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Title: Molecular Epidemiology of Agents of Human Chromoblastomycosis in Brazil with the Description of Two Novel Species}
Article:
Abstract:
The human mutilating disease chromoblastomycosis is caused by melanized members of the order Chaetothyriales. To assess population diversity among 123 clinical strains of agents of the disease in Brazil we applied sequencing of the rDNA internal transcribed spacer region, and partial cell division cycle and β-tubulin genes. Strains studied were limited to three clusters divided over the single family Herpotrichiellaceae known to comprise agents of the disease. A Fonsecaea cluster contained the most important agents, among which F. pedrosoi was prevalent with 80% of the total set of strains, followed by 13% for F. monophora, 3% for F. nubica, and a single isolate of F. pugnacius. Additional agents, among which two novel species, were located among members of the genus Rhinocladiella and Cyphellophora, with frequencies of 3% and 1%, respectively.
Introduction:
Chromoblastomycosis is a chronic granulomatous infection of the skin caused by melanized fungi. It has a worldwide distribution mainly in tropical and subtropical climate zones, with a preference for humid climates with dense forestation, with Cladophialophora carrionii being the only species that is restricted to semi-arid areas with Cactaceae as main vegetation. Endemic areas are in Japan, Southeast Asia, Australia, Madagascar, as well as South and Central America[1–7]. In Brazil, the infection is observed in all states, with an estimated prevalence of 1/196 thousand inhabitants, but in some hyperendemic regions a considerably higher prevalence is noted[8]. Infection is assumed to occur through accidental inoculation of the fungus via contaminated plant debris, being favored by agricultural activities denoting an occupational nature of the disease. Chromoblastomycosis is one of the most frequent implantation mycoses found among rural populations[2, 8–11]. Clinically, the disease is characterized by pseudoepitheliomatous hyperplasia with epidermal microabscesses and dermal granulomata[12, 13]. The disease has a slow evolution, but finally may result in disfigurement of affected body sites[8]. The initial lesion is noted as a small pink papule at the site of inoculation which gradually enlarges. Development of superficial erythematous plaques with scaly or warty appearance probably takes several months or years. As a result of acanthosis these lesions may develop into large papillomatous and verrucous warts. Species of the humid climate are particularly members of the genus Fonsecaea, with F. pedrosoi, F. monophora and F. nubica as prevalent agents[14–17]. Recently another species, F. pugnacius was described[18]. Rhinocladiella aquaspersa is an uncommon species of humid as well as of dry climates[19]. Other reported agents such as Phialophora verrucosa and Exophiala dermatitidis[17, 20] are extremely rare and mostly cause other types of infections. Fonsecaea pedrosoi is nearly exclusively isolated from chromoblastomycosis, while F. monophora repeatedly causes brain infection and F. pugnacius combines the two disorders by starting as chromoblastomycosis with cerebral dissemination in a single patient[18]. Species distinction of agents of the disease is clinically significant because of the differences in prognosis of the infection. The present study evaluates the diversity of agents in endemic areas of Brazil based on multilocus sequence data, clinical aspects, direct mycological examination and culture. An enumeration of currently proven cases with molecular support in endemic areas in Brazil is provided.
Discussion:
In this study, we describe two novel species of black fungi causing chromoblastomycosis infections. Among a set of 123 strains from cases of this disease, representatives of three genera were recognized, i. e. Fonsecaea, Rhinocladiella, and Cyphellophora. No member of Cladophialophora was encountered, which is explained by climatic conditions, as C. carrionii is prevalent in arid environmental conditions. In Brazil C. carrionii is rarely reported[24, 25]. The prevalent species in humid tropical climates of South America remains Fonsecaea pedrosoi, followed by F. monophora[2], while the latter species is predominant in southern China[26]. All four species of genus Fonsecaea related to chromoblastomycosis were found in the Brazilian endemic area. Judging from literature data, F. pedrosoi and F. nubica seem to be pathogens that are strictly associated with chromoblastomycosis, while F. monophora and F. pugnacius show some degree of neurotropism eventually leading to dissemination to the brain and other organs[14, 27]. The genus Cyphellophora is characterized by phialides producing sickle-shaped, septate conidia[28]. The group clusters with some phialidic species with small, one-celled conidia. Although the generic type species of Phialophora, P. verrucosa clusters in the ‘carrionii-clade’ distant from Cyphellophora, Feng et al.[22] classified them in Phialophora on morphological criteria. Later Réblová et al.