Introduction

2018 marks the eightieth anniversary of the founding of Mycopathologia (Fig. 1). The founding editors Piero Redaelli and Raffaele Ciferri ‘wanted to diffuse the understanding of fungal diseases in man and animals among mycologists’ [1]. This was a critical mission considering that pathogenic fungi for humans and animals represent a tiny minority of the estimated 1.5–5 million fungal inhabitants on Earth [2]. These pathogens have diverged from the usual saprotrophic lifestyles of most fungi to colonize and infect human and animals. Medical and veterinary mycology is the subdiscipline of microbiology that deals with the mysteries of parasitic, fungal lifestyles. Much is now known about the etiology of fungal infections, and the diagnosis and treatment of fungal diseases due to the pioneering efforts of scientists and physicians. At the beginning of the journal, the availability of expertise was patchy around the globe as were the resources, and the integration with related disciplines remains a work in progress. Mycopathologia, one of the oldest scientific publications on the subject, has served the discipline well by enhancing the awareness and understanding of pathogenic fungi for humans and animals.

Fig. 1
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Title page of the first issue of Mycopathologia from 1938

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In the early years, Mycopathologia was closely associated with a large group of physicians and scientists responsible for laying the foundation of the ‘modern era of medical mycology.’ Earlier articles by the two former editors-in-chief, commemorating the twenty-fifth and fiftieth anniversaries of Mycopathologia, respectively, detailed the unique personalities of the early editorial teams and the extraordinary challenges they faced during the war years [1]. The narrative style of these editorials gave a rare behind the scene look at the personalities who were crucial during the formative years of the journal. The commemorative approach was common to that of other journals, an excellent example being the write-up of Edsall about the founding of the Journal of Biological Chemistry and its association with key discoveries in the life sciences [3]. For the eightieth anniversary, we decided to follow a different path in the style, wherein the Management Science journal celebrated its fiftieth anniversary by measuring the journal’s metrics [4].

We summarize the most cited publications from the last eight decades of Mycopathologia to gauge the progress made on understanding medically important fungi. We also examined whether the longevity of Mycopathologia has any implications, especially in an era of the phenomenal growth of new journals for medically important fungi. Among the most common journal metrics, the impact factor (IF) and the total number of citations are widely used to gauge the impact on the field even though the citation counts remain an imperfect measurement [5]. We used two citation databases (Google Scholar and Scopus) to ensure good representations of the Mycopathologia articles [6]. This overview did not include non-English articles and articles describing mycotoxins and plant pathogenic fungi as they constitute a small proportion of nearly 6885 articles published in Mycopathologia.

Distribution of High Citations

We tallied 138 articles into six subcategories (Tables 1, 2) with fifty or more citations (Google Scholar or Scopus 1961–2018) (Tables 3, 4, 5, 6, 7, 8). The distribution of the articles was: experimental mycology (36% articles), diagnostic mycology (16%), ecology and epidemiology (15%), clinical mycology (14%), taxonomy and classification (10%), and veterinary mycology (9%) (Fig. 2). The geographic origin of highly cited articles showed that overwhelming numbers came from USA and Europe, which was especially true for the first 50 years of the journal (Fig. 3). Overall, twenty-five countries on four continents accounted for highly cited articles. This picture is evolving as the community and journal witness more contributions from parts of Africa, Asia, Australia, and South America.

Table 1 Most cited articles published in Mycopathologia 1938–1950
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Table 2 Most cited articles published in Mycopathologia 1951–1960
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Table 3 Most cited articles published in Mycopathologia 1961–1970
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Table 4 Most cited articles published in Mycopathologia 1971–1980
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Table 5 Most cited articles published in Mycopathologia 1981–1990
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Table 6 Most cited articles published in Mycopathologia 1991–2000
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Table 7 Most cited articles published in Mycopathologia 2001–2010
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Table 8 Most cited articles published in Mycopathologia 2011–2018
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Fig. 2
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Distribution of highly cited (> 50 citations in at least one database) publications from Mycopathologia (1961–2018)

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Fig. 3
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Geographic distribution of most cited publications in Mycopathologia (1938–2018)

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Diagnostic Mycology

The challenges in diagnostic mycology received full attention in the initial issues of Mycopathologia with the focus on the laboratory culture of oleaginous yeasts and the value of assimilation and fermentation tests for yeast identifications (Table 1) [7, 8]. Ajello and George [9] published the all-time classic in vitro hair perforation test for the laboratory differentiation of Trichophyton mentagrophytes from T. rubrum (Table 2). Nearly parallel to this discovery was the demonstration of the utility of monospecific antisera for laboratory identifications of yeasts by Tsuchiya et al. [10]. Further refinements of the serological methods were described such as micro-titration, immunoelectrophoresis, and ELISA (Tables 3, 4) [11,12,13]. The differentiation of fungal pathogens was refined by the applications of yeast killer toxins and species-specific exoantigens [14, 15]. Morisita et al. [16] described an early implementation of the culture-independent, molecular diagnosis of pityriasis versicolor by deploying Malassezia species-specific nested PCR test. Another notable innovation was the application of mitochondrial DNA analysis for the typing of Sporothrix schenckii and related fungi (Tables 5, 6) [17, 18]. There were quite a few notable contributions on the laboratory susceptibility testing for antifungals and the relevance of molecular testing in the diagnostic laboratory (Tables 6, 7, 8) [19,20,21,22]. The description of new diagnostic technologies remains a favorite topic of Mycopathologia articles as the discipline moves into exciting areas such as whole genome sequencing, metagenomics, and proteomics [23,24,25].

