Annals of Oncology Advance Access originally published online on April 13, 2007
Annals of Oncology 2007 18(11):1774-1781; doi:10.1093/annonc/mdm108
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© 2007 European Society for Medical Oncology
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The expanding role of PET technology in the management of patients with colorectal cancer
1 Ludwig Institute for Cancer Research, Melbourne Centre for Clinical Sciences
2 Ludwig Institute Oncology Unit
3 Centre for Positron Emission Tomography
4 Department of Medicine, University of Melbourne, Austin Health, Heidelberg, Victoria, Australia
* Correspondence to: Dr R. A. Herbertson, Ludwig Institute for Cancer Research, Melbourne Centre for Clinical Sciences, 1st Floor, Harold Stokes Building, Austin Hospital, 145 Studley Road, Heidelberg, Victoria 3084 Australia. Tel: +61-394963098; Fax: +61-94965892; E-mail: rebecca.herbertson{at}ludwig.edu.au
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Abstract |
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The therapeutic options and subsequent survival of colorectal cancer (CRC) patients has increased substantially over recent years. While surgical excision of the primary cancer results in cure of
50% of patients, recurrence and metastatic disease still remains a significant cause of death. Although resection of liver or lung metastases can result in cure, relapse rates remain high, indicating that patient selection needs improvement. Positron emission tomography (PET) technology has a great deal to offer with respect to CRC management, particularly in the setting of patient selection for metastasectomy and in the evaluation of possible recurrent disease, however it has not yet become a routine part of the management of all CRC patients. This review article aims to discuss the current and future implications of PET technology in the optimal management of CRC patients throughout their care pathway. Key words: colorectal cancer, positron emission tomography
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introduction |
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TopAbstractintroductionthe role of PET...summaryReferences |
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colorectal cancer
The last 5 years have brought significant improvements in the disease-free and overall survival of colorectal cancer (CRC) patients both in the primary and metastatic setting. This has largely been achieved by more accurate staging of disease, the improved and expanded role of surgery, and an increased number of available chemotherapeutic options. While the prognosis for untreated patients with metastatic disease is likely to be 6–12 months, the routine use of chemotherapeutics such as oxaliplatin and irinotecan and the future role of combinations with epidermal growth factor receptor and vascular endothelial growth factor targeted antibodies means patients have many more lines of potentially efficacious treatment. For those with unresectable disease, median survival is currently up to 20 months with combination chemotherapy [1, 2]. The increased role of surgery for metastatic disease is now well established, although the extent of resectability remains the topic of debate within the multi-disciplinary team. Liver-specific imaging in this situation often includes computed tomography (CT), magnetic resonance imaging (MRI), or 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG)–PET, usually as directed by local surgical unit protocol. Less than 20% of patients who present with hepatic metastases are potentially resectable, but it is clear that surgery is their only chance of potential cure. Five year overall survival following complete resection of isolated liver metastases has been reported as 30%–40% with a 10 year survival of 23%–26% [3, 4], indicating the proportion of patient who relapse following potentially curative resection remains high.
FDG–PET
Positron emission tomography (PET) technology uses radiotracers to detect and quantify cellular and biochemical processes non-invasively. 18F-2-fluoro-2-deoxy-D-glucose (FDG) is the most common radiotracer currently used in oncology. This is a glucose analogue attached to a positron emitting radionuclide 18F, which is taken up by cells overexpressing cell surface GLUT1 transporters, such as cancer cells. Once inside the cell, it is phosphorylated by hexokinase into glucose-6-phosphate and becomes trapped, as it is unable to enter the normal cellular glycolytic pathways. This intracellular trapping occurs preferentially in malignant cells as they are also known to have an increased metabolic rate and reduced glucose-6-phosphatase activity. The PET scanner is able to detect the positrons emitted by 18F as it decays intracellularly, and represent this visually. Semi-quantitative analysis of FDG–PET images can be carried out by calculating the standardised uptake value (SUV), which represents the metabolic activity for the tumour compared with that in surrounding tissue, corrected for injected dose and patient weight. PET imaging with radiotracers specific to other cellular processes such as membrane synthesis, cell proliferation, cellular perfusion, and tumour hypoxia are also under investigation, and will also be discussed.
