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The Genus Madurella: Molecular Identification and Epidemiology in Sudan

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The Genus Madurella: Molecular Identification and Epidemiology in Sudan PLOS NEGLECTED TROPICAL DISEASES RESEARCH ARTICLE The genus Madurella: Molecular identification and epidemiology in Sudan 1 2 3 2 Elhadi A. AhmedID *, Bakri Y. M. Nour , Adam D. Abakar , Samirah Hamid , Ahmed 4 5 5 6 A. Mohamadani , Mohamed DaffallaID , Mogahid Mahmoud , Hisham N. Altayb , Marie Desnos-Ollivier7, Sybren de Hoog8,9, Sarah A. Ahmed8,9,10 1 Department of Medical Microbiology, Faculty of Medical Laboratory Sciences, University of Gezira, Sudan, 2 Blue Nile National Institute for Communicable Diseases (BNNICD), University of Gezira, Sudan, 3 Department of Medical Parasitology, Faculty of Medical Laboratory Sciences, University of Gezira, Sudan, 4 Department of Pathology, Faculty of Medicine, University of Gezira, Sudan, 5 Department of Surgery, Faculty of Medicine, University of Gezira, Sudan, 6 Biochemistry Department, Faculty of Sciences, King Abdulaziz University, Saudi Arabia, 7 Institut Pasteur, Molecular Mycology Unit, National Reference Center for Invasive Mycoses and Antifungals, Paris, France, 8 Foundation Atlas of Clinical Fungi, Hilversum, The Netherlands, 9 Center of Expertise in Mycology of Radboud University Medical Center / Canisius Wilhelmina a1111111111 Hospital, Nijmegen, The Netherlands, 10 Faculty of Medical Laboratory Sciences, University of Khartoum, a1111111111 Khartoum, Sudan a1111111111 a1111111111 * [email protected] a1111111111 Abstract Eumycetoma (mycotic mycetoma) is the fungal form of mycetoma, a subcutaneous infection OPEN ACCESS occurring in individuals living in endemic areas of the disease. The Sudan is hyperendemic Citation: Ahmed EA, Nour BYM, Abakar AD, Hamid for mycetoma, with the highest incidence being reported from Gezira State, Central Sudan. S, Mohamadani AA, Daffalla M, et al. (2020) The The present study was conducted at the Gezira Mycetoma Center and aimed to determine genus Madurella: Molecular identification and epidemiology in Sudan. PLoS Negl Trop Dis 14(7): the cause of black-grain eumycetoma in the state and describe its epidemiology. Black- e0008420. https://doi.org/10.1371/journal. grain specimens were collected during the surgical operation and direct detection of the pntd.0008420 causative agent was performed using M. mycetomatis species-specific PCR and ITS PCR Editor: Abdallah M. Samy, Faculty of Science, Ain followed by sequencing. Black-grain was reported from 93.3% of all confirmed mycetoma Shams University (ASU), EGYPT cases (n = 111/119), with a prevalence in young males. Of the 91 samples subjected to Received: February 12, 2020 direct PCR, 90.1% (n = 82) gave positive results. The predominant species (88.2%) was Accepted: May 23, 2020 Madurella mycetomatis. One sample was identified as M. fahalii, one as M. tropicana, and one matched the phytopathogenic species Sphaerulina rhododendricola. The highest Published: July 30, 2020 endemic zones were Southern Gezira (76.6%) and Northern Sinnar (23.4%). The study con- Copyright: © 2020 Ahmed et al. This is an open firmed that direct molecular detection on grains provides rapid and specific diagnosis of access article distributed under the terms of the Creative Commons Attribution License, which agents of eumycetoma. permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are Author summary within the manuscript and its Supporting Information files. Eumycetoma is a neglected fungal disease endemic in Africa, India, and Latin America. Funding: The authors received no specific funding Black-grain eumycetoma is the most common type in Africa and is mainly caused by for this work. Madurella spp. The Sudan, and in particular Gezira State, central Sudan is hyperendemic for black-grain eumycetoma. Patients with this type of mycetoma are treated with surgery Competing interests: The authors have declared that no competing interests exist. in combination with antifungal therapy. In this study, we collected surgical biopsies from PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0008420 July 30, 2020 1 / 15 PLOS NEGLECTED TROPICAL DISEASES Madurella species in Sudan patients attending Gezira Mycetoma Center to directly identify the etiology of black-grain eumycetoma in this state. We also studied the epidemiology of the disease based on the demography of the patients' population. Our result showed that the highest endemic regions were Southern Gezira (76.6%) and Northern Sinnar (23.4%). By applying direct PCR and sequencing we confirmed that the most common etiology of the disease is Madurella mycetomatis (88.2%). In addition, we found one case of M. fahalii and the first Sudanese case of M. tropicana and Sphaerulina