cephalosporium serraeGibellulopsis serrae19741974 1 1
Acremonium polychromumGliomastix polychroma20042004 1 1
Graphium basitruncatum 200720172 1 3
Gymnascella dankaliensis 19892007 2 2
Hongkongmyces pedis 20142014 1 1
Hormographiella aspergillata 19962019 32 111 1 3 21
Hypocrea orientalis 20082008 1 1
Inonotus (Phellinus) tropicalis 200520171 1 1 2 5
Isaria farinosa 20132013 1 (2) 1 (2)
Paecilomyces fumosoroseusIsaria fumosorosea20152015 1 1
Knufia epidermidis 20192019 1 1
Laetisaria arvalis 20182018 1 1
Botryodiplodia theobromaeLasiodiplodia theobromae19751976 1 1 2
Malbranchea pulchella 19511994 1 1 2
Medicopsis romeroi 20162019 1 1 17 10
Metarhizium anisopliae 19972017 4 1 5
Metarhizium pingshaense 20172017 1 1
Metarhizium robertsii 20172017 1 1 2
Paecilomyces viridisMetarhizium viride19751975 1 1
Microcyclosporella mali 20152015 1 1
Fusarium nivaleMicrodochium nivale19661966 1 1
Monascus ruber 20102018 1 1 2
Mycotypha microspora 20182018 1 1
Myriodontium keratinophilum 19851985 1 1
Ramichloridium schulzeriMyrmecridium schulzeri19851985 1 1
Nannizziopsis obscura 201720171 1 1 3
Nattrassia mangiferae 19972010 34 (5) 7 (41) 14 (49)
Hendersonula toruloideaNattrassia mangiferae19702004 1 34 35
Acremonium falciformeNeocosmospora falciformis197620191 3 2 1 10 17
Neocucurbitaria keratinophila 20192019 2 1 3
Nigrograna mackinnonii 20132020 4 4
Onychocola canadensis 19942016 17 17
Ophiostoma piceae 20092009 1 1 2
Ovadendron sulphureo-ochraceum 19951995 1 1
Paecilomyces formosus 20162017 1 1 2
Paecilomyces marquandii 19792000 2 2
Thermoascus taitungiacusPaecilomyces taitungiacus (Anamorph)20012001 1 1
Paecilomyces variotii 198120196 (7)342 310 (12)11 (4)10 (12)22 1 (2) (1)8 (9) 53 (64)
Paecilomyces variotiPaecilomyces variotii (Orthographic Variant)197119981 2 32 1 11 11
Pallidocercospora crystallina 20192019 1 1
Parathyridaria percutanea 20192019 1 1
Pestalotiopsis clavispora 20132013 1 1
Petromyces alliaceus 20072007 1 1 2
Phaeoisaria clematidis 20002000 1 1
Phanerochaete chrysosporium 20142014 1 1
Phanerochaete sordida 20172017 1 1
Pleurostoma ootheca 20142014 1 1
Pleurostoma richardsiae 201720191 1 1 0 2 5
Podospora austroamericana 20182018 1 1
Pseudopestalotiopsis theae 20192019 1 1
Pseudotaeniolina globosa 200320031 1
Purpureocillium lilacinum 20112020119 33 2 9 28
Pythium insidiosum 1993202115136 21 1111 114 65
Ramichloridium obovoideumRamichloridium makenziei19881999 3 3
Rasamsonia aegroticola 20152017 1 3 1 1 1 11 9
Rasamsonia argillacea 201020181(3) (1)5 (13) (1) (1) 6 (20)
Geosmithia argillaceaRasamsonia argillacea20102015 3 18 1 1 14
Penicillium emersoniiRasamsonia emersonii19991999 1 1
Rasamsonia piperina 20162019 1 1 1 3
Rhizoctonia solani 20122013 1 1 2
Rhytidhysterium rufulum 20142018 4 4
Roussoella solani 20172017 1 1
Sarocladium kiliense --(5) (7) (1)(2) (1)(2) (2) (10) (30)
Acremonium kilienseSarocladium kiliense198120175 6 12 12 2 8 27
Cephalosporium maduraeSarocladium kiliense19621966 2 2
Cephalosporium niveolanosumSarocladium kiliense19601960 1 1
Acremonium strictumSarocladium strictum19842015721 8 2311 1 9 35
Stachybotrys atra 19991999 3 3
Stachybotrys chlorohalonata 20212021 1 1
Stachybotrys eucylindrospora 20142014 1 1
Thermoascus aurantiacus 19671967 1 1
Thermoascus crustaceus 20102019 2 4 6
Thielavia subthermophila 20092011 11 2
Tilletiopsis minor 19972018 11 1 3
Tintelnotia destructans 20182019 2 2
Toxicocladosporium irritans 20112011 1 1
Triadelphia pulvinata 200120131 1 2
Trichoderma bissettii 20142014 11 1 1 4
Trichoderma citrinoviride 199920081 1 2
Trichoderma harzianum 19962014111 23 1 1 10
Trichoderma longibrachiatum 1995201923 2 69 472 5 40
Trichoderma orientale 201420141 11 1 1 5
Trichoderma pseudokoningii 19952000 1 1 1 1 4
