Available via license: CC BY-NC 4.0
Content may be subject to copyright.
DOI: 10.1159/000501497
Received: 10/8/2018 2:05:36 AM
Accepted: 6/16/2019
Published(online): 6/17/2019
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Added Value of Contrast Medium in Whole-Body Hybrid PET/MRI: Comparison Between Contrast-
Enhanced and Non-Contrast-Enhanced Protocols
Celebi F. Cindil E. Sarsenov D. Unalan B. Balci C.
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ISSN: 1011-7571 (Print), eISSN: 1423-0151 (Online)
https://www.karger.com/MPP
Medical Principles and Practice
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Added Value of Contrast Medium in Whole-Body Hybrid PET/MRI:
Comparison Between Contrast-Enhanced and Non-Contrast-Enhanced
Protocols
Filiz Celebia, Emetullah Cindilb, Dauren Sarsenovc, Bulent Unalana, Cem Balcıd
Department of aRadiology, Gayrettepe Florence Nightingale Hospital, Department of bRadiology
Gazi University, Departments of cGeneral Surgery & dNuclear Medicine, Florence Nightingale
Hospital, Gayrettepe, Turkey, Department of eRadiology, Cleveland Clinic, Lerner School of
Medicine, Abu Dhabi, UAE.
Address all correspondence to:
Filiz Çelebi,
Gayrettepe Florence Nightingale Hospital Radiology Department
Cemil Aslan Guder sok. No: 8 Gayrettepe Istanbul
Turkey.
Email: elbuken.filiz@gmail.com
Running Head : Whole Body Hybrid PET/MRI
Key Words: PET/MRI ● Malignancy ● Fast Protocol ● Contrast Medium
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Highlights
• A comprehensive oncologic imaging is achieved with PET/MRI when appropriate protocol is
used.
• One single examination can cover all organ systems and may detect all types of malignancies.
• A shorter and more accurate Whole Body PET/MRI protocol can be developed for the evaluation
of malignancies.
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Abstract
Objective: To compare the diagnostic ability and time efficiency of contrast-enhanced (CE) whole
body FDG PET/MRI protocol and non-contrast-enhanced (NCE) protocol. Subjects and Methods:
Ninety-three patients with known primary tumors underwent whole-body hybrid FDG PET/MRI
during the follow-up of their malignancies with the use of NCE and CE protocols. The NCE
PET/MRI protocol consisted of diffusion-weighted (b = 0 s/mm2 and 800 s/mm2) and T1-weighted
Turbo Flash in the axial plane and T2-weighted HASTE sequence in the coronal planes (∑ = 25
minutes). The CE PET/MRI protocol was performed by acquiring axial serial CE 3D FS VIBE
images in the upper abdomen, completing the whole body in late phase in the axial plane (∑ = 30
minutes). Results: There was a statistically significant difference between the total number of lesions
detected by the CE protocol (median 2, IQR 0-14) and that detected by the NCE protocol (median 1,
IQR 0-5) (p < 0.001). More malignancies were detected in the abdomen (p < 0.001) and brain (p <
0.001) with the CE PET/MRI protocol, whereas no significant difference was present when
comparing the two protocols in the detection of malignancies in the head and neck (p = 0.356), thorax
(p = 0.09), lymph nodes (p = 0.196) and bone (p = 0.414). Conclusion: The CE FDG PET/MRI
protocol enables fast and accurate detection of malignancies compared to NCE FDG PET/MRI
protocol particularly in the upper abdomen and brain. The diagnostic ability and time efficiency can
be increased with the proposed short CE protocol in place of the whole body PET/MRI protocol
including both NCE and CE imaging sequences.
.
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Introduction
Hybrid positron emission tomography/magnetic resonance imaging (PET/MRI) scanners
have the potential to become an effective tool for the evaluation of oncology patients before, during,
and after treatment and can influence patient management [1,2]. Hybrid PET/MRI uses PET data to
assess the metabolic information of malignant tumors and relies on the uptake of radiotracers.
