Eur Radiol (2004) 14:318–325 DOI 10.1007/s00330-003-2118-y Tsutomu Tamada Teruki Sone Kiyohisa Nagai Yoshimasa Jo Masayuki Gyoten Shigeki Imai Yasumasa Kajihara Masao Fukunaga Received: 31 December 2002 Revised: 22 May 2002 Accepted: 15 September 2003 Published online: 18 October 2003 © Springer-Verlag 2003 T. Tamada (✉) · T. Sone · K. Nagai M. Gyoten · S. Imai · Y. Kajihara M. Fukunaga Department of Radiology, Kawasaki Medical School, 577 Matsushima, 701-0192 Kurashiki City, Okayama, Japan e-mail: [email protected] Tel.: +81-86-4621111 Fax: +81-86-4621199 Y. Jo Department of Urology, Kawasaki Medical School, 577 Matsushima, 701-0192 Kurashiki City, Okayama, Japan U R O G E N I TA L T2-weighted MR imaging of prostate cancer: multishot echo-planar imaging vs fast spin-echo imaging Abstract The aim of the present study was to assess the performance of pre-biopsy T2-weighted MR imaging using multishot echo-planar imaging (EPI) sequence for visualization of prostate cancer and to compare image quality with that of fast spin-echo (FSE) sequence. Thirty-nine patients with suspected prostate cancer and one healthy male volunteer were examined on a 1.5-T MR scanner equipped with a pelvic phased-array coil. Axial MR images were obtained using multishot EPI sequence with a multishot number of 16 and FSE sequence without fat suppression. Paired EPI and FSE images were independently evaluated by three radiologists. Furthermore, signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) were compared between EPI and FSE images of 12 pathologically proven lesions of prostate cancer. Delineation of the periprostatic venous plexus, prostate zonal anatomy, Introduction The incidence of prostate cancer is high in Caucasians and the mortality rate from prostate cancer is higher than that from lung cancer and colorectal cancer in males aged 65 years or more in the United States [1]. The incidence of prostate cancer in Japanese has been several-fold lower than that in Caucasians but is likely to increase with recent westernization of life style and with the increase in the number of the aged [2, 3]. and seminal vesicle on EPI was graded to be superior/inferior to FSE in 15.8/0, 14.6/0, and 21.5/4.3% of cases, respectively. On the other hand, delineation of the neurovascular bundle was superior/inferior to FSE in 2.6/13.2% of cases. The SNR and CNR of prostate cancer on EPI were significantly higher than those on FSE (7.99±2.51 vs 3.36±0.58, p<0.0001, and 5.51±2.02 vs 2.21±0.79, p<0.0001, respectively). In conclusion, multishot EPI has higher quality of contrast resolution for imaging of prostate cancer compared with FSE and would have the potential usefulness in the detection of prostate cancer, although these results obtained with a phased-array coil cannot be extrapolated to examinations performed with an endorectal coil. Keywords Prostate · Neoplasms · MR imaging · Echo-planar imaging · Comparative studies Magnetic resonance imaging is used for detection of the location and extracapsular spread of tumor in prostate cancer, and its usefulness is being established [4]. In MR imaging, T2-weighted images using fast spinecho (FSE) sequence are generally used for an evaluation of the internal structure of the prostate [5, 6]. The most cancer nodules arise in the peripheral zone and are of low signal intensity compared with an inherently high signal intensity of the peripheral zone by this method. Since 512 matrix can be used in T2-weighted FSE imaging either with body coil or endorectal surface 319 coil, high spatial resolution is obtained with a short acquisition time; however, the limitation of conventional or FSE imaging also exists and 30–40% of prostate cancer in the peripheral zone are undetectable because the lesions are isointense to the peripheral zone [7, 8, 9, 10]. Echo-planar imaging (EPI) with high temporal and contrast resolution developed by Mansfield [11] is used in diffusion-weighted imaging of acute stroke [12], perfusion imaging [13], and functional imaging [14]. In the imaging of prostate lesions, however, the usefulness of EPI sequence has not been thoroughly evaluated. In the present study, we focused on high contrast resolution rather than high temporal resolution in EPI, applied the EPI sequence to the imaging of the prostate, and assessed its usefulness in the delineation of prostate normal