Evaluation of acquired cholesteatoma with PROPELLER diffusion imaging

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1 The Egyptian Journal of Radiology and Nuclear Medicine (2011) 42, 9 17 Egyptian Society of Radiology and Nuclear Medicine The Egyptian Journal of Radiology and Nuclear Medicine Evaluation of acquired cholesteatoma with PROPELLER diffusion imaging Sabry A. El Mogy a, *, Jehan A. Mazroa a,1, Mahmoud Abd El Ghaffar b,2, Mohamed S. El Mogy c,3, Ibraheem S. El Mogy c,4 a Faculty of Medicine, Mansoura University, Egypt b Faculty of Medicine, Banha University, Egypt c Fellowship Ministry of Health, Mansura, Egypt Received 25 October 2010; accepted 30 December 2010 Available online 4 March 2011 KEYWORDS PROPELLER diffusion; Acquired cholesteatoma; Imaging of middle ear lesions Abstract Purpose: Was to evaluate the role of periodically rotated overlapping parallel lines with enhanced reconstruction (PROPELLER) diffusion imaging in evaluation of middle ear acquired cholesteatomas (primary and recurrent) and differentiating them from middle ear granulation tissue. Patients and methods: Forty two patients with suggested acquired cholesteatomas were included in this prospective study, they underwent spiral CT and MRI (PROPELLER diffusion) for all. The Abbreviations: PROPELLER, periodically rotated overlapping parallel lines with enhanced reconstruction; SE, spin echo; DWI, diffusion weighted imaging; NPV, negative predictive value; PPV, positive predictive value; EPI, echo-planar imaging * Corresponding author. Mobile: addresses: drsabryelmogy@yahoo.com (S.A. El Mogy), jehanras@hotmail.com (J.A. Mazroa), mhgh55@yahoo.co.uk (M.A.E. Ghaffar), dr_m_sabry@yahoo.com (M.S.ELS. El Mogy), imogy@hotmail.com (I.S.ElS. El Mogy). 1 Mobile: Mobile: Mobile: Mobile: X Ó 2011 Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V. Open access under CC BY-NC-ND license. Peer review under responsibility of Egyptian Society of Radiology and Nuclear Medicine. doi: /j.ejrnm Production and hosting by Elsevier

2 10 S.A. El Mogy et al. two radiologist analyzed the imaging data of plain spiral CT and PROPELLER diffusion MR images. Sensitivity and specificity were assessed. Results were compared with endoscopic and surgical results, which were regarded as the standard reference. Results: Ten patients had middle ear granulation tissue, 21 patients had acquired primary cholesteatomas, and 11 patients had acquired recurrent (post operative) cholesteatomas. PROPELLER diffusion MR successfully diagnosed and differentiated between granulation tissue and cholesteatomas (primary and recurrent. Sensitivity (lesions detection) and specificity (lesions characterization) of PROPELLER diffusion MR was 100%. In recurrent cholesteatomas, plain CT detected abnormal densities without any differentiation resulting in 0% specificity while in primary cholesteatomas, CT successfully diagnosed them based on associated bone erosions/destruction. Conclusion: PROPPLER diffusion Imaging is both sensitive and specific for detection and characterization of primary and recurrent cholesteatomas as it lack susceptibility and chemical-shift artifacts, and ghosts in the phase-encoding direction which occur in Echo-planar diffusion, it can detect small cholestatoma as 3 mm. It provides the highest sensitivity, specificity for detection and characterization of acquired cholesteatomas. Ó 2011 Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V. All rights reserved. 