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Cite this article as:
Dudau C, Draper A, Gkagkanasiou M, Charles-Edwards G, Pai I, Connor S. Cholesteatoma: multishot echo-planar vs non echo-planar
diusion-weighted MRI for the prediction of middle ear and mastoid cholesteatoma 2019; 1: 20180015.
Received:
31 July 2018
Accepted:
15 December 2018
Revised:
31 October 2018
ORIGINAL RESEARCH
Cholesteatoma: multishot echo-planar vs non echo-
planar diusion-weighted MRI for the prediction of
middle ear and mastoidcholesteatoma
1CRISTINA DUDAU, 2ASHLEIGH DRAPER, 3MARIA GKAGKANASIOU, 4GEOFFREY CHARLES-EDWARDS,
5IRUMEE PAI and 1STEVE CONNOR
1Department of Radiology, Guy’s and St Thomas’ Hospital, and Department of Neuroradiology, King’s College Hospital, London,
2GKT School of Medicine, King's College, London, United Kingdom
3General & VA Air Force Hospital, Athens, Greece
4Department of Medical Physics, Guy’s and St Thomas’ Hospital, and School of Biomedical Engineering and Imaging Sciences, King's
College London, London,
5Department of Otolaryngology, Guy’s and St. Thomas’ Hospital, London,
Address correspondence to: Dr Cristina Dudau
E-mail: cristinadudau@ doctors. org. uk
INTRODUCTION
Diusion-weighted MRI (DW-MRI) is a powerful tool
for the detection of cholesteatoma. Over the past decade,
numerous imaging studies have been performed looking
into detection of cholesteatomas, investigating both echo
planar imaging (EPI) and non-EPI DWI sequences.1–3
e single shot EPI (SS-EPI) DWI sequence is a standard,
fast and relatively insensitive to motion artefact technique,
however, limited by a poorer resolution due to the single
shot.3–7 Furthermore, it is very sensitive to B0 inhomoge-
neities such as those arising at bone–tissue and air–tissue
interfaces, with resulting susceptibility artefacts and
geometric distortion masking areas of restricted diusion.8
Cholesteatomas of smaller size can be missed using SS-EPI,
with the limit of detection of 5 mm in a study by Vercruysse
et al.3
Non-EPI DWI sequences are turbo spin echo (TSE)-based
techniques and have been most extensively evaluated with
a single shot TSE (SS-TSE) sequence. ese generally have
a lower SNR than EPI (Figure1) but are much less sensi-
tive to magnetic susceptibility mismatches and geometric
distortion, leading to better lesion detection.9–12 In a
study by De Foer et al13 the detection of cholesteatomas
https:// doi. org/ 10. 1259/ bjro. 20180015
Objective: We aimed to compare a newer readout-seg-
mented echoplanar imaging (RS-EPI) technique with
the established single shot turbo spin echo (SS-TSE)
non-EPI diusion-weighted imaging (DWI) in detecting
surgically validated cholesteatoma.
Methods: We retrospectively reviewed 358 consecutive
MRI studies in 285 patients in which both RS-EPI and
non-EPI DWI sequences were performed. Each diu-
sion sequence was reviewed independently and scored
negative, indeterminate or positive for cholesteatoma in
isolation and after reviewing the T1W sequence. Average
artefacts scores were evaluated and the lesion size
measured as a distortion indicator. The imaging scores
were correlated with surgical validation, clinical and
imaging follow-up.
Results: There were 239 middle ear and central mastoid
tract and 34 peripheral mastoid lesions. 102 tympa-
nomastoid operations were performed. The positive
predictive value ( PPV), post-operative PPV, primary
PPV, negative predictive value were 93%, 95%, 87.5%,
70% for RS-EPI and 92.5%, 93.6%, 90%, 79% for non-EPI
DWI. There was good agreement between the two tech-
niques (k = 0.75). Non-EPI DWI is less susceptible to skull
base artefacts although the mean cholesteatoma meas-
urement dierence was only 0.53 mm.
