ADC Measurement of Abdominal Organs and Lesions Using Parallel Imaging Technique

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1 ADC Measurement of Abdomen Using Parallel Imaging Abdominal Imaging Original Research A C D E M N E U T R Y L I A M C A I G O F I N G Takeshi Yoshikawa 1 Hideaki Kawamitsu 2 Donald G. Mitchell 1 Yoshiharu Ohno 2 Yonson Ku 3 Yasushi Seo 4 Masahiko Fujii 2 Kazuro Sugimura 2 Yoshikawa T, Kawamitsu H, Mitchell DG, et al. Keywords: abdomen, diffusion-weighted MRI, MRI DOI: /AJR Received May 10, 2005; accepted after revision October 25, Supported by the Smoking Research Foundation, Tokyo, Japan. 1 Department of Radiology, Division of Magnetic Resonance Imaging, Thomas Jefferson University, 132 S 10th St., Suite 1096, Philadelphia, PA Address correspondence to T. Yoshikawa. 2 Department of Radiology, Kobe University Graduate School of Medicine, Kobe, Japan. 3 Department of Liver and Transplantation Surgery, Kobe University Hospital, Kobe, Japan. 4 Department of Clinical Molecular Medicine, Division of Diabetes, Digestive and Kidney Diseases, Kobe University Graduate School of Medicine, Kobe, Japan. AJR 2006; 187: X/06/ American Roentgen Ray Society ADC Measurement of Abdominal Organs and Lesions Using Parallel Imaging Technique OBJECTIVE. The purpose of our study was to assess the reliability and usefulness of parallel imaging for apparent diffusion coefficient (ADC) measurement of abdominal organs and lesions. MATERIALS AND METHODS. Single-shot spin-echo echo-planar diffusion-weighted MRI (TE = 66, b = 0, 600 s/mm 2 ) was performed in phantom and clinical studies. The b value was set to minimize the effects of perfusion in tissue and to maintain signal-to-noise ratio. Bottle phantoms were scanned with and without parallel imaging and with various parallel imaging factors and at various positions to evaluate the effects of parallel imaging on ADCs. In 200 consecutive clinical patients (122 men and 78 women: mean age, 61.9 years), ADCs were calculated for liver (four segments), spleen, pancreas (head, body, tail), gallbladder, renal parenchyma, and back muscle, and then compared to evaluate the reliability of clinical ADC measurements with parallel imaging. ADCs were also calculated for diffuse diseases and focal lesions (94 malignant and 93 benign) of abdominal organs to evaluate the clinical usefulness of ADC. RESULTS. Location-dependent changes in water ADCs were minimal with parallel imaging factors first of 3, then of 4, and were small except for measurements at the image periphery. Acetone ADCs were saturated at mm 2 /s. Degraded image quality prevented ADC measurement of the left hepatic lobe and pancreas in 7 18 patients. There was no significant difference among ADCs of four liver segments (1.50 ± 0.24 [SD] 10 3 mm 2 /s 1.56 ± mm 2 /s) and between ADCs of the right and left kidneys (2.65 ± mm 2 /s, 2.59 ± mm 2 /s). ADC of the pancreas tail (1.65 ± mm 2 /s) was significantly lower than those of the head (1.81 ± mm 2 /s) and body (1.81 ± mm 2 /s) (p < 0.005). Renal ADCs were significantly lower in patients with renal failure (right: 2.15 ± mm 2 /s; left: 2.11 ± mm 2 /s) than in those without disease (right: 2.67 ± mm 2 /s; left: 2.60 ± mm 2 /s) (p < 0.005). ADC of pancreatic cancer was significantly higher than that of healthy pancreas (p < 0.05). ADC of renal angiomyolipoma was significantly lower than those of renal cell carcinoma and healthy renal parenchyma (p < ). CONCLUSION. Clinical ADC measurements of abdominal organs and lesions using parallel imaging appear to be reliable and useful, and the effect of parallel imaging on calculated values is considered to be minimal. ecently, diffusion-weighted MRI R and apparent diffusion coefficient (ADC) measurement have been applied to the abdomen [1 4]. The results suggest that ADC measurement can be useful in the evaluation of diffuse liver [2, 3, 5 7] and renal diseases [8 12] and for characterizing focal hepatic [2, 5, 13 17], pancreatic [18], and renal [19 21] lesions. Breath-hold single-shot spin-echo echo-planar imaging (EPI) is mainly used for diffusion-weighted imaging in the abdomen. However, the image quality suffers from blurring because of the long readout interval and from artifacts caused by high susceptibility to resonance offsets. In addition, various artifacts caused by cardiac motion and air in the lung and intestine were found to degrade image quality and diminish the reliability of ADC values in the abdominal field. Parallel imaging techniques, which use the spatial information from a phased-array multicoil to reduce the number of signals needed for a given spatial resolution, could be used to reduce the time of readout and scanning time, improving the quality of EPI [22, 23]. However, parallel imaging has been reported to have some problems. Signal intensity and signal-to-noise ratio (SNR) on the image can AJR:187, December