1. Introduction Cholesteatoma is a cystic lesion lined with keratin-producing squamous epithelium filled with desquamation debris in the middle ear, mastoid air cells, or petrous apex. Patients are treated surgically, but the procedure carries the risk of residual cholesteatoma and recurrence. The detection of cholesteatoma in patients who have undergone middle ear surgery using otoscope is often difficult. Therefore, second-look operations are frequently performed [1 4]. Imaging of cholesteatomas can be problematic especially in cases of recurrent disease. Computed tomography scans have been recommended before primary surgery, but cholesteatoma tissue looks similar to inflammatory tissue [5 7]. Non-enhanced magnetic resonance imaging (MRI) shows less detail of the temporal bone than CT. Enhanced scanning using gadolinium contrast, following a 45-minute delay, granulation tissue gives a hyperintense signal, whereas cholesteatoma, being avascular, does not enhance at all and can therefore be distinguished from other tissues. However, this is very time-consuming, and gadolinium is also known to occasionally cause side effects [11 15]. In echo-planar diffusionweighted MRI scans cholesteatoma is seen as a hyperintense signal, distinguishing it from other middle-ear and mastoid structures. This imaging modality is therefore useful for diagnosis of primary or recurrent cholesteatoma when the clinical diagnosis is uncertain, and also for the postoperative detection of residual cholesteatoma following canal wall up mastoidectomy [16 18]. Unfortunately susceptibility artifact occurs in echo-planar diffusion, when bone and air occur next to each other, a higher intensity MRI signal is produced, termed a susceptibility artifact. Where the temporal lobe lies adjacent to the temporal bone and the mastoid air space, a characteristic high intensity curvilinear artifact is often seen. As this is an area in which cholesteatomas can form, differentiation between susceptibility artifact and cholesteatoma can be difficult, making accurate diagnosis of small cholesteatomas problematic. There is also the risk of false positives, when the artifact is mistaken for cholesteatoma, and false negatives, when the cholesteatoma is hidden in the hyperintense artifact signal [8 10]. Periodically rotated overlapping parallel lines with enhanced reconstruction (PROPPLER) diffusion is a spin echo diffusion-weighted image, scans give images free from susceptibility artifacts. This means that small cholesteatomas as 4 mm can be detected as a bright, hyperintense signal diagnostic of cholesteatoma [19 22]. Aim of the work was to evaluate the role of periodically rotated overlapping parallel lines with enhanced reconstruction (PROPELLER) diffusion imaging in evaluation of middle ear acquired cholestatomas (primary and recurrent: post operative) and differentiating them from middle ear granulation tissue. 2. Patients and methods This prospective study conducted at a private center in Mansoura, Egypt from the period of February 2010 till Table 1 Showing plain CT imaging features of our patients. Imaging findings Middle ear lesions Differentiation between granulation tissue and cholesteatoma Ossicular chain and bone erosions or destruction Complications (temporal lobe meningitis:3, inner ear fistula:2) Mastoiditis Granulation tissue (10) +ve in all 1ry cholesteatomas (21) +ve in all +ve (5) +ve in all 2ry cholesteatomas (11) Post operative changes +ve in all Sensitivity (lesions detection): 1.00 [0.81; 1.00]...100%. Specificity (lesions characterization): 0.50 [0.34; 0.66]...50%.

