14
views
0
recommends
+1 Recommend
1 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      A holistic approach to the mycetoma management

      research-article

      Read this article at

      ScienceOpenPublisherPMC
      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Mycetoma, one of the badly neglected tropical diseases, it is a localised chronic granulomatous inflammatory disease characterised by painless subcutaneous mass and formation of multiple sinuses that produce purulent discharge and grains. If untreated early and appropriately, it usually spread to affect the deep structures and bone resulting in massive damage, deformities and disabilities. It can also spread via the lymphatics and blood leading to distant secondary satellites associated with high morbidity and mortality. To date and despite progress in mycetoma research, a huge knowledge gap remains in mycetoma pathogenesis and epidemiology resulting in the lack of objective and effective control programmes. Currently, the available disease control method is early case detection and proper management. However, the majority of patients present late with immense disease and for many of them, heroic substantial deforming surgical excisions or amputation are the only prevailing treatment options. In this communication, the Mycetoma Research Center (MRC), Sudan shares its experience in implementing a new holistic approach to manage mycetoma patients locally at the village level. The MRC in collaboration with Sennar State Ministry of Health, Sudan had established a region mycetoma centre in one of the endemic mycetoma villages in the state. The patients were treated locally in that centre, the local medical and health personals were trained on early case detection and management, the local community was trained on mycetoma advocacy, and environmental conditions improvement. This comprehensive approach had also addressed the patients’ socioeconomic constraints that hinder early presentation and treatment. This approach has also included the active local health authorities, community and civil society participation and contributions to deliver the best management. This holistic approach for mycetoma patients’ management proved to be effective for early case detection and management, optimal treatment and treatment outcome and favourable disease prognosis. During the study period, the number of patients with massive lesions and the amputation rate had dropped and that had reduced the disease medical and socioeconomic burdens on patients and families.

          Author summary

          Mycetoma enjoys all the neglected tropical diseases (NTDs) characteristics. It frequently affects the poorest of the poor in poor communities in remote regions. The affected population are of low socio-economic status, of low visibility and low political and social voice and hence they are neglected. The disease is considered as a social stigma in particularly among females and children thus they tend to hide it for prolong period and when they are compelled to seek medical care the condition is then at a late stage. The mycetoma patients have many financial constraints that hinder them from seeking medical and health care. In the remote mycetoma endemic areas, the health and medical facilities are meagre, and it is difficult for the patients to reach the regional health centres and thus the majority of patients present with late advanced disease. To overcome these treatment difficulties, the MRC had adopted this holistic management approach to decentralised the patient's care, improve the disease awareness and advocacy, provide free medical and surgical treatment locally at the village level, and to improve the affected villages environmental and hygienic conditions. In this communication, the MRC is reporting on this unique experience, discussing the advantages and difficulties faced it and suggesting recommendations to improve it to be adopted worldwide. Reviewing the medical literature revealed, no report on such management approached for mycetoma patients and thus it worth reporting it.

          Related collections

          Most cited references45

          • Record: found
          • Abstract: found
          • Article: found
          Is Open Access

