Eur Radiol (2014) 24:889–901
DOI 10.1007/s00330-013-3083-8
UROGENITAL
Whole-body MRI with diffusion-weighted sequence for staging
of patients with suspected ovarian cancer: a clinical feasibility
study in comparison to CTand FDG-PET/CT
Katrijn Michielsen & Ignace Vergote & Katya Op de beeck & Frederic Amant &
Karin Leunen & Philippe Moerman & Christophe Deroose & Geert Souverijns &
Steven Dymarkowski & Frederik De Keyzer & Vincent Vandecaveye
Received: 8 August 2013 / Revised: 13 November 2013 / Accepted: 14 November 2013 / Published online: 11 December 2013
# European Society of Radiology 2013
Abstract
Objectives To evaluate whole-body MRI with diffusion-
weighted sequence (WB-DWI/MRI) for staging and assessing
operability compared with CT and FDG-PET/CT in patients
with suspected ovarian cancer.
Methods Thirty-two patients underwent 3-T WB-DWI/MRI,
18
F-fluorodeoxyglucose positron emission tomography/
computed tomography (FDG-PET/CT) and CT before diag-
nostic open laparoscopy (DOL). Imaging findings for tumour
characterisation, peritoneal and retroperitoneal staging were
Electronic supplementary material The online version of this article
(doi:10.1007/s00330-013-3083-8) contains supplementary material, which
is available to authorized users.
K. Michielsen : K. Op de beeck : S. Dymarkowski : F. De Keyzer :
V. Vandecaveye (*)
Department of Radiology, Medical Imaging Research Centre,
University Hospitals Leuven, Herestraat 49, 3000 Leuven, Belgium
e-mail: vincent.vandecaveye@uzleuven.be
I. Vergote : F. Amant : K. Leunen
Department of Obstetrics and Gynaecology, Leuven Cancer Institute,
University Hospitals Leuven, Herestraat 49, 3000 Leuven, Belgium
P. Moerman
Department of Morphology and Molecular Pathology, University
Hospitals Leuven, Herestraat 49, 3000 Leuven, Belgium
C. Deroose
Department of Nuclear Medicine, Medical Imaging Research Centre,
University Hospitals Leuven, Herestraat 49, 3000 Leuven, Belgium
G. Souverijns
Department of Radiology, Jessa Ziekenhuis – Campus Virga Jessa,
Stadsomvaart 11, 3500 Hasselt, Belgium
correlated with histopathology after DOL and/or open surgery.
For distant metastases, FDG-PET/CT or image-guided biop-
sies were the reference standards. For tumour characterisation
and peritoneal staging, WB-DWI/MRI was compared with
CT and FDG-PET/CT. Interobserver agreement for WB-
DWI/MRI was determined.
Results WB-DWI/MRI showed 94 % accuracy for primary
tumour characterisation compared with 88 % for CT and 94 %
for FDG-PET/CT. WB-DWI/MRI showed higher accuracy of
91 % for peritoneal staging compared with CT (75 %) and FDG-
PET/CT (71 %). WB-DWI/MRI and FDG-PET/CT showed
higher accuracy of 87 % for detecting retroperitoneal lymphade-
nopathies compared with CT (71 %). WB-DWI/MRI showed
excellent correlation with FDG-PET/CT (κ=1.00) for detecting
distant metastases compared with CT (κ=0.34). Interobserver
agreement was moderate to almost perfect (κ=0.58–0.91).
Conclusions WB-DWI/MRI shows high accuracy for
characterising primary tumours, peritoneal and distant staging
compared with CT and FDG-PET/CT and may be valuable for
assessing operability in ovarian cancer patients.
Key Points
• Whole-body MRI with diffusion weighting (WB-DWI/MRI)
helps to assess the operability of suspected ovarian cancer.
• Interobserver agreement is good for primary tumour char-
acterisation, peritoneal and distant staging.
• WB -DWI /MRI improves mesenteric /serosal metastatic
spread assessment compared with CTand FDG-PET/CT.
• Retroperitoneal/cervical-thoracic nodal staging using qual-
itative DWI criteria was reasonably accurate.
• WB-DWI/MRI and FDG -PET /CTshowed the highest diag-
nostic impact for detecting thoracic metastases.
890
Keywords Diffusion-weighted MRI . Whole-body imaging .
Ovarian cancer . Tumour staging . Gynaecologic surgical
procedures
Abbreviations and acronyms
WB-DWI/MRI whole-body MRI with diffusion-weighted
sequence
DOL diagnostic open laparoscopy
PC peritoneal carcinomatosis
FIGO International Federation of Gynaecology
and Obstetrics
NACT neoadjuvant chemotherapy
CA cancer antigen
MPR multiplanar reformatting
TSE turbo spin-echo
SI signal intensity
PPV positive predictive value
NPV negative predictive value
Introduction
Ovarian cancer is often diagnosed with extensive peritoneal
and/or distant metastases [International Federation of
Gynaecology and Obstetrics (FIGO) stages IIIc and IV], de-
creasing the patient’s survival rate to 20–40 % in FIGO stage
IIIc disease and to 10 % in FIGO stage IV [1].
Complete macroscopic tumour resection (R0 resection) has
been demonstrated to be the single most important prognostic
factor [2–9]. If disease extent precludes upfront radical
debulking surgery, neoadjuvant chemotherapy (NACT)
followed by interval debulking, represents a valid alternative
in patients with advanced stage IIIc or IV ovarian cancer [2].
Imaging aims to identify patients unfit for surgery, either by
diagnosing a primary tumour other than ovarian cancer, or by
depicting disease volume and/or extent beyond the reach of
surgery [10, 11]. Although 18 F-fluorodeoxyglucose positron
emission tomography/computed tomography (FDG-PET/CT)
surpasses CT in the detection of lymphadenopathies and dis-
tant metastases, both may underestimate peritoneal and par-
ticularly mesenteric and serosal bowel disease extent, neces-
sitating surgical staging to assess operability [12–17].
Conversely, the combination of contrast-enhanced magnetic
resonance imaging (MRI) with diffusion-weighted imaging
(DWI) has shown high accuracy for staging of peritoneal
carcinomatosis (PC) [18, 19]. Because at least 11 % of patients
have distant metastases, including cervical-thoracic metasta-
ses, the development of whole-body MRI with diffusion-
weighted sequence (WB-DWI/MRI) over abdominal DWI/
MRI may be justified [20].
Eur Radiol (2014) 24:889–901
The aim of this study was to evaluate the diagnostic value
of WB-DWI/MRI for staging and assessing operability com-
pared with CT and FDG-PET/CT in patients with suspected
ovarian cancer.
Materials and methods
Patients and selection of treatment
Approval was obtained from the local Institutional Review
Board and all patients provided written informed consent.
The inclusion criterion for the study was suspicion of
ovarian cancer based on gynaecological ultrasound or CA-
125. Patients with contraindications to MRI were excluded.
Thirty-two women (mean age 61.9, range 20–83 years) were
consecutively enrolled in this prospective study between
October 2010 and February 2012. Routine diagnostic workup
included clinical and CA-125 assessment, gynaecological ul-
trasound by an expert sonographer, thoraco-abdominal CT
and diagnostic open laparoscopy (DOL) [21]. Additionally,
all patients underwent WB-DWI/MRI and FDG-PET/CT be-
fore DOL.
The decision to treat by primary debulking surgery, or by
NACT with interval debulking, was determined according to
well-defined criteria [22]. In short, the main criteria precluding
upfront debulking surgery consisted of medical comorbidities
preventing major surgery and disease-related factors:
(1) Distant metastases, except for resectable inguinal lymph
nodes, solitary resectable retrocrural or paracardiac
lymph nodes, and pleural fluid with cytological proof
of tumour but without detectable macroscopic tumour
deposits on imaging;
(2) The presence of hepatic metastases;
(3) Tumoral infiltration of the duodenum, stomach, pancre-
as, large vessels of the coeliac trunk and hepatoduodenal
ligament, and metastases behind the portal vein;
(4) Diffuse serosal carcinomatosis necessitating multiple in-
testinal resections;
(5) Deep tumoral involvement of the superior mesenteric
artery and mesenteric root of the small bowel.
Imaging techniques
Computed tomography
Breath-hold contrast-enhanced [intravenous injection of
120 ml iodinated contrast agent (Visipaque, GE Healthcare);
320 mg/ml; chest after 17 s, abdomen after 90 s] CT
(Sensation 16, Sensation 64, Definition Flash, Siemens
Medical Systems, Erlangen, Germany) was obtained 90 min
Eur Radiol (2014) 24:889–901 891

