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10.1245/s10434-006-9259-6
Annals of Surgical Oncology 14:818-826 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Comparison of Multiphase CT, FDG-PET and Intra-Operative Ultrasound in Patients with Colorectal Liver Metastases Selected for Surgery

B. Wiering1, T. J. M. Ruers1, P. F. M. Krabbe2, H. M. Dekker3 and W. J. G. Oyen4

1 Department of Surgical Oncology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
2 Department of Medical Technology Assessment, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
3 Department of Radiology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
4 Department of Nuclear Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

Correspondence: Address correspondence and reprint requests to: B. Wiering, Department of Surgery, Radboud University Nijmegen Medical Centre, P.O. BOX 9101, 6500 HB, Nijmegen, The Netherlands; E-mail: b.wiering{at}chir.umcn.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: For patients with colorectal liver metastases, resection is the treatment of choice. Careful selection of these patients is crucial in order to reduce the chance of unexpected findings at laparotomy and abandoning further surgical intervention. Here, we evaluate the predictive value of CT and FDG-PET of the liver and extrahepatic findings compared to findings during laparotomy and 6 months follow-up.

Methods: 131 consecutive patients, selected for hepatic surgery for colorectal liver metastases by CT and FDG-PET, were evaluated prospectively. During surgery, the liver was assessed by intra-operative ultrasound, palpation and histology.

Results: In 127 patients (97%), CT was true-positive for liver metastases. In 3 patients, CT was false-positive and in 1 patient false-negative. In 126 patients (96%), FDG-PET was true-positive for liver metastases, in 2 patients FDG-PET was false-negative, in 3 patients true-negative (negative FDG-PET, false-positive CT). At laparotomy a total of 363 liver metastases was identified: 63 lesions <10 mm [10 (16%) detected by both CT and FDG-PET], 172 lesions of 10–20 mm [123 (72%) CT-positive, 129 (75%) by FDG-PET-positive], and 28 lesions >20 mm [124 (97%) CT-positive, 121 (95%) FDG-PET-positive].

CT and FDG-PET missed approximately 30% of the smaller liver lesions, resulting in a significant change in clinical management during surgery in only nine patients.

Conclusions: CT and FDG-PET have a similar diagnostic yield for the identification of liver metastases; both modalities being adequate on a patient-basis but inadequate to detect the smallest of liver lesions. However, the clinical relevance of the latter is limited.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Survival in colorectal cancer is strongly associated with the stage of the disease.1,2 Approximately 50–60% of the patients with primary colorectal tumour develop hepatic metastases. These metastases are either identified at the time of diagnosis and treatment of the primary tumour (synchronic metastases) or during follow-up (metachronous metastases).3–5 Surgery is the only potentially curative treatment in a select group of patients with colorectal liver metastases. Data in the literature suggest that only 20% of the patients with colorectal liver metastases qualify for curative treatment.6,7 After resection, 5-year survival rates between 35 and 45% have been reported. 8–11 However, in up to 50% of the patients who undergo curative liver resection, recurrent disease is detected in the first year after surgery. These figures strongly suggest that both before and during surgery minimal hepatic and extrahepatic metastatic disease remains undiagnosed. Therefore, a critical evaluation of preoperative and intra-operative diagnostic modalities is necessary.

In the last two decades, both computed tomography (CT) and magnetic resonance imaging (MRI) in the preoperative setting for colorectal hepatic metastases have been proven superior to preoperative abdominal ultrasound.12,13 These techniques are essential to obtain information on the anatomical location of the lesions and the possibilities for curative surgical treatment, although recently these modalities have shown more and more functional imaging potential.

Positron emission tomography (PET) with 18[F]-fluorodeoxyglucose (FDG) is a promising and upcoming modality for evaluation of recurrent colorectal disease.14–19 FDG-PET imaging is based on metabolic changes, instead of anatomic and structural changes as is the case in conventional imaging by CT or MRI. As such, FDG-PET has the potential of demonstrating tumour activity ahead of CT.