However, certain tumors such as mucinous carcinoma or signet cell-type adenocarcinoma may not
reveal the uptake of fluorodeoxyglucose (FDG), which is the most commonly used radiotracer. On
the other hand, physiological uptake of FDG in the liver and brain may prevent the depiction of
tumors. Therefore, MRI data collected from hybrid PET/MRI systems not only provide superior soft
tissue contrast and anatomic detail but may also improve the evaluation of malignant tumors.
Therefore, the choice of imaging protocol is crucial for increasing the sensitivity of MRI. The use of
intravenous contrast media is essential to oncologic imaging, especially for the detection of malignant
tumors in the brain and in the upper abdomen [3-5]. In this study, we investigated whether contrast-
enhanced (CE) whole-body PET/MRI protocols increase the sensitivity of detection of malignant
tumors compared to non-contrast-enhanced (NCE) protocols.
Subjects and Methods
In our study, 93 consecutive patients with histopathologically proven primary malignant
tumors aged between 20-87 were retrospectively evaluated (mean age±standard deviation, 55.1
years±14.1) during the period of August 2015 to January 2018. 54 of these patients were men
(53.4±14.7 years), and 39 of them were women (56.4±13.6 years). The institutional review board
approved the study; the requirement of informed consent was waived since the study was a
retrospective investigation. The patients referred to PET/MRI from the hematology/oncology and
surgery departments as part of the standard oncology imaging were included in the study. Patients
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with a history of allergy to gadolinium based contrast agents and end stage renal failure were
excluded from the study. All patients had histopathological proof of their primary malignant tumors
by surgery (n=56) and/or biopsy (n=37).
Metastatic lesions without histopathologic evidence were identified based on the
progression of their size or the appearance of new lesions during follow-up. The malignancy of the
lymph nodes was determined based on their size and/or FDG uptake.
Eight patients underwent neoadjuvant therapy, and PET/MRI was performed at follow-up;
45 patients had their primary tumor surgically removed, followed by adjuvant chemotherapy and/or
chemoradiotherapy. In 40 patients, the primary tumor was not deemed operable according to the
criteria of other imaging modalities, and these patients either underwent chemotherapy and/or
chemoradiotherapy.
All patients fasted for at least 6 hours before imaging. The blood glucose level was
assessed with a blood glucose meter (OneTouch Vita; LifeScan, Milpitas, California, USA) before
imaging to ensure that it was less than 140 mg/dL (7.77 mmol/L).
PET/MRI was performed 45±10 minutes after the injection of FDG (mean dose, 4.54 MBq
per kilogram of body weight±1; range, 370-400 MBq). The images were acquired in supine position
on a 3 Tesla Biograph mMR scanner (Siemens Healthcare, Erlangen, Germany) using a 16-channel
head and neck surface coil and three 12-channel body coils. These body coils were combined to form
a multichannel whole-body coil by using the Total Imaging Matrix technology. The whole-body
images were obtained in five to six bed positions according to the size of the patient and each bed
time position is kept between 2-2.5 minutes. PET acquisition occurred simultaneously during the
whole-body MRI acquisition. In all patients, the whole-body PET/MRI covered the entire body from
head to knee. For the attenuation correction, four-point Dixon images were obtained in the coronal
plane. The whole-body MRI protocol consisted of both NCE images and CE images and provided
the most comprehensive oncologic imaging dataset in the routine in our institution. The imaging
stations were arranged consecutively in the caudocranial direction. The comprehensive MRI protocol
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that included both CE and NCE studies consisted of T2-weighted single-shot echo train (HASTE)
(TR/TE,1500 msec/87 msec) in the coronal plane, T1-weighted slice-selective Turbo Flash
(TR/TE,1600 msec/2.5 msec) and free breath diffusion-weighted imaging using EPI technique
(TR/TE, 12000 msec/78 msec, b=0 s/mm2 and b800 s/mm2) in the axial planes. After the NCE
protocol was performed, a weight-adapted dose of a gadolinium-based contrast agent was
administered, and serial CE images were obtained using breath-hold 3D VIBE (TR/TE, 4.56
msec/2.03 msec) in the arterial, portal venous and equilibrium phases covering the upper abdomen
in the axial plane. After the serial CE images were acquired, continuous breath-hold 3D VIBE images
were obtained from head to knee in the axial plane, and all the sections were combined, resulting in
uninterrupted whole-body coverage. Detailed information regarding the whole-body PET/MRI
protocol is shown in Table 1. The total scan duration of the PET/MRI examination was 50-60
minutes. The durations of both the NCE and CE protocols were 25-30 minutes.
