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Diseases of the Esophagus (2017) 0, 1–7
DOI: 10.1093/dote/dox121
Original Article
Prediction of pathologic responders to neoadjuvant chemoradiotherapy by
diffusion-weighted magnetic resonance imaging in locally advanced esophageal
squamous cell carcinoma: a prospective study
Q.-W. Li,1,† B. Qiu,1,† B. Wang,1 D.-L. Wang,2 S.-H. Yin,2 H. Yang,3 J.-L. Liu,4 J.-H. Fu,3 M.-Z. Liu,1
C.-M. Xie,2,‡ H. Liu1,∗
1
2
3
4
Departments of Radiation Oncology, Departments of Medical Imaging, Thoracic Oncology, and Medical
Oncology, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer
Medicine, Sun Yat-sen University Cancer Center Guangzhou, Guangdong, China
SUMMARY. This study aims to investigate the role of diffusion-weighted magnetic resonance imaging (DWMRI) in ESCC patients receiving neoadjuvant concurrent chemoradiotherapy (CCRT), and the efficacy of apparent
diffusion coefficient (ADC) values in predicting pathologic response to neoadjuvant CCRT. Twenty-eight locally
advanced ESCC patients treated with neoadjuvant CCRT followed by radical resection were prospectively enrolled.
DW-MRI was recommended to be performed within 2 weeks before and 4–6 weeks after neoadjuvant CCRT.
The calculated ADCs pre- (ADC1) and post- (ADC2) neoadjuvant CCRT, the definite (ADC) and percentage
changes (ADC%) were analyzed for the efficacy of predicting pathologic response to neoadjuvant CCRT. Twenty
patients had been identified as responders (tumor regression grade 1–2). Among them, ADC2 (3.02 ± 0.84 vs.
2.12 ± 0.44 × 10−3 mm2 /s, P = 0.001) and ADC (1.22 ± 0.78 vs 0.64 ± 0.26 × 10−3 mm2 /s, P = 0.007) were
significantly higher than those of nonresponders (tumor regression grade: 3–5). Receiver operating characteristic
analysis revealed that ADC2 exhibited an overall accuracy of in 71.4% in predicting pathologic response, with a
sensitivity of 60.0%, a specificity of 100%, a positive predictive value of 100%, and a negative predictive value of
50.0%, when 3.04 × 10−3 mm2 /s was used as the cutoff value. ADC value could be useful in predicting pathologic
response to neoadjuvant CCRT in ESCC patients. High postneoadjuvant CCRT ADC is a predictive indicator for
good response.
KEY WORDS: apparent diffusion coefficient, esophageal squamous cell carcinoma, neoadjuvant chemoradiotherapy, tumor regression grade.
INTRODUCTION
Neoadjuvant concurrent chemoradiotherapy (CCRT)
is currently regarded as a standard treatment option
∗ Address
correspondence to: Hui Liu, MD, PhD, Department of
Radiation Oncology, Sun Yat-sen University Cancer Center, No.
651 Dongfeng Road East, Guangzhou 510060, China.
Email: liuhui@sysucc.org.cn
† Dr. Qi-Wen Li and Dr. Bo Qiu contributed equally to this work.
‡ Dr. Chuan-Miao Xie was the co-corresponding author.
Specific author contributions: QWL and BQ analyzed and
interpreted data, as well as drafted the article. DLW and SHY
contributed in data acquisition, image analysis, and manuscript
revision. BW, HY, JLL, JFH, MZL, CMX participated in data
acquisition, data interpretation, and revised the manuscript. HL
designed the study, interpreted data and revised the article. All
authors gave final approval of the version to be submitted and
agreed to be accountable for all aspects of the work in ensuring
that questions related to the accuracy or integrity of any part of
the work are appropriately investigated and resolved.
for locally advanced esophageal cancer, yielding a
greater chance of locoregional control and longer
overall survival compared with surgery alone.1,2 However, response to neoadjuvant CCRT varies among
individuals. It was reported that 29% of surgical specimen were completely free of tumor cells in pathologic
examination.3 Forty-two percent of patients obtained
tumor regression grade (TRG) 1–2, recognized as
pathologic complete remission (pCR) or almost-pCR,
while approximately half were found of poor response
(TRG 3–5).4
The relationship between pathologic response and
long-term prognosis has been widely investigated.