Trichoderma viride 19762005 2 21 5
Tritirachium oryzae 20102018 4 4
Tritirachium roseum 19751975 1 1
Truncatella angustata 20152015 1 1
Stemphylium lanuginosumUlocladium lanuginosum19831983 1 1
Ustilago echinata 20162016 1 1
Ustilago esculenta 19962007 2 2
Valsa sordida 20062008 21 3
Westerdykella dispersa 201420181 1 2
Xanthothecium peruvianum 20172017 1 1
Acremonium recifeiXeneoacremonium recifiei19792010 2 3 5
Xylaria enteroleuca 20062006 1 1
Total---6296699582591210462511143333541182522147462139249974110,435
CNS: central nervous system; ORL: oto-rhino-laryngological; OA: osteo-articular; and (nb): number of publications corresponding to all isolates from the same species on the basis of their current taxonomic.
Table
Table 2. Anatomical sites and nosological framework of the different taxa. CNS: central nervous system; and ORL: oto-rhino-laryngological. The numbers in the table correspond to PMIDs.
Table 2. Anatomical sites and nosological framework of the different taxa. CNS: central nervous system; and ORL: oto-rhino-laryngological. The numbers in the table correspond to PMIDs.
AspergillusDematiaceousPseudallescheria/ScedosporiumOtherMucoralesFusariumPenicilliumTotal
 Systemic19375105564613854678
Anatomical site
 Unspecified19 8 182 47
 Blood914978241312831427
 Bone marrow5124 1325
 Lymph nodes171576221057
Semiology
 Aortitis2966111 44
 Vasculitis324421125 78
 CNS288205133384183710
Anatomical site
 Unspecified1273946162522255
Specimen
 Brain abscess79114591383 273
Semiology
 Encephalitis1411 6
 Mass3719345 67
 Meningitis392517333193
 Meningo-encephalitis5471 16
 Ocular3211681471552020791021
Anatomical site
 Unspecified42928724194
 Conjonctival6232 13
 Orbital2028531 38
Specimen
 Lacrimal fluid 3 211 7
Semiology
 Blepharitis1 1
 Endophthalmitis873943194413240
 Granuloma5 5
 Keratitis15711663121101615623
 Auditory system193172981316263
Anatomical site
 Unspecified1781013 38
Semiology
 Implant-associated otomycosis 11 1 3
 Otomycosis1768187916222
 Dental and gums551 1113
Anatomical site
 Unspecified44 1110
Specimen
 Abscess 11 2
Semiology
 Peridontitis1 1
 ORL sphere6581538713317938221246
Anatomical site
 Unspecified5 11 119
 Cervical lymphadenopathy1 1
 Laryngeal181 1 222
 Nasal 8123511784139
 Oesophagus733114222
 Oral mucosa2072352 39
 Rhinitis 1 1
 Rhino-facial131479 60
 Rhino-orbital51861133 105
 Rhino-orbito-cerebral20 1964 89
 Rhino-sinusal28287513841178514
 Sino-oral113 381 26
 Tongue7 1 9
 Tonsil 1 1
 Tracheal1036105931135
Semiology
 Fungus ball44874 2162
 Pharyngeal abscess3 3
 Pharyngitis42 39
 Pulmonary308823842421829251654353
Anatomical site
 Unspecified208132513219 287
 Lower respiratory tract9991001669312120221509
 Lymph nodes84138132112141
 Mediastinum372234 48
 Parenchymal cavity 331124682816430
 PleurisyPleura74111381115125
 Upper respiratory tract694481113431812934
Specimen
 Abscess40313621 63
Semiology
 Hypersensitivity/Allergy 1068 3 13120
 Invasive389912142819462
 Pneumonia 1261928232586234
 Breast731211116
Anatomical site
 Unspecified13 111 7
 Breast implant2 11 4
 Nipples1 1
Specimen
 Milk3 14
 Heart21931542429133372
Anatomical site
 Unspecified374111164 74
 Myocardium3039242 49
 Pericardium233352 237
 Thrombus8 2 1 11
Semiology
 Implanted device endocarditis 55141210 2196
 Native valve endocarditis 66717665 105
 Digestive149494354942212422
Anatomical site
 Unspecified9244131336
 Appendix1 23 6
 Biliary tract632 11
 Bowel1413591336
 Gastric10115151 34
 Pancreas7 3 31 14
 Peritoneum43327271681135
 Spleen335153186180
Specimen
 Abscess2 111 5
 Faecal specimen1545663443
Semiology
 Colitis2 2 1 5
 Enteritis2 16 9
 Mucosal necrosis51 31 10
 Liver431017113442120
Anatomical site
 Unspecified2781710233289