          Global Burden of Human Mycetoma: A Systematic Review and Meta-analysis

          Introduction Mycetoma is a chronic infectious disease, characterized by the formation of tumor like-swellings and the formation of grains. This disease usually begins with a small trauma on the foot which introduces the causative agent into the subcutaneous tissue. Inside this tissue the causative agent will organize itself into small granules called grains. A small nodule will arise which gradually will grow into a large subcutaneous mass with sinuses which will secrete pus and grains. Eventually the bone will be invaded and a large mutilating lesion will be formed and the foot will be amputated [1]. Although mycetoma is usually found in the foot, other body sides can be affected as well [2]. Although, the first documented clinical cases of mycetoma were already described in 1842 by Gill, uncertainty remains about the total number of cases world-wide as already mentioned by Gokhale in 1981 [3]. A first attempt to map the number of mycetoma cases in a certain region was made by Abbott in the early 1950s [4]. Abbott, studied 1321 mycetoma cases in the Sudan in a 2.5 year period and published his findings in 1956 [4]. Many scientists were surprised by the amount of cases to be retrieved in such a small period, which could indicate that the burden of mycetoma was higher than previously thought. Therefore, others started to determine the burden of mycetoma in other countries known to be endemic for mycetoma, such as Congo [5], Somalia [6], [7], [8], [9], Argentina [10], [11] and Mexico [12], [13]. Although several studies have been performed to determine the prevalence of mycetoma in a certain region or country, no overall study has been performed to determine the prevalence of mycetoma world-wide. Furthermore mycetoma is not a reportable disease; therefore it is currently still not known what the global burden of mycetoma is. In the surveys performed in the past and based on case-studies it appeared many different species, both bacteria and fungi, are able to cause mycetoma. In the review written by Ahmed et al. 48 species were listed as causative agents [1]. Some of these agents were considered to be common causative agents of mycetoma while others were found only rarely. A definition on common or rare was not given. Recently, based on sequencing either the 16S region (for bacteria) or the ITS region (for fungi) more causative agents were added to this list [14], [15], [16]. Since molecular identification is not used in the endemic regions, the total number of species able to cause mycetoma is still not known. Furthermore, no clear definition is given which species are common causative agents of human mycetoma and which are only rarely implicated. The distribution of the mycetoma causative agents is not equal around the globe. In overall, actinomycetoma – mycetoma caused by bacteria – is more commonly found in Middle and South-America while eumycetoma – mycetoma caused by fungi – is more commonly found in Africa [4], [13]. But within a country, this could also differ per region [17], [18]. In order to estimate what the true burden of mycetoma is globally, a meta-analysis was performed in which all studies in which the epidemiology of the mycetoma causative agents was studied were reviewed. Studies with more than 10 cases were included. The burden of mycetoma was determined in terms of prevalence and the number of reported cases per year per country. Furthermore we determined which species were most commonly associated with mycetoma and prepared definitions based on the ∼8000 cases to determine which species were commonly, occasionally or rarely associated with mycetoma development. Methods Search strategy A systematic review of available literature on the epidemiology of mycetoma was searched using the electronic database PubMed with the use of the following search terms: Mycetoma AND epidemiology or Madura foot AND epidemiology. Studies published in languages other than English, French, Spanish, Portuguese, German or Dutch were excluded. The search was supplemented by reviewing the reference lists of all selected studies. Studies were excluded if the number of patients studied was 2000 cases while others reported only 11. To determine the global prevalence, the sum of the means for each country for a certain species was taken and then divided by the total of countries included. To determine which species were most prevalent the following definitions were used: common: >5% of the reported cases world-wide was caused by this species; occasional: 1–5% of the reported cases world-wide was caused by this species; rare: 5% of the studied cases. Nocardia otidiscaviarum was only found occasionally, and Actinomyces israeli rarely. 