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DOI:10.2214/AJR.05.1005
AJR 2006; 187:181-184
© American Roentgen Ray Society

Technical Innovation

High-B-Value Diffusion-Weighted MRI in Colorectal Cancer

Tomoaki Ichikawa1, Sukru Mehmet Erturk2,3, Utarou Motosugi1, Hironobu Sou1, Hiroshi Iino4, Tsutomu Araki1 and Hideki Fujii4

1 Department of Radiology, Yamanashi University, Shimokato, Japan.
2 Brigham and Women's Hospital, Harvard Medical School, Radiology Suite, c/o One Brigham Circle, 1620 Tremont St., Boston, MA 02120.
3 Department of Radiology, Sisli Etfal Training and Research Hospital, Istanbul, Turkey.
4 First Department of Surgery, University of Yamanashi, Shimokato, Japan.

Received June 11, 2005; accepted after revision September 13, 2005.

 
Address correspondence to S. M. Erturk (mehmeterturk{at}superonline.com).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this article is to evaluate the usefulness of high-b-value diffusion-weighted MRI (DW-MRI) in the detection of colorectal adenocarcinoma.

CONCLUSION. High-b-value DW-MRI allows detection of colorectal adenocarcinoma with a high sensitivity and specificity.

Keywords: cancer • colon • diffusion-weighted MRI • MRI


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Diffusion-weighted MRI (DW-MRI) is becoming increasingly important in the assessment of malignant tumors [1, 2]. It is generally accepted that DW-MRI enables noninvasive characterization of biologic tissues on the basis of their water diffusion properties [3]; it provides information about the biophysical properties of tissues such as cell organization and density, microstructure, and microcirculation [4]. DW-MRI is widely used in neuroimaging [5], but its application within the abdomen is hindered by the presence of bulk physiologic motion such as respiration, peristalsis, and blood flow, in which orders of magnitude are greater in amplitude than that of diffusion [6].

Takahara et al. [7] proposed a DW-MRI technique that might provide images with improved signal-to-noise ratios (SNRs); reversal of the contrast of these images resulted in black-and-white images with contrast characteristics closely resembling those of PET. We hypothesized that high-b-value DW-MRI images could be directly used for tumor detection because of the different cellular structures of healthy and neoplastic tissues. We decided to study colorectal adenocarcinoma because of the general challenges of colonic MRI, including the nonsolid nature of the organ, peristalsis, and movement of the intraluminal contents. Thus, our aim in this preliminary study was to evaluate the usefulness of high-b-value DW-MRI in the detection of colorectal adenocarcinoma.


Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
During a period of 6 months between August 2004 and February 2005, 33 consecutive patients (mean age, 59; range, 33-69 years; 15 women, 18 men) with 33 endoscopic colonoscopically proven colorectal cancers ranging from 20 to 70 mm (mean, 33 mm) were found in our institution and two related hospitals and were included in this study. The lesions were located in the rectum (n = 14), sigmoid colon (n = 8), transverse colon (n = 2), ascending colon (n = 8), and cecum (n = 1). Another 15 patients who underwent endoscopic colonoscopy during the same period with negative results were included as controls. All patients with colorectal cancer finally underwent surgical resection and the diagnoses were confirmed. Contrastenhanced CT was performed in all patients and negative cases in the control group before MR examinations. Informed consent was obtained from all patients before participation in the study, which was approved by our institutional review board.