Specimen
 Abscess111 1110 24
 Ascites fluid31 1 5
Semiology
 Hepatitis2 2
 Urinary tract15916511461161314
Anatomical site
 Unspecified3 3
 Bladder61 4 11
 Kidney86103094671185
 Prostate gland711 1 10
Specimen
 Urine28313278 62
Semiology
 Mass26 2 1 29
 Pyelonephritis21232 9
 Urinary tract infection1 3 1 5
 Genital913161 21
Anatomical site
 Unspecified3 3
 Epididymis 1 1
 External genitalia 3 1 4
 Glans1 31 5
 Ovaries 1 1
 Testis4 4
 Vaginal mucosa1 11 3
 Osteo-articular system287841512228194589
Anatomical site
 Unspecified38918492 79
 Joint26821141 60
Specimen
 Synovial fluid81320114 46
Semiology
 Arthritis61328326 57
 Bursitis 1 1
 Mass (including mycetoma)63 9
 Osteomyelitis1473555121154266
 Spondylodiscitis5629111 71
 Skeletal muscles21848231 61
Anatomical site
 Unspecified21848231 61
 Soft-tissue44132112504 137
Anatomical site
 Unspecified44132112504 137
 Skin system4571154239361376270232801
Anatomical site
 Unspecified4376175265 173
 Nails931563773651394
 Subcutaneous 5634347788425 610
 Superficial cutaneous 21537091149248139211195
Semiology
 Dermatitis12 11117
 Intertrigos 1 1
 Mycetoma 151556446 16 282
 Tinea capitis11 2
 Tinea corporis 1 3 4
 Tinea manuum 3 3
 Tinea pedis 8 1 9
 Ulcer33391711418 121
Endocrine gland407184152 84
Anatomical site
 Unspecified 12 3
 Adrenal72 31 13
 Parathyroid1 1
 Thymus 1 1
 Thyroid324164111 66
Placental infection1 1
Anatomical site
 Placenta1 1
Total6182223715281121130879720613,222
Table
Table 3. Details of cardiac sites affected by native valve endocarditis and associated species.
Table 3. Details of cardiac sites affected by native valve endocarditis and associated species.
Current NameTricuspid ValveMitral ValveAortic ValveAll 4 ChambersMural EndocardiummPulmonary ValveAtriumVentricleND
Absidia corymbifera1 [65]
Arnium leporinum 1 [66]
Arthrographis kalrae 1 [67]
Aspergillus clavatus 1 [68]
Aspergillus flavus6 [69,70,71,72,73,74]9 [69,73,75,76,77,78,79,80,81]2 [74,82]
Aspergillus fumigatus4 [83,84,85,86]18 [87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104]10 [100,105,106,107,108,109,110,111,112,113]2 [114,115]2 [116,117]2 [116,118]3 [119,120,121] 2 [122,123]
Aspergillus nidulans 1 [124]
Aspergillus niger 1 [125]
Aspergillus terreus1 [126]2 [126,127]1 [128]1 [126] 1 [127] 1 [129]
Aspergillus udagawae 1 [130]
Cunninghamella bertholletiae 1 [131] 1 [132]
Engyodontium album 1 [133]
Exophiala dermatitidis 1 [134]
Fusarium incarnatum 1 [135]
Fusarium solani 1 [136]1 [137] 1 [138]
Fusarium solani complex 1 [139]
Lomentospora prolificans 1 [140]
Myceliophthora thermophila 1 [141] 1 [142]
Paecilomyces javanicus 1 [143]
Phaeoacremonium parasiticum1 [144]1 [144]1 [144]
Phialemonium obovatum1 [145] 1 [146]
Pseudallescheria boydii1 [147]3 [148,149,150] 1 [151]
Saksenaea vasiformis 1 [152]
Scedosporium apiospermum 1 [153]
Scedosporium boydii 1 [154]
Scedosporium inflatum
Scedosporium prolificans1 [155]2 [156,157]2 [158,159] 1 [160]
Trichoderma longibrachiatum 1 [161]
Total164124334718
ND: not determined.
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Menu, E.; Filori, Q.; Dufour, J.-C.; Ranque, S.; L’Ollivier, C. A Repertoire of Clinical Non-Dermatophytes Moulds. J. Fungi 2023, 9, 433. https://doi.org/10.3390/jof9040433

AMA Style

Menu E, Filori Q, Dufour J-C, Ranque S, L’Ollivier C. A Repertoire of Clinical Non-Dermatophytes Moulds. Journal of Fungi. 2023; 9(4):433. https://doi.org/10.3390/jof9040433

Chicago/Turabian Style

Menu, Estelle, Quentin Filori, Jean-Charles Dufour, Stéphane Ranque, and Coralie L’Ollivier. 2023. "A Repertoire of Clinical Non-Dermatophytes Moulds" Journal of Fungi 9, no. 4: 433. https://doi.org/10.3390/jof9040433

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