Accuracy of contrast-enhanced ultrasound in the detection of bladder cancer.

Abstract

To assess the accuracy contrast-enhanced ultrasound (CEUS) in bladder cancer detection using transurethral biopsy in conventional cystoscopy as the reference standard and to determine whether CEUS improves the bladder cancer detection rate of baseline ultrasound.
43 patients with suspected bladder cancer underwent conventional cystoscopy with transurethral biopsy of the suspicious lesions. 64 bladder cancers were confirmed in 33 out of 43 patients. Baseline ultrasound and CEUS were performed the day before surgery and the accuracy of both techniques for bladder cancer detection and number of detected tumours were analysed and compared with the final diagnosis.
CEUS was significantly more accurate than ultrasound in determining presence or absence of bladder cancer: 88.37% vs 72.09%. Seven of eight uncertain baseline ultrasound results were correctly diagnosed using CEUS. CEUS sensitivity was also better than that of baseline ultrasound per number of tumours: 65.62% vs 60.93%. CEUS sensitivity for bladder cancer detection was very high for tumours larger than 5 mm (94.7%) but very low for tumours <5 mm (20%) and also had a very low negative predictive value (28.57%) in tumours <5 mm.
CEUS provided higher accuracy than baseline ultrasound for bladder cancer detection, being especially useful in non-conclusive baseline ultrasound studies.

Full text

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Accuracy of contrast-enhanced ultrasound in the detection of
bladder cancer
1C NICOLAU, MD,1L BUNESCH, MD,2L PERI, MD,1R SALVADOR, MD,2J M CORRAL, MD,3C MALLOFRE, MD
and1C SEBASTIA, MD
1Diagnostic Imaging Center, Hospital Clinic, University of Barcelona, Villarroel 170, 08036 Barcelona, Spain and
Departments of2Urology3Pathology, Hospital Clinic, University of Barcelona, Villarroel 170, 08036 Barcelona, Spain
ABSTRACT. Objective: To assess the accuracy of contrast-enhanced ultrasound (CEUS) in
bladder cancer detection using transurethral biopsy in conventional cystoscopy as the
reference standard and to determine whether CEUS improves the bladder cancer
detection rate of baseline US. Methods: 43 patients with suspicion of bladder cancer
underwent conventional cystoscopy with transurethral biopsy of the suspicious lesions.
64 bladder cancers were confirmed in 33 out of 43 patients. Baseline US and CEUS were
performed the day before surgery and the accuracy of both techniques for bladder
cancer detection and for number of detected tumours were analysed and compared
with the final diagnosis. Results: CEUS accuracy was significantly better than US
accuracy in terms of presence or absence of bladder cancer: 88.37% vs 72.09%. Seven of
eight uncertain baseline US results were correctly diagnosed using CEUS. CEUS
sensitivity was also better than that of baseline US per number of tumours: 65.62% vs
60.93%. CEUS sensitivity for bladder cancer detection was very high for tumours larger
than 5 mm (94.7%) but very low for tumours ,5 mm (20%) and also had a very low
negative predictive value (28.57%) in tumours ,5 mm. Conclusion: CEUS provided
higher accuracy than baseline US for bladder cancer detection, being especially useful
in non-conclusive baseline US studies.
Received 22 September
2009
Revised 21 March 2009
Accepted 13 April 2010
DOI: 10.1259/bjr/43400531
’ 2011 The British Institute of
Radiology
Carcinoma of the urinary bladder is the most common
malignancy of the urinary tract that must be ruled out in
patients with haematuria with negative upper urinary
tract findings [1]. Cystoscopy remains the most sensitive
method of detecting bladder cancer, but has several
limitations: it is an invasive procedure; it is uncomfor-
table in some patients and requires sedation or anaes-
thesia. Conventional ultrasound (US) is one of the
imaging techniques used to screen for bladder cancer,
but with variable accuracy. The best results are obtained
using the latest equipment and new imaging tools such
as three-dimensional (3D) US [2–5]. Angiogenesis is
essential to allow growth of malignancies, and the
detection of the tumoural neovascularisation is one of
the keys of imaging modalities to achieve a definite
diagnosis. CT and MRI are accurate techniques for
bladder cancer detection when they are performed with
the injection of intravascular contrast agents. Detection
relies on the identification of bladder cancer neovascu-
larisation and recent studies have shown high accuracy
with both techniques [6, 7]. The introduction of micro-
bubble contrast agents and the development of contrast-
specific software have increased the value of US in the
field of oncology [8, 9]. US contrast agents are strictly
intravascular and are very sensitive in revealing tumour
microvascularisation, helping in the detection and
characterisation of malignancies [10–13]. Recently, the
behaviour of bladder cancer has been described after the
administration of US contrast agent, and its diagnosis
relies on the detection of hypervascular wall bladder
thickening [14].