Conclusion: RS-EPI has comparable PPV with non-EPI
DWI in both primary and post-operative cholesteatoma
but slightly lower negative predictive value. When there
is a mismatch, non-EPI DWI better predicts the presence
of cholesteatoma. There is good agreement between
the sequences for cholesteatoma diagnosis. The T1W
sequence is very important in downgrading indetermi-
nate DWI signal lesions to a negative score.
Advances in knowledge: This is, to our knowledge, the
first study to compare a multishot EPI DWI technique
with the established non- EPI DWI in cholesteatoma
diagnosis.
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measuring 2–3 mm has been possible using non-EPI DWI. A
recent meta-analysis by Li et al14 calculated an overall sensi-
tivity and specicity of 94% for non-EPI DWI techniques, with
more recent literature reviews also concluding a strong recom-
mendation of using non-EPI DWI for clinical detection of
cholesteatomas.15
Multishot-EPI (MS-EPI) is an alternative echo planar approach
in which signal-intensity acquisition can be divided into several
“shots” or repetition time periods, with substantially shorter
echo-spacing than SS-EPI, greatly reducing the sensitivity to
the eects of magnetic susceptibility mismatches. is results
in reduced image distortion and a similar signal-to-noise ratio
(SNR) compared with SS-EPI, at the expense of a longer imaging
time.16,17 Yamashita et al18 found MS-EPI superior to the SS-EPI
techniques in diagnosing recurrent or residual cholesteatoma,
with increased accuracy from 74.1 to 87.9% when comparing
29 patients prospectively. More recently, Algin et al19 also found
better sensitivity, specicity, positive predictive value (PPV) and
negative predictive value (NPV) as well as fewer artefacts and
better visibility scores when comparing MS-EPI with SS-EPI in
30 patients.
However, non-EPI DWI remains the standard for the MRI diag-
nosis of cholesteatoma, and there is currently no study directly
comparing MS-EPI with non-EPI DWI.
Our primary aim was to compare the PPV of a readout segmented
EPI (RS-EPI) (RESOLVE = REadout Segmentation Of Long
Variable Echo trains) which is a type of MS-EPI DWI sequence,
with a SS-TSE non-EPI DWI sequence (HASTE = Half-Fourier
Acquisition SS-TSE) in detecting primary and postoperative
cholesteatoma.
Secondary objectives were to evaluate the PPV in primary vs
post-operative residual cholesteatoma, estimate NPV of the two
techniques, assess the likelihood of cholesteatoma when there
is a mismatch between the DWI signal on the two sequences,
investigate the impact of additional T1W MRI sequence on the
DWI based diagnosis, evaluate percentage agreement between
the two sequences and investigate the eects of image distortion
on cholesteatoma size measurements.
METHODS AND MATERIALS
Institutional review board approval with waiver of informed
consent was obtained for this retrospective analysis. e
radiology management system (CRISTM; Healthcare Soware
Solutions; Manseld, UK) was retrospectively interrogated over
a 40 months period from 2013 to 2017. MR studies were included
if the clinical request for imaging or the report text contained
“cholesteatoma”. Studies that did not have both non-EPI and
RS-EPI DWI sequences (11) were excluded. Some patients had
multiple studies performed and several patients had more than
one lesion analyzed.
MRI was performed using a 1.5 T Aera MR imaging system
(Siemens, Erlangen, Germany). e sequence parameters
(TR/TE/acquired spatial resolution/acquisition time) were
3240/68/1.2 × 1.2 × 2 mm/1.45 s for RS-EPI and 2000/103/1.15 ×
1.53 × 3/278 s for non-EPI DWI. Both sequences were acquired
in coronal plane with b-values of 0 and 1000 s mm–2. RS-EPI had
seven segments.
e studies were viewed on a GE Centricity PACS workstation
(GE Medical Systems, Milwaukee, WI). Each diusion sequence
was reviewed independently from the other sequence by one of
two neuroradiologists with 2 and 3.5 years of experience and was
Figure 1. Matched slice thickness images demonstrate higher SNR for RS-EPI DWI (A) vs SS-TSE non-EPI DWI (B). DWI, diu-
sion-weighted imaging; RS-EPI, readout-segmented echoplanar imaging; SNR, signal-to-noise ratio; SS-TSE, single shot turbo spin
echo.
