Ann Surg Oncol (2015) 22:1708–1715 DOI 10.1245/s10434-014-4041-7
ORIGINAL ARTICLE – REGIONAL CANCER THERAPIES
Comparison of MRI and CT for Predicting the Peritoneal Cancer Index (PCI) Preoperatively in Patients Being Considered for Cytoreductive Surgical Procedures Russell N. Low, MD1, Robert M. Barone, MD2, and Janelle Lucero, BA2 Department of Radiology, Sharp Memorial Hospital, San Diego, CA; 2Department of Surgical Oncology, Sharp Memorial Hospital, San Diego, CA 1
ABSTRACT Purpose. To compare the accuracy of MRI and CT for predicting the Peritoneal Cancer Index (PCI) preoperatively compared with the PCI tabulated at surgery. Methods. Twenty-two patients underwent preoperative MRI and CT scanning followed by cytoreductive surgery for appendiceal (n = 17) and ovarian (n = 5) cancer. MR and CT examinations were retrospectively reviewed to determine the PCI. The results of these scores were compared with PCI tabulated at surgery. Patients were categorized as small volume tumor (PCI 0–9), moderate volume (PCI 10–20), and large volume (PCI [ 20). Respective anatomic site scores for MRI and CT were compared with surgical findings. Results. Compared with surgical PCI, MRI correctly categorized tumor volume in 20 (0.91) of 22 patients, including 3 of 4 patients with small volume tumor, 2 of 2 patients with moderate volume tumor, and 15 of 16 patients with large volume tumor. CT correctly categorized tumor volume in 11 of 22 (0.50) patients, including 2 of 4 patients with small-volume tumor, 2 of 2 patients with moderate volume tumor, and 7 of 16 patients with large-volume tumor. In 19 of 22 patients, CT underestimated the volume of tumor found at surgery. For all patients, the median PCI score at surgery was 33 compared with 36 for MRI and 15 for CT. Surgery confirmed 222 sites of tumor. MRI
Presented at Ninth International Symposium on Regional Cancer Therapies, Steamboat Springs, Colorado, February 18–21, 2014. Ó Society of Surgical Oncology 2014 First Received: 14 April 2014; Published Online: 9 September 2014 R. N. Low, MD e-mail: [email protected]
demonstrated per site sensitivity of 0.95, specificity 0.70, and accuracy 0.88. CT showed a corresponding per site sensitivity 0.55, specificity 0.86, and accuracy 0.63. Conclusions. MRI more accurately predicts PCI preoperatively in patients undergoing evaluation for cytoreductive surgery.
The peritoneal cancer index (PCI) provides a measurement of the volume and extent of peritoneal tumor found at laparotomy. The PCI score combines the distribution of peritoneal tumor at 13 abdominal and pelvic regions with the tumor size.1 The PCI is the most widely validated and precise quantitative prognostic indicator.2,3 For patients undergoing surgical cytoreduction (CRS) and heated intraperitoneal chemotherapy (HIPEC), the PCI is one factor associated with determining whether a complete surgical cytoreduction can be achieved.4 While CT is routinely used for preoperative assessment of patients being considered for CRS and HIPEC,5,6 CT is characterized by its limited soft tissue contrast. On all imaging studies, soft-tissue contrast allows one to distinguish tumors from adjacent normal tissues. With CT, small peritoneal tumors may be indistinguishable from the surrounding tissues, resulting in reduced sensitivity for peritoneal carcinomatosis.7–9 A recent study found that preoperative CT consistently underestimated the PCI compared to operative findings detecting only 11 % of tumors \5 mm.9 MR imaging uses different types of image contrast to produce images that are more sensitive for showing peritoneal tumors.10–13 Delayed gadolinium-enhanced images obtained 5 min following the IV injection of gadolinium contrast material depicts peritoneal tumors due to their slow accumulation of contrast.10–13 Diffusion-weighted MR imaging (DWI) evaluates the microscopic movement
MRI More Accurate than CT for Predicting PCI
of water protons. Many tumors cause restricted diffusion of water protons, which results in an area of altered signal on DWI. Our experience has shown that the combination of delayed gadolinium-enhanced MRI and DWI provides the most sensitive test to evaluate for peritoneal cancer.13,14 A direct comparison of preoperative MRI and CT in patients being considered for surgical cytoreduction and HIPEC is important. Despite our prior reports describing the sensitivity of MRI for depicting peritoneal tumor,10–13 CT continues to be the predominant imaging modality used at most institutions. Earlier reports directly comparing CT and MRI used much older CT and MR imaging techniques8 and did not calculate the PCI. Both imaging modalities have advanced considerably. Multidetector CT now offers speed advantages not present in prior comparisons. For MRI, new diffusion-weighted imaging significantly improves accuracy of peritoneal tumor depiction. This is particularly true for serosal and mesenteric peritoneal tumor. In this study, we compare newer multidetector CT and MRI techniques in the same patient to compare their accuracy in determining the PCI score in patients being considered for surgical cytoreductive procedures. MATERIALS AND METHODS This retrospective study was approved by our institutional review board who waived requirement for written, informed consent. Patient selection began with a review of a database listing patients who underwent surgical cytoreduction and HIPEC from April 2007 until January 2013. Letters of inquiry were sent to the referring hospitals requesting CT scans of the abdomen and pelvis. We received 50 CT scans based on these requests. CT scans were excluded if they were not preoperative, did not include the abdomen and pelvis, were not performed on a multidetector CT scanner, or were obtained more than 3 months prior to the operation. The final study group included 22 patients (14 women and 8 men, mean age 55 years) who underwent preoperative MRI and CT followed by cytoreductive surgery for primary tumors of the appendix17 and ovary.5 These nonconsecutive patients included all patients for whom we could obtain preoperative CT scans from outside institutions or from our hospital to compare with the preoperative MR examination and surgical findings. MR Imaging All patients were imaged on a 1.5T GE Discovery MR 450 MR scanner equipped with high-performance gradients (50 mT/m, 200 mT/m/s) (GE HealthCare, Waukesha, WI) using an external phased array surface coil. MR imaging
1709
included T1-weighted, T2-weighted, DWI, and gadolinium-enhanced MR imaging. Table 1 lists imaging parameters for each sequence. The time of the MR examination was 30 min. This retrospective review was limited to DWI, and delayed gadolinium-enhanced images obtained 5 min following injection of 0.15 mmol/kg gadobenate dimeglumine (Multihance) (Bracco Diagnostics, Inc. Princeton, NJ). MRI Intraluminal Contrast Material All patients received oral and rectal water soluble contrast material to distend the gastrointestinal tract; 1,200 ml of dilute barium sulfate was administered orally starting 45 min before the MR examination. A balloon-tipped barium enema catheter was used to administer 500– 1,000 cc of rectal tap water to distend the rectum and colon. An antiperistaltic agent (Levsin 0.25 mg IV) was administered before the examination. CT Scanning All patients underwent preoperative CT scanning. Six patients had CT scanning performed at our institution on a 64-slice multidetector General Electric (Waukesha, WI) CT scanner. Sixteen patients had CT scanning performed at their referring institution using various multidetector CT scanners. For 17 patients, the CT scan was performed with intravenous and oral contrast material. For the remaining 5 patients, the CT scan was performed with oral contrast but without IV contrast due to renal insufficiency. Specific CT imaging parameters include slice thickness of 5 mm and kVP 120. Scanning was from the dome of liver through the symphysis pubis. Review of CT Scans and MR Images CT scans MR examinations were reviewed by the same observer at separate sessions separated by at least 6 months without knowledge of surgical or histopathologic findings. MR examinations were reviewed first followed by review of the CT scan. The observer independently determined the PCI for MR and CT. The PCI score represents the combination of tumor at 13 anatomic sites and the tumor size. The abdominal and pelvic intraperitoneal spaces are divided into nine regions and the small bowel into four regions. Each of the 13 regions was scored for implant size on a scale of 0–3 (0, no visible tumor implants; 1, implants \0.50 cm in greatest diameter; 2, implants 0.50–5.0 cm; 3, implants [5.0 cm or a confluence of implants).
