This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ruers, T.J.M. Articles by Oyen, W. J.G. Search for Related Content PubMed PubMed Citation Articles by Ruers, T.J.M. Articles by Oyen, W. J.G. Social Bookmarking                            What's this?

Value of Positron Emission Tomography With [F-18]Fluorodeoxyglucose in Patients With Colorectal Liver Metastases: A Prospective Study

From the Departments of Surgery, Nuclear Medicine, and Radiology, University Medical Center Nijmegen, Nijmegen, the Netherlands.

Address reprint requests to T.J.M. Ruers, MD, Department of Surgery, University Medical Center Nijmegen, PO Box 9101, 6500 HB Nijmegen, the Netherlands; email: t.ruers{at}heel.azn.nl

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To assess prospectively the value of fluor-18-deoxyglucose (FDG) positron emission tomography (PET), in addition to conventional diagnostic methods (CDM), as a staging modality in candidates for resection of colorectal liver metastases.

PATIENTS AND METHODS: In 51 patients analyzed for resection of colorectal liver metastases, clinical management decisions were recorded after a complete work-up with CDM. Afterward, FDG-PET scans were performed and any change of clinical management according to FDG-PET results was carefully documented. Discordances between FDG-PET and CDM results were identified and related to the final diagnosis by histopathology, intraoperative findings, and follow-up.

RESULTS: In 10 (20%) out of 51 patients, clinical management decisions based on CDM were changed after FDG-PET findings were known. FDG-PET detected unresectable pulmonary (n = 5) and hepatic metastases (n = 1) and ruled out extrahepatic (n = 2) and hepatic disease (n = 2). Due to FDG-PET, eight patients were spared unwarranted liver resection or laparotomy and two other patients were identified as candidates for liver resection. When the results of FDG-PET were regarded as decisive in a retrospective analysis, potential change of management was 29% (15 patients). FDG-PET and CDM showed discordant extrahepatic results in 11 patients (22%) and discordant hepatic results in eight patients (16%). Compared with CDM, FDG-PET resulted in true upstaging (n = 11), true downstaging (n = 5), false upstaging (n = 1), and false downstaging (n = 2). The detection rate of liver metastases on a lesion basis was generally better for computed tomography than for FDG-PET (80% v 65%); this was related to tumor size.

CONCLUSION: FDG-PET as a complementary staging method improves the therapeutic management of patients with colorectal liver metastases, especially by detecting unsuspected extrahepatic disease.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
AFTER APPARENTLY curative resection of colorectal carcinoma, approximately 50% of patients will develop liver metastases in 5 years’ time. For patients with recurrent disease confined to the liver, resection of the metastases is the treatment of choice and can result in a 5-year survival rate of 35% to 40%.^1-3 However, 60% to 65% of patients will develop recurrent tumor after hepatic resection, indicating that many of the patients must have harbored unrecognized tumor foci at the time of liver resection.⁴ Moreover, several studies report unresectable disease at the time of laparotomy in 40% to 70% of patients brought to the operating room for liver resection.^5-7 These data indicate that intensive efforts should be used to improve staging in order to avoid unnecessary laparotomy and nontherapeutic resection procedures, especially since today resection of liver metastases is pursued with increasing aggressiveness.

Positron emission tomography (PET) using fluor-18-deoxyglucose (FDG) has emerged as a promising diagnostic staging modality in recurrent colorectal cancer. In this patient category, FDG-PET can potentially improve patient selection for surgery and hence may have a positive effect on treatment outcome. Unlike conventional diagnostic modalities (CDM), such as computerized tomography (CT) and ultrasonography, which require anatomic alterations for detection of malignancy, FDG-PET provides information on tumor growth based on increased glucose uptake and metabolism of malignant cells. FDG is transported into cells analogous to glucose and converted to FDG-6-phosphate. This metabolite cannot be processed via the citric acid cycle and hence will accumulate preferentially in those cells with high glucose uptake, such as tumor cells. The first reports on the clinical application of FDG-PET in colorectal cancer concerned the differentiation between scar tissue and local recurrence in rectal cancer, which often shows a similar appearance on CT.^8,9 As enthusiasm ensued, recent studies concentrated on the added value of FDG-PET in staging patients with liver metastases of colorectal carcinoma, ie, identifying patients who will benefit from resection and excluding those who will not.^10-18 However, these studies focused mainly on the diagnostic yield of FDG-PET and generally suffered from retrospective analysis concerning clinical management decisions. Here, we report the results of a prospective study on the clinical impact of FDG-PET as an adjunct to CDM in patients potentially eligible for resection of colorectal liver metastases.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
Between November 1998 and September 1999, 59 consecutive patients with suspected liver metastases from colorectal cancer were preoperatively staged for liver resection. There were 37 men and 22 women with a mean age of 62.6 years. The primary tumor was located in the colon in 43 patients and in the rectum in 16 patients. Dukes’ stage of the primary tumor was Dukes’ B in 14 patients, Dukes’ C in 19 patients, Dukes’ D in 22 patients, and unknown in four patients. Sixteen patients received adjuvant chemotherapy after resection of the primary tumor, and eight patients received adjuvant radiotherapy after resection of a rectal carcinoma. In one patient with rectal carcinoma, a local recurrence was resected earlier.

