1
THE CLINICAL APPLICATION OF 4D 18F-FDG PET/CT ON GROSS
TUMOR VOLUME DELINEATION FOR RADIOTHERAPY PLANNING IN
ESOPHAGEAL SQUAMOUS CELL CANCER
Yao-Ching Wang1,2 , Chia-Hung Kao 3,4, Te-Chun Hsieh4,5, Shang-Wen Chen1,3,
Chun-Ru Chien1,3, Chun-Yen Yu1,5, Kuo-Yang Yen4,5, , Shih-Neng Yang1,5, Yu-Cheng
Kuo1,3, Shih-Ming Hsu6, Tinsu Pan7, Ji-An Liang1,3
Affiliation
1
Department of Radiation Oncology, China Medical University Hospital, Taichung,
Taiwan; 2 School of Medicine, Graduate Institute of clinical Medical Science, China
Medical University, Taichung, Taiwan; 3School of Medicine, China Medical University,
Taichung, Taiwan, 4Department of Nuclear Medicine and PET Center, China Medical
University Hospital, Taichung, Taiwan; 5 Department of Biomedical Imaging and
Radiological Science, China Medical University, Taichung, Taiwan; Biomedical
Imaging and Radiological Science, China Medical University, Taiwan; 7 University of
Texas MD Anderson cancer center
Address correspondence and/or reprint requests to: Ji-An Liang, MD, Department of
Radiation Oncology, China Medical University Hospital, No. 2, Yuh-Der Road, Taichung
404, Taiwan. TEL: 886-4-22052121-7461; FAX: 886-4-22339372; E-mail:
d4615@mail.cmuh.org.tw
2
Running title: 4D PET/CT-based gross tumor volume in esophageal cancer
Abstract
Objectives: To estimate the feasibility of the combined four-dimensional computed
tomography with four-dimensional 18F-fluorodeoxyglucose positron emission
tomography (4D CT-FDG PET) in gross tumor volume (GTV) delineation of
esophageal cancer.
Methods: Eighteen patients with esophageal cancer eligible for radical surgery or
definitive radiotherapy were prospectively enrolled. In 4D images during respiratory
cycle, an average phase of CT images was fused with average phase of FDG PETs for
analysis of optimal standardized uptake values (SUV) or threshold. PET-based GTV
(GTVPET) was determined with 8 different threshold methods by autocontouring
function at the PET workstation. The difference in volume ratio (VR) and
conformality index [1] between GTVPET and CT based GTV (GTVCT) was
investigated.
Results: The image sets via automatic co-registrations of 4D CT-FDG PET were
available in 12 patients with 13 GTVCT. The decision coefficient (R2) of tumor length
difference at the threshold levels of SUV2.5, SUV20% and SUV25% were 0.79, 0.65
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and 0.54, respectively. The mean volume of GTVCT was 29.41 ± 19.14 mL (range,
3.65 to 70.76 mL). The mean VR ranged from 0.30 to 1.48 (0.86±0.24). The optimal
VR, 0.98 , close to 1, was at SUV 20% or SUV 2.5. The mean CI ranged from 0.28 to
0.58. The best CI was at SUV 20% (0.58) or SUV 2.5 (0.57).
Conclusions: The autocontouring function by SUV threshold has the potential for
assisting the contouring the GTV in radiation planning for esophageal cancer. The
SUV threshold setting of SUV 20% or SUV 2.5 achieves the optimal correlation in
tumor length, VR and CI using 4D-PET/CT images.
Introduction
The use of 18Fluoro-deoxyglucose positron emission tomography (18F-FDG PET)
in radiotherapy (RT) provides a supplement of this already interdisciplinary process to
include information on the biologic status of tumors, which is complementary to
conventional computed tomogram (CT) images and may result in a change of the
tumor volume delineation[2]. RT is an important part of the multidisciplinary
treatment in esophageal cancer (EC) , but tumor control and overall survival are still
disappointed [3]. 18F-FDG PET has been shown to improve the staging of EC [4, 5].