The aim of our study was to retrospectively assess the
value of contrast-enhanced US (CEUS) in bladder cancer
detection in a selected high-risk group of patients using
transurethral biopsy in conventional cystoscopy as the
reference standard and to determine whether CEUS
improves the bladder cancer detection rate of baseline
US.
Methods
Patients
The study was approved by the Ethical Committee of
our institution, and informed consent was obtained from
all the subjects who participated in the study. From
September 2007 to April 2008 about 160 patients with
bladder tumours were diagnosed in our hospital. From
these patients with bladder tumours we selected a sub-
group referred to the operating theatre of the Department
of Urology for conventional cystoscopy under general
anaesthesia. The selection of this subgroup was at random
since it depended only on the availability of the
radiologists of the Radiology Department to perform the
US study on the day prior to the surgical procedure. Thus,
43 non-consecutive patients (ranging in age from 29 to
89 years (mean age 71.4 ¡ 12.5 years) were included in
Address correspondence to: C Nicolau, Diagnosis Imaging Center,
Hospital Clinic, Villarroel 170, 08036 Barcelona, Spain. E-mail:
cnicolau@clinic.ub.es
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The British Institute of Radiology, doi: 10.1259/bjr/43400531
Published online before print December 1, 2010

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this study. Flexible cystoscopy was indicated because of
the presence of macroscopic haematuria (25 cases, 58.1%),
surveillance after transurethral resection (14 cases, 32.6%)
andincidentalsonographic findings (4 cases, 9.3%).When
cystoscopically suspicious lesions were detected, transur-
ethral biopsies were performed and the final diagnoses
were obtained by histology.
All patients underwent a blind baseline US and CEUS
the day before surgery. The urologists who performed
the cystoscopy did not know the results of the previous
US studies.
Imaging techniques
All US studies were performed by one of the
radiologists of the urogenital department with at least
8 years of experience in US using Sequoia 512 equipment
(Siemens Sequoia Mountain View, CA). First of all, a
baseline US of the total bladder in fundamental mode,
using greyscale, was performed with a multifrequency
4C1 convex array probe in order to identify bladder wall
thickening or bladder lesions. Patients were instructed
not to void for at least 1 h before the US study and were
not scanned until they had the sensation of a full bladder
in order to ensure good bladder distension. After the
baseline study, a dynamic CEUS of the whole bladder
was performed using the specific contrast software
Cadence contrast pulse sequencing technology (CPS),
which allows real time evaluation of contrast agents with
minimum bubble destruction at low MI power levels.
CPS was performed with the same convex array probe,
with a double focus in the area of interest, using the
following settings: insonating frequency, 3 MHz; acous-
tic power, 275 to 290 dB; frame rate, 17–20. A low
mechanical index (,0.2) was used in order to avoid
microbubble disruption. CEUS studies were performed
after the administration of 2.4 ml of Sonovue as a bolus
using a 21 gauge peripheral intravenous cannula, fol-
lowed by a 5 ml saline flush.
Bladder wall enhancement was studied up to 3 min.
Images and cine-loops of baseline, arterial and venous
phases were selected and stored on digital cine-loops by
the same radiologists who performed the US studies for
the off-line analysis after changing the name of patients
using a correlative code.
Imaging analysis
Two radiologists, each with at least 5 years of experi-
ence in interpreting CEUS studies, independently inter-
preted the acquired images and cine-loops of the bladder
off-line at least 3 weeks after the recruitment of patients.
Both radiologists were blinded to the final diagnosis, but
they knew that all patients were referred to cystoscopy
because of a diagnosis of bladder cancer by flexible
cystoscopy. All bladders were reviewed before and after
contrast agent injection. Reviewers were asked to identify,
record the presence, number, size and classify the location
of bladder tumours using the same classification of five
segments used by the urologists on cystoscopy in our
centre (right lateral wall, left lateral wall, anterior wall–
domus, fundus, posterior wall–floor). US diagnoses of all
discrepant studies were established by consensus. In the
baseline study, bladder cancer was defined as the
presence of focal bladder wall thickening or the presence
of focal masses protruding into the bladder lumen. From
the CEUS study, bladder cancer was defined as the
presence of focal hyperenhanced wall thickening or
enhancing masses that protrude into the bladder lumen.
