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10.1245/s10434-006-9013-0
Annals of Surgical Oncology 14:771-779 (2007)
© 2007 Society of Surgical Oncology
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Original Article

The Role of FDG-PET in the Selection of Patients with Colorectal Liver Metastases

B. Wiering, MD1, P. F. M. Krabbe, MD, PhD2, H. M. Dekker, MD3, W. J. G. Oyen, MD, PhD4 and T. J. M. Ruers, MD, PhD1

1 Department of Surgical Oncology, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands
2 Department of Medical Technology Assessment, Radboud University Nijmegen Medical Centre, P. O. Box 9101, 6500 HB, Nijmegen, The Netherlands
3 Department of Radiology, Radboud University Nijmegen Medical Centre, P. O. Box 9101, 6500 HB, Nijmegen, The Netherlands
4 Department of Nuclear Medicine, Radboud University Nijmegen Medical Centre, P. O. Box 9101, 6500 HB, Nijmegen, The Netherlands

Correspondence: Address correspondence and reprint requests to: T. J. M. Ruers, MD, PhD; E-mail: t.ruers{at}chir.umcn.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Selection of patients for hepatic resection of colorectal liver metastases is still limited. After conventional work up by computed tomography (CT) scan, 60% of patients will develop recurrent disease in the early years after resection. The aim of the present study was to evaluate whether an additional fluorine-18-deoxyglucose positron emission tomography (FDG-PET) improves patient selection and therefore adds value to select patients for curative liver resection.

Methods: Data from 203 patients selected for surgical treatment of colorectal liver metastases between 1995 and 2003 were collected in a prospective database. Group A consisted of 100 consecutive patients selected for hepatic surgery by conventional diagnostic imaging (CT chest and abdomen) only. Group B consisted of 103 consecutive patients selected for hepatic surgery by conventional diagnostic methods plus an additional FDG-PET.

Results: The number of patients with futile surgery, in which further treatment was considered inappropriate at laparotomy, was 28.0% in group A and 19.4% in group B. The reason for unresectable disease differed between groups. In group A, 10/100 (10.0%) patients showed extrahepatic abdominal disease versus 2/103 patients (1.9%) in group B (P = .017). In all other cases, resection was not performed because liver disease proved too extensive at laparotomy. For patients ultimately undergoing surgical treatment of the metastases, survival was comparable between groups. Overall survival at 3 years was 57.1% in group A versus 60.1% in group B. Disease-free survival at 3 years was 23.0% in group A and 31.4% in group B.

Conclusions: In patients with colorectal liver metastases, FDG-PET may reduce the number of negative laparotomies. However, the effect size on the selection of these patients seems not sufficient enough to affect the overall and disease-free survival after treatment.

Key Words: Colorectal • Liver metastases • FDG-PET • CT • Surgery • Extrahepatic disease


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer is one of the most common causes of cancer-related death in the Western world. After apparently curative resection of the primary tumor, recurrence of the disease is observed in up to 60% of patients. The liver is often the first site of metastatic disease and may be the only site of spread in as many as 30% 1–3 of patients. Surgery is the only possible curative treatment in a subset of patients with colorectal liver metastases. Eligibility for hepatic surgery of colorectal metastases depends on (1) the absence of extra hepatic tumour, and (2) the technical ability to completely resect all hepatic metastases.

Preoperative workup for resection of colorectal liver metastases is generally focused on imaging of the number and location of liver lesions by contrast-enhanced computed tomography (CT) or magnetic resonance imaging (MRI) of the liver and the exclusion of extrahepatic disease by abdominal and chest CT. Still, within 1 year, up to 50%4–7 of patients with potentially curative resection of liver metastases show recurrent disease at other sites of the liver or at extrahepatic sites. This suggests that these common modalities of diagnostic imaging frequently overlook minimal metastatic disease, which becomes apparent shortly after resection of the liver metastases.