MRI Protocol and Parameters
MRI used a combination of a commercially available 1.5-T superconducting MR unit and a body coil (Signa EchoSpeed, GE Healthcare). First, breathhold, coronal T1-weighted MR images with gradient-echo sequences were obtained to confirm the optimal scan range. Then, axial T1-weighted and respiratory-triggered, fast spin-echo T2-weighted MRI (TR/TE, 2,000-4,000/80), and high-b-value DW-MRI were performed in all patients including the control group. The patients did not undergo any preparation such as bowel cleansing before the examinations. High-b-value DW-MR images were obtained without breath-holding during the acquisition. Detailed parameters for high-b-value DW-MRI were sequence: single-shot spin-echo echo-planar (SE-EPI); fat-suppression technique, chemical shift selective technique; scan direction, axial, b value, zero and 1,000 s/mm2; TR/TE/inversion time (TI), 8,000-10,000/73.2-73.4/70; matrix, 128 x 64; slice numbers, 60; slice thickness/gap = 4 mm/0 mm; field of view, 40 cm; number of excitations, 6; acquisition time, approximately 5 minutes. Inversion pulse was used not for fat suppression but for suppression of background signals. The upper abdomen and pelvis were scanned separately. All axial source images were provided with black-and-white reversed-contrast display. Coronal maximum-intensity-projection (MIP) images were reconstructed from the axial source images and evaluated three-dimensionally using the rotational cine mode on monitors.


Figure 1
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  		Fig. 1A —49-year-old man with adenocarcinoma of the ascending colon. Axial high-b-value diffusion-weighted (DW) MR image; localized, strong dark signal is visible at posterior wall of ascending colon (arrow).

 


Figure 2
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  		Fig. 1B —49-year-old man with adenocarcinoma of the ascending colon. Maximum-intensity-projection (MIP)-reconstructed coronal high-b-value DW-MR image. Lesion seen on Figure 1A is also shown on this image as "dark spot." Note that spinal cord and spleen also have strong black signals because of their small apparent diffusion coefficient (ADC) values (arrow).

 


Figure 3
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  		Fig. 1C —49-year-old man with adenocarcinoma of the ascending colon. Axial contrast-enhanced CT image; the lesion seen on Figures 1A and 1B is poorly visualized on this image (arrow).

 


Figure 4
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  		Fig. 1D —49-year-old man with adenocarcinoma of the ascending colon. Photograph of gross colectomy specimen; a 2-cm colon adenocarcinoma is presented at posterior wall of ascending colon; this location corresponds accurately to location determined on the high-b-value DW-MR images.

 
Tumor Detection
On the basis of clinicopathologic results, two radiologists serving as study coordinators attempted to determine the location of the lesions and to correlate the pathologically confirmed lesions anatomically with imaging as accurately as possible to allow detection of false-positive interpretations. The study coordinators had access to all imaging and clinical data of the patients and the controls, including endoscopic colonoscopy and surgical pathology.

All high-b-value DW-MR images were then independently interpreted in random order and blinded fashion by three abdominal radiologists (reviewers) other than the study coordinators. The reviewers were aware that the study was performed to detect colonic cancers. However, they were blinded to all other information, such as patient identity, clinical history, the results of other imaging examinations, and histopathologic evaluations. The reviewers interpreted only the high-b-value DW-MR image series, including axial source and MIP images alone without referring to any other MR images. MIP images were evaluated with the rotational cine mode together with the axial source images in different windows on diagnostic monitors. Each reviewer graded the presence (or absence) of lesions on a 5-point confidence scale based on the strength and the appearance of dark signals on high-b-value DW-MR images as follows: 1 = definitely absent (no signal); 2 = probably absent (nonlocalized, mild to moderate signal); 3 = undetermined (localized, mild to moderate signal); 4 = probably present (localized, strong signal with no definite margins); 5 = definitely present (localized, strong signal with definite margins). If a lesion was considered to be present on a high-b-value DW-MR image, the lesion location was recorded. Only lesions recorded at the correct location determined by the study coordinators were accepted as true-positive.


Figure 5
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  		Fig. 2 —44-year-old man with rectal adenocarcinoma (arrow); maximum-intensity-projection (MIP)-reconstructed sagittal high-b-value diffusion-weighted MR image.

 


Figure 6
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  		Fig. 3 —54-year-old man with rectal adenocarcinoma (arrows); maximum-intensity-projection (MIP)-reconstructed coronal high-b-value diffusion-weighted MR image; two metastatic lymph nodes are also visualized (arrowheads).