After colorectal resection, all patients were followed up at 3- to 6-month intervals by physical examination, serum carcinoembryonic antigen analyses, and incidentally radiological follow-up. Colonoscopy was performed 1 year after surgery and at 3-year intervals thereafter if no adenomatous polyps were found.

Patients in whom, during these follow-up examinations or during work-up of the primary tumor, liver metastases were suspected and confirmed by ultrasound and in whom resection was considered a possible option were referred to our clinic and included in this study.

CDM
When hepatic recurrence was suspected or identified, all patients underwent extensive work-up with CDM. The following investigations were performed: spiral CT scan of the liver, abdomen, and pelvis (in case of earlier rectal cancer); spiral CT scan of the chest; and colonoscopy or x-ray of the colon. CT examination was performed with a spiral CT scanner (Somatom Volume Zoom; Siemens, Erlangen, Germany). All patients received oral contrast 1 hour before the CT examination. Scans were performed before and after intravenous contrast injection. Injection of intravenous contrast material was performed by using an Envision CT injector (Medrad, Pittsburgh, PA) at a rate of 4 mL/sec through an 18-gauge intravenous catheter placed in an antecubital vein. A total of 100 mL of nonionic contrast material, iohexol (Omnipaque; Nycomed, Princeton NJ), 350 mg of iodine per milliliter, was injected. Scanning of the liver was in the venous phase, 70 seconds after start of the injection.

Both unenhanced and enhanced helical sequences were performed at 120 kV and 15 to 300 mAS. Continuously reconstructed sections (pitch 1:1) were obtained with 7-mm collimation.

FDG-PET
A dedicated, rotating, half-ring PET scanner (ECAT-ART; Siemens/CTI, Knoxville, TN) was used for data acquisition. Before FDG injection, patients fasted for at least 6 hours. Intake of sugar-free liquids was permitted. Diabetics were not excluded from the study. Immediately before the procedure, the patients were hydrated with 500 mL of water. One hour after intravenous injection of 200 to 220 MBq of FDG (Mallinckrodt Medical, Petten, the Netherlands) and 20 mg of furosemide, emission images of the area between the proximal femora and the base of the skull were acquired (10 minutes per bed position). The images were not corrected for attenuation and reconstructed using filtered back projection (Butterworth filter with a cutoff frequency of 0.4 Nyquist). The reconstructed images were displayed in coronal, transverse, and sagittal planes.

Data Analysis
CT and FDG-PET readings. Results of CT were reported by two senior radiologists with a special interest in hepatic imaging. FDG-PET scans were evaluated by one nuclear physician who was completely blinded to the results of CDM. Areas of marked focal FDG accumulation greater than the background activity of the examined organ were interpreted as sites of malignant disease. Equivocal FDG-PET readings were classified as negative.

Clinical management decisions. On the basis of the information obtained by CDM, one surgeon who specialized in liver surgery judged whether there was a preliminary indication for laparotomy and subsequent resection of liver metastases. Decisions were recorded, and afterward, whole-body FDG-PET scanning was performed within 3 weeks of CT scanning. After acquisition of the FDG-PET scan, the preliminary indication for laparotomy was reconsidered by the surgeon with full knowledge of both the CT and FDG-PET findings, and a definitive management decision to proceed to surgery or to initiate other treatment was made. Changes in therapeutic management before and after the results of the FDG-PET scanning were recorded.

