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Articles

Mycetoma In Asia: Still Veiled In Mystery

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Harsimran Kaur and Arunaloke Chakrabarti
Postgraduate Institute of Medical Education and Research
Chandigarh, India

Epidemiology

Mycetoma is a chronic granulomatous subcutaneous disease caused by bacteria (actinomycetoma) or fungi (eumycetoma). The disease progresses over months to years from a localized painless swelling to plaques, nodules and multiple discharging sinuses extruding grains (Figure), subsequently spreading to underlying muscle, tendons and bone, causing permanent deformities. Because of its typical tropical and subtropical distribution extending between 15º south and 30º north latitude (a zone called the ‘mycetoma belt’), comprising developing countries mainly, and its neglected status, the World Health Organization (WHO) declared mycetoma as a neglected tropical disease.1-3 However, its true distribution extends beyond this belt.

A rough estimate of mycetoma epidemiology by van de Sande indicated the most cases in Mexico, Sudan, Senegal and India, with few reports from Uganda, Romania, Nigeria, Bulgaria and Thailand.3 The frequency varies with different geographic locations.3-15 Actinomycetomas are predominant in dry areas, especially in North Africa, Central and South America and a few Asian countries, while eumycetoma prevails in tropical and subtropical regions of Asia (Mid-East, India) and Africa (Sub-Saharan Africa), where rainfall is abundant.16 This is in contrast to the distribution in India, where eumycetoma is common in the dry western regions of Rajasthan, while eastern Rajasthan and southern India report a high rate of actinomycetomas despite sufficient rainfall in these regions.3,17 Although the meta-analysis by van de Sande gave an overview of epidemiology, the true magnitude of the disease is still ambiguous, as majority of the cases from the endemic regions are not reported in literature.

Figure. Mycetoma of foot with multiple discharging sinuses
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Photo courtesy of Professor BM Hemashettar, India

Regional data

The data on mycetoma in Asia are scarce and mostly based on case reports from single centers. The heaviest burden of the disease is limited to Southeast Asia, the Middle East and, less commonly, in the Far East.2 It was in Madurai (formerly Madura), India, where Gill, Colebrook and Godfrey first described this disease as ‘Madura foot’, which was later renamed ‘mycetoma’ by Carter.2 Current available data show pockets of distribution of mycetoma in Rajasthan, Tamil Nadu and West Bengal provinces in India, with few scattered case reports from Punjab, Madhya Pradesh and Andhra Pradesh.3 Overall, eumycetoma is more common in Rajasthan (62.5%), while actinomycetoma is more prevalent (54.3%-83.3%) in the rest of the country.3 Causative agents also vary within India. Madurella mycetomatis is the most common agent, followed by M. grisea and Aspergillus nidulans in North West India, while species causing eumycetoma in South India include M. mycetomatis, Neoscytalidium dimidiatum and A. flavus.17 The red grain mycetoma, Actinomadura pelletieri, is rare in India.17

Studies from Iran and Thailand have shown predominance of actinomycetoma (84.5% and 64.7%, respectively), while studies from Yemen demonstrate high prevalence of eumycetoma (71%).15,18-21 The most common agents of actinomycetoma in Iran are Actinomadura madurae (23.5%), Nocardia asteroides (20.6%), Nocardia caviae (13.2%); Pseudoallescheria boydii (10.3%) is the common cause of eumycetoma.18,19,22 The prevalence of mycetoma in China is quite low, with around 19 cases reported between 1960 and 2010 (10 eumycetoma; 9 actinomycetoma). The etiologic agents reported from Chinese population include Nocardia brasiliensis, Nocardia asteroides, Nocardia otitidiscaviarum, Actinomadura madurae, Acremonium falciforme, Scopulariopsis maduromycosis, Pseudallescheria boydii, Madurella mycetomatis, Madurella pseudomycetomatis, Trichophyton verrucosum and Aspergillus spp.23 Sporadic cases of mycetoma are reported from Singapore (Monosporium apiospermum), Malaysia (Phialophora jeanselmei, Madurella mycetomi, Streptomyces somaliensis), Philippines (Madurella grisea), Indonesia (Madurella tropicana), Laos (Actinomadura madurae), Cambodia (Pyrenochaeta romeroi, Madura mycetes), Thailand (Nocardia asteroids, N. caviae, N. brasiliensis, N. rosatii, Madurella mycetomii, Pseudallescheria boydii, Exophiala jeanselmei, Actinomadura madurae, Cladosporium carrionii), and Vietnam (Nocardia otitidiscaviarum).24

Presentation and diagnosis

The disease generally affects young men from rural areas working barefoot outdoors (for activities such as farming, for instance). However, in Thailand, there is an equal prevalence of mycetoma in men and women.3 The disease usually occurs by inoculation of the etiologic agent at the body site, most commonly foot (80%), followed by leg, trunk (less common in Asia) and arm.3

