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Transactions of the Royal Society of Tropical Medicine and Hygiene 106 (2012) 738–742

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Transactions of the Royal Society of


Tropical Medicine and Hygiene
journal homepage: http://www.elsevier.com/locate/trstmh

New MRI grading system for the diagnosis and management of


mycetoma
M.E. EL Shamy a , A.H. Fahal b,∗ , M.Y. Shakir b , M.M.A. Homeida a
a
Radiology Department, Alzaytouna Specialist Hospital, Khartoum, Sudan
b
The Mycetoma Research Centre, University of Khartoum, Khartoum, Sudan

a r t i c l e i n f o a b s t r a c t

Article history: The management of patients with mycetoma depends on accurate identification of the
Received 1 April 2012 causative organisms and of the extent of disease involvement along the different tissue
Received in revised form 15 August 2012
planes. Disease involvement cannot accurately be assessed with the available diagnostic
Accepted 15 August 2012
tools, so in this study we set out to evaluate the effectiveness of MRI in the diagnosis
Available online 14 September 2012
and management of mycetoma. Forty-two patients with confirmed mycetoma had MRI
examination of the affected parts. A grading system, The Mycetoma Skin, Muscle, Bone
Keywords:
Mycetoma Grading System (MSMBS), was used to describe and grade disease severity on the basis of
MRI MRI findings. The logistic regression test was used to correlate the clinical and MRI find-
Grading system ings. The study showed that MRI can help in the diagnosis and management of mycetoma
Diagnosis patients. The dot-in-circle sign, conglomerated foci with low signal intensity and macro-
Management and micro-abscesses on a background of a hypointense matrix are all diagnostic of myce-
toma. In patients with mycetoma, the MSMBS can grade disease severity, compare patients
and help to manage them. Further studies are needed to determine to what extent the
grading system can be used to determine a patient’s prognosis.
© 2012 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd.
All rights reserved.

1. Introduction in destruction, deformity and loss of function (Figure 1A);


occasionally it is fatal.5 Mycetoma has many medical and
Mycetoma is a chronic, granulomatous, progressive and socioeconomic impacts on patients, their families and the
destructive inflammatory disease.1,2 It usually involves community.6
the subcutaneous tissue and most probably develops The management of patients with mycetoma depends
after a traumatic inoculation of the causative organ- on accurate identification of the causative organisms and
ism. Mycetoma may be caused by true fungi or higher the site and extent of the disease.2 The available diagnos-
bacteria and hence is usually classified into eumycetoma tic tools for mycetoma are numerous but invasive, and
and actinomycetoma, respectively.3 The triad of painless they cannot accurately assess disease spread and tissue
subcutaneous mass, sinus formation and purulent and involvement.3 Hence this study set out to describe the MRI
sero-purulent discharge that contains grains is pathog- appearance of mycetoma and determine its value as a non-
nomonic of mycetoma.4 The disease commonly spreads invasive technique for identification of the type and extent
to involve the skin, deep structures and bone, resulting of a patient’s mycetoma.

2. Patients and methods


∗ Corresponding author. Tel.: +249 912 346702; fax: +249 183 771211.
E-mail addresses: ahfahal@hotmail.com, ahfahal@uofk.edu This prospective study was conducted at the Mycetoma
(A.H. Fahal). Research Centre, Soba University Hospital, University of

0035-9203/$ – see front matter © 2012 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.trstmh.2012.08.009
M.E. EL Shamy et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 106 (2012) 738–742 739

Table 1
Distribution of MRI findings among the study population of 42 patients
with mycetoma seen at the Mycetoma Research Centre, Khartoum, Sudan,
according to the Mycetoma Skin, Muscle, Bone Grading (MSMB) System

Score MRI finding No. (%)