Particularly, several studies suggested PET overlay on CT has shown to have some
4
impact on the definition of the gross tumor volume (GTV), decrease inter-observer
variability and change the treatment planning. [6-8]. However, when radiation
oncologists contour the GTVs on a fused PET and CT image or an integrated PET/CT,
a problem appears in setting the appropriate threshold for the PET. Despites several
investigations declared autocontouring or manual contouring of the PET-based tumor
volume results in a change of the GTV compared to CT-based GTV[9-11], some
standards should be followed for the PET/CT–based tumor delineation..
The published methods based on a threshold determined as a percentage of the
maximal standardized uptake value (SUVmax) have used values ranging from 15% to
50% for non-small-cell lung cancer [12-14]. Similarly, there was a great variations of
validated standardized methods for EC in setting this threshold [7, 15-17]; these
include using mean activity in the liver plus various standard deviation, the various
absolute standardized uptake value (SUV) (i.e., GTV = SUV of ≧2), or using
percentages of the SUVmax (i.e., GTV = volume encompassed by ≧ 25% the
SUVmax). Organs or tumor motion always influenced the accuracy and quality of CT
images in the thoracic malignancy, including EC during free breathing cycle. Concern
should be taken when considering the extent of tumor motion and different spatial
tumor position by four-dimensional (4D) CT as described in non-small-cell lung
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cancer [18, 19]. A recent study reported EC moved with respiratory cycle, especially
at lower third and in the cranial-caudal direction. [20]. Respiratory 4D PET/CT
techniques are highly useful in target volume definition accurately representative of
organ and lesion motion despite the real benefits of clinical outcome need further
investigation [21]. It is still unknown about the feasibility of implementing
four-dimensional PET/CT (4D-PET/CT) in determining the GTV for EC. Thus, there
is a need to conduct a pilot study by using 4D-PET/CT in contouring.
We hypothesized that some standards can be obtained when defining GTV for
EC by using biological target volume from 4D-PET/CT images. This prospective
study was conducted to evaluate the feasibility of 4D-PET/CT simulation in RTO
planning for esophageal cancer. Also, appropriateness of the percentage threshold
method would be investigated for determining the best volumetric match between
PET-based and CT-based GTV when contouring primary tumor volume of esophageal
cancer.
Materials and Methods
Patients
This study was a prospective analysis, approved by local institutional review
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board (DMR98- IRB-171), of 4D-PET/CT in radiotherapy planning of esophageal
cancer. Patients with histologically approved esophageal cancer who would
undergo definitive radiotherapy, concurrent chemoradiotherapy or radical surgery were
eligible for this study. Eighteen patients with esophageal squamous cell cancer were
enrolled between December 2009 and January 2011. The image data from 12 patients
with 13 GTVCT were available for this study and were analyzed. The median age was
48.5years (range, 38-76 years). All patients were men. The characteristics of these
patients included are presented in Table 1.
PET-CT image acquisition
All patients were asked to fast for at least 4 hours before 18F-FDG PET/CT imaging.
Each of them was administered intravenously with 370 MBq (10 mCi) of 18F-FDG
and rested supine in a quiet and dimly room. All images were acquired with an
integrated PET/CT scanner (Discovery STE, GE Medical Systems, Milwaukee, WI).