DWI, diffusion-weighted imaging; mDIXON, multi-echo 2-point Dixon; eTHRIVE, T1-weighted high-resolution isotropic volume examination; SSTSE, single-shot turbo spin-echo imaging; STIR, short
SPAIR (eTHRIVE)
after per-oral contrast ingestion [30 ml iodinated contrast
agent (Telebrix Gastro, Guerbet), 300 mg/ml, in 900 ml water]

Transverse

0.98×0.97
375×304
1.49×1.5
Chest (1)
using the following parameters: pitch 1.2, rotation speed 0.5 s,

None

148
1.5
3.2
1.5
slice thickness 5 mm, slice gap 1 mm and collimation 0.6 mm.

1
The reference tube voltage was set at 120 kV, and the refer-
ence current was 110 mAs for the thorax and 200 mAs for the
abdomen using automated Care Dose software.

Abdominopelvic (2)

SPAIR (mDIXON)

1.25 – 2.20
FDG-PET(/CT)

0.71×0.71
Contrast-enhanced 3D T1 gradient-echo

400×352
1.49×1.5
Coronal

None

133
1.5
3.6
Hybrid FDG-PET/CT (Biograph 40 TruePoint with TrueV,

1
Siemens Medical Solutions, Erlangen, Germany) was performed
for 25/32 patients, whereas stand-alone FDG-PET (HR+,
Siemens, Knoxville, TN, USA) was performed for 7/32 patients.