A three-point scale was used for lesion detection using
baseline US and CEUS (1, absence of tumour; 2, presence
of bladder cancer; 3, results uncertain). The results of
baseline US and CEUS were compared with the findings
of conventional cystoscopy and biopsy, which were
considered the reference standard.
Statistical analysis
The SPSS programme (version 14.0) was used for
statistical analysis. Baseline characteristics of the patients
and bladder tumours are expressed as mean ¡ SE. The
relationship between the classification of cancer or
absence of cancer at baseline, CEUS and the final
diagnosis was analysed with the Fisher exact test. The
overall sensitivity, specificity, accuracy, positive predic-
tive value and negative predictive value for bladder
cancer detection using US and CEUS were analysed by
number of patients and number of lesions. For the
estimation of sensitivity uncertain results were classified
as negative for cancer. For the estimation of specificity
uncertain results were classified as positive for cancer. A
value of p , 0.05 was considered statistically significant.
Results
43 non-consecutive patients (36 men, 7 women) ran-
ging in age from 29 to 89 years (mean age 71.4 ¡
12.5 years) sent to the operating theatre to undergo
cystoscopy because of the suspicion of bladder cancer
were finally included in the study. Reference standard
tests (cystoscopy and biopsy) revealed 64 bladder cancers
in 33 out of 43 patients. All cancers except one were
transitional cell carcinomas. The other was an undiffer-
entiated carcinoma. Of the 10 patients without bladder
cancer, absence of bladder disease was confirmed by
cystoscopy and biopsies in 7 patients. Biopsy of the other
three patients showed chronic inflammatory bladder wall
changes (two cases) and a papillary hyperplasia (one
case). Of the 33 patients with bladder cancer, the number
of lesions in each bladder detected by conventional
cystoscopy was 1 in 22 patients, and multifocal in
11 patients (range 2–7 lesions), with a total of 64 bladder
lesions. The size of the bladder cancer lesions ranged from
0.3 to 7 cm, with a mean size of 1.34 ¡ 0.35 cm (1 tumour
was not measured because of diffuse occupation of the
bladder). 39 tumours were larger than 5 mm and the
other 25 were #5 mm.
US/CEUS tumour detection
All US/CEUS studies were technically good and
considered suitable for diagnosis. Only one dose of
contrast agent was necessary in all patients. Figures 1
C Nicolau, L Bunesch, L Peri et al
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and 2 summarise the results in the format of a Standards
for Reporting of Diagnostic Accuracy (STARD) flow
diagram [15]. Baseline US and CEUS were able to detect
tumours from 5 mm in size (Figure 3). Following the
established criteria, baseline US suspicion was absence
of tumour 7 patients, presence of bladder cancer 28
patients, results uncertain 8 patients. Causes of uncertain
US results were presence of bladder clots that could not
be differentiated from bladder cancer two cases; doubtful
irregularity of the bladder wall without polypoid mass
six cases (Figure 4). The final diagnosis of uncertain
cases was absence of cancer in five patients (included as
Figure 1. Flow diagram of baseline ultrasound based on Standards for Reporting of Diagnostic Accuracy. Two parameters
(presence or absence of bladder cancer and presence or absence with respect the total number of bladder cancers (in
parentheses) were evaluated in all patients.
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US false positives in our analysis) and presence of cancer
in three patients (included as false negatives in our
analysis). CEUS suspicion was absence of tumour
11 patients, presence of bladder cancer 32 patients,
uncertain results 0 patients. All bladder cancers identi-
fied on baseline US were also identified with CEUS.
The accuracy of baseline US in bladder cancer detection
per patient was 72.09% (31/43 patients) with a sensitiv-
ity of 81.81% (27/33), specificity of 40% (4/10), positive
predictive value of 81.81% (27/33) and a negative
predictive value of 40% (4/10) (Figure 1). In contrast,
the accuracy of CEUS to detect bladder cancer per
Figure 2. Flow diagram of contrast-enhanced ultrasound based on Standards for Reporting of Diagnostic Accuracy. Two
parameters (presence or absence of bladder cancer and presence or absence with respect to the total number of bladder cancers
(in parentheses) were evaluated in all patients.