1710
R. N. Low et al.
TABLE 1 Peritoneal MR imaging protocol Pulse sequence
TR (ms)
TE
Matrix
NSA
Thick (mm)
Gap (mm)
FOV cm
FA
Plane
Note
Time
SSFSE
Infinite
80
320 9 226
0.6
7
0.5
40
90
C
12
T1 SGE
173
4.4/2.2
256 9 224
1
7
3
36
80
A
22
T2 FRFSE
2,500
85
512 9 256
1
7
3
36
90
A
ETL 18
22 9 2
DWI
3,000
Minimum
192 9 224
3
8
0
36
90
A
b20 b500
24
7.06
2.39
320 9 288
1
4.4
-2.2
36
12
26 s
Gadolinium injection 3D FSPGR Dixon 2D SGE
150
Minimum
512 9 192
1
8
2
36
70
Ax2
Dixon
C
water
A
Fat sat
22
Table shows imaging parameters for complete prostate MR examination SGE spoiled gradient-echo, FRFSE fast recovery fast spin echo, LAVA Liver Acceleration Volume Acquisition; 3D FSPGR Dixon 3D fast spoiled gradient-echo with Dixon water reconstruction (LAVA-FLEX)
MRI Criteria for Peritoneal Tumor For delayed gadolinium-enhanced MR images, tumor was recorded if there was peritoneal thickening and or enhancement, peritoneal tumor nodules, or masses involving the peritoneum, omentum, or mesentery. Serosal tumor was recorded if there were bowel wall masses or bowel wall thickening and enhancement. Normal peritoneal enhancement is equal to muscle enhancement. For the DWI images, tumor was recorded if there was restricted diffusion involving the peritoneum indicated by high signal on the magnitude DWI images. High signal tumor masses or nodules involving the peritoneum, omentum, mesentery, or bowel serosa on the DWI b500 images also were recorded as tumor. CT Criteria for Peritoneal Tumor For CT scans, peritoneal tumor was recorded for peritoneal thickening, enhancement, peritoneal tumor nodules or masses involving the peritoneum, omentum, or mesentery. Serosal tumor was recorded if there were bowel masses, bowel wall thickening, and enhancement. Ascites by itself was not recorded as tumor in the absence of the findings listed above. The results of the CT PCI and MRI PCI scores were then compared to PCI score tabulated at surgery. Patients were categorized as small volume tumor (PCI 0–9), moderate volume (PCI 10–20), and large volume (PCI [ 20). These results were compared to the surgical PCI using the same categories of tumor volume. CT or MR scans in which no tumor was depicted were scored as false negative cases if tumor was recorded at laparotomy. Respective anatomic site scores for both MRI and surgery were compared. Depiction of peritoneal tumor nodules was compared to operative and histopathologic findings. The CT and MRI site sensitivity, specificity, and accuracy were calculated.
In this evaluation, tumor depiction on CT, and MRI per site was recorded independent of lesion size. Surgical Cytoreductive Surgery and HIPEC All 22 patients underwent cytoreductive surgery with the intention to remove all intraperitoneal tumors. The cytoreductive surgery involved exploratory laparotomy initially with determination of the PCI score before initiating any cytoreductive procedures. Standard multisite peritonectomies and gastrointestinal resections15 were performed to remove all visible tumors. HIPEC was performed with Mitomycin-C (10– 15 mg/m2) for appendiceal and colon carcinomas, cisplatin (60 mg/m2), and Adriamycin (15 mg/m2) for ovarian and mesothelioma carcinomas. Statistical Analysis The MRI PCI and surgical PCI were compared using the paired t test reporting two-tailed p values. The null hypothesis was rejected or p \ 0.05.
RESULTS Figure 1 shows the CT PCI, MRI PCI, and the surgical PCI for all 22 patients. Using the paired t test, there was a statistical difference between the CT PCI and surgical PCI (p \ 0.05) but no statistical difference between the MRI PCI and surgical PCI (p = 0.67). CT underscored the PCI compared with surgical findings in 19 of 22 patients. For all patients, the median PCI score at surgery was 33 compared with 36 for MRI and 15 for CT. The median percentage difference between the surgical PCI and the CT PCI was 50 % compared with 6 % for the MRI PCI versus the surgical.
MRI More Accurate than CT for Predicting PCI
1711
FIG. 1 Comparison of PCI on preoperative MRI and surgical PCI score
Peritoneal Cancer Index MRI vs. CT Surgery MRI CT
40
Peritoneal Cancer Index
35
30
25
20
15
10
5
0 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
Patients FIG. 2 A 54-year-old patient with mucinous appendiceal cancer. CT scan (left) shows perihepatic ascites (arrow). DWI MRI b500 s/m2 (middle) and delayed gadolinium-enhanced MRI (right) through the upper abdomen demonstrate a thin rim of right subphrenic tumor (arrows). The preoperative CT PCI was 4, MRI PCI was 19, and the surgical PCI was 26
Categorization of Tumor Volume on MRI Versus Surgery
tumor in 3 (0.50) of the 6 patients. In 2 patients with lowvolume tumor, CT failed to detect any peritoneal tumor.
The categorization of PCI as small, moderate, and large volume tumor on MRI and at surgery showed overall very good agreement. MRI correctly predicted the PCI category in 20 (0.91) of 22 patients. The results for CT were less favorable with CT correctly predicting the PCI category in 11 (0.50) of 22 patients.
Large Tumor Burden (PCI [ 20) In 16 patients with large-volume peritoneal tumor at surgery, MRI correctly predicted PCI [ 20 in 15 (94 %) patients and underestimated tumor volume as moderate in 1 (6 %) patient (PCI 19). CT correctly predicted large volume tumor in 7 (0.44) patients and underestimated tumor volume in the remaining 9 (0.66) patients (Figs. 2, 3).