structures and the detectability of the prostate cancer as compared with T2-weighted FSE imaging. Subjects and methods Patient characteristics Thirty-nine male patients (age range 53–84 years, mean age 71 years) with suspected prostate cancer were referred for MR imaging of the pelvis between October 1997 and April 1998. One healthy male volunteer 29 years old also underwent MR examination for selection of the imaging parameters on multishot EPI. The inclusion criteria of the patients were based on a positive digital rectal examination and/or high prostate-specific antigen (PSA) levels, and a transrectal ultrasound (TRUS)-guided biopsy of the prostate performed after MR imaging. Informed consent was obtained from all participants after the nature of the procedures had been fully explained. MR imaging The MR images were obtained with a 1.5-T whole-body imager (Signa Horizon, General Electric, Milwaukee, Wis.). The pelvic phased-array coil (Pelvic Array, General Electric) was used as a receive-only surface coil. After intramuscular administration of glucagon to decrease intestinal peristalsis, imaging was performed in all patients under fasting. After a localized series of coronal T1weighted images were obtained, axial and sagittal T2-weighted FSE sequence, axial EPI sequence, and other routine sequences were performed sequentially. The examination was generally completed in 40–50 min. Axial sections were obtained with 4- to 5mm slice thickness and 0- to 1-mm interslice gap and a 24-cm field of view. T2-weighted FSE images were obtained using a TR time of 4000 ms, an effective TE time of 110 ms, an echo train length of 9 or 10, a receiver band width of 15.6 kHz, two or three averagings, a 512¥320 acquisition matrix, and no fat-suppression technique. The T2-weighted EPI parameters were examined in the healthy subject. In EPI, the spin-echo type, which has been reported to be less sensitive to the magnetic susceptibility and blood flow artifacts [11], was used. As EPI parameters, the multishot number, effective TE, and the receiver bandwidth were examined. The optimal parameters obtained from the study were used for EPI of the remaining subjects. The imaging time was 5 min 23 s in EPI, and between 4 min 48 s and 6 min 24 s in FSE. Image interpretation and data analysis Paired axial images of T2-weighted EPI and FSE sequences were evaluated. Three radiologists independently compared EPI and FSE images in terms of delineation of normal structures, i.e., the periprostatic venous plexus in 40 subjects, the prostate zonal anatomy in 32 subjects, the neurovascular bundle in 38 subjects, and the seminal vesicle in 31 subjects, and judged using a relative three-point scale to determine whether the EPI images were better than, the same as, or worse than the FSE images. The prostate zonal anatomy in 8 patients, the neurovascular bundle in 2 patients, and the seminal vesicle in 9 patients were excluded for the evaluation because normal structure was disappeared due to the tumor invasion or hemorrhage. The pooled results of three reviewers were used to compare the ratings in the two sequences. The statistical analyses were performed using the paired sign test with a value of p<0.05 considered significant. Twenty-seven patients were pathologically confirmed prostate cancer by transrectal needle biopsy. The biopsy specimen was obtained from each sextant under the guidance of TRUS. An additional biopsy was taken when necessary from the area as close as possible to the suspected region on MR images. All biopsy specimens were evaluated by a pathologist in our hospital. Of the 27 patients, 15 patients with tumor in the inner gland, hemorrhage in the prostate, or disappearance of the normal peripheral zone caused by tumor invasion were excluded, and signal-to-noise ratio (SNR) of the tumor and contrast-to-noise ratio of the tumor [CNR; (SI of the peripheral zone as the control-SI of lesion) noise] of EPI and FSE T2-weighted images were calculated. On MR images, the lesion fulfilling the following criteria was regarded to be the prostate cancer: an area in the posterior aspect of the peripheral zone with (a) diffuse low SI with mass effect, or (b) circumscribed, round, or triangular-shaped localized hypointensity in comparison with the normally hyperintense appearance of the peripheral zone, and (c) a size larger than 5 