Experimental Mycology

Experimental mycology included nearly one-third of all highly cited articles published in Mycopathologia starting with an article on yeast pseudomycelia in the very first issue (Table 1) [26]. The experimental results described in the journal covered all facets of medically important fungi and experimental disease models. Among the topics covered were antifungals and inhibitors [27,28,29,30,31,32], biofilms [33,34,35,36,37,38,39], immunity and virulence [25, 40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56], fungal structure, function, and nutrition [26, 57,58,59,60,61,62,63,64,65,66,67], and fungal metabolites and toxins [68,69,70,71,72,73,74,75]. The most common fungal pathogens investigated were Candida albicans and other Candida species followed by Aspergillus fumigatus, Paracoccidioides brasiliensis, Cryptococcus neoformans, Blastomyces dermatitidis, Histoplasma capsulatum, Coccidioides immitis, Saccharomyces cerevisiae, Malassezia species, Rhizopus species, Sporothrix species, and Stachybotrys species. These extensive collections of highly cited publications contain the reports of many trailblazing discoveries. Among the most remarkable publications in experimental mycology was the discovery of a linkage between C. albicans proteolysis and virulence by Staib (Table 3) [76]. Candida proteases are now widely recognized as crucial elements in the infectious processes [77, 78]. Similarly, Buffo et al. [63] described how temperature and pH regulate C. albicans yeast–hyphae transitions (Table 5). The Soll laboratory went on to discover the white-opaque colony phenotype switching, an important developmental pathway with crucial roles in the pathogenesis of candidiasis [79].

Clinical Mycology

Clinical mycology articles with high citations were few and far between in the earlier decades of publication of Mycopathologia most likely because as large case series were not compiled or were published in more clinically oriented journals. The first noteworthy contribution appeared in 1976 on a clinical model of paracoccidioidomycosis based upon a detailed analysis of 46 cases of the disease (Table 4) [80]. The relevance of the clinical model was enhanced subsequently by other investigators with detailed descriptions of the immunopathology of paracoccidioidomycosis [81,82,83]. In the early 1970s, an influential publication described the higher prevalence of pathogenic fungi including known agents of onychomycosis in toenails and toe-webs of diabetic patients [84]. Similarly, Vález and Diaz [85] highlighted the role of saprobic fungi as agents of onychomycosis, and Godoy and colleagues [86] highlighted Fusarium solani and F. oxysporum as agents of onychomycosis (Tables 5, 7). Gupta and Cooper [87] had the unique distinction of publishing the highest cited Mycopathologia article to date that described the antifungal therapy of dermatophytosis (Table 7). Uribe et al. [88] characterized the histopathological changes presented at different stages of chromoblastomycosis, a significant tropical disease caused by black molds. A subsequent publication by Silva et al. [89] documented the extent of chromoblastomycosis in Amazon region with a predominance of Fonsecaea pedrosoi (Table 6). Queiroz-Telles and Santos [90] published an expert opinion on the treatment challenges and available options for chromoblastomycosis in resource-poor parts of the world. Finally, a valuable addition to the growing collection of high-impact publications on chromoblastomycosis came from Lyon et al. [91] who showed clinical evidence of the effectiveness of photodynamic therapy in ten patients (Table 8). Queiroz-Telles’ group have continued their productive work on chromoblastomycosis with a recent update in Clinical Microbiology Reviews [92].

A relatively recent overview of candidiasis by Martins and colleagues [93] was well received for its emphasis on predisposition, prevention and control, and the role of alternative treatment approaches (Table 8). A brief report on the etiologic role of C. albicans in otitis externa received notable citations given enhanced interests in the multidrug resistance C. auris from aural specimens [94, 95]. The reviews of cryptococcosis in Brazil by Rozenbaum et al. [96] and in China by Chen et al. [97] received high citations (Tables 6, 8). The authors highlighted the distribution of different Cryptococcus pathogenic species and molecular genotypes among patients with or without underlying immune deficiencies. The disease pattern in these geographically diverse countries with large populations differed from earlier knowledge of the disease reported from North America. Xi et al. [98] provided a comprehensive clinical and mycological profile of penicilliosis due to Talaromyces (Penicillium) marneffei from Guangdong, China, with strong supportive evidence for the natural distribution of the fungus in Southeast China (Table 7). Xi’s group expanded their excellent overview of the penicilliosis by classifying it as an important emerging disease in China [99]. Other notable contributions in clinical mycology were the overview of filamentous fungal infections among patients receiving hematopoietic stem cell therapy, appropriate laboratory diagnostic methods for coccidioidomycosis, and clinical efficacy and relevance of isavuconazole, then a new triazole antifungal (Table 7) [100,101,102].