Low to Moderate Tumor Burden (PCI B 20) In six patients with low to moderate tumor burden, MRI correctly predicted the PCI category in 5 of 6 (83 %) and was incorrect in 1 of 6 (17 %) patients. In one patient, small volume tumor MRI over estimated the PCI score. CT scanning correctly predicted low to moderate volume
MRI and CT Depiction of Tumor at Individual Anatomic Sites At surgery, 222 regions were involved with peritoneal tumor. MRI correctly depicted tumor in 201 regions with 11 false-negative regions, 52 true-negative regions, and 22
1712
R. N. Low et al.
FIG. 3 a A 59-year-old woman with appendiceal cancer. CT scan (left) through the upper abdomen shows ascites (arrow) without definite peritoneal tumor. DWI MRI b-value 500 s/m2 (middle) shows abnormal restricted diffusion within the right and left subphrenic fluid (arrows), indicating that the fluid is not simple ascites. Gadoliniumenhanced MRI (right) shows a thin enhancing rim of right and left subphrenic peritoneal tumor (arrows). Surgery confirmed diffuse upper abdominal peritoneal tumors. b A 59-year-old woman with
appendiceal cancer. CT scan (left) through the middle abdomen shows small amount of right paracolic ascites without evidence of tumor. DWI MRI b-value 500 s/m2 (middle) shows diffuse serosal and mesenteric tumor (arrows) with restricted diffusion. Gadoliniumenhanced MRI (right) shows abnormal thick-walled and enhancing small bowel (arrows). At surgery, diffuse small-bowel serosal tumor was confirmed with a surgical PCI 37 compared with CT PCI 14 and MRI PCI 39
false-positive regions. The MRI region sensitivity was 95 %, specificity 70 %, and accuracy 88 %. CT correctly depicted tumor in 116 regions with 96 false-negative regions, 64 true-negative regions, and 10 false-positive regions. The CT region sensitivity was 55 %, specificity 86 %, and accuracy 63 % (Table 2).
Multidetector CT continues to be utilized at most institutions for abdominal imaging because of its speed and excellent spatial resolution. However, the more limited contrast resolution of CT can present challenges in depicting subtle peritoneal tumors. Coakley et al.7 noted sensitivity of helical CT for peritoneal tumors \1 cm was only 25–50 % compared with 85–95 % for all tumors. Low et al.8 reported the sensitivity of gadolinium-enhanced MR images for depicting peritoneal tumors at \1 cm was 85– 90 % compared with 22–33 % for CT. The average sensitivity of MR for depicting peritoneal tumors of all sizes was 84 % compared with 54 % for CT. In a more recent report,16 the accuracy in depicting peritoneal lesions using CT regardless of size, ranged from 51 to 88 % in the nine abdominopelvic regions and 21–25 % in the four small intestinal regions in pseudomyxoma peritonei. In comparing the radiologic CT PCI to the operative PCI in the study, the radiologic PCI consistently underestimated the volume of peritoneal disease. Koh et al.9 in another study reported that CT identified the presence of disease and portrayed true lesion size in only 60 % of the cases of colorectal carcinoma. Small nodules, \0.5 cm were visualized on CT with only a sensitivity of 11 %. Radiologic PCI scores significantly underestimated the intraoperative PCI with the operative score almost double the radiologic PCI score. CT detection of peritoneal nodules was 67 % in the epigastrium,
DISCUSSION Surgical cytoreduction and HIPEC provides significant survival benefits for patients with disseminated peritoneal tumors.17,18 Preoperative MRI and CT of the abdomen and pelvis play an integral role in determining the extent of peritoneal and visceral disease in patients being considered for cytoreductive surgery and HIPEC for appendiceal, ovarian, colorectal, primary peritoneal, gastric, mesothelioma, and other rare types of gastrointestinal disease involving the peritoneum. Careful patient selection based on preoperative imaging may prevent unnecessary surgeries in patients whose tumors are too extensive and cannot be adequately cytoreduced. In the past 6 years using MR for preoperative assessment, we have had only two patients who have been subjected to open and close surgical procedures. Both patients had high-grade tumor histology.
MRI More Accurate than CT for Predicting PCI
1713
TABLE 2 Peritoneal tumor detection at 13 anatomic sites on MRI and CT compared with surgical and histopathologic findings Regions
TP
FN
TN
FP
Sen
Spec
Acc
MRI
18
0
2
2
1.00
0.50
0.91
CT
18
0
4
0
1.00
1.00
1.00
MRI
17
0
3
2
1.00
0.60
0.91
CT
8
9
4
1
0.47
0.80
0.55
Area 2 MRI
14
3
3
2
0.82
0.60
0.77
CT
9
8
4
1
0.53
0.80
0.59
MRI
15
1
5
1
0.94
0.83
0.91
CT
13
3
5
1
0.81
0.83
0.82
MRI
13
1
6
2
0.93
0.75
0.86
CT
9
5
8
0
0.64
1.00
0.77
MRI
17
1
3
1
0.94
0.75
0.91
CT
12
6
4
0
0.67
1.00
0.73
MRI
17
3
1
1
0.85
0.50
0.82
CT
13
7
2
0
0.65
1.00
0.68
Area 7 MRI
17
0
3
2
1.00
0.60
0.91
CT
11
6
3
2
0.65
0.60
0.64
MRI
14
0
4
4
1.00
0.50
0.82
CT
7
7
4
4
0.50
0.50
0.50
Area 0
Area 1
Area 3
Area 4
Area 5
Area 6
Area 8
Area 9 MRI
12
2
7
1
0.86
0.88
0.86
CT
1
13
8
0
0.07
1.00
0.41
Area 10 MRI
15
0
6
1
1.00
0.86
0.95
CT
2
13
7
0
0.13
1.00
0.41
Area 11 MRI
14
0
7
1
1.00
0.88
0.95
CT
1
13
8
0
0.07
1.00
0.41
18 12
0 6
2 3
2 1
1.00 0.67
0.50 0.75
0.91 0.68
MRI
201
11
52
22
0.95
0.70
0.88
CT
116
96
64
10
0.55
0.86
0.63
Area 12 MRI CT Totals
Numbers represent the number of patients in which MRI and CT detected peritoneal tumor and categorized each patient site as true positive, false negative (FN), false positive (FP), or true negative (TN) based on comparison with surgical and histopathologic findings
54 % in the right upper quadrant, and 60 % in the pelvis. Small-bowel involvement had the least sensitivity of all the regions 8–17 %. These results agree with those of our study, which is the first direct comparison of MRI and CT in patients undergoing preoperative evaluation for peritoneal cancer surgery. In our study for comparison purposes, the CT epigastric detection rate was 100 %, right upper quadrant 55 %, the pelvis 68 %, and the small bowel 48 % (41– 68 %). The radiologic calculated CT PCI underestimated the surgical PCI score in 19 of 22 patients. The median surgical PCI was 33 compared with median CT PCI of 15. The median percentage difference between the surgical PCI and the CT PCI was 50 % compared with 6 % for the MRI PCI versus the surgical PCI. Compared with the surgical PCI, MRI PCI correctly categorized tumor volume in 91 % of the patients as opposed to only 50 % with CT scanning. Notably in the small-bowel areas (sites 9–12), MRI had an accuracy of 92 % versus 48 % for CT. Previously, we reported19,20 no significant difference between MRI calculated PCI and the surgical PCI. Compared with surgical findings, MRI correctly predicted small-volume (89 %), moderate-volume (75 %), and largevolume tumor (90 %). Comparable results were found in this study: 91, 83, and 94 % respectively for low-, moderate-, and large-volume tumor. In our experience, delayed gadolinium-enhanced imaging combined with diffusion-weighted MRI has been the best imaging tool to determine which patients will be able to have a complete primary cytoreductive surgery for appendiceal, ovarian, and primary peritoneal carcinoma. Based on our MRI preoperative staging PCI, of the patients who were deemed to be surgical candidates, 90 % subsequently underwent an R/0/1 resection. This study is limited by its retrospective nature and the small number of patients who had both CT scans and MRI examinations performed preoperatively. A prospective comparison of MRI and CT at our institution would be challenging, because we have not used CT preoperatively in patients with peritoneal tumor for more than 10 years. All patients referred to our institution for possible cytoreductive surgery and HIPEC have already had a CT scan performed at an outside hospital. The cost of an additional CT scan and the unnecessary radiation exposure to patients was felt to be unacceptable. For this reason, many of the CT scans from other institutions were performed on different scanners. All CT scans included in this study were performed on multidetector scanners with similar, although not identical imaging protocols. Some of the scans were performed without contrast because of compromised renal
1714
function. This may limit the sensitivity of some of the CT study results. In our study, we found no difference in tumor detection between those CT scans performed with and without intravenous contrast. We used the same observer to calculate the MRI and CT PCI. We determined that this approach would remove the possible inconsistencies of image interpretation between different radiologists. The 6 months between MRI and CT interpretation was established to remove any recall bias from the prior study. MR exams were reviewed first so that any possible recall would benefit the CT interpretation. Despite the overwhelming superiority of MRI over CT the major detractors against MRI are the longer exam times and the cost of the MRI. It takes an average of 30 min to perform the procedure, which can be influenced by motion artifacts related to respiration and bowel peristalsis. We routinely use Glucagon or Levsin to decrease peristalsis and insist upon optimal breath hold technique for MRI. At our institution, the charges for CT are determined by the hospital, whereas MRI charges are established by the MRI center. The charges for the MRI in our institution are considerably less than that for a CT scan. Establishing a successful peritoneal MR imaging program requires close collaboration between the MRI radiologist and surgical oncologist. At our institution, a dedicated MRI radiologist and the surgeon are committed to working together closely communicating preoperative physical findings as well as surgical findings. The surgeon and radiologist review all the MR imaging before the surgery. Following the procedure, we correlate the surgical and MR imaging findings to continually fine tune the process of image interpretation. In addition, we recommend that the radiologist at first visit the operating room to view the actual pathology and distribution of peritoneal tumor. By repeating this process of collaboration and communication, we can improve interpretation of MR examinations, resulting in better surgical decisions and patient management.
