Gastrointestinal Imaging • Original Research Chen et al. CT Versus MRI for Presurgical Evaluation of Pancreatic Cancer
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Gastrointestinal Imaging Original Research
Presurgical Evaluation of Pancreatic Cancer: A Comprehensive Imaging Comparison of CT Versus MRI Fang-Ming Chen1 Jian-Ming Ni Zhui-Yang Zhang Lei Zhang Bin Li Chun-Juan Jiang Chen FM, Ni JM, Zhang ZY, Zhang L, Li B, Jiang CJ
OBJECTIVE. The purpose of this study was to compare comprehensive CT and MRI in the presurgical evaluation of pancreatic cancer. MATERIALS AND METHODS. Thirty-eight patients with pathologically proven pancreatic cancer were included in a retrospective study. CT with negative-contrast CT cholangiopancreatography and CT angiography (CTA) (CT image set) versus MRI with MRCP and MR angiography (MRI image set) were analyzed independently by two reviewers for tumor detection, extension, metastasis, vascular invasion, and resectability. These results were compared with the surgical and pathologic findings. RESULTS. The rate of detection of tumors was higher with MRI than with CT but not significantly so (reviewer 1, p = 1.000; reviewer 2, p = 0.500). In the evaluation of vessel involvement, nodal status, and resectability, although CT had higher ROC AUC values than did MRI (reviewer 1, 0.913 vs 0.858, 0.613 vs 0.503, and 0.866 vs 0.774; reviewer 2, 0.879 vs 0.849, 0.640 vs 0.583, and 0.830 vs 0.815), the differences were not statistically significant (p = 0.189 vs 0.494, 0.328 vs 0.244, and 0.193 vs 0.813 for reviewers 1 and 2). In the evaluation of tumor extension and organ metastases in the 38 patients, correct diagnosis of one of two liver metastases was achieved with both image sets, one case of omental and one case of peritoneal seeding were underestimated, and one case of stomach invasion was overestimated. CONCLUSION. MRI and CT had similar performance in the presurgical evaluation of pancreatic cancer. ancreatic cancer (PC) is among the leading causes of cancer-related deaths around the world. According to a 2012 review [1], the relative 5-year overall survival rate is 5–18%. Complete surgical resection with chemotherapy offers the best outcome in this particular cancer [2]. However, early presurgical diagnosis of PC remains difficult with noninvasive imaging modalities [3, 4]. The major difficulties involve detection of small PC tumors [1] and accurate TNM staging, particularly in assessing vascular structure and microspread (i.e., nodal involvement and peritoneal seeding) [5]. Some studies have shown that endoscopic ultrasound has higher sensitivity and specificity than CT and MRI in the diagnosis of PC, especially for smaller tumors (≤ 2 cm) [1]. However, endoscopic ultrasound is an invasive technique, and successful procedures are operator dependent [5]. With the advent of MDCT, which affords submillimeter scanning and reconstruction
P
Keywords: CT, MRI, pancreatic cancer, presurgical evaluation DOI:10.2214/AJR.15.15236 Received July 1, 2015; accepted after revision October 26, 2015. 1
All authors: Department of Radiology, Wuxi Second People’s Hospital Affiliated to Nanjing Medical University, 68 Zhongshan Rd, Jiangsu 214002, PR China. Address correspondence to Z. Y. Zhang ([email protected]).
AJR 2016; 206:526–535 0361–803X/16/2063–526 © American Roentgen Ray Society
526
coupled with a variety of postprocessing techniques, such as high-quality multiplanar reformation, CT angiography (CTA), and negativecontrast CT cholangiopancreatography, images can be acquired simultaneously [6–11]. The additional diagnostic value of negative-contrast CT cholangiopancreatography with minimum intensity projection allows better definition of sites of biliary obstruction [6] and plays a key complementary role in identifying each of the periampullary tumors of four origins [10]. Thus, it is necessary to reestimate their role in patients with suspected PC. Although MRI has comparable performance to CT because multiparametric images are generated [12–15], to our knowledge, there have been no reports regarding CT with negative-contrast CT cholangiopancreatography and CTA versus MRI with MRCP and MR angiography (MRA) in the preoperative evaluation of PC. The purpose of this study was to conduct a comprehensive presurgical imaging comparison of CT and MRI in patients with PC.