Comparative analysis of CT and FDG-PET. Concordant and discordant findings of CDM and FDG-PET were compared in a patient-based analysis with the true lesion status obtained by intraoperative inspection, intraoperative ultrasound, histopathology, and follow-up imaging of more than 6 months. During follow-up, true lesion status was proven by progression of disease on scanning. Patients were classified as truly upstaged, falsely upstaged, truly downstaged, or falsely downstaged by FDG-PET. Moreover, the detection of liver metastases by FDG-PET was related to the size of the liver metastases, as determined by histopathologic examination or intraoperative ultrasound.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
At the introduction of the FDG-PET protocol, conventional chest x-ray instead of chest CT was part of the CDM protocol. In six of the initial eight patients of the study, FDG-PET indicated pulmonary metastases with diameters of 1 to 2 cm, whereas chest x-rays had initially been reported normal. Revision of the chest x-rays gave rise to suspicion of pulmonary metastases in two of these six patients. Since additional CT scans of the chest confirmed the presence of pulmonary metastases in the other four cases, CT scans of the chest were incorporated in the CDM protocol for future patients. All initial eight patients were excluded from further analysis in the study.

Detection of Extrahepatic Metastases
In the remaining 51 patients, complete CDM were used, enabling comparison with FDG-PET. In 40 patients, the extrahepatic results of CT were concordant with the results of FDG-PET and were confirmed by histopathology or follow-up. In 28 of these 40 patients, neither CT nor FDG-PET gave evidence of disease outside the liver. In 12 of the 40 patients, CT and FDG-PET detected similar extrahepatic metastases, as illustrated in Fig 1.

View larger version (119K): [in this window] [in a new window]   Fig 1. Concordant findings on CT and FDG-PET scans. The abdominal CT scans (A-C) and FDG-PET scan (D, coronal slice) show identical lesions. The two liver metastases and the extrahepatic lesion near the lower pole of the right kidney proved to be a local recurrence of colon carcinoma.

View larger version (53K): [in this window] [in a new window]   Fig 2. Upstaging by FDG-PET in a patient with liver metastasis of colon carcinoma and a history of prostate cancer. FDG-PET (A) identified a lesion in the chest; CT scan (B) was normal. Three months after liver resection, the patient showed spinal cord compression, resulting from an epidural metastasis, confirmed by magnetic resonance imaging (C) (histologic lesion: prostate carcinoma).

Clinical Staging According to FDG-PET and CT Scan Results
Preoperative staging data from complete CDM (including CT of the chest) and FDG-PET were compared with true lesion status, obtained by intraoperative inspection and ultrasound, histopathology, and clinical follow-up (Table 1). In 19 patients (37%), there were discordant findings that resulted in either upstaging or downstaging of the disease.

Downstaging by FDG-PET. Seven patients were downstaged by FDG-PET. Five patients were correctly downstaged by FDG-PET. In two patients with CT-positive liver lesions and negative FDG-PET findings, long-term follow-up did not show any progression of the lesions, making malignancy unlikely. In the third patient (Fig 3), a CT-positive and FDG-PET–negative liver lesion was surgically removed after chemotherapy. Histology showed only fibrosis. The fourth patient, analyzed for liver metastases, was also suspected of having a local recurrence after resection of the rectosigmoid, which was visualized by CT but not confirmed by FDG-PET and follow-up. The fifth patient had suspect lung lesions on CT, but FDG-PET was negative, which was confirmed by follow-up after liver operation. Two cases were falsely downstaged by FDG-PET. One patient had small progressive lung metastases that were missed with FDG-PET, and the other had widespread liver disease not detected by FDG-PET because of a high glucose level (10.4 mmol/L).

View larger version (63K): [in this window] [in a new window]   Fig 3. Downstaging by FDG-PET scan. Patient with proven liver metastasis in the left lobe was treated by chemotherapy. Postchemotherapy CT scan (A) shows persisting lesion. FDG-PET scan (B) shows no abnormal accumulation in the liver. The liver lesion was resected. Histology showed only fibrosis.

In 25 patients, a laparotomy was performed with the intention to resect all liver metastases. In 10 (40%) of the 25 patients, liver metastases proved unresectable at laparotomy because of either extensive liver involvement (n = 7), diaphragmatic and intestinal tumor involvement (n = 2), or the presence of a retroperitoneal/peritoneal metastasis (n = 1). In 15 (60%) of the 25 patients, liver resection with curative intent was performed, without or with additional cryosurgery (n = 6) or radiofrequent ablation (n = 2). In the group of eight patients with incomplete CDM, two patients underwent laparotomy. In both cases, hepatic resection was performed. At a later time point, one of these two patients also underwent resection of two peripheral pulmonary metastases. The overall resectability rate was 63% (17 of 27 patients).