Ecology and Epidemiology

The ecology and epidemiology subcategory articles have few common themes: the natural occurrence of pathogenic fungi in the soil, air, and water in diverse habitats; the association of fungal pathogens with birds and other animals in nature; and the epidemiology of dermatophytosis (Tables 2, 3, 4, 5). The evolving appreciation for the extensive occurrence of pathogenic fungi in soil was reinforced with well-documented reports from California, Brazil, Saudi Arabia, and Antarctica [103,104,105,106]. Ajello’s natural history of dermatophytes and related fungi, a citation classic, is a comprehensive description of the natural habitats of Epidermophyton, Microsporum, and Trichophyton since their earliest recognition in 1847 [107]. Sinski and Flouras [108] provided a global picture of the distribution of dermatophytic fungi by comparing their occurrence in the US patients vis-à-vis clinical reports from other parts of the world. The aerial prevalence of fungal pathogens over cities was reported with sophisticated samplers, and the role of aerial microbiota inside the hospitals and damp buildings was correlated with the occurrence of fungal diseases [109,110,111,112]. Littman and Borok [113] brought scientific rigor to the known association of pigeons with Cryptococcus neoformans by carefully delineating the heat tolerance of the pathogen, its survival in the pigeon body and excreta, and the possible carrier role that pigeons play in the urban environments. Over 40 years later, another notable contribution on cryptococcosis was published and concerned the unique ecological niche of Cryptococcus gattii on trees found on the Vancouver Island, British Columbia, Canada (Table 8) [114]. Additional bird associations were reported for Histoplasma capsulatum from Venezuela and thermophilic fungi with the passerine bird species in Britain [115, 116]. Among other notable publications in ecology and epidemiology were Talaromyces (Penicillium) marneffei isolated from bamboo rats in Thailand, black yeasts in public bathwater from Japan, and Aspergillus fumigatus in moldy silage on the Azores Islands (Tables 6, 7) [117,118,119].

Taxonomy and Classification

Taxonomy and classification especially related to yeasts dominated the initial volumes of Mycopathologia [120,121,122,123], and there was an appeal to unify taxonomy, a theme familiar to many of us even today (Table 1) [124, 125]. However, the high-impact contributions to taxonomy and classification in the coming decades were not that many except for the two remarkable contributions on the black yeasts and the serological approaches to yeast classification based upon cell surface antigens (Table 3) [126, 127]. This subcategory has undergone a sort of rejuvenation in Mycopathologia with two articles in the last decade by Profs. de Hoog, Gräser and their colleagues on the re-appraisal of taxonomy and species concept in dermatophytes (Tables 7, 8) [128, 129]. The very high citations and downloads of the two articles suggested that high-quality communications on the taxonomy and classification of medically important fungi remained relevant as this area is transformed with the applications of genome sequencing [130].

Veterinary Mycology

Veterinary mycology-associated reports first appeared in the inaugural issue of Mycopathologia and concerned a case of simian dermatophytosis (Table 1) [131]. This subcategory remained underrepresented until recently. However, the last decade marked the publication of many important descriptions of dermatophytosis, Malassezia and Sporothrix carriage in dogs and cats, respectively (Table 7) [132,133,134,135,136]. There were also notable reports on birds as the carriers of yeasts, especially Cryptococcus species [137, 138]. It is clear that veterinary mycology will be crucial in the coming years because of the emerging consensus on One Health approaches for the welfare of the animal and human health [139].

Concluding Remarks

As we conclude this commemorative article, it is pertinent to ask whether Mycopathologia has met its original mission, if the journal is still providing valuable services to the scientists and physicians interested in pathogenic fungi, and finally, what changes will come as Mycopathologia moves toward its hundredth anniversary in 2038? The answer is an emphatic yes! For the first question with an archive of nearly 6885 articles online and in print (Fig. 2), and each issue continuing the tradition of publishing a mix of articles on pathogenic fungi and fungal diseases. The answer to the second question is complicated as there are many more journals and options for sharing new developments on pathogenic fungi. Thus, Mycopathologia has to seek and share interesting articles with other journals. This is easier to implement, as the investigations of pathogenic fungi have grown manifold with a significant upsurge from the authors in Africa, Asia, and South America (Fig. 3). They are also well represented in the Mycopathologia Editorial Board with more than half of the editors coming from the areas outside of Europe and North America as mentioned earlier. Further answers to questions two and three are tied to the technical and business strengths of our publisher Springer Nature. The publisher is at the forefront of technological changes and business evolution, and indeed, Mycopathologia would be a beneficiary from being part of this progressive company. In recent years, the journal has devoted one-third of its pages annually to the special issues, which bring together recognized experts on a selected topic, and this feature will be further enhanced along with a new feature Mycopathologia Images. We anticipate that emerging and re-emerging fungal pathogens will continue to cause significant health burden in the coming decades [140]. It is, therefore, vital that scientists and physicians continue to collaborate by learning each other’s language for the study of fungal diseases, and Mycopathologia will strive to be their partner in this endeavor to its 100th anniversary in 2038 and beyond.