AJR:206, March 2016
CT Versus MRI for Presurgical Evaluation of Pancreatic Cancer
Downloaded from www.ajronline.org by The Chinese University on 02/28/16 from IP address 137.189.171.235. Copyright ARRS. For personal use only; all rights reserved
Materials and Methods Patient Selection
Our institutional review board approved this retrospective study, and informed consent was not required. From January 2008 to November 2014, patients with clinically suspected PC were identified from the database of our hospital information system. The inclusion criteria were as follows: PC treated surgically (including curative and palliative operations) and had detailed operative records; no chemoradiotherapy before either CT (unenhanced and dual-phase contrast-enhanced CT with negative-contrast CT cholangiopancreatography) or MRI (MRCP and dynamic contrastenhanced examinations); interval between CT or MRI examination and surgery less than 1 month; and final pathologic diagnosis based on biopsy of surgical specimen obtained at laparotomy. Of the 137 patients initially included, 99 patients were excluded from the study for the following reasons: CT without MRI (n = 59) or MRI without CT (n = 9); no surgical exploration instead of endoscopic nasobiliary drainage before CT or MRI (n = 8); histologic proof of PC obtained only by means of endoscopic biopsy (n = 19); and interval greater than 1 month between CT or MRI examination and surgery (n = 4). The other 38 patients (20 men, 18 women; age range, 47–82 years; mean, 64.5 years) composed the study population. The mean interval between CT and MRI examinations was 3.2 days (range, 1–10 days). The mean interval between imaging and surgery was 8.8 days (range, 1–24 days) for CT and 6.2 days (1–21 days) for MRI. At many
institutions [16–18], as it is at ours, CT is the preferred method for initial imaging of patients with suspected PC because it is fast and simple to perform and is well tolerated [13]. Although MRI has been found to be equally sensitive and specific in the staging of PC [12, 13, 17], it is not as widely used as CT as the primary imaging modality because of cost and lack of availability [17, 18].
cholangiopancreatography with a low-spatial-resolution algorithm for reducing image noise. The other parameters were as follows: slice thickness, 0.5–1.0 mm; reconstruction interval, 0.6–0.8 mm; matrix, 512 × 512; FOV, 22–30 cm2. All reconstructed 2D source images (volume data) were transferred to the workstation (Advantage Workstation version 3.1, GE Healthcare).
CT
MRI
All CT scans were obtained with an MDCT scanner (Aquilion 64, Toshiba Medical Systems). The standard scanning protocol at our hospital consists of unenhanced and biphasic contrastenhanced scans. An automatic trigger scanning mode with a 5-second delay was used when an ROI was set on the descending aorta, for which the preset CT number was 200 HU. For this mode, the arterial and portal venous phases were set at delays of 20–30 and 60–68 seconds after the start of the injection of 90–100 mL of nonionic contrast agent (ioversol, Optiray 320, Tyco Healthcare) at a rate of 3–4 mL/s through an antecubital vein. The parameters were as follows: 120 kVp; 0.5-second scanning time per rotation; detector collimation, 1.0 mm × 32 or 0.5 mm × 64; pitch factor, 0.844 or 0.828; tube current with automatic dose modulation ranging, 91–380 mA; FOV, 30–34 cm2. For the arterial and portal venous phase raw data, volume data were automatically reconstructed with both a slice thickness and a reconstruction interval of 1.0 mm. The portal venous phase raw data were reconstructed for negative-contrast CT