Recently, fluorine-18-deoxyglucose positron emission tomography (FDG-PET) has been introduced as an additional staging modality in patients with colorectal liver metastases. FDG-PET is a sensitive imaging modality for the detection of tumour tissue based on the increased utilisation of glucose by tumour cells. Being a functional imaging modality, FDG-PET may be of value in the detection of additional liver lesions or extrahepatic disease. Moreover, FDG-PET may be helpful in determining the nature of liver lesions detected by CT. Several studies showed the impact of FDG-PET in clinical decision making in patients with suspected colorectal recurrence.8–16 Most of these studies concern recurrent colorectal cancer in general. Data on the specific impact of FDG-PET for selection of patients for hepatic surgery are, however, more limited.17–20 Moreover, direct comparison between patients selected for hepatic surgery with or without FDG-PET are still lacking.

In the present study, we investigated the effect of FDG-PET on disease-free and overall survival after hepatic surgery for colorectal liver metastases. For this purpose, we identified two homogeneous groups of patients with colorectal liver metastases who were selected for hepatic surgery of liver metastases, either with or without additional FDG-PET.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Protocol and Patient Groups
Between January 1995 and November 2003, a consecutive series of 203 patients was identified from our prospective colorectal liver metastases database who underwent laparotomy for intended resection of colorectal liver metastases. During the study protocol, all patients underwent a standardised diagnostic protocol consisting of conventional diagnostic imaging (CDM) by CT of liver, abdomen and chest; and colon visualisation, either with colonoscopy or barium enema. From January 1999, an FDG-PET was added to the standard diagnostic protocol. After diagnostic workup, patients were selected for hepatic surgery only when (1) preoperative imaging showed no extrahepatic disease (except for the presence of ≤ 2 resectable lung metastases, n = 5) and when (2) all liver lesions could be resected or treated adequately by local tumour ablation or a combination of both. Ultimately, two groups of patients could be identified: one group of 100 consecutive patients (January 1995 to December 1998) selected for hepatic surgery by standard CDM only (group A) and a second group consisting of 103 patients (January 1999 to November 2003) selected for hepatic surgery by CDM and additionally FDG-PET (group B).

Patient Characteristics
For comparison of both groups, patient and tumour characteristics were analysed according to the prognostic scoring system of Fong et al.21 Five prognostic variables were assigned one point each: disease-free interval of 12 months or more after resection of the primary tumour, number of tumours > 1, size of tumour > 5 cm, node-positive primary tumour, and carcinoembryonic antigen (CEA) > 200 ng/ml. The total score ranging from 0 to 5 proved to be highly prognostic for long-term outcome and could be used to compare groups of patients for baseline prognostic variables.21

CT Scanning
Between 1995 and December 1998, CT examinations of the abdomen and chest were performed with a one-slice CT scanner with 8-mm slices (Siemens, Erlangen, Germany); from 1999, examinations were performed with a spiral CT scanner (Somaton Volume Zoom, Siemens, Erlangen, Germany). All patients received diluted ionic oral contrast 1 h before CT examination. The liver was scanned before and after intravenous injection of iohexol nonionic contrast material (Omnipaque, iodine 350 mg/ml; Nycomed, Princeton, NJ, USA). By use of an Envision CT injector (Medrad, Pittsburgh, PA, USA) at a rate of 4 ml/s, intravenous contrast was injected through a 18-gauge catheter placed in an antecubital vein. A total of 100 ml of contrast material was injected. The liver was scanned in the venous phase 70 s after the start of the injection. Both nonenhanced and enhanced helical sequences were performed at 120 kV and 150–300 mAs. Contiguous reconstructed sections (pitch 1:1) were obtained with 7-mm collimation. All examination results were stored on a optical disc for further review and were analysed by two reviewers, both radiologist with an expertise in hepatic imaging.

FDG-PET
All FDG-PET studies were performed with a dedicated PET scanner (initially ECAT-ART, later 2001 ECAT-EXACT; Siemens/CTI, Knoxville, TN, USA) at the Radboud University Nijmegen Medical Centre. Patients had to fast for at least 6 h before the study. Immediately before the procedure, the patients were hydrated with 500 ml of water. One hour after intravenous injection of 200–260 MBq of FDG and 20 mg of furosemide, emission images of the area between the proximal femora and the base of the skull were acquired in 10-min-per-bed position in a series of seven to eight positions. The images were corrected for attenuation and reconstructed using the ordered-subsets expectation maximisation (OSEM) algorithm. The reconstructed images were displayed in coronal, transverse and sagittal planes. Patients with diabetes mellitus were not excluded.