Most studies report on the diagnostic accuracy of FDG-PET in recurrent colorectal disease in general 15,19,20; only a few focus on liver involvement.14,16–18 In patients with colorectal liver metastases FDG-PET is considered particularly important to identify extrahepatic disease, which is generally considered a contraindication for surgical treatment of colorectal liver metastases.7,10,21–24 As described previously, approximately 25% of patients who are eligible for surgery on the basis of CT of the chest and abdomen are excluded from surgery by PET due to the identification of previously unknown extrahepatic disease.18 The combination of FDG-PET with CT and/ or MRI could allow better patient selection before hepatic surgery is performed, due to the fusion of functional and anatomical imaging. In patients with too extensive liver involvement or extrahepatic disease, futile laparotomy can thus be prevented.11,14–20,25,26 However, the relative contribution of each technique is still not well defined, and this often results in either suboptimal or inappropriate use of both techniques.

In the present study, we evaluated the accuracy of preoperative and intra-operative imaging in a subgroup of patients with colorectal liver metastases, who were selected for liver resection by both preoperative CT of the chest and abdomen and preoperative FDG-PET.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients and Study Design
Between January 1999 and November 2004, 132 consecutive patients were identified in our prospective database of patients operated for colorectal liver metastases. All patients were selected for resection of colorectal liver metastases with a standardized diagnostic protocol consisting of diagnostic imaging by CT of liver, abdomen and chest, FDG-PET, and colon visualization (either colonoscopy or colonography with barium enema). In all patients, surgical treatment of the liver was considered feasible on CT, i.e. favourable localization of the liver metastases in relation to the main vascular and biliary structures and absence of extrahepatic disease except for less than three lung metastases.27–30 Local recurrence had to be absent on colonoscopy or barium enema. FDG-PET was predominantly used to exclude extrahepatic disease and as an adjunct to CT to evaluate disease activity in the liver.

None of the patients had a history of previous liver surgery; thus excluding false positive findings on CT, FDG-PET and intra-operative ultrasound, due to postoperative fibrosis, inflammation, or altered liver architecture.

Patient and tumour characteristics were analysed according to the prognostic scoring system of Fong et al.22, in which the combination of five criteria (a disease-free interval of less than 12 months after resection of the primary tumour, number of tumours more than one, size of tumour more than 5 cm, node-positive primary tumour, and CEA >200 ng/ml) in a preoperative scoring system was highly predictive of poor outcome. As the Fong score proved to be highly prognostic for long-term outcome, it can be used to compare groups of patients for baseline prognostic variables between different studies.22

Postoperative follow-up after liver surgery was performed according to a stringent protocol: the first 3 years patients underwent a CT scan of the abdomen every 3 months and a CT scan of the chest every 6 months, and in case CT was inconclusive (e.g. indiscriminant results to whether the found lesion was malignant or benign), an additional FDG-PET scan, an ultrasound and/or MR scan of the liver were performed. Disease-free survival for at least 6 months after surgery was set as the criterion that justified laparotomy for curative liver surgery. In case of a relapse within 6 months or surgery for unexpected benign disease, the laparotomy was considered not appropriate. This time frame was chosen because FDG-PET generally shows lesions 6 month prior to CT and hence in this way FDG-PET could possibly have predicted these cases.17 Furthermore, laparotomy has a profound impact on the quality of life in the first months after surgery.31 Such negative effect on HRQoL hardly outweighs the benefit of resection when disease recurs within 6 months time.