 
Statistical Analysis
Receiver operating characteristic (ROC) curves were used to represent the performance of individual radiologists for tumor detection. The diagnostic accuracy for each radiologist was determined by calculating the area under the ROC curve (Az). Grades 4 and 5 were accepted as positive for the presence of colorectal adenocarcinoma, and the sensitivity and specificity were calculated with 95% confidence intervals (CIs).

The interobserver agreement among reviewers for tumor detection was calculated with the linearweighted kappa statistics. A kappa statistic greater than 0.75 was considered excellent agreement beyond chance; 0.4-0.75, fair to good agreement; and less than 0.4, poor agreement.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
ROC analysis yielded Az values of 0.96, 0.96, and 0.97 for the three radiologists, respectively. The sensitivities for the three radiologists were 90.9% (30/33; 95% CI, 74.7-100%), 87.9% (29/33; 95% CI, 70.9-96%), and 90.9% (30/33; 95% CI, 74.7-100%), respectively. For each radiologist, the specificity was 100% (15/15; 95% CI, 74.7-100%). The mean sensitivity and specificity of high-b-value DW-MRI for detection of colorectal adenocarcinoma were 90.9% (30/33; 95% CI, 74.5%-97.6%) and 100% (15/15; 95% CI, 74.6-100%), respectively. Figures 1A, 1B, 1C, 1D, 2, and 3 show representative patients with colorectal adenocarcinomas. All kappa values indicating interobserver agreement were in the category of excellent (range, 0.83-0.89).


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
To investigate the reason why only colonic adenocarcinomas and not the healthy colon showed strong signal intensity on the high-b-value DW-MR images is a challenging issue that warrants further studies. However, a theoretical explanation might be constructed by means of a well-described general hypothesis of DW-MRI. It is well known that diffusion is caused by random translational molecular motion, also known as Brownian motion. DW-MRI is the only imaging method that can evaluate the diffusion process in vivo. The speed of diffusion of water molecules is different in the extracellular and intracellular components of the tissues [3]. In the intracellular component, the diffusion is relatively slow because of the presence of cellular membranes. Thus, apparent diffusion coefficients (ADCs), which are quantitative expressions of diffusion characteristics of tissues, are related to the proportion of extracellular and intracellular components. They tend to decrease with increased tissue cellularity or cell density [8]. Conversely, the cell density may be indicative of tumor aggressiveness; Lyng et al. [9] reported an increased metastatic capacity of tumors with high cellularity. Moreover, in addition to the cellular membranes, the intracellular cytoskeleton, organelles, matrix fibers, and soluble macromolecules contribute to diffusion restrictions in tumors. Thus, diffusion curves that decay quickly or large ADC values may be typical for healthy tissues or benign pathologic processes with large extracellular space and little cellularity, whereas curves that decay slowly or small ADC values may indicate malignancies or hypercellularity. Therefore, DW-MRI should be sensitive for differentiating histopathologic tissue characteristics. In fact, several authors have already reported decreased ADC values in various malignant lesions [1-3]. However, there are no previous studies using a direct visual assessment of DW-MR images and reporting the diagnostic performance of this technique for abdominal pathologies.

Although the technique used in the present study is principally based on DW-MRI, our concept was different from the standard use of this technique for abdominal pathologies. In fact, DW-MRI has not been routinely used in clinical settings for the detection of colorectal cancers but is proposed as a potential tool for therapy monitoring [2, 3], and the proposed application was not qualitative but quantitative and based on ADC measurements. The high-b-value DW-MRI technique we used in this study uses an acquisition method with multiple excitations and without breath-holding to improve SNR. The limitation of scanning time by breath-hold does not permit obtaining thinslice diffusion-weighted images with adequate SNR and multiple excitations that can be used as source images for multiplanar reconstructions [7]. Conversely, an increase in motion artifacts might be assumed a theoretical shortcoming [2]; in practice, however, motion artifacts are averaged during multiexcitations by the motion-probing gradients applied for DW-MRI and become inconspicuous on the reconstructed images. Thus, images with a better SNR are achieved in exchange for absolute ADC values that become impossible to calculate because of signal averaging.

