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Eur Radiol (2008) 18: 716–721 DOI 10.1007/s00330-007-0795-7 Bengi Gürses Neslihan Kabakci Arzu Kovanlikaya Zeynep Firat Ali Bayram Aziz Müfit Uluð İlhami Kovanlikaya Received: 10 April 2007 Revised: 13 September 2007 Accepted: 28 September 2007 Published online: 25 October 2007 # European Society of Radiology 2007 B. Gürses . N. Kabakci . A. Kovanlikaya . Z. Firat . A. Bayram . İ. Kovanlikaya Department of Radiology, Yeditepe University Hospital, Kozyatagi, Istanbul, 34752, Turkey A. M. Uluð Department of Biomedical Engineering, Yeditepe University, School of Engineering, Kayisdagi, Istanbul, 34755, Turkey A. M. Uluð Department of Radiology, Weill Medical College of Cornell University, New York, NY, 10021, USA B. Gürses (*) Yeditepe Üniversite Hastanesi, Devlet Yolu Ankara Caddesi, No: 102-104, Kozyatagi, 34752, İstanbul, Turkey e-mail: [email protected] Tel.: +90-216-5784371 Fax: +90-216-4693796 UROGENI TAL Diffusion tensor imaging of the normal prostate at 3 Tesla Abstract The aim of this study was to assess the feasibility of diffusion tensor imaging (DTI) of the prostate and to determine normative fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values of healthy prostate with a 3-Tesla magnetic resonance imaging (MRI) system. Thirty volunteers with a mean age of 28 (25–35) years were scanned with a 3-Tesla MRI (Intera Achieva; Philips, The Netherlands) system using a six-channel phased array coil. Initially, T2-weighted turbo spin-echo (TSE) axial images of the prostate were obtained. In two subjects, a millimetric hypointense signal change was detected in the peripheral zones on T2-weighted TSE images. These two subjects were excluded from the study. DTI with single-shot echoplanar imaging (ssEPI) was performed in the remaining 28 subjects. ADC and FA values were measured using the manufacturer supplied software by positioning 9-pixel ROIs on each zone. Differences between parameters Introduction Prostate cancer is one of the most common forms of malignancy in men, with an increasing incidence. Magnetic resonance imaging (MRI) has gained clinical acceptance in the preoperative evaluation of prostatic carcinoma patients in terms of extracapsular spread, seminal vesicle-neurovascular bundle invasion, lymph node metastases in patients with biopsy proven prostatic carcinoma [1]. On the other hand, the accuracy of T2-weighted sequences in the diagnosis of prostate cancer is limited, due to lack of sensitivity and specificity [2, 3]. Both prostatitis and tumoral infiltration have overlapping features and are seen of the central and peripheral zones were assessed. Mean ADC value of the central (1.220±0.271×10−3 mm2/s) was found to be significantly lower when compared with the peripheral gland (1.610±0.347×10−3 mm2/s) (P<0.01). Mean FA of the central gland was significantly higher (0.26), compared with the peripheral gland (0.16) (P<0.01). This study shows the feasibility of prostate DTI with a 3-Tesla MR system and the normative FA and ADC values of peripheral and central zones of the normal prostate. The results are compatible with the microstructural organization of the gland. Keywords Prostate . MRI . Diffusion as decreased signal intensity foci on conventional T2weighted images [1, 4]. In order to increase the accuracy, new functional techniques, such as dynamic contrast enhanced MRI and MR spectroscopy, have been added to the routine protocol in many centers [5]. Recently, a number of studies have shown the feasibility of diffusion-weighted imaging of the prostate [6–9]. It is well known that diffusion-weighted imaging provides valuable data about the microstructural and pathophysiological aspects of various structures. Fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values provided from diffusion tensor imaging (DTI) data reflect the degree of water diffusion restriction in different tissues. FA is obtained 717 by using at least six tensor applications, which provides directional data about diffusion anisotropy [8]. DTI has found wide clinical applications, especially in neuro-and musculoskeletal imaging. In neuroradiology, diffusion MRI have been mainly used for stroke, multiple sclerosis and tumor patients. Pathological processes may cause change in normative FA values and disruption of fibers in tractography [9, 10]. There are only a few clinical studies about diffusionweighted imaging of the normal prostate and prostatic carcinoma. The majority of these studies have been carried