CT Scanning
Multislice CT scan of the abdomen and chest was performed with a 4-slice scanner (Somatom Volume Zoom, Siemens, Erlangen, Germany). All patients received 900 ml diluted ionic oral contrast (Telebrix gastro, 30 g/3 l) 1 h before the CT examination. A noncontrast liver scan was followed by three distinct enhancement phases (arterial, portal and late venous phase). In combination with the portal phase the whole chest and abdomen were scanned. For multi-slice CT in the portal venous phase, initially 100 ml of contrast medium was administered [100 ml Omni-paque (iodine 350 mg/ml; Nycomed)], from January 2003 150 ml Xenetix (iodine 300 mg/ml; Guerbet). In all patients an Envision CT injector (Medrad, Pittsburgh, PA, USA) was used, with an injection rate of 4 ml/s. The scan parameters were 120 kV and 150–200 mAs. The detector configuration used was initially 4 x 5 mm2 (slice width 8 mm) and from April 2004 4 x 2.5 mm2 (slice width 3 mm). The timing of the venous phase was 70 s. Contiguous reconstructed sections were obtained. A Picture Archiving Communication System (PACS) was introduced in our hospital in April 2003. All images were evaluated by a radiologist with special experience in hepatic imaging.

FDG-PET
All PET scans were acquired using a full-ring dedicated PET scanner (Siemens ECAT Exact 47, Siemens AG, Germany). Patients fasted for at least 6 h prior to the study. Then all the patients had a serum glucose evaluated to interpretate potential poor imaging due to high glucose levels. One hour after injection of 250 MBq FDG (Tyco-Mallinckrodt, Petten, The Netherlands), emission images were acquired in 3D mode. Germanium-68 based transmission imaging was performed for attenuation correction. Acquisition time per bed position was 5 min for emission and 3 min for transmission. All PET scans were reconstructed using an iterative 2D Ordered Subset Expectation Maximization (OSEM) algorithm 32 using default settings (two iterations, eight subsets, and a three-dimensional Gaussian filter of 6 mm). Attenuation correction was based on segmented transmission images. All images were evaluated by a nuclear medicine physician with more than 5 years experience in hepatic imaging.

Surgical Technique
Nearly all surgical procedures were performed by one experienced surgical oncologist (TJMR) with more than 5 years experience in hepatic surgery. Surgery was performed through a right subcostal incision. Upon entering the abdomen, an initial exploration was performed to identify any previously undetected extrahepatic disease. Biopsy specimens and fresh frozen sections were taken in case of suspicious lymph nodes or peritoneal deposits. Intra-operative ultrasound was then performed (see subsequently). Resection was always considered to be the treatment of choice. Histopathological examination was performed on all resected tissues.

When complete resection with negative resection margins was considered impossible, local tumour destruction by radio-frequency ablation (RFA) or cryosurgery (in the first 2 years of our study) was considered. Ablative techniques were performed in those cases in which complete tumour clearance of the liver could still be obtained, either by local tumour destruction alone or in combination with resection. Both techniques were monitored by intra-operative ultrasound. In principle, hepatic surgery was abandoned in case of intra-abdominal extrahepatic disease or in case liver lesions were too extensive to be treated completely by resection or local ablation. The findings at a laparotomy and any reason for unresectable disease were recorded prospectively (e.g. too much tumour load or an involvement of the greater biliary or vascular structures). After curative hepatic surgery patients did not receive any standard chemotherapy. Chemotherapy was only initiated in case of tumour recurrence that was not amenable for surgical re-intervention.

Intra-Operative Ultrasound
Intra-operative ultrasound was performed using a Toshiba Diagnostic Ultrasound (SSA-340 with a PVF-738H Microprobe, Toshiba/Tustin, CA, USA) to detect, delineate, and characterize liver lesions relative to major biliary and vascular structures to assess resectability. All ultrasounds were performed by a radiologist with more than 5 years experience in hepatic imaging.