[29] took phylogeny as the leading principle and reclassified all species of the ‘europaea-clade’ in Cyphellophora, the only genus of the newly established family Cyphellophoraceae. Since the taxonomy of Chaetothyriales is in a flux with numerous species to be added, we judge establishment of categories above the species level premature. Currently, phylogenetic data do not match with any other criterion established thus far in Chaetothyriales[21], and therefore phylogenetic genera and families in this order inevitably will remain counterintuitive. Cyphellophora ludoviensis is not effective to produce conidia on common mycological media; it was placed in the genus based on DNA sequence analyses. Members of the genus Cyphellophora colonize different habitats including, in addition to humans, plant debris, ant nests and abiotic substrates[22]. Our species is genetically close to C. capiguarae, described as living in association with ants( Atta capiguara), and to C. oxyspora from decaying leaves[30, 31]. Other members of Cyphellophora originate from mild cutaneous infections in humans, mostly from skin and nails[22]. Cyphellophora europaea in particular has been encountered globally as an agent of mild skin disease and onychomycosis[31] and was noted co-occurring with dermatophytes, mainly Trichophyton rubrum affecting the skin of diabetic patients[32]. Environmental strains of this species were found in indoor wet cells, such as bathrooms and washing machines[33, 34]. Cyphellophora ludoviensis is the first species in the Cyphellophoraceae that had muriform cells in tissue and showed acanthosis rather than necrosis; on the basis of these features the infection was classified as chromoblastomycosis. The new species Rhinocladiella tropicalis is a cryptic species close to R. phaeophora and R. aquaspersa. Rhinocladiella phaeophora was known from a single strain recovered from maize field soil in Colombia[35]. It has recently been reported from a case of human chromoblastomycosis, but the sequence of this strain was not available for comparison[36]. This report nevertheless suggests that all members of the cluster consistently are able to cause chromoblastomycosis when inoculated into human skin. Rhinocladiella aquaspersa is a classical agent of chromoblastomycosis, nearly all cases having been reported from the American continent[19], but the majority of historical clinical cases have not been verified by sequence data. Strain CBS 132913 was originally reported as R. aquaspersa but was found to be 100% identical with R. tropicalis. The three species are phenotypically and clinically similar, but their sequence diversity interferes with molecular recognition of R. aquaspersa as a single species. According to Chen et al.[37] the term ‘species complex’ could be applied used to indicate closely related species do not seem to differ in clinically relevant parameters. The present rhinocladiella-like lineages have sufficient molecular distance to be recognized as species, but additional studies of antifungal susceptibility, clinical course, virulence and physiology are needed to verify significance of distinction of the three agents as individual species in hospital routine. Chromoblastomycosis is clinically highly variable, with six different clinical types[8, 38]. Despite the polymorphic nature of lesions, common factor at the patient side is the absence of necrosis and often even hyper-growth of dermal tissues, which distinguishes the disease from its clinical counterpart, phaeohyphomycosis. At the fungal side, the invasive form is the muriform cell, which is likely to be the cause of the growth-promoting dermal response. As such the disease is polyphyletic within the Chaetothyriales, but has not or extremely rarely been observed outside this order. In both cases caused by these two new species here described it was encountered polymorphic lesions frequently related to clinical cases of chromoblastomycosis[8]. In the State of Maranhão, Brazil, five chaetothyrialean agents of chromoblastomycosis are endemic. A potential source of infection has been suggested[39] to be the harvest of babassu coconuts from a wild palm tree( Orbignya phalerata). A large part of the local rural population is involved in the collection of nuts to extract babassu oil, an important component for local and international beauty product manufacturers. Members of Chaetothyriales are indeed enriched on babassu shell fragments, which are considered a risk factor for developing chromoblastomycosis after trauma sustained at work[39, 40]. A direct link between shells and agents of the disease has however not unambiguously been established. In other Brazilian regions the number of new cases of chromoblastomycosis is decreasing[8, 41, 42]. This is thought to reflect changes in agricultural practices, the extensive use of agricultural antifungals, especially azole derivatives, and the progressive mechanization of plantations resulting in a reduction of the risk of occupational exposure[8, 43, 44]. Our results showed that C. ludoviensis and R. tropicalis had their optimal development at 30 and 27°C, respectively, the maximum growth temperature of all strains analyzed being at 37°C. The chronic nature of the infection corresponds with borderline survival of the fungus in tissue. Epidermal temperatures are usual below 37°C, allowing infection by fungi that barely support this temperature. This agrees with the clinical observation that members of the Cyphellophoraceae( ‘europaea-clade’), which have their maximum growth at 36°C, cause only mild, superficial infections, having a very low degree of invasive ability and virulence[22]. According to the World Health Organization( WHO)[45] the Neglected Tropical Diseases include a series of endemic diseases that prevail in tropical or subtropical areas worldwide. The prevalence of causative microbes is linked to poverty and disadvantage. However, fungal diseases were still not included in this list, except mycetoma, another implantation mycosis[46]. Chromoblastomycosis has been reported in the literature as an overlooked disease[11]. Its global burden is comparable to or greater than that of mycetoma. Considering to its global distribution, its impact on the impoverished, and its refractoriness, it also should be considered a true neglected disease as defined by WHO.
Chromoblastomycosis , a skin disease found among rural populations in tropical and subtropical regions , is caused by melanized fungi related to the black yeasts . The present study evaluates the species distribution among 123 clinical strains from endemic areas in Brazil based on multilocus sequence data , and describes two new agents of the disease which proved to be affiliated to Rhinocladiella and Cyphellophora .