The images were evaluated by two radiologists; one had 25 years of experience, and the
other had 8 years of experience in reading MRI and hybrid imaging. Both readers were blinded to
patient data and diagnosis. One research associate separated each study into two parts, and the loaded
images had a NCE part and a CE part. The data were analyzed on a dedicated workstation (Syngo
Via; Siemens Healthcare, Erlangen, Germany). The NCE and CE protocols were reviewed one month
apart to avoid bias. The review of the cases for CE and NCE studies took one hour each. All images
with diagnostic quality for PET and MRI were evaluated separately and as fused images, the number
of lesions was recorded for both protocols. The radiologists and a nuclear medicine physician
evaluated the images in a joint reading session and made consensus.. The NCE dataset was evaluated
using NCE MR images, PET/MRI fusion images and attenuation-corrected raw data PET images.
The CE dataset was evaluated by reviewing CE MR images, fused PET/MRI images and attenuation-
corrected raw data PET images.
Statistical analyses were performed using SPSS software version 20. The variables were
investigated using visual methods (histograms, probability plots) and analytical methods
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(Kolmogorov-Smirnov) to determine whether or not the distribution was normal.
As most of the variables excepting “age” were not represented by real numbers, descriptive
analyses for tests were presented using medians and interquartile range (IQR). Friedman’s test was
conducted to evaluate whether there is a significant change in the total number of detected lesions
among different MRI sequences separately for each anatomic region (due to violations of parametric
test assumptions as number of lesions detected can only be integer). Pairwise comparisons were
performed using Wilcoxon signed rank test. A p value of less than or equal to 0.05 was accepted as
statistically significant.
Results
Of the 93 patients, 17 patients had non FDG-avid malignant tumors. The rest of the
patients had FDG avid malignant tumors, 36 patients had distance metastasis (M) and 40 patients
had lymph node metastases (N).
Distribution of the primary malignant tumors is shown in Table 2. Gastrointestinal tumors
include gastric, pancreatic, colorectal cancers , hepatocellular carcinoma and cholangiocarcinoma.
The number of lesions detected using the CE protocol (median 2, IQR 0 - 14) was
significantly higher than that detected using the NCE protocol (median 1, IQR 0 - 5) (p < 0.001). The
total number of lesions detected using the CE protocol varied between 0 - 120 (minimum-maximum),
whereas that detected using the NCE protocol was 0 - 75 (minimum-maximum). The total number
of lesions detected with only the PET component (median 1, IQR 0 - 11) was significantly lower than
the number of lesions detected with the CE PET/MR protocol (median 2, IQR 0 - 14) (p < 0.001).
Regarding the number of region-based lesions, the number of lesions in the brain detected
with the CE protocol (median 2, IQR 1 - 2) was significantly higher than that detected with the NCE
protocol (median 0, IQR 0-1) (p = 0.001, n = 11). (Fig. 1)
In the abdomen, the CE PET/MRI protocol (median 2, IQR 1 - 6) was superior to the NCE
protocol (median1, IQR 0-2) (p < 0.001, n = 65) (Fig. 2).
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There was no difference between the number of malignant tumors detected by the two
protocols for the head and neck (p = 0.356, n = 13), bone (p = 0.414, n = 28), thorax (p = 0.09, n =
31) (Fig. 3), and lymph nodes (p = 0.196, n = 32) (Table 3).