Influence of FDG-PET on Therapeutic Management
Management decisions recorded after complete CDM (n = 51) were changed in 10 cases after the results of additional FDG-PET findings were known (Table 2). In five patients, the decision was taken to refrain from scheduled surgery when additional FDG-PET showed extrahepatic pulmonary metastases not detected on CT scan. One patient underwent radiofrequent ablation of liver metastases when FDG-PET correctly ruled out pulmonary metastases, which were suggested by CT. In one patient, an initial CT scan showed limited liver metastases, whereas FDG-PET showed more diffuse liver involvement. Surgery was postponed and a CT scan confirmed diffuse liver disease 3 months later. CT raised suspicion of a local recurrence in another patient, but FDG-PET did not, and this patient was therefore planned for liver resection. Finally, two patients with suspect liver lesions on CT were not operated on because FDG-PET results were negative and follow-up showed no progression of the lesions, making malignancy unlikely. So, in prospective analysis, FDG-PET resulted in an actual change of management in 20% of the patients.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
The present study shows that FDG-PET is a valuable adjunct to conventional staging in patients who are candidates for resection of colorectal liver metastases. In the current series, FDG-PET significantly changed the management in 20% of the patients. Furthermore, when FDG-PET was considered a more decisive technique for determining whether to perform surgery, management would have been changed in 29% of the patients.

Accurate detection of extrahepatic disease remains a drawback in the staging of patients with colorectal liver metastases. The additional value of FDG-PET may reside mainly in this area. FDG-PET allows a whole-body survey, and analysis by metabolic activity, as performed during FDG-PET, may substantially add to conventional anatomic imaging. In this series, FDG-PET led to clinically relevant extrahepatic findings different from conventional imaging in nine out of 51 patients. These results are in concordance with earlier reports.^11,14,17 Fong et al¹⁷ showed unexpected extrahepatic disease by FDG-PET in 10 out of 40 patients, whereas Lai et al¹¹ reported the detection of unsuspected extrahepatic disease by FDG-PET in 11 out of 34 patients analyzed for operable colorectal liver metastases. In the last series, however, chest CT was not routinely performed, which may explain the high percentage of patients with unsuspected extrahepatic lesions. The accuracy of FDG-PET and CT was more specifically investigated by Delbeke et al.¹⁴ In a series of 52 patients with recurrent colorectal cancer, they concluded that FDG-PET was more accurate than CT for the detection of extrahepatic disease (92% v 71%, respectively).

In our study design, we chose independent reading of CT and FDG-PET images and did not use joined reading of CT and FDG-PET scans. After the study, a re-review of CT scans was performed for those patients with positive FDG-PET results and negative CT results in whom FDG-PET proved correct during follow-up imaging for extrahepatic disease. Of the five patients with FDG-PET–positive/CT-negative lung lesions, three patients showed suspicious lesions on re-review (two patients with a suspicious hilar region on CT scans and one with suspicious parenchymal lesions). The two others were negative on re-review. Re-review of the CT scan of the patient with epidural metastases did not show any tumor lesion as depicted (Fig 2). In the patient with retroperitoneal metastasis, re-review of the CT scan could identify a suspicious retroperitoneal lesion. These data stress the importance of combined reading of CT and FDG-PET images in daily practice.

The detection rate of liver metastases in our series was generally better for CT scans than for FDG-PET scans (80% v 65%). Sensitivity of FDG-PET for colorectal liver metastases was directly related to tumor size, which was also reported by Fong et al.¹⁷ As demonstrated in the present study, FDG-PET may, however, contribute to liver imaging in cases of equivocal lesions on CT scans. Indeed, it may detect unsuspected liver metastases in some cases. Several authors have reported a higher accuracy for FDG-PET compared with CT in detecting liver metastases. In a series by Vitola et al,¹⁹ sensitivity for the detection of liver metastases by FDG-PET and CT was 93% and 76%, respectively; in a study by Hustinx et al,²⁰ these figures were 92% and 85%, respectively.

CT is currently regarded as the best method for evaluating the anatomy and resectability of colorectal liver metastases. Resectability of liver metastases is generally determined by the extent of liver involvement and the specific relation of metastases to anatomic structures. Given the limited anatomic information provided by FDG-PET, FDG-PET by itself will not become a substitute for the excellent anatomic imaging provided by spiral CT. Further development of combined modalities of CT and PET imaging, thereby presenting overlays of anatomic (CT) and functional (PET) information, may, however, lead to significant improvement of preoperative liver staging and preoperative judgment on resectability.²¹

In contrast with our present study, most of the prior studies were retrospective, patient groups were often not uniform, and many patients were not routinely examined by CT of the chest, precluding appropriate comparison with whole-body FDG-PET. The reported influence on therapeutic management of patients with presumed resectable recurrent colorectal cancer in these studies varied considerably, from 15% to 44%.^10-18 In a study by Delbeke et al,¹⁴ the effect of FDG-PET imaging was reviewed retrospectively. FDG-PET helped to clarify the final diagnosis misinterpreted on CT scan and led to a change in management in 28% (n = 17) of the patients. Vitola et al¹⁹ and Fong et al¹⁷ reported a radical change in clinical management after FDG-PET in 25% (n = 6) and 23% (n = 9), respectively. These percentages of mainly retrospective analyses are only slightly higher than the 20% change of management observed in this prospective study.