Skin and subcutaneous tissue


0 No skin or subcutaneous involvement 0 (0)
1 Obliteration of skin and fascial planes 2 (4.8)
2 Abscess formation 1 (2.4)
3 Formation of sinus tract without grains 6 (14.3)
4 Formation of sinus tract with grains 33 (78.6)
Total 42 (100)
Muscle
0 No muscle involvement 5 (11.9)
1 Muscle oedema 2 (4.8)
2 Formation of micro-abscess 25 (59.5)
3 Formation of macro-abscess 10 (23.8)
Total 42 (100)
Bone
0 No bone involvement 9 (21.4)
1 Bone oedema 14 (33.3)
2 Bone cavitation 11 (26.2)
3 Bone destruction 8 (19.1)
Total 42 (100)

Khartoum, in the period between April 2010 and December


2011. The study included 42 patients with confirmed
mycetoma. The diagnosis of mycetoma was established
by careful clinical interview and thorough general and
local clinical examinations. All patients had x-ray exami-
nation of the affected part in anteroposterior and lateral
views, ultrasonic examination of their lesions and fine-
needle aspiration (FNA) for cytology. Surgical biopsy was
performed to collect grains for culture identification and
for histopathological examination in most of the patients.
After informed consent all patients had MRI examina-
tion of the affected part. MRI examination was performed
using a 1.5T MRI scanner (Toshiba Medical Systems,
Tochigi, Japan). The sequences were obtained using a
phased-array surface coil and included fat-suppressed
T2-weighted and T1- and T2-weighted images. Intravenous
gadolinium contrast was administered.
A grading system, the Mycetoma Skin, Muscle, Bone
grading system (MSMBS), was used to describe and grade
the mycetoma severity on the basis of MRI findings
(Table 1).
The logistic regression test was applied to correlate the
clinical and MRI findings, using the statistical software
package SPSS V.18.

3. Results

The study included 32 males (76%) and 10 females (24%).


Their ages ranged between 16 and 70 years, with a mean
of 33.7±17.5 years. Disease duration was 1–40 years, mean

extension displacing the urinary bladder (short arrow) to the left, and
the small, spherical hyperintense lesions separated by tissue of low sig-
Figure 1. (A) Extensive actinomycetoma involving the anterior abdom- nal intensity. Some of these lesions show central tiny hypointense foci,
inal wall and thigh, with intra-abdominal extension. (B) Coronal resulting in the dot-in-circle sign (curved arrow). (C) Axial T2-weighted
T2-weighted MR image of the same patient’s right upper thigh and MR image of the same patient’s upper thigh, showing multiple spheri-
pelvis, showing extensive inflammatory mass with predominant bright cal hyperintense lesions infiltrating the muscles (short arrows). Multiple
signal intensity granulomatous tissue (long arrow). Note the intra-pelvic central tiny hypointense foci are noted (curved arrow).
740 M.E. EL Shamy et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 106 (2012) 738–742

