Jpn J Clin Oncol 2004;34(10)620–626

doi:10.1093/jjco/hyh108

Technical Note

Diffusion-weighted Single Shot Echo Planar Imaging of Colorectal

Cancer Using a Sensitivity-encoding Technique
Katsuhiro Nasu1, Yoshihumi Kuroki1, Seiko Kuroki2, Koji Murakami1, Shigeru Nawano1 and Noriyuki Moriyama2
1
National Cancer Center Hospital East, Department of Radiology, Kashiwa, Chiba and 2National Cancer Center
Hospital, Department of Radiology, Tokyo, Japan
Received January 26, 2004; accepted July 11, 2004

Background: We wanted to determine the feasibility of diffusion-weighted single shot echo planar
imaging using a sensitivity-encoding technique (SENSE-DWI) in depicting colorectal cancer.

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Methods: Forty-two patients with sigmoid colon cancer and rectal cancer, all proven patholo-
gically, were examined on T2-turbo spin echo (TSE) and SENSE-DWI. No bowel preparation was
performed before examination. The b-factors used in SENSE-DWI were zero and 1000 s/mm2. In
10 randomly selected cases, the images whose b-factors were 250 and 500 s/mm2 were also
obtained. The reduction factor of SENSE was 2.0 in all sequences. Two radiologists evaluated the
obtained images from the viewpoints of tumor detectability, image distortion and misregistration
of the tumors. The apparent diffusion coefficients (ADCs) of the tumors and urine in the urinary
bladders in each patient were measured to evaluate the correlation between ADC and patholo-
gical classification of each tumor.
Results: All tumors were depicted hyperintensely on SENSE-DWI. Even though single shot echo
planar imaging (EPI) was used, the image distortion and misregistration was quite pronounced
because of simultaneous use of SENSE. On SENSE-DWI whose b-factor was 1000 s/mm2, the
normal colon wall and feces were always hypointense and easily differentiated from the tumors.
The mean ADC value of each tumor was 1.02 – 0.1 (·10 3) mm2/s. No overt correlation can be
pointed out between ADC and pathological classification of each tumor.
Conclusion: SENSE-DWI is a feasible method for depicting colorectal cancer. SENSE-DWI
provides strong contrast among colorectal cancers, normal rectal wall and feces.

Key words: rectal cancer – diffusion-weighted images – echo planar imaging – sensitivity
encoding – apparent diffusion coefficient

INTRODUCTION clinical scenarios. On the other hand, there have been few
reports of DWI being applied to the abdomen (5–7). This is
Diffusion-weighted imaging (DWI) is in wide use in the field
for two reasons: the first is that the images are greatly distorted,
of neuroradiology (1–3). Nowadays, DWI is performed by
especially at the surface of body and around the air in the lungs
the following method. Motion-probing gradient (MPG) pulses
and bowel tract because of susceptibility artifact. The second
are placed before and after a 180 RF pulse, which com-
reason is that chemical shift artifacts cause severe misregistra-
prises the spin echo method along with a 90 pulse. The
tion of fat tissue; this makes it impossible to gain accurate
k-space is then filled with the spin echo signal and continuous
positional information from the abdomen, where fat tissue is
gradient echoes that are generated by echo planar imaging
far more plentiful than it is in the head (8,9).
(EPI) (4). This method can shorten the total image acquisition
A parallel imaging technique, represented by sensitivity
time to a few dozens of seconds, making DWI applicable in
encoding (SENSE), a recent development of magnetic reson-
ance imaging (MRI), can both shorten image acquisition time
and reduce the peculiar artifacts of EPI caused by susceptibility
For reprints and all correspondence: Katsuhiro Nasu, National Cancer Center and chemical shifts, since it can reduce the number of phase-
Hospital East, Department of Radiology, 6-5-1 Kashiwanoha, Kashiwa,
Chiba 277-8577, Japan. E-mail: kanasu@east.ncc.go.jp
encoding steps (10,11). Accordingly, with DWI using SENSE