2 Fig. 1 Positions of bottles in phantom study. Position A indicates center, B indicates adjacent to coils, C indicates intermediate position, and D indicates periphery of image. D C A 18.0 cm change, depending on the location in the section plane. We are aware of only one report that evaluated the reliability of ADC measurements using parallel imaging [24], and it was restricted to ADC of the right hepatic lobe in young, healthy volunteers. Furthermore, to our knowledge, no systematic study using phantoms to evaluate changes of ADCs related to parallel imaging and location relative to coil geometry has been described. This study s purpose was to assess the reliability and usefulness of parallel imaging for measurement of ADC of abdominal organs and lesions. Materials and Methods Patients During a 5-month period from March 2004 to July 2004, 203 consecutive patients who were suspected of having malignant lesions of the liver, pancreas, gallbladder, kidney, intestine, and abdominal lymph nodes, or who were suspected of having diffuse liver, pancreatic, or renal disease, underwent MRI at our hospital. The institutional review board approved this retrospective study, and informed consent was obtained from all participating patients. Three patients who were referred from other hospitals and whose patient records were not available were excluded from this study. The remaining 200 patients included 122 men and 78 women, ages years (mean, 61.9 years), all of whom were eligible for this study. Four patients had undergone liver resection before the MRI examinations. Liver cirrhosis was diagnosed in 57 patients (surgically, 14; biopsy, five; clinically, 38); chronic hepatitis in 29 patients (surgically, three; biopsy, nine; clinically, 17); chronic pancreatitis in three patients; acute pancreatitis in three patients; hydronephrosis or ureteral stone in seven patients; and chronic renal failure in eight patients. Clinical diagnosis of liver cirrhosis was based on the results of 14.0 cm Receiver Coils B 9.5 cm Receiver Coils 1.5 cm 19.0 cm previous reports [25 27]. Fifty-two patients were diagnosed with cirrhosis associated with viral hepatitis (four with hepatitis B; 47 with hepatitis C; and one with both). Four patients had ethanol-induced cirrhosis and one had primary biliary cirrhosis. Primary liver cancer was diagnosed in 40 patients (resection, 14; biopsy, two); secondary liver cancer in 19 patients (resection, 19); hepatic cavernous hemangiomas in 25 patients; hepatic cysts in 11 patients; pancreatic cancer in five patients (resection, five); renal cell carcinoma in 12 patients (resection, eight); renal angiomyolipoma in six patients (resection, two); renal cysts in 30 patients; gastrointestinal cancer in six patients (resection, five); and lymph node metastasis in eight patients. The lesions for which histologic proof were not available were mainly diagnosed on the basis of pathognomonic findings from sonography, CT, and MRI, other clinical findings, and follow-up examinations in 3 12 months. Phantoms To assess the reliability of ADCs and the locationin-plane-dependent ADC changes with parallel imaging, bottle phantoms filled with water or acetone (at 24 C) were scanned applying a reduction factor for parallel imaging (parallel imaging factor) of 1 4 or without parallel imaging at various positions, including at image center, 18 and 14 cm lateral from center, and 1.5 cm from the receiver coils. Figure 1 shows the details of the phantom positioning. Imaging Technique All clinical and phantom MR studies were performed with a 1.5-T superconducting imaging system (Gyroscan Intera, Philips Medical Systems). The system provides a maximum gradient strength of 23 mt/m with a peak slew rate of 105 mt/m/msec. A body coil was used for signal transmission and a four-element phased-array multicoil for the body was used for reception. In the clinical study, all patients underwent breath-hold single-shot echo-planar diffusionweighted imaging (TR/TE = 1,500/66; matrix size = [reconstructed to ]; field of view = mm; number of excitations = 2 [for each motion probing gradient direction]; EPI factor = 33 [i.e., the number of gradient-recalled echoes per spin echo]; slice thickness and gap = 6 and 2 mm, respectively; 30 transverse slices; parallel imaging factor = 3; bandwidth = 32.2 khz; selective presaturation using inversion recovery [SPIR] for fat saturation) in addition to a routine abdominal imaging protocol that included T1-weighted dual fast gradient-recalled echo (TR/first-echo TE, second-echo TE = 126/2.3, 4.6; flip angle = 70 ; matrix size = ; field of view = mm; number of excitations = 1; slice thickness and gap = 8 and 0 mm, respectively; 30 transverse slices; parallel imaging factor = 2), T2-weighted respiratory-triggered fast spin-echo (TR/TE eff = 2,500/80; echo-train length = 9; matrix size = ; field of view = mm; number of excitations = 2; slice thickness and gap = 8 and 0 mm, respectively; 30 transverse slices; SPIR for fat saturation; parallel imaging factor = 2), and T1-weighted 3D gradient-echo (TR/TE = 4.2/1.2; flip angle = 30 ; matrix size = ; field of view = mm; number of excitations = 1; slice thickness = 8 mm; 30 transverse slices; SPIR was used for fat saturation; parallel imaging factor = 2). The single-shot technique was chosen to reduce motion-related artifacts arising with the EPI technique [1, 28]. The values of b factor were set at 0 and 600 s/mm 2 to reduce the effect of perfusion in the tissues [2, 5, 12, 14, 15, 29]. The parallel imaging factor was set at 3 to keep the EPI factor small and to reduce image blurring. Values of b factor greater than 600 and parallel imaging factor of 4 were not used considering SNR on the diffusionweighted images. The motion-probing gradient pulses were placed in the three orthogonal axes. Phase encoding direction was set anteroposteriorly in all sequences. For diffusion-weighted imaging, 15 sections were obtained during a breath-hold of 15 seconds, so two to three sequential acquisitions were required to encompass the entire upper abdomen. Saturation bands were not used for diffusionweighted imaging. In the phantom study, diffusion-weighted imaging as detailed was performed using the Gyroscan Intera MRI scanner three times for each position and for each parallel imaging factor or nonparallel imaging scans. Without using parallel imaging and with parallel imaging factors of 1, 2, 3, and 4, the shortest respective TEs were 68, 68, 62, 58, and 58 milliseconds. TE was set at 68 milliseconds for all conditions. A body coil was used for signal transmission and a four-element phased-array multicoil for the body was used for reception AJR:187, December 2006