Figure 2. Sagittal T2 MR image with fat saturation of a patient’s foot, Figure 3. Coronal T2-weighted fat saturation image of eumycetoma in the
showing an extensive eumycetoma lesion infiltrating and obliterating the foot; a spherical hyperintense lesion is surrounded has a low-signal sur-
subcutaneous tissue plane. A skin sinus (long arrow) contains low-signal rounding rim and a central hypointense focus (dot-in-circle sign) (arrow).
fungal grains. Note also multiple low signal intensity fungal grains (short
arrow), bone marrow oedema (curved arrow) and a dot-in-circle sign
(arrow head). most patients, with or without low-signal mycetoma grains
(Figure 2).
8.8±8.1 years. The foot was affected in 25 patients (60%); Muscle infiltration was seen as muscle oedema on fat-
this was the most commonly affected part, followed by the suppressed images or muscle infiltration with soft tissue
leg and knee (six patients; 14%), hand and gluteal region abscesses. Two types of abscess were seen: microabscesses
(for each, three patients affected [7%]), anterior abdominal of <1 cm diameter and macroabscesses of >1 cm in diameter
wall (two patients; 5%) and the thigh, forearm, head and (Figures 1C, 4). Signs of bone infiltration included extensive
neck (each affected in one patient; 2%). Most of the patients bone cavities containing low-signal mycetoma grains or
(69%) had massive lesions more than 10 cm in diameter. just early bone marrow oedema on fat-suppressed images
The majority of patients (89%) had active or healed sinuses. (Figure 2).
In 74% of them, the lesions were painless and 66% of them In most of the actinomycetoma patients, MRI showed
had recurrent disease. soft tissue microabscesses, bony periosteal reaction and
All patients had x-ray examination of the affected parts reactive sclerosis, whereas soft tissue macroabscesses,
and the findings were as follows: soft tissue swellings
(6/42, 14%), periosteal reaction (1/42, 2%), bone destruc-
tion (2/42, 5%) and combined findings (15/42, 36%); the
remaining patients (18/42, 43%) had no abnormal findings
on x-ray. The diagnosis was confirmed by histopatholog-
ical examination of the surgical biopsies or lesion FNA
and the cell-block technique, or both. The diagnosis of
eumycetoma caused by Madurella mycetomatis was con-
firmed in 24 patients (57%) and actinomycetoma caused by
Streptomyces somaliensis in 18 patients (43%).
In most patients, MRI examination revealed an ill-
defined lesion of abnormal signal intensity extending
from the subcutaneous tissue plane and infiltrating the
underlying muscle and bone planes. The lesions showed
predominant bright signal intensity on fat-suppressed
T2-weighted images of granulomatous tissue and iso-
intense signal on T1-weighted images. In addition, multiple
discrete, spherical hyper-intense lesions, separated by a
low signal intensity fibrous network, were noted on T2-
weighted images. Some of these lesions showed central foci
of low signal intensity, forming the dot-in-circle sign (tar-
get sign) that indicates mycetoma grains (Figures 1B, 2, 3). Figure 4. Sagittal T1-weighted post-contrast image of eumycetoma in the
hand, showing an extensive lesion infiltrating the subcutaneous, muscle
The mycetoma grains appeared as a low-intensity signal at
and carpal bone planes; note enhanced granulomatous tissue (long arrow)
all pulse sequences and did not enhance on post-contrast with non-enhanced low-signal foci (fungal grains) and microabscesses
study (Figure 4). Skin sinuses and sinus tracts were seen in (arrow heads).
M.E. EL Shamy et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 106 (2012) 738–742 741