Abdominopelvic (2)

SPAIR (mDIXON)
20 s breath-hold
Patients fasted for 6 h before the examination. For FDG-PET/

Transverse

1.25 – 2.20

0.71×0.71
CT, whole-body, free-breathing spiral CT was performed first

375×304
1.49×1.5
(85 mAs, 120 kV, slice thickness 5 mm, collimation 24×1.2 mm,

None

1.5
3.6

90
2

1
table feed 23 mm/rotation), with per-oral and intravenous iodin-
ated contrast agent. PET images were acquired (mean 69 min,
range 53– 99 min) after intravenous administration of a weight-

Respiratory
adjusted amount of FDG (average activity of 303 MBq, range

0.93×0.93
35/station

375×447
Coronal
220–388). PET images were corrected for attenuation using the

3,000
None
None

1×1
0.6
87
6
3

1
CT data. Because of constraints on imaging time, no attenuation
correction was performed for the PET-only acquisitions. All PET
images were iteratively reconstructed.
Transverse

Respiratory
T2 SSTSE

0.78×0.78
41/station

357×339
WB-DWI/MRI

3,000
None
None

1×1
0.6
87
6
4

1
Patients drank 1 l of pineapple juice 2 h before the MRI to
distend the bowel lumen and suppress the signal from bowel
contents because of the negative contrast properties resulting
Sagittal

MPR

from its manganese content [23, 24]. In addition, an antispas-

5

modic agent (butylhyoscine, 20 mg IV) was administered at

the start of abdominal DWI. Three-Tesla WB-DWI/MRI
(Ingenia, Philips Healthcare, Best, The Netherlands) was per-

T1 inversion recovery; SPAIR, spectrally adiabatic inversion recovery

Coronal

formed with parallel radiofrequency transmission and phased-

MPR

array head-neck and surface coils. Free-breathing WB-DWI

5

was acquired at four imaging stations, covering the head and

neck, chest, upper abdomen and pelvis. Multiplanar
reformatted (MPR) coronal and sagittal WB-DWI images
STIR (TI=250 ms)
Table 1 Sequence parameters for WB-DWI/MRI

were reconstructed from the transverse b1000 images. WB

Free-breathing
Transverse

4.57×4.71
2.19×2.16

transverse and coronal respiratory triggered T2-weighted tur-

50/station

420×329
0-1,000

8,454
DWI

bo spin-echo (TSE) and breath-hold abdominal-pelvic and

0.1
2.5

67
5

1
4

thoracic contrast-enhanced 3D T1-weighted gradient-echo se-

quences obtained 80 s after injection of 15 ml gadolinium-
DOTA were used for anatomical reference. The total imaging
Number of signal averages (NSA)
Image stations head to mid-thigh

time was 40 min. A detailed overview of the imaging protocol

Reconstructed voxel size (mm)

is shown in Table 1.
Field of view (FOV) (mm)
Acquired voxel size (mm)
Repetition time (TR) (ms)
Parallel imaging factor

Intersection gap (mm)

Slice thickness (mm)
Echo time (TE) (ms)

Interpretation of imaging
b-Values (s/mm2)
Fat suppression

Slice number
Respiration

CT, WB-DWI/MRI and FDG-PET/CT were separately eval-

uated, by two abdominal radiologists (12 and 10 years of
892
experience, respectively) and a nuclear medicine physician
(11 years of experience). Observers were blinded to all infor-
mation regarding the other imaging tests, clinical, laboratory
and pathological findings. The interpretation criteria are
outlined in Table 2 following the previously published imag-
ing criteria [10, 25–29].
WB-DWI/MRI: interobserver agreement
Interobserver variability between an academic and a non-
academic radiologist was assessed. Of the 32 cases, 8 were
randomly selected for 1-week training of the second reader.
Subsequently, the WB-DWI/MRI findings for the remaining
24 cases were interpreted by the non-academic reader, who
was blinded to the results of the academic radiologist.
Reference standard
Primary tumours and peritoneal and hepatic-hilar metastases
were primarily confirmed during DOL and/or surgery with
histopathology whenever possible. Retroperitoneal lymph-
adenopathies were primarily confirmed by histopathology
after surgery. For distant metastases, FDG-PET/CT was used
as reference standard if biopsy was technically impossible.
Endobronchial ultrasound-guided fine-needle aspiration of a
mediastinal lymphadenopathy was performed for three pa-
tients and cytology was performed after pleural drainage in
one patient.
In the case of NACT, the findings at interval debulking and
histopathology were used for additional correlation with the
initial DOL. To facilitate this correlation, lesions recorded at
preoperative imaging were topographically correlated and
annotated at imaging follow-up before interval debulking.
Primary tumours were classified as benign, primary ovar-
ian (borderline-malignant) or non-ovarian in origin. The ex-
tent of PC was classified as follows: the bladder peritoneal
surface, Douglas pouch, peritoneal left and right pelvic,
lateroconal area and diaphragm, subhepatic space/Morrison’s
pouch, hepatic surface, splenic surface, omentum, small bow-
el, and colonic mesentery and serosa. Retroperitoneal nodal
extent was classified as infrarenal (aorto-caval, right and left
iliac) and suprarenal. Hepatic-hilar metastases encompassed
the portal vein, gallbladder and falciform ligament.
The extent of abdominal disease at imaging, surgery and
histopathology was assessed following higher mentioned clas-
sification (Fig. 1). Accordingly, resection specimens were
labelled before fixation, and histopathological findings were
reported. When surgical and pathological findings were dis-
cordant, pathological findings prevailed. The size distribution
of metastatic lesions was recorded at surgical evaluation by
measuring the largest lesion per region or by correlative
anatomical imaging.
Eur Radiol (2014) 24:889–901
Statistical Analysis
Statistica 9.1 software (Statsoft Inc., Tulsa, OK, USA) was
used for all statistical analyses, with P <0.05 indicating statis-
tical significance. The sensitivity, specificity, accuracy, and
positive (PPV) and negative predictive values (NPV) of the
imaging techniques were determined for primary tumour char-
acterisation, detection of PC and retroperitoneal lymphade-
nopathy. Statistical differences in sensitivity between WB-
DWI/MRI and CT and between WB-DWI/MRI and FDG-
PET/CT were calculated using two-tailed McNemar tests. In
order to exclude bias in the FDG-PET results, potential differ-
ences in accuracy between hybrid FDG-PET/CT and stand-
alone PET with CT correlation were statistically assessed
using McNemar’s test with Bonferroni correction. The accu-
racy of WB-DWI/MRI, CT and FDG-PET/CT for detecting
distant metastases was compared using Cohen’s kappa statis-
tic. The accuracy of all imaging techniques for FIGO staging
was determined in correlation with the definitive stage deter-
mined by the clinician who had access to all clinical, surgical
and imaging information. Statistical differences among the
three imaging techniques were evaluated using McNemar’s
statistics. Finally, interobserver agreement was assessed by
site-by-site comparison of all anatomical regions using
Cohen’s kappa statistic, as described in the standardised scor-
ing template.
Results
Patients
Definitive clinical diagnosis, pathological characteristics and
type of therapy are provided in Table 3. Peritoneal carcino-
matosis was confirmed in 208 peritoneal regions (44 %, 208/
475) in 32 patients: the bladder surface was involved in 17
patients, the Douglas pouch in 19, right pelvic and lateroconal
surfaces in 20 and 15 patients, respectively, and left pelvic and
lateroconal surfaces in 21 and 16 patients, respectively. The
peritoneal subhepatic/Morrison’s space was involved in ten
patients, whereas the hepatic capsule was infiltrated in four
patients. The right and left diaphragm was involved in 12 and
nine patients, respectively, and one patient showed involve-
ment of the splenic capsule. Omental involvement was con-
firmed in 23 patients, and small bowel serosal and mesenteric
involvement was observed in 6 and 12 patients, respectively.
Colonic serosal and mesenteric metastases were identified in
11 and 12 patients, respectively. The PC was smaller than
1 cm in 75 peritoneal regions (36 %, 75/208) and larger than
1 cm in 60 regions (29 %, 60/208), and 73 regions showed
confluent disease (35 %, 73/208).
Infrarenal retroperitoneal malignant lymphadenopathy was
confirmed in ten patients, suprarenal retroperitoneal
Table 2 Interpretation of imaging for CT, FDG-PET/CT and WB-DWI/MRI

