International Journal of Urology (2017)
13289
Original Article
Diagnostic performance of contrast-enhanced ultrasonography and
magnetic resonance imaging for the assessment of complex renal
cysts: A prospective study
Guillaume Defortescu,1 Jean-Nicolas Cornu,1 Sofiane B
ejar,2 Anthony Giwerc,1 Francßoise Gobet,3
Claire Werquin,2 Christian Pfister1 and Francßois-Xavier Nouhaud1
1
Urology Department, 2Radiology Department, and 3Pathology Department, Rouen University Hospital, Rouen, France
Abbreviations & Acronyms
CEUS = contrast-enhanced
ultrasonography
CT = computed tomography
MRI = magnetic resonance
imaging
NPV = negative predictive
values
PPV = positive predictive
values
US = ultrasonography
Correspondence: Francßois-
Xavier Nouhaud M.D., Urology
Department, Rouen University
Hospital, 1 rue de Germont,
76031 Rouen Cedex, France.
Email: fx.nouhaud@chu-rouen.fr
Received 19 May 2016;
accepted 5 December 2016.
© 2017 The Japanese Urological Association
doi: 10.1111/iju.
Objectives: To compare the diagnostic performance of computed tomography,
magnetic resonance imaging and contrast enhanced ultrasonography for the assessment
of complex renal cysts.
Methods: We carried out a prospective single-center study from January 2012 to
December 2013. We included patients with Bosniak category 2F or 3 renal cysts found
on computed tomography and reviewed by two expert radiologists. Magnetic resonance
imaging and contrast-enhanced ultrasonography were then carried out. Patients with a
Bosniak ≥3 cyst on magnetic resonance imaging, as well as those upgraded as
appearing malignant on contrast-enhanced ultrasonography, were surgically managed.
Imaging results were compared with histological data. For patients without surgery,
imaging examinations were compared with follow-up data. For each imaging
examination, diagnostic performance and Cohen’s kappa coefficient were assessed.
Results: A total of 47 patients were included. The median follow up was 36 months
(range 17–48 months). At initial computed tomography, cysts were classified as
Bosniak 2F and Bosniak ≥3 in 34 and 13 patients, respectively. Magnetic resonance
imaging found 13 Bosniak ≥3 cysts, and contrast-enhanced ultrasonography upgraded
six more patients with cysts that appeared malignant. A total of 19 patients had surgery.
Histological analysis reported 14 malignant tumors. No tumor progression was found in
followed-up patients. Computed tomography showed poor sensitivity (36%) and
specificity (76%; j = 0.11). Magnetic resonance imaging showed 71% sensitivity and 91%
specificity (j = 0.64). Contrast-enhanced ultrasonography showed high sensitivity (100%)
and specificity (97%), and a negative predictive value at 100% (j = 0.95).
Conclusions: The present results suggested that contrast-enhanced ultrasonography
could be useful in improving the assessment of complex renal cysts. Indeed, computed
tomography accuracy might be limited in this indication requiring further investigations
to determine the best treatment strategy.
Key words: computed tomography, contrast media, diagnostic imaging, magnetic
resonance imaging, renal cyst.
Introduction
Renal cysts are frequently encountered in clinical practice, with an incidence rate of approxi-
mately 50% in patients aged >50 years.1 At diagnosis, the main challenge is to discriminate
benign cysts from cystic renal cell carcinomas requiring specific oncological care. These cys-
tic cancers are reported in up to 10% of renal cancers.2 Although radiological diagnosis of
simple cysts and highly suspicious lesions is quite simple, characterizing complex cysts can
be difficult.2 Indeed, these atypical cysts consist of a set of benign or malignant lesions, and
their characterization is sometimes difficult, but nonetheless essential to determine the best
treatment strategy.
To date, the Bosniak classification is used most commonly to guide the management of
renal cysts. It allows the classification of cysts according to morphological criteria, representa-
tive of their oncological potential.3–5 However, in this classification, two categories remain
undetermined: cysts 2F and 3 corresponding to malignant lesions, respectively, in 10% and
50% of cases.6 For these cysts, the guidelines recommend using all imaging techniques avail-
able (MRI, CEUS and CT scan) as soon as necessary to narrow down the diagnosis.6 In
1
G DEFORTESCU ET AL.
addition, biopsy of these cystic lesions is not recommended,
thus limiting histological evidence for the best treatment strat-
egy.6,7 As a result, the therapeutic decision is based mainly
on radiological findings.
In this context, CEUS seems to be the optimal examination