Assessment
All CT images were reviewed by a radiologist with special expertise in hepatic and abdominal imaging. All FDG-PET imaging was evaluated by a nuclear medicine physician with expertise in FDG-PET in colorectal cancer. First, CT and FDG-PET were reported independently. Subsequently, results of all preoperative diagnostic procedures, including verification of the imaging procedures by reviewing the images, were evaluated in a multidisciplinary oncology meeting by surgical oncologists, radiologists and nuclear medicine physicians. A joint assessment of all available data was performed to review clinical information and diagnostic imaging on a case-by-case basis, in order to decide which patients qualified for surgical treatment. Also if treatment consisted of liver resection, tumour ablation, or a combination of both. To avoid a too stringent patient selection for liver resection, which could deny patients a potentially curative intervention, laparotomy was performed in case of conflicting or equivocal diagnostic results in both CT and PET (intention to treat). However, CT was always considered the dominant technique for clinical decision making. The gold standard for intra-operative lesions was considered histopathology and if this was not possible, the intra-operative ultrasound.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patients
Table 1Go shows the characteristics of the study population. A total of 131 of 132 patients were included for evaluation.


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  		TABLE 1. Patients characteristics
 
One patient with poorly regulated diabetes mellitus and high blood glucose levels was excluded, as his FDG-PET scan was of poor quality and noninter-pretable. No patients were lost to follow-up in the first 6 months after laparotomy. The interval between CT and FDG-PET was in most cases less than 2 weeks (mean 10.4 days, range 0–32 days), and the interval between completion of the diagnostic procedures and surgical intervention was always less than 6 weeks, except in one patient (mean 31.0 days, range 1–54 days).

Liver Metastases
As shown in Table 2Go, in a patient-based analyses CT detected liver metastases in 127 patients (true-positive CT results) as compared to the findings at laparotomy, with intra-operative ultrasound. In three patients, the CT lesions proved to be benign (false-positive CT) and in one patient a liver metastasis was missed (false-negative CT). FDG-PET was true-positive in 126 patients, false-negative in 2 patients, and true-negative in the 3 patients with benign liver lesions.


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  		TABLE 2. Patient-based analysis of preoperative imaging results in 131 patients as compared to the histologically proven metastases at laparotomy
 
At laparotomy, 363 histologically proven liver metastases were found with intra-operative ultrasound and palpation. As shown in Table 3Go, both CT and FDG-PET missed most lesions smaller than 10 mm, many of which were only a few millimeters. Approximately 25% of lesions between 10 and 20 mm were missed by both CT and FDG-PET, while both techniques adequately detected lesions larger than 20 mm. More specifically, of the 63 lesions smaller than 10 mm, 10 were found with CT and 10 with FDG-PET (both 16%). Of the 172 lesions between 10 and 20 mm, 123 (71%) were seen on CT and 129 (75%) on FDG-PET. Of the 128 lesions greater than 20 mm, 124 (97%) were found on CT and 121 (95%) on FDG-PET. Figures 1Go and 2Go show that FDG-PET and CT may be discongruent and complementary for detection of metastases.


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  		TABLE 3. Detection rate of histologically proven liver metastases
 

Figure 1
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  		FIG. 1. Two liver metastases identified on CT (left panel), one of which was FDG-PET negative (right panel).

 

Figure 2
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  		FIG. 2. Liver metastasis missed on CT (left panel), but detected on FDG-PET (right panel).

 
During laparotomy, it proved to be technically impossible to perform a liver resection in 21 (16%) of the 131 patients. This was caused by too close proximity of the metastases to major biliary or vascular structures in 12 patients or by too extensive liver involvement in 9 patients; the latter being predicted by FDG-PET in 5 patients. Furthermore, 75 patients had hepatic resection alone, 13 patients had RFA only and 15 had resection in combination with ablative therapy. Three patients had benign liver disease, not requiring any further treatment. The remaining four patients were not treated surgically due to irresectable extrahepatic disease.