# 2004 Foundation for Promotion of Cancer Research


(SENSE-DWI), image distortion theoretically can be improved.
Bammer et al. have reported the usefulness of SENSE-DWI in
the diagnosis of brain infarction (12). They stated that SENSE-
DWI could provide finer images than conventional DWI, as
would be expected theoretically. However, the usefulness of
this technique will become truly apparent when applied to
abdominal imaging where artifacts significantly worsen
image quality.
In this report, we present the interesting results of applying
SENSE-DWI to depict colorectal cancer.
SUBJECTS AND METHODS
PATIENT POPULATION
The patient group consisted of 42 cases in which sigmoid colon
cancer and/or rectal cancer had been diagnosed. It comprised
35 males and seven females, ranging in age from 38 to 78 years
(mean 63.4). The locations of their tumors were sigmoid colon
in two, in the upper third of the rectum in eight cases, in the
middle third of the rectum in 13 cases and in the lower third of
the rectum in 19 cases. The pathological diagnosis of each
tumor was established by means of histological specimens
excised during resection. Detailed investigation of histological
specimens revealed that, according to the UICC classification,
the study group included one pT1, five pT2, 33 pT3 and three
pT4 tumors. The maximum diameter of each tumor, as meas-
ured after removal, ranged from 1.5 to 10 cm (mean 5.8).
Pathological investigation also revealed that this study
group included 15 well-differentiated adenocarcinomas, 24
moderately differentiated adenocarcinomas and three poorly
differentiated adenocarcinomas. The three cases of poorly dif-
ferentiated adenocarcinoma consisted of two mucinous adeno-
carcinomas and one signet ring cell adenocarcinoma.
Conditions set before examination were 6 h of fasting with
no restriction on drinking water and normal oral administration
of regularly used drugs. No bowel preparation was carried out
in any of the patients. Just before the examination, intramus-
cular or intravenous injection of 20 mg of butyl scopolamine
bromide was given to all the patients. Oxygen was supplied
during the examination. Informed consent was obtained from
all patients before examination.
IMAGING PROTOCOLS
The MRI apparatuses we used were a Gyroscan Intera 1.5 T
and a synergy body coil (Philips Medical, Best and Heeren,
The Netherlands). The apparatuses and sequences used in this
study were normally purchased from the manufacturer as
Release 8.1. All are commercially available products. A work-
station (Easyvision, release 4.4) was also used. The imaging
sequences were T2-weighted turbo spin echo [T2-TSE: repeti-
tion time (TR)/echo time (TE) = 3656/90 ms, echo train length
(ETL) = 13, matrix size = 512 · 211, field of view (FOV) =
30 · 21 cm, number of excitations = 1, slice thickness/gap =
6 mm/1 mm, 16 sagittal slices] and diffusion-weighted single
shot echo planar imaging (SENSE-DWI: TR/TE = 2750/95,
Jpn J Clin Oncol 2004;34(10) 621
matrix size = 256 · 77, FOV = 30 · 30 cm, half scan
factor = 0.693, number of excitations = 1, slice thickness/
gap = 6 mm/1 mm, 16 sagittal slices, spectral presaturation
with inverse recovery (SPIR) pulse was used for fat suppres-
sion). The reduction factor for SENSE was 2.0 in both
sequences, and the acquisition time of each sequence was
22 and 16 s, respectively. The phase encode direction was
set antero-posteriorly in both sequences. The b-factor values
of SENSE-DWI were set at zero and 1000 s/mm2. The MPG
pulses were placed in the x-, y- and z-axes. At image acquisi-
tion, no cardiac triggering was used in SENSE-DWI. The
images obtained in SENSE-DWI were as follows: (i) images
whose b-factors were zero (hereinafter T2-EPI); (ii) images in
which the MPG pulse (b = 1000) was placed in each direction
(hereinafter DWI-X, DWI-Y and DWI-Z); and (iii) isotropic
images which were synthesized from DWI-X, DWI-Y and
DWI-Z (hereinafter DWI-I/1000). Isotropic images with b-
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factor values of 250 and 500 s/mm2 were also obtained in
10 randomly selected cases (nine males and one female, here-
inafter DWI-I/250 and DWI-I/500, respectively). All patients
held their breath while the images were being acquired.
IMAGING ANALYSIS
The visual evaluation was performed on each of the above-
mentioned images and on the fusion images, which were
synthesized from T2-TSE and DWI-I/1000 using the work-
station by simply pasting high intensity areas extracted from
SENSE-DWI onto T2-TSE. Two radiologists carried out the
visual evaluation of the following items in consultation with
each other. (i) It was recorded whether the appearance of the
tumors, normal rectal wall and feces were depicted hyperin-
tensely or not on DWI-I/1000. (ii) The changes in imaging
findings attributable to different b-factor values were recorded
in the 10 cases in which DWI-I/250 and DWI-I/500 were
obtained. (iii) The anisotropy of each tumor was evaluated
after all the findings using DWI-I/1000 had been compared
with those using DWI-X, DWI-Y and DWI-Z. (iv) The mis-
registration of the tumors was recorded if it was observed in
fusion images. It was noted to what extent these misregistra-
tions interfered with the interpretation of our images.
The apparent diffusion coefficient (ADC) value was also
calculated for each tumor from T2-EPI and DWI-I/1000.
The correlation between ADC value and pathological classi-
fication of each tumor was then evaluated. The ADC value of
urine was also calculated as reference data for each patient.
ADC values of the normal colorectal wall should have been
measured but, in reality, it was impossible to create reliable
regions of interest in the normal colorectal wall on DWI-I/1000
or ADC maps.
RESULTS
On DWI-I/1000, all tumors were clearly depicted as hyperin-
tense areas, with the normal colon wall and feces hypointense
in all cases (Table 1, Figs 1 and 2).
622 Diffusion-weighted single shot echo planar imaging of colorectal cancer