In our preliminary results, high-b-value DW-MRI showed a sufficient diagnostic ability for detecting colorectal cancers as reflected in its high sensitivity (91%, 30/33) and specificity (100%, 15/15). Additional advantages of this technique are that it is completely noninvasive, does not require exposure to ionizing radiation or injection of contrast materials, and does not cause patient discomfort [1]. Furthermore, because it is derived from the well-established DW-MRI technique, high-b-value DW-MRI does not require operators with sophisticated technical skills or high-cost investments in infrastructure such as the cyclotron in the PET example. Another advantage of high-b-value DW-MRI is that it can be easily added to an MR examination protocol because it requires only a very short prolongation of examination time [5].

We did not evaluate lymph node metastasis in the present study; our purpose was to evaluate the diagnostic ability of high-b-value DW-MRI for detecting colorectal adenocarcinoma. Nevertheless, in several patients, lymph nodes were visualized on the images (Fig. 3). Based on our brief radiologic-pathologic correlation, most of the metastatic lymph nodes were detected because of their high signal intensity, but in some patients healthy lymph nodes also showed similarly high signal intensities. Regarding the specificity for detecting lymph node metastasis, this observation might be a challenging issue for clinical applications and needs to be studied further.

Our study had some limitations. First, the study population was relatively small, and our results need to be confirmed in larger clinical studies. Second, the study included negative cases but did not include other benign conditions such as inflammatory bowel disease or benign neoplasms. Thus, the specificitSy reported in the present study should be considered relative rather than absolute.

In conclusion, according to the results of our preliminary study, high-b-value DW-MRI might be a useful tool for detecting colorectal cancers; it shows a high sensitivity and specificity. Nevertheless, further studies with larger clinical settings are needed to support our findings because of the limitations just described.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Thoeny HC, De Keyzer F, Chen F, et al. Diffusion-weighted MR imaging in monitoring the effect of a vascular targeting agent on rhabdomyosarcoma in rats. Radiology 2005;234 : 756-764[Abstract/Free Full Text]
  2. Dzik-Jurasz A, Domenig C, George M, et al. Diffusion MRI for prediction of response of rectal cancer to chemoradiation. Lancet 2002; 360:307 -308[CrossRef][Medline]
  3. Roth Y, Tichler T, Kostenich G, et al. High-b-value diffusion-weighted MR imaging for pretreatment prediction and early monitoring of tumor response to therapy in mice. Radiology2004; 232:685 -692[Abstract/Free Full Text]
  4. Squillaci E, Manenti G, Cova M, et al. Correlation of diffusion-weighted MR imaging with cellularity of renal tumours. Anticancer Res 2004;24 : 4175-4179[Abstract/Free Full Text]
  5. Cova M, Squillaci E, Stacul F, et al. Diffusion-weighted MRI in the evaluation of renal lesions: preliminary results. Br J Radiol 2004; 77:851 -857[Abstract/Free Full Text]
  6. Chow LC, Bammer R, Moseley ME, Sommer FG. Single breath-hold diffusion-weighted imaging of the abdomen. J Magn Reson Imaging 2003; 18:377 -382[CrossRef][Medline]
  7. Takahara T, Imai Y, Yamashita T, Yasuda S, Nasu S, Van Cauteren M. Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display. Radiat Med 2004;22 : 275-282[Medline]
  8. Sugahara T, Korogi Y, Kochi M, et al. Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging1999; 9:53 -60[CrossRef][Medline]
  9. Lyng H, Haraldseth O, Rofstad EK. Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging. Magn Reson Med 2000;43 : 828-836[CrossRef][Medline]

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