MRI was performed with a 1.5-T (Signa Excite, GE Healthcare) (n = 24) or 3-T (Magnetom Skyra, Siemens Healthcare) (n = 14) MRI system with an eight-channel phased-array body coil. The examination protocol included the following sequences at both 1.5 and 3 T: axial unenhanced T1-weighted imaging with in- and out-of-phase fast spoiled gradient-recalled echo or volume-interpolated breathhold examination; axial T2-weighted imaging with fast recovery fast spin-echo (FSE) or periodically rotated overlapping parallel lines with enhanced reconstruction technique (Blade, a Siemens Healthcare implementation of this technique); coronal image with fast imaging employing steady-state acquisition or HASTE; coronal oblique thick-slab MRCP with single-shot FSE or HASTE with a breath-hold and acquisition of 6–12 images at a 15–30° rotation for each; and coronal oblique 3D MRCP with fast recovery FSE or spatial and chemical-shift encoded excitation combined with a respiratory-gated sequence. For dynamic contrast-enhanced MRI, a single breath-hold was used for each of the following dynamic sequences. One sequence included axial un-
TABLE 1: Sequences and Parameters for 1.5- and 3-T MRI Flip Angle Section Intersection (°) Thickness (mm) Gap (mm)
TR/TE (ms) Sequence
Coverage (mm)
FOV (cm2)
Matrix
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
185/4.88, 185/2.33
4.1/2.46, 4.1/1.23
80
9
8
3.3
2
0
147–210 (179)
189–221 (195)
38
38
288 × 170
288 × 187
6000–8000/ 88.6–89.3
4281–12,349/ 80
90
160
8
6
2
1.2
133–210 (180)
166–209 (204)
38
38
288 × 224 256 × 256
3.4/1.5
1400/87
55
180
6
5
1
1
120–147 (138)
150–174 (170)
35
40
256 × 224 256 × 256
6000/1113–1148
4500/735
90
180
50
50
0
15
50
50
23–32
30
288 × 288 269 × 384
2800–4300/ 850–1100
4783–7413/ 698
90
140
2
1.5
−1
0
84–124 (109)
64–96 (77) 20–37
38
288 × 256 376 × 384
Axial T1-weighted
3.7/1.8
4.3/1.99
12
9
4.4
3
−2.2 −0.8
174–209 (185)
189–213 (195)
40
38
288 × 224
384 × 218
Coronal T1-weighted
4.2/2.0
5.48/2.46
12
9
4.4
3
−2.2 −0.8
147–183 (168)
153–189 (183)
40
40
300 × 200
291 × 416
Unenhanced Axial T1-weighted in and out of phase Axial T2-weighted Coronal MRCP Thick slab 3D Contrast-enhanced MRI
Note—Values in parentheses are means.
AJR:206, March 2016 527
Downloaded from www.ajronline.org by The Chinese University on 02/28/16 from IP address 137.189.171.235. Copyright ARRS. For personal use only; all rights reserved
Chen et al. enhanced, arterial, and axial or coronal portal venous phases; coronal equilibrium phase; and axial delayed phase imaging with liver acceleration volume acquisition technique. The other sequence included axial unenhanced, early and late arterial, and portal venous phases; coronal equilibrium phase; and axial delayed phase imaging with volume-interpolated breath-hold examination technique. The arterial, portal venous, equilibrium, and delayed phase images were obtained 18–25 seconds (36–40 seconds for the late arterial phase on the 3-T system), 60 seconds, 120–180 seconds, and 300–360 seconds after the start of the injection of 15–20 mL of gadodiamide (Omniscan, GE Healthcare) through an antecubital vein at a rate of 2 mL/s. Fat suppression was regularly used for T2-weighted imaging, thick-slab MRCP, volume acquisition for 3D MRCP, and contrast-enhanced MRI sequences. The acquisition parameters and sequences for MRI are listed in Table 1. The unenhanced and contrast-enhanced T1and T2-weighted images, thick-slab MRCP, and the source images for 3D MRCP were transferred to the workstations (Advantage Workstation version 4.3, GE Healthcare; Syngo Multimodality Workplace version D13, Siemens Healthcare). A radiologist with 8 years of experience in abdominal CT and MRI undertook the CT and MR image postprocessing at each of the workstations. The radiologist first created 2D CT images, including multiplanar reformations and curved planar reconstructions with the portal venous phase volume data and then generated negative-contrast CT cholangiopancreatograms with 3D tools as described in previous reports [10, 19]. For 3D MRCP, a 3D maximum-intensity-projection (MIP) tool was used to create 3D MRCP and MIP images saved as negative-contrast CT cholangiopancreatograms. For CTA and MRA, both thick-slab (thickness, 32–64 mm) and 3D CT and MR arteriograms and portovenograms were created with MIP and volume-rendering techniques and the arterial and portal venous phase data. All of the CT and MR images were transferred to a PACS (MultiView with Synapse software, Fujifilm Medical Systems).
