Fungi are gaining importance with the increased recognition of chronic, often fatal mycoses in immunocompromised patients. This Atlas means to stimulate interest in the identification of pathogenic and opportunistic agents. Increasing precision of identification can augment adequate and timely therapy. We hope the user will publish cases of new mycoses and deposit voucher specimens in recognized culture collections, so that a more balanced picture of the diversity of clinical fungi can be built up. Those particularly at risk are patients with leukemia, solid tumours, AIDS, transplants, or ketoacidotic diabetes. Hospitalised patients who have undergone major surgery or suffer from circulation failure or extended burn wounds and those subjected to prolonged radiotherapy, corticosteroids, cytostatics or antibiotics are also susceptible to mycotic infection. The number of uncommon infections in bone marrow transplant (BMT) patients is increasing rapidly. Mycoses decrease the chance of recovery of these patients and can seriously hamper the improvement of their quality of life. The taxonomic diversity of etiologic agents seems to be widening. In addition to long established mycoses caused by dermatophytes, systemic dimorphic fungi, Candida, Cryptococcus and Aspergillus, moulds and yeasts are encountered which were formerly only known to be saprobic. A surprisingly large number of these species are now seen to survive in human tissue. However, whether or not new fungi are emerging as clinical agents is difficult to verify with certainty. Comparison with older literature is often impossible, because many fungi have been described under names which have not been clarified. In the period between 1920 and 1940 a wide variety of purported pathogens were described whose identity is still uncertain. Therefore the same fungi may later have been described again under a different name. An example is Scedosporium boydii. This species is now emerging as an agent of systemic mycoses. However, the same fungus, under the name Glenospora graphii had already been described before 1900 as an agent of otitis externa. It is likely that the etiologic agents of many of these infections have frequently been misdiagnosed as aspergillosis. Correct identification of the etiologic agent gives an impression of emerging appearance. Numerous fungi could not be recognized in the past because of absence of sporulation and thus lacking diagnostic characters. With modern molecular diagnostics this problem has been solved and thus large numbers are being identified that we previously only knew from the environment. The vast number of reports of unverified names, listed in the Atlas under the heading ‘doubtful’, actually indicates that fungi were clinically relevant long before the emergence of the ‘modern’ hospital mycoses. Comparison of historic and recent fungal overviews will be possible when obsolete names have been clarified. This Atlas contains a full nomenclature of each species, and is supplemented by a checklist of every fungal name which has appeared in medical literature. Proper recognition of rare agents of disease necessitates the availability of a broad taxonomic skill and experience in clinical laboratories, to correctly interpret molecular and automated identifications. Incorrect identification has a negative impact on the growth of knowledge and understanding of these mycoses. Uncommon agents are often identified by comparing the fungus at hand to the limited species lists published of major handbooks in medical mycology. But many of these lists are incomplete. When cases are ‘recognized’ on the basis of such insufficient data, the supposed restricted etiology of the respective mycosis becomes self-fulfilling. Erroneous identifications tend to persist in the literature. In a number of opportunistic clinical settings, such as in mycetoma, the spectrum of agents is probably much larger than generally supposed. Conversely, current sequence-based identification enables identification of species that were not recognized as agents of disease, and may concern contaminants. This Atlas mainly accepts species for which at least one proven case report has been published.