3 ADC Measurement of Abdomen Using Parallel Imaging Image Analysis All ADCs were calculated on a workstation with standard software (Diffusion Calculation, Philips Medical Systems). The signal intensities for ADC calculation were measured by using operator-defined region-of-interest (ROI) measurements performed by the same radiologist. All clinical MR images were analyzed retrospectively. ADCs were calculated for liver (four segments), spleen, pancreas (head, body, tail), gallbladder, renal parenchyma, back muscle, and focal lesions of liver, pancreas, kidney, gastrointestinal tract, and lymph nodes. The ROIs for liver (four segments), spleen, pancreas (head, body, tail), gallbladder, renal parenchyma, and back muscle were an oval of 100 mm 2. The ROI of liver was located peripherally in each segment, and the ROI of the spleen was placed centrally. In the liver and spleen, vessels were avoided as much as possible. In the pancreas, vessels, pancreatic duct, and common bile duct were avoided as much as possible. The ROI within the gallbladder was placed in the largest possible area. The ROI of the renal parenchyma was placed peripherally in the posterior labrum. ADCs of cortex and medulla could not be separately measured because the matrix sizes used for the diffusion-weighted imaging were so small that it was difficult to distinguish these structures on the images [30]. At the time of ROI placement, the operator was aware of the location of the lesions and could refer to routine MR images but was blinded to the final diagnoses. ROI placements were checked by another experienced radiologist who was aware of the final diagnoses, and consensus opinion was then attained by the two operators for each ROI placement. The initial ROI was modified in one case of pancreatic cancer with secondary pancreatitis. ADCs were compared among four liver segments, among three pancreatic parts, and between right and left renal parenchyma to evaluate anatomic changes in ADC. For liver ADC, mean values of three subgroups with chronic hepatitis, with cirrhosis, and without liver disease were compared in each segment. Patients with fatty infiltration, hemochromatosis, malignant liver tumors, or diffuse biliary disease, or after undergoing transarterial chemoembolization, systemic chemotherapy, or biliary intervention, or with a history of acute hepatitis (cured), were excluded from analysis of these subgroups. For pancreatic ADC, the mean values of the three subgroups with chronic pancreatitis, with acute pancreatitis, and without pancreatic diseases were compared in each pancreatic part. Patients with diabetes, a history of acute pancreatitis (cured), pancreatic tumors, diffuse biliary disease, or duodenal or retroperitoneal tumors were excluded. For renal ADC, the mean values of the three subgroups with chronic renal failure, with hydronephrosis or ureteral stone, and without renal or urinary tract disease were compared in bilateral kidneys. Patients with abnormally increased serum creatinine (without a diagnosis of renal failure), malignant renal tumors, renal benign tumors larger than 5 cm, and retroperitoneal tumors were excluded. These pathologic conditions were chosen for analysis because previous reports using diffusion-weighted imaging without parallel imaging suggested their clinical usefulness for ADC measurements [2, 3, 5 9, 11 14, 16]. ADCs of patients without disease were used to establish the normal values for our system. In the ADC measurement of lesions, only lesions larger than 10 mm in diameter were analyzed because measurements of smaller lesions would not be sufficiently reliable owing to the partial volume averaging effect. The ROI within each lesion was oval and was placed on the largest possible area, including necrotic or cystic parts. For measurement purposes in each patient, a maximum of three large lesions seen on diffusion-weighted images were chosen for analysis. Thus, the measurement was performed in 94 malignant lesions and 93 benign lesions. The measured lesions included 28 primary liver cancers (mean diameter ± SD, 3.9 ± 3.1 cm), 26 secondary liver cancers (3.7 ± 2.5 cm), 19 hepatic hemangiomas (4.0 ± 1.3 cm), 13 hepatic cysts (4.1 ± 3.4 cm), five pancreatic cancers (5.3 ± 2.6 cm), three pancreatic simple cysts (2.4 ± 1.4 cm), three pancreatic pseudocysts (4.1 ± 1.8 cm), 12 renal cell carcinomas (5.7 ± 3.3 cm), eight renal angiomyolipomas (2.8 ± 1.0 cm), 42 renal cysts (2.6 ± 1.2 cm), five complicated renal cysts (2.4 ± 0.7 cm), six gastrointestinal cancers (4.1 ± 1.7 cm), and 17 lymph node metastases (3.5 ± 1.4 cm). Three follow-up cases with two intraductal papillary tumors and one serous cystadenoma of the pancreas were excluded from these measurements. Mean ADCs of the various lesion types and mean values of all hepatic segments (overall liver parenchyma), of all pancreatic parts (overall pancreatic parenchyma), and of bilateral renal parenchyma (overall renal parenchyma) were compared. In the phantom study, ADCs were calculated on the sections for the center of phantom in the z-axis. The ROI was placed at the center of phantom on the image and was an oval of 600 mm 2. Mean ADCs were compared