Variable resectability rates have been reported, ranging from 30% to 79% after CDM and FDG-PET.^10-18 Low resectability rates may reflect inadequate staging or low aggressiveness in liver resection. However, even with an aggressive approach as advocated by Fong et al,¹⁷ one fourth of the patients who were brought to the operating theater proved unresectable at laparotomy. Also in our study, a significant number of patients were not treated at laparotomy. In most cases (n = 7), this was due to more extensive liver involvement than judged preoperatively. This can be explained in part by our liberal indications for treatment. For example, patients with up to eight metastases were scheduled for surgical exploration and were planned for cryosurgery with or without additional resection of resectable lesions. It is not surprising that within this group of patients resectability rates, including cryosurgery or radiofrequency treatment, is lower compared with a highly selected group of patients with limited liver involvement. To improve resectability, especially in this category of patients, the role of diagnostic laparoscopy and laparoscopic ultrasound should be explored further.^22,23 It is likely that FDG-PET and laparoscopy may be complementary in this regard. FDG-PET may show nodal or retroperitoneal involvement, which is easily missed by laparoscopy, whereas peritoneal seedings and small liver lesions are more easily detected by laparoscopy and laparoscopic ultrasound.

In this series, FDG-PET was less accurate for small liver lesions, and in one patient, small lung lesions were missed by FDG-PET. This may be attributed to the small tumor volume or the relative indolence of some lesions, since FDG-PET requires enhanced glucose metabolism. Furthermore, the current FDG-PET studies were reconstructed using nonattenuation-corrected, filtered back projection. The recently developed software tools for attenuation-corrected FDG-PET image processing (ordered-subsets expectation maximization) may result in an improvement of image quality. This may result in a higher accuracy for detection of smaller lesions and a decrease in the number of equivocal lesions.²⁴ On the other hand, FDG-PET is not tumor-specific, and inflammatory processes as well as physiologic tracer activity in the gastrointestinal and urinary tracts may mimic pathologic lesions.^10-18 To reduce the possible negative impact of occasional false-positive FDG-PET results on patient management, FDG-PET images should be preferentially correlated with conventional imaging techniques.

In conclusion, in this prospective study, FDG-PET provided significant additional information to the conventional ways of diagnostic imaging. FDG-PET results led to a radical change in clinical management in 20% of the patients analyzed for resection of colorectal liver metastases. According to these results, several staging algorithms for patients with detected colorectal liver metastases can de proposed. Some would reserve FDG-PET scanning for patients with a high risk of extrahepatic disease after initial conventional work-up has demonstrated resectability of liver metastases.¹⁷ Others would initially perform FDG-PET scanning and, when extrahepatic disease is not detected, proceed with liver imaging by CT.¹⁴ In the near future, prospective trials are sorely needed to define the optimal strategy for FDG-PET in the selection of patients for resection of colorectal liver metastases.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
1. Scheele J, Stangl R, Altendorf-Hofmann A: Hepatic metastases from colorectal carcinoma: Impact of surgical resection on the natural history. Br J Surg 77: 1241–1246, 1990[Medline]

2. Gayowski TJ, Iwatsuki S, Madariaga JR, et al: Experience in hepatic resection for metastatic colorectal cancer: Analysis of clinical and pathologic risk factors. Surgery 116: 703–711, 1994[Medline]

3. Fong Y, Cohen AM, Fortner JG, et al: Liver resection for colorectal metastases. J Clin Oncol 15: 938–946, 1997[Abstract/Free Full Text]

4. Scheele J, Stangl R, Altendorf-Hofmann A, et al: Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 110: 13–29, 1991[Medline]

5. Fortner J, Silva JS, Golbey RB, et al: Multivariate analysis of a personal series of 247 consecutive patients with liver metastases from colorectal cancer: I. Treatment by hepatic resection. Ann Surg 199: 306–316, 1984[Medline]

6. Gibbs JF, Weber TK, Rodriguez-Bigas MA, et al: Intraoperative determinants of unresectability for patients with colorectal hepatic metastases. Cancer 82: 1244–1249, 1982[CrossRef]