Pathological CR is becoming a marker of favored survival and provided potential chance of omission of
surgery.5 On the contrary, nonresponders are under
the risk of disease progression, delayed resection,
and unnecessary exposure to CCRT toxicities.6,7 It
C The Authors 2017. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus.
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
1
2 Diseases of the Esophagus
is important to discriminate responders from nonresponders at an early stage, for the sake of individualizing the following treatments.
Conflicting results have appeared when current
modalities are assessed for response evaluation or
prediction. Computed tomography (CT) and endoscopic ultrasonography (EUS) are routinely adopted
but often suspected of difficulties in distinguishing
residual tumor from fibrosis, tumor necrosis, or
post-CCRT edema.8–9 18 fluorine-2-deoxy-D-glucose
positron emission tomography-computed tomography (18 F-FDG PET/CT) also showed insufficient
accuracy of only around 44%, along with the criticisms of high cost and radiation exposure.10 In contrast, diffusion-weighted magnetic resonance imaging
(DW-MRI), a functional MR technique, allows a
noninvasive way for assessing tumor cellularity quantitatively. The results are measured quantitatively by
apparent diffusion coefficient (ADC), a parameter
measuring the degree of restriction to diffusion of
water protons within tissues in a certain volume.11
The indicative value of ADC on tumor response has
been verified under several circumstances.12–15 In
our previous study, the addition of DW-MRI to CT
and endoscopy overwhelmed traditional modalities
in response assessment for locally advanced ESCC
treated by definitive chemoradiotherapy.16 Although
a few studies have investigate the utility of DW-MRI
in the neoadjuvant chemotherapy of esophageal
cancer or gastro-oesophageal cancer,17,18 we focused
our study on esophageal squamous cell carcinoma,
and assess the predictive effect of DW-MRI in this
radiosensitive pathologic subtype.
The primary goal of this study is to investigate the
role of DW-MRI-based ADC, both before and after
neoadjuvant CCRT, in the prediction of pathologic
response to neoadjuvant CCRT in ESCC.
therapy, and without distant metastasis. Patients with
contraindications for MRI, chemoradiotherapy, or
surgery were excluded. Comprehensive work-ups
consisting of contrast-enhanced CT of chest and
abdomen, EUS and barium esophagram were performed at diagnosis for clinical staging. The staging
procedure was based on American Joint Committee
on Cancer 2009 standard.
MATERIALS AND METHODS
DW-MRI and imaging analysis
Ethics, consent, and permissions
All patients underwent two series of DW-MRI scanning, recommended within 2 weeks before and 4–6
weeks after neoadjuvant CCRT. A 1.5-T MR imaging
unit (GE signaHDx 1.5T, General Electric, Milwaukee, WI, USA) with eight-channel phased array
body coil was used. All patients were scanned in
supine position and trained for shallow slow breath
before the examination. Respiratory and electrocardiographically gated T2-weighted fast spin echo
images were obtained. Parameters included repetition
time (TR) 8500 ms, echo time (TE) 85 ms, thickness 5
mm, spacing 1 mm, field of view (FOV) 40 cm, matrix
320 × 224, incentive times (NEX) 1.00. Esophageal
sagittal T2-weighted scans were adopted using the fast
spin echo sequence with the following parameters: TR
5400 ms, TE 85 ms, thickness 3 mm, spacing 1mm,
FOV 40 cm, matrix 320 × 224, NEX 1.00.
This study was in accordance with the ethical
standards of Helsinki Declaration, reviewed, and
approved by the Ethic Committee of Sun Yat-sen
University Cancer Center. Written informed consent
was obtained from each participant. All records were
anonymized and deidentified before analysis.