rhododendricola. Introduction Black-grain mycetoma is caused exclusively by fungi, and to date around 23 species have been reported as being responsible for this infection [1, 2, 3]. Agents of black grain mycetoma are affiliated to three orders of Ascomycota, viz. Pleosporales, Sordariales and Chaetothyriales [1]. Although eight species of Chaetothyriales, belonging to Exophiala and Cladophialophora have been incriminated in mycetoma, members of this order are less frequent. The largest diversity of black-grain agents is found in Pleosporales: ten species belonging to eight genera have been reported [1,4, 5, 6]. In contrast, Sordariales harbor only a small number of species able to cause mycetoma, but among these are the predominant agents worldwide in the genus Madurella [7, 8]. Irrespective of phylogenetic positions, all agents of black-grain mycetoma produce similar clinical features, i.e. progressive tumefaction, sinuses, and black grains in discharge or embed- ded in tissue [9]. For this reason, it is difficult to differentiate the 23 species histologically [1,10]. After culturing of the grains, members of Chaetothyriales produce dark olivaceous black colonies and microscopically yeast cells or more or less characteristic conidia [4]. Species of Pleosporales produce dark grey or olive green velvety or woolly colonies, but clinical strains may remain sterile or produce ascomata or conidiomata with delay [6, 11]. Members of Sor- dariales produce brownish to dark yellow or grey colonies which are mostly cerebriform and glabrous or with very short aerial mycelium. Sordariales species usually remain sterile, only chlamydospores or large swollen hyphae being observed [4]. Culture differences can be used for approximate differentiation of agents of the three orders, while identification down to the species level requires molecular techniques [5, 10, 12]. The importance of species identification in black-grain eumycetoma infection has been indicated in several studies [10, 11, 12, 13]. The pathogens differ in susceptibility to antifungal agents, as well as in their epidemiology [12, 14]. For example, in Pleosporales, Medicopsis romeroi showed low susceptibility to several antifungal agents including amphotericin B, flu- conazole, itraconazole and caspofungin [14, 15, 16]. In addition, differences are noted between the closely interrelated species of Madurella in their susceptibility to the main drug used for treating eumycetoma, itraconazole. While M. mycetomatis, the predominant species world- wide, is inhibited by low concentration of itraconazole, M. fahalii has high Minimum Inhibi- tory Concentrations (MICs) to this drug [12, 17]. Of note, the epidemiology of the two species may be overlapping, as both species are found in Sudan [12, 18]. Sudan is a hyperendemic region for mycetoma and it is considered as the disease homeland [2, 19]. The incidence of newly diagnosed cases per year in the Mycetoma Research Centre in Khartoum is 355 [18]. Of the 6,792 patients reported with myceoma in this center, 2,476 patients (37%) were from Gezira State, Central Sudan [18]. Therefore, in 2012, the Gezira Mycetoma Center was established to provide medical care for mycetoma patients in that region. During the period January 2013 to December 2016, a total of 1,654 patients were seen PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0008420 July 30, 2020 2 / 15 PLOS NEGLECTED TROPICAL DISEASES Madurella species in Sudan at the Gezira Mycetoma Center; of them, 584 underwent surgery, including amputation in 71 patients (12.2%). Diagnoses were made by clinical evaluation, imaging, fine-needle aspiration cytology and histology [20]. Although culture and molecular identification of the causative pathogen is considered the gold standard for diagnosis of mycetoma, culturing is rarely performed even in highly special- ized centers [10, 5]. One of the reasons is that mycetoma agents require several weeks to grow, and risks of absence of growth or contamination are very high [10, 21]. Recently, culture-free methods have been introduced for direct detection of agents of eumycetoma in clinical materi- als. These include recombinase polymerase amplification (RPA), loop-mediated isothermal amplification (LAMP), and direct PCR amplification followed by sequencing [22]. Despite the high accuracy of these methods, none of them has been installed for routine diagnostics in endemic regions. In the present study, we applied direct PCR and sequencing for diagnosis of black-grain eumycetoma cases seen at the Gezira Mycetoma Center. Since M. mycetomatis is known as the main agent of mycetoma in Sudan, we also applied species-specific PCR using primers described by Ahmed et al. [25]. Furthermore, we studied the epidemiology of the disease in the Gezira State based on stored information
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