Table 1. Results of tumor depiction on SENSE-DWI (DWI-I/1000) The tumors were always depicted on T2-TSE and T2-EPI;
however, it was often difficult to identify the tumors intuitively
Colorectal cancer Normal colon wall Feces because the contrast between the tumor and the normal rectal
High 42 0 0 wall was often poor. On the other hand, in the investigation
Low 0 42 42 of the 10 cases in which DWI-I/250 and DWI-I/500 were
obtained, the contrast between the tumor and normal rectal

A B

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C D

Figure 1. A 63-year-old male with rectal cancer in the middle third of the rectum. (A) A T2-TSE image shows thickening in the anterior wall of the rectum. However,
the contrast between the tumor and the normal rectal wall is low. (B) On DWI-I/1000, the tumor is clearly depicted hyperintensely in the surrounding structure. This
image reveals that the tumor involves not only the anterior wall but also the posterior wall. The small intestine, prostate, seminal vesicles and testes are also observed
hyperintensely. However, the normal rectal wall and feces are hypointense. (C) The fusion image reveals no misregistration in the tumor between T2-TSE and DWI-I/
1000. Slight misregistration is observed in the testes. (D) Barium enema. The tumor depicted on DWI-I/1000 closely agrees with that obtained on barium enema.
(E) Change in image quality as a function of b-factor value. On T2-EPI (left), the tumor shows a moderately high signal. However, it is difficult to differentiate the
tumor from the normal rectal wall. For DWI-I/250 (center), the signal of the tumor becomes more prominent than the normal rectal wall. However, it is difficult to
identify the lower end of the tumor because the internal sphincter is still bright and difficult to differentiate from the tumor. On DWI-I/500 (left), the tumor is more
clearly observed and the normal rectal wall is less prominent. However, as compared with the barium enema (D), DWI-I/1000 (B) more accurately depicts the extent of
the tumor than DWI-I/500. (F) Change in image quality as a function of MPG direction. The presented images are DWI-X, DWI-Y and DWI-Z from left to right. Slight
differences are observed among these images; however, no obvious anisotropy can be seen in the tumor.
 Jpn J Clin Oncol 2004;34(10) 623