out with 1.5-Tesla MRI systems [6–9]. The main limitations of DTI application in the abdomen have been the presence of motion and poor signal-to-noise ratio values obtained, especially in low-Tesla systems [10]. With the advent of 3-Tesla MRI, parallel imaging technology, and ultrafast single-shot echo-planar sequence, diffusion and diffusion tensor imaging has been more feasible for abdominal and pelvic viscera, including the prostate gland [10]. Three-Tesla MR scanners, providing a twofold increase in signal-to-noise ratio, provide better spatial and temporal resolution, and significantly shorter acqusition times [2]. In 3-Tesla systems, a major disadvantage is increased susceptibility artifacts, but the use of parallel imaging technique, by reducing susceptibility artifacts, has been shown to provide less distorted diffusion images of the prostate [10]. The aim of this prospective study is to show the feasibility of prostate DTI with a 3-Tesla scanner, using the parallel imaging technique with optimized parameters in healthy volunteers, to determine the normative FA and ADC values in peripheral and central zones of the gland, and to correlate these values with zonal microstructural organization. Materials and methods All MRI examinations were performed with a 3-Tesla scanner (Intera Achieva; Philips, The Netherlands) equipped with high-performance gradients of a maximum strength of 80 mT/m and a slew rate of 200 mT/m/ms, using six-channel phased array SENSE Torso coil. Thirty volunteers with a mean age of 28 (range between 25 and 35 years) were scanned in this study. The subjects did not mention any history of prostatic disease with established diagnosis. The examination protocol included axial T2-weighted TSE and DTI with EPI. Initially, T2weighted turbo spin echo images (TR: 2,569 ms; TE: 80 ms; FOV: 430 mm; matrix: 243×512; slice thickness: 2.7 mm; gap: 0.0 mm; flip angle: 90°) were obtained in the axial plane for all subjects. In two patients, there were millimetric hypointense foci in the peripheral zone on T2weighted images and these two patients were excluded from the study and referred to the urology clinic. Signal intensity of the prostate was normal on T2weighted images in the remaining 28 subjects. DTI was performed in this group. DTI was obtained using a singleshot echo-planar-imaging technique (TR: 10,000 ms; TE: 53 ms; FOV: 430 mm; matrix: 128×126; SENSE factor: 2; slice thickness: 2.7 mm; gap: 0.0 mm; flip angle: 90°; voxel size: 1.68×1.68×2.70 mm). The diffusion gradients were applied in 32 directions, images were acquired at b values of 0 and 700 s/mm2. The optimal b value was determined considering the ADC value of the prostate tissue. In a diffusion experiment, the optimal b value for any tissue should be such that b×ADC is equal to 1. The ADC of interest in our study was 1.220×10−3 mm2/s for the central zone and 1.610×10−3 mm2/s for the peripheral zone. The average ADC is 1.415×10−3 mm2/s. The optimal b value is calculated as: 1/(1.415×10−3)=706.7 s/mm2. We chose the b_value of 700, which is within 1% of the theorotical optimal value. Slice locations, thickness, FOV and gap values were identical on T2 and DTI sequences in order to maintain accurate zonal and anatomical correlation. The total scan duration was 8 min. DTI image acquisition time was 6 min. Analysis of DTI data After data acqusition, all images were transferred to the Workstation for analysis with the special manufacturersupplied software (“PRIDE”). ROIs were drawn on b=0 images, using axial T2-weighted images as anatomical guide. Each ROI consisted of 9 pixels (1.68×1.68× 2.70 mm each). For detection of FA and ADC values, four ROIs were used, two on each side. On each side, one ROI was placed on the central, the other ROI on the periperal zone. ROI placements were performed on the level of midgland in each subject where peripheral zone is largest on axial images. In the young people with no prostatic disease, the peripheral zone of the prostate is rather thin, that’s why the ROIs could only be placed in the mid-gland where the peripheral zone is large enough. Larger ROIs could not be used because of age-related anatomical reasons. The average of both values on each sides were obtained for both zones as the final value. During ROI selection in the central zone, great care was taken to exclude the urethra. The neurovascular bundle was avoided while putting ROIs on the peripheral gland. FA and ADC values of the selected ROIs were calculated by the manufacturersupplied software system (Fig. 1). The significance of the difference in ADC and FA values of the central and peripheral zones were determined using Student’s t-test. P values <0.05 were regarded as statistically significant. Tractography was performed using manufacturer supplied software with streamlines fiber tracking algorithm. 