Scanning began 40 minutes after injection of FDG. Arms were elevated above the
head. Staging whole body PET/CT images were taken first according to the
standardized protocol. The CT images were reconstructed onto a 512×512 matrix and
converted to a 128×128 matrix, 511-keV-equivalent attenuation factors for attenuation
correction of the corresponding PET emission images. Immediately after whole body
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PET/CT images, patients were repositioned and simulated in a radiotherapy planning
position using the Real-time Position Management (RPM) system respiratory gating
hardware (Varian Medical Systems Inc, Palo Alto, CA, USA). Four-dimensional CT
images with 2.50-mm slice thickness, and 4D PET images with two table positions, 7
minutes per position, were acquired. The respiration cycle was divided in 10 phases
each other. All CT images were automatically sorted by 4D software (Advantage 4D,
GE, Healthcare). The images were transferred from the PET/CT workstation via
DICOM3 to the RTP (Eclipse version 8.6, Varian Medical System Inc, CA, USA) for
GTV delineation. All phases of CT images and PET images were automatically fused
for this gating study. PET/CT-based GTV of the primary tumor (GTVPET) was defined
by autocontouring function at the AW workstation (Advantage SimTM 7.6.0, GE,
Healthcare), either applying the isodensity volumes by adjusting different percentage
of the maximal threshold levels, or simply using a fixed value of SUV. The threshold
strategies for assessing the optimized SUV for GTV contouring were derived from
other investigation [7, 8, 16, 22]. Eight different threshold methods were used in this
study. They were SUV 15%, SUV 2, SUV 2.5, SUV 20%, SUV 25%, SUV 30%, SUV
40% and SUV 50%. The length of the GTVPET provided by autocontouring function
was not changed at all. All the artifacts within the GTVPET, including the area overlaid
with heart, bone and great vessels, were excluded manually in the RTP system (figure
8
1).
CT-based GTV definition
The PET temporal resolution is an average of several respiratory cycles. In
contrast to the helical CT, the temporal resolution of averaged CT (ACT) is
comparable with PET. Furthermore, Chi et al. demonstrated respiration artifacts in
PET from PET/CT can be minimized with ACT, and ACT was temporally and
spatially consistent with the PET [23] . On the basis of axial ACT images, contouring
of the tumor volume and critical structures was performed without knowing PET
results in an effort to reduce bias. The information of tumor extent from the contrast
CT scan, panendoscopy and endoscopic ultrasonography (EUS) were used when
delineating the GTVCT. Excluding the adjacent metastatic lymph nodes, the volume of
primary tumors (GTVCT) was contoured as a reference tumor volume. To reduce
inter-observer variations, at least 2 different radiation oncologists carried out the
contouring of the tumors for each patient.
Conformality index and volume ratio comparison
After the completion of the GTVCT contouring in RTP system, the radiation
oncologists reviewed the consistency of PET/CT images with nuclear medicine
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physicians. The volume of GTVCT and GTVPET was compared by conformality index
[1] and volume ratio (VR). CI is the ratio of the volume of intersection of two
volumes (A∩B) compared with the volume of union of the two volumes (A∪B)
under comparison [ CI =
A B
][22, 24]. VR is the ratio of two volumes, and the
A B
denominator is the volume of GTVCT. A suitable threshold level could be defined
when GTVPET was observed to be the best fitness of the length, CI or VR from the
GTVCT.
Statistical analysis
All statistical test were performed using the SPSS 15 (SPSS Chicago,IL), each
GTVs were analyzed by one-way ANOVA test with the post hoc test by scheffe
method, and a P-values ≦0.05 were considered statistically significant. Pearson
correlation was performed to assess the correlation of tumor length of the GTVCT with
that of the GTVPET.
Results
Of the 18 patients, automatic co-registrations of 4D-PET/CT were successful in 13
tumors from 12 patients. In 6 patients, the fused images were not available for the
analysis. One had small T1 tumor which could not be detected by PET scan. A
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SUVmax was 2.96 in another patient with T1 lesion, and he was not suitable for
further analysis. Because of different table positions between 4D-PET and 4D-CT,
fusion failure occurred in the first patient enrolled this study. The other two patients
were excluded due to irregular respiration rhythms, which caused failure in image
fusion. One patient was also excluded, because of diffuse lung and bone metastatic
status. Autocontouring function for GTVPET was insufficient for primary GTV
delineation. Table 1 summarizes the characteristics of the 13 patients. The histological
type for all the patients was squamous cell carcinoma. The median age were 48.5
(range, 38-76). Eleven lesions (85%) were T3 and T4 stage. Endoscopic ultrasound
(EUS) was performed for 9 patients (75%). The mean length of GTVCT was 5.73 ±
2.40cm (range, 1.75-10.01cm). The mean volume of GTVCT was 29.41 ± 19.14mL
(range, 3.65-70.76 mL). The mean SUVmax was 13.26 ± 2. 78 (range, 9.4-16.9).