mm. Locations of all the suspected lesions on MR images were consistent with the estimation by TRUS-guided needle biopsy. All 12 patients had adenocarcinoma, and pathologically Gleason score was 2 in 2 patients, 3 in 1 patient, 5 in 5 patients, 7 in 2 patients, 8 in 1 patient, and 9 in 1 patient. Only one lesion per patient was analyzed. The region of interest (ROI) for the SI measurements was established in the largest possible area to lesion and in the same site for each sequence (Fig. 1). In the peripheral zone, 5 ROIs were placed in the normal area excluding the lesion, and 5 ROIs were placed at arbitrary positions in the areas of anterior and posterior across the pelvis which for the noise measurements. Their means were used for the determination of the SNR and CNR. Calculated SNR and CNR values of each sequence were expressed as the means±SD, and compared using Student’s t test. The results were considered significant at p<0.05. Results Evaluation of T2-weighted EPI parameters The EPI images obtained from healthy subject using 1, 2, 4, 8, 16, or 32 shots, an effective TE time of 40, 60, 80, 100, and 120 ms, and a receiver band width of 16, 32, and 64 kHz were evaluated. The images obtained using 16 and 32 shots had less distortion (Fig. 2). The images with high contrast resolution of prostate zonal anatomy were obtained using an effective TE of 80 ms (Fig. 3), and images with fewer artifacts were obtained using a receiver bandwidth of 64 kHz (Fig. 4). Based on 320 Fig. 1 Example of the placement of region of interest (ROI) for signal intensity (SI) measurements in a axial multishot echo-planar image and b fast spin-echo image for the patient with pT3 prostate cancer. Both images show low SI lesion in the left peripheral zone. ROI 1 and ROI 2–6 are the regions for the SI measurement of lesion and control area in the peripheral zone, respectively. S/N SI of lesion/noise, C/N [(SI of the peripheral zone (the average of SI in ROI 2–6)-SI of lesion)/noise] Fig. 2a–f A 29-year-old healthy man. Axial sections by echo-planar imaging with the shot number of a 1, b 2, c 4, d 8, e 16, and f 32. With four averagings and an effective TE time of 80 ms, acquisition times were a 20 s, b 45 s, c 1 min 25 s, d 1 min 23 s, e 2 min 43 s, and f 5 min 23 s. Image matrix size was 256¥128 in single-shot images and 256¥256 in multishot images these results, 16 shots, TR time of 2499 ms, an effective TE time of 80 ms, a receiver band width of 62 kHz, eight averagings, and a 256¥256 acquisition matrix on EPI sequence were the optimal conditions to obtain images using the same sections and almost the same acquisition time as T2-weighted FSE imaging. Comparison between EPI and FSE images in delineating normal anatomy The ratings of the delineation for normal anatomy are shown in Table 1. According to the judgment of the delineation of the normal anatomy performed by individual three radiologists, the periprostatic venous plexus, prostate zonal anatomy, and seminal vesicle on EPI sequence was rated superior to that on FSE sequence in 19 321 Fig. 3a–e A 29-year-old healthy man. Axial sections by multishot echo-planar imaging with the multishot number of 16, and four averagings. The effective TE times were a 40, b 60, c 80, d 100, and e 120 ms Fig. 4a–c A 29-year-old healthy man. Axial sections by multishot echo-planar imaging with the multishot number of 16, effective TE time of 80 ms, and four averagings. The receiver bandwidth was a 16, b 32, and c 64 kHz (15.8%) of 120 cases, 14 (14.6%) of 96 cases, and 20 (21.5%) of 93 cases, respectively, whereas EPI images was judged to inferior to that on FSE images only in 4 (4.3%) of the 93 cases in the seminal vesicle (Figs. 5, 6). On the other hand, neurovascular bundle on EPI images was rated inferior to that on FSE images in 15 (13.2%) of 114 cases, and superior to that in only 3 cases (2.6%). Comparison between EPI and FSE sequences in SNR and CNR of tumor The SNR was 7.99±2.51 in EPI sequence and 3.36±0.58 in FSE sequence, whereas the CNR was 5.51±2.02 in EPI sequence and 2.21±0.79 in FSE sequence. Both re- sults showed significantly higher values in EPI sequence than in FSE sequence (Table 2). Discussion Virtually any combination of radio-frequency pulses used in conventional pulse sequences can be used in EPI, and spin-echo type or gradient-echo type are usually adopted in