per each parallel imaging factor and per each position. Image distortion on the phantom image was visually scored on a 3-point scale (1, severe; 2, moderate; 3, mild) by two experienced radiologists who recorded a consensus opinion. The average score was calculated for each parallel imaging factor and for each position. Statistical Analysis Statistical analysis of the mean ADCs of the liver segments, pancreas parts, liver with and without diseases, focal liver lesions, and focal renal lesions was done by one-way analysis of variance and using the Scheffé test. Statistical analysis of the mean ADCs of pancreas with and without disease, of renal parenchyma with and without disease, and of focal pancreatic lesions was done using the Kruskal-Wallis and Scheffé tests. The Student s t test was used for statistical analysis of the mean ADCs of bilateral renal parenchyma. Statistical analysis of the mean ADCs and of the image distortion scores of the phantoms was performed with the one-way analysis of variance and Scheffé test to determine the effects of parallel imaging technique and location-dependent changes. All values were expressed as mean ± SD. For all tests used, a p value of less than 0.05 was considered statistically significant. Results For measurements of ADC of acetone, values became saturated at mm 2 /s. For measurements of ADC of water, locationdependent changes in ADCs were minimal with parallel imaging factors first of 3 and then of 4, and were small except for measurements at the image periphery (Table 1). Table 2 shows the results of the image distortion scoring. With parallel imaging, image quality of the diffusion-weighted imaging was improved (Fig. 2). Tables 3 and 4 show the results of the patient studies. There was no significant difference among ADCs of the four liver segments or between ADCs of the right and left renal parenchyma. The ADC of the pancreas tail was significantly lower than those of the head and body (p < 0.005). ADCs of spleen, gallbladder, and back muscle were 1.26 ± 0.23, 3.50 ± 0.51, and 2.13 ± mm 2 /s, respectively. ADCs of the liver in patients with chronic hepatitis or cirrhosis had a nonsignificant trend toward being lower than those in patients without disease in each segment. ADC of the pancreas in patients with chronic pancreatitis had a nonsignificant trend toward being lower than those in patients without disease in each part. ADCs of renal parenchyma in patients with renal failure were significantly lower than those in patients without disease in both kidneys (p < 0.005). Mean ADCs of hydronephrosis and ureteral stones were not significantly different from those of normal renal parenchyma in both kidneys. There was no significant difference among mean ADCs of primary liver cancer, secondary AJR:187, December

4 TABLE 1: Apparent Diffusion Coefficients of Water ( 10 3 mm 2 /s, at 24 C) Parallel Imaging Factor a Center of Image liver cancer, and the overall liver parenchyma (mean values of all segments). Mean ADCs of hepatic hemangioma and cyst were significantly higher than those of overall liver parenchyma and primary and secondary liver cancers (p < ). Mean ADC of hepatic cyst was significantly higher than that of hepatic hemangioma (p < ). Mean ADC of pancreatic cancer was significantly lower than those of pancreatic simple cyst (p < ) and pseudocyst (p < ), and significantly higher than that of overall pancreatic parenchyma (mean values of all parts) (p <0.05) (Fig. 3). Mean ADCs of pancreatic simple cyst and pseudocyst were significantly higher than those of overall pancreatic parenchyma (p < ). There was no significant difference between the mean ADCs of pancreatic simple cyst and pseudocyst. Mean ADC of renal angiomyolipoma was significantly lower than those of renal cell carcinoma (p < ), renal cyst (p < ), renal complicated Location of Measurement Adjacent to Receiver Coils Intermediate Position Periphery of Image b None 2.48 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.04 Note Data are mean ± 1 SD. a No significant difference was found among apparent diffusion coefficients without parallel imaging and with parallel imaging factors of 1 4. b Mean value at periphery of image was significantly higher than values at center of image (p < ), adjacent to receiver coils (p < 0.005), and at intermediate position (p < ). TABLE 2: Distortion Scores of the Phantom Images Parallel Imaging Location of Measurement Adjacent to Receiver Periphery Factor Center of Image Coils a Intermediate Position of Image a None b 2.83 ± ± ± ± b 2.83 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.41 Note Image distortion was visually scored on a 3-point scale (1, severe; 2, moderate; 3, mild). Data are overall mean scores of acetone and water phantom images ± 1 SD. a Mean value at periphery of image was significantly lower than values at center of image (p < ), adjacent to receiver coils (p < ), and at intermediate position (p < ). Mean value adjacent to receiver coils was significantly lower than value at center of image (p < 0.05). b Mean value without parallel imaging was significantly lower than values with parallel imaging factors of 2 (p < 0.001), 3 (p < 0.001), and 4 (p < 0.005). Mean value with parallel imaging factor of 1 was significantly lower than values with parallel imaging factors of 2 (p <0.01), 3 (p < 0.01), and 4 (p <0.05). cyst (p < ), and overall renal parenchyma (mean values of bilateral kidneys) (p < ) (Fig. 4). Mean ADC of renal cyst was significantly higher than those of renal cell carcinoma, complicated cyst, and overall renal parenchyma (p < ). There was no significant difference among mean ADCs of renal cell carcinoma, complicated cyst, and overall renal parenchyma. Table 5 shows the reasons for unsuccessful ADC measurement. The number of cases with difficulty breath-holding was small. ADC could not be measured in the lateral segment of the liver in 18 patients, in the medial segment in seven patients, in the pancreas head in 16 patients, the body in 16 patients, and the tail in 10 patients because of degraded image quality. Discussion In the field of neuroradiology, several reports have discussed application of parallel imaging to diffusion-weighted imaging or to ADC measurement [28, 31, 32]. These reports suggested that parallel imaging improves image quality and allows faster clinical ADC measurement, with minimal effect on calculated values. However, there is only one report that evaluated the reliability of ADC measurement with parallel imaging in the abdomen [24], including only ADC of the right hepatic lobe in young healthy volunteers. Several recent reports have suggested the clinical application of abdominal ADC measurements [12, 19 21, 33], but without systematic study using phantoms to evaluate the potential effects of parallel imaging and location on ADC reliability. The measured ADCs in our phantom study were relatively higher than those of previous reports [5, 15, 16, 34]. This might be a result of differences in imaging sequence, workstation, and software, and suggests that ADCs should be considered as relative values, with calibration needed for each MR scanner. ADC measurements at the image periphery were not reliable, possibly because of the sensitive area of surface coils or of EPI. Our results suggest that the parallel imaging technique may help reduce artifacts and improve the reliability of the measured values. For the measurement of the ADC of acetone, the values were saturated, possibly caused by extremely low SNR in the ROIs on the diffusion-weighted images. When imaging sequences with many sections, a short acquisition time, and a single high b value are used, acetone might not be suitable as a standard substance. Our hepatic ADC measurements were in the midrange of those in recent reports [24, 35]. Compared with our results, some investigators reported lower ADCs [16, 29], whereas others reported slightly higher ADCs [1, 7, 14]. These discrepancies may come from the differences in patient population, imaging sequence used, TE, b value, or special techniques that were applied, such as peripheral pulse gating, longer acquisition time, and diffusion tensor imaging (with increased acquired signals). Previous studies did not address possible differences in ADC measurement throughout the liver [1 4, 9, 13, 14, 16, 29]; we found no differences among four liver segments. Also consistent with prior reports, we found that livers with chronic hepatitis and cirrhosis had lower a ADC than did healthy liver, and we found a similar ADC among primary and secondary liver cancer and healthy liver and a 1524 AJR:187, December 2006

5 ADC Measurement of Abdomen Using Parallel Imaging A C E Fig. 2 Diffusion-weighted images of bottle phantom. Acetone phantom was located at periphery of image (D in Fig. 1) and scanned without parallel imaging (A) and with parallel imaging factors of 1 (B), 2 (C), 3 (D), and 4 (E). Although phantom is clearly visualized on every image, image distortion is severe on images without parallel imaging and with parallel imaging factor of 1. Parallel imaging improved image quality of diffusion-weighted images. Distortion scores were assigned as 1 for images A and B and assigned as 2 for images C, D, and E. B D AJR:187, December

6 TABLE 3: Apparent Diffusion Coefficients ( 10 3 mm 2 /s) of Abdominal Organs and Diffuse Lesions Organ Overall Without Disease With Disease Liver Chronic hepatitis Cirrhosis Right posterior segment 1.52 ± 0.28 (n = 197) Right anterior segment 1.50 ± 0.24 (n = 192) Left medial segment 1.56 ± 0.28 (n = 162) Left lateral segment 1.56 ± 0.31 (n = 149) Pancreas Head 1.81 ± 0.40 (n = 174) Body 1.81 ± 0.41 (n = 167) Tail 1.65 ± 0.37 a (n = 171) Spleen 1.26 ± 0.23 (n = 185) Gallbladder 3.50 ± 0.51 (n = 151) Renal parenchyma Right 2.65 ± 0.30 (n = 193) Left 2.59 ± 0.33 (n = 191) Back muscle 2.13 ± 0.25 (n = 198) 1.55 ± 0.30 (n = 74) 1.55 ± 0.17 (n = 69) 1.61 ± 0.21 (n = 51) 1.63 ± 0.31 (n = 45) 1.82 ± 0.40 (n = 131) 1.81 ± 0.41 (n = 124) 1.65 ± 0.34 (n = 129) 2.67 ± 0.29 (n = 145) 2.60 ± 0.32 (n = 144) 1.50 ± 0.14 (n = 21) 1.46 ± 0.13 (n = 21) 1.60 ± 0.28 (n = 19) 1.60 ± 0.36 (n = 18) Chronic pancreatitis 1.71 ± ± ± 0.39 Chronic renal failure 2.15 ± 0.30 b (n = 5) 2.11 ± 0.25 b (n = 5) Note Data are mean ± 1 SD. a Mean value was significantly lower than values of pancreas head and body (p < 0.005). b Mean values were significantly lower than value of kidney without disease (p < 0.005). lower ADC for hemangioma versus cyst [2, 3, 5, 6, 8, 13, 14]. We are aware of only two publications discussing ADC of the pancreas [1, 3], each of which reported ADCs higher than those in our study. The highest pancreatic ADCs were reported by Chow et al. [1], who evaluated young healthy volunteers, unlike Ichikawa et al. [3] and us, who evaluated clinical patients with a mean age of approximately 60 years. As a person ages, the pancreas shows several age-related changes such as atrophy, fatty infiltration, and fibrosis, and our results suggest that pancreatic ADC may also change with age. Moreover, age-related changes have been reported in the structure and functions of the liver and kidney. The volume of the