Primary tumour Implants: peritoneum, Lymphadenopathies Distant metastases

mesentery, serosa, omentum
Eur Radiol (2014) 24:889–901

CT [10, 25, 26] - Size - Contrast enhancement: - Short-axis diameter/threshold - Established imaging criteria
- Morphology *Peritoneal surface, omentum, *Chest: 5-mm
mesentery or serosa
* Nodules *Nodular, infiltrative or confluent *Abdomen:10-mm
* Contrast enhancement *Necrosis or cystic change
FDG-PET/CT [27] - Size - FDG-uptake higher than liver - Higher than background FDG uptake - Higher than background
not attributable to physiological FDG uptake in correlation to CT
uptake
- Morphology *Peritoneal surface, omentum, *Irrespective of nodal size
mesentery or serosa
*Nodules *Nodular or confluent. - Coregistered or clinical CT:
*Contrast enhancement - Coregistered or clinical CT: *Topographic correlation
- FDG-avidity *Lesions below spatial resolution *Necrosis or cystic change
limit of FDG-PET (6–8 mm)
* Nodular * topographic correlation
WB-DWI/MRI [28, 29] - (Size) - B1000 SI: - B1000 SI: - B1000 SI:
- Morphology *Peritoneal surface, omentum, *Equal to or higher than the solid *Hyperintensity not attributable to
mesentery or serosa component of the primary tumour T2 shine- through or anatomical
*Nodules *Nodular, infiltrative or confluent relative to surrounding lymph nodes structure
* T2-weighted signal *Not attributable to T2 shine-through
intensity (SI) or physiologically impeded diffusion
in anatomical structures.
*Contrast enhancement - Coregistered T2/contrast-enhanced MRI *Irrespective of nodal size
- Functional: *Lesions below spatial resolution
limit of DWI (< 4 mm)
*Nodules *Topographic correlation - Coregistered T2/contrast-enhanced
*b1000 DWI SI MRI:
*Topographic correlation
*Necrosis or cystic change
893
894 Eur Radiol (2014) 24:889–901

Fig. 1 Demonstration of the

correlation between imaging and
surgical findings during
diagnostic open laparoscopy
(DOL). (a) Whole-body DWI/
MRI identifies multiple small
mesenterial implants as small
b1000 hyperintense lesions
compared with the background
(arrows, dashed circle), (b, c)
FDG-PET/CT identifies the larger
lesions (arrows). (d, e) DOL
confirms the multiple metastatic
deposits in the designated areas at
imaging