clinical application. From these two types of EPI sequence, we selected multishot spin-echo type, of which the contrast resolution is high, because this type of EPI is less sensitive to the motion artifact, susceptibility artifact caused by air-containing bowel loop in the pelvis, and blood-flow artifact compared with gradient- 322 Table 1 Three-point scale assessed by three reviewers to grade echo-planar imaging (EPI) of normal anatomy. FSE fast spin echo Fig. 5a, b A 74-year-old man with pathologically confirmed non-malignancy in the prostate. Paired axial sections by a multishot echo-planar image and b fast spin-echo image at the level of prostate. Three reviewers judged visualization of small vessels of periprostatic venous plexus (arrows, a) to be superior in a Fig. 6a, b A 75-year-old man with pathologically confirmed prostate cancer (pathological Gleason score 5). Paired axial sections by a multishot echoplanar image and b fast spinecho image at the level of prostate. Three reviewers judged prostate zonal anatomy to be more definite in a than in b Anatomic sites Number Venous plexus Reviewer 1 Reviewer 2 Reviewer 3 Total 40 Prostate zonal anatomy Reviewer 1 Reviewer 2 Reviewer 3 Total 32 Neurovascular bundle Reviewer 1 Reviewer 2 Reviewer 3 Total 38 Seminal vesicle Reviewer 1 Reviewer 2 Reviewer 3 Total 31 Comparison with FSE images p Better Same Worse 8 5 6 19 32 35 34 101 0 0 0 0 <0.0001 5 4 5 14 27 28 27 82 0 0 0 0 0.0001 1 1 1 3 31 32 33 96 6 5 4 15 0.0075 7 6 7 20 22 24 23 69 2 1 1 4 0.0015 323 Table 2 Signal-to-noise ratios (SNR) and contrast-to-noise ratios (CNR) of prostate cancer on echo-planar imaging (EPI) and fast spin-echo (FSE) T2weighted images a p<0.0001 compared with FSE Patient no. 1 2 3 4 5 6 7 8 9 10 11 12 Mean±SD SNR CNR EPI FSE EPI FSE 6.24 9.46 12.46 5.76 7.95 7.80 7.28 3.28 6.09 8.69 9.95 10.88 7.99±2.51a 3.80 3.35 3.60 2.80 4.10 2.56 2.83 3.16 3.16 3.47 2.99 4.53 3.36±0.58 4.38 10.26 6.61 7.01 4.89 4.16 5.34 6.81 2.66 4.04 3.82 6.16 5.51±2.02a 3.19 3.20 2.68 2.21 0.72 2.18 2.88 1.51 2.07 1.56 1.42 2.94 2.21±0.79 echo EPI [11, 15, 16]. It has been demonstrated that an endorectal coil gives a better SNR and improved spatial resolution for prostate imaging compared with the body coil [17, 18]. On the other hand, an endorectal coil is often not well tolerated and increased susceptibility effects associated with EPI have been reported to deteriorate the quality of diffusion-weighted images of the prostate [19]. In the present study, an endorectal coil was not used because of its possible susceptibility effects on EPI MR images. The evaluation of the performance of T2-weighted EPI and T2-weighted FSE imaging in delineating normal prostate anatomy demonstrated that EPI was equivalent to or better than FSE in the regions except for neurovascular bundle. The superiority of EPI in the imaging of structures such as the periprostatic venous plexus and seminal vesicle composed of small vascular complex or fluid-filled tubules [20] may be attributed to its heavily T2-weighted contrast and overall fat-suppression effect [16, 21] induced by water selective-excitation for suppression of chemical-shift artifact. These characteristics of EPI would also favor the visualization of prostate zonal anatomy since the peripheral zone of prostate is high in water content with abundant glandular components and less stroma [20, 22]. This is in contrast to uterine zonal anatomy, which has been reported to be poorly visualized in multishot EPI compared with FSE imaging [15]. In our study, glucagon was used to decrease the motion artifact caused by intestinal peristalsis. This medication would also favor the improvement of the visualization. The reduction of delineation ability of EPI images in neurovascular bundle, which are visualized as low signal intensity structures within fat tissues locating at 5 and 7 o’clock positions in the angle between the prostate and the rectum, would have been caused by fat-suppression effect. With regard to the detectability of prostate cancer in the peripheral zone, both SNR and CNR of lesions were significantly higher in EPI than in FSE. The high CNR may reflect the property of EPI that the heavily T2weighted imaging enhance the subtle difference in water content between the lesion and the surrounding peripheral zone tissue [20, 22]. Generally, the SNR of singleshot