with bone cavitation or destruction or both, were com- the extent of tissue involvement. Furthermore, the radio-
monly seen in patients with eumycetoma. Thus MRI allows logical differential diagnosis of mycetoma includes many
a degree of differentiation between eumycetoma and conditions such as osteogenic sarcoma, bone cysts and
actinomycetoma, but cannot be used to make an accurate osteomyelitis.4,10,12
distinction between the two conditions. A literature review revealed a few case reports that
The MRI findings were grouped into three sets accord- had described MRI findings in mycetoma.13–15 However,
ing to the Mycetoma Skin, Muscle, Bone Grading System the present study is the first prospective study to describe
(MSMBS): and grade mycetoma severity on the basis of MRI findings.
The findings described in this study are characteristic of
• skin and subcutaneous plane findings, including fascial mycetoma. The dot-in-circle sign, described by Sarris and
plane obliteration, abscess formation, and sinus tract for- colleagues, is a unique MRI sign for mycetoma.14 It is seen
mation with or without the presence of grains. as a tiny, hypointense focus within high-intensity spherical
• muscle plane findings, namely muscle oedema, and for- lesions on T2-weighted, STIR (short T1 inversion recov-
mation of microabscesses or macroabscesses or both. ery), and T1-weighted fat-saturated gadolinium-enhanced
• bone plane findings, including bone marrow oedema, images. The sign represents mycetoma grains surrounded
bone cavitation and bone destruction. by inflammatory granulomata. Czechowski and associates
have suggested that the dot-in-circle sign is attributable to
The incidences of these findings are shown in Table 1. metabolic products within the grains,16 but further studies
The MSMBS allows a patient’s mycetoma lesion to be clas- are needed to confirm this.
sified as mild (1–3), moderate (4–7) or severe (8–10). It is not uncommon for histopathological sections taken
Of the patients in our study, four (9.5%) had mild disease, from mycetoma biopsies to reveal features of a chronic,
20 (47.6%) had moderate disease and 18 patients (42.9%) non-specific granulomatous inflammatory reaction, with
had severe disease. There was no statistically significant no grains; in these situations it is difficult to substanti-
correlation between the MRI findings and disease duration ate the diagnosis of mycetoma. Grains may be few, and
(p=0.234) or mycetoma type (p=0.712). There was a sta- scattered in small areas of the extensive tissue involved,
tistically significant correlation between MRI findings and and therefore missing in many histopathological sections.
lesion size (p<0.0). However, MRI can show the grains as conglomerated
hypointense foci scattered in the lesion, and that is diag-
4. Discussion nostic.
The study showed that non-invasive MRI imaging can
Although mycetoma is a chronic granulomatous disease help in the early diagnosis of mycetoma, even in the
it has many features of a malignant neoplasm, includ- absence of sinuses and discharge. The dot-in-circle sign,
ing massive local destruction, spread along fascial planes conglomerated foci of low signal intensity, or macro-
and via lymphatic and blood vessels, and recurrence after and microabscesses on a background of a hypointense
adequate treatment; hence a severity grading system is matrix are all diagnostic of mycetoma. MRI can differen-
essential for disease assessment.2,7 It also worth noting that tiate between eumycetoma and actinomycetoma, but the
the apparent clinical features of mycetoma are not always distinction is not clear cut and this aspect needs further
a reliable indicator of the extent and spread of the dis- refinement.
ease; some small lesions with few sinuses may have a deep We found no correlation between MRI findings and dis-
network of connecting tracts, through which the disease ease duration, which can be explained by the nature of the
has spread quite extensively.3,8,9 The proper management disease. Actinomycetoma usually spreads and affects vari-
of patients with mycetoma requires both identification of ous tissues fairly quickly, as it is more inflammatory than
the causative organism and determination of the extent eumycetoma and has no surrounding capsule, whereas
to which the disease has spread along the different tissue eumycetoma is a more localised disease and commonly
planes. well encapsulated.
In mycetoma, many imaging and diagnostic tools are CT scanning is used for the diagnosis of mycetoma,
available; however, many of them are invasive and cannot but the technique is not specific and the differential diag-
accurately determine how far the mycetoma has spread or nosis includes many other conditions; however, bone
the extent of tissue involvement.10,11 A mycetoma lesion involvement can be determined more accurately with
has a characteristic appearance on ultrasound, which is this modality. Bonifaz and colleagues showed that heli-
able to differentiate between eumycetoma and actino- cal computed tomography, with its three-dimensional
mycetoma, and between mycetoma and other conditions. reconstruction, can provide precise information on actino-
However, the size of lesions and the extent of spread along mycetoma invasion at the different tissue planes.17
different tissue planes, knowledge of which is important
in planning surgical incisions, cannot be accurately deter- 5. Conclusion
mined ultrasonically.11
X-ray examination is not very helpful in the manage- MRI is recommended for the diagnosis of mycetoma
ment of mycetoma patients. In the early stages of the and to determine its severity and the extent of tissue
disease x-ray appearances are essentially normal, radiolog- invasion. MRI is also helpful in planning the different
ical findings being evident only in advanced disease, so it treatment modalities for mycetoma. The MSMB grading
is not possible by this technique to determine accurately system allows disease in different patients to be classified
742 M.E. EL Shamy et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 106 (2012) 738–742

and compared. Further studies are needed to determine to 5. Ahmed AA, van de Sande WW, Fahal AH, et al. Management of myce-
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Ethical approval: The study was approved by the Ethical 2003;27:233–5.
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rative study group. MRI of mycetoma of the foot: two cases
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