ers’ learning bias, a 2-week interval was observed between the two readings, and the images were provided randomly from the two image sets. The reviewers were asked to evaluate detection of the tumor as visible or invisible; to assess the presence or absence of peripancreatic major organs, vessel involvement, or metastases; and to determine resectability according to the evaluation criteria (described later) on CT or MR images. The assessment results were compared with the surgical and the pathologic records. PC was defined at contrast-enhanced CT and MRI as a low- or high-attenuation or hypointense or hyperintense mass compared with the surrounding pancreatic parenchyma [3, 14, 15]. If no mass was discerned, indirect signs, including focal contour changes in the pancreas with abrupt termination of the bile duct, pancreatic duct, or both (double-duct sign) or the presence of the four-segment sign were suggestive of PC with both modalities [20, 21]. Once a mass was found, the reviewers further measured the maximal diameter of the low- or high-attenuation or hypointense or hyperintense region. Peripancreatic major organ (i.e., stomach or colon) invasion was considered present if a suspected low-attenuation or hypointense lesion directly invaded or reached the surface of the structures [8]. Regional lymph node evaluation followed the Japanese Pancreas Society classification [22]. Nodal metastasis was considered present when the shortaxis diameter was longer than 10 mm or when central necrosis was present at any size or its attenuation or signal intensity was greater than that of liver parenchyma in the portal venous phase [13, 23]. For the diagnostic criteria for vascular invasion in this study, we used the three-criterion image grading system suggested by Valls et al. [24] and modified in more recent literature [18, 25]. We graded the tumor-to-vessel contact for the five major peripancreatic vessels (celiac artery, hepatic artery, superior mesenteric artery [SMA] and vein, and portal vein) as follows: imaging grade 0, no contiguity between tumor and vessel; 1, tumor-to-vessel contiguity ≤ 50%; and 2, tumor-to-vessel contiguity > 50%, including complete vessel occlusion. This evaluation required approximately 5–10 minutes for each image set per patient.
Image Analysis
Criteria for Unresectability at CT and MRI
Image Postprocessing
Two radiologists (one with 14 years of experience in abdominal CT, the other with 8 years of experience in MRI) independently evaluated the two image sets (both postprocessing and source images) on the PACS screen. The CT set consisted of 2D CT images including negative-contrast CT cholangiopancreatograms and CTA images. The MRI set consisted of 2D MR images including MRCP and MRA images. To minimize the read-
528
According to the defined criteria, a tumor was considered unresectable if one or more of the following findings was present on CT or MR images. First, the tumor-to-vessel contiguity reached imaging grade 2, including the superior mesenteric–to–portal vein confluence [18, 26]. Second, peripancreatic organ involvement, such as of the stomach or colon [1, 13], other than choledochal or duodenal invasion was present, because the in-
vaded choledochal or duodenal organs can be resected en bloc during a radical operation in patients with PC. Third, distant metastasis, such as to the liver, consisted of solid low-attenuation or hypointense masses with poor margin and rim enhancement on contrast-enhanced images [18], peritoneum and omentum presented with nodular thickening and contrast enhancement, or ascites presented without an underlying systemic condition [18, 27]. Fourth, positive lymph nodes were present around the celiac artery (lymph node station 9) or along the left lateral SMA (station 14) or abdominal aorta (station 16), as described in the literature [22, 28].