7. Steele G, Bleday R, Mayer RJ: A prospective evaluation of hepatic resection for colorectal carcinoma metastases to the liver: Gastrointestinal Tumor Study Group Protocol 6584. J Clin Oncol 9: 1105–1112, 1991[Abstract]

8. Strauss LG, Clorius JH, Schlag P, et al: Recurrence of colorectal tumors: PET evaluation. Radiology 170: 329–333, 1989[Abstract/Free Full Text]

9. Ito M, Takashi K, Tadokoro M, et al: Recurrent rectal cancer and scar: Differentiation with PET and MR imaging. Radiology 182: 549–552, 1992[Abstract/Free Full Text]

10. Beets G, Penninckx F, Schiepers C, et al: Clinical value of whole-body positron emission tomography with [18F]fluorodeoxyglucose in recurrent colorectal cancer. Br J Surg 81: 1666–1670, 1994[Medline]

11. Lai DTM, Fulham M, Stephen MS, et al: The role of whole-body positron emission tomography with [18F]fluorodeoxyglucose in identifying operable colorectal cancer metastases to the liver. Arch Surg 131: 703–707, 1996[Abstract/Free Full Text]

12. Ogunbiyi OA, Flanagan FL, Dehtashti F, et al: Detection of recurrent and metastatic colorectal cancer: Comparison of positron emission tomography and computed tomography. Ann Surg Oncol 4: 613–620, 1997[CrossRef][Medline]

13. Abdel-Nabi H, Doerr RJ, Lamonica DM, et al: Staging of primary colorectal carcinomas with fluorine-18-fluorodeoxyglucose whole-body PET: Correlation with histopathologic and CT findings. Radiology 206: 755–759, 1998[Abstract/Free Full Text]

14. Delbeke D, Martin WH, Sandler MP, et al: Evaluation of benign vs malignant hepatic lesions with positron emission tomography. Arch Surg 133: 510–516, 1998[Abstract/Free Full Text]

15. Flanagan FL, Dehdashti F, Ogunbiyi OA, et al: Utility of FDG-PET for investigating unexplained plasma CEA elevation in patients with colorectal cancer. Ann Surg 227: 319–323, 1998[CrossRef][Medline]

16. Flamen P, Stroobants S, Van Cutsem E, et al: Additional value of whole-body positron emission tomography with fluorine-18-2-fluoro-deoxy-D-glucose in recurrent colorectal cancer. J Clin Oncol 17: 894–901, 1999[Abstract/Free Full Text]

17. Fong Y, Saldinger PF, Akhurst T, et al: Utility of 18F-FDG positron emission tomography scanning on selection of patients for resection of hepatic colorectal metastases. Am J Surg 178: 282–287, 1999[CrossRef][Medline]

18. Whiteford MH, Whiteford HM, Yee LF, et al: Usefulness of FDG-PET scan in the assessment of suspected metastatic or recurrent adenocarcinoma of the colon and rectum. Dis Colon Rectum 43: 759–767, 2000[CrossRef][Medline]

19. Vitola JV, Delbeke D, Sandler MP, et al: Positron emission tomography to stage suspected metastatic colorectal carcinoma to the liver. Am J Surg 171: 21–26, 1996[CrossRef][Medline]

20. Hustinx R, Paulus P, Jacquet N, et al: Clinical evaluation of whole-body ¹⁸F-fluorodeoxyglucose positron emission tomography in the detection of liver metastases. Ann Oncol 9: 397–401, 1998[Abstract/Free Full Text]

21. Beyer T, Townsend DW, Brun T, et al: A combined PET/CT scanner for clinical oncology. J Nucl Med 41: 1369–1379, 2000[Abstract/Free Full Text]

22. Babineau TJ, Lewis D, Jenkins RL, et al: Role of staging laparoscopy in the treatment of hepatic malignancy. Am J Surg 167: 151–154, 1994[CrossRef][Medline]

23. Rahusen FD, Cuesta MA, Borgstein PJ, et al: Selection of patients for resection of colorectal metastases to the liver using diagnostic laparoscopy and laparoscopic ultrasonography. Ann Surg 230: 31–37, 1999[CrossRef][Medline]

24. Lonneux M, Borbath I, Bol A, et al: Attenuation correction in whole-body FDG oncological studies: The role of statistical reconstruction. Eur J Nucl Med 26: 591–598, 1999[CrossRef][Medline]