integrated FDG–PET/CT
Although FDG–PET allows the evaluation of the whole body, it is limited in the detection of small lesions (i.e. <1 cm) [5], not all tumour types are FDG avid, and it lacks specific anatomical detail. False positives in the presence of chronic inflammation and following surgery or radiotherapy may occur secondary to increased FDG uptake in neutrophils, granulation tissue, and macrophages. CT has long been established as the standard imaging modality for the assessment of malignancy, which is able to provide anatomical information and detect pathological change by identifying abnormal contrast enhancement. Depicting malignant change in normal sized structures such as lymph nodes or distinguishing residual scar tissue from active tumour are difficult with CT. Combining the functional information obtained from a FDG–PET scan with the anatomical detail of a CT scan has been shown to improve sensitivity, specificity, and accuracy of disease assessment [6–8]. Although much of the published evidence supporting the use of PET technology in CRC focuses on FDG–PET [6, 9, 10], it is increasingly well recognised that integrated FDG–PET/CT may provide superior information and is now the modality of choice where the resources are available. This article will review the evidence for FDG–PET and the more recent studies using FDG–PET/CT in CRC patients.
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the role of PET technology in CRC |
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primary diagnosis and staging
The low sensitivity of FDG–PET for small lesions (<1 cm), and the chance of false positives in inflammatory bowel lesions, explains the current lack of evidence to indicate FDG–PET should be part of the routine screening or staging of patients. That is not to say it does not contribute to more accurate staging. While FDG–PET alone has a low sensitivity for lymph node involvement, small studies have shown FDG–PET/CT is more accurate in assessing tumour–node–metastasis stage compared with CT and FDG–PET alone [6, 9–13]. However, another study found it not superior to conventional staging with CT [12]. The primary staging of rectal cancers is one specific indication where FDG–PET/CT is likely to significantly impact on patient management, through more accurate staging. Although MRI already has an established role in rectal tumour staging by facilitating accurate assessment of the mesorectal fascia (and hence prospects for carrying out a total mesorectal excision) [14], the addition of FDG–PET/CT is likely to optimise accurate assessment of nodal [15] and metastatic disease. Combining accurate evaluation of tumour extent and local disease should aid the multi-disciplinary team in their decision making regarding the need for neo-adjuvant radiotherapy, however current published evidence is in a small cohort [15].
The detection of liver metastases is directly related to the size of the lesions. When detecting lesions <1.5 cm, spiral CT has been shown to be more sensitive than FDG–PET alone, but the addition of FDG–PET to standard staging CT is complementary, and improves therapeutic management of patients with liver metastases [5]. FDG–PET can lead to changes in management in 2%–36% of CRC patients undergoing initial staging [11–13, 15, 16], but this small body of evidence (and lack of cost–benefit analysis) is yet to impact on general clinical practice, particularly when resources in many countries are currently limited.
patient selection for metastasectomy
One of the most compelling indications for the routine inclusion of FDG–PET/CT in CRC patient assessment is in those being considered for metastasectomy, as avoiding major surgery in patients with undetected nodal or distant metastatic disease is vital [17, 18]. Despite the now well-established role of liver metastasis resection in CRC patients, studies have indicated up to 75% of patients who undergo this potentially curative surgery still relapse [3, 19, 20], fuelling the debate as to what should be considered ‘resectable’. This high relapse rate is at least partly a reflection of inaccurate staging, with occult extra-hepatic metastatic disease going undetected before surgery. Two meta-analyses demonstrate high sensitivity and specificity for FDG–PET in this setting [17, 18]. Wiering et al. [17] found that the pooled sensitivity and specificity of FDG–PET were 91.5% and 95.4% for extra-hepatic disease, compared to 60.9% and 91.1%, respectively, with CT. Bipat et al. [18] found a sensitivity of 94.6% on a per-patient basis with FDG–PET (64.7% with helical CT and 75.8% 1.5-T MRI) and 75.9% on a per-lesion basis (63.8% with helical CT and 64.4% 1.5-T MRI). On a per-lesion basis, Gadolinium and superparamagnetic iron oxide-enhanced MRI had significantly better sensitivity compared with non-enhanced MRI, but comparable sensitivity when compared with FDG–PET [18]. Currently, the need for liver-specific contrast-enhanced MRI in addition to CT is often reserved for the accurate characterisation of liver lesions in the presence of fatty infiltration (or after chemotherapy), but this is determined by local surgical unit policy. A change in therapeutic strategy on the basis of FDG–PET/CT in this setting in up to 30% of patients has been demonstrated [7, 17, 21], although it can also falsely upstage a small minority of patients [21]. Small studies have identified improved disease-free and overall survival in patients who were evaluated with FDG–PET before surgery [22, 23]. A considerable cost saving in terms of avoiding postoperative intensive care and potentially lengthy hospital stays is likely to be made by avoiding major surgery in patients with undetected extra-hepatic (or extra-pulmonary) disease. Figure 1 illustrates the use of FDG–PET/CT in the assessment of extra-hepatic disease before metastasectomy.