A B

C D

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Figure 2. A 72-year-old male with rectal cancer in the lower third of the rectum to the anal canal. (A) On T2-TSE, the tumor is depicted in the lower end of the
rectum to the anal canal. However, it is difficult to identify the tumor intuitively in this image. Notice that the rectal lumen contains a large volume of feces. (B) On
DWI-I/1000, the tumor is clearly depicted hyperintensely and can be easily differentiated from the normal rectal wall and feces. (C) On the fusion image, slight
misregistration is observed in the tumor. However, it does not impede practical image interpretation. This is assumed to occur because the gas present in the
feces enhances susceptibility, which in turn causes misregistration. (D) Barium enema. The tumor depicted on DWI-I/1000 closely agrees with that obtained on
barium enema.

wall became clearer and hyperintensely depicted objects
became fewer in number with gradually increasing b-factor
value; finally, at a b-factor value of 1000 s/mm2, only the
tumors and a few structures such as small intestine, prostate,
seminal vesicles, testes and endometrium remained as hyper-
intense regions (Table 2).
Comparing DWI-I/1000 with DWI-X, DWI-Y and DWI-Z,
no overt differences were observed among these images.
Accordingly, the tumors were assumed not to have any obvious
anisotropy (Fig. 1f ).
The outline of the body was always observed as a slight
signal increase. On fusion images, slight distortion was
observed in the surface of the bodies including the testes;
however, it was always possible to grasp the anatomical infor-
mation at least roughly. The misregistration of the tumor
between DWI-I/1000 and T2-TSE occurred in four cases
(Fig. 2). Nevertheless, the grade of misregistration was so
slight that we experienced no difficulty in interpreting the
images. In all of the four misregistration cases, the bowel tracts
contained relatively large quantities of gas or feces, which
we concluded enhanced susceptibility to misregistration. How-
ever, in other cases in which gas collection was observed, no
misregistration occurred. These observations suggested that
the real cause of misregistration may be more complicated
than we thought.
No overt artifacts due to pulsation of vessels were observed
even though no cardiac triggering was used in this study.
Each tumor had a mean ADC value of 1.05 · 10 3 mm2/s
with an SD of 0.1 · 10 3 mm2/s (Fig. 3a). The resultant means
for the tumors of this study showed very little ADC value
scattering. Although no statistical analysis was performed
because we had not collected enough cases, we presumed
there to be no correlation between the ADC value and the
pathological classification of each tumor (Fig. 3b). The
ADC value of the urine in each patient, which was measured
as reference data, was 3.35 – 0.49 (·10 3) mm2/s. This result
closely agreed with previously reported ADC values for cere-
brospinal fluid (16).
DISCUSSION
Up to now, MRI has been used to a limited extent in
the diagnosis of colorectal cancer (13). The usefulness of
MRI for detecting tumor extension of advanced rectal
cancer is clearly established (14,15), but its disadvantage as
an examination tool for colorectal cancer is the poor contrast
624 Diffusion-weighted single shot echo planar imaging of colorectal cancer