Submitted January 30, 2001; accepted September 4, 2001.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				J. MONTEIL, N. MAHMOUDI, S. LEOBON, P.Y. ROUDAUT, A. EL BADAOUI, S. VERBEKE, L. VENAT-BOUVET, J. MARTIN, V. LE BRUN-LY, S. LAVAU-DENES, et al. Chemotherapy Response Evaluation in Metastatic Colorectal Cancer with FDG PET/CT and CT Scans Anticancer Res, July 1, 2009; 29(7): 2563 - 2568. [Abstract] [Full Text] [PDF]

				P. Bystrom, A. Berglund, U. Garske, H. Jacobsson, A. Sundin, P. Nygren, J.-E. Frodin, and B. Glimelius Early prediction of response to first-line chemotherapy by sequential [18F]-2-fluoro-2-deoxy-D-glucose positron emission tomography in patients with advanced colorectal cancer Ann. Onc., June 1, 2009; 20(6): 1057 - 1061. [Abstract] [Full Text] [PDF]

				A. M. Scott, D. H. Gunawardana, B. Kelley, J. G. Stuckey, A. J. Byrne, J. E. Ramshaw, and M. J. Fulham PET Changes Management and Improves Prognostic Stratification in Patients with Recurrent Colorectal Cancer: Results of a Multicenter Prospective Study J. Nucl. Med., September 1, 2008; 49(9): 1451 - 1457. [Abstract] [Full Text] [PDF]

				L.F. de Geus-Oei, H. W. M. van Laarhoven, E. P. Visser, R. Hermsen, B. A. van Hoorn, Y. J. L. Kamm, P. F. M. Krabbe, F. H. M. Corstens, C. J. A. Punt, and W. J. G. Oyen Chemotherapy response evaluation with FDG-PET in patients with colorectal cancer Ann. Onc., February 1, 2008; 19(2): 348 - 352. [Abstract] [Full Text] [PDF]

				R. A. Herbertson, S. T. Lee, N. Tebbutt, and A. M. Scott The expanding role of PET technology in the management of patients with colorectal cancer Ann. Onc., November 1, 2007; 18(11): 1774 - 1781. [Abstract] [Full Text] [PDF]

				F. H. Miller, A. L. Keppke, D. Reddy, J. Huang, J. Jin, M. F. Mulcahy, and R. Salem Response of Liver Metastases After Treatment with Yttrium-90 Microspheres: Role of Size, Necrosis, and PET Am. J. Roentgenol., March 1, 2007; 188(3): 776 - 783. [Abstract] [Full Text] [PDF]

				H. Kuehl, P. Veit, S. J. Rosenbaum, A. Bockisch, and G. Antoch Can PET/CT Replace Separate Diagnostic CT for Cancer Imaging? Optimizing CT Protocols for Imaging Cancers of the Chest and Abdomen J. Nucl. Med., January 1, 2007; 48(1_suppl): 45S - 57S. [Abstract] [Full Text] [PDF]

				D. L. Joyce, R. L. Wahl, P. V. Patel, R. D. Schulick, S. L. Gearhart, and M. A. Choti Preoperative Positron Emission Tomography to Evaluate Potentially Resectable Hepatic Colorectal Metastases Arch Surg, December 1, 2006; 141(12): 1220 - 1226. [Abstract] [Full Text] [PDF]

				L. de Geus-Oei, B Wiering, P. Krabbe, T. Ruers, C. Punt, and W. Oyen FDG-PET for prediction of survival of patients with metastatic colorectal carcinoma Ann. Onc., November 1, 2006; 17(11): 1650 - 1655. [Abstract] [Full Text] [PDF]

				H Furukawa, H Ikuma, A Seki, K Yokoe, S Yuen, T Aramaki, and S Yamagushi Positron emission tomography scanning is not superior to whole body multidetector helical computed tomography in the preoperative staging of colorectal cancer Gut, July 1, 2006; 55(7): 1007 - 1011. [Abstract] [Full Text] [PDF]

				G. K. von Schulthess, H. C. Steinert, and T. F. Hany Integrated PET/CT: Current Applications and Future Directions Radiology, February 1, 2006; 238(2): 405 - 422. [Abstract] [Full Text] [PDF]

				C. Lejeune, M. J. Bismuth, T. Conroy, C. Zanni, P. Bey, L. Bedenne, J. Faivre, P. Arveux, and F. Guillemin Use of a Decision Analysis Model to Assess the Cost-Effectiveness of 18F-FDG PET in the Management of Metachronous Liver Metastases of Colorectal Cancer J. Nucl. Med., December 1, 2005; 46(12): 2020 - 2028. [Abstract] [Full Text] [PDF]