CONCLUSIONS MRI combining gadolinium-enhanced imaging and diffusion-weighted imaging is more accurate than CT for staging patients with abdominal carcinomatosis. The surgical PCI correlates better with MRI findings, which may assist with patient selection. REFERENCES 1. Glenhen O, Gilly FN. Quantitative preoperative indicators of peritoneal surface malignancies: carcinomatosis, sarcomatosis, and peritoneal mesothelioma. Surg Oncol Clin N Am. 2003;12:649–71.
R. N. Low et al. 2. Harmon RL, Sugarbaker PH. Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol. 2005;2:3. http://www.issoonline.com/content/2/1/3. Accessed 01 Oct 2013. 3. Sugarbaker PH, Jablonski KA. Prognostic features of 51 colorectal and 130 appendiceal cancer patients with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann Surg. 1995;221:124–32. 4. Yan TD, Sim J, Morris DL. Selection of patients with colorectal peritoneal carcinomatosis for cytoreductive surgery and perioperative intraperitoneal chemotherapy. Ann Surg Oncol. 2009;14:1807–17. 5. Jacquet P, Jelinek JS, Sugarbaker PH. Abdominal computed tomographic scan in the selection of patients with mucinous peritoneal carcinomatosis for cytoreductive surgery. J Am Coll Surg. 1995;181:530–8. 6. Esquivel J, Chua TC, Stojadinovic A, Melero JT, Levine EA, Gutman M, Howard R, Piso P, Nissan A, Gomez-Portilla A, Gonzalez-Bayon L, Gonzalez-Moreno S, Shen P, Stewart JH, Sugarbaker PH, Barone RM, Hoefer R, Morris DL, Sardi A, Sticca RP. Accuracy and clinical relevance of computed tomography scan interpretation of peritoneal cancer index in colorectal cancer peritoneal carcinomatosis: a multi-institutional study. J Surg Oncol. 2010;102:565–70. 7. Coakley FV, Choi PH, Gougoutas CA, et al. Peritoneal metastases: detection with spiral CT in patients with ovarian cancer. Radiology. 2002;223:495–500. 8. Low RN, Barone RM, Lacey C, Sigeti JS, Alzate GD, Sebrechts CP. Peritoneal tumor: MR imaging with dilute oral barium and intravenous gadolinium-containing contrast agents compared with unenhanced MR imaging and CT. Radiology. 1997;204:513–20. 9. Koh JL, Tan TD, Glenn D, Morris DL. Evaluation of preoperative computed tomography in estimating peritoneal cancer index in colorectal peritoneal carcinomatosis. Ann Surg Oncol. 2009;16:327–33. 10. Low RN, Barone RM, Gurney JM. Mucinous appendiceal neoplasms: preoperative MR staging and classification compared with surgical and histopathologic findings. Am J Roentgenol. 2008;190:656–65. 11. Low RN, Duggan B, Barone RM, Saleh F, Song SYT. Treated ovarian cancer: MR imaging, laparotomy reassessment, and serum CA-125 values compared with clinical outcome at 1 year. Radiology. 2005;235:918–26. 12. Low RN, Gurney J. Diffusion-weighted MRI (DWI) in the oncology patient: value of breathhold DWI compared to unenhanced and gadolinium-enhanced MR. J Magn Reson Imaging. 2007;25:848–58. 13. Low RN, Sebrechts CP, Barone RM, Muller W. Diffusionweighted MRI of peritoneal tumors: comparison with conventional MRI and surgical and histopathologic findings–a feasibility study. Am. J. Roentgenol. 2009;193:461–70. 14. Kyriazi S, Collins DJ, Morgan VA, Giles SL, deSouza NM. Diffusionweighted imaging of peritoneal disease for noninvasive staging of advanced ovarian cancer. Radiographics. 2010;30:1269–85. 15. Sugarbaker PH. Peritonectomy procedures. Surg Oncol Clin N Am. 2003;12:703–27. 16. Chua, TC, AL-Zahrani A, Saxena A, Glenn D, et al. Determining the association between preoperative computed tomography findings and postoperative outcomes after cytoreductive surgery and perioperative intraperitoneal chemotherapy for Pseudomyxoma peritonei. Ann Surg Oncol. 2011;18:1582–9. 17. Levine EA, Stewart KH, Russell GB, Keisinger KR, Loggie BL, Shen P. Cytoreductive surgery and intraperitoneal hyperthermic chemotherapy for peritoneal surface malignancy. Experience with 501 procedures. J Am Coll Surg. 2007;2004:943–55. 18. Glehen O, Kwiakowsky F, Sugarbaker PH, et al. Cytoreductive surgery combined with perioperative intraperitoneal chemotherapy
MRI More Accurate than CT for Predicting PCI in colorectal cancer: multi-institutional study. J Clin Oncol. 2004;22:3284–92. 19. Low RN, Barone RM. Combined diffusion weighted and gadolinium-enhanced MRI can correctly predict peritoneal cancer index preoperatively in patient’s being considered for cytoreductive surgical procedures. Ann Surg Oncol. 2012;19:1395–401.
1715 20. Low RN, Barone RM, Lee M. Surveillance MR imaging is superior to serum tumor markers for detecting early tumor recurrence in patients with appendiceal cancer treated with cytoreduction and HIPEC. Ann Surg Oncol. 2013;20:1079–81.