liver decreases, despite an increase in the size of hepatocytes, suggesting loss of liver cells. In 1.45 ± 0.13 (n = 17) 1.47 ± 0.12 (n = 17) 1.60 ± 0.19 (n = 16) 1.53 ± 0.21 (n = 15) Acute pancreatitis 1.88 ± ± ± 0.18 Hydronephrosis, ureteral stone 2.68 ± 0.08 (n = 2) 2.49 ± 0.15 (n = 5) addition, the hepatic blood flow and the synthesis of urea and cholesterol are reduced. The aging kidney is characterized by a decrease in renal blood flow and glomerular filtration rate, mainly as a result of glomerulosclerosis. These age-related factors may affect ADCs of the organs. We found ADC of the pancreatic tail to be lower than ADC of other parts of the pancreas, which is possibly caused by differences of surrounding tissues. ADC of pancreatic cancer was higher than ADC of a healthy pancreas and lower than simple and complicated cysts; however, the number of patients was small. Parenchymal ADC in chronic renal failure was significantly lower than that of healthy parenchyma, which was consistent with the previous reports [8, 12]. We did not find any significant differences in ADC between healthy and hydronephrotic kidneys. In our study population, renal dysfunction was mild in the hydronephrotic patients. Toyoshima et al. [11] reported normally functioning hydronephrotic kidneys showed ADCs similar to those of healthy kidneys, whereas dysfunctioning kidneys showed lower ADCs. Although there are a few publications on ADC measurement of renal tumors, benign and malignant tumors were not evaluated separately [19 21]. We found that angiomyolipoma had significantly lower ADC than did renal cell carcinoma, cyst, complicated cyst, and overall healthy parenchyma. Renal cell carcinoma and complicated cyst had similar ADCs to overall healthy parenchyma. ADC of the gallbladder was slightly lower than ADCs of hepatic and renal cysts and was consistent with the results of Yamada et al. [2]. ADC of back muscle has not been reported previously. Our results showed the ADC measurement adjacent to the receiver coils is sufficiently reliable and might be usable for calibrating ADC and measurement of background noise for calculation of the SNR of the images. Without parallel imaging, ADC measurements at the left hepatic lobe and pancreas are often difficult to perform, although unsuccessful measurements have not been reported. With parallel imaging, we can reduce the percentage of unsuccessful measurement to approximately 5% for the left medial segment of the hepatic lobe, 11% for the left medial segment of the liver, 9% for the pancreatic head, 10% for the pancreatic body, and 7% for the pancreatic tail. In addition, segmental ADC analysis of the liver and pancreas is possible and may be useful for the evaluation of various diffuse parenchymal diseases. In some patients, however, image degradation was still severe for the left hepatic lobe and pancreas. As for the left hepatic lobe, either cardiac or peripheral pulse triggering or reducing the number of motion-probing gradient directions might be helpful [24, 29]. However, pulse triggering requires more acquisition time, and reducing motion-probing gradient directions affects ADC of the kidney, which has anisotropic diffusion [1, 30, 36]. In the pancreas, the main causes of image degradation are thought to be susceptibility effect by gastrointestinal air and atrophy of the organ by aging. Some investigators have used the free-breathing technique for ADC measurements in the kidney to increase the number of signal acquisitions and to obtain 1526 AJR:187, December 2006

7 ADC Measurement of Abdomen Using Parallel Imaging TABLE 4: Apparent Diffusion Coefficients (ADCs) of Lesions Organs Lesion Type ADC ( 10 3 mm 2 /s) Liver Primary cancer (n = 28) 1.60 ± 0.37 Secondary cancer (n = 26) 1.51 ± 0.35 Hemangioma (n = 19) a 2.28 ± 0.67 Cyst (n = 13) a,b 3.81 ± 0.43 Overall liver parenchyma (n = 700) 1.53 ± 0.28 Pancreas Primary cancer (n = 5) c 2.32 ± 0.26 Simple cyst d 3.96 ± 0.14 Pseudocyst d 3.60 ± 0.69 Overall pancreatic parenchyma (n = 512) 1.76 ± 0.40 Kidney Renal cell carcinoma (n = 12) 2.49 ± 0.72 Angiomyolipoma (n = 8) e 1.81 ± 0.41 Cyst (n = 42) f 3.82 ± 0.39 Complicated cyst (n = 5) 2.78 ± 0.71 Overall renal parenchyma (n = 384) 2.62 ± 0.32 Stomach, intestine Primary cancer (n = 6) 2.31 ± 0.53 Lymph node Metastasis (n = 17) 1.56 ± 0.27 Note Data are mean ± 1 SD. a Mean values were significantly higher than values of overall liver and primary and secondary liver cancers (p < ). b Mean value was significantly higher than value of hepatic hemangioma (p < ). c Mean value was significantly lower than values of pancreatic simple cyst (p < ) and pseudocyst (p < ), and significantly higher than value of overall pancreatic parenchyma (p <0.05). d Mean values were significantly higher than values of overall pancreatic parenchyma (p < ). e Mean value was significantly lower than values of renal cell carcinoma (p < ), renal cyst (p < ), renal complicated cyst (p < ), and overall renal parenchyma (p < ). f Mean value was significantly higher than values of renal cell carcinoma, complicated cyst, and overall renal parenchyma (p < ). multiple and high b values [12, 37]. This technique may be applicable to other retroperitoneal organs, such as the pancreas, large intestine, and duodenum, in which respiratory artifacts are relatively smaller than in the liver and spleen. The multishot (interleaved) EPI technique is reportedly effective for ADC measurement of the kidney [36]. This technique can reduce the EPI factor and susceptibility artifacts caused by gastrointestinal and lung air, although it requires