10.1371/journal.pntd.0002550.t001 Table 1 Number of species identified by selected papers. Species Colour of the grain* Number of isolates Percentage Prevalence** Actinomycetoma 4832 50.84 Actinomadura madurae W/Y/P 594 10.21 C Streptomyces somaliensis Y/Br 677 10.16 C Actinomadura pelletieri R 594 6.71 C Nocardia brasiliensis W 1946 5.78 C Nocardia asteroides W 108 5.58 C Nocardia otidiscaviarum (synonym: Nocardia caviae) W/Y 51 1.08 O Actinomyces israeli W/Y 1 0.07 R Nocardia spp W/Y 371 4.64 Unidentified actinomycetes 590 6.60 Eumycetoma 2704 41.72 Madurella mycetomatis B 2032 26.44 C Scedosporium boydii (synonym: Scedosporium apiospermum or Pseudallescheria boydii) W 83 3.52 O Falciformispora senegalensis (synonym: Leptosphaeria senegalensis) B 167 2.01 O Trematosphaeria grisea (synonym: Madurella grisea) B 116 1.62 O Acremonium falciforme (synonym: Cephalosporium falciforme) W 3 0.73 R Aspergillus fumigatus 2 0.40 R Exophiala jeanselmei B 9 0.37 R Geotrichum candidum 1 0.33 R Neotestudina rosatii W 4 0.33 R Medicopsis romeroi B 22 0.26 R Medicopsis romeroi or Biatriospora mackinnonii (synonym: Pyrenochaeta spp) B 7 0.21 R Aspergillus flavus G 2 0.07 R Microsporum audouini W 1 0.04 R Cochliobolus lunatus (synonym: Curvularia lunata) B 2 0.01 R Rhinocladiella atrovirens 2 0.01 R Aspergillus nidulans W 1 0.003 R Neoscytalidium dimidiatum 1 0.003 R Fusarium spp W 13 0.34 Cladosporium spp 1 0.14 Exophiala spp B 2 0.006 Unidentified fungi 220 4.72 Unknown etiology 217 7.49 TOTAL 7753 100 : colour of the grain: black (B), brown (Br), green (G), pink (P), red (R), white (W), yellow (Y). : prevalence: common (C): species isolated >5%; occasional (O): species isolated 1–5%; rare species isolated <1%. For the eumycetoma cases, 18 different fungal species were identified as causative agents. Furthermore, for some cases the fungus could not be identified to the species level, but only to the genus level. These belonged to the genera Fusarium, Cladosporium or Exophiala. For 219 fungi, the fungus was not even identified to the genus level. Only the fungus Madurella mycetomatis was considered to be a common causative agent. In fact it appeared the most common causative agent of all mycetoma cases since 24.3% of all studied cases were caused by this fungus. Scedosporium boydii, Falciformispora senegalensis and Trematosphaeria grisea were occasionally isolated from mycetoma cases, and Acremonium falciforme, Aspergillus fumigatus, Exophiala jeanselmei, Geotrichum candidum, Neotestudina rosatii, Medicopsis romeroi, Biatriospora mackinnonii, Aspergillus flavus, Microsporum audouini, Cochliobolus lunatus, Rhinocladiella atrovirens, Aspergillus nidulans and Neoscytalidium dimidiatum only rarely. The identified species were not evenly distributed throughout the world (Figure 5). M. mycetomatis, S. somaliensis and A. pelletieri were highly prevalent in Africa and Asia but hardly found in South-America. In contrast, the most prevalent species encountered in South America, N. brasiliensis, was hardly found in Africa, Europe and Asia. The only species which was found on all continents in equal amount was A. madurae. 10.1371/journal.pntd.0002550.g005 Figure 5 Distribution of the most common causative agents per country. The distribution of Madurella mycetomatis, Actinomadura madurae, Streptomyces somaliensis, Actinomadura pelletieril, Nocardia brasiliensis and Nocardia asteroids per country. For each country the number (N) of species identified is given. The percentage of Madurella mycetomatis, Actinomadura madurae, Streptomyces somaliensis, Actinomadura pelletieril, Nocardia brasiliensis and Nocardia asteroids were calculated from these data and displayed in the corresponding panels. India, as example Until now, we generalized all studies per country, but within a country there can be large differences. As an example India is taken, since from this country we had data from 11 different studies. These studies originated from different parts of the country, namely Punjab, Rajasthan, Madhya Pradesh, Adhra Pradesh, Tamil Nadu and West-Bengal. Most of these states have roughly the same population size at the time most studies were performed (∼50,000,000 inhabitants/state in 1981), only Punjab had a smaller population (16,788,915 inhabitants/state in 1981). As is seen in figure 6, in Rajasthan most cases were reported per year (33.3), followed by Tamil Nadu (16.8 reported cases/year) and West-Bengal (13.2 reported cases/year). The reported species per state also differed, in Rajasthan 62.5% of all mycetoma cases was caused by fungi, while in the other states most cases were caused by actinomycetoma's (54.3%–83.3% of all mycetoma cases). Not surprisingly, the species encountered also differed per state (figure 6). 10.1371/journal.pntd.0002550.g006 Figure 6 India. Average number of mycetoma cases reported per year in India per state and the causative agents per state. Discussion Since it is currently not known what the global burden of mycetoma is in terms of prevalence and incidence, we tried to make a rough estimation by performing a meta-analysis on the published literature from 1955 onwards. The number of papers published around the globe was relatively little. Only 50 papers could be used, which resulted in a total number of 8763 mycetoma cases documented since 1944. The globally reported number of cases is therefore 127 cases/year. The 8763 mycetoma cases were reported from 23 different countries. For some countries we only had data on 11 cases (e.g. Uganda), while for others we had data on 2607 cases (Mexico). The more cases reported per country the more reliable the data are. Since for most studies we knew in which years the cases were