DOI:10.2214/AJR.05.0559
AJR 2006; 187:1280-1287
© American Roentgen Ray Society
Potential of Surface-Coil MRI for Staging of Esophageal Cancer
Angela M. Riddell1,
Julia Hillier2,
Gina Brown1,
D. Michael King1,
Andrew C. Wotherspoon3,
Jeremy N. Thompson4,
David Cunningham5 and
William H. Allum4
1 Department of Diagnostic Radiology, The Royal Marsden Hospital, Downs Road,
Sutton, Surrey, London, United Kingdom, SM2 5PT.
2 Department of Radiology, The Chelsea and Westminster Hospital, London, United
Kingdom.
3 Department of Histopathology, The Royal Marsden Hospital, London, United
Kingdom.
4 Department of Surgery, The Royal Marsden Hospital, London, United
Kingdom.
5 Department of Medical Oncology, The Royal Marsden Hospital, London, United
Kingdom.
Received March 30, 2005;
accepted after revision June 13, 2005.
Address correspondence to A. M. Riddell
(Angela.Riddell{at}rmh.nhs.uk).
Abstract
OBJECTIVE. The aim of this pilot study was to assess the feasibility
of external surfacecoil MRI as a new method of imaging the esophagus and
esophageal cancer.
CONCLUSION. The results for the 10 patients investigated indicate
that by using a high-resolution axial T2-weighted sequence (small field of
view, thin section images), MRI provides detailed imaging of the anatomic
layers of the esophageal wall and tumor. Three independent radiologists found
good correlation in the morphologic appearance and extent of tumor between MRI
and matched histology sections. This study illustrates the potential of the
technique as an alternative form of local staging for esophageal cancer.
Keywords: CT • esophageal cancer • esophagus • MRI • oncologic imaging • surface-coil MRI
Introduction
Esophageal cancer is the eighth most common cancer worldwide
[1]. In the West,
adenocarcinoma is now the predominate form of esophageal cancer, having
recently surpassed the incidence of esophageal squamous cell carcinoma
[2]. Surgical resection remains
the only curative treatment for adenocarcinoma of the esophagus but carries
significant morbidity and mortality. It is essential for imaging to accurately
identify patients with localized, resectable disease.
Locoregional staging is currently undertaken by CT and endoscopic
sonography. The latter is more accurate than CT in determining T stage, with
rates between 60% and 80% depending on tumor stage and operator experience
[3,
4]. However, endoscopic
sonography examinations may be limited by tightly stenosed tumors and
differentiation of ulcer-associated inflammation from infiltration
[5,
6]. The transducers used are
high frequency (7.5-12 MHz) to maximize resolution, but have a restricted
sonographic range, limiting visualization of structures that are deep to the
tumor. This limits determination of tumor-free surgical resection planes.
To date, MRI has not been used for locoregional staging. An early study
[7] comparing conventional CT
and 0.35-T MRI found MRI to have lower accuracy for staging esophageal tumors
than CT, although a more recent study
[8] concluded that MRI and CT
had similar accuracy in predicting resectability of tumors in patients with
esophageal cancer. However, because CT also provides information regarding
distant metastatic disease and is more widely available, it has remained the
technique of choice. Technical challenges have to be overcome when using MRI
for esophageal imaging—the deep location of the esophagus and the degree
of movement related to cardiac motion, peristalsis, and respiration, combined
with the relatively slow acquisition time of MRI, conspire to degrade image
quality. Recent research has focused mainly on endoluminal MRI because
reducing the distance between the coil and the esophagus increases the
signal-to-noise ratio, improving image quality. However, limited in vivo and
ex vivo studies are available on endoluminal MRI esophageal imaging. Analysis
of the optimal sequence indicates that T2-weighted images provide the best
delineation of the layers of the esophageal wall
[9-12].
To our knowledge, the use of an external surface coil to acquire
high-resolution images of the esophagus has not previously been described.
The aim of this pilot study was to establish whether MRI of esophageal
cancer is feasible using an externally placed surface coil. We also evaluated
the ability of the technique to depict normal esophageal wall and
periesophageal planes and to clearly delineate tumor by correlation with
histopathology of the resected specimen.