Figure 2 shows the results of the mean tumor lengths on CT (CT
mean tumor length by different SUV thresholds (PET
length).
length)
and the
Figure 3 illustrates the
correlation of CT length compared with PET length at SUV2.5, SUV 20% and SUV25%.
The decision coefficient (R2) of tumor length difference at the threshold levels of
SUV2.5, SUV20% and SUV25% were 0.79, 0.65 and 0.54, respectively. The mean
VR ranged from 0.30 to 1.48 (0.86±0.24) (F = 29.34, P < 0.001). Mean VR at
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different SUV threshold levels are shown in Figure 4. The VR values gradually
decreased from SUV15% to SUV50%. The best fitness for VR was found at SUV
20% (mean SUV 2.65 ± 0.56) and SUV 2.5, and achieved the most optimal VR value
0.98 ± 0.24 and 0.98 ± 0.26, respectively. The VR at SUV40% (0.41 ± 0.14) or
SUV50% (0.30 ± 0.12) were not an ideal threshold level for GTV contouring of
esophageal cancer. The mean CIs ranged from 0.29 to 0.58 (F = 11.34, P < 0.001).
Mean CI at different SUV threshold levels are shown in Figure 5. The best fitness for
CI was at SUV 20% (0.58 ± 0.10) or SUV 2.5 (0.57 ± 0.13).
Discussion
This work was a pilot study to investigate the feasibility of 4D-PET/CT when
contouring the GTV for EC. By comparing eight interested threshold levels, the result
showed the GTVPET using a threshold setting of SUV 20% or SUV 2.5 correlated well
with tumor length, VR and CI of the GTVCT. The result was compatible with previous
studies which investigated the optimal contouring threshold by using non-respiratory
controlled PET or PET/CT [6, 8, 16, 22]. Zhong et al. presented the FDG GTVPET at
SUV2.5 provided the closest estimation of gross tumor length in EC [16]. Han et al.
reported a study of combined
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F-flurorothymidine (FLT) and FDG PET/CT in
assessing the feasibility of GTV delineation in EC and found a threshold setting of
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SUV1.4 on FLT PET/CT or SUV2.5 on FDG PET/CT was correlated well with the
pathologic GTV length [8]. When using a threshold level of SUV 40%, the PET-based
tumor length was obviously underestimated to the pathologic length [8, 16]. Similarly,
based on the result of our study, a threshold setting with SUV ≧ 30 % is not
adequate for the autocontouring.
To optimize the GTV contouring for EC, panendoscopy, EUS and CT images
were usually used for the information regarding the precise tumor location and
volume. Nonetheless, panendoscope and EUS cannot pass through the obstructive
lumen in locally advanced tumors. In this situation, the actual location regarding distal
margin of tumor should be interpreted by CT image only. However, the precise tumor
length and extent are not always discernible because the mucosa or submucosa lesions
might not be visualized by CT scan. Konski et al. reported that EUS finding
correlated well with PET-based tumor length than that with CT scans in a series of 25
patients [6]. The International Atomic Energy Agency expert group promised
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F-FDG PET/CT provides the best available imaging for accurate target delineation
in RT planning [25]. With the implementation of PET/CT, the risk of geographic miss,
underdosing and normal tissue complication probability might be reduced [10].
Certainly, the use of FDG-PET/CT for GTV delineation for RT planning should be
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validated based on loco-regional control and survival in the future [26].
Four-dimensional CT in target volume delineation and motion were well studied
in non-small-cell lung cancer, including fractionationated radiotherapy and
stereotactic radiotherapy [18, 19], but there was a paucity in investigating esophageal
motility during RT. Dieleman et al. reported a retrospective study of analyzing 29
patients with nonesophageal cancer, mostly stage 1 lung cancer, using 4D-CT [27].