In the first 6 months of follow-up after laparotomy 42 new liver lesions developed in 15 patients, found by both CT and PET, suggesting that approximately 10% of liver metastases are too small to be detected during laparotomy, by either palpation or intra-operative ultrasound. Only one of these patients had a local recurrence (at the margin of a previous liver resection) in the liver, 14 patients had a recurrence elsewhere in the liver, including 1 patient with a recurrence in both the liver and the lung, and 1 patient with recurrence in both the liver and the lower abdomen. None of the three patients with benign liver lesions developed hepatic metastases in the first 6 months after surgery.

Intra-abdominal Extrahepatic Disease
As shown in Table 2Go, intra-abdominal extrahepatic disease was found in 10 patients (8%) during laparotomy. Although not unequivocally, CT had predicted extrahepatic disease in 2 of these patients, so it was missed in 8. In contrast, FDG-PET had predicted extrahepatic disease in 6 of these patients, so missed 4. In 6 patients, the liver metastases and the extrahepatic deposits were resected, while in 4 the laparotomy was terminated.

In one patient, an equivocal extrahepatic lesion on CT was considered false-positive as laparotomy was negative and no recurrence occurred in the first 6 months after laparotomy; in this case FDG-PET was negative for extrahepatic disease. In another patient with a no extrahepatic abnormalities on CT, FDG-PET was false-positive in a biopsy-proven inflammatory deposit in the abdomen. During follow-up, no metastatic disease occurred in this patient. In case of any discrepancies between CT and FDG-PET, CT was always considered the dominant technique for clinical decision making.

Extrahepatic disease in the abdomen not identified during laparotomy was unequivocally diagnosed at follow-up in seven additional patients (5%). Preoperative CT scan showed very small abnormalities in two of these patients. FDG-PET was positive in five of these patients, including the two patients with abnormal CT.

Pulmonary Disease
At the time of laparotomy, eight patients (6%) were known with pulmonary disease (14 lesions); all had curative resections of these lesions shortly after liver resection. Both CT and FDG-PET predicted these pulmonary lesions. Nine patients with pulmonary lesions on preoperative CT had to be classified as false-positive (no progression during follow-up), whereas FDG-PET hadno false-positive intrapulmonary results.

However, in the first 6 months after the liver surgery an additional 10 patients (8%) unequivocally developed pulmonary lesions. None of these patients were correctly diagnosed on the preoperative CT, but 6 patients already had small pulmonary lesions on the preoperative FDG-PET. These lesions were always located in the perihilar regions of the lungs.

Overall Disease Activity
Figure 3Go summarizes the overall results of the study. Immediately after resection of liver and lung metastases, 106 (81%) of the 131 patients were considered to be free of disease, so in 25 patients (19%) curative treatment was not possible. As indicated above, in 21 of these patients liver lesions could technically not be resected, and in 4 cases laparotomy was terminated because of unresectable extrahepatic disease. However, in the first 6 months after surgery, 24 (23%) of the 106 patients who were initially considered free of disease after surgery had developed new lesions in liver, abdomen, lungs or multiple sites. Of these patients, 6 were eligible for a curative surgical re-intervention and in 18 patients surgery was considered impossible and systemic therapy was started. These 24 patients who developed an early recurrence did not differ from the rest of the surgically treated patients with respect to the histological grade of the primary tumour, histological grade of the metastases, or according to prognostic variables of the Fong classification.