Assessment
Results of both CDM and FDG-PET were reported at 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.

Surgical Technique
Surgery was performed through a right subcostal incision. Upon the abdomen being entered, an initial exploration was performed to preclude the presence of extrahepatic disease. Biopsy specimens and fresh frozen sections were taken in case of suspicious lymph nodes or peritoneal deposits. Intraoperative ultrasound was then performed to identify, count and characterise the nature, number and localisation of lesions relative to major biliary and vascular structures, and resectability was assessed. Resection was always considered to be the treatment of choice. The majority of resections were anatomical or segmental in both groups. Wedge resections accounted for 25% of procedures. When complete resection with negative resection margins was deemed not possible, local tumour destruction by radiofrequency ablation (RFA) or cryosurgery was considered.

In case of intraabdominal extrahepatic disease or if liver lesions were too extensive to be treated completely, further hepatic surgery was abandoned. The reason for unresectable disease was recorded prospectively. After hepatic surgery, patients did not receive any standard chemotherapy. Chemotherapy was only started in case of tumour recurrence that was not amenable for surgical reintervention.

Follow-up
After surgical intervention, all patients were followed prospectively at regular predetermined intervals. Standard follow-up in the first 3 years after hepatic surgery consisted of abdominal CT and serum CEA levels every 3 months and chest CT or chest X-ray every 6 months. After 3 years, imaging and serum CEA were reduced to twice yearly until 5 years after surgery. Colonoscopy or barium enema were performed regularly every 3 years. When one of the tests results indicated possible recurrent disease, further investigations were performed to confirm recurrence. Recurrence was defined as one or more new lesions on CT or, in case of inconclusive imaging, cytological or histological proof of recurrent disease was utilised. An isolated rise in serum CEA level was not considered sufficient evidence for recurrence. Median follow-up was 53 (range 13–116) months for all patients, 87 (range 72–116) months for group A and 43 (range 13–72) months for group B.

Statistic Analysis
The time from date of surgery to date of death was used as the end point in overall survival (OS); patients alive at the end of study were censored. The time interval between hepatic surgery and the first relapse, irrespective of its localisation, was taken as the period for disease-free survival (DFS). No secondary DFS was taken into account. Overall survival and DFS analyses were performed by the Kaplan–Meier method. All statistical analyses were performed with the SPSS programme (version 12.0.1). For comparison of differences in quantitative and ordinal variables between the groups, a chi-square test was used; for other comparisons, a t test was used. Group differences for survival analyses were analysed with the log-rank test; P values of less than .05 were considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Analysis at Laparotomy
After diagnostic workup, 203 patients underwent laparotomy: 100 in group A and 103 in group B. For group comparison, tumour and patient characteristics were analysed according to the prognostic scoring system of Fong.12 As shown in Table 1Go, the distribution of Fong criteria between groups was comparable. Also, the yield of intraoperative ultrasound was similar in both groups. At laparotomy, 28 patients (28.0%) in group A (n = 100) and 20 (19.4%) in group B (n = 103) were considered ineligible for surgical treatment at laparotomy, and further treatment consisted of chemotherapy only (Table 2Go). Remarkably, futile laparotomy was due to extrahe-patic disease in only two (1.9%) patients in group B compared with 10 (10%) in group A (P = .017).


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  		TABLE 1. Prognostic score according to Fong for patients analysed without FDG-PET (group A) and with fluorine-18-deoxyglucose positron emission tomography (group B)
 

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  		TABLE 2. Summary of findings at laparotomy
 
In the other irresectable patients, metastases were considered too extensive or too close to main vasculare structures in group A in 18 patients (18.0%) and in group B in 18 patients (17.4%) to permit resection or local tumour ablation.

Treatment Analysis
At laparotomy, 155 patients (76%) ultimately underwent surgical treatment of liver metastases. One group of 72 patients (January 1995 to December 1998) had been selected by standard CDM and laparotomy (group A) and a second group consisting of 83 patients (January 1999 up to November 2003) had been selected by CDM and additionally FDG-PET and laparotomy (group B).