Criteria for Unresectability at Surgery
In this study, peripancreatic vessel involvement was also categorized into three surgical grades according to exploration records: 0, separable peripancreatic vessel without adherence to tumor; 1, peripancreatic vessel adherent to the tumor but separable; and 2, peripancreatic vessel inseparable from or encased within the tumor. Patients were considered to have surgically unresectable tumors on the basis of the following criteria. First, a peripancreatic vessel was inseparable from or encased within the tumor (surgical grade 2) [12]. Although limited invasion of the portal or superior mesenteric vein (
Downloaded from www.ajronline.org by The Chinese University on 02/28/16 from IP address 137.189.171.235. Copyright ARRS. For personal use only; all rights reserved
Gastrointestinal Imaging Original Research
Presurgical Evaluation of Pancreatic Cancer: A Comprehensive Imaging Comparison of CT Versus MRI Fang-Ming Chen1 Jian-Ming Ni Zhui-Yang Zhang Lei Zhang Bin Li Chun-Juan Jiang Chen FM, Ni JM, Zhang ZY, Zhang L, Li B, Jiang CJ
OBJECTIVE. The purpose of this study was to compare comprehensive CT and MRI in the presurgical evaluation of pancreatic cancer. MATERIALS AND METHODS. Thirty-eight patients with pathologically proven pancreatic cancer were included in a retrospective study. CT with negative-contrast CT cholangiopancreatography and CT angiography (CTA) (CT image set) versus MRI with MRCP and MR angiography (MRI image set) were analyzed independently by two reviewers for tumor detection, extension, metastasis, vascular invasion, and resectability. These results were compared with the surgical and pathologic findings. RESULTS. The rate of detection of tumors was higher with MRI than with CT but not significantly so (reviewer 1, p = 1.000; reviewer 2, p = 0.500). In the evaluation of vessel involvement, nodal status, and resectability, although CT had higher ROC AUC values than did MRI (reviewer 1, 0.913 vs 0.858, 0.613 vs 0.503, and 0.866 vs 0.774; reviewer 2, 0.879 vs 0.849, 0.640 vs 0.583, and 0.830 vs 0.815), the differences were not statistically significant (p = 0.189 vs 0.494, 0.328 vs 0.244, and 0.193 vs 0.813 for reviewers 1 and 2). In the evaluation of tumor extension and organ metastases in the 38 patients, correct diagnosis of one of two liver metastases was achieved with both image sets, one case of omental and one case of peritoneal seeding were underestimated, and one case of stomach invasion was overestimated. CONCLUSION. MRI and CT had similar performance in the presurgical evaluation of pancreatic cancer. ancreatic cancer (PC) is among the leading causes of cancer-related deaths around the world. According to a 2012 review [1], the relative 5-year overall survival rate is 5–18%. Complete surgical resection with chemotherapy offers the best outcome in this particular cancer [2]. However, early presurgical diagnosis of PC remains difficult with noninvasive imaging modalities [3, 4]. The major difficulties involve detection of small PC tumors [1] and accurate TNM staging, particularly in assessing vascular structure and microspread (i.e., nodal involvement and peritoneal seeding) [5]. Some studies have shown that endoscopic ultrasound has higher sensitivity and specificity than CT and MRI in the diagnosis of PC, especially for smaller tumors (≤ 2 cm) [1]. However, endoscopic ultrasound is an invasive technique, and successful procedures are operator dependent [5]. With the advent of MDCT, which affords submillimeter scanning and reconstruction
P
Keywords: CT, MRI, pancreatic cancer, presurgical evaluation DOI:10.2214/AJR.15.15236 Received July 1, 2015; accepted after revision October 26, 2015. 1
All authors: Department of Radiology, Wuxi Second People’s Hospital Affiliated to Nanjing Medical University, 68 Zhongshan Rd, Jiangsu 214002, PR China. Address correspondence to Z. Y. Zhang ([email protected]).
AJR 2016; 206:526–535 0361–803X/16/2063–526 © American Roentgen Ray Society
526
coupled with a variety of postprocessing techniques, such as high-quality multiplanar reformation, CT angiography (CTA), and negativecontrast CT cholangiopancreatography, images can be acquired simultaneously [6–11]. The additional diagnostic value of negative-contrast CT cholangiopancreatography with minimum intensity projection allows better definition of sites of biliary obstruction [6] and plays a key complementary role in identifying each of the periampullary tumors of four origins [10]. Thus, it is necessary to reestimate their role in patients with suspected PC. Although MRI has comparable performance to CT because multiparametric images are generated [12–15], to our knowledge, there have been no reports regarding CT with negative-contrast CT cholangiopancreatography and CTA versus MRI with MRCP and MR angiography (MRA) in the preoperative evaluation of PC. The purpose of this study was to conduct a comprehensive presurgical imaging comparison of CT and MRI in patients with PC.