3 Evaluation of acquired cholesteatoma with PROPELLER diffusion imaging 11 Table 2 Showing imaging features using PROPELLER diffusion scan combined with conventional MRI. Imaging findings middle ear lesions Hyperintense signal Granulation tissue (10) 1ry cholesteatomas (21) +ve in all 2ry cholesteatomas (11) +ve in all Sensitivity (lesions detection): 1.00 [0.81; 1.00]...100%. Specificity (lesions characterization): 1.00 [0.81;1.00]...100%. January 2011, it contained 42 patients: 32 with acquired middle ear cholesteatomas and 10 with middle ear granulation/ inflammatory tissue. They were 23 females, 19 males, their ages ranged from 12 to 53 years with a mean of 32.5 years. Patients referred from oto-rhino-laryngology clinic of Mansoura University hospital on the bases of suspected acquired cholesteatomas whether primary or recurrent. The 32 acquired cholesteatomas were classified into: primary cholesteatomas: 21 patients and recurrent (post operative) cholesteatomas: 11 patients. Among the 32 patients of cholesteatomas, 7 were bilateral and the remaining 25 were unilateral. PROPELLER diffusion MR Plain spiral CT Lesions characterization imaging modality Graph 1 Showing lesions characterization by the plain spiral CT and PROPELLER diffusion MR imaging. All patients performed spiral CT of petrous bone. Axial and coronal images were taken with the following parameters: KV;120/mAm: /WW:2740/WL:376/thickness: 1.25 mm. All patients performed MRI using 1.5 T GE medical system. Sequences obtained were the following: GRE scout (axial, coronal, sagittal), and periodically rotated overlapping parallel patients number Figure 1 (A G) Patient aged 27 years with primary acquired RT. Cholesteatoma complicated with RT. Extra axial cerebeller collection (abscess). (A) Axial T2FSE showing RT. Middle ear soft tissue mass (long arrow), mastoiditis (short arrow) and RT. Extra axial cerebellar collection (arrow head). (B and C) early post contrast axial and coronal T1WI: showing thickened enhanced cerebellar meningese (arrows) with non enhancing middle ear soft tissue mass and mastoiditis. (D) Echo-planar diffusion showing susceptibility artifacts near the skull base. (E) PROPELLER diffusion showing hyperintense signal at RT. Middle ear + extra axial abscess with no susceptibility artifacts. (F and G) Coronal and sagittal PROPELLER diffusion sowing RT middle ear cholesteatoma and extra axial cerebellar abscess.

4 12 S.A. El Mogy et al. Figure 2 (A D) Patient aged 30 years with primary LT cholesteatoma. (A and B) axial and coronal CT scan showing LT. middle ear (epitympanum) soft tissue density with ossicular rarification (arrows). (C) Axial T2WI FSE showing hyperintense signal at LT middle ear (arrow). (D) PROPELLER DWI showing hyperintense signal at LT. Middle ear confirming the diagnoses of recurrent cholesteatoma. Figure 3 (A G) Patient aged 36 years with bilateral primary cholesteatomas. (A and B) Axial and coronal CT scan showing bilateral middle ear soft tissue densities. (C) Axial T2FSE showing bilateral middle ears abnormal signal intensity. (D and E) PROPELLER diffusion images showing bilateral hyperintense signal at both middle ears consistent with bilateral cholesteatomas. (F and G) Sagittal PROPELLER diffusion images. (E) Showing RT. Cholesteatoma, (F) LT. Cholesteatoma.

5 Evaluation of acquired cholesteatoma with PROPELLER diffusion imaging 13 lines with enhanced reconstruction (PROPPLER) diffusion sequence Parameters of PROPELLER diffusion TR/TE:7000/105/FOV:22 22, matrix; /NEX:2/ thickness; 4 mm/acquisition time:4 min + 35 s. Axial images were taken then coronal and sagittal reformat were done. Correlation with endoscopic and surgical findings were done for all patients Image analysis The two radiologists worked independently, analyzed the images using a workstation (Advantage Windows, GE Healthcare). Observers assessed CT images for middle ear abnormal density, ossicular chain destruction/erosions, scutum and tygmen tympani erosions, semicircular canal fistulation, mastoid air cells, and facial nerve canal. PROPELLER diffusion images were assessed for presence of middle ear hyperintense lesion (cholestatoma) opposite the black back ground. Approval of the ethical committee was taken. Written consent was obtained from adult patients or parents of pediatric patients Statistical analyses The statistical analysis of data done by using excel program and SPSS (SPSS, Inc, Chicago, IL) program statistical package for social science version 16. The description of the data done in form of mean (+/ ) SD for quantitative data. And frequency and proportion for qualitative data. The analysis of the data was done to test statistical significant difference between groups. Paired sample t-test to compare one group at different time. Chi square test was used for qualitative data. N.B: P is significant if at confidence interval 95%. 4. Results Our study contained 42 patients, 10 had granulation tissue, 21 had primary cholesteatoma and 11 had recurrent post operative cholesteatoma. Regarding plain CT, all patients showed soft tissue density at middle ear. Ossicular chain erosions/ destruction was found in the 21 patients having primary cholesteatoma, all patients had mastoiditis. Facial nerve canal was normal in all patients. Five patients of primary cholesteatoma had complications in the form of: 3 temporal lobe and cerebellar meningitis and extra axial collections and 2 inner ear fistula. Only bone erosions diagnosed primary cholestea- Figure 4 (A E) Patient aged 21 years with LT. Acquired primary cholesteatoma. Patient complained from bilateral ear discharge. (A and B) axial CT images showing bilateral middle ear soft tissue densities. (C) Axial T2FSE showing bilateral middle ear hyperintense signals. (D & E) PROPELLER diffusion images showing LT. Middle ear cholesteatoma. Endoscopy of RT. Ear revealed granulation tissue.