seen, a rough prevalence figure was calculated by dividing the number of cases seen in each year through the total population of that country in that year. This resulted in prevalence numbers ranging from <0.01 cases per 100,000 inhabitants (several countries) to 1.8 cases per 100,000 inhabitants (Sudan) and an average of cases reported per year ranging from 0.9 (Tunesia) to 106 (Sudan) (Figures 2A and 2B). These numbers are gross underestimations of the true prevalence, since only cases reported to literature could be used. Most of these cases were found by searching archives from a single hospital in a single city of that country. Only those studies which searched multiple centres throughout the country, such as the studies performed by Abbott in Sudan [4] and by Lopez Martinez in Mexico [13], more than 1000 patients were documented. Based on these short-comings we estimate that the total number of mycetoma cases will be much higher. Some evidence of a higher prevalence exists, although not reported to literature. For instance, in 1991 the Mycetoma Research Centre in Khartoum, Sudan was established. Since its founding, 6334 patients have been seen. In 2012 only, 5158 patients were seen of which 402 were new cases. This means that there were (5158 cases/year) seen in Sudan only, which were not reported to literature (prof A. Fahal, personal communication). Furthermore, the incidence calculated on the figures from the Mycetoma Research Centre are most probably also an underestimation, since a cohort study performed in the endemic village Abu Gumri in Sudan performed in 1960, indicated that there was a prevalence of 6.2 per 1000 inhabitants in that particular village [72]. Although the reported number of cases seen per year in this study is an underestimation, they are comparable with the number of cases reported for Buruli Ulcer and human African trypanosomiasis in many countries [73]. For instance, the number of reported Buruli Ulcer cases in 2009 were below 100 cases for Australia, Sudan, Gabon, Nigeria, and Guinea, while there were between 100 and 500 cases reported in Cameroon, Congo and the Democratic republic for the Congo in that year [73]. The number of reported Human African Trypanosomiasis (HAT) from surveillance studies in 2009 were below 100 reported cases for Kenya, Tanzania, Malawi, Zambia, Zimbabwe, Congo, Cameroon and Gabon [74]. The countries in which between 100 and 500 HAT cases were reported included Sudan, Angola and Uganda [74]. The data obtained for both Buruli Ulcer and HAT were from surveillance data, which makes these numbers more reliable than, the number of mycetoma cases/year reported here were derived from single center studies, and represent an underestimation. Therefore the prevalence of mycetoma is probably higher than that of either Buruli Ulcer or HAT. Still, Buruli Ulcer and HAT are reported on the list of neglected diseases while mycetoma is not. In this study it was shown that mycetoma could be caused by many different micro-organisms, both bacteria and fungi. Globally, most cases were caused by bacteria (50.8%) and a smaller percentage by fungi (41.7%) (Table 1), although this differed per country. In many African countries actually more eumycetoma cases were found as actinomycetoma cases. In table 1 it was also shown that there are many different bacteria and fungi able to cause mycetoma. There were 7 different bacterial species and 16 different fungal species reported. The total list of species able to cause mycetoma is actually longer. Since we only focused on studies reporting more than 10 cases per study, we missed the many species named in case reports. Other bacterial species implicated in mycetoma are Actinomadura latina, Gordonia terrae, Nocardia farcinica, Nocardia harenae, Nocardia mexicana, Nocardia transvalensis, Nocardia veterana, Nocardia yamanashiensis, Nocardiopsis dassonvillei and Streptomyces sudanensis [1], [14], [75], [76], [77], [78], [79], [80], [81], [82], [83]. Other fungal species implicated in mycetoma are Acremonium recifei, Cladophialophora bantiana, Corynespora cassiicola, Curvularia geniculata, Diaporthe phaseolorum, Fusarium oxysporum, Gibberella fujikuroi (synonym: Fusarium monoliforme), Haematonectria haematococca (synonym: Fusarium solani), Ilyonectria destructans (synonym: Cylindrocarpon destructans), Falciformispora tompkinsii (synonym: Leptosphaeria tompkinsii), Madurella fahalii, Madurella pseudomycetomatis, Madurella tropicana, Microsporum canis, Phaeoacremonium parasiticum, Phialophora cyanescens (synonym: Cylindrocarpon cyanescens), Phialophora verrucosa, Pleurostomophora ochracea, Pseudochaetosphaeronema larense, Rhinocladiella atrovirens, Sarocladium kiliense (synonym: Acremonium kiliense), Setosphaeria rostrata (synonym: Exserohilum rostrata) [1], [15], [16], [84], [85], [86], [87], [88], [89], [90], [91], [92], [93], [94], [95], [96], [97], [98]. Since most of these species are only found in case studies, these are probably only rarely associated with mycetoma, if associated at all. Although most species represented in Table 1 were isolated from multiple cases, some species were only isolated from 1–5 cases, which makes one wonder if this was the true causative agent. Only for Nocardia