for characterization of these lesions.8 Indeed, it provides a
better time resolution than CT or MRI, because it allows a
real-time view of enhancement.8,9 Thus, it improves the
detection of blood vessels in renal masses. It also has a
higher spatial resolution.8,9 As such, the advantages of CEUS
make it a useful tool for improving the radiological diagnosis
of atypical cysts, as several recent studies have suggested.8–12
The aim of the present study was to compare the diagnos-
tic performances of CEUS, CT scan and MRI in the treat-
ment of atypical cystic renal tumors classified as Bosniak 2F
or 3.
Methods
Patients
We carried out a prospective single-center observational study
from January 2012 to December 2013. During this period, 59
patients referred consecutively to our tertiary care center for
an asymptomatic renal cyst Bosniak 2F or 3 on contrast-
enhanced CT were considered for inclusion. A total of 47
patients were definitely included after a centralized CT
review by two expert radiologists had confirmed the cysts
were Bosniak 2F or 3. Patients with contraindication to con-
trast-enhanced MRI were excluded, as well as patients with a
symptomatic cyst and those without a CT scan available or
of low quality, especially slice thickness >2.5 mm (see
below). A flow chart of the study is represented in Figure 1.
All included patients gave their informed consent for renal
MRI and CEUS for diagnostic purposes, and the principles of
Helsinki were respected.
Radiological study
At Rouen University Hospital, Rouen, France, CTs were car-
ried out with a 64-slice scanner (GE discovery HD 750; GE
Healthcare, Chicago, IL, USA). Studies were carried out
using 120 KVp and 280 mAs. Contrast media (1.5 mL/kg of
non-ionic Omnipaque 350 mg/mL Ihhexol; GE Healthcare)
was intravenously injected at the rate of 2–3 mL s through a
power injector. Images were obtained at the unenhanced,
nephrographic and early excretory phase. The following
parameters were used: section 1.25/1.25 mm, pitch 1375,
rotation time 0.7 s, detector width 0.675 9 64 = 40 mm,
scan field of view 50 cm and matrix 512.2 Outside CTs were
also considered if they were carried out according to a similar
protocol with slice thickness up to 2.5 mm. Renal MRI and
CEUS were then carried out for each included patient within
1 month after enrolment. These radiological examinations
were carried out blinded to previous imaging data.
CEUS
All CEUS were carried out by a third different radiologist,
experienced in renal CEUS (>100 cases), according to a stan-
dardized protocol using ultrasonography machine ACUSON
2 © 2017 The Japanese Urological Association
59 patients considered for
inclusion with a Bosniak 2F
or 3 renal cyst on a CT-scan
12 patients excluded
3 upgraded Bosniak 4
Centralized radiological
review of the CT-scans 2 downgraded Bosniak 2
7 no or low quality CT scans
47 patients included
Having both MRI an CEUS
Bosniak ≥3 on MRI?
No
Malignant on CEUS? Yes
No Yes
Imaging follow-up Surgical treatment
Fig. 1 Flow chart of the included patients and surgical treatment strategy.
S2000-Siemens–10 (Siemens Healthcare, Erlangen, Germany).
A convex probe was used with frequency ranging from 3 to
4.5 MHz. Each lesion was scanned first using unenhanced
gray-scale ultrasonography in the harmonic mode. Then, each
cyst was scanned after injection of an intravenous bolus of
(1.2 mL) microbubbles (Sonovue; Bracco Imaging, Milan,
Italy) followed by 10 mL normal saline flash. Technical
parameters were: Cadence Contrast Pulse Sequencing (Acu-
son – Siemens Healthcare) as the contrast-specific mode with
sensitivity similar to the microbubble harmonic signal, low
transmission power insonation (mechanical index 0.06–0.1),
dynamic range of 80 dB, temporal resolution between frames
of 71–100 ms (10–14 frames/s) and one focus below the
renal cyst.
MRI
MRI was carried out on MRI ACHIEVA 1.5T-PHILIPS-07
device (Philips Healthcare, Amsterdam, The Netherlands).
MRI examinations were carried out with a phase-array body
coil with the patient in the supine position. Each examination
included: axial and coronal half Fourier single shot fast (or
turbo) spin echo images (TE: 80 ms, TR: 362 ms, Flip angle:
90°, breath hold), axial T2-weighted TSE with fat suppres-
sion (TR: 3466 ms, TE: 70 ms, Flip angle: 90°, slice: 5 mm,
respiratory triggering, matrix 272 9 156), axial T1-weighted
gradient echo sequence, in phase and opposed phase (TR:
103 ms, TE: 4.6/2.3 ms, flip angle 55°, slice 5 mm, breath
hold matrix 192 9 94) as dual echo sequence and axial 3-D
fat-suppressed GRE T1-weighted imaging (TR: 415 ms, TE:
2.2 ms, flip angle 10, slice 2.5 mm, matrix 256 9 18)
 Imaging assessment of complex renal cyst