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scored according to the signal intensity relative to that of white
matter. e score was negative if there was hypointense DWI
signal, indeterminate if there was DWI isointense signal and
positive for cholesteatoma in the presence of hyperintense DWI
signal. Each scoring was performed twice on separate occasions,
both in isolation and aer reviewing the T1W sequence, when
some lesions were “downgraded” to negative if shown to be T1W
hyperintense (Figure2). Only a nal positive score was consid-
ered to represent cholesteatoma.
e lesion size was recorded on each sequence as the maximum
coronal diameter of maximal hyperintense signal, without
penumbra, on standardized unadjusted non-magnied window
settings. e presence of artefact and the susceptibility score
were also documented (0–3: 0, no artefact; 1, artefact at the
skull base; 2, artefact below the skull base; 3, artefact interfering
with diagnosis; Figure3). e lesion location was designated as
involving the middle ear and central mastoid tract (MECMT)
or the peripheral mastoid air cells (PM). In the case of the PM,
only the largest lesion was considered. Lesions of the external
auditory meatus and petrous apex (10) were excluded. If a lesion
was extending between two compartments, it was placed into
the compartment that contained the majority of the lesion. Clin-
ical and demographic information was recorded. For patients
undergoing subsequent tympanomastoid surgery, the intraop-
erative diagnosis of cholesteatoma was recorded and correlated
with the imaging ndings. Where surgical validation was not
performed, the clinical and imaging follow-up was recorded
in order to determine whether cholesteatoma was felt likely at
follow-up. A lesion was deemed clinically stable if there was no
upgrade in lesion size or suspicion score on follow-up imaging
and there was no clinical suspicion of recurrence. Primary and
postoperative cholesteatomas were analyzed both together and
separately.
Statistical analysis was performed with JMP soware (JMP
14.0, SAS Institute, Cary, NC). Cohen's κ was used to calculate
the lesions score agreement and the paired t-test for calculating
the mean dierence between lesion measurements, (p < 0.01).
e impact of T1W sequence on downgrading the two diusion
sequences scores was compared using χ2.
RESULTS
ere were a total of 285 patients, 59 of whom had more than
one study performed and 43 patients had more than one lesion
analyzed; a total of 358 MRI studies were reviewed, in which 426
entries were scored.
Figure 2. Hyperintensity score. T1 hyperintensity (A) downgrades the DWI reading on both RS-EPI (B) and non-EPI (C), arrows.
RS-EPI, readout-segmented echoplanar imaging.
Figure 3. Susceptibility artefact scores for RS-EPI, examples: 0, no artefact (image A thin arrow); 1, usual artefact at the skull base
(image B and image C, arrowheads); 2, artefact below the skull base (image A thick arrow); 3, artefact interfering with diagnosis
(image C dash arrow). RS-EPI,readout-segmented echoplanar imaging.
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e mean age was 43 years (7–87), M:F ratio 1.13:1.
ere were 239 MECMT and 34 PM lesions detected on either
RS-EPI and/or non-EPI DWI while 153 studies were negative for
cholesteatoma on both sequences.
Documented surgical validation allowed evaluation of PPV in
97/239 MECMT lesions (Table 1) and in 5/34 PM lesions. e
mean interval between imaging and surgery was of 250.3 ± 20.3
days.
e PPV of RS-EPI in the 57 positive surgical validated cases was
93%, with post-operative and primary cholesteatoma PPVs of 95
and 87.5% respectively.
Non-EPI DWI had an overall PPV of 92.5% when analyzing
the 67 positive surgically validated cases, with PPVs of 93.6% in
post-operative and 90% in primary cases.
For the selected group of 40 operated negative RS-EPI cases,
the NPV was 70%, while for the 30 operated negative non-EPI
DWI cases, the NPV was 80%. e combined NPV for the 25
operated cases which were negative on both techniques was 84%
(Table1).