Table 2. Correlation between various structures and b-factors seen between the tumor and normal colon wall. Unless this
issue is resolved, it will be difficult to apply this technique for
b=0 b = 250 b = 500 b = 1000 examining colorectal cancer, as it is inferior to computed
Colorectal cancer tomography (CT) scanning in terms of both spatial resolution
High 5 7 8 10 and time resolution.
Moderate 5 3 2 0 Various efforts have been made to resolve this problem. For
Low 0 0 0 0
example, the use of an endorectal coil (17,18) or an enema of
contrast material (19,20) has been attempted. The former
Normal colon wall
method can provide a high signal-to-noise ratio in the local
High 0 0 0 0 site, and can also depict the zonal structure of the bowel wall.
Moderate 10 9 5 0 Consequently, it is also very useful for T-staging. Neverthe-
Low 0 1 5 10 less, the visible range achieved by this method is extremely
Small intestine narrow. The endorectal coil cannot evaluate the extent to
High 3 3 5 7
which large tumors grow into surrounding organs, although
it can be used for tumors near the anus. Some authors have
Moderate 7 7 5 3
reported the usefulness of a surface coil installed at the tip of an
Low 0 0 0 0 endoscope, although such a specialized device is unlikely to be

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Urine used widely in the near future (21).
High 10 5 0 0 As for the latter method, use of an air enema or superpara-
Moderate 0 4 3 0 magnetic Ferristene contrast agent has been reported. In
Low 0 1 7 10
particular, the usefulness of a double contrast approach using
intravenous administration of Gd-DTPA plus an enema of
Prostate
superparamagnetic Ferristene is of interest (20,21). However,
High 9 9 7 6 this method requires almost the same degree of preparation as
Moderate 0 0 2 3 barium enema and endoscopy. We can easily predict problems
Low 0 0 0 0 likely to arise, such as the heavy burden patients would bear in
Seminal vesicle order for the examination to be performed, if this intricate
High 9 9 9 7
procedure were to be carried out in a clinical environment.
In our method, we used a synergy body coil, with the result
Moderate 0 0 0 2
that no bowel preparation was necessary at all. Therefore, our
Low 0 0 0 0 technique was non-invasive and completely different from the
Endometrium methods mentioned above. SENSE-DWI was able to depict
High 1 1 1 1 tumors hyperintensely, while the normal colon wall and feces
Moderate 0 0 0 0 were always depicted hypointensely. Consequently, no addi-
Low 0 0 0 0
tional imaging methods were needed to make a diagnosis of the
presence of a tumor. It is impossible to carry out T-staging with

Figure 3. Results of ADC measurement of the tumors. (A) The ADC values of the tumor and urine. The mean ADC of the tumors is 1.05 – 0.1(·10 3) mm2/s. There is
very little scattering in their ADC value. The ADC value of the urine is 3.35 – 0.49 (·10 3) mm2/s. This agrees with the previously reported ADC value for
cerebrospinal fluid. (B) Correlation between ADC values and pathological grading of each tumor. Although no statistical analysis is performed, since we have not
collected sufficient cases, we assume there to be no correlation between ADC value and pathological classification.