obtained before and after the intravenous administration of

contrast media (Gadovist 1 mmol/mL; Bayer, Leverkusen, Table 1 Patient’s characteristics

Germany) at the corticomedullary, nephrographic and delayed Variables n (%)

phases. No. patients 47
For CT and MRI, the cystic lesions were classified accord- Median age at diagnosis 64.7 (37–76)
ing to the Bosniak classification using the described criteria Sex (male/female) 30 (64%)/17 (36%)
for CT and MRI classification (3–5.13). A 1-mm threshold Median body mass index (kg/m2) 25.8 (18.7–38.4)
was used to determine the boundary between perceptible and Median tumor size (cm) 3.8 (1.8–5.8)
Tumor side (left/right) 28 (60%)/19 (40%)
measurable enhancement, and classify the cyst as 2F (percep-
Tumor location (anterior/posterior) 27 (57%)/20 (43%)
tible, ≤1 mm) or 3 (measurable, >1 mm). CEUS classified Tumor location (lateral) 23 (49%)
the cysts as appearing benign or malignant. The malignancy Surgical treatment 19 (40%)
criteria for CEUS were contrast enhancement of the septa Histological data (n = 19)
and/or the walls, the same 1-mm threshold was used between Clear cell carcinoma 8 (42%)
perceptible and measurable. Perceptible enhancement was Papillary carcinoma 3 (16%)
Chromophobe carcinoma 2 (11%)
considered as benign.
Other renal cell carcinoma 1 (5%)
Infected cyst (benign) 1 (5%)
Treatment strategy Cystic nephroma (benign) 4 (21%)

Patients with a cyst described as Bosniak ≥3 on MRI and

those with a cyst upgraded as appearing malignant on CEUS
underwent surgical treatment (Fig. 1). For patients with both
MRI and CEUS pointing to a benign lesion (≤Bosniak 2F), a
follow up by renal imaging (CT or MRI) was scheduled
every 6 months for 5 years, according to the guidelines.3,6 In
cases of radiological progression during follow up, patients
were offered surgical treatment.
Statistical analysis
Demographic, clinical and imaging data (including age at
inclusion, sex, Bosniak classification, tumor location, surgical
treatment and imaging follow-up data) were collected in a
dedicated database at inclusion and during follow up. In addi-
tion, histological data were collected for patients who had
surgery.
The initial radiological diagnosis of each examination (CT,
MRI and CEUS) was compared with the final diagnosis in
order to determine the sensitivity, specificity, PPV, NPV,
accuracy and the rate of undetected cancers for each imaging
technique. In this aim, the final diagnosis was defined accord-
ing to Bertolotto et al. and Chen et al.8,9 For patients who
had surgery, tumors were classified as either benign or malig-
nant based on histological diagnosis. For patients followed
up, classification was based on tumor progression on imaging
examination, with a median follow up of 36 months (range
17–48 months). Lesions, which had not evolved at last fol-
low-up imaging examination, were considered as benign.
The Cohen kappa coefficient was also calculated to assess
the agreement of imaging techniques and final diagnosis.
Statistical analyses were made with the 12.0.3.0 version of
MedCalc software (MedCalc Software bvba, Ostend, Bel-
gium).
Results
A total of 47 patients were included in the present study – 30
men (64%) and 17 women (36%). The median age was
64.7 years (range 37–76 years) with a median follow up of
36 months (range 17–48 months).
Patient and tumor characteristics are detailed in Table 1.
On CT, cysts were classified as Bosniak 2F and Bosniak 3 in
34 and 13 patients, respectively (Table 2). On MRI, cysts
were classified as Bosniak 2F and Bosniak ≥3 in 34 patients
and 13 patients, respectively, with five patients upgraded to
Bosniak ≥3 compared with CT scan (Table 2). On CEUS, 15
cysts (31.9%) were classified as malignant and 32 (68.1%) as
benign, including nine patients who were upgraded to
malignant compared with the CT results (Table 2).
A total of 19 patients (40%) had surgery according to the
aforementioned criteria. Histological analysis found 14 malig-
nant tumors and five benign tumors. Histological data are
given in Table 1. Among the 28 patients followed up, none
presented any upgrade of their cyst during a median follow
up of 36 months.
The diagnostic values of the different imaging examina-
tions are detailed in Table 2 and Figure 2. We found that CT
had low sensitivity (36%) and specificity (76%), with a low
kappa coefficient (0.11). MRI showed higher sensitivity
(71%) and specificity (91%), and a kappa coefficient of 0.64
(range 0.39–0.88). CEUS showed superior results, with a sen-
sitivity of 100% and a specificity of 97%, a positive predic-
tive value of 93%, and a negative predictive value of 100%.
Furthermore, it was the only examination with a 0% rate of
undetected cancer. Finally, the kappa coefficient of CEUS
was also high: 0.95 (range 0.85–1). Figure 3 shows a sample
CEUS usefulness.
Discussion
Bosniak classification based on review of a single CT of a
cyst might be insufficient to determine optimal treatment
strategy. Further morphological assessment using more accu-
rate imaging examinations appears necessary.
In this context, the present results suggested that CEUS
provides higher diagnostic accuracy than MRI or CT. Stan-
dard US has a low contrast resolution combined with high
acoustic disturbance, and Doppler is too limited for the detec-
tion of microvessels. This explains the need to use CT and