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evaluation of recurrence
There is no evidence to support the use of FDG–PET in routine surveillance following curative primary surgery, however, FDG–PET and more recently integrated FDG–PET/CT now has an established role in the standard of care of patients with suspected recurrent disease (often presenting with a rising carcinoembryonic antigen) [24]. A meta-analysis of FDG–PET in the detection of recurrent CRC by Huebner et al found an overall sensitivity and specificity of 97% and 76% respectively, which led to a change in management in 29%. This is similar to the 32% demonstrated in the summary of Gambhir et al. [16, 25].The prospective, blinded comparison by Valk et al. [26] of FDG–PET and CT in CRC recurrence found that sensitivity and specificity were 93% and 98%, respectively, compared with 69% and 96% for CT. FDG–PET can be particularly helpful in the detection of omental or peritoneal disease, which is often difficult to detect on CT alone [27], but there are limitations to its sensitivity in the assessment of small pulmonary nodules (<1 cm) due to the resolution limitations of PET scanners. As well as being an important tool in the diagnosis of recurrence, FDG–PET also has a role in predicting resectability of recurrence, and hence improving the selection of patients suitable for further surgery [28]. Figure 2 demonstrates how FDG–PET/CT can aid in the detection of recurrent disease after liver surgery.
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radiotherapy planning
Increasingly, it has been recognised that FDG–PET/CT can have a significant impact on radiotherapy planning in many tumour types. Although the data focusing specifically on rectal cancer are limited, it is likely that the results obtained in other tumour types translate to improved rectal tumour volume delineation in primary rectal carcinoma, but this requires further investigation. In a study by Ciernik et al. [29] of 39 cancer patients undergoing radiotherapy planning for lung, head and neck, and pelvic tumours, integrated FDG–PET/CT led to an increase in the estimated gross tumour volume (GTV) in 17%–33%, and reduction in 19%–67% of cases. They concluded that in 56% of cases, GTV delineation was changed significantly if information from metabolic imaging was used in the planning process. The use of FDG–PET also reduced volume delineation variability between oncologists and revealed distant metastases in 16% leading to a change in treatment strategy from curative to palliative. Dizendorf et al. [30] found FDG–PET led to a change in management in 27% of 202 consecutive cancer patients as a result of the detection of distant or lymph node metastases, changing radiation volume or intention of treatment. Although small studies indicate that tumour target volume assessment may be improved with the addition of FDG–PET, further clarification of this specifically in rectal cancer patients is required.
response assessment
assessing early metabolic response to chemotherapy.
Responding tumours undergo functional metabolic changes before any structural stabilisation or shrinkage can be visualised on CT scanning, and the development of FDG–PET means imaging the earliest of physiological changes in response to treatment is now becoming a reality. Neo-adjuvant chemotherapy (usually with an oxaliplatin-based regimen) is considered one of the standard options for multiple colorectal liver metastases to improve complete resection rate and overall survival [31], and is known to downstage a proportion of those initially deemed unresectable [32]. This strategy can also help identify those with biologically aggressive disease as unsuitable for subsequent resection. FDG–PET can provide the opportunity to assess early metabolic response to neo-adjuvant chemotherapy, and may aid the decision regarding the most appropriate length of neo-adjuvant chemotherapy required to maximize response before surgery [33–36]. Findlay et al. [33] found tumour to liver ratio could discriminate responders from non-responders at 4–5 weeks, and review by Young et al. [37] stated that although reduction in SUV after one cycle of chemotherapy could predict response and correlate with subsequent tumour shrinkage, this measurement became more reliable after two or three cycles. Figure 3 demonstrates a complete metabolic response to chemotherapy on FDG–PET/CT.
