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Multi-disciplinary team (MDT) meetings offer an integrated approach to health care in which medical and allied health professionals consider relevant options and collaboratively develop individual treatment recommendations for patients. They are a mandatory forum to discuss all new cancer patients in the UK (Department of Health, 2000) and in recent years have also been adopted in North America (Tripathy, 2003), Australia (Luxford and Rainbird, 2001; Zorbas et al, 2003) and other parts of continental Europe (Valdagni et al, 2005; Van Nes and Van de Velde, 2005). Discussion within the context of a MDT ensures patients benefit from the knowledge and experiences of a variety of specialists and this has resulted in improvements in care such as decreasing the time from diagnosis to treatment (Kingsmore et al, 2004), and greater patient and participant satisfaction (Tripathy, 2003). It is especially important when potential survival benefits must be balanced with the risks conferred by the radical treatment of some cancers, such as oesophago-gastric disease (Avery et al, 2007; Abate et al, 2010). Careful MDT treatment selection and accurate detection of metastatic disease is therefore crucial in the staging pathway to inform treatment plans for these patients.

Over the past decade, fluorodeoxyglucose (FDG) positron emission tomography-computed tomography (PET-CT) has been introduced to improve the staging of oesophago-gastric cancer. PET-CT integrates functional and anatomical imaging to allow precise localisation of areas of high-metabolic activity within a single superimposed picture and may, therefore, detect metastatic disease not identified by standard computerised tomography scanning (CTS) alone. Although UK national radiological guidelines recommend the use of PET-CT for staging oesophageal and oesophago-gastric cancer (The Royal College of Radiologists and the Royal College of Physicians, 2012), Scottish Intercollegiate Guidelines do not currently endorse routine use and recent evidence suggests that uptake varies considerably between centres with rates ranging between 48 and 98% (National Oesophago-Gastric Cancer Audit, 2010). Moreover, there is no consensus as to how the impact of PET-CT should be evaluated and reported in clinical research studies (Tunis and Whicher, 2009). To date, different approaches have been used, including correlation with post-operative histology, examination of response to neoadjuvant treatments, and prediction of survival (Salahudeen et al, 2008; Noble et al, 2009; Gillies et al, 2011; Brown et al, 2012; Gillies et al, 2012; Klayton et al, 2012; Shum et al, 2012; Yanagawa et al, 2012; Zhu et al, 2012; Tan et al, 2013). One study reported that PET-CT helped to plan the management of 174 cases (91%), changed staging in 65 (34%), and changed management in 50 cases (26%); however, it is unclear how this was assessed (Gillies, 2011).

The aim of this study was to assess the use of PET-CT in MDT decision making and to propose a method for evaluating this role.

Materials and Methods

Patients with oesophageal or oesophago-gastric adenocarcinoma or squamous cell carcinoma were identified from a prospective MDT database. Included were all those considered for radical treatment between June 2008 and June 2010. The MDT, based at University Hospitals Bristol NHS Foundation Trust, receives referrals from Musgrove Park Hospital (Taunton), North Bristol NHS Trust, Royal United Hospital NHS Trust (Bath), Yeovil District Hospital NHS Foundation Trust, and Weston Area Health NHS Trust, serving a resident population of approximately 1.5 million. All radiological, clinical, and pathological patient information are recorded in electronic databases and MDT recommendations are recorded and supplemented with a detailed letter written by the specialist team to the referring hospital to allow timely dissemination of information to the relevant personnel.

Staging pathway

The MDT protocol for management of patients with oesophageal and oesophago-gastric cancer includes review of endoscopic biopsies to confirm the histological diagnosis and review of the chest and abdominal CTS. Patients identified with definitive metastatic disease on CTS, or those unsuitable for radical treatment because of co-morbidities or frailty, are offered palliative treatments including best supportive care. If the CTS does not show metastatic disease or where there is any uncertainty, PET-CT is performed and this is also reviewed at the MDT meeting. A consultant radiologist is always present at the MDT meeting, and full reports of the CT from the referring Trust are also reviewed before the discussion. The database, therefore, contains prospective records of the MDT decisions before and after PET-CT review and details of final treatment recommendations after completion of all investigations including endoscopic ultrasound scan (EUS), laparoscopy, and bronchoscopy when performed (Figure 1).

Figure 1
figure 1

Staging pathway for patients with oesophageal and oesophago-gastric cancer within the Avon, Wiltshire, and Somerset Cancer network.

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Data extraction, analyses, and classification of the influence of PET-CT on MDT decision making

Details including age, gender, histological diagnosis, and recommendations recorded at each MDT meeting following CTS, PET-CT, other staging investigations, and the final treatment plan were extracted for each patient.

The number of patients recommended for radical treatment by the MDT was recorded and whether a PET-CT was performed. The influence of PET-CT on the MDT decision making was examined by calculating the proportions of patients in whom the PET-CT did not influence MDT recommendations (i.e., PET-CT confirmed the CT stage of M0 and the staging pathway continued) or PET-CT lead to a change in MDT recommendations (i.e., PET-CT showed unsuspected metastatic disease, refuted CTS suspected metastases, or detected another abnormality leading to the need for further investigations; Table 1).