asteroides [99], Nocardia brasiliensis [99], [100], [101], [102], Nocardia caviae [99], [100], Nocardia transvalensis [103], Madurella mycetomatis [104], [105] the pathogenicity in animal models has been demonstrated. In all these animal models pathology resembling mycetoma and the formation of grains was demonstrated. The only attempt ever recorded for Actinomadura madurae, Actinomadura pelletieri and Streptomyces somalienis failed [104]. So, one could wonder if all species listed in Table 1 and in the discussion are true causative agents for mycetoma. The causative agents presented in Table 1 were identified based on histology only or on histology combined with culture. Therefore, the possibility arises that some of the causative agents were misidentified. Although widely used, the limitations of histological diagnosis have been known since the early 1960s. It is impossible to differentiate Nocardia spp. to the species level based on histology only, all species form white to yellow, small spherical grains [106], [107]. Also S. boydii, Acremonium spp and Fusarium spp are difficult to differentiate [106], [107]. These species produce white to yellow grains with a dense mass of slender, septate, hyaline hyphae with occasional vesicles or swollen hyphae [107]. The black-grain causative agents F. senegalensis, F. tompkinsii, M. romeroi, Exophiala jeanselmei and T. grisea also produce similar type of grains [107]. These species produce black grains, which can be tubular or hollow with a darker periphery [107]. The Falciformispora grains usually contain larger vesicles than the other species [107]. Some causative agents can cause multiple grain types in histological slides. Madurella mycetomatis is known to produce three structural forms of the fungal grain: the filamentous type, the vesicular type and a mixture of both [2]. In the vesicular type of grain the center is light colored and the hyphae in the periphery are brown, just as the ones described above for F. senegalensis, F. tompkinsii, M. romeroi, Exophiala jeanselmei and T. grisea [2]. For some of the studies culturing of the causative agents was also included. But identification of species based on culturing only, has known to be troublesome too, especially for the fungi. Identification of the fungi is usually achieved by observation of the growth rate, colony morphology, production of conidia and assimilation patterns. Most of the black-grain eumycetoma causative agents only rarely produce conidia and therefore misidentifications are known to occur frequently [108]. A well-known example is T. grisea, previously known as Madurella grisea. Due to the numerous misidentifications McGinnis suggested in 1996 that this species should be considered a complex of different fungi, classified together because of their sclerotial color and architecture and colony characteristics [109]. Some isolates of B. mackinnonii are known to be misidentified as T. grisea, since some of these isolates did not form pycnidia at standard media, but only after stimulation [109]. Furthermore, with classical culture methods, not all species can be differentiated. An example is Streptomyces sudanensis, which morphologically is equal to Streptomyces somaliensis. Only by sequencing the 16S gene of these species, it appeared that out of 9 previously identified S. somaliensis strains, 5 were actually misidentified and were renamed S. sudanensis [14]. The same was true for M. mycetomatis, in 2012 it appeared that M. mycetomatis had some close relatives which could only be identified by ITS sequencing, not on morphology [15]. Even when the species was already known, misidentifications have occurred in the past. N. brasiliensis has always been considered the most common causative agent of actinomycetoma in Mexico. Sánchez-Herrara demonstrated in 2012, that from the 18 previously identified N. brasiliensis isolates obtained from mycetoma patients in Mexico City between 1947 and 1959, only 7 were N. brasiliensis, the other 11 were proven to be N. farcinica based on sequencing and phenotypic profiles [110]. Therefore it remains doubtful that the data derived from the studies used for this meta-analysis were based on correctly identified species. Even with all these short-comings listed of this meta-analysis, it still gives a good overview of our current knowledge on the burden of mycetoma world-wide. In order to better estimate the burden, global surveillance programs should be erected, like for instance the surveillance program for Buruli Ulcer. This program is the result of the Global Buruli Ulcer initiative established in 1998 by the WHO and recognized by the 57th World Health Assembly in 2004 [111]. For this surveillance program, standardized forms (BU02) were generated which are now used in the endemic countries. If such a system was developed for mycetoma, better understanding on the global burden, and the epidemiology of this disease will be gained. Supporting Information Checklist S1 PRISMA checklist. (DOC) Click here for additional data file. Diagram S2 PRISMA flow chart. (DOC) Click here for additional data file.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Mycetoma caused by Madurella mycetomatis: a neglected infectious burden.