Study population
Twenty-eight consecutive patients pathologically
diagnosed with locally advanced ESCC and hospitalized in our institution from November 2012 to
May 2016 were prospectively enrolled. The following
criteria were met: patients were ≥18 of age, without
previous history of any malignancy or anticancer
Neoadjuvant chemoradiotherapy
Radiation of 40–44 Gy/20 fractions/4 weeks, planned
and delivered by three-dimensional conformal
radiotherapy, intensity modulated radiotherapy, or
volumetric modulated arc therapy technique was
administrated. The gross tumor volume (GTV) covered primary tumor and suspected metastatic lymph
nodes determined by pretreatment examinations. The
clinical target volume (CTV) included: 3 cm expansion of GTV to craniocaudal boundaries and 5 mm
towards other directions, and area of regional lymph
nodes. Planning target volume (PTV) was created
from CTV by adding a uniform margin of 6 mm. One
of the two regimens was selected for concomitant
chemotherapy: 2 cycles of vinorelbine ditartrate (25
mg/m2 , d 1, d 8, d 22, d 29) and cisplatin (25 mg/m2 ,
d 1–4 and d 22–25); or weekly docetaxel (25 mg/m2 , d
1, d 8, d 15, d 22) and cisplatin (25 mg/m2 , d 1, d 8, d
15, d 22). Radical surgery was performed 4–8 weeks
following the completion of neoadjuvant CCRT. The
en bloc resection with two-field lymphadenectomy
was performed, consisting of esophagectomy through
right-sided posterolateral thoracotomy, gastric tube
mobilization through midline laparotomy and anastomosis through left-side cervical incision. Alimentary
tract reconstruction was achieved by a retrosternal or
posterior mediastinal route.
Response prediction in esophageal cancer 3
Table 1
Baseline clinicopathologic characteristics and their predictive effects
Characteristics
Sex
Male
Female
Age (Mean ± SD)
Length on pretreatment MRI (Mean ± SD)
Location
Proximal third
Middle third
Distal third
Gastroesophageal junction
Differentiation
Low
Middle
High
Missing
cT
cT2
cT3–4
cN
cN0–1
cN2–3
Stage
II
III
Dose
44 Gy
40 Gy
Radiation technique
3D-CRT
IMRT/VMAT
Chemotherapy
docetaxel + platinum
vinorelbine + platinum
All patients
Responders
Nonresponders
p
25
3
56.86 ± 6.47
47.11 ± 16.04
18
2
57.85 ± 6.12
43.43 ± 15.47
7
1
54.38 ± 7.09
56.30 ± 14.4
>0.99
4
16
7
1
3
11
5
1
1
5
2
0
0.92
6
15
1
6
4
11
1
4
2
4
0
2
0.91
6
22
6
14
0
8
0.14
20
8
16
4
4
4
0.17
4
24
4
16
0
8
0.30
12
16
9
11
3
5
>0.99
12
16
7
13
5
3
0.23
12
16
8
12
4
4
0.69
0.21
0.053
Values of continuous variables are presented as means ± standard deviation (SD). ADC, apparent diffusion coefficient; 3D-CRT, threedimensional conformal radiotherapy; IMRT, intensity modulated radiotherapy; TRG, tumor regression grade; MRI, magnetic resonance
imaging; VMAT, volumetric modulated arc therapy.
DW-MRI were then obtained by a respiratory gated
single-shot echo-planar imaging sequence and array
spatial sensitivity encoding technique, with b values of
0 and 700 s/mm2 (TR 7500 ms, TE 70 ms, thickness
5 mm, spacing 1 mm, FOV 40 cm, matrix size
128 × 128, NEX 4.00).