Only one out of the ve operated PM lesion was found to have
cholesteatoma.
ere were 10/114 “mismatch” cases in which the RS-EPI
sequence was positive but non-EPI DWI was either indeter-
minate or negative (Figure 4 and Figure 5). Conversely, there
were 20/124 mismatch cases which were non-EPI DWI positive
but RS-EPI indeterminate or negative (Figure6 and Figure 7).
Non-EPI DWI positive but RS-EPI negative scores were more
likely to demonstrate cholesteatoma (12/20, 60%) on surgical
and clinical follow-up than RS-EPI positive but non-EPI DWI
negative scores (2/10, 20%).
None of the non-operated RS-EPI positive mismatched lesions
and only one of the non-operated mismatched non-EPI positive
cases was clinically suspected to have cholesteatoma over 469 ±
Table 1. PPV, NPV and combined NPV for the 97 MECMT lesions
RS-EPI Non-EPI
Positive 57 67
Primary 16 20
Secondary 41 47
True positive 53 62
Negative 40 30
True negative 28 24
PPV 93% 92.5%
NPV 70% 80%
Negative on both 25
True negative on both 21
Combined NPV 84%
NPV, negative predictive value; PPV, positive predictive value.
Figure 4. Mismatched definite RS-EPI lesions and surgical validation. DWI,diusion-weighted imaging; RS-EPI, readout-seg-
mented echoplanar imaging.
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162 days of follow-up. ere was no further imaging performed
for the non-operated mismatched cases.
Of the 171/273 non-operated studies, 94.8% of negative studies
on RS-EPI (n = 163) and 96.7% of negatives (n = 147) showed
stability/no clinical suspicion of recurrence over a clinical
follow-up of 458.8 ± 20 days. 76 RS-EPI and 78 non-EPI DWI
studies had no clinical data available. 33 lesions with one or more
further follow-up imaging studies remained stable and negative
by both techniques, including two lesions clinically suspicious
for cholesteatoma.
e evaluation of the impact of subsequent T1W image review on
the DWI diagnosis of cholesteatoma (Table 2) revealed similar
percentages of intermediate scored MECMT lesions by each
sequence, 27.5% of RS-EPI and 32.2% of non-EPI DWI cases on
initial assessment, respectively. Aer T1 signal assessment, 58.7%
indeterminate lesions were downgraded to negative on RS-EPI
and 62.5% indeterminate studies were downgraded to negative
on non-EPI DWI. When looking at the mastoid studies only, the
T1 sequence contribution was even greater, dismissing 78.6%
indeterminate RS-EPI lesions and 66.7% indeterminate non-EPI
DWI lesions. ere was no statistical dierence in downgrading
Figure 5. Mismatch cases in which the non-EPI DWI sequence was negative (A) but RS-EPI was positive (B, arrowhead). DWI,
diusion-weighted imaging; RS-EPI, readout-segmented echoplanarimaging.
Figure 6. Mismatched definite non-EPI DWI lesions and surgical validation. DWI, diusion-weighted imaging; RS-EPI, readout-seg-
mented echoplanar imaging.
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by T1w on the two DWI sequences for CECT/PM lesions (p <
0.001).
For the 426 scored entries, the statistical agreement of nal
scoring by the two DWI techniques was good, k = 0.75. 10.8% of
lesions diered by one score point and 4.2% by two score points.
e average artefact score for RS-EPI (0–3) was 0.73, when
considering all the 426 scored entries. e average non-EPI DWI
artefact score was 0; there were three braces distortion. For the
239 MECM lesions, the average measurement dierence between
the two sequences was 0.53 mm (0.15–0.91).