Materials and Methods
Ten patients with confirmed esophageal carcinoma (seven with
adenocarcinoma, two with squamous cell carcinoma, and one with spindle-cell
melanoma), who were deemed medically fit for surgery and shown to have
resectable disease using endoscopic sonography and CT, underwent
high-resolution MRI of their primary tumors on the day before surgery. The
study group contained 7 men and 3 women with median age of 60 years (range,
47-82 years). Nine patients had preoperative combination chemotherapy, and one
patient with spindle cell melanoma underwent primary surgery. Nine patients
underwent esophagogastrectomy, and one underwent total gastrectomy and
esophagogastrectomy with a colonic interposition. The resections were
performed by two surgeons with 16 and 17 years experience in esophageal
surgery.
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Fig. 1A —61-year-old man with squamous cell carcinoma of esophagus.
High-resolution axial images show normal esophagus (arrow).
Esophageal wall layers cannot be defined on T1-weighted image (A),
whereas corresponding T2-weighted image (B) clearly shows individual
layers.
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Fig. 1B —61-year-old man with squamous cell carcinoma of esophagus.
High-resolution axial images show normal esophagus (arrow).
Esophageal wall layers cannot be defined on T1-weighted image (A),
whereas corresponding T2-weighted image (B) clearly shows individual
layers.
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Ethics approval was obtained from the local research ethics committee.
Informed, written consent was obtained from each patient.
MRI Technique
Images were acquired using a 1.5-T system (Intera, Philips Medical
Systems). T1-weighted and T2-weighted images were evaluated. The four-element
Philips Medical Systems sensitivity-encoding (SENSE) phased-array body coil
was used for tumors of the lower third of the esophagus and gastroesophageal
junction (seven patients); for tumors of the middle third (three patients),
elements 1 and 2 of phased-array Synergy Spine Coil (Philips Medical Systems)
were used. This minimized the distance between the esophagus and the receiver
coil, maximizing the signal-to-noise ratio. The patients were positioned
supine, and the body coil was placed over the lower thorax with two elements
anterior and two posterior. Initially, a T2-weighted sagittal sequence was
acquired to localize the tumor and to plan 3-mm axial images perpendicular to
the long axis of the tumor.
Axial sequence parameters for T1-weighted images were as follows: TR/TE,
643/15; field of view, 225; matrix, 200/512; number of signal averages (NSA),
6; turbo spin-echo (TSE) factor, 31. The parameters for T2-weighted images
were: 6,000/120; field of view 225; matrix, 208/512; NSA, 6; TSE factor, 31.
The in-plane resolution for the T2-weighted sequence was 225/208 x
225/512 (1.08 x 0.44), giving a voxel volume of (1.08 x 0.44
x 3) 1.42 mm3 and for the T1-weighted sequence of 1.48
mm3, thus producing high-resolution images.
A saturation band was placed over the heart, but no cardiac or respiratory
gating was used.
MRI Analysis
Three radiologists, who were aware that the patients were considered
eligible for surgical resection but were blinded to the endoscopic sonography,
CT, and histology reports, independently reviewed the MR images on a
workstation (Merge eFilm Workstation 1.9.3, eMed). The images were magnified
to the same extent as the corresponding histology section to improve
measurement accuracy. The radiologists had 3, 10, and 26 years of
cross-sectional imaging experience.
Feasibility of MRI
The following were noted for each patient: whether the scan was tolerated,
scan duration, and image quality. Image quality was graded by two interpreters
as good (3), moderate (2), or poor (1) for the following parameters:
visualization of the esophageal wall and its component layers, visualization
of the lumen, and depiction of periesophageal tissues and adjacent
structures.
MRI Tumor Assessment
Morphology—Tumor signal intensity, location (mucosal,
submucosal, muscularis propria), and position were noted.
Measurements—Normal esophageal wall, tumor thickness, and
depth of extramural disease were measured.
Histology section orientation and matching with MR
images—Each surgical specimen was fixed by total immersion in
buffered formalin, and the lumen was distended with formalin. The
circumferential (surgical) resection margin was inked to enable anatomic
orientation. The specimen was sectioned transversely at intervals of 5-6 mm,
giving sections corresponding with the MR images (each alternate image).
Whole-mount glass slides were prepared and stained with H and E.
One interpreter oriented the slides in conjunction with the
histopathologist and matched the histology slides with the corresponding MR
image. The documented level of the tumor and morphologic appearance of the
esophagus were used for matching. The interpreter remained blinded to the
exact location and extent of the tumor and final histologic stage. To reduce
the impact of any potential unblinding, the interpreter allowed 1 month
between matching and recording the study data.
In total for the 10 patients, 50 histology slides with matched MR images
were used for recording data.