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The recent evidence indicating early metabolic response to chemotherapy correlates with later RECIST (Response Evaluation Criteria in Solid Tumours) response on CT [24, 33, 38, 39], has led to the proposed European Organisation for Research and Treatment of Cancer criteria for FDG–PET determined metabolic response [37]. The National Cancer Institute have also acknowledged the importance of FDG–PET in assessing therapeutic efficacy, and have published protocols to standardise methods for obtaining and analysing FDG–PET across multicentre clinical trials [40]. FDG–PET in the assessment of response of metastatic gastrointestinal stromal tumours to imatinib mesylate is a good example of a clinical scenario where PET has proven benefit over CT in the assessment of early response to a molecular targeted therapy [41]. Using FDG–PET in the early assessment of new agents in early-phase clinical trials may also provide a way of assessing efficacy early and speeding up the drug development process.
assessing response to other treatment modalities.
Including FDG–PET in response assessment at treatment completion may help in determining the presence of residual disease following radiotherapy, chemoradiotherapy or local ablative therapy [24, 42], and act as a baseline before ongoing follow-up. Although it can generally be carried out within 4 weeks of the completion of chemotherapy, there should be a longer interval left following radiation or surgery owing to the possibility of false positives with inflammation or regenerating tissue [24]. When carried out at an appropriate time point following treatment, it has the potential to offer information on residual tumour cell viability, differentiate tumour from fibrosis or scarring, and help predict survival [43]. Two small studies looked at the ability of pre-operative FDG–PET to aid in assessing response to neo-adjuvant chemoradiation and subsequent outcome in rectal cancer. Guillem et al. [44] found a greater mean percentage decrease in SUVmax correlated with a better outcome in 15 rectal cancer patients, and Kalff et al. [45] found FDG–PET response following neo-adjuvant chemoradiation was associated with disease-free and overall survival.
molecular imaging using other PET radiotracers
With the development of novel molecular targeted therapies and biological agents, PET technology is the focus of much interest for its potential role in non-invasive molecular imaging, and the assessment of the molecular effects of new agents. PET is likely to have an increasingly important future role in translational research, having the ability to focus on underlying tumour cell biology and image malignant cellular processes. While the assessment of standard chemotherapeutics have focused on tumour shrinkage, novel therapies may have a cytostatic rather than cytotoxic effect, hence creating challenges especially in early-phase clinical trials using standard RECIST response criteria. Recognition that molecular imaging techniques must be developed alongside new therapies that specifically target molecular processes such as proliferation and angiogenesis has led to the investigation of newer radiotracers. 18F-3'-deoxy-3- fluorothymidine (18F-FLT), 11C-choline, 15O-water, and 18F-fluoromisonidazole (18F-FMISO) are all such investigational agents being evaluated in clinical trials.
markers of proliferation.
Recent development of a biologically stable thymidine analogue 18F-FLT can be used to detect cellular amino acid (and hence DNA) synthesis when it becomes trapped intracellularly following phosphorylation by thymidine kinase-1, which is elevated in malignant cells. These properties indicate that it may act as a potential marker of colorectal tumour cell proliferation, and hence provide a possible method for non-invasive grading of tumours. Although this remains an experimental indication, it has potential as a non-invasive method for predicting early response to adjuvant chemotherapy or assessing efficacy of cytostatic drugs [46].
Radiolabelled choline radiotracers such as 11C-choline and 18F-choline are also potential markers of cellular proliferation. Choline is needed for many cellular processes, but in tumour cells radiolabelled choline is thought to correlate with cell membrane phosopholipid synthesis, and hence cellular proliferation rate [47]. 15O-water is a freely diffusible radiotracer which is under investigation as a marker of perfusion [48]. It has the potential to be used in clinical trials to monitor changes in blood flow in response to chemotherapy or anti-angiogenic agents such as bevacizumab [49].
hypoxia imaging.