longer acquisition time to encompass the abdomen. The optimal b value and TE for abdominal diffusion-weighted imaging have not yet been determined. Some investigators recommended a b value larger than 400 s/mm 2 because it can reduce T2-shine-through and intravoxel perfusion effects [2, 5, 12, 14, 15, 29]. However, a higher b value leads to a lower SNR. For our study, the b values were set at 0 and 600 s/mm 2 to maintain SNR. A shorter TE has been recommended because it can increase SNR and reduce susceptibilityinduced image distortions [1, 24]. A smaller EPI factor also has been recommended to reduce susceptibility-induced image distortions, and we accomplished this by using parallel imaging, filling 96 lines of k-space in the phase-encoding axis with a single-shot EPI factor of only 33. This required an increase in the parallel imaging factor up to 3. We are not aware of any previously published data of abdominal diffusion-weighted imaging using a parallel imaging factor of 3. Our results sug- Fig year-old man with pathologically proven invasive ductal carcinoma of the pancreas. A and B, Tumor of pancreatic tail (arrows, A) shows hyperintensity compared with normal parenchyma on T2-weighted (A) and diffusion-weighted (B) images. (Fig. 3 continues on next page) A B AJR:187, December

8 C Fig. 3 (continued) 56-year-old man with pathologically proven invasive ductal carcinoma of the pancreas. C and D, Apparent diffusion coefficients (ADCs) were calculated (C). Tumor on ADC image shows hyperintensity compared with normal parenchyma. Regions of interest (ROIs) were placed on normal parenchyma (ROI 1, D) and tumor (ROI 2, D). ADCs of normal parenchyma and tumor were 1.66 and mm 2 /s, respectively. A Fig year-old woman with pathologically proven angiomyolipoma of kidney. A and B, Tumor in lower pole of left kidney (arrows, A) shows hyperintensity compared with normal parenchyma on T2-weighted image (A) and hypointensity on diffusionweighted image (B). (Fig. 4 continues on next page) gest that reducing the EPI factor is effective for improving image quality. Further studies are needed to determine the feasibility of ADC measurement with a parallel imaging factor of 4. Our study has several limitations. First, only a small number of patients had histopathologic proof. However, our results show the average values in clinical populations. In addition, most cases of cirrhosis and chronic hepatitis in our population were diagnosed without histologic proof the diagnoses were based on laboratory and imaging criteria. The sensitivity and specificity for the noninvasive distinction between cirrhosis and chronic hepatitis are reported to be % and %, respectively [25 27]. Second, direct comparison of diffusion-weighted images with and without parallel imaging was not performed in our retrospective clinical study and should be done in clinical cases to confirm our results in the phantom part of our study. Third, only the b value of 600 s/mm 2 was evaluated. Further evaluation of higher b D B 1528 AJR:187, December 2006

9 ADC Measurement of Abdomen Using Parallel Imaging C Fig. 4 (continued) 40-year-old woman with pathologically proven angiomyolipoma of kidney. C and D, Apparent diffusion coefficients (ADCs) were calculated (C). Tumor shows hypointensity compared with normal parenchyma on ADC image. Regions of interest (ROIs) were placed on normal parenchyma (ROI 1, D) and tumor (ROI 2, D). ADCs of normal parenchyma and tumor were 2.85 and mm 2 /s, respectively. TABLE 5: Overall Reasons for Unsuccessful Apparent Diffusion Coefficient Measurement Poor Image Quality Difficulty of Breath-hold Atrophy of Organ Post Resection Replaced by Lesion Out of Field of View Organs Liver Right posterior segment Right anterior segment Left medial segment Left lateral segment Pancreas Head Body Tail Spleen Gallbladder Renal parenchyma Right Left Back muscle Note Data are numbers of patients. values is needed, because higher b values can reduce the effect of perfusion on the calculated ADC values. Fourth, clinical diffusionweighted imaging without parallel imaging, or with parallel imaging factors less than 3, was not obtained. Fifth, we evaluated only ADC of renal parenchyma because of the difficulty in distinguishing cortex and medulla parenchyma [30]. In addition, our imaging sequence had a small matrix size and we had many elderly patients. Finally, posttreatment lesions were not evaluated, although Kamel et al. [38] report the usefulness of diffusionweighted imaging in the posttreatment evaluation of malignant liver tumors. In conclusion, clinical ADC measurements of abdominal organs and lesions using parallel imaging appear to be reliable and useful, and the effect of parallel imaging on calculated values is considered minimal. However, some problems still remain in measurements at the left lobe of the liver and pancreas. Measurement at the periphery of the image should be avoided. Acknowledgment We wish to express special thanks to Kazuhiro Kubo of Kobe University Hospital for his outstanding technical assistance. References 1. Chow LC, Bammer R, Moseley ME, Sommer FG. Single breath-hold diffusion-weighted imaging of the abdomen. J Magn Reson Imaging 2003; 18: Yamada I, Aung W, Himeno Y, Nakagawa T, Shibuya H. Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. Radiology 1999; 210: Ichikawa T, Haradome H, Hachiya J, Nitatori T, Araki T. Diffusion-weighted MR imaging with single-shot echo-planar imaging in the upper abdomen: preliminary clinical experience in 61 patients. Abdom Imaging 1999; 24: Yamashita Y, Tang Y, Takahashi M. Ultrafast MR imaging of the abdomen: echo planar imaging and diffusion-weighted imaging. J Magn Reson Imaging 1998; 8: Kim T, Murakami T, Takahashi S, Hori M, Tsuda K, Nakamura H. Diffusion-weighted single-shot D AJR:187, December