All original DW-MRIs were transferred to a Workstation (AW4.4; GE Healthcare, Milwaukee, Wis) and
processed by Functool workstation, in order to create
ADC maps. Two experienced radiologists who were
blinded to clinical data were responsible for the interpretation of pictures. The lesion location was determined on the T2-weighted images. The lesion length
was measured on sagittal T2-weighted images with
a caliper tool. Meanwhile, T2-weighted images were
used as a slice selection reference for ADC value
assessment. DW-MRI reconstructed images were furtherly evaluated for image analysis. An axial slice
showing the most predominant tumor size corresponding to T2-weighted images was selected. Region
of interest (ROI) was contoured manually encompassing the entire essence of tumor displayed on the
ADC map, excluding areas of necrotic, cystic, or hemorrhagic change. In case no residual tumor could
be differentiated on the ADC map, the ROI was
delineated according to the apparent tumor bed. The
average ADC was extracted from the ADC map from
the ROI, labeled as ADC1 (preneoadjuvant CCRT)
and ADC2 (post neoadjuvant CCRT). The other
parameters were calculated as follows:
ADC = ADC2 − ADC1
ADC% = ADC/ADC1
Response evaluation
An experienced pathologist, who was blinded to the
DW-MRI data, evaluated the pathologic response
based on TRG classification system:4 TRG 1, complete disappearance of tumor cells; TRG 2, rare
residual tumor cells scattering throughout the fibrosis;
TRG 3, an increased number of residual tumor cells
outgrown by fibrostic tissue; TRG 4, residual cancer
outgrowing fibrotic tissue; and TRG 5, no regressive signs. Patients were then divided into two groups,
responders (TRG 1–2) and nonresponders (TRG 3–5),
for statistical analysis.
4 Diseases of the Esophagus
Table 2 ADCs and their predictive effects
ADC (Mean ± SD)
ADC1 (× 10−3 mm2 /s)
ADC2 (× 10−3 mm2 /s)
ADC (× 10−3 mm2 /s)
ADC% (%)
All patients
Responders
Nonresponders
p
1.72 ± 0.44
2.77 ± 0.85
1.05 ± 0.72
64.17 ± 46.44
1.81 ± 0.41
3.02 ± 0.84
1.22 ± 0.78
71.25 ± 51.39
1.48 ± 0.44
2.12 ± 0.44
0.64 ± 0.26
46.49 ± 25.52
0.077
0.001
0.007
0.10
ADC, Apparent diffusion coefficient.
Statistical methods
Compared t-test was performed to assess the change
of ADC pre- and postneoadjuvant CCRT. T-test of
independent sampler was conducted to evaluate the
association between ADCs and TRG classifications.
ADC values significantly correlated with TRG were
furtherly processed by receiver operating characteristic (ROC) analysis to calculate the best cutoff values.
Sensitivity, specificity, positive predictive value (PPV),
and negative predictive value (NPV) were calculated
and reported. Comparisons of continuous and categorical clinic-pathologic factors were achieved by
t-test and Fisher’s exact test, respectively. A statistically significant difference was identified when pvalue <0.05 (two-sided). All tests were performed
using SPSS 16.0, except for ROC analysis, which was
performed by MedCalc software 10.1.6.0.
RESULTS
Baseline clinicopathologic characteristics and their
statistical association with TRG were detailed in
Table 1. The median interval was 35 (range: 12–53)
days between the end of neoadjuvant CCRT and the
time of postneoadjuvant CCRT DW-MRI, and 48.5
(range: 37–72) days between the end of neoadjuvant
CCRT and surgery. Fifteen patients were identified as
TRG 1 (pCR), 5 as TRG 2, 4 as TRG 3, 3 as TRG 4 and
1 as TRG 5 in pathologic evaluation, or 20 (73.9%) as
responders and 8 (26.1%) as nonresponders.
As detailed in Table 2, the mean value of
ADC increased significantly after neoadjuvant CCRT
(1.72 ± 0.44 vs 2.77 ± 0.85 × 10−3 mm2 /s, P < 0.0001),
and this trend was consistent among each participant,
with 1.05 ± 0.72 × 10−3 mm2 /s as mean ADC and
64.17 ± 46.44% as ADC%.
ADC1 was significantly inversely associated with
clinical stage (2.13 ± 0.37 × 10−3 mm2 /s in stage II
vs 1.65 ± 0.41 × 10−3 mm2 /s in stage III, P = 0.035).
ADC2 (3.02 ± 0.84 vs 2.12 ± 0.44 × 10−3 mm2 /s,
P = 0.001, Fig. 1) and ADC (1.22 ± 0.78 vs
0.64 ± 0.26 × 10−3 mm2 /s, P = 0.007) were significantly higher in patients with a good response
compared with nonresponders. ADC1 advocated a marginally significant increase in responders (1.81 ± 0.41 vs 1.48 ± 0.44 × 10−3 mm2 /s,
Fig. 1 ADC2 values in responders and nonresponders. ADC2
was significantly higher in patients with a good response compared
with non-responders (3.02 ± 0.84 vs. 2.12 ± 0.44 × 10−3 mm2 /s,
P = 0.001). ADC, apparent diffusion coefficient.