718 Fig. 1 Axial T2 TSE (a), b=0 (b), b=700 (c) images, color-coded FA map (d) of a subject. ROI selection is shown on b=0 and FA map image (d) in the central and peripheral zones Anisotropy and angular thresholds were selected in the range of 0.12–0.20 and 30–40°, respectively. The orientation of prostate fibers in different zones were assessed using tractography images. Blue color represented craniocaudal orientation of diffusion; red color, right-left; green color, antero-posterior. Changes in intensity of the color represented different strengths of anisotropy. Results In all the subjects, there was statistically significant difference in ADC and FA values between central and peripheral zones. The mean ADC value of the central zone (1.220±0.271×10−3 mm2/s) was significantly lower than the mean ADC of the peripheral gland (1.610±0.347×10−3 mm2/s) (P<0.01). 719 Table 1 ADC and FA values for central and peripheral prostate zones n=28 Central zone Peripheral zone ADC (×10−3 mm2/s) FA Mean SD Mean SD 1.220 1.610 0.271 0.347 0.260 0.160 0.060 0.030 The mean FA value of the peripheral gland (0.16) was significantly lower than the mean FA value of the central zone (0.26) (P<0.01) (Table 1). Tractography revealed dark blue dominancy on the central, and light blue on the peripheral gland. Blue color was consistent with supero-inferior orientation of fiber structure within the gland. Moreover, darker color indicated increased anisotropy in the central zone compatible with higher FA values obtained from statistical analysis (Fig. 2). On the tractography of the central gland, the urethra could be seen in the center with no detectable fiber structure compatible with the free fluid content (Fig. 3). Discussion DTI is known to provide valuable data about the microstructural and pathophysiological aspects of many tissues which influence diffusion of water molecules. The main ongoing clinical applications of DTI are in neuro- and musculoskeletal imaging [11–14]. In neuro-imaging, DTI is mainly used for cerebral ischemia, multple sclerosis, and differential diagnosis of tumoral processes. Fig. 3 Tractography of a subject on the coronal plane (a) showing the central zone with urethra in the center devoid of fibers. Sagital plane tractography (b), each zone shown is displayed with a different color Fig. 2 Tractography image of the prostate with dark blue dominancy in the center, and light blue in the periphery Tissues with a random and less-organized microstructure, such as CSF and gray matter, exhibit isotropic diffusion characterized with lower FA values. On the other hand, tissues such as muscle and white matter with organized microstructural features are anisotropic with higher FA values [8, 9, 11]. The reason why DTI had been mostly limited to neuro- and musculoskeletal imaging so far is probably motion, pulsation artifacts and magnetic susceptibility from air in the bowel in body imaging. 720 Recently, diffusion imaging has also been applied for some of the abdominal organs. With the advent of higher magnetic field systems and phased-array coils with parallel imaging technology, DTI of some of the intraabominal organs has been feasible in a clinically acceptable scan time [9, 12–14]. MRI has been accepted as a clinical tool in the preoperative evaluation of patients with prostatic carcinoma. Due to the lack of sensitivity and specificity of MRI in the detection of prostatic carcinoma, clinical MRI has some important limitations in the differential diagnosis [2, 3]. Both prostatic carcinoma and prostatitis are seen as hypointense foci on T2weighted images, and the sole criteria for tumoral infiltration is nodular appearance and invasive behaviour [1, 4, 5]. In the last few years, attempts are made to increase the sensitivity and specificity by MR spectroscopy and contrast enhanced dynamic studies, that are added in some centers to the routine protocol [6, 15, 16]. DTI is a relatively new technique for prostate imaging. In the recent literature, there are conflicting FA and ADC values reported for normal gland and tumoral foci [6, 8, 16, 17]. The aim of the current study was to establish the normative values for the central zone and