© 2004 Foundation for Promotion of Cancer Research
Technical Note |
Diffusion-weighted Single Shot Echo Planar Imaging of Colorectal Cancer Using a Sensitivity-encoding Technique
1 National Cancer Center Hospital East, Department of Radiology, Kashiwa, Chiba and 2 National Cancer Center Hospital, Department of Radiology, Tokyo, Japan
For reprints and all correspondence: Katsuhiro Nasu, National Cancer Center Hospital East, Department of Radiology, 6-5-1 Kashiwanoha, Kashiwa, Chiba 277-8577, Japan. E-mail: kanasu{at}east.ncc.go.jp
Received January 26, 2004; accepted July 11, 2004
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Abstract |
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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.
Methods: Forty-two patients with sigmoid colon cancer and rectal cancer, all proven pathologically, 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 pathological 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 (x10–3) 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
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INTRODUCTION |
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TOPAbstractINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONReferences |
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Diffusion-weighted imaging (DWI) is in wide use in the field of neuroradiology (1–3). Nowadays, DWI is performed by the following method. Motion-probing gradient (MPG) pulses are placed before and after a 180° RF pulse, which comprises the spin echo method along with a 90° pulse. The k-space is then filled with the spin echo signal and continuous gradient echoes that are generated by echo planar imaging (EPI) (4). This method can shorten the total image acquisition time to a few dozens of seconds, making DWI applicable in clinical scenarios. On the other hand, there have been few reports of DWI being applied to the abdomen (5–7). This is for two reasons: the first is that the images are greatly distorted, especially at the surface of body and around the air in the lungs and bowel tract because of susceptibility artifact. The second reason is that chemical shift artifacts cause severe misregistration of fat tissue; this makes it impossible to gain accurate positional information from the abdomen, where fat tissue is far more plentiful than it is in the head (8,9).
A parallel imaging technique, represented by sensitivity encoding (SENSE), a recent development of magnetic resonance imaging (MRI), can both shorten image acquisition time and reduce the peculiar artifacts of EPI caused by susceptibility and chemical shifts, since it can reduce the number of phase-encoding steps (10,11). Accordingly, with DWI using SENSE (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.
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SUBJECTS AND METHODS |
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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 measured 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 differentiated adenocarcinoma consisted of two mucinous adenocarcinomas 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, intramuscular 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 workstation (Easyvision, release 4.4) was also used. The imaging sequences were T2-weighted turbo spin echo [T2-TSE: repetition time (TR)/echo time (TE) = 3656/90 ms, echo train length (ETL) = 13, matrix size = 512 x 211, field of view (FOV) = 30 x 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, matrix size = 256 x 77, FOV = 30 x 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 suppression). 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 acquisition, 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-factor values of 250 and 500 s/mm2 were also obtained in 10 randomly selected cases (nine males and one female, hereinafter 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 workstation 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 hyperintensely 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 misregistration of the tumors was recorded if it was observed in fusion images. It was noted to what extent these misregistrations 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 classification 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.
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RESULTS |
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TOPAbstractINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONReferences |
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On DWI-I/1000, all tumors were clearly depicted as hyperintense areas, with the normal colon wall and feces hypointense in all cases (Table 1, Figs 1 and 2).
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The tumors were always depicted on T2-TSE and T2-EPI; however, it was often difficult to identify the tumors intuitively because the contrast between the tumor and the normal rectal wall was often poor. On the other hand, in the investigation of the 10 cases in which DWI-I/250 and DWI-I/500 were obtained, the contrast between the tumor and normal rectal 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 hyperintense regions (Table 2).
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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 information 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. However, 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 x 10–3 mm2/s with an SD of 0.1 x 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 (x10–3) mm2/s. This result closely agreed with previously reported ADC values for cerebrospinal fluid (16).
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DISCUSSION |
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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 seen between the tumor and normal colon wall. Unless this issue is resolved, it will be difficult to apply this technique for examining colorectal cancer, as it is inferior to computed tomography (CT) scanning in terms of both spatial resolution and time resolution.
Various efforts have been made to resolve this problem. For example, the use of an endorectal coil (17,18) or an enema of contrast material (19,20) has been attempted. The former method can provide a high signal-to-noise ratio in the local site, and can also depict the zonal structure of the bowel wall. Consequently, it is also very useful for T-staging. Nevertheless, the visible range achieved by this method is extremely narrow. The endorectal coil cannot evaluate the extent to which large tumors grow into surrounding organs, although it can be used for tumors near the anus. Some authors have reported the usefulness of a surface coil installed at the tip of an endoscope, although such a specialized device is unlikely to be used widely in the near future (21).
As for the latter method, use of an air enema or superparamagnetic Ferristene contrast agent has been reported. In particular, the usefulness of a double contrast approach using intravenous administration of Gd-DTPA plus an enema of superparamagnetic Ferristene is of interest (20,21). However, this method requires almost the same degree of preparation as barium enema and endoscopy. We can easily predict problems likely to arise, such as the heavy burden patients would bear in order for the examination to be performed, if this intricate procedure were to be carried out in a clinical environment.
In our method, we used a synergy body coil, with the result that no bowel preparation was necessary at all. Therefore, our technique was non-invasive and completely different from the methods mentioned above. SENSE-DWI was able to depict tumors hyperintensely, while the normal colon wall and feces were always depicted hypointensely. Consequently, no additional imaging methods were needed to make a diagnosis of the presence of a tumor. It is impossible to carry out T-staging with SENSE-DWI alone because its spatial resolution and its image quality were still very low. Therefore, it is of crucial importance 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 identified 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 recognize 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 hyperintensely. 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 hyperintensity for the same reason.
The high ADC values of the poorly differentiated adenocarcinomas 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 adenocarcinomas.
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 that this method directly reflects the cellularity of tumors suggests the possibility that this method can be used not only for tumor detection but also for evaluating the effects of radiotherapy 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. 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 physiological 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 diagnosis 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 provide entirely new information which conventional diagnostic radiology has never yielded.
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Acknowledgments |
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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 Control. 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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