Histologic analysis—The slides were digitally scanned
(Expression 1680 Professional, Seiko Epson). The computerized histology
sections were magnified to three times their original size, and measurements
identical to those for the MR images were taken. Histologic sections matched
with an MR image that showed no macroscopic abnormality were reviewed by the
pathologist to establish the extent of the microscopic abnormality.
Statistical Analysis
Bland-Altman plots were used to compare the agreement between measurements
of normal wall thickness and tumor thickness. This statistical method allowed
comparison of a new measurement technique (MRI) with an established one
(histology) and assessment of the extent by which the techniques differ
[13]. The same method was
applied to assess interobserver variability by analyzing the repeatability of
measurements among different interpreters. In this case, the value for 2 SDs
from the mean represented the coefficient of repeatability.
When a discrepancy greater than ± 2 mm from the mean difference
occurred between MRI and histology for two or more interpreters, the images
were reviewed to establish the cause of the discrepancy.
Results
MRI Analysis
Feasibility of MRI—All 10 patients tolerated the scan. The
mean axial T2-weighted sequence time was 6.89 ± 1.19 minutes. The mean
overall scanning time was 15.74 ± 2.50 minutes.
MRI sequence evaluation—The T1-weighted images were graded
as poor. Layers of the esophageal wall were not clearly delineated, tumors
could not be identified separate from the surrounding wall, and visualization
of periesophageal tissues was poor (Figs.
1A and
1B). As a result, after the
first two patients were scanned, only the T2-weighted sequence was run. The
T2-weighted sequence provided clear delineation of normal structures.
Visualization of the esophageal wall layers was good in four patients and
moderate in five. Visualization of the periesophageal tissues was good in four
patients and moderate in six. The results are shown in
Table 1.
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Fig. 2A —47-year-old woman with adenocarcinoma of lower esophagus.
Axial T2-weighted image (A) shows normal esophageal wall layers.
Low-signal-intensity mucosa (white arrow) is surrounded by
higher-signal submucosa (arrowhead) and low-signal-intensity
muscularis propria (black arrow).
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Fig. 3A —59-year-old man with adenocarcinoma of lower esophagus.
T2-weighted image shows intermediate-signal-intensity tumor involving right
side of esophageal wall (arrow). Tumor replaces high-signal-intensity
submucosa and infiltrates into muscularis propria. Involved lymph node is seen
just anterior to aorta (arrowhead). Normal esophageal wall layers are
preserved on left side.
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Fig. 3B —59-year-old man with adenocarcinoma of lower esophagus.
Histology slide matching image in A confirms tumor involving submucosa
and muscularis on right side (arrow) and replacing periesophageal
lymph node (arrowhead).
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Fig. 4A —Bland-Altman scatterplots show mean difference between MRI
and histology for esophageal wall and tumor thickness. The mean difference for
interpreter 1 (A) was 0.54 mm (2 SDs ± 8.37 mm); for interpreter
2 (B) was 0.86 mm (2 SDs ± 7.06 mm); and for interpreter 3
(C) was 1.01 mm (2 SDs ± 8.22 mm). Value for 2 SDs provides 95%
CI in each case, which determines limits of agreement for scatterplots. Path =
histology.
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Fig. 4B —Bland-Altman scatterplots show mean difference between MRI
and histology for esophageal wall and tumor thickness. The mean difference for
interpreter 1 (A) was 0.54 mm (2 SDs ± 8.37 mm); for interpreter
2 (B) was 0.86 mm (2 SDs ± 7.06 mm); and for interpreter 3
(C) was 1.01 mm (2 SDs ± 8.22 mm). Value for 2 SDs provides 95%
CI in each case, which determines limits of agreement for scatterplots. Path =
histology.
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Fig. 4C —Bland-Altman scatterplots show mean difference between MRI
and histology for esophageal wall and tumor thickness. The mean difference for
interpreter 1 (A) was 0.54 mm (2 SDs ± 8.37 mm); for interpreter
2 (B) was 0.86 mm (2 SDs ± 7.06 mm); and for interpreter 3
(C) was 1.01 mm (2 SDs ± 8.22 mm). Value for 2 SDs provides 95%
CI in each case, which determines limits of agreement for scatterplots. Path =
histology.
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Fig. 5A —Bland-Altman scatterplots show good correlation between
interpreters, particularly for measurements less than 5 mm. Mean difference
between interpreters 1 and 2 (A) was 0.30 mm (2 SDs ± 5.63 mm).