Table 3 Clinical and pathologi-

cal characteristics of the included Patient Primary tumour FIGO stage Therapy
patients
1 Serous papillary ovarian cancer IIIb 3×TC+IDS (R0)
2 Serous papillary endometrial cancer IV 6×TC+debulking (R0)
3 Signet ring cell gastric cancer IV Referred to digestive oncology
4 Serous cystadenofibroma benign Staging laparotomy
5 Serous borderline ovarian tumour Ia Staging laparotomy (R0)
6 Ancient schwannoma benign Follow-up
7 Serous/clear cell endometrial cancer IV 3×TC, no IDS
8 Serous papillary ovarian cancer IV 3×TC+IDS (R0)
9 Serous papillary ovarian cancer IIIc Primary debulking (R0)
10 Serous papillary ovarian cancer IIIc Primary debulking (R0)
11 Serous papillary ovarian cancer IV 3×TC+IDS (R0)
12 Serous papillary ovarian cancer IIIc 3×TC+IDS (R0)
13 Serous papillary ovarian cancer IIIc Primary debulking
14 Mucinous borderline ovarian tumour Ia Diagnostic laparotomy
15 Serous papillary ovarian cancer IIIc Conservative primary debulking
16 Serous papillary ovarian cancer IV 3×TC, no IDS
17 Serous papillary ovarian cancer IIIc 3×carboplatinum monotherapy
18 Pancreatic cancer IV Referred to digestive oncology
19 Adnexial hydropic myoma benign Primary debulking
20 Serous papillary ovarian cancer IIIc 2×TC, no IDS
21 Mature cystic teratoma benign Primary debulking
22 Serous papillary ovarian cancer IV 3×TC+IDS
23 Serous papillary ovarian cancer IIIc 3×TC+IDS (R0)
24 Serous papillary ovarian cancer IV 3×TC+IDS
25 Serous papillary ovarian cancer IIIa Diagnostic laparotomy
26 Serous papillary ovarian cancer IV 3×TC+IDS (R0)
27 Serous papillary ovarian cancer IV 3×carboplatinum monotherapy
28 Serous papillary ovarian cancer IIIc Primary debulking (R0)
29 Serous papillary ovarian cancer IV 3×TC+IDS (R0)
TC, paclitaxel/carboplatin; IDS,
interval debulking surgery; R0, 30 Serous papillary endometrial cancer IV 6×TC, no IDS
complete tumour resection; 31 Serous papillary ovarian cancer IV 3×TC+IDS (R0)
FIGO, International Federation of 32 Serous papillary ovarian cancer IIIc Primary debulking (R0)
Gynaecology and Obstetrics
Eur Radiol (2014) 24:889–901 895

lymphadenopathy in three and hepatic-hilar involvement in
five. Distant metastases in the liver (n =1), pleura (n =1),
mediastinal lymph nodes (n =11) and neck (n =1) were con-
firmed in 14 patients (44 %, 14/32).
Site-based analysis
There were no statistically significant differences in sensitivity
or specificity between hybrid FDG-PET/CT and stand-alone
PET correlated with routine CT images (P >0.05).
Characterisation of primary lesions
WB-DWI/MRI showed 100 % sensitivity, 50 % specificity,
94 % accuracy, NPV of 100 % and PPV of 93 % for the
characterisation of primary lesions (malignant versus benign,
irrespective of tumour origin) compared with 96 % sensitivity,
25 % specificity, 88 % accuracy, NPV of 50 % and PPV of
90 % for CT and 100 % sensitivity, 33 % specificity, 94 %
accuracy, NPV of 100 % and PPV of 94 % for FDG-PET/CT.
Peritoneal carcinomatosis
Comparative sensitivities, specificities, accuracies, PPVs and
NPVs of WB-DWI/MRI, CT and FDG-PET/CT for detecting
PC are shown in Table 4 and the supplementary table.
For overall peritoneal staging, the sensitivity and specificity
of WB-DWI/MRI were significantly higher than CT and PET/
CT (P <0.00001). WB-DWI/MRI showed a significantly higher
sensitivity for detecting peritoneal metastases at the bladder
peritoneal surface than CT and FDG-PET/CT (P =0.0455 and
P =0.0055, respectively). WB-DWI/MRI showed a significant-
ly higher sensitivity for detection of peritoneal metastases over
the left and right pelvic cavity and Douglas pouch than FDG-
PET/CT (P =0.0077, P =0.0159 and P =0.0159, respectively).
WB-DWI/MRI enhanced the detection of small bowel and
colonic mesenteric metastases compared with CT (P =0.0269)
and FDG-PET/CT (P =0.0003), and also enhanced the detec-
tion of small bowel and colonic serosal metastases compared
with CT (P =0.0771) and FDG-PET/CT (P =0.0159; Figs. 2
and 3 and supplementary table).
Retroperitoneal and hepatic-hilar metastases
Comparative sensitivities, specificities, accuracies, PPVs and
NPVs of WB-DWI/MRI, CT and FDG-PET/CT for retroper-
itoneal and hepatic-hilar lymphadenopathies are shown in
Table 4 and the supplementary table. WB-DWI/MRI showed
equivalent accuracy to FDG-PET/CT for retroperitoneal nodal
staging and was superior to CT. For hepatic-hilar lymphade-
nopathies, WB-DWI/MRI was slightly more sensitive than