Discussion
Our study showed that the CE fast PET/MRI protocol depicted more malignant tumors in
the upper abdomen and in the brain compared to the NCE protocol. In addition, our CE fast protocol
may increase patient comfort due to its short duration and is an effective tool for the evaluation of
oncology patients before, during, and after treatment.
PET/MRI is a new imaging modality that combines the sensitivity of molecular imaging
of PET and the superior radiologic diagnostic capabilities of MRI. In addition, PET/MRI provides
detailed background anatomical landmarks from MRI images. MRI also bestows superior tissue
contrast that helps to localize tumors and assist in the local staging (T staging) of tumors. PET/MR
is superior to PET/CT because its resolves soft tissue without the need for radiation exposure. The
metabolic information from PET data together with the diagnostic accuracy of CE whole-body MRI
may increase the sensitivity of tumor detection.
Several studies have shown that the detection of primary and metastatic liver and brain
tumors by MRI is superior to that by PET [3,5]. In liver imaging, serial CE images are essential to
depict hypervascular lesions, and only CE images can depict brain metastases [3,4,6-9]. In the
pancreas, CE images may depict hypervascular neuroendocrine tumors that are not FDG avid [10-
12]. Additionally, renal tumors may be evaluated with CE images to differentiate between benign
and malignant lesions [13]. PET images rely on the uptake of FDG, which is taken up physiologically
by the tissues of the liver and brain. Primary liver tumors such as HCC can only take up FDG if they
are less differentiated [14,15]. In our dataset, CE PET/MRI depicted more HCC with the serial CE
images. HCC is a hypervascular tumor with arterial blood supply, and arterial enhancement with
venous washout is diagnostic for HCC in serial CE images [8].
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In contrast to our results, Lee at al presented that the effect of gadolinium based contrast
agents on PET image can be negligible quantitatively and qualitatively [16]. In imaging renal and
bladder tumors, MRI is superior to PET with CE protocols. Renal lesions, including cysts, can only
be categorized according to their enhancement pattern [17]. In our dataset, we did not observe any
primary renal tumor; however, CE MRI protocols can further help to distinguish between malignant
and benign renal lesions. We did not observe any significant difference in bone metastasis and lymph
node involvement.
FDG-PET detection of hypometabolic metastasis and increased bone marrow activity after
chemotherapy is not sensitive [18-19-20]. Bone marrow-sensitive MRI techniques can provide
diagnostic information on FDG-negative cases [21]. Our data showed that the combined evaluation
of PET and MRI with either diffusion-weighted imaging (DWI) or post-contrast VIBE equally
assessed the bone marrow metastases. Previous studies have shown that CE MRI and DWI have
similar sensitivities for the detection of bone metastases [22,23].
Stolzman et al. [24] and Catalano et al. [25] compared lung nodule detection rates using
CT, MR and PET either in different combinations or separately. They found similar detection rates
for both PET/CT and PET/MRI. Our study revealed similar results for the detection of lung nodules.
The duration of the whole-body PET/MRI examination is long, and it is unpleasant for the patient to
undergo a one-hour examination in a closed environment. Therefore, shorter protocols have been
performed [26,27]. Our CE protocol may be used as standard protocol for shorter examinations,
which may increase patient throughput and patient comfort.
The limitation of our study may include the limited number of cases with each
malignancies to group and see which particular malignancies may benefit the most for contrast
enhanced protocol. Also not all cases were histopathologically proven. Further prospective studies
may needed for tailored PETMRI protocols for specific malignancies especially in terms of local
staging. Contrast enhanced studies may be performed with the use of improved temporal resolution
to calculate the contrast passage (Ktrans) and monitor the antiangiogenic treatments.