Organization of the Atlas
The main aim of the Atlas is to illustrate the diversity of fungal agents. For detailed clinical data we refer to specialised handbooks, of which Badillet et al. (1986), Rippon (1988), Kwon-Chung & Bennett (1992) and Dismukes et al. (2003) are particularly recommended. Excellent overviews of histopathology of major mycoses are those of Chandler et al. (1980) and Salfelder (1990, 2000). The rare opportunists, with which most clinicians are unfamiliar, are dealt with in detail in this Atlas. Each fungus is described with colony characteristics on one of the recommended identification media after 14 days incubation at room temperature (unless stated otherwise). Colony diameters may vary but fall roughly into three categories: rapidly expanding (over 4 cm), moderate (2-4 cm) or slow, restricted (less than 2 cm). Microscopy of asexual / sexual (anamorph / teleomorph) phases shown in species where both forms are commonly observed in culture. Physiological profiles are provided for all yeasts, yeast-like fungi, and for a limited number of filamentous fungi. In addition, literature data are provided. Occasionally a brief differential diagnosis is given to segregate the species from its neighbouring species including saprobic taxa. This has systematically been done with the yeasts, using physiological characteristics; data for this comparison have been taken from Barnett et al. (1990) and Kurtzman et al. (2011). Pathogenicity of established species is briefly described in the chapter on clinical pathology; essential references and exceptional cases are listed under each species. With each species RG and BSL attributions are given according to the most widely accepted classification (de Hoog, 1997). The normal ecological niche of opportunistic fungi is supposed to be in environments outside the human or animal body. Data on antimycotic susceptibility are partly taken from the literature. Finally, with each fungus some selected references for taxonomic data and further reading are given, plus full nomenclature. Note that separate naming of sexual and asexual (teleomorph / anamorph) has been abandoned, but nomenclatural rules are somewhat inconsistent and not yet applied on every single species. Several fundamental problems were encountered during compilation. Reported new fungal agents should match the first description of that species. Unfortunately, the state of taxonomy in many groups is insufficient to be certain of such matching. Species occurring in nature may be very similar but not identical to their pathogenic counterparts. In the case of rare mycoses we have used type or representative strains of that species. Often the strain from the case report is no longer available, thus it sometimes remains uncertain whether the actual opportunist being described.
All those who have helped us in collecting the data used in the Atlas are gratefully acknowledged: Bert Gerrits van den Ende, Kasper Luijsterburg, Gé Poot, Francis Snippe-Claus, Marlene Setropawiro, Marjan Vermaas, Rina Verwoerd-Kuyt, and all staff members who provided us with media, equipment and facilities. Molecular data were kindly provided by Derlene Attili, Rachel Caligiorne, Eric Dannaoui, Shuwen Deng, Yvonne Gräser, Cecile Gueidan, Gerhard Haase, Regine Horré, Isabel Iturrrieta González, Natteewan Poonwan, Deanna Sutton, Vania Vicente, Katja Sterflinger; Nadja Yurlova, Jingsi Zeng and many other guest workers at CBS; numerous sequences were taken from the public domain. Antifungal susceptibility data were provided by G. Quindós, B. Fernández-Torres, M. Ortoneda and I. Pujol. Data on yeasts were donated by Claudia Cafargia, Eveline Guého, Yingqian Kang, Marie-Louise Kerkmann, Kyun-jo Kwon-Chung, Maudy Smith and David Yarrow; Emory Simmons commented on Dematiaceae. We thank Hub van der Aa, André Aptroot, Hamid Badali, Anne van Diepeningen, Somayeh Dolatabadi, Peiying Feng, Elke Göttlich, X. Guan, Eveline Guého, Vit Hubka, Richard Humber, Macit Ilkit, Connie Jacobs-van Oorschot, Hazal Kandemir, Dongming Li, Qirui Li, Michael McGinnis, Frank Odds, Elisabeth Presterl, Yu Quan, Dongming Shi, Derek Sullivan, Richard Summerbell, Chao Tang and Yu Zhang for their comments on and additions to parts of the manuscript and illustrations. C.M. Aliouat-Denis, M. Chabé, Eduard Dei-Cas, Henrik Elvang Jensen, Matthew Fisher, Hein van der Lee, Lizel Mostert, Rui Kano, Ton Rijs, Janos Varga, Rob Verdijk, Alieke Vonk, Yanping Jiang and Neriman Yilmaz provided significant contributions to individual chapters. Sevtap Arikan and Ana Alastruy-Izquierdo donated antifungal susceptibility data. Thomas Weniger and Dag Harmsen were involved in the electronic version of the Atlas. We thank Tineke van den Berg-Visser for excellent secretarial help. Samira Boughrini, Jongsoo Choi, Bita Tarazooie and Leo Yang assisted with tables and illustrations. We are indebted to Shuwen Deng, Jingsi Zeng, Dongmei Shi, Peiying Feng, Ruoyu Li, Weida Liu, Yinggai Song and Nadja Yurlova who are involved in translation of the Atlas in alternative languages. We are also indebted to the Curators of the following culture collections for supplying cultures: AMMRL, ATCC, CDC, FMC, IFM, IFO, IMI, IP, NCPF, NHL, RV, TRTC, UAMH, UTHSC and WCLR. We would also like to acknowledge Vincent Robert and the BioAware team for their support to transfer all the data to BioloMICS software.
Hilversum / Reus, 1 January 2021