Table 4 Per-site accuracy for

WB-DWI/MRI Site TP FN FP TN Sens Spec PPV NPV Acc

Peritoneal cavity
Bladder surface 15 2 0 11 0.88 1.00 1.00 0.85 0.93
Douglas pouch 18 1 1 9 0.95 0.90 0.95 0.90 0.93
Right pelvic 19 1 0 10 0.95 1.00 1.00 0.91 0.97
Right lateroconal 14 1 2 11 0.93 0.85 0.88 0.92 0.89
Subhepatic+Morrison’s space 10 0 0 41 1.00 1.00 1.00 1.00 1.00
Right diaphragm 11 1 2 14 0.92 0.88 0.85 0.93 0.89
Hepatic surface 3 1 0 21 0.75 1.00 1.00 0.95 0.96
Left diaphragm 6 3 1 18 0.67 0.95 0.86 0.86 0.86
Surface spleen 0 1 1 20 0.00 0.95 0.00 0.95 0.91
Left lateroconal 16 0 2 11 1.00 0.85 0.89 1.00 0.93
Left pelvic 21 0 0 10 1.00 1.00 1.00 1.00 1.00
Omentum 22 1 0 8 0.96 1.00 1.00 0.89 0.97
Small bowel serosa 3 3 2 19 0.50 0.90 0.60 0.86 0.81
Small bowel mesentery 12 0 5 12 1.00 0.71 0.71 1.00 0.83
Colonic serosa 9 2 4 15 0.82 0.79 0.69 0.88 0.80
Colonic mesentery 10 2 4 13 0.83 0.76 0.71 0.87 0.79
Summary 189 19 24 243 0.91 0.91 0.89 0.93 0.91
Retroperitoneum
TP, true positive; FN, false nega- Infrarenal 8 2 3 22 0.80 0.88 0.73 0.92 0.86
tive; FP, false positive; TN, true
negative; Sens, sensitivity; Spec, Suprarenal 2 1 0 7 0.67 1.00 1.00 0.88 0.90
specificity; PPV, positive predic- Summary 10 3 3 29 0.77 0.91 0.77 0.91 0.87
tive value; NPV, negative predic- Liver-hilum 5 3 2 64 0.63 0.97 0.71 0.96 0.93
tive value; Acc, accuracy
896 Eur Radiol (2014) 24:889–901

Fig. 2 Comparative (a) sensitivity, (b) specificity, (c) positive and (d) negative predictive values among WB-DWI/MRI, CT and FDG-PET/CT for the
detection of bowel serosal and mesenterial metastases

CT or FDG-PET/CT at the cost of a lower specificity com- (κ=1.00), whereas the correlation between CT and FDG-
pared with PET/CT. PET/CT was poor (κ=0.34).

Distant/non-peritoneal metastases Patient-based analysis: clinical impact

Whole-body DWI/MRI showed excellent correlation with With respect to primary tumour characterisation (ovarian ver-
FDG-PET/CT for characterisation of distant metastases sus non-ovarian origin), WB-DWI/MRI correctly identified