DISCUSSION
DW MRI imaging has become instrumental in the detection of
both primary and post-operative cholesteatoma, with preferen-
tial use of non-EPI DWI techniques over standard EPI DWI as
the current recommendation. To our knowledge, this is the rst
direct comparison of a multishot EPI (in this case RS-EPI) with
a widely used non-EPI DWI (SS-TSE) in cholesteatoma evalu-
ation. As RS-EPI sequence can be achieved with a signicantly
shorter TE, there is resultant higher SNR than with non-EPI
DWI (Figure1), which could be potentially traded for shorter
acquisition time or thinner slices. e shorter TE also accounts
for reduced imaging distortion in comparison with SS-EPI,16,17,19
hence we felt this new technique merits evaluation against the
established non-EPI DWI.
When examining 273 lesions in which both RS-EPI and non-EPI
DWI sequences were performed, 102 of which had subsequent
surgical correlation, we found very similar PPV’s for the two
techniques of 93/92.5% respectively, results comparable with the
generally accepted PPV values for non-EPI DWI.13,14,20 Both
techniques had better PPV in post-operative cholesteatoma
when compared to primary disease, similarly to the system-
atic review by Van Egmond15 which found superior PPV’s for
non-EPI DWI, of 96–100% in post-operative cases compared
to 85–100% in primary cholesteatoma. is is presumed due
to incipient disease and small retraction pockets in primary
cholesteatomas,21 however a signicant dierence in primary
vs post-operative lesion size has not been found in our lesion
sample.
Although the lack of comprehensive surgical validation
precluded calculation of an encompassing NPV, a comparison
was made between imaging ndings and the available surgical
and clinical outcomes. e NPV for RS-EPI was slightly lower
at 70% vs non-EPI DWI which had an NPV of 80%, however
only a limited number of operations were performed (40 and
30 respectively) and so NPV was largely based on a stable
Figure 7. Mismatch cases in which the non-EPI DWI sequence was positive (A, arrowhead) but RS-EPI was negative (B). DWI,
diusion-weighted imaging; RS-EPI, readout-segmented echo planar imaging.
Table 2. Initial lesion scores by RS-EPI and non-EPI DWI and role of T1 sequence in resolving them
RS-EPI RS-EPI mastoid Non-EPI Non-EPI mastoid
Indeterminate lesions, rst reading 75 14 88 18
Aer T1 assessment, downgraded to negative 44 11 55 12
Denite lesions, rst reading 143 16 152 10
Aer T1 assessment, downgraded to negative 11 9 5 3
DWI, diusion-weighted imaging; RS-EPI, readout-segmented echoplanar imaging.
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clinical follow-up period without surgical validation. A similar
percentage of studies showed no clinical suspicion of residual
or recurrent disease over the clinical follow-up period, 94.8% of
RS-EPI (n = 163) and 96.7% of non-EPI DWI (n = 147) studies.
ere appears to be only a small proportion of additional false
negative studies in the RS-EPI lesion group, the calculation is,
however, limited by the large number of studies with no clinical
data available.
ere was a modest increase in the NPV value when looking
at the operated studies that were negative on both DWI tech-
niques, to 84%, this may be used to increase the condence of a
true-negative study in selected cases such as before discharging
a patient from clinical follow-up or to avoid imaging follow-up
in dicult settings such as children requiring general
anaesthesia.
When looking at our mismatched lesions (scored denite by one
technique and intermediate/negative by the other), we validated
them against surgery, clinical and imaging follow-up. Although
based on very small numbers, the small series of 17 operated
mismatched studies reveal a greater proportion of false-negative
studies in the RS-EPI group, 11 vs 2 in the non-EPI DWI group.
We found that non-EPI DWI positive but RS-EPI negative scores
were more likely to demonstrate cholesteatoma on surgical and
clinical follow-up than RS-EPI positive but non-EPI DWI nega-
tive scores, by a ratio of 3:1.
ere is little literature available looking at the additional role
of T1W sequences in cholesteatoma diagnosis and although
their impact has been recognised, it has not formally been
quantied. To objectively assess this, we performed two sets
of readings, before and aer T1 sequence assessment, the
second reading more in keeping with a clinical setting reading.