ORIGINAL ARTICLE – REGIONAL CANCER THERAPIES
Comparison of MRI and CT for Predicting the Peritoneal Cancer Index (PCI) Preoperatively in Patients Being Considered for Cytoreductive Surgical Procedures Russell N. Low, MD1, Robert M. Barone, MD2, and Janelle Lucero, BA2 Department of Radiology, Sharp Memorial Hospital, San Diego, CA; 2Department of Surgical Oncology, Sharp Memorial Hospital, San Diego, CA 1
ABSTRACT Purpose. To compare the accuracy of MRI and CT for predicting the Peritoneal Cancer Index (PCI) preoperatively compared with the PCI tabulated at surgery. Methods. Twenty-two patients underwent preoperative MRI and CT scanning followed by cytoreductive surgery for appendiceal (n = 17) and ovarian (n = 5) cancer. MR and CT examinations were retrospectively reviewed to determine the PCI. The results of these scores were compared with PCI tabulated at surgery. Patients were categorized as small volume tumor (PCI 0–9), moderate volume (PCI 10–20), and large volume (PCI [ 20). Respective anatomic site scores for MRI and CT were compared with surgical findings. Results. Compared with surgical PCI, MRI correctly categorized tumor volume in 20 (0.91) of 22 patients, including 3 of 4 patients with small volume tumor, 2 of 2 patients with moderate volume tumor, and 15 of 16 patients with large volume tumor. CT correctly categorized tumor volume in 11 of 22 (0.50) patients, including 2 of 4 patients with small-volume tumor, 2 of 2 patients with moderate volume tumor, and 7 of 16 patients with large-volume tumor. In 19 of 22 patients, CT underestimated the volume of tumor found at surgery. For all patients, the median PCI score at surgery was 33 compared with 36 for MRI and 15 for CT. Surgery confirmed 222 sites of tumor. MRI
Presented at Ninth International Symposium on Regional Cancer Therapies, Steamboat Springs, Colorado, February 18–21, 2014. Ó Society of Surgical Oncology 2014 First Received: 14 April 2014; Published Online: 9 September 2014 R. N. Low, MD e-mail: [email protected]
demonstrated per site sensitivity of 0.95, specificity 0.70, and accuracy 0.88. CT showed a corresponding per site sensitivity 0.55, specificity 0.86, and accuracy 0.63. Conclusions. MRI more accurately predicts PCI preoperatively in patients undergoing evaluation for cytoreductive surgery.
The peritoneal cancer index (PCI) provides a measurement of the volume and extent of peritoneal tumor found at laparotomy. The PCI score combines the distribution of peritoneal tumor at 13 abdominal and pelvic regions with the tumor size.1 The PCI is the most widely validated and precise quantitative prognostic indicator.2,3 For patients undergoing surgical cytoreduction (CRS) and heated intraperitoneal chemotherapy (HIPEC), the PCI is one factor associated with determining whether a complete surgical cytoreduction can be achieved.4 While CT is routinely used for preoperative assessment of patients being considered for CRS and HIPEC,5,6 CT is characterized by its limited soft tissue contrast. On all imaging studies, soft-tissue contrast allows one to distinguish tumors from adjacent normal tissues. With CT, small peritoneal tumors may be indistinguishable from the surrounding tissues, resulting in reduced sensitivity for peritoneal carcinomatosis.7–9 A recent study found that preoperative CT consistently underestimated the PCI compared to operative findings detecting only 11 % of tumors \5 mm.9 MR imaging uses different types of image contrast to produce images that are more sensitive for showing peritoneal tumors.10–13 Delayed gadolinium-enhanced images obtained 5 min following the IV injection of gadolinium contrast material depicts peritoneal tumors due to their slow accumulation of contrast.10–13 Diffusion-weighted MR imaging (DWI) evaluates the microscopic movement
MRI More Accurate than CT for Predicting PCI
of water protons. Many tumors cause restricted diffusion of water protons, which results in an area of altered signal on DWI. Our experience has shown that the combination of delayed gadolinium-enhanced MRI and DWI provides the most sensitive test to evaluate for peritoneal cancer.13,14 A direct comparison of preoperative MRI and CT in patients being considered for surgical cytoreduction and HIPEC is important. Despite our prior reports describing the sensitivity of MRI for depicting peritoneal tumor,10–13 CT continues to be the predominant imaging modality used at most institutions. Earlier reports directly comparing CT and MRI used much older CT and MR imaging techniques8 and did not calculate the PCI. Both imaging modalities have advanced considerably. Multidetector CT now offers speed advantages not present in prior comparisons. For MRI, new diffusion-weighted imaging significantly improves accuracy of peritoneal tumor depiction. This is particularly true for serosal and mesenteric peritoneal tumor. In this study, we compare newer multidetector CT and MRI techniques in the same patient to compare their accuracy in determining the PCI score in patients being considered for surgical cytoreductive procedures. MATERIALS AND METHODS This retrospective study was approved by our institutional review board who waived requirement for written, informed consent. Patient selection began with a review of a database listing patients who underwent surgical cytoreduction and HIPEC from April 2007 until January 2013. Letters of inquiry were sent to the referring hospitals requesting CT scans of the abdomen and pelvis. We received 50 CT scans based on these requests. CT scans were excluded if they were not preoperative, did not include the abdomen and pelvis, were not performed on a multidetector CT scanner, or were obtained more than 3 months prior to the operation. The final study group included 22 patients (14 women and 8 men, mean age 55 years) who underwent preoperative MRI and CT followed by cytoreductive surgery for primary tumors of the appendix17 and ovary.5 These nonconsecutive patients included all patients for whom we could obtain preoperative CT scans from outside institutions or from our hospital to compare with the preoperative MR examination and surgical findings. MR Imaging All patients were imaged on a 1.5T GE Discovery MR 450 MR scanner equipped with high-performance gradients (50 mT/m, 200 mT/m/s) (GE HealthCare, Waukesha, WI) using an external phased array surface coil. MR imaging
1709
included T1-weighted, T2-weighted, DWI, and gadolinium-enhanced MR imaging. Table 1 lists imaging parameters for each sequence. The time of the MR examination was 30 min. This retrospective review was limited to DWI, and delayed gadolinium-enhanced images obtained 5 min following injection of 0.15 mmol/kg gadobenate dimeglumine (Multihance) (Bracco Diagnostics, Inc. Princeton, NJ). MRI Intraluminal Contrast Material All patients received oral and rectal water soluble contrast material to distend the gastrointestinal tract; 1,200 ml of dilute barium sulfate was administered orally starting 45 min before the MR examination. A balloon-tipped barium enema catheter was used to administer 500– 1,000 cc of rectal tap water to distend the rectum and colon. An antiperistaltic agent (Levsin 0.25 mg IV) was administered before the examination. CT Scanning All patients underwent preoperative CT scanning. Six patients had CT scanning performed at our institution on a 64-slice multidetector General Electric (Waukesha, WI) CT scanner. Sixteen patients had CT scanning performed at their referring institution using various multidetector CT scanners. For 17 patients, the CT scan was performed with intravenous and oral contrast material. For the remaining 5 patients, the CT scan was performed with oral contrast but without IV contrast due to renal insufficiency. Specific CT imaging parameters include slice thickness of 5 mm and kVP 120. Scanning was from the dome of liver through the symphysis pubis. Review of CT Scans and MR Images CT scans MR examinations were reviewed by the same observer at separate sessions separated by at least 6 months without knowledge of surgical or histopathologic findings. MR examinations were reviewed first followed by review of the CT scan. The observer independently determined the PCI for MR and CT. The PCI score represents the combination of tumor at 13 anatomic sites and the tumor size. The abdominal and pelvic intraperitoneal spaces are divided into nine regions and the small bowel into four regions. Each of the 13 regions was scored for implant size on a scale of 0–3 (0, no visible tumor implants; 1, implants \0.50 cm in greatest diameter; 2, implants 0.50–5.0 cm; 3, implants [5.0 cm or a confluence of implants).