Solid tumours become hypoxic when cellular proliferation exceeds the supply of oxygen from inadequate tumour vasculature, and it is thought to contribute to chemotherapy and radiotherapy resistance through a number of mechanisms in variety of tumour types [50]. Hypoxia is involved in initiating angiogenesis (via its influence on the ‘angiogenic switch’), which is directly associated with metastatic potential and cancer progression [50, 51].18F-FMISO is a hypoxia selective agent that shows potential as a radiotracer for non-invasive imaging of tumour hypoxia and hence may have a future role in the evaluation of molecular response to agents such as bevacizumab. It is a nitromidazole derivative, which becomes trapped in hypoxic tissue as low partial pressure of Oxygen prevents re-oxidation of 18F-FMISO metabolites. In glioma, it has been shown to provide a non-invasive assessment of hypoxia and be prognostic for treatment outcome [52], but studies in CRC patients are still in progress. Early resolution of 18F-FMISO abnormality during treatment has been shown to be associated with improved locoregional control in head and neck cancer [53], and similar findings may be possible in CRC, but no published evidence is available. One limitation to hypoxia imaging is that it is often associated with reduced perfusion, meaning it maybe difficult for the radiotracer to be delivered to the area of interest [48], but Bruehlmeier et al. [54] found hypoxia was independent of perfusion in gliomas. Using 18F-FMISO and 15O-water for molecular response imaging in patients receiving agents like bevacizumab is under investigation. Selecting patients most likely to benefit from such targeted therapies and assessing early molecular response (e.g. reduced tumour hypoxia as a result of vasculature normalization), could improve cost-effectiveness, individualise treatment, and potentially improve outcome.
incidental colorectal lesions
FDG–PET has been shown to have an 84% specificity for detecting colonic adenomas, and the diagnostic test characteristics improve with the size and grade of adenoma [55]. Incidental FDG accumulations in the gastrointestinal tract have been reported in 1.3%–3% of patients having a FDG–PET/CT, and have been shown to be associated with a substantial risk of underlying cancer or pre-cancerous lesion [56, 57]. Further investigation of such lesions is essential, as early detection of an occult CRC is likely to have a significant impact on patient management and outcome.
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TopAbstractintroductionthe role of PET...summaryReferences |
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Although PET technology cannot replace CT or MRI for accurate anatomical imaging of CRC, there is sufficient evidence to indicate that FDG–PET can impact significantly on patient management. The strongest evidence currently supports its routine use in the assessment of suspected recurrence and in patient selection for metastasectomy. The Centers for Medicare and Medicaid Services (CMS) in the United States expanded its reimbursable coverage for FDG–PET to include ‘all clinically appropriate uses of PET in CRC’ in December 2000 [58]. For primary diagnosis coverage, ‘PET must be used to potentially avoid or direct an invasive diagnostic procedure’. For use in staging or restaging of disease, PET is only covered if staging is uncertain following conventional imaging and if "the clinical management of the patient may differ according to the stage of the disease" [58]. Despite this, it is yet to become a routine component of the investigation of CRC patients for these indications in many other countries. While the CMS have accepted that accuracy data and evidence of impact on management are sufficient for its inclusion in routine care in CRC patients, others have called for more prospective randomized trials to prove its ability impact on patient outcome. PET is a diagnostic test rather than an intervention; therefore, this type of outcome study is largely inappropriate. It would be very difficult to attribute an improvement in outcome on the addition of a diagnostic test, as any result would be confounded by the effects of therapy [59]. Prospective studies are important, but guidelines for the funding of FDG–PET should be based on the evidence for impact on patient management, rather than outcome. Cost–benefit analysis for the use of FDG–PET in CRC patients before metastasectomy is likely to fuel the support for public funding for this indication, as small studies have already indicated that it can reduce overall costs [60, 61]. Further similar studies for other CRC indications are warranted. The evidence presented (summarized in Table 1) clearly demonstrates FDG–PET impact on patient management, particularly in detection of metastatic or possible recurrent disease, and should therefore be utilized in patients with CRC in these clinical scenarios.
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Received for publication January 21, 2007. Revision received February 20, 2007. Accepted for publication February 20, 2007.
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