P = 0.077), while neither ADC% (71.25 ± 51.39 vs
46.49 ± 25.52%, P = 0.21) nor other baseline clinicopathologic characteristics was statistically associated
with pathologic endpoint (Table 1). Typical DW-MRI
images for different tumor responses are presented in
Fig. 2.
ROC analysis was performed to determine the best
cutoff value for prediction of pathologic response.
With an area under curve (AUC) of 0.791, ADC2
exhibited a sensitivity of 60.0%, a specificity of 100%,
a PPV of 100%, a NPV of 50.0% and an overall accuracy of 71.4%, when 3.04 × 10−3 mm2 /s was used as
the cutoff value. The absence of statistical significance
precluded ROC analysis for other ADC values.
DISCUSSIONS
Our study investigated the role of DW-MRI-based
ADC values and its dynamic change in predicting
early pathologic response to neoadjuvant CCRT
in ESCC. Generally, neoadjuvant CCRT has been
regarded as the standard therapy of locally advanced
ESCC. In the era of precision medicine, early and
accurate predictive markers for therapeutic response
are highly desirable. Though efforts has been made
on searching for clinical, molecular as well as radiological indicators, such as microRNA19 or PET/CT,10
none of them satisfactorily strikes a balance among
Response prediction in esophageal cancer 5
Fig. 2 Typical magnetic resonance imaging pictures of responder and nonresponder. In a patient diagnosed with cT2N2 esophageal squamous cell carcinoma who obtained good pathologic response (TRG = 1), the mean ADC increased from 1.58 to 3.22 × 10−3 mm2 /s after
neoadjuvant concurrent chemoradiotherapy (CCRT). T2-weighted, DW-MRI images and ADC maps with contoured regions of interest,
before (a, b, c) and after (d, e, f) neoadjuvant CCRT were shown. In another case, staged cT3N1 identified with poor response (TRG = 5),
the mean ADC did not change obviously during neoadjuvant CCRT (from 1.37 to 1.94 × 10−3 mm2 /s).T2-weighted, DW-MRI images
and ADC maps before (g, h, i) and after (j, k, l) CCRT were presented. ADC, apparent diffusion coefficient; DW-MRI, diffusion-weighted
magnetic resonance imaging; TRG, tumor regression grade.
6 Diseases of the Esophagus
accuracy, harmlessness and convenience. Thus, ADC
in DW-MRI was investigated in our study as a potential predictor of therapeutic response to neoadjuvant
CCRT.
In this study, 73.9% of patients were pathologically determined as responders, with 65.2% confirmed
as pCR. The promising results might be related to
the pathological type (squamous cell carcinoma),20
higher fractionated dose (44 Gy/20 fractions), sufficient chemotherapy and relatively longer interval
between neoadjuvant CCRT and surgical intervention
(mostly 6–8 weeks). Elevated ADC implied the change
of characteristics of tumor cells and stroma, including
loss of tumor cell membrane integrity, loss of stroma
and angiogenesis, tumor apoptosis and necrosis,21
In our previous study, ADC value > 2.64 × 10−3
mm2 /s has become an additional criteria to CT and
endoscopy, which significantly improved the accuracy
of response assessment in ESCC patients treated by
CCRT.16 In this study, ADCs had been identified as
the response predictor as well. ADC2 > 3.04 × 10−3
mm2 /s was in a strong relation to good response, with
overall accuracy of 71.4% and specificity of 100%.