6 14 S.A. El Mogy et al. toma. Recurrent cholestatoma cannot be diagnosed from CT as there were no ossicular chain. Imaging features of CT were shown at Table 1. All patients performed PROPELLER diffusion MRI. It successfully identified cholesteatomas in all the 32 patients, patients showed hyperintense signal at the region of middle ear with no susceptibility artifacts. Patients with granulation tissue did not show any hyperintense signal. Imaging features of cholesteatoma by PROPELLER diffusion scan were shown in 2Table 2. Lesions characterization by plain CT and PROPELLER diffusion MR are shown on Graph Discussion In cholesteatomas, computed tomography (CT) scans are used to identify bony structures such as ossicles, lateral semicircular canals and the facial nerve canal. Some otologists use these images before operating to familiarize themselves with any anatomical variation. However, CT differentiates poorly between different soft tissues and as such is less useful for cholesteatoma diagnosis. Granulation tissue, scar tissue, cholesterol granulomas and oedematous mucosa can all be mistaken for cholesteatoma on CT scanning, and vice versa. In CT images showing bony erosion, cholesteatoma is likely the diagnoses, in cases with previous mastoid surgery the anatomy will have been altered at the initial operation, and the diagnosis is more difficult [5 7,11]. In the current study, plain CT successfully evaluated bony structures of the middle ear, it demonstrated ossicular erosions/destruction in all primary cholesteatoma patients, it also showed erosions of tygmen tympani with subsequent meningitis and extra axial collections in three patients, also showed inner ear fistula in 2 patients, however it didn t differentiate between cholesteatomas and granulation tissue (Table 1). MR imaging is able to discriminate the non enhancing cholesteatoma from enhancing inflammatory or granulation tissue. Several reports have discussed the appearance of acquired cholesteatoma on EPI-DWI images, cholesteatomas demonstrate a hyperintensity probably based on a T2 shinethrough effect [23 25]. However, a major limitation of the EPI-DWI images still seems to be the important susceptibility artifact at the skull base (among other artifacts), the low resolution, and relatively thick sections, thus causing a size limit for detection on EPI-DWI of approximately 5 mm. [26 29]. Figure 5 (A F) Patient aged 19 years with RT. Aquired primary cholesteatoma. (A and B) Axial T2FSE, T1FSE showing RT. Middle ear, mastoid abnormal signal intensities. (C) Coronal FLAIR showing RT. Middle ear abnormal signal intensity. (D) Echo-planar diffusion MRI showing susceptibility artifacts at the region of petrous bone. (E and F) Axial and coronal PROPELLER diffusion images clearly demonstrate RT. Middle ear cholesteatoma.