SENSE-DWI alone because its spatial resolution and its image
quality were still very low. Therefore, it is of crucial import-
ance to evaluate T2-TSE for obtaining T-staging. However,
the interpretation with both T2-TSE and SENSE-DWI
will provide us with more accurate T-staging than that with
T2-TSE only, because the location of the tumor can be identi-
fied more easily in the interpretation using SENSE-DWI as
reference images. In addition, fusion images synthesized from
T2-TSE and SENSE-DWI will be able to compensate for
the low spatial resolution characteristic of SENSE-DWI.
The seminal vesicles, prostate and endometrium were never
misinterpreted as rectal cancer when the fusion images were
available for reference.
On SENSE-DWI, although EPI was employed, distortion
was minimal. Misregistration in the tumors, even though it
occurred, was very slight and did not impede interpretation
of the images. These phenomena could be explained by
the fact that the use of SENSE had reduced the filling time
of the k-space by half and had also markedly diminished
susceptibility and chemical shift artifacts. The misregistrations
shown in Figure 2 would not be likely to be encountered in
clinical settings, because any radiologist could easily recog-
nize which area on T2-TSE was equivalent to the high signal
on SENSE-DWI, when these two sequences were interpreted
simultaneously in actual image reading (12,22).
It is difficult to explain precisely why SENSE-DWI can
depict colorectal cancer hyperintensely. However, it was
certain that the tumor delineation was not due to T2-
shinethrough, judging from the comparison between T2-
EPI and DWI-I with various b-factors ranging from 250 to
1000 s/mm2. On T2-EPI, the tumors were hypointense for
urine and isointense with the small intestine in many cases,
although the tumors gained intensity with increasing b-factor.
Eventually, when the b-factor had reached 1000 s/mm2, only
the tumors and a few normal structures were depicted hyper-
intensely. Moreover, the result of comparison among DWI-X,
DWI-Y, DWI-Z and DWI-I/1000 revealed that the tumor did
not have any overt diffusion anisotropy. Therefore, we were
confident that the tumor depiction was due to a decreased
absolute value of diffusion. In past reports on DWI of brain
tumors, the higher cellularity of the brain tumor than that of
the surrounding brain parenchyma was the main reason why
they showed hyperintensity on DWI (23,24). It was highly
likely that SENSE-DWI delineated colorectal cancer hyper-
intensity for the same reason.
The high ADC values of the poorly differentiated adenocar-
cinomas probably assisted this presumption. Two cases out
of three poorly differentiated adenocarcinomas of this study
were mucinous carcinomas and the remaining one was a signet
ring cell carcinoma (25). These tumors contained a lot of
mucin in the extracellular spaces, therefore, their cellularity
was relatively lower than that of well-differentiated adeno-
carcinomas.
SENSE-DWI has markedly high detectability for colorectal
cancer. The detectability using this method is a clear potential
that has never been available before. In other words, the fact
Jpn J Clin Oncol 2004;34(10) 625
that this method directly reflects the cellularity of tumors sug-
gests the possibility that this method can be used not only for
tumor detection but also for evaluating the effects of radio-
therapy and chemotherapy. For example, Galons et al. reported
that breast cancer in in vitro experiments showed a significant
increase in the ADC value within 48 h of administration of
anti-cancer drugs (26). The information revealed in their
report suggests that the ADC value can be taken as a new
index for evaluating chemotherapeutic effects. This method
also has potential for application to differential diagnosis
between post-operative changes and local recurrence in the
pre-sacral space.
Finally, we will discuss the appropriateness of the method
we used in this study. The ADC values of urine, which we
measured in this study, closely agreed with the ADC values for
cerebrospinal fluid, as reported previously (16). These values
were consistent with those for free water in the human body.
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Moreover, the SD of the ADC value of each tumor was
quite small. These data suggest that ADC measurement was
feasible even in the abdominal cavity which was full of phy-
siological motion. Breath-holding and administration of butyl
scopolamine were of course indispensable; however, we
thought that any cardiac gating which was usually used in
ADC measurement was not necessary to perform our method,
because the rectum did not have any pulsating structures such
as large arteries or cerebrospinal fluid surrounding it.
We have described the usefulness of SENSE-DWI for dia-
gnosis of colorectal cancer. Even in DWI using single shot EPI,
sharp images with little distortion were obtained when SENSE
was used simultaneously. On SENSE-DWI, all tumors were
depicted as hyperintense. This method affords not only high
detectability of colorectal cancer, but also a high possibility of
reflecting tumor cellularity. SENSE-DWI is thus likely to pro-
vide entirely new information which conventional diagnostic
radiology has never yielded.
Acknowledgments
The work was supported in part by Grant for Scientific Research
Expenses for Health Labour and Welfare Programs and the
Foundation for the Promotion of Cancer Research, and by
2nd-Term Comprehensive 10-year Strategy for Cancer Con-
trol. The authors thank Makoto Obara, Marc van Cauteren,
Yoshito Kato, Hideyuki Fujikawa and Narumi Akimoto for
their help in performing this study. The authors also thank
Susumu Kataoka for his assistance in producing this manuscript.
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