They suggested that distal esophagus had the largest motion margins with 9 mm in
medio-lateral direction and 8 mm in dorso-ventral direction. PET is generally
performed in the free breathing status without breath-hold or respiratory gating
techniques, so PET is an average image obtained during several respiratory cycles.
Therefore, FDG quantification, tumor margin definition and smaller tumor detection
can be improved with the application of respiratory gating or 4D-PET [1, 28]. Chi et
al. demonstrated respiration artifacts in PET from PET/CT could be minimized with
ACT, and ACT was temporally and spatially consistent with the PET [23]. Based on
this concept, we assumed that the GTV contouring using an average phase of images
on 4D-CT would minimize the impact of tumor motion when they were fused with the
PET.
Several studies have explored the use of a fixed or adaptive threshold setting for
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accurate tumor dimensions in thoracic cancer [8, 12, 22], but no study reported
comprehensive parameters, including the VR, CI and tumor length when compared to
the GTVCT. Probably, it might be attributed to the complexity of organ motion and
uncertainty of image registration. Hanna et al. investigated the impact of PET/CT
simulation for GTV definition in non-small-cell lung cancer (NSCLC) by using the
concordance index (equivalent to CI in our study) [29]. The mean concordance index
of their study was 0.64 and 0.57 in GTVPET-CT and GTVCT, respectively. This
indicated a significant reduction in inter-observer variation by adding PET in GTV
delineation. In EC study, Vali et al. compared a short long segment of esophageal the
GTVPET and GTV
CT and EUS
of EC at the level of the tumor epicenter and found a
threshold setting of SUV2.5 and SUVL4σ ( equal to SUV2.4) resulted in the highest CI
value (0.48 and o.47, respectively) [22]. Gondi et al. demonstrated the values CI of
NSCLC and EC with the incorporation of FEG-PET and CT were 0.44 and 0.46,
respectively [24]. To the best of our knowledge, this is the first study that compared
the CI value between the GTVPET and GTV
CT using
4D PET/CT in contouring EC
and using whole tumor volume. Our results were similar to the studies mentioned
above. The CIs of our study implied approximately 75% overlapping in the two
volumes. The CI levels of SUV40% or 50% were inferior to to the other thresholds,
and were not ideal for autocontouring of the GTVPET. Furthermore, the VR was close
15
to 1 at SUV 20% or SUV 2.5, it was better than the other studies of partial VR of EC
[22] and the VR of NSCLC[12]. When using smaller cutoff values, such as SUV2 or
SUV 15% in threshold setting, more adjacent normal tissue would be included within
the GTVPET. Thus, primitive values of CI or VR were changed and became better
when some artifacts were corrected. But, this manual procedures were very time
-consuming.
Our result should be interpreted with two limitations. First, the study was based on
the comparison of the GTVCT and GTV
PET
without knowing the pathologic
information about the tumor length, axial extent, and real volume. Certainly, the
biological volume could not be definitely related to the real tumor volume. Similarly,
the GTVCT could identify areas without the tumor tissue. Because of the popularity of
using neoadjuvant or definitive CCRT in treating EC [3, 30], it seems difficult to
perform a direct pathologic comparison from the surgical specimen. Second, it is not
flawless that the averaged phase of 4D-CT images fused with the averaged PETs was
used to delineate the GTVs. This approach might provide more accurate functional
images supplemental to CT without increasing the clinical overwork during
contouring; however, the actual impact of tumor motion from maximum intensity
projection should be investigated further. In addition, lower resolution of PET images
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than CT images might limit the results of this study.
Conclusion
This study demonstrated that 4D-PET/CT is applicable when contouring the GTV
in radiation planning for esophageal cancer. The use of threshold levels of SUV 20%
or SUV 2.5 achieves the optimal correlation with tumor length, VR and CI. To assess
final treatment outcome, the benefits of RT planning using 4D-PET/CT need more
clinical investigations.
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