            Tropical eumycetoma is frequently caused by the fungus Madurella mycetomatis. The disease is characterised by extensive subcutaneous masses, usually with sinuses draining pus, blood, and fungal grains. The disease affects individuals of all ages, although disability is most severe in adults who work outdoors. Compared with major diseases such as tuberculosis, malaria, and HIV, disease from M mycetomatis is underestimated but socioeconomically important. Many scientific case reports on mycetoma exist, but fundamental research was lacking until recently. We present a review on developments in the clinical, epidemiological, and diagnostic management of M mycetomatis eumycetoma. We describe newly developed molecular diagnostic and gene typing procedures, and their application for management of patients and environmental research. Fungal susceptibility tests have been developed as well as a mouse model of infection. These advances should greatly further our understanding of the molecular basis of eumycetoma.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: found
              Is Open Access

              Mycetoma in the Sudan: An Update from the Mycetoma Research Centre, University of Khartoum, Sudan

              This communication reports on the Mycetoma Research Centre of the University of Khartoum, Sudan experience on 6,792 patients seen during the period 1991–2014.The patients were predominately young (64% under 30 years old) males (76%). The majority (68%) were from the Sudan mycetoma belt and 28% were students. Madurella mycetomatis eumycetoma was the most common type (70%). In 66% of the patients the duration of the disease was less than five years, and 81% gave a history of sinuses discharging mostly black grains (78%). History of trauma at the mycetoma site was reported in 20%. Local pain was reported in 27% of the patients, and only 12% had a family history of mycetoma. The study showed that 57% of the patients had previous surgical excisions and recurrence, and only 4% received previous medical treatment for mycetoma. Other concomitant medical diseases were reported in 4% of the patients. The foot (76%) and hand (8%) were the most commonly affected sites. Less frequently affected sites were the leg and knee (7%), thigh (2%), buttock (2%) and arm and forearm (1%). Rare sites included the chest wall, head and neck, back, abdominal wall, perineum, oral cavity, tongue and eye. Multiple sites mycetoma was recorded in 135 (2%) of cases. At presentation, 37% of patients had massive lesions, 79% had sinuses, 8% had local hyper-hydrosis at the mycetoma lesion, 11% had regional lymphadenopathy, while 6% had dilated tortuous veins proximal to the mycetoma lesions. The diagnosis of mycetoma was established by combined imaging techniques and cytological, histopathological, serological tests and grain culture. Patients with actinomycetoma received a combination of antimicrobial agents, while eumycetoma patients received antifungal agents combined with various surgical excisions. Surgical excisions in the form of wide local excision, debridement or amputation were done in 807 patients, and of them 248 patients (30.7%) had postoperative recurrence. Different types of amputations were done in 120 patients (1.7%).
                Bookmark

                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Project administration
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: Methodology
                Role: Data curationRole: Funding acquisitionRole: Project administrationRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                10 May 2018
                May 2018
                : 12
                : 5
                : e0006391
                Affiliations
                [1 ] The Mycetoma Research Centre, University of Khartoum, Khartoum, Sudan
                [2 ] Department of Molecular Biology, Institute of Endemic Diseases, University of Khartoum, Khartoum, Sudan
                [3 ] Department of Medical Imaging, Soba University Hospital, University of Khartoum, Khartoum, Sudan
                [4 ] Department of Biostatistics, Faculty of Mathematical Sciences, University of Khartoum, Khartoum, Sudan
                [5 ] Department of Surgery, Faculty of Medicine, University of Khartoum, Khartoum, Sudan
                [6 ] The Minister of Health, Ministry of Health, Sennar State, Sennar, Sudan
                [7 ] Department of Surgery, Faculty of Medicine, Sennar University, Sennar, Sudan
                Hospital Infantil de Mexico Federico Gomez, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-4922-7321
                http://orcid.org/0000-0001-9968-9853
                Article
                PNTD-D-17-01857
                10.1371/journal.pntd.0006391
                5944909
                29746460
                4ced1438-1411-4c97-be41-e594f628fb0a
                © 2018 Bakhiet et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 December 2017
                : 18 March 2018
                Page count
                Figures: 7, Tables: 4, Pages: 20
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Fungal Diseases
                Mycetoma
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Mycetoma
                Medicine and Health Sciences
                Health Care
                Health Education and Awareness
                Medicine and Health Sciences
                Health Care
                Patient Advocacy
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Lesions
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Lesions
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                People and Places
                Geographical Locations
                Africa
                Sudan
                Medicine and Health Sciences
                Public and Occupational Health
                Hygiene
                Medicine and Health Sciences
                Health Care
                Socioeconomic Aspects of Health
                Medicine and Health Sciences
                Public and Occupational Health
                Socioeconomic Aspects of Health
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

                Comments

                Comment on this article