AJR:206, March 2016
CT Versus MRI for Presurgical Evaluation of Pancreatic Cancer
Downloaded from www.ajronline.org by The Chinese University on 02/28/16 from IP address 137.189.171.235. Copyright ARRS. For personal use only; all rights reserved
Materials and Methods Patient Selection
Our institutional review board approved this retrospective study, and informed consent was not required. From January 2008 to November 2014, patients with clinically suspected PC were identified from the database of our hospital information system. The inclusion criteria were as follows: PC treated surgically (including curative and palliative operations) and had detailed operative records; no chemoradiotherapy before either CT (unenhanced and dual-phase contrast-enhanced CT with negative-contrast CT cholangiopancreatography) or MRI (MRCP and dynamic contrastenhanced examinations); interval between CT or MRI examination and surgery less than 1 month; and final pathologic diagnosis based on biopsy of surgical specimen obtained at laparotomy. Of the 137 patients initially included, 99 patients were excluded from the study for the following reasons: CT without MRI (n = 59) or MRI without CT (n = 9); no surgical exploration instead of endoscopic nasobiliary drainage before CT or MRI (n = 8); histologic proof of PC obtained only by means of endoscopic biopsy (n = 19); and interval greater than 1 month between CT or MRI examination and surgery (n = 4). The other 38 patients (20 men, 18 women; age range, 47–82 years; mean, 64.5 years) composed the study population. The mean interval between CT and MRI examinations was 3.2 days (range, 1–10 days). The mean interval between imaging and surgery was 8.8 days (range, 1–24 days) for CT and 6.2 days (1–21 days) for MRI. At many
institutions [16–18], as it is at ours, CT is the preferred method for initial imaging of patients with suspected PC because it is fast and simple to perform and is well tolerated [13]. Although MRI has been found to be equally sensitive and specific in the staging of PC [12, 13, 17], it is not as widely used as CT as the primary imaging modality because of cost and lack of availability [17, 18].
cholangiopancreatography with a low-spatial-resolution algorithm for reducing image noise. The other parameters were as follows: slice thickness, 0.5–1.0 mm; reconstruction interval, 0.6–0.8 mm; matrix, 512 × 512; FOV, 22–30 cm2. All reconstructed 2D source images (volume data) were transferred to the workstation (Advantage Workstation version 3.1, GE Healthcare).
CT
MRI
All CT scans were obtained with an MDCT scanner (Aquilion 64, Toshiba Medical Systems). The standard scanning protocol at our hospital consists of unenhanced and biphasic contrastenhanced scans. An automatic trigger scanning mode with a 5-second delay was used when an ROI was set on the descending aorta, for which the preset CT number was 200 HU. For this mode, the arterial and portal venous phases were set at delays of 20–30 and 60–68 seconds after the start of the injection of 90–100 mL of nonionic contrast agent (ioversol, Optiray 320, Tyco Healthcare) at a rate of 3–4 mL/s through an antecubital vein. The parameters were as follows: 120 kVp; 0.5-second scanning time per rotation; detector collimation, 1.0 mm × 32 or 0.5 mm × 64; pitch factor, 0.844 or 0.828; tube current with automatic dose modulation ranging, 91–380 mA; FOV, 30–34 cm2. For the arterial and portal venous phase raw data, volume data were automatically reconstructed with both a slice thickness and a reconstruction interval of 1.0 mm. The portal venous phase raw data were reconstructed for negative-contrast CT