We found similar considerable proportions of indeterminate
scored lesions on initial assessment with either sequence,
27.5% by RS-EPI and 32.2% by non-EPI respectively. Over
half of intermediate MECMT lesions were dismissed aer
T1W signal assessment on both techniques. e T1W sequence
had an even greater role in downgrading over two-thirds of
PM lesions, which appear to be mostly not cholesteatomas. In
addition, there was no statistical dierence in the likelihood of
downgrading by T1W sequence on the two DWI sequences for
CECT and PM lesions.
A similar lesion scoring approach and rationale was used by
Yamashita,18 however, at a single time point, so that the impact of
the T1W sequence in lesion solving was not separately quantied.
Several authors reported false-positive studies corresponding to
hyperintense signal on the conventional T1 weighted images and
attributed them to fat in the mastoidectomy cavity or blood.22,23
We presume that these appearances may also be due to inspis-
sated secretions, and our ndings are further supported by
the lack of lesion progression on follow-up imaging. Our nd-
ings emphasise the major contributory role of conventional T1
weighted sequences in correlation with DWI in cholesteatoma
assessment.
It is well established that non-EPI techniques are associated
with decreased susceptibility artefacts at the skull base by
comparison with EPI techniques.10 Not entirely surprisingly,
when calculating average artefacts scores for each technique
we found our average non-EPI DWI artefact score was 0. e
average artefact for RS-EPI (0–3) was 0.73 in the 426 scored
entries, overall less than the usual artefact expected at the skull
base, implying a signicant proportion of studies with no arte-
fact. Although non-EPI DWI is less susceptible to skull base
artefacts, RS-EPI artefact was mild and not interfering with
diagnosis.
Severe distortion caused by dental devices was recorded in three
cases, precluding imaging interpretation on both sequences.
To further quantify distortion, we calculated the mean lesion
measurement dierence by the two techniques, while excluding
the smaller mastoid lesions from the calculation in order to avoid
skewing the data. ere was only 0.53 mm dierence in the 239
MECM lesions inferring little dierence in distortion. e posi-
tive condence interval suggests the lesions measured larger on
RS-EPI compared to non-EPI DWI.
We also found a good nal score agreement between the two
DWI sequences, k = 0.75, with only 18/426 lesions disagreeing
by two score points.
Our study has several limitations. ere was a dierence in
slice thickness between the two techniques, with thinner
RS-EPI sections at 2 vs 3mm for non-EPI DWI sections,
potentially increasing the lesion detection by RS-EPI DWI.
Our scoring was performed by two dierent observers, with
possible bias from interobserver variability. Furthermore, not
all the patients had available clinical follow up data. Only 102
cases had surgical correlation, limiting our calculation of NPV.
ere was also a time gap from scan acquisition to surgery
of 250.3 days, during which time a lesion could have poten-
tially developed or self-evacuated, confounding the predictive
values calculations.
RS-EPI appears to be an improved EPI DWI sequence with
reduced susceptibility artefacts whilst having similar PPV
and good agreement with the established non-EPI DWI. Our
results suggest that if RS-EPI was to replace non-EPI DWI,
there is a potential risk of failure to detect some cholestea-
tomas. As a solution, there is scope to increase the number
of segments to reduce distortion at the expense of acquisi-
tion time and if further validated, RS-EPI could eventually
provide the advantage of shorter acquisition time and better
SNR. As it stands, RS-EPI could be introduced in addition to
non-EPI DWI in selected cases, to increase the condence of a
true-negative study.
CONCLUSIONS
RS-EPI has comparable PPV with non-EPI DWI in both
primary and post-operative cholesteatoma but slightly lower
NPV. When there is a mismatch, non-EPI DWI better predicts
the presence of cholesteatoma and has slightly higher PPV
than RS-EPI. ere is good agreement between the sequences
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for cholesteatoma diagnosis. e T1W sequence is equally
important to both sequences in downgrading indeterminate
DWI signal lesions to a negative score, particularly in the PM
region. Non-EPI is less susceptible to skull base artefacts, but
there is <1 mm dierence in lesion measurement as a result of
dierential distortion.
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