C Nicolau, L Bunesch, L Peri et al
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(a)(b)
(c)
(e)
(d)
Figure 3. 62-year-old man with bladder cancer. (a) Greyscale baseline ultasound (US) of the bladder showed a 1 cm polypoid
mass on the left posterior wall of the bladder. (b) contrast-enhanced (CE) US at 22 s showed early enhancement of the polypoid
lesion (arrow). Enhancement of the normal wall bladder (cap arrows) is almost imperceptible in the early arterial phase. (c) CEUS
at 40 s showed homogeneous enhancement of the polypoid lesion (arrow). Enhancement of the normal wall bladder (cap
arrows) is very tiny throughout the arterial and venous phases (Figure 1d) and cannot be differentiated from the
microvascularisation of the perivesical tissue. (d) CEUS at 120 s showed faint enhancement of the polypoid lesion.
Enhancement of the bladder wall is also faint at this time. (e) Cystoscopy confirmed the existence of a bladder wall tumour.
Diagnosis by biopsy (not shown) was urothelial bladder cancer.
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patient significantly increased to 88.37% (38/43 pa-
tients), with a sensitivity of 90.9% (30/33), specificity of
80% (8/10), positive predictive value of 93.75% (30/32)
and a negative predictive value of 72.72% (8/11)
(Figures 2 and 5). All bladder cancers identified on
baseline US were identified with CEUS. Furthermore,
CEUS was able to rule out the presence or absence of
bladder cancer in 87.5% (7/8) of uncertain baseline US
cases, with the detection of 3 bladder cancers not
correctly identified on baseline US. On analysing the
accuracy of the technique according to the number of
bladder cancers detected, the accuracy of baseline US
was 58.1% (43/74) with a sensitivity of 60.93% (39/64),
specificity of 40% (4/10), positive predictive value of
86.6% (39/45) and a negative predictive value of 13.79%
(4/29) (Figure 1). In contrast, the accuracy of CEUS
according to the number of bladder cancers increased to
67.56% (50/74) with a sensitivity of 65.62% (42/64),
specificity of 80% (8/10), positive predictive value of
95.45% (42/44) and a negative predictive value of 26.66%
(8/30) (Figure 2).
There were only two false positive CEUS findings
for bladder cancer. The first was a patient with a growth
of the prostate mimicking a bladder tumour and the
other was a papillary hyperplasia considered to be a
precursor lesion of bladder neoplasm by the World
Health Organization and the International Society of
Urological Pathologists [16], that was indistinguishable
from bladder cancer by both CEUS and conventional
cystoscopy. The false negative CEUS findings for bladder
cancer were 22 bladder cancers detected on cystoscopy.
20 of these 22 were ,5 mm and were located at the left
lateral wall (n53), right lateral wall (n53), domus–
anterior wall (n53), fundus (n55), or posterior bladder
wall–floor (n57), two of them at the bladder neck. Only 2
sessile tumours larger than 5 mm (a 15 mm tumour at
(a)(b)
(c)
Figure 4. 69-year-old man with suspicion of bladder cancer. (a) Baseline ultrasound (US) showed irregularity of the right
bladder wall that was suggestive but not conclusive of bladder cancer and classified as uncertain. (b) Contrast-enhanced (CE) US
at 42 s showed homogeneous enhancement of the bladder wall without focal masses, suggesting the absence of a bladder
tumour. (c) CEUS at 135 s did not show focal enhancing masses. Cystoscopy and bladder wall biopsies confirmed the absence of
bladder tumour.
C Nicolau, L Bunesch, L Peri et al
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the bladder fundus and a 10 mm tumour at the left
lateral wall) were missed. Therefore, CEUS sensitivity
for bladder cancer detection was significantly better
for tumours larger than 5 mm, with a very low sensiti-
vity for bladder cancer #5 mm of 20% (5/25) and
negative predictive value of 28.57% (8/28), which rose
to a sensitivity of 94.87% (37/39) and negative predictive
valueof 80% (8/10)for
(Figure 6).
bladdercancer
.5 mm
Discussion
This study demonstrates the high bladder cancer
detection rate of CEUS, with a very high sensitivity for
the presence of bladder cancer per patient (90.9%).