MRI was performed with a 1.5-T (Signa Excite, GE Healthcare) (n = 24) or 3-T (Magnetom Skyra, Siemens Healthcare) (n = 14) MRI system with an eight-channel phased-array body coil. The examination protocol included the following sequences at both 1.5 and 3 T: axial unenhanced T1-weighted imaging with in- and out-of-phase fast spoiled gradient-recalled echo or volume-interpolated breathhold examination; axial T2-weighted imaging with fast recovery fast spin-echo (FSE) or periodically rotated overlapping parallel lines with enhanced reconstruction technique (Blade, a Siemens Healthcare implementation of this technique); coronal image with fast imaging employing steady-state acquisition or HASTE; coronal oblique thick-slab MRCP with single-shot FSE or HASTE with a breath-hold and acquisition of 6–12 images at a 15–30° rotation for each; and coronal oblique 3D MRCP with fast recovery FSE or spatial and chemical-shift encoded excitation combined with a respiratory-gated sequence. For dynamic contrast-enhanced MRI, a single breath-hold was used for each of the following dynamic sequences. One sequence included axial un-
TABLE 1: Sequences and Parameters for 1.5- and 3-T MRI Flip Angle Section Intersection (°) Thickness (mm) Gap (mm)
TR/TE (ms) Sequence
Coverage (mm)
FOV (cm2)
Matrix
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
1.5 T
3T
185/4.88, 185/2.33
4.1/2.46, 4.1/1.23
80
9
8
3.3
2
0
147–210 (179)
189–221 (195)
38
38
288 × 170
288 × 187
6000–8000/ 88.6–89.3
4281–12,349/ 80
90
160
8
6
2
1.2
133–210 (180)
166–209 (204)
38
38
288 × 224 256 × 256
3.4/1.5
1400/87
55
180
6
5
1
1
120–147 (138)
150–174 (170)
35
40
256 × 224 256 × 256
6000/1113–1148
4500/735
90
180
50
50
0
15
50
50
23–32
30
288 × 288 269 × 384
2800–4300/ 850–1100
4783–7413/ 698
90
140
2
1.5
−1
0
84–124 (109)
64–96 (77) 20–37
38
288 × 256 376 × 384
Axial T1-weighted
3.7/1.8
4.3/1.99
12
9
4.4
3
−2.2 −0.8
174–209 (185)
189–213 (195)
40
38
288 × 224
384 × 218
Coronal T1-weighted
4.2/2.0
5.48/2.46
12
9
4.4
3
−2.2 −0.8
147–183 (168)
153–189 (183)
40
40
300 × 200
291 × 416
Unenhanced Axial T1-weighted in and out of phase Axial T2-weighted Coronal MRCP Thick slab 3D Contrast-enhanced MRI
Note—Values in parentheses are means.
AJR:206, March 2016 527
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Chen et al. enhanced, arterial, and axial or coronal portal venous phases; coronal equilibrium phase; and axial delayed phase imaging with liver acceleration volume acquisition technique. The other sequence included axial unenhanced, early and late arterial, and portal venous phases; coronal equilibrium phase; and axial delayed phase imaging with volume-interpolated breath-hold examination technique. The arterial, portal venous, equilibrium, and delayed phase images were obtained 18–25 seconds (36–40 seconds for the late arterial phase on the 3-T system), 60 seconds, 120–180 seconds, and 300–360 seconds after the start of the injection of 15–20 mL of gadodiamide (Omniscan, GE Healthcare) through an antecubital vein at a rate of 2 mL/s. Fat suppression was regularly used for T2-weighted imaging, thick-slab MRCP, volume acquisition for 3D MRCP, and contrast-enhanced MRI sequences. The acquisition parameters and sequences for MRI are listed in Table 1. The unenhanced and contrast-enhanced T1and T2-weighted images, thick-slab MRCP, and the source images for 3D MRCP were transferred to the workstations (Advantage Workstation version 4.3, GE Healthcare; Syngo Multimodality Workplace version D13, Siemens Healthcare). A radiologist with 8 years of experience in abdominal CT and MRI undertook the CT and MR image postprocessing at each of the workstations. The radiologist first created 2D CT images, including multiplanar reformations and curved planar reconstructions with the portal venous phase volume data and then generated negative-contrast CT cholangiopancreatograms with 3D tools as described in previous reports [10, 19]. For 3D MRCP, a 3D maximum-intensity-projection (MIP) tool was used to create 3D MRCP and MIP images saved as negative-contrast CT cholangiopancreatograms. For CTA and MRA, both thick-slab (thickness, 32–64 mm) and 3D CT and MR arteriograms and portovenograms were created with MIP and volume-rendering techniques and the arterial and portal venous phase data. All of the CT and MR images were transferred to a PACS (MultiView with Synapse software, Fujifilm Medical Systems).