For interpreters 2 and 3 (B), mean difference was 0.20 mm (2 SDs
± 6.3 mm). For interpreters 1 and 3 (C), mean difference was
0.47 mm (2 SDs ± 7.19 mm). Value for 2 SDs from mean represents
coefficient of repeatability.
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Fig. 5B —Bland-Altman scatterplots show good correlation between
interpreters, particularly for measurements less than 5 mm. Mean difference
between interpreters 1 and 2 (A) was 0.30 mm (2 SDs ± 5.63 mm).
For interpreters 2 and 3 (B), mean difference was 0.20 mm (2 SDs
± 6.3 mm). For interpreters 1 and 3 (C), mean difference was
0.47 mm (2 SDs ± 7.19 mm). Value for 2 SDs from mean represents
coefficient of repeatability.
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Fig. 5C —Bland-Altman scatterplots show good correlation between
interpreters, particularly for measurements less than 5 mm. Mean difference
between interpreters 1 and 2 (A) was 0.30 mm (2 SDs ± 5.63 mm).
For interpreters 2 and 3 (B), mean difference was 0.20 mm (2 SDs
± 6.3 mm). For interpreters 1 and 3 (C), mean difference was
0.47 mm (2 SDs ± 7.19 mm). Value for 2 SDs from mean represents
coefficient of repeatability.
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All interpreters identified signal abnormality on T2-weighted images that
corresponded to the site of macroscopic disease pathologically in eight
patients. The other two patients had only microscopic foci of disease
histologically. Four of the six patients with extramural extension of disease
were predicted with MRI, with no false-positive results
(Table 1).
Tumor Assessment
MRI signal characteristics—Normal mucosa had intermediate
signal intensity surrounded by high-signal-intensity submucosa and
low-signal-intensity muscularis propria (Figs.
2A and
2B). Macroscopic tumor returned
intermediate signal intensity in seven patients (Figs.
3A and
3B). For all these patients,
MRI indicated that the tumor extended into the muscularis propria. This was
confirmed histologically in all patients.
In addition, for one patient macroscopic tumor had high signal intensity,
and the corresponding histology revealed mucinous adenocarcinoma. For another
patient, no abnormality was identifiable on MRI, and histology only showed
microscopic tumor foci. A polypoidal region at the gastroesophageal junction
in a third patient was interpreted on MRI as macroscopic disease, but
histology showed microscopic submucosal tumor only
(Table 1).
Correlation with histology—In total, 50 MR images were
obtained and matched with histologic slides from the resected specimens.
Abnormal intermediate signal intensity identified on T2-weighted MR images
(and interpreted as tumor) corresponded to macroscopic tumor pathologically
for 13 (26%) of the 50 images and to fibrotic change with microscopic foci of
residual tumor for 28 (56%) of them. No demonstrable abnormality was seen on
nine MR images (9/50, 18%). The corresponding histology for these nine images
showed microscopic foci of tumor (6/9), no tumor (2/9), and widespread
submucosal infiltration with mucinous adenocarcinoma (1/9).
The Bland-Altman scatterplots for the three interpreters (Figs.
4A,
4B, and
4C) show the degree of
agreement among individual interpreters and histology for measurements of
normal esophageal wall and tumor thickness. The plots show better agreement
occurred at distances less than 5 mm.
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Fig. 6A —78-year-old man with mucinous gastroesophageal junction
tumor. High-resolution T2-weighted image (A) shows
high-signal-intensity submucosa (arrowhead), interpreted as
submucosal edema by all three interpreters; however, corresponding histology
(B) reveals mucinous adenocarcinoma. On MRI, muscularis propria appears
thinned on right side because of invasion of tumor (arrow). This
misinterpretation accounted for four of seven images where MRI measurement
underestimated tumor thickness.
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Fig. 6B —78-year-old man with mucinous gastroesophageal junction
tumor. High-resolution T2-weighted image (A) shows
high-signal-intensity submucosa (arrowhead), interpreted as
submucosal edema by all three interpreters; however, corresponding histology
(B) reveals mucinous adenocarcinoma. On MRI, muscularis propria appears
thinned on right side because of invasion of tumor (arrow). This
misinterpretation accounted for four of seven images where MRI measurement
underestimated tumor thickness.
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Bland-Altman scatterplots (Figs.
5A,
5B, and
5C) for repeatability of
measurements among the three interpreters show good correlation between
interpreters 1 and 2 with the mean difference between these interpreters being
0.30 mm (2 SDs ± 5.63).