Tumoural neovascularisation can be evaluated using
imaging modalities after the administration of contrast
agents and bladder cancer is a hypervascular tumour
that shows strong enhancement in the arterial phase,
followed by a plateau of enhancement and a slow
washout when evaluated with imaging modalities after
the administration of contrast agents [14, 17–19]. Despite
conventional US currently being the preferred non-
invasive imaging technique for the screening of bladder
cancers, its accuracy depends on several factors, includ-
ing distension of the bladder, tumour size, morphology
and location of the lesions [2]. The main limitation of US
is its low sensitivity in detecting lesions smaller than
1 cm [3, 20] occurred in the present study with CEUS
sensitivity for the number of detected bladder cancers
being 65.5%, which may be explained by the high
number of tumours #5 mm detected by cystoscopy
(n525). These very small tumours are usually flat and do
not produce focal bladder wall thickening or abnormal
enhancement due to the absence of considerable neo-
vascularisation, as has been hypothesised in studies
using other imaging techniques [20]. Our results are
slightly worse than those obtained using CT or MRI with
contrast agents [18, 21–23], or using MDCT urography
(a)(b)
(c) (d)
Figure 5. 74-year-old man with bladder cancer. (a) Axial and (b) saggital images of baseline ultrasound (US) that did not detect
bladder wall abnormalities. (c) Contrast-enhanced (CE) US at 90 s showed a homogeneous enhancing mass of 5 mm of the left
bladder wall (arrow). (d) Persistent enhancement of the small tumour was detected at 140 s (arrow). Urothelial bladder cancer
was confirmed by cystoscopy and resection.
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[24–26]. In the study by Kim et al [18], using MDCT the
detection rate was 97% for all bladder cancers and 85%
for bladder cancers smaller than 1 cm. However, all their
cancers were invasive and only 13 out of 77 were smaller
than 1 cm. In a more recent study using dynamic
contrast-enhanced MDCT with multiplanar reconstruc-
tions, Jinzaki et al [22] obtained an overall sensitivity of
90% and a sensitivity of 25% for bladder lesions 5 mm or
smaller when using 5 mm axial sections as the recon-
struction protocol or a sensitivity of 58% using 2.5 mm
axial sections with a 1.25 mm overlap. With the use of
MDCT urography Turney et al [25] and Sadow et al [26]
found a sensitivity of 93% and 79% respectively in
detecting bladder cancer but with a high number of
equivocal (20% in the study by Turney) or misinter-
preted (9% in the study by Sadow) studies.
With respect to location, we missed lesions from all
segments but especially on the bladder floor and fundus.
In the literature, there is no agreement regarding the
most difficult places to detect bladder cancers using US:
anterior and posterior bladder wall [3]; bladder neck or
dome areas [20], anterior wall [27]. Detection of small
tumours in the bladder floor can be a challenge in male
patients with benign prostatic hyperplasia (BPH) [28–30].
A large prostatic central gland protruding into the
bladder lumen can be difficult to differentiate from
bladder cancer. In our experience, bladder tumours
enhance faster than the normal prostate gland due to
its arterial neovascularisation, but intense enhancement
in areas of benign prostatic hyperplasia can be found
using CEUS, mimicking tumoural enhancement [31].
Another difficulty when evaluating patients with BPH is
the possibility of bladder wall thickening with trabecula-
tions, which in some cases may mimic urothelial cancers.
When compared with baseline US, in our study CEUS
did not significantly improve the sensitivity in detecting
more bladder cancers, detecting only three lesions more.
However, CEUS significantly increased the accuracy of
baseline US according to the presence or absence of
bladder tumour, especially in uncertain baseline US
cases. In clinical practice, several reasons such as the
presence of bladder clots, surgical wall changes, bladder
wall trabeculation or the impossibility to retain urine to
totally distend the bladder may hamper good visualisa-
tion of the bladder using baseline US. In our experience,
CEUS is helpful in differentiating these entities from
bladder cancer, detecting bladder cancer neovascularisa-
tion enhancement [14].
One limitation of this study is the recruitment of
patients with high suspicion of bladder cancer obtained
by flexible cystoscopy who were to undergo rigid
cystoscopy, and the absence of inclusion of healthy
patients. However, radiologists who carried out the US
and CEUS studies and who reviewed the US and CEUS
images did not know the cystoscopic and histological
results. With the introduction of this recruitment bias,
the real value of CEUS as a screening for bladder cancer
in patients with haematuria cannot be provided.
In conclusion, CEUS improves the bladder cancer
detection rate of US, especially in US studies that are
non-conclusive.
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