© 2017 The Japanese Urological Association 3

G DEFORTESCU ET AL.

Table 2 Imagung results and diagnostic value of CT scan, MRI and CEUS for complex renal cysts assessment

Imaging Final diagnosis Diagnostic value of imaging exams

Type Diagnostic Benign Malignant Total Sensitivity Specificity PPV NPV Accuracy Missed cancers j (Cohen)
CT scan Bosniak 2F 25 9 34 36% 76% 38% 74% 64% 64% 0.11 (0–0.4)
≥ Bosniak 3 8 5 13
Total 33 14 47
MRI Bosniak 2F 30 4 34 71% 91% 77% 88% 85% 29% 0.64 (0.39–0.88)
≥ Bosniak 3 3 10 13
Total 33 14 47
CEUS Benign 32 0 32 100% 97% 93% 100% 98% 0% 0.95 (0.85–1)
Malignant 1 14 15
Total 33 14 47

Sensitivity on the results of CEUS in the present study. CEUS might be

100%
80%
κ (Cohen) Specificity
60%
40%
20%
0%
1-missed
PPV
cancers
Accuracy NPV
Fig. 2 Radar chart of diagnostic performances of the different types of radi-
ological examinations.
MRI to assess or characterize the nature of cysts.13,14 How-
ever, these two examinations might not be completely help-
ful, because the phenomenon of partial volume is high, and
the contrast resolutions of CT and the spatial resolutions of
MRI are poor. Indeed, they are too limited for assessment of
small renal lesions, whereas the spatial resolution of US is
optimal for this category of lesion.15–17 Using contrast during
US enables enhancement of this examination. This method
requires intravenous injections of microbubbles, allowing
exclusive intravascular marking when detecting microbubbles
in cyst walls or septa. There is neither enhancement of the
urinary route nor accumulation in the renal parenchyma,
which eases exploration.15 CEUS is a valuable tool to iden-
tify contrast enhancement in the cysts septa or wall, or septal
or mural nodules. This is due to the high sensitivity of the
contrast-specific mode to the harmonic signals produced by
microbubbles, which probably makes CEUS even more effec-
tive than contrast material-enhanced CT and MR in the detec-
tion of contrast enhancement in cystic renal tumors.
However, some limitations inherent to the technique have to
be considered: back shadowing from calcification, bowel gas
interposition and US beam attenuation in cases of deep lesion
location can obscure contrast enhancement after microbubble
injection. Although we enrolled several obese patients, they
were too rare to assess the impact of a high body mass index
too sensitive, as it can detect only a few microbubbles travel-
ing in thin septa with a superior time and spatial resolution
compared with any other imaging modalities, leading to over-
classifying certain cases of benign cysts.
The findings in the present study were close to those
already reported in the literature, showing the high diagnostic
CT-scan performance of CEUS. Indeed, we found a sensitivity and
MRI specificity of 100% and 97%, respectively. These findings are
close to those reported by Bertolotto et al. in a study also
CEUS including 47 patients, and in which they used the same defi-
nition for the final diagnosis. Their two radiologists found a
sensitivity of 96.7% and 93.3%, respectively, and a speci-
ficity of 94.1%.8 Furthermore, Chen et al. in their study on
59 patients, reported a sensitivity of 97.2% and a specificity
of 71.4% using the same definition for the final diagnosis.9
Furthermore, similar to the present findings, Chen et al.
also reported a high rate of diagnostic accuracy (84.5%), a
low rate of undetected cancers (2.8%) and a high kappa coef-
ficient (0.7).9 The values we found were greater than those
already reported in the literature. These differences might be
explained by the operator-dependent variation of US even
though Bertolotto et al. reported a good match between the
results of their two operators (j = 0.7). Also, in the present
study, surgical treatment was guided mainly by MRI and US
examination, which could lead to a potential selection bias
among tumors with histological analysis.8 Finally, Barr et al.,
in a large retrospective study of 721 patients with indetermi-
nate renal mass on CT, found similar results to ours on
CEUS with 100% sensitivity, 95% specificity, 94.7% positive
predictive value and a 100% negative predictive value.16 That
study did not include only cystic tumors; however, Aoki
et al. reported similar results for both solid and cystic tumors
on CEUS.16,18
Recently, Graumann et al. reported different results in a
prospective study including 46 patients. Indeed they found
that CEUS and MRI results were both in agreement with CT
diagnosis with a high kappa score (0.86 and 0.91, respec-
tively), and they concluded that enhanced CT should remain
the gold standard for the Bosniak classification.19 However,
these discrepancies with the present results could be
explained by different methods. First, in their study, they
included a majority of Bosniak 2 (n = 27), which are less