10 echoplanar MR imaging for liver disease. AJR 1999; 173: Amano Y, Kumazaki T, Ishihara M. Single-shot diffusion-weighted echo-planar imaging of normal and cirrhotic livers using a phased-array multicoil. Acta Radiol 1998; 39: Boulanger Y, Amara M, Lepanto L, et al. Diffusionweighted MR imaging of the liver of hepatitis C patients. NMR Biomed 2003; 16: Namimoto T, Yamashita Y, Mitsuzaki K, Nakayama Y, Tang Y, Takahashi M. Measurement of the apparent diffusion coefficient in diffuse renal disease by diffusion-weighted echo-planar MR imaging. J Magn Reson Imaging 1999; 9: Chan JH, Tsui EY, Luk SH, et al. MR diffusionweighted imaging of kidney: differentiation between hydronephrosis and pyonephrosis. Clin Imaging 2001; 25: Verswijvel G, Vandecaveye V, Gelin G, et al. Diffusion-weighted MR imaging in the evaluation of renal infection: preliminary results. JBR-BTR 2002; 85: Toyoshima S, Noguchi K, Seto H, Shimizu M, Watanabe N. Functional evaluation of hydronephrosis by diffusion-weighted MR imaging: relationship between apparent diffusion coefficient and split glomerular filtration rate. Acta Radiol 2000; 41: Thoeny HC, De Keyzer F, Oyen RH, Peeters RR. Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience. Radiology 2005; 235: Namimoto T, Yamashita Y, Sumi S, Tang Y, Takahashi M. Focal liver masses: characterization with diffusion-weighted echo-planar MR imaging. Radiology 1997; 204: Ichikawa T, Haradome H, Hachiya J, Nitatori T, Araki T. Diffusion-weighted MR imaging with a single-shot echoplanar sequence: detection and characterization of focal hepatic lesions. AJR 1998; 170: Taouli B, Vilgrain V, Dumont E, Daire JL, Fan B, Menu Y. Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients. Radiology 2003; 226: Moteki T, Horikoshi H, Oya N, Aoki J, Endo K. Evaluation of hepatic lesions and hepatic parenchyma using diffusion-weighted reordered turbo- FLASH magnetic resonance images. J Magn Reson Imaging 2002; 15: Chan JH, Tsui EY, Luk SH, et al. Diffusionweighted MR imaging of the liver: distinguishing hepatic abscess from cystic or necrotic tumor. Abdom Imaging 2001; 26: Yamashita Y, Namimoto T, Mitsuzaki K, et al. Mucin-producing tumor of the pancreas: diagnostic value of diffusion-weighted echo-planar MR imaging. Radiology 1998; 208: Squillaci E, Manenti G, Di Stefano F, Miano R, Strigari L, Simonetti G. Diffusion-weighted MR imaging in the evaluation of renal tumours. J Exp Clin Cancer Res 2004; 23: Squillaci E, Manenti G, Cova M, et al. Correlation of diffusion-weighted MR imaging with cellularity of renal tumours. Anticancer Res 2004; 24: Cova M, Squillaci E, Stacul F, et al. Diffusionweighted MRI in the evaluation of renal lesions: preliminary results. Br J Radiol 2004; 77: Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P. SENSE: sensitivity encoding for fast MRI. Magn Reson Med 1999; 42: Kurihara Y, Yokushiji YK, Tani I, Nakajima Y, Van Cauteren M. Coil sensitivity encoding in MR imaging: advantages and disadvantages in clinical practice. AJR 2002; 178: Taouli B, Martin AJ, Qayyum A, et al. Parallel imaging and diffusion tensor imaging for diffusionweighted MRI of the liver: preliminary experience in healthy volunteers. AJR 2004; 183: Awaya H, Mitchell DG, Kamishima T, Holland G, Ito K, Matsumoto T. Cirrhosis: modified caudateright lobe ratio. Radiology 2002; 224: Ikeda K, Saitoh S, Kobayashi M, et al. Distinction between chronic hepatitis and liver cirrhosis in patients with hepatitis C virus infection: practical discriminant function using common laboratory data. Hepatol Res 2000; 18: Wai CT, Greenson JK, Fontana RJ, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 2003; 38: Bammer R, Keeling SL, Augustin M, et al. Improved diffusion-weighted single-shot echo-planar imaging (EPI) in stroke using sensitivity encoding (SENSE). Magn Reson Med 2001; 46: Murtz P, Flacke S, Traber F, van den Brink JS, Gieseke J, Schild HH. Abdomen: diffusionweighted MR imaging with pulse-triggered singleshot sequences. Radiology 2002; 224: Fukuda Y, Ohashi I, Hanafusa K, et al. Anisotropic diffusion in kidney: apparent diffusion coefficient measurements for clinical use. J Magn Reson Imaging 2000; 11: Bammer R, Auer M, Keeling SL, et al. Diffusion tensor imaging using single-shot SENSE-EPI. Magn Reson Med 2002; 48: Willinek WA, Gieseke J, von Falkenhausen M, Neuen B, Schild HH, Kuhl CK. Sensitivity encoding for fast MR imaging of the brain in patients with stroke. Radiology 2003; 228: Nasu K, Kuroki Y, Kuroki S, Murakami K, Nawano S, Moriyama N. Diffusion-weighted single shot echo planar imaging of colorectal cancer using a sensitivity-encoding technique. Jpn J Clin Oncol 2004; 34: Bihan DL, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986; 161: Chiu FY, Jao JC, Chen CY, et al. Effect of intravenous gadolinium-dtpa on diffusion-weighted magnetic resonance images for evaluation of focal hepatic lesions. J Comput Assist Tomogr 2005; 29: Ries M, Jones RA, Basseau F, Moonen CT, Grenier N. Diffusion tensor MRI of the human kidney. J Magn Reson Imaging 2001; 14: Siegel CL, Aisen AM, Ellis JH, Londy F, Chenevert TL. Feasibility of MR diffusion studies in the kidney. J Magn Reson Imaging 1995; 5: Kamel IR, Bluemke DA, Ramsey D, et al. Role of diffusion-weighted imaging in estimating tumor necrosis after chemoembolization of hepatocellular carcinoma. AJR 2003; 181: AJR:187, December 2006