Analysis of the discrepancies (> ± 2 mm for two or more
interpreters) between MRI and pathology measurements of tumor thickness showed
underestimation on seven MR images and overestimation on 20 images. Two of the
most frequent causes are described and illustrated in Figures
6A,
6B,
7A, and
7B. In addition to the
illustrated examples, underestimation resulted from poor visualization of the
tumor (two images), and overestimation resulted from inclusion of normal
signal wall in the measurement of tumor depth (six images).
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Fig. 7A —78-year-old woman with bulky tumor. Tumor-narrowing lumen
(arrow) makes accurate measurement of single wall thickness difficult
on MRI (A). Tumor, however, does not invade muscularis
(arrowhead). Corresponding histology (B) confirms extensive
intraluminal tumor-narrowing lumen (arrow) and normal surrounding
muscularis propria (arrowhead). Five of 20 overestimations of tumor
thickness were because of this difficulty.
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Fig. 7B —78-year-old woman with bulky tumor. Tumor-narrowing lumen
(arrow) makes accurate measurement of single wall thickness difficult
on MRI (A). Tumor, however, does not invade muscularis
(arrowhead). Corresponding histology (B) confirms extensive
intraluminal tumor-narrowing lumen (arrow) and normal surrounding
muscularis propria (arrowhead). Five of 20 overestimations of tumor
thickness were because of this difficulty.
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Discussion
The study shows that surface-coil MRI of the esophagus is feasible and,
when using a T2-weighted sequence, that the esophageal wall layers are
accurately depicted and the tumor can be identified separately from
surrounding tissue. The results regarding the optimum sequence concur with the
in vitro studies performed by Yamada et al.
[12,
14]. We chose not to use
respiratory or cardiac gating in an attempt to minimize scanning time, which
undoubtedly impaired the quality of images obtained. Further work is needed to
assess whether this is a satisfactory compromise. We acknowledge that the use
of oral and IV contrast media and multiplanar imaging also require
investigation to maximize the potential of this technique.
Statistical analysis of the study is limited by the small sample size and
the fact that individual patients contributed an average of five of the total
50 images analyzed in the study. Interpretation errors were therefore carried
over between the images, exaggerating their impact overall. The appearance of
the mucinous tumor, for example, was misinterpreted by all three interpreters,
and measurements of tumor depth were underestimated on four MR images as, in
each case, high signal intensity within the submucosa was considered to be
edema rather than tumor. The measurements taken by the interpreters were at
the interface with the unaffected esophageal wall rather than at the maximal
extent of the tumor. Overestimation of disease occurred in tumors at the
gastroesophageal junction because of the obliquity of the sections. This will
undoubtedly remain a difficult area to image, as it is for endoscopic
sonography. Further work using tangential MR images at the gastroesophageal
junction may provide more accurate assessment of these tumors.
Tumor filling in the esophageal lumen resulted in inaccuracies in tumor
measurement because it was difficult to accurately measure the single wall
thickness. In reality, it is the mural and, in particular, the extramural
component of the tumor that is important for staging and assessment of
resectability, and these distances are likely to be more accurately
measured.
The discrepancies between interpreters 1 and 2 were essentially for
distances greater than 5 mm. At short distances, more important for tumor
staging, the correlation between the interpreters was good. Interpreter 3 had
26 years of cross-sectional imaging experience, but had limited previous
experience in gastrointestinal MRI, which might explain the wider coefficient
of repeatability for interpreter 3 and illustrates that a learning curve is
associated with image interpretation.
We acknowledge a limitation within the study design involving interpreter
2, who potentially could have been unblinded by the process of matching the MR
images with histology. All attempts were made to prevent this, as explained in
the methodology. The results indicate that unblinding is unlikely to have
occurred because results from this interpreter were similar to the other
two.
Specific correlation with pathologic T staging is required to reinforce the
potential of this imaging technique. However, this study has shown that
external surface-coil MRI of the esophagus is technically feasible and enables
detailed imaging of the esophageal wall, delineation of tumor, and depiction
of the surrounding periesophageal tissues.
Acknowledgments
The authors thank Cheryl Richardson and Erica Scurr for their expertise in
the development of the MRI technique. We also thank Andrew Norman for his
advice regarding the statistical analysis of the study data, Ian Chau for his
contribution to the patient treatment protocol that incorporated the MRI study
and for his recruitment of patients, and finally Sally Legge for her
assistance in the recruitment of patients to the study.
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Abstract
Introduction