Fig. 3 (a, b) Whole-body DWI/MRI shows small peritoneal metastases on the lateral hepatic surface as a small hypermetabolic lesion (arrow) but
on the lateral hepatic surface as b1000 hyperintense lesions (arrows), reveals no mesenteric or serosal lesions. During debulking surgery, (e) the
small mesenteric deposits (square) and small bowel serosal deposits mesenteric and serosal metastases were confirmed as well as (f) the small
(arrowheads). (c, d) FDG-PET/CT shows the small peritoneal metastasis metastases on the lateral hepatic surface
Eur Radiol (2014) 24:889–901
the six tumours that were non-ovarian in origin, compared
with three out of six for CT and two out of six for FDG-PET/
CT (Fig. 4). WB-DWI/MRI correctly identified two of the
three benign ovarian lesions compared with one out of three
for CT and FDG-PET/CT.
By WB-DWI/MRI a significantly higher number of patients
were assigned to the correct FIGO stage or correctly assigned as
benign or non-ovarian in origin compared with CT [94 %
(30/32) for WB-DWI/MRI vs. 56 % (18/32) for CT;
P =0.0015]. There was no statistically significant difference
between WB-DWI/MRI and FDG-PET/CT [72 % (23/32);
P =0.13).
With WB-DWI/MRI and FDG-PET/CT, distant metastases
(stage IV) were detected in eight patients negative at CT
(Fig. 5), while two patients with mediastinal lymphadenopa-
thy on CT were correctly downstaged to a stage IIIc operable
tumour. In two patients WB-DWI/MRI and FDG-PET/CT
detected a suprarenal retroperitoneal lymphadenopathy that
was negative at CT. In the patient group staged as IIIc or
IIIb by all imaging techniques (n =10), WB-DWI/MRI addi-
tionally detected multifocal serosal/mesenteric metastases in
three patients deemed inoperable at DOL (Fig. 6).
Interobserver agreement
Interobserver agreement was moderate for hepatic-hilar ana-
tomical sites (κ=0.581), but substantial for small bowel, colon
and retroperitoneal involvement (κ=0.701, 0.735 and 0.776,
respectively) and almost perfect for primary tumour character-
isation, peritoneal involvement and detection of distant metas-
tases (κ=0.860, 0.906 and 0.829, respectively; Table 5). For
Fig. 4 Whole-body DWI/MRI shows a diffuse (a) b1000 hyperintense
and (b) T2 moderately intense confluent mass over the small bowel
mesentery and serosa in the upper abdomen (arrows) and pelvis (oval
shape). (c) DWI b1000 image shows a heterogeneously iso- to hyperin-
tense mass in the pancreatic head. (d) This is confirmed by the contrast-
897
tumour staging the two observers agreed on 20/24 cases
(83 %).
Discussion
In this prospective study, WB-DWI/MRI allowed more accu-
rate tumour characterisation and detection of peritoneal,
mesenterial and serosal metastases than CT or FDG-PET/
CT. With similar performance to FDG-PET/CT, WB-DWI/
MRI significantly improved the detection of thoracic lymph-
adenopathies compared with CT. The ability to simultaneous-
ly and accurately determine the extent of peritoneal and distant
metastatic disease—pivotal in determining the operability of
ovarian cancer [22]—suggests the potential value of WB-
DWI/MRI for presurgical staging of ovarian cancer.
DWI visualises tumoral lesions by combining heavy diffu-
sion weighting and background signal suppression of organs
and ascites. Additionally, the suppressive effect of the short T1
inversion recovery (STIR) prepulse on the bowel wall, having
a short T1 value, facilitates detection of serosal metastases
[30]. WB-DWI benefits from the STIR prepulse as it is robust
to inhomogeneity-induced fat suppression and susceptibility
artefacts. Importantly, even when using STIR, physiological
bowel wall b1000 hyperintensity and susceptibility artefacts
caused by intraluminal air may obscure or be mistaken for
serosal deposits [31]. This was compensated for by giving an
intravenous antispasmodic and per-oral pineapple juice.
Owing to constraints in imaging time and parameters, WB-
DWI/MRI appears unlikely to be used for evaluating ovarian
masses equivocal at gynaecological ultrasound. However, the
enhanced image, which shows hypo-enhancement in the mass. These
findings suggest primary pancreatic cancer with diffuse mesenterial and
serosal metastases. (e) FDG-PET/CT (only PET portion shown) failed to
show any hypermetabolic lesions. Findings of WB-DWI/MRI were con-
firmed during DOL and endoscopic ultrasound with biopsy
898
Fig. 5 (a, b) Whole-body DWI/MRI depicts multifocal b1000 hyperin-
tense lesions, indicating peritoneal cavity dissemination combined with
mesenterial/serosal deposits over the caecum, right and left colic flexure,
the sigmoid, the small bowel in the right fossa and the duodenum in the
capacity for identifying non-ovarian primary tumours may be
useful in patients with PC of unknown origin or those with
ovarian masses uncertain to be primary or metastatic.
Corroborating previous study findings using abdominal
DWI, WB-DWI/MRI showed high overall accuracy for peri-
toneal staging [13, 19, 32]. Previously, combined gadolinium-
enhanced MRI and DWI had the highest accuracy compared
with either sequence alone. Therefore, we did not evaluate the
Fig. 6 (a) FDG-PET and (b) CT show peritoneal metastases under the
right diaphragm (arrow), the right lateroconal area (arrowheads) and
small bowel mesenteric metastases in the lower abdomen (dashed ar-
rows). (c, d) WB-DWI/MRI confirms the diaphragmatic (arrow) and
right lateroconal metastases (arrowheads). However, lower abdominal
small bowel mesenteric metastases appear much more widespread and
confluent (dashed arrows). In addition, WB-DWI/MRI shows multifocal
Eur Radiol (2014) 24:889–901
right upper abdomen, in addition to (c, d) FDG-PET/CT). WB-DWI/
MRI findings were confirmed by DOL. (e) WB-DWI also depicts a right
intrathoracic nodal metastasis (arrow) confirmed by (f) FDG-PET/CT
(arrow)
separate contributions of the functional and anatomical se-
quences [32]. Combining gadolinium-enhanced MRI with
DWI reduces false readings, especially in lesions obscured
by impeded diffusion in the spleen or by distortion artefacts at
the boundaries of aerated organs. Nevertheless, we found
lower accuracy for detecting left diaphragmatic metastases
close to the spleen and stomach compared with detection of
other peritoneal metastases.
b1000 hyperintense metastases in the gastrohepatic ligament (oval shape)
as well as in the small bowel mesentery over the entire abdomen (hyper-
intense dots on image c, not indicated by arrows). Also, the small bowel
wall in the left hypochondrium appears hyperintense (arrow outline),
indicating serosal metastases. All suspect locations found on WB-DWI/
MRI were confirmed by DOL. (b) Renal graft can be seen on the CT
image (asterisk)
Eur Radiol (2014) 24:889–901 899