1710
R. N. Low et al.
TABLE 1 Peritoneal MR imaging protocol Pulse sequence
TR (ms)
TE
Matrix
NSA
Thick (mm)
Gap (mm)
FOV cm
FA
Plane
Note
Time
SSFSE
Infinite
80
320 9 226
0.6
7
0.5
40
90
C
12
T1 SGE
173
4.4/2.2
256 9 224
1
7
3
36
80
A
22
T2 FRFSE
2,500
85
512 9 256
1
7
3
36
90
A
ETL 18
22 9 2
DWI
3,000
Minimum
192 9 224
3
8
0
36
90
A
b20 b500
24
7.06
2.39
320 9 288
1
4.4
-2.2
36
12
26 s
Gadolinium injection 3D FSPGR Dixon 2D SGE
150
Minimum
512 9 192
1
8
2
36
70
Ax2
Dixon
C
water
A
Fat sat
22
Table shows imaging parameters for complete prostate MR examination SGE spoiled gradient-echo, FRFSE fast recovery fast spin echo, LAVA Liver Acceleration Volume Acquisition; 3D FSPGR Dixon 3D fast spoiled gradient-echo with Dixon water reconstruction (LAVA-FLEX)
MRI Criteria for Peritoneal Tumor For delayed gadolinium-enhanced MR images, tumor was recorded if there was peritoneal thickening and or enhancement, peritoneal tumor nodules, or masses involving the peritoneum, omentum, or mesentery. Serosal tumor was recorded if there were bowel wall masses or bowel wall thickening and enhancement. Normal peritoneal enhancement is equal to muscle enhancement. For the DWI images, tumor was recorded if there was restricted diffusion involving the peritoneum indicated by high signal on the magnitude DWI images. High signal tumor masses or nodules involving the peritoneum, omentum, mesentery, or bowel serosa on the DWI b500 images also were recorded as tumor. CT Criteria for Peritoneal Tumor For CT scans, peritoneal tumor was recorded for peritoneal thickening, enhancement, peritoneal tumor nodules or masses involving the peritoneum, omentum, or mesentery. Serosal tumor was recorded if there were bowel masses, bowel wall thickening, and enhancement. Ascites by itself was not recorded as tumor in the absence of the findings listed above. The results of the CT PCI and MRI PCI scores were then compared to PCI score tabulated at surgery. Patients were categorized as small volume tumor (PCI 0–9), moderate volume (PCI 10–20), and large volume (PCI [ 20). These results were compared to the surgical PCI using the same categories of tumor volume. CT or MR scans in which no tumor was depicted were scored as false negative cases if tumor was recorded at laparotomy. Respective anatomic site scores for both MRI and surgery were compared. Depiction of peritoneal tumor nodules was compared to operative and histopathologic findings. The CT and MRI site sensitivity, specificity, and accuracy were calculated.
In this evaluation, tumor depiction on CT, and MRI per site was recorded independent of lesion size. Surgical Cytoreductive Surgery and HIPEC All 22 patients underwent cytoreductive surgery with the intention to remove all intraperitoneal tumors. The cytoreductive surgery involved exploratory laparotomy initially with determination of the PCI score before initiating any cytoreductive procedures. Standard multisite peritonectomies and gastrointestinal resections15 were performed to remove all visible tumors. HIPEC was performed with Mitomycin-C (10– 15 mg/m2) for appendiceal and colon carcinomas, cisplatin (60 mg/m2), and Adriamycin (15 mg/m2) for ovarian and mesothelioma carcinomas. Statistical Analysis The MRI PCI and surgical PCI were compared using the paired t test reporting two-tailed p values. The null hypothesis was rejected or p \ 0.05.
RESULTS Figure 1 shows the CT PCI, MRI PCI, and the surgical PCI for all 22 patients. Using the paired t test, there was a statistical difference between the CT PCI and surgical PCI (p \ 0.05) but no statistical difference between the MRI PCI and surgical PCI (p = 0.67). CT underscored the PCI compared with surgical findings in 19 of 22 patients. For all patients, the median PCI score at surgery was 33 compared with 36 for MRI and 15 for CT. The median percentage difference between the surgical PCI and the CT PCI was 50 % compared with 6 % for the MRI PCI versus the surgical.
MRI More Accurate than CT for Predicting PCI
1711
FIG. 1 Comparison of PCI on preoperative MRI and surgical PCI score
Peritoneal Cancer Index MRI vs. CT Surgery MRI CT
40
Peritoneal Cancer Index
35
30
25
20
15
10
5
0 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
Patients FIG. 2 A 54-year-old patient with mucinous appendiceal cancer. CT scan (left) shows perihepatic ascites (arrow). DWI MRI b500 s/m2 (middle) and delayed gadolinium-enhanced MRI (right) through the upper abdomen demonstrate a thin rim of right subphrenic tumor (arrows). The preoperative CT PCI was 4, MRI PCI was 19, and the surgical PCI was 26
Categorization of Tumor Volume on MRI Versus Surgery
tumor in 3 (0.50) of the 6 patients. In 2 patients with lowvolume tumor, CT failed to detect any peritoneal tumor.
The categorization of PCI as small, moderate, and large volume tumor on MRI and at surgery showed overall very good agreement. MRI correctly predicted the PCI category in 20 (0.91) of 22 patients. The results for CT were less favorable with CT correctly predicting the PCI category in 11 (0.50) of 22 patients.
Large Tumor Burden (PCI [ 20) In 16 patients with large-volume peritoneal tumor at surgery, MRI correctly predicted PCI [ 20 in 15 (94 %) patients and underestimated tumor volume as moderate in 1 (6 %) patient (PCI 19). CT correctly predicted large volume tumor in 7 (0.44) patients and underestimated tumor volume in the remaining 9 (0.66) patients (Figs. 2, 3).