Patient and tumour characteristics of the patients who underwent surgical treatment within both groups are given in detail in Table 3Go. No significant differences could be observed. Also, prognostic score according to the Fong criteria12 was comparable between both subgroups (Table 1Go).


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  		TABLE 3. Demographics and tumour characteristics of patients undergoing surgical treatment without (group A) or with (group B) fluorine-18-deoxyglucose positron emission tomography (FDG-PET)
 
In group A (CDM), 49 patients (68.1%) were treated by resection, 16 (22.2%) by resection plus local tumour ablation and seven (9.7%) by local tumour ablation alone. For group B (CDM plus FDG-PET), these figures were 47 (56.6%), 25 (30.1%), and 11 (13.3%), respectively.

Overall Survival
Survival analysis of the patients who underwent surgical treatment of metastases is given in Fig. 1Go. For patients in group A (without FDG-PET, n = 72), 1- and 3-year OS was 86.1% and 57.1%, respectively. For patients in group B (with FDG-PET, n = 83), these figures were 94.0% and 60.1%, respectively. No significant difference was observed in OS between groups (log rank, P value = .678). Perioperative mortality in both groups was similar; three patients (3%) in group A and three (3%) in group B.


Figure 1
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  		FIG. 1. Overall survival for patients who underwent surgical treatment selected either without (group A) or with (group B) fluorine-18-deoxyglucose positron emission tomography (FDG-PET).

 
For those patients who underwent resection only (and no local tumour ablation), OS at 1 and 3 years was 93.8% and 69.2% in group A (n = 49) and 93.6% and 63.7% in group B (n = 47). Again, survival curves between groups were not statistically significant (log rank, P value = .840). Subgroup analysis based on tumour characteristics (number of liver lesions, size of liver tumours and synchronous or metachronous occurrence) showed no significant differences in survival between the two groups.

Disease-free Survival
DFS at 1 and 3 years for patients who underwent surgical treatment was 54.4% and 23.0%, respectively, in group A (without FDG-PET) and 56.9% and 31.4%, respectively, in group B (with FDG-PET) (Fig. 2Go). For those patients who underwent resection only, DFS at 1 and 3 years was 62.6% and 29.9%, respectively, in group A (n = 49) and 67.4% and 29.2%, respectively, in group B (n = 47). DFS curves did not show any significant difference between groups (log rank, P value = .656).


Figure 2
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  		FIG. 2. Disease-free survival for patients who underwent surgical treatment selected either without (group A) or with (group B) fluorine-18-deoxyglucose positron emission tomography (FDG-PET).

 
Site of Recurrence
Recurrence rate for the first site of recurrence in both groups is depicted in Fig. 3Go. Recurrence in the liver was found in 25/72 patients in group A (34.7%) and in 21/83 (25.3%) in group B. Extrahepatic recurrence was the first site of recurrence in 19 patients from group A (26.3%) and in 21 from group B (25.3%). Combined recurrence was observed in six patients (8.3%) from group A and 11 patients (13.3%) from group B. No significant differences were observed between groups.


Figure 3
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  		FIG. 3. Site of first recurrence for patients who underwent surgical treatment selected either without (group A, n = 72) or with (group B, n = 83) fluorine-18-deoxyglucose positron emission tomography (FDG-PET). Percentages indicate patients within one group (A or B) who developed recurrence at the indicated site. Actual numbers are noted above the bars.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
It has been recognised that FDG-PET may have a role in the selection of patient who would benefit from surgical resection of colorectal liver metastases. Previous studies demonstrate that FDG-PET may, in particular, detect additional extrahepatic lesions missed by conventional CT. It is generally assumed that, except for isolated lung lesions, these extrahepatic lesions indicate poor prognosis and preclude further liver resection. The present study shows that FDG-PET decreases the number of futile laparotomies for resection of colorectal liver metastases by better detection of extrahepatic abdominal disease. The number of patients in which resection was refrained from during laparotomy because of extrahepatic intraabdominal disease was significantly lower in patients screened by FDG-PET. However, when surgical exploration of the abdomen did result in resection or local ablation of liver metastases, in this subgroup of the population, no significant differences between patients selected with or without FDG-PET were observed for both DFS and OS.