				H. W. M. van Laarhoven, L.-F. de Geus-Oei, B. Wiering, J. Lok, M. Rijpkema, J. H. A. M. Kaanders, P. F. M. Krabbe, T. Ruers, C. J. A. Punt, A. J. van der Kogel, et al. Gadopentetate Dimeglumine and FDG Uptake in Liver Metastases of Colorectal Carcinoma as Determined with MR Imaging and PET Radiology, October 1, 2005; 237(1): 181 - 188. [Abstract] [Full Text] [PDF]

				S. Bipat, M. S. van Leeuwen, E. F. I. Comans, M. E. J. Pijl, P. M. M. Bossuyt, A. H. Zwinderman, and J. Stoker Colorectal Liver Metastases: CT, MR Imaging, and PET for Diagnosis--Meta-analysis Radiology, October 1, 2005; 237(1): 123 - 131. [Abstract] [Full Text] [PDF]

				D. V. Sahani, S. P. Kalva, A. J. Fischman, R. Kadavigere, M. Blake, P. F. Hahn, and S. Saini Detection of Liver Metastases from Adenocarcinoma of the Colon and Pancreas: Comparison of Mangafodipir Trisodium-Enhanced Liver MRI and Whole-Body FDG PET Am. J. Roentgenol., July 1, 2005; 185(1): 239 - 246. [Abstract] [Full Text] [PDF]

				M. C.A. van Kouwen, F. M. Nagengast, J. B.M.J. Jansen, W. J.G. Oyen, and J. P.H. Drenth 2-(18F)-Fluoro-2-Deoxy-D-Glucose Positron Emission Tomography Detects Clinical Relevant Adenomas of the Colon: A Prospective Study J. Clin. Oncol., June 1, 2005; 23(16): 3713 - 3717. [Abstract] [Full Text] [PDF]

				J.-H. Kim, J. Czernin, M. S. Allen-Auerbach, B. S. Halpern, B. J. Fueger, J. R. Hecht, O. Ratib, M. E. Phelps, and W. A. Weber Comparison Between 18F-FDG PET, In-Line PET/CT, and Software Fusion for Restaging of Recurrent Colorectal Cancer J. Nucl. Med., April 1, 2005; 46(4): 587 - 595. [Abstract] [Full Text] [PDF]

				M. Torabi, S. L. Aquino, and M. G. Harisinghani Current Concepts in Lymph Node Imaging J. Nucl. Med., September 1, 2004; 45(9): 1509 - 1518. [Abstract] [Full Text] [PDF]

				I. Kantorova, L. Lipska, O. Belohlavek, V. Visokai, M. Trubac, and M. Schneiderova Routine 18F-FDG PET Preoperative Staging of Colorectal Cancer: Comparison with Conventional Staging and Its Impact on Treatment Decision Making J. Nucl. Med., November 1, 2003; 44(11): 1784 - 1788. [Abstract] [Full Text] [PDF]

				C. Cohade, M. Osman, J. Leal, and R. L. Wahl Direct Comparison of 18F-FDG PET and PET/CT in Patients with Colorectal Carcinoma J. Nucl. Med., November 1, 2003; 44(11): 1797 - 1803. [Abstract] [Full Text] [PDF]

				B B Chin and R L Wahl 18F-Fluoro-2-deoxyglucose positron emission tomography in the evaluation of gastrointestinal malignancies Gut, June 1, 2003; 52(90004): iv23 - 29. [Abstract] [Full Text] [PDF]

				L. Kostakoglu, H. Agress Jr, and S. J. Goldsmith Clinical Role of FDG PET in Evaluation of Cancer Patients RadioGraphics, March 1, 2003; 23(2): 315 - 340. [Abstract] [Full Text] [PDF]

				L. Kostakoglu and S. J. Goldsmith 18F-FDG PET Evaluation of the Response to Therapy for Lymphoma and for Breast, Lung, and Colorectal Carcinoma J. Nucl. Med., February 1, 2003; 44(2): 224 - 239. [Abstract] [Full Text] [PDF]

				B. G.M. Durie, A. D. Waxman, A. D'Agnolo, and C. M. Williams Whole-Body 18F-FDG PET Identifies High-Risk Myeloma J. Nucl. Med., November 1, 2002; 43(11): 1457 - 1463. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ruers, T.J.M. Articles by Oyen, W. J.G. Search for Related Content PubMed PubMed Citation Articles by Ruers, T.J.M. Articles by Oyen, W. J.G. Social Bookmarking                            What's this?