peripheral gland, and to display the tractography in healthy volunteers using 3-Tesla MRI system and parallel imaging technology with optimized sequence parameters. The optimization included choosing the optimal b value for prostate and other sequence parameters such as slice thickness, matrix and FOV values. All of these values were adapted for the prostate. There are different studies regarding diffusionweighted imaging of the prostate that have used different b values. Yet, there is no consensus about the parameters and we believe that prospective studies with large groups should be performed to define the optimal parameters in a 3-Tesla system. Most of the previous literature included diffusionweighted imaging of the prostate using the single parameter of ADC without any direction data [8, 18]. On the other hand, recently, DTI of the prostate has been carried out in only a small number of clinical studies. In 2004, Sinha et al. [9] performed DTI of the prostate in six volunteers with a 1.5-Tesla system. The b values used in this study were 0–349.76 mm/s. They have reported that the mean FA value of the peripheral gland (0.46±0.04) was slightly higher than the central zone (0.40±0.08) (P<0.01). They have also mentioned that their results were not in concordance with the microstructural organization of the zones. Desouza et al. [18] performed diffusion-weighted MR imaging in patients with prostate cancer using an endorectal coil with a 1.5-Tesla system. They reported that ADC values decreased in tumoral areas. Using an endorectal coil is an advantage due to improved signalto-noise ratio, but in this study an endorectal coil could not be used since it was not available at the time of the study. In 2006, Gibbs et al. [10] performed diffusion and diffusion tensor imaging in patients with prostatic carci- noma using 3-Tesla system. They used DTI sequences with b=0-700 mm/s. Tumoral foci were found to have higher FA values (0.24±0.05) when compared with the normal appearing peripheral gland (0.16±0.06). The FA values they have found in the peripheral gland is similar to our study. Haker et al. [19] in 2005 performed DTI of the prostate in eight patients with the suspicion of cancer using 1.5-Tesla MRI equipment. The normative mean FA value on benign peripheral zone was reported to be 0.15±0.06, which is similar to the results of the current study. The mean FA values of the peripheral gland (0.18± 0.06) obtained in the study by Chen et al. [20] is again compatible with our results. To our knowledge, there is no published prospective large series regarding the normal diffusion tensor parameters of prostate zones. On the other hand, although there is a limited number of DTI studies performed on healthy and diseased prostates, there is no concensus on normative values [6, 10, 16, 21]. Different parameters used in these studies, such as different signal-to-noise ratio values, imaging protocols, technical limitations, and b values, may be the reason of this conflict. This study establishes the normative values within given parameters of the central and peripheral zones of prostate. We used the state-of-the-art MR hardware to optimize the calculations in a large group of volunteers. The slice thickness, gap and location were similar for T2-weighted and DTI sequence for accurate anatomical localization. Our results are in concordance with the microstructural organization of central and peripheral gland. The prostate gland is a partly glandular and partly muscular organ enclosed by a firm fibrous capsule. This capsule is firmly adherent to the gland and is structurally continuous with the stroma of the gland. The stroma of the gland is mainly composed of smooth muscle and fibrous tissue. The central gland with compact and organized smooth muscle fibers and accompanying glands create more restricton against the diffusion of water molecules in certain directions with resultant anisotropy. On the other hand, peripheral gland with rather loose microstructural organization exhibits less restriction to diffusion with resultant anisotropy. The results of our study and the tractography images reflect these facts with higher FA values in the central zone compared with the peripheral gland. Meanwhile, there is an ongoing study on DTI of prostate cancer in our center. The preliminary data show increased FA and decreased ADC values at the tumoral foci. This finding correlates well with the recent literature [17, 19, 20, 22]. 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