Low to Moderate Tumor Burden (PCI B 20) In six patients with low to moderate tumor burden, MRI correctly predicted the PCI category in 5 of 6 (83 %) and was incorrect in 1 of 6 (17 %) patients. In one patient, small volume tumor MRI over estimated the PCI score. CT scanning correctly predicted low to moderate volume
MRI and CT Depiction of Tumor at Individual Anatomic Sites At surgery, 222 regions were involved with peritoneal tumor. MRI correctly depicted tumor in 201 regions with 11 false-negative regions, 52 true-negative regions, and 22
1712
R. N. Low et al.
FIG. 3 a A 59-year-old woman with appendiceal cancer. CT scan (left) through the upper abdomen shows ascites (arrow) without definite peritoneal tumor. DWI MRI b-value 500 s/m2 (middle) shows abnormal restricted diffusion within the right and left subphrenic fluid (arrows), indicating that the fluid is not simple ascites. Gadoliniumenhanced MRI (right) shows a thin enhancing rim of right and left subphrenic peritoneal tumor (arrows). Surgery confirmed diffuse upper abdominal peritoneal tumors. b A 59-year-old woman with
appendiceal cancer. CT scan (left) through the middle abdomen shows small amount of right paracolic ascites without evidence of tumor. DWI MRI b-value 500 s/m2 (middle) shows diffuse serosal and mesenteric tumor (arrows) with restricted diffusion. Gadoliniumenhanced MRI (right) shows abnormal thick-walled and enhancing small bowel (arrows). At surgery, diffuse small-bowel serosal tumor was confirmed with a surgical PCI 37 compared with CT PCI 14 and MRI PCI 39
false-positive regions. The MRI region sensitivity was 95 %, specificity 70 %, and accuracy 88 %. CT correctly depicted tumor in 116 regions with 96 false-negative regions, 64 true-negative regions, and 10 false-positive regions. The CT region sensitivity was 55 %, specificity 86 %, and accuracy 63 % (Table 2).
Multidetector CT continues to be utilized at most institutions for abdominal imaging because of its speed and excellent spatial resolution. However, the more limited contrast resolution of CT can present challenges in depicting subtle peritoneal tumors. Coakley et al.7 noted sensitivity of helical CT for peritoneal tumors \1 cm was only 25–50 % compared with 85–95 % for all tumors. Low et al.8 reported the sensitivity of gadolinium-enhanced MR images for depicting peritoneal tumors at \1 cm was 85– 90 % compared with 22–33 % for CT. The average sensitivity of MR for depicting peritoneal tumors of all sizes was 84 % compared with 54 % for CT. In a more recent report,16 the accuracy in depicting peritoneal lesions using CT regardless of size, ranged from 51 to 88 % in the nine abdominopelvic regions and 21–25 % in the four small intestinal regions in pseudomyxoma peritonei. In comparing the radiologic CT PCI to the operative PCI in the study, the radiologic PCI consistently underestimated the volume of peritoneal disease. Koh et al.9 in another study reported that CT identified the presence of disease and portrayed true lesion size in only 60 % of the cases of colorectal carcinoma. Small nodules, \0.5 cm were visualized on CT with only a sensitivity of 11 %. Radiologic PCI scores significantly underestimated the intraoperative PCI with the operative score almost double the radiologic PCI score. CT detection of peritoneal nodules was 67 % in the epigastrium,
DISCUSSION Surgical cytoreduction and HIPEC provides significant survival benefits for patients with disseminated peritoneal tumors.17,18 Preoperative MRI and CT of the abdomen and pelvis play an integral role in determining the extent of peritoneal and visceral disease in patients being considered for cytoreductive surgery and HIPEC for appendiceal, ovarian, colorectal, primary peritoneal, gastric, mesothelioma, and other rare types of gastrointestinal disease involving the peritoneum. Careful patient selection based on preoperative imaging may prevent unnecessary surgeries in patients whose tumors are too extensive and cannot be adequately cytoreduced. In the past 6 years using MR for preoperative assessment, we have had only two patients who have been subjected to open and close surgical procedures. Both patients had high-grade tumor histology.
MRI More Accurate than CT for Predicting PCI
1713
TABLE 2 Peritoneal tumor detection at 13 anatomic sites on MRI and CT compared with surgical and histopathologic findings Regions
TP
FN
TN
FP
Sen
Spec
Acc
MRI
18
0
2
2
1.00
0.50
0.91
CT
18
0
4
0
1.00
1.00
1.00
MRI
17
0
3
2
1.00
0.60
0.91
CT
8
9
4
1
0.47
0.80
0.55
Area 2 MRI
14
3
3
2
0.82
0.60
0.77
CT
9
8
4
1
0.53
0.80
0.59
MRI
15
1
5
1
0.94
0.83
0.91
CT
13
3
5
1
0.81
0.83
0.82
MRI
13
1
6
2
0.93
0.75
0.86
CT
9
5
8
0
0.64
1.00
0.77
MRI
17
1
3
1
0.94
0.75
0.91
CT
12
6
4
0
0.67
1.00
0.73
MRI
17
3
1
1
0.85
0.50
0.82
CT
13
7
2
0
0.65
1.00
0.68
Area 7 MRI
17
0
3
2
1.00
0.60
0.91
CT
11
6
3
2
0.65
0.60
0.64
MRI
14
0
4
4
1.00
0.50
0.82
CT
7
7
4
4
0.50
0.50
0.50
Area 0
Area 1
Area 3
Area 4
Area 5
Area 6
Area 8
Area 9 MRI
12
2
7
1
0.86
0.88
0.86
CT
1
13
8
0
0.07
1.00
0.41
Area 10 MRI
15
0
6
1
1.00
0.86
0.95
CT
2
13
7
0
0.13
1.00
0.41
Area 11 MRI
14
0
7
1
1.00
0.88
0.95
CT
1
13
8
0
0.07
1.00
0.41
18 12
0 6
2 3
2 1
1.00 0.67
0.50 0.75
0.91 0.68
MRI
201
11
52
22
0.95
0.70
0.88
CT
116
96
64
10
0.55
0.86
0.63
Area 12 MRI CT Totals
Numbers represent the number of patients in which MRI and CT detected peritoneal tumor and categorized each patient site as true positive, false negative (FN), false positive (FP), or true negative (TN) based on comparison with surgical and histopathologic findings
54 % in the right upper quadrant, and 60 % in the pelvis. Small-bowel involvement had the least sensitivity of all the regions 8–17 %. These results agree with those of our study, which is the first direct comparison of MRI and CT in patients undergoing preoperative evaluation for peritoneal cancer surgery. In our study for comparison purposes, the CT epigastric detection rate was 100 %, right upper quadrant 55 %, the pelvis 68 %, and the small bowel 48 % (41– 68 %). The radiologic calculated CT PCI underestimated the surgical PCI score in 19 of 22 patients. The median surgical PCI was 33 compared with median CT PCI of 15. The median percentage difference between the surgical PCI and the CT PCI was 50 % compared with 6 % for the MRI PCI versus the surgical PCI. Compared with the surgical PCI, MRI PCI correctly categorized tumor volume in 91 % of the patients as opposed to only 50 % with CT scanning. Notably in the small-bowel areas (sites 9–12), MRI had an accuracy of 92 % versus 48 % for CT. Previously, we reported19,20 no significant difference between MRI calculated PCI and the surgical PCI. Compared with surgical findings, MRI correctly predicted small-volume (89 %), moderate-volume (75 %), and largevolume tumor (90 %). Comparable results were found in this study: 91, 83, and 94 % respectively for low-, moderate-, and large-volume tumor. In our experience, delayed gadolinium-enhanced imaging combined with diffusion-weighted MRI has been the best imaging tool to determine which patients will be able to have a complete primary cytoreductive surgery for appendiceal, ovarian, and primary peritoneal carcinoma. Based on our MRI preoperative staging PCI, of the patients who were deemed to be surgical candidates, 90 % subsequently underwent an R/0/1 resection. This study is limited by its retrospective nature and the small number of patients who had both CT scans and MRI examinations performed preoperatively. A prospective comparison of MRI and CT at our institution would be challenging, because we have not used CT preoperatively in patients with peritoneal tumor for more than 10 years. All patients referred to our institution for possible cytoreductive surgery and HIPEC have already had a CT scan performed at an outside hospital. The cost of an additional CT scan and the unnecessary radiation exposure to patients was felt to be unacceptable. For this reason, many of the CT scans from other institutions were performed on different scanners. All CT scans included in this study were performed on multidetector scanners with similar, although not identical imaging protocols. Some of the scans were performed without contrast because of compromised renal
1714
function. This may limit the sensitivity of some of the CT study results. In our study, we found no difference in tumor detection between those CT scans performed with and without intravenous contrast. We used the same observer to calculate the MRI and CT PCI. We determined that this approach would remove the possible inconsistencies of image interpretation between different radiologists. The 6 months between MRI and CT interpretation was established to remove any recall bias from the prior study. MR exams were reviewed first so that any possible recall would benefit the CT interpretation. Despite the overwhelming superiority of MRI over CT the major detractors against MRI are the longer exam times and the cost of the MRI. It takes an average of 30 min to perform the procedure, which can be influenced by motion artifacts related to respiration and bowel peristalsis. We routinely use Glucagon or Levsin to decrease peristalsis and insist upon optimal breath hold technique for MRI. At our institution, the charges for CT are determined by the hospital, whereas MRI charges are established by the MRI center. The charges for the MRI in our institution are considerably less than that for a CT scan. Establishing a successful peritoneal MR imaging program requires close collaboration between the MRI radiologist and surgical oncologist. At our institution, a dedicated MRI radiologist and the surgeon are committed to working together closely communicating preoperative physical findings as well as surgical findings. The surgeon and radiologist review all the MR imaging before the surgery. Following the procedure, we correlate the surgical and MR imaging findings to continually fine tune the process of image interpretation. In addition, we recommend that the radiologist at first visit the operating room to view the actual pathology and distribution of peritoneal tumor. By repeating this process of collaboration and communication, we can improve interpretation of MR examinations, resulting in better surgical decisions and patient management.