Similarly, De Cobelli et al. analyzed post-CCRT ADC
with ROC curves, suggesting 1.84 × 10−3 mm2 /s as a
favorable cut-off value.17 Another peer study included
patients receiving definitive CCRT and radiological
response assessment. When post-CCRT ADC was
higher than 2.6 × 10−3 mm2 /s, not only a favored
complete remission rate (81.1% vs 45.9%), but also
an increased overall survival (2-year overall survival:
81.5% vs 16.9%) were identified.22 The various cutoff
values suggested by different studies called for several considerations. First, the measurement of ADC2
relied primarily on method of ROI delineation. The
contouring of residual tumor on DW-MRI was sometimes confusing, especially when the tumor disappeared completely on the image. In that case, the contouring of tumor bed was applied instead. Second, the
postneoadjuvant CCRT ADC value might be dependent on the interval between the end of neoadjuvant
CCRT and the time of postneoadjuvant CCRT DWMRI.18 In our study, the median interval was 35 days,
which was comparable with that in van Rossums’
study and longer than that in De Cobelli’s.17,18 The
most appropriate timing of second DW-MRI remains
to be investigated.
The predictive value of initial ADC was marginally
significant in our study but varied among previous
researches. According to Aoyagi et al., both radiological response and long-term survival were significantly
better in patients with initially higher ADC, which
was explained by the correlating increasing expression
of vascular endothelial growth factor (VEGF) protein.15,21 In contrast, some researchers documented
the opposite, yet with majority of participants diagnosed with gastric cancer and mostly consisted of
adenocarcinoma.17 Another study focusing on definitive CCRT denied any statistical association between
pre-treatment ADC and clinical outcomes.22 Therefore, the instability of predictive effect of ADC1 suggested the influence of heterogeneous study population, various adopted b-values and neoadjuvant
CCRT protocols. Investigations with larger sample
size are required for further explanation.
ADC revealed its potential in response prediction, though less accurate than ADC2 in our
study. The incompetence of prediction by ADC%
was also noticed. It seemed that tumor regression was better reflected by postneoadjuvant CCRT
DW-MRI directly, regardless of initial tumor status.
Interestingly, in spite of contradictory results about
ADC%,17,18 some suggested the increased rate of
ADC early during CCRT, i.e. two weeks after treatment start, as an important indicator.18,23 It could
be explained by the fact that incomplete pathologic
response at early time-point might facilitate accurate
contouring of residual tumor and increased the reliability of picture interpretation.
ADC1 in stage II patients was found significantly
higher than those of stage III in the current study.
According to Van Rossum et al., a similar inverse association was noticed between T stage and initial ADC,
which implied stratification of stage might be considered in the design of on-going studies. Besides, initial ADC was found to be higher in esophageal adenocarcinomas and poorly differentiated tumors, compared with squamous cell carcinomas and moderately
differentiated tumors.18 Although the potential utility
of ADC in squamous cell carcinoma and adenocarcinoma was demonstrated separately,17 subdivision of
clinic-pathologic characteristics in future researches
will reduce the complexity in interpretation of results.
Growing interest has emerged in the use metabolic
imaging techniques, such as PET/CT, in the assessment and prediction for tumor response. Although
PET/CT and DW-MRI have not been compared
directly, DW-MRI is known as a noninvasive method
of apparent insensitivity to inflammation, with no
exposure to radiation, no injection of contrast agent,
short examination duration, and less cost. The measurement of ADC, no matter by manual or by semiautomated volumetric methods, presented with satisfactory interobserver reproducibility.24 The selection
of imaging techniques and the optimal way to combine them is still an open question.
Small sample size limited us from validating the
results and cut-off points. Intervals between neoadjuvant CCRT and surgery covered a wide range in
this study, inferring potential confounding factors.
Another interesting research topic for future investigation is whether ADC remains its effectiveness in predicting progression-free survival or overall survival,
which requires long-term follow-up.
Response prediction in esophageal cancer 7
CONCLUSIONS
In conclusion, this study showed that ADC postneoadjuvant CCRT, and the change of ADC after
neoadjuvant treatment, were potential predictors
of pathologic response in ESCC. Postneoadjuvant
CCRT ADC showed remarkable accuracy in prediction of good response. Further prospective studies
with larger sample size, homogenous population, and
controlled procedures are required for validation.
10
11
12
13
ACKNOWLEDGMENTS
14
This work was supported by Medical Scientific
Research Foundation of Guangdong Province, China
[Grant Number A2015120].
We appreciate the assistance of Mr. Zhan Yihang
for figure preparation.
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