ers’ learning bias, a 2-week interval was observed between the two readings, and the images were provided randomly from the two image sets. The reviewers were asked to evaluate detection of the tumor as visible or invisible; to assess the presence or absence of peripancreatic major organs, vessel involvement, or metastases; and to determine resectability according to the evaluation criteria (described later) on CT or MR images. The assessment results were compared with the surgical and the pathologic records. PC was defined at contrast-enhanced CT and MRI as a low- or high-attenuation or hypointense or hyperintense mass compared with the surrounding pancreatic parenchyma [3, 14, 15]. If no mass was discerned, indirect signs, including focal contour changes in the pancreas with abrupt termination of the bile duct, pancreatic duct, or both (double-duct sign) or the presence of the four-segment sign were suggestive of PC with both modalities [20, 21]. Once a mass was found, the reviewers further measured the maximal diameter of the low- or high-attenuation or hypointense or hyperintense region. Peripancreatic major organ (i.e., stomach or colon) invasion was considered present if a suspected low-attenuation or hypointense lesion directly invaded or reached the surface of the structures [8]. Regional lymph node evaluation followed the Japanese Pancreas Society classification [22]. Nodal metastasis was considered present when the shortaxis diameter was longer than 10 mm or when central necrosis was present at any size or its attenuation or signal intensity was greater than that of liver parenchyma in the portal venous phase [13, 23]. For the diagnostic criteria for vascular invasion in this study, we used the three-criterion image grading system suggested by Valls et al. [24] and modified in more recent literature [18, 25]. We graded the tumor-to-vessel contact for the five major peripancreatic vessels (celiac artery, hepatic artery, superior mesenteric artery [SMA] and vein, and portal vein) as follows: imaging grade 0, no contiguity between tumor and vessel; 1, tumor-to-vessel contiguity ≤ 50%; and 2, tumor-to-vessel contiguity > 50%, including complete vessel occlusion. This evaluation required approximately 5–10 minutes for each image set per patient.
Image Analysis
Criteria for Unresectability at CT and MRI
Image Postprocessing
Two radiologists (one with 14 years of experience in abdominal CT, the other with 8 years of experience in MRI) independently evaluated the two image sets (both postprocessing and source images) on the PACS screen. The CT set consisted of 2D CT images including negative-contrast CT cholangiopancreatograms and CTA images. The MRI set consisted of 2D MR images including MRCP and MRA images. To minimize the read-
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According to the defined criteria, a tumor was considered unresectable if one or more of the following findings was present on CT or MR images. First, the tumor-to-vessel contiguity reached imaging grade 2, including the superior mesenteric–to–portal vein confluence [18, 26]. Second, peripancreatic organ involvement, such as of the stomach or colon [1, 13], other than choledochal or duodenal invasion was present, because the in-
vaded choledochal or duodenal organs can be resected en bloc during a radical operation in patients with PC. Third, distant metastasis, such as to the liver, consisted of solid low-attenuation or hypointense masses with poor margin and rim enhancement on contrast-enhanced images [18], peritoneum and omentum presented with nodular thickening and contrast enhancement, or ascites presented without an underlying systemic condition [18, 27]. Fourth, positive lymph nodes were present around the celiac artery (lymph node station 9) or along the left lateral SMA (station 14) or abdominal aorta (station 16), as described in the literature [22, 28].
Criteria for Unresectability at Surgery
In this study, peripancreatic vessel involvement was also categorized into three surgical grades according to exploration records: 0, separable peripancreatic vessel without adherence to tumor; 1, peripancreatic vessel adherent to the tumor but separable; and 2, peripancreatic vessel inseparable from or encased within the tumor. Patients were considered to have surgically unresectable tumors on the basis of the following criteria. First, a peripancreatic vessel was inseparable from or encased within the tumor (surgical grade 2) [12]. Although limited invasion of the portal or superior mesenteric vein (