Figure 3
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  		FIG. 3. Flowchart of patients and outcome.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Both CT and FDG-PET contribute to the selection of patients with colorectal liver metastases, potentially eligible for surgical treatment. It is clear that those patients who are eventually taken to surgery represent a fraction of the total population of patients with colorectal liver metastases, which also includes those who do not qualify for surgery on the basis of diagnostic imaging. Nevertheless, the present study shows that both CT and FDG-PET have a number of limitations when comparing the CT and FDG-PET results to the findings during surgery and at follow-up. The majority of lesions smaller than 10 mm were missed by both modalities. However, the presence of unexpected additional small metastases did not have a major impact on surgical management. In only 9 of 131 (6.8%) patients, liver involvement was considered to be too extensive to achieve a curative resection. Unexpected technical issues due to close proximity of liver metastases to vessels or bile ducts are a relevant cause for unsuccessful surgery in 12 of 131 patients (9.2%). Although integrated PET-CT does have superior accuracy in patients with a history of prior liver surgery, it is unlikely that FDG-PET will play a major role to solve this issue in patients without prior liver surgery.33 Nevertheless, when FDG-PET indicates more extensive liver disease than CT (5 of 131 patients), the impact of this finding needs to be evaluated carefully as it may predict irresectability during laparotomy. Furthermore, technical issues may become less important by improvements in CT and contrast-enhanced MRI.33,34 In most of the patients with new liver metastases in the first 6 months after surgery, the CT scan was performed according the first protocol (i.e. 8 mm slices, 100 ml contract medium) and nearly all were read from film. With further optimalization of the CT liver protocol and the use of PACS, more adequate identification of metastases should be feasible, due to the possibility for peer reviewing and cataloguing of images. The same holds true for intra-operative ultrasound. Although it is currently considered to be the best technique to evaluate the liver during surgery.35–37 10% of patients develop new metastases in the first 6 months after surgery. Although speculative, these lesions may have been present during laparotomy, but too small for detection. Improvement of the sensitivity of ultrasound e.g. by using ultrasound contrast agents.38–40 may result in identification of more lesions, better surgical treatment and thus improving disease-free survival.

As expected in a patient population selected for surgery on the basis of CT of the chest and abdomen and FDG-PET, the number of patients with extra-hepatic disease at laparotomy was low (10 patients, 8%). FDG-PET was superior to CT in predicting these findings, which is in line with reports that evaluate the added value of FDG-PET when added to the staging procedure with CT alone.11,16,25 FDG-PET only missed four patients with extrahepatic abdominal disease, established during surgery. Although FDG-PET was false-positive in one patient with an inflammatory focus, the present study shows that positive extrahepatic intra-abdominal lesions on FDG-PET require very careful inspection during laparotomy. In five of six patients, FDG-PET find-ings were initially classified as false-positive during surgery, but metastases developed at these locations in the first 6 months thereafter. This finding suggests that it may be very difficult in a subgroup of patients to identify intra-abdominal lesions at laparotomy, even if the surgeon is aware of abnormalities on FDG-PET and/or CT.

CT of the chest is considered the gold standard to identify lung metastases.41–44 Data in literature suggest that small pulmonary metastases are better detected with CT than with FDG-PET.45–47 However, the present study shows that patients with a negative chest-CT but FDG-positive lesions in the perihilar region of lungs should be monitored carefully as the FDG-PET findings are strongly suggestive of metastases.

In the present study, a curative resection could not be achieved in 25 of 131 patients (19%). These patients require postoperative systemic therapy. Furthermore, 24 of the 106 patients (23%) in whom surgery was considered curative developed new metastases during the first 6 months of follow-up. This subgroup of patients might benefit from surgical re-intervention or from (initially adjuvant) systemic therapy after initial resection of the liver and lung metastases. In the present study, such adjuvant chemotherapy was not administered after hepatic resection.

In conclusion, the present study shows that in patients with colorectal liver metastases the frequency of unexpected findings at laparotomy is relatively low when using CT and FDG-PET in the preoperative work-up. The main challenge for improvement of diagnostic techniques is a more adequate assessment of the liver itself, as the liver often proves to be more involved than expected with regard to both the number of lesions and the exact localization. Unexpected extrahepatic FDG-PET findings require careful evaluation because these findings could potentially alter surgical patient management. FDG-PET may reveal occult disease both in the abdomen and chest earlier than CT. Furthermore, even at explorative laparotomy it appears to be very difficult to identify all metastases detected by FDG-PET.

Received for publication August 11, 2006. Accepted for publication October 4, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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