Although many studies have evaluated the additional diagnostic accuracy of FDG-PET, data on the effect of FDG-PET on OS after liver resection of colorectal metastases are limited. Strasberg et al.22 reported a 3-year survival rate of 77% after resection in patients selected for liver surgery by conventional CT plus additional FDG-PET. The authors concluded an improved survival rate in comparison with previous published series, showing 3-year survival rates between 30% and 58% without the use of FDG-PET.23–35 When identifying a comparable group of patients in our series—patients who underwent resection without local ablative procedures—the 3-year survival rate in the FDG-PET group was 63.4% versus 69.9% in the group without FDG-PET. Since we included a well-matched control group of patients without FDG-PET, our series differs significantly from the study by Strasberg et al.22 In particular because resection criteria, diagnostic protocols and CT readings were identical in both arms of our study. When using a well-balanced control group, the effect of FDG-PET on OS seems lower than reported in several other studies. Even more clearly, in patients who indeed underwent resection, we could not identify any significant difference in survival between patients selected for surgery with or without FDG-PET. This at least suggests that the intraoperative surgical approach to disease control and postoperative care were similar. Moreover, it shows that the determinants of survival remain primarily the biology of the tumour, its resectability and its response to chemotherapy, none of which apparently was altered by imaging techniques used primarily for lesion detection.

Similarly, technical advances in CT scanning implemented during the study do not seem to have had an impact on survival data. It may well be that, except for the well-matched control group, the identical quality of radiological reading in both groups is of overriding importance. It seems inevitable that a high accuracy of conventional radiological workup will influence the beneficial effect of additional FDG-PET scanning. As CT techniques improved concurrent with the use of FDG-PET, it would be a reasonable assumption that some patients with extrahepatic disease who may have been missed using older CT technology were now detected, therefore reducing the potential incremental yield of FDG-PET imaging.

Although FDG-PET significantly reduced the number of patients who could not be resected at laparotomy because of extrahepatic intraabdominal disease, FDG-PET had no influence on the number of patients who did not proceed to resection because of more extensive liver disease than estimated before surgery. In these cases, unexpected additional small liver lesions not detected by imaging methods before surgery precluded resection. As noted by various other studies, the sensitivity of FDG-PET for liver lesions smaller than 1 cm is relatively low, and for these cases, FDG-PET did not show any added value compared with CT or MRI.20,22,36 The finding that FDG-PET mainly influences resection rates by detecting additional extrahepatic disease is in accordance with earlier observation by others and our own group.13,15,19,20,37–39 Several studies9,10,12,13,15–18,20,37,40–46 show that additional FDG-PET may change clinical management in up to 30% of patients analysed by conventional workup, mainly because of additional extrahepatic lesions detected by FDG-PET.

In conclusion, in this study the introduction of FDG-PET reduced the number of futile laparotomies in patients with extrahepatic disease due to better detection of these tumour laesions. However, after surgical treatment, both OS and DFS were similar, irrespective whether or not FDG-PET was used.

The main shortcoming of the present study is that only patients were analysed who were already selected for explorative laparotomy either with or without additional FDG-PET. Thus, the precise impact and relevance of FDG-PET on clinical management decisions during the diagnostic workup is not taken into account. However, any major benefit from the addition of FDG-PET in the preoperative workup would have been noted in our data by improved survival in the FDG-PET group. Moreover, patients were not randomised, and results may have been influenced by the improved performance and interpretation of CT. Such issues can only be overcome in a randomised controlled clinical trial. To date, data from such a trial are not available, which means that the role of FDG-PET in patients with colorectal liver metastases can only be defined from well-controlled, case-mixed, cohort studies, such as presented here.

Our study indicates that screening of patients with FDG-PET who are considered for resection of colorectal liver metastases remains appropriate. As newer modalities such as PET-CT become more widely available, reevaluation may be considered.

Received for publication October 27, 2005. Accepted for publication February 20, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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