CONCLUSIONS MRI combining gadolinium-enhanced imaging and diffusion-weighted imaging is more accurate than CT for staging patients with abdominal carcinomatosis. The surgical PCI correlates better with MRI findings, which may assist with patient selection. REFERENCES 1. Glenhen O, Gilly FN. Quantitative preoperative indicators of peritoneal surface malignancies: carcinomatosis, sarcomatosis, and peritoneal mesothelioma. Surg Oncol Clin N Am. 2003;12:649–71.
R. N. Low et al. 2. Harmon RL, Sugarbaker PH. Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol. 2005;2:3. http://www.issoonline.com/content/2/1/3. Accessed 01 Oct 2013. 3. Sugarbaker PH, Jablonski KA. Prognostic features of 51 colorectal and 130 appendiceal cancer patients with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann Surg. 1995;221:124–32. 4. Yan TD, Sim J, Morris DL. Selection of patients with colorectal peritoneal carcinomatosis for cytoreductive surgery and perioperative intraperitoneal chemotherapy. Ann Surg Oncol. 2009;14:1807–17. 5. Jacquet P, Jelinek JS, Sugarbaker PH. Abdominal computed tomographic scan in the selection of patients with mucinous peritoneal carcinomatosis for cytoreductive surgery. J Am Coll Surg. 1995;181:530–8. 6. Esquivel J, Chua TC, Stojadinovic A, Melero JT, Levine EA, Gutman M, Howard R, Piso P, Nissan A, Gomez-Portilla A, Gonzalez-Bayon L, Gonzalez-Moreno S, Shen P, Stewart JH, Sugarbaker PH, Barone RM, Hoefer R, Morris DL, Sardi A, Sticca RP. Accuracy and clinical relevance of computed tomography scan interpretation of peritoneal cancer index in colorectal cancer peritoneal carcinomatosis: a multi-institutional study. J Surg Oncol. 2010;102:565–70. 7. Coakley FV, Choi PH, Gougoutas CA, et al. Peritoneal metastases: detection with spiral CT in patients with ovarian cancer. Radiology. 2002;223:495–500. 8. Low RN, Barone RM, Lacey C, Sigeti JS, Alzate GD, Sebrechts CP. Peritoneal tumor: MR imaging with dilute oral barium and intravenous gadolinium-containing contrast agents compared with unenhanced MR imaging and CT. Radiology. 1997;204:513–20. 9. Koh JL, Tan TD, Glenn D, Morris DL. Evaluation of preoperative computed tomography in estimating peritoneal cancer index in colorectal peritoneal carcinomatosis. Ann Surg Oncol. 2009;16:327–33. 10. Low RN, Barone RM, Gurney JM. Mucinous appendiceal neoplasms: preoperative MR staging and classification compared with surgical and histopathologic findings. Am J Roentgenol. 2008;190:656–65. 11. Low RN, Duggan B, Barone RM, Saleh F, Song SYT. Treated ovarian cancer: MR imaging, laparotomy reassessment, and serum CA-125 values compared with clinical outcome at 1 year. Radiology. 2005;235:918–26. 12. Low RN, Gurney J. Diffusion-weighted MRI (DWI) in the oncology patient: value of breathhold DWI compared to unenhanced and gadolinium-enhanced MR. J Magn Reson Imaging. 2007;25:848–58. 13. Low RN, Sebrechts CP, Barone RM, Muller W. Diffusionweighted MRI of peritoneal tumors: comparison with conventional MRI and surgical and histopathologic findings–a feasibility study. Am. J. Roentgenol. 2009;193:461–70. 14. Kyriazi S, Collins DJ, Morgan VA, Giles SL, deSouza NM. Diffusionweighted imaging of peritoneal disease for noninvasive staging of advanced ovarian cancer. Radiographics. 2010;30:1269–85. 15. Sugarbaker PH. Peritonectomy procedures. Surg Oncol Clin N Am. 2003;12:703–27. 16. Chua, TC, AL-Zahrani A, Saxena A, Glenn D, et al. Determining the association between preoperative computed tomography findings and postoperative outcomes after cytoreductive surgery and perioperative intraperitoneal chemotherapy for Pseudomyxoma peritonei. Ann Surg Oncol. 2011;18:1582–9. 17. Levine EA, Stewart KH, Russell GB, Keisinger KR, Loggie BL, Shen P. Cytoreductive surgery and intraperitoneal hyperthermic chemotherapy for peritoneal surface malignancy. Experience with 501 procedures. J Am Coll Surg. 2007;2004:943–55. 18. Glehen O, Kwiakowsky F, Sugarbaker PH, et al. Cytoreductive surgery combined with perioperative intraperitoneal chemotherapy
MRI More Accurate than CT for Predicting PCI in colorectal cancer: multi-institutional study. J Clin Oncol. 2004;22:3284–92. 19. Low RN, Barone RM. Combined diffusion weighted and gadolinium-enhanced MRI can correctly predict peritoneal cancer index preoperatively in patient’s being considered for cytoreductive surgical procedures. Ann Surg Oncol. 2012;19:1395–401.
1715 20. Low RN, Barone RM, Lee M. Surveillance MR imaging is superior to serum tumor markers for detecting early tumor recurrence in patients with appendiceal cancer treated with cytoreduction and HIPEC. Ann Surg Oncol. 2013;20:1079–81.