Table 5 Interobserver agreement for per-site lesion detection breathing acquisition and single-phase contrast, may have
Region Cohen’s kappa contributed to the lower sensitivity. Pfannenberg et al. found
better evaluation of subcentimetric lesions by using multi-
Primary tumour 0.86 phase contrast-enhanced and breath-hold CT as an integrated
Bladder peritoneal surface 0.83 component of FDG-PET/CT [41].
Douglas pouch 0.91 To our knowledge, only two previous studies compared
Peritoneal right pelvic 1.00 DWI and FDG-PET/CT for assessing PC. In the study by
Peritoneal right lateroconal 1.00 Soussan et al., DWI showed non-significantly higher sensitiv-
Peritoneal subhepatic+Morrison’s space 1.00 ity for detecting PC [36]. In the study by Satoh et al., DWI
Right diaphragm 0.92 showed similar sensitivity but lower specificity compared
Hepatic surface 0.83 with FDG-PET/CT [42]. Both studies mainly evaluated diges-
Left diaphragm 0.56 tive cancer patients and used a different site-based classifica-
Surface spleen 0.65 tion from our study. Furthermore, in the study of Satoh et al.,
Peritoneal left lateroconal 0.92 PC consisted mainly of supracentimetric lesions. Importantly,
Peritoneal left pelvic 1.00 in these studies DWI showed lower sensitivity for the detec-
Omentum 0.83 tion of small or serosal metastases. We probably overcame this
Small bowel serosa 0.48 limitation by combining STIR-DWI, per-oral bowel prepara-
Small bowel mesentery 0.83 tion and an antispasmodic agent.
Colonic serosa 0.82 Assessment of nodal disease poses a major challenge. As
Colonic mesentery 0.65 apparent diffusion coefficient (ADC)-based nodal differentia-
Summary peritoneum 0.86 tion has not been firmly validated in gynaecological malig-
Retroperitoneal infrarenal 0.75 nancies, we opted to assess lymphadenopathies in a qualitative
Retroperitoneal suprarenal 0.86
way [43–45]. Potential impediments include the high work-
Summary retroperitoneum 0.78
load of manual region of interest (ROI) delineation and the
Liver-hilum 0.58
possible lack of reproducibility of ADC measurements [46].
Moreover, the frequent cystic, necrotic and mucinous degen-
Distant metastases 0.83
eration of ovarian cancer probably increases the ADC vari-
ability. Using predetermined qualitative interpretative criteria
relating the b1000 SI of nodal disease to that of the primary
WB-DWI/MRI better described the extent of PC than CT, tumour [47], we demonstrated equivalent performance of
particularly mesenteric and serosal deposits and WB-DWI/MRI and FDG-PET/CT, with substantial interob-
subcentimetric lesions. The sensitivity of CT for the detection server agreement. Qualitative interpretation of high b-value
of subcentimetric peritoneal metastases is substantially re- images has been shown to allow the detection of lymphade-
duced by 7–28 %, especially when ascites is absent, and in nopathies in abdominopelvic and pulmonary cancers, similar
subdiaphragmatic, omental, mesenteric and serosal locations to ADC-based differentiation and FDG-PET [27, 47, 48].
[33, 34]. In our study, 36 % of peritoneal lesions were Nevertheless, further research involving larger patient groups
subcentimetric, while 14 patients had no ascites. These factors and dedicated radiological-histopathological correlation are
did not impact WB-DWI/MRI, likely explained by the high mandatory to optimise qualitative nodal evaluation by STIR-
image contrast [35]. DWI.
This high image contrast combined with the capacity to The value of DWI in ovarian cancer was recently suggested
identify lesions as small as 4 mm also explains the discrepancy by Espada et al. where abdominal DWI could predict subop-
in sensitivity for detecting PC with FDG-PET/CT [36]. FDG- timal cytoreduction [19]. However, comparative data for CT
PET/CT has shown variable sensitivity between 58 and and FDG-PET/CT were lacking. The three imaging tech-
100 %. FDG uptake in small volume or infiltrative disease niques were not significantly different in assigning patients
can be underestimated owing to low tracer concentrations, to the correct FIGO stage considering peritoneal disease
physiological uptake in the bowel or liver or respiratory mo- spread (stage I to IIIc). However, WB-DWI/MRI allowed
tion, which cannot always be compensated for by CT [25, more accurate per-site evaluation of PC, enabling better de-
37–40]. This mainly affects the detection of mesenteric, sero- scription of—potentially surgically critical—disease extent. In
sal and right supramesocolonic lesions [12]. In our study, our study, WB-DWI/MRI detected mesenteric and serosal
FDG-PET/CT showed lower sensitivity relative to WB- disease in three patients, underestimated by CT and FDG-
DWI/MRI for detecting right perihepatic, subdiaphragmatic, PET/CT and deemed inoperable at DOL. Therefore, WB-
mesenteric and serosal metastases. Additional technical CT- DWI/MRI may improve operative planning and patient selec-
related factors in the hybrid examination, including free- tion for treatment.
900
Importantly, in this limited patient group, WB-DWI/MRI
and FDG-PET/CT were superior to CT for detecting suprare-
nal retroperitoneal and thoracic lymphadenopathies, thereby
providing the greatest clinical impact. This finding under-
scores the need for developing WB-DWI/MRI rather than
abdominal DWI for assessing the operability of ovarian
cancer.
There were some limitations to this study. Seven patients
underwent stand-alone PET with correlation by clinical CT.
Although no statistically significant differences were observed
with the results of the PET/CT subgroup, this might have been
attributed partly to the lower accuracy for peritoneal staging.
Not all supradiaphragmatic metastases could be confirmed
histopathologically and FDG-PET/CT was considered an im-
perfect standard. FDG-PET/CT has been shown to accurately
detect supradiaphragmatic lymphadenopathy in ovarian can-
cer [49]. Furthermore, the disease pattern, mostly involving
parasternal nodes, is not typical for inflammatory FDG up-
take. Additionally, a relatively large number of patients pre-
sented with advanced disease, potentially increasing the pre-
test likelihood of detecting metastases. This limits the extrap-
olation of our results to lower stage ovarian cancer and re-
quires further research in balanced patient populations.
In conclusion, WB-DWI/MRI showed greater accuracy in
the characterisation of primary tumours and peritoneal staging
in patients with suspected ovarian cancer compared with CT
and FDG-PET/CT. For detecting retroperitoneal lymphade-
nopathy and distant metastases, WB-DWI/MRI performed
similarly to FDG-PET/CT but was superior to CT. By com-
bining accurate characterisation of primary tumours with de-
tection of small metastases at critical peritoneal, retroperito-
neal and distant sites, including serosal, mesenteric and
supradiaphragmatic metastases, WB-DWI/MRI may be of
value for the preoperative management of ovarian cancer.
Acknowledgments This research was supported by the Belgian Founda-
tion against Cancer (Stichting Tegen Kanker – Fondation Contre le Cancer).
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