EPI images is lower than that of standard pulse sequences [16, 23], but a high SNR was obtained in the present study, probably because of the reduction of susceptibility artifacts by increasing of the number of shots, and using a large signal averagings; however, when the same matrix size is used in FSE and EPI, the SNR may be equivalent in both methods. Furthermore, these results are valid only for examinations performed with a phased-array coil and that they cannot be extrapolated to examinations performed with an endorectal coil. Approximately 70% of cases in prostate cancer arise in the peripheral zone [24], and the accuracy of tumor detection for cancers originating in the peripheral zone using MR imaging is reported to be approximately 50–70% [7, 8, 9, 10]. The remaining prostate cancer cannot be detected because the lesions were essentially isointense to the peripheral zone [25]. The lesions of prostate cancer that were missed on MR images are reported to be small in size [25, 26, 27, 28, 29] or poorly differentiated [25, 26, 28]. Pariver [25] and Schiebler [26] reported that poorly differentiated tumor have no defined boundaries and blend with normal prostate architecture, because of tending to infiltrate within the gland, resulting in uniform signals for the prostate gland. On the other hand, well to moderately differentiated carcinomas grow in nodules of densely packed glandular elements with little central space mucin storage; therefore, the high cellularity and reduced fluid content of cancer generate a low signal intensity. In the 2 patients with poorly differentiated adenocarcinoma examined in the present study, both SNR and CNR of the tumors were high in T2-wighted EPI, suggesting that some of the tumors of which the signal intensity is the same as that of the surrounding prostate structures in T2-wighted FSE images can be visualized by EPI. 324 The potential limitation of the present study is that MR findings are not compared with the results of histological mapping of the prostate. We interpreted MR lesions as prostate cancer from morphological criteria. It has been reported that on MR images the low-SI cancerous areas appear as more round and triangular-formed lesions [10], whereas the hypointense benign tissue changes show more wedge-shaped, linear, stripy forms, and diffuse extension without mass effect [10, 30]. It has also been pointed out that the tumor detection in the peripheral zone on MR images differs according to size and location of the lesions [25, 26, 27, 28, 29]. In the present study, we calculated SNR and CNR only in the lesions that were larger than 5 mm in size, fulfilled the common morphologic criteria of the prostate cancer, and located in the posterior aspect of the outer gland. Furthermore, locations of all these lesions were consistent with the estimation by TRUS-guided needle biopsy. Although even the TRUS-guided needle biopsy is not a gold standard for localizing cancer within prostate [31, 32], we believe that our criteria for selecting the lesion could improve the accuracy to a considerable degree. In T2-weighted MR imaging, low signal intensity lesions in the peripheral zone do not represent a specific finding for cancer because benign conditions, such as prostatitis, hemorrhage, or dystrophic changes related to radiation or androgen-deprivation therapy, can mimic cancer [18]. This situation would more or less apply to EPI T2-weighted imaging. The gradient-echo EPI may be sensitive for detecting intraprostatic hemorrhage due to susceptibility dephasing associated with hemorrhage. On the other hand, the spin-echo EPI would be less sensitive because of its less sensitivity for susceptibility changes. Indeed, the spin-echo EPI was not significantly different from FSE in detecting susceptibility dephasing associated with chronic intracranial hemorrhage, although the gradient-echo EPI showed higher sensitivity [33]. In the present study for the comparison of T2-wighted images between EPI and FSE, the patients in whom tumors were visualized in both images were examined. In FSE, a 512 matrix can be used, but currently not in EPI; therefore, the spatial resolution of EPI is lower than that of FSE, and EPI would be inferior to FSE in evaluating the precise extension of the tumor such as capsular invasion. 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