4 © 2017 The Japanese Urological Association


(a)
(b)
Fig. 3 Sample of MRI and CEUS for one patient. (a) MRI showed a measur-
able enhancement of the wall of the cyst (Bosniak 3). (b) CEUS also found a
tissue element inside the cyst (arrow), not described on the MRI, making this
lesion probably malignant. A clear cell renal cell carcinoma, Fuhrman 2, was
found after surgery in this patient.
problematic for CT diagnosis than Bosniak 2F or 3 cysts,
representing just 19 cases, whereas we included only such
cysts. Furthermore, they chose the CT diagnosis as the stan-
dard for the CEUS and MRI accuracy assessment, and histo-
logical data were available for just six patients. In the present
study, we used the final diagnosis as previously described
using histological data, when available, or follow-up data.
This method provided an accuracy assessment independently
from the CT results, that could be more relevant.
MRI has already been reported to be more accurate than
CT for the evaluation of renal cysts.3 Indeed, applied to
MRI, the Bosniak classification leads to an increase in the
number of lesion categories detecting more septa, by thor-
oughly analyzing the thickness of the septa or walls and their
enhancement.3 The present study has also suggested the supe-
rior diagnostic performance of MRI compared with CT. Fur-
thermore, the diagnostic performance of MRI we found was
close to that reported by Chen et al.: sensitivity of 80.6%, a
specificity of 77.1%, a PPV of 78.4%, a NVP of 79.4% and
a kappa coefficient of 0.58.9 Thus, MRI is a more accurate
examination compared with CT, but nevertheless potentially
inferior to CEUS.3,16,20
Cystic tumors represent up to 10% of renal cell cancers.2
As far as a CT diagnosis is concerned, Bosniak category 2F
cysts are associated with malignant tumors in 5–20% of
cases, and with a high disparity between the series.6 For
© 2017 The Japanese Urological Association
Imaging assessment of complex renal cyst
Bosniak category 3, from 20% to more than 50% of malig-
nancies have been reported.4,6 In the present series, 26% of
Bosniak category 2F cysts and 39% of Bosniak category 3
cysts according to initial CT corresponded to malignant
tumors. These findings were close to those expected, even
though the rate of malignant tumors for category 2F lesions
was superior to that reported in the literature.
One of the main limitations of the present study was the
low number of patients included. However, the population
samples found in the literature for prospective studies on this
topic were also low. Despite exclusion of low-quality CT,
included examinations had heterogeneous slice thickness, up
to 2.5 mm, that could have affected the CT results. Further-
more, CEUS is operator dependent. In the present study, as
in other series, only an expert radiologist carried out these
examinations. The present findings are also representative of
the value of CEUS in expert hands, but not necessarily rele-
vant in daily practice. However, this point underlines the
need to refer such types of lesions to tertiary care referral
centers, which are used to carrying out these examinations.
This is indeed recommended in some guidelines.21 Finally,
our primary end-point, for 28 patients, was based on lesion
progression during imaging follow up, and in the absence of
histological evidence. This was less reliable than histology
diagnosis, and might also be limited because of the relatively
short follow up, which was less than the 5-year observation
period recommended for Bosniak 2F cysts.6,22
In conclusion, the present results suggested the diagnostic
performance of CEUS in improving the characterization of
complex renal cysts, which can be limited in some cases if
using only CT scan or MRI. CEUS appeared to be a relevant
examination to achieve accurate diagnosis and to optimize
treatment strategy of complex renal cysts.
Acknowledgments
The authors are grateful to Nikki Sabourin Gibbs for editing
the manuscript.
Conflict of interest
None declared.
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