An early diagnosis of the disease is necessary to prevent disfigurement, and identification of the etiologic agent is required for guiding management. The diagnosis is quite challenging in developing countries, where there is a lack of facilities, forcing the clinicians to assess the disease clinically and manage the patient without accurate identification of the pathogen or determining the extent of disease by imaging. Ultrasound and fine needle aspiration are the minimum requirements to accurately diagnose the disease. Other imaging modalities include X-ray, computed tomography (CT) and magnetic resonance imaging (MRI), which are lacking in peripheral and remote areas of developing nations. Culture methods, the gold standard for identification, have limitations of long turnaround time, difficulty isolating the true causative agent from contaminating bacteria and saprophytic fungi, and the need for experienced personnel. Matrix assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) is a rapid technique of identification but is available only in a few reference centers. Other modalities like histology, cytology, skin test and serology lack specificity for identification. Molecular methods may improve diagnostic capabilities, but are too expensive to be available at all centers in developing countries.

Treatment and prognosis

The treatment is chosen only after distinguishing if the disease is an actinomycetoma or a eumycetoma. Surgical debridement and medical management by antibiotics or antifungal agents are the cornerstones of mycetoma treatment.2 However, the rate of recurrence is quite high, probably due to poor compliance or poor response to the drugs. The prognosis of actinomycetoma is better than eumycetoma.

Conclusion

There are many gaps in knowledge regarding the epidemiology and management of mycetoma. The exact magnitude of disease burden in Asia is still a mystery that needs to be solved to fill in these gaps. Clearly, awareness must be raised among health professionals for early diagnosis and treatment of mycetoma.

References:

  1. World Heath Organization. Neglected tropical diseases. Available at: www.who.int/neglected_diseases/diseases/en/. Accessed May 2017.
  2. Nenoff P, van de Sande WW, Fahal AH, Reinel D, Schöfer H. Eumycetoma and actinomycetoma–an update on causative agents, epidemiology, pathogenesis, diagnostics and therapy. J Eur Acad Dermatol Venereol 2015;29:1873-1883.
  3. van de Sande WW. Global burden of human mycetoma: a systematic review and meta-analysis. PLoS Negl Trop Dis 2013;7:e2550.
  4. Fahal A, Mahgoub el S, El Hassan AM, Abdel-Rahman ME. Mycetoma in the Sudan: an update from the Mycetoma Research Centre, University of Khartoum, Sudan. PLoS Negl Trop Dis 2015;9:e0003679.
  5. Maiti PK, Ray A, Bandyopadhyay S. Epidemiological aspects of mycetoma from a retrospective study of 264 cases in West Bengal. Trop Med Int Health 2002;7:788-792.
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  7. Padhi S, Uppin SG, Uppin MS, et al. Mycetoma in South India: retrospective analysis of 13 cases and description of two cases caused by unusual pathogens: Neoscytalidium dimidiatum and Aspergillus flavus. Int J Dermatol 2010;49:1289-1296.
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  14. Balabanoff VA. Mycetomas originated from South-East Bulgaria (author’s transl) [Article in French]. Ann Parasitol Hum Comp 1980;55:605-613.
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  16. Zijlstra EE, van de Sande WW, Fahal AH. Mycetoma: A Long Journey from Neglect. PLoS Negl Trop Dis 2016;10:e0004244.
  17. Venkatswami S, Sankarasubramanian A, Subramanyam S. The madura foot: looking deep. Int J Low Extrem Wounds 2012;11:31-42.
  18. Bassiri-Jahromi S. Mycetoma in Iran: causative agents and geographic distribution. Indian J Dermatol 2014;59:529.
  19. Zarei Mahmoudabadi A, Zarrin M. Mycetomas in Iran: a review article. Mycopathologia 2008;165:135-141.
  20. Yu AM, Zhao S, Nie LY. Mycetomas in northern Yemen: identification of causative organisms and epidemiologic considerations. Am J Trop Med Hyg 1993;48:812-817.
  21. Khatri ML, Al-Halali HM, Fouad Khalid M, Saif SA, Vyas MC. Mycetoma in Yemen: clinicoepidemiologic and histopathologic study. Int J Dermatol 2002;41:586-593.
  22. Khodavaisy S, Shokohi T, Zarei Mahmoudabadi A. Mycetoma in Iran with emphasis on north of Iran a review of the literatures. J Mazandaran Univ Med Sci 2010;20:96-107
  23. Yan J, Deng J, Zhou CJ, Zhong BY, Hao F. Phenotypic and molecular characterization of Madurella pseudomycetomatis sp. nov., a novel opportunistic fungus possibly causing black-grain mycetoma. J Clin Microbiol 2010;48:251-7.
  24. Rattanavong S, Vongthongchit S, Bounphamala K, et al. Actinomycetoma in SE Asia: the first case from Laos and a review of the literature. BMC Infect Dis 2012;12:349.
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