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Conclusion
An optimal oncologic imaging was achieved using the appropriate protocol for PET/MRI,
and a variety of tumor types and involvement of the organ systems can be reviewed by optimizing
the protocol. We investigated the use of the CE whole-body PET/MRI protocol for the assessment
of malignant tumors, and our results indicated that MRI with intravenous contrast might increase the
sensitivity of PET/MRI. The protocol with the emphasis of CE examination can further shorten the
PET/MRI exam with increased detection rate of neoplasms.
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Table 1: Detailed Whole-Body PET/MRI protocol
NCE protocol Image
plane
Slice thickness
(mm) Gap (%) Slices
(no.)
Acquisition
time (min:s) TR/TE Matrix Field of view
(mm)
Resolution
(mm2) FA Breath-hold
Method
DWI (b=0 s/mm
2
and 800 s/mm
2
)
axial 6 0.6 300 11:25 7200/81 126x128 440 128/100 NA Breath-free
T1-weighted Turbo flash axial 5 1 175 6:16 1600/2.46 194x320 450 320/81 20 Resp trigger
T2-weighted HASTE coronal 5 1 175 5:59 1500/87 320x320 440 320/100 136 Resp trigger
CE protocol
Image
plane
Slice thickness
(mm)
Gap (%)
Slices
(no.)
Acquisition
time (min:s)
TR/TE Matrix
Field of view
(mm)
Resolution
(mm2)
FA
Breath-Hold
Method
3D FS VIBE for upper
abdomen
axial 3 0 96 0:23 4.56/2.03 195x320 380 320/75 9 Breath-hold
3D VIBE FS Dixon coronal 1.90 0 144X5 1:49 4.02/1.23 149x288 460 288/75 9 Breath-hold
3D FS VIBE for the brain axial 1 0 176 2:30 9.50/3.69 256x320 231 320/80 12 Breath-free
CE: Contrast-enhanced, NCE: Non-contrast-enhanced
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Table 2: Distribution of primary malignant tumors
Primary malignant tumors Number of patients
Hepatobiliary 28
Other Gastrointestinal 16
Genitourinary 10
Breast 18
Immunoproliferative 6
Lung Carcinoma 6
Other 9
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Table 3:
Distribution of malignant tumors for different body regions
CE protocol NCE protocol
Region Median IQR Median IQR p
Brain 2 1-2 0 0-1 p<0.001
Head & Neck 2 1-3.5 2 1-4 p=0.356
LN 1 1-4 1 1-3 p=0.196
Thorax 1 1-4 1 1-3 p=0.09
Abdomen 2 1-6 1 0-2 p< 0.001
Bone 5 1-30 4.5 1-30 p=0.414
Total 2 0-14 1 0-5 p< 0.001
Friedman’s test
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Figure Legend
Fig. 1. A 56-year-old patient with chronic liver disease. An enhancing nodule is present in segment
6 of the liver in the arterial phase (arrow, a) that reveals contrast washout on the portal venous phase
(arrow, b) during the contrast-enhanced PET/MRI protocol. On the diffusion-weighted MRI (c) and
PET/MRI fusion images (d), no lesion is visible during the non-contrast-enhanced PETMRI protocol.
.
Fig. 2. A 67-year-old patient with breast cancer. Non-contrast-enhanced PET/MRI fusion images
reveal two FDG-avid lesions in the cerebellum (arrows, a) that are not seen on the diffusion-weighted
MRI (b). 3D VIBE postcontrast images acquired using the contrast-enhanced PET/MRI protocol
reveal both metastases (white arrows, c) and an additional smaller lesion (black arrow, c).
Fig. 3. A 72-year-old patient with advanced colon cancer. Contrast-enhanced PET/MRI protocol
reveals multiple lung metastases and bone involvement in the thoracic vertebra (arrow, a) on the
postcontrast 3D VIBE axial image. Non-contrast-enhanced protocol with diffusion-weighted MRI
reveals bone involvement (arrow, b) with less apparent lung lesions. Fusion PETMRI images of the
non-contrast protocol depicts both lung and bone metastases (arrow, c).
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Fig 1 (a-d)
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Fig 2 (a –c)
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Fig 3 (a – c).
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