7 Evaluation of acquired cholesteatoma with PROPELLER diffusion imaging 15 The ability of DWI to be used consistently to evaluate the temporal bone is hindered by image distortion caused by susceptibility artifacts, chemical-shift artifacts, and ghosts in the phaseencoding direction. This is due to the high bone attenuation of the inner ear and the numerous air-bone interfaces present within the mastoid air cells and the middle ear cavity [30 31]. With Multishot fast spin-echo (SE) periodically rotated overlapping parallel lines with enhanced reconstruction PRO- PELLER MR imaging, the marked reduction in off resonance artifacts is primarily caused by the type of sequence (fast SE): Fast SE imaging is less sensitive to changes in the constant magnetic induction field, because of multiple 180 refocusing pulses. Reduction of susceptibility artifacts is particularly important for adequate visualization of the middle ear [12]. PROPELLER DWI presents a better contrast and reduces artifacts. PROPELLER is a multishot fast SE acquisition and is based on special methods that results in an over sampling of the center of the k-space, providing a more signal-intensityrich image, removes structured motion artifacts, and enables the reduction of bulk patient motion artifacts [22]. In the current study, PROPELLER diffusion sequence successfully diagnosed all cases of cholesteatomas whether primary or secondary, it successfully differentiated cholesteatomas from granulation tissue, cholesteatomas showed hyperintense signal Figure 6 (A G) Patient aged 33 years with recurrent RT. Cholesteatoma. (A C) Axial (A and B) and coronal (c) CT scan at different levels showing RT. Middle ear soft tissue density. Note post operative changes in the form of connection of RT. Mastoid air cells with middle ear cavity (arrow). (D and E) Axial T2FSE at different levels showing RT. Middle ear + mastoid abnormal signal intensity. (F and G) PROPELLER diffusion images showing hyperintense signal at RT. Middle ear consistent with RT. Cholesteatoma.

8 16 S.A. El Mogy et al. while granulation tissue showed hypointense signal (Table 2), (Figs. 1 6). In the study of E. Flook et al., 2011, using echo-planar diffusion-weighted MRI they detected cholesteatomas as small as 4 mm, they reported that the detection of smaller cholesteatomas may also be possible. P.Lehman et al., 2009 reported that the smallest recurrent cholesteatoma diagnosed by PROPELLER diffusion was 3 mm and was surgically proved. In the current study the smallest cholesteatoma detected was 3 mm (primary) which was surgically proved and removed. Delayed post contrast MR imaging is able to discriminate the non enhancing cholesteatoma from enhancing inflammatory or granulation tissue, however it s cost and probable side effects limits it s use [28]. In the study of Aikele et al., 2003 Echo-planar diffusionweighted MR imaging combined with conventional MR imaging depicted 10 of 13 cholesteatomas (sensitivity, 77%). The three lesions that were missed were smaller than 5 mm. All the MR images of patients without cholesteatoma were correctly interpreted as showing negative findings for cholesteatoma (specificity, 100%). The positive predictive value and negative predictive value were 100% and 75%, respectively). Jindal et al., 2010 stated that echo-planar diffusion weighted imaging demonstrated a sensitivity of 83% and a specificity of 82% in the diagnosis of residual cholesteatoma. In the study of Lehman et al., 2009, he reported that PRO- PELLER provides the heights sensitivity (100%), specificity (100%), PPV (100%) and NPV (100%), for all the observers with a significant difference compared to echo planar diffusion (36.1%, 100%, 100%, 58.2%, respectively) and post contrast MRI (91.2%, 81.2%, 84.5%, 89.2%), respectively (for observers 1,2). In the current study sensitivity (lesions detection) and specificity (lesions characterization) of PROPELLER diffusion was 100% as it successfully detected, characterized the lesions. In recurrent cholesteatomas, plain CT detected abnormal densities but with out any differentiation (Fig. 6), CT detected 21 patients (50%) with primary cholesteatoma from associated bone erosions (Figs. 1 5). The principal limitation of our study was PROPELLER scan time: 4 min + 35 s, hoping in the near future the advanced technology can decrease scan time. 6. Conclusion PROPPLER diffusion Imaging is both sensitive and specific for detection and characterization of primary and recurrent cholesteatomas as it lack susceptibility and chemical-shift artifacts, and ghosts in the phase-encoding direction which occur in Echo-planar diffusion, it can detect small cholestatoma as 3 mm. It provides the highest sensitivity, specificity for detection and characterization of acquired cholesteatomas. References [1] Stangerup SE, Drozdziewicz D, Tos M, Hougaard-Jensen A. Recurrence of attic cholesteatoma: different methods of estimating recurrence rates. 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