Table 1 Examples of CTS and PET-CT report findings and categorisation of changes in MDT decision making
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Final treatments received were verified by independent review of pathological databases and hospital notes. Where the MDT-recommended radical treatment and this was not received, reasons for this were documented.

Results

During the study 418 new patients with oesophageal or oesophago-gastric cancer were discussed at 102 MDT meetings, of whom 240 were considered for radical treatment following MDT review of the CTS. Most patients were male and the predominant histological subtype was adenocarcinoma (Table 2).

Table 2 Details of patients being considered for radical treatment for oesophageal or oesophago-gastric cancer at a specialist MDT
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Of the 240 patients, 238 underwent PET-CT. One patient, selected for endoscopic mucosal resection, was not scanned and the reason for the other missing PET-CT was unclear (Figure 2). In 147 (61.8%) patients, the PET-CT results did not change MDT recommendations (Figure 2 and Table 3). In 91 (38.2%), however, PET-CT changed MDT recommendations by:

  1. i

    Refuting the possibility of widespread disease (n=25)

  2. ii

    Identifying metastatic disease (n=43)

  3. iii

    Identifying lesions that required further investigations (n=23)

Figure 2
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Flow of included patients within the study.

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Table 3 Categorisation of the influence of PET-CT on MDT decision making
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The distribution of histological tumour types was similar within each group although this was not assessed statistically due to small patient numbers (Table 3). The sites of metastatic disease detected by PET-CT are listed in Table 4. Further investigations included colonoscopy (n=11), excision biopsy (n=5), EUS-guided biopsy (n=2), bronchoscopy (n=2), fine needle aspiration (n=1), magnetic resonance imaging (n=1), and bone marrow aspiration (n=1). Of these, four confirmed M1 disease and patients received palliative treatments. In total, therefore, PET-CT prevented 47 patients (19.7%) from undergoing radical treatment in the presence of previously undetected metastatic disease.

Table 4 Location of M1 disease in patients in whom PET-CT showed metastases where the CTS did not
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Of the remaining patients, 143 (73.3%) commenced and 128 (65.6%) completed radical treatment (Table 5). Reasons for radical treatment were not started in certain patients included the detection of metastatic disease by other staging modalities (n=10), issues regarding fitness for surgery (n=22), patient choice (n=4), and in six patients the reason could not be determined. Disease progression or toxicity during neoadjuvant treatment precluded 10 patients from completing radical treatment and in a further 6 patients occult metastatic disease was detected at the time of planned surgical resection.

Table 5 Patients undergoing radical treatment according to staging category
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Discussion

This study examined the influence of PET-CT on MDT decision making in patients with oesophageal and oesophago-gastric cancer, and found that PET-CT influenced management by changing treatment pathways from radical to palliative intent in 43 patients (18.1%), uncertainty to curative intent in 25 (10.4%), and prompting further investigations in 23 patients (9.5%). Undertaking PET-CT prevented 47 (19.7%) patients from receiving radical treatment in the presence of undetected metastatic disease, thereby confirming the importance of incorporating this investigation into the routine staging pathway for oesophago-gastric cancer. It is therefore concluded that PET-CT is a valuable adjunct to decision making in oesophageal and oesophago-gastric cancer.

Previous studies of oesophago-gastric cancer patients have used PET-CT to assess response to neoadjuvant treatments (Klayton et al, 2012; Yanagawa et al, 2012; Tan et al, 2013) and investigate how it might predict survival (Brown et al, 2012; Shum et al, 2012; Zhu et al, 2012), but its potential benefits in improving the staging pathway have been less well examined. One study documented PET-CT findings in 191 oesophageal cancer patients discussed at a central MDT, which received referrals from 12 peripheral hospitals (Noble et al, 2009). Results of PET-CT scans were categorised as ‘true positives’ (PET-CT correctly identifying metastases not detected by CTS or EUS), ‘false positives’ (PET-CT incorrectly identifying metastases not detected on CTS or EUS), ‘true negatives’, and ‘false negatives’. Neither of the latter two categories was defined in the paper and the process for categorising PET-CT results was only partially reported, meaning that the classification system was difficult to interpret. The authors concluded that PET-CT helped to plan the management of 174 cases (91%), changed staging in 65 (34%) and altered management in 50 cases (26%); however, it is unclear what the authors meant by these terms. Information was also provided regarding the specificity (94%) and sensitivity (91%) of PET-CT but details of how these figures were calculated were missing. Another study, conducted within a central MDT, included 200 patients and compared PET-CT reports with the results of all other staging investigations (Gillies et al, 2011). Patients were categorised into five groups: ‘PET-CT upstaged disease to unresectable’, ‘PET-CT downstaged disease to potentially resectable’, ‘PET-CT demonstrated metastatic disease that was subsequently determined by cytology to be benign’, ‘PET-CT demonstrated potentially resectable disease that was subsequently determined by EUS or laparoscopy to be unresectable’, and ‘PET-CT agreed with combined CTS, EUS, and laparoscopy’. No definitions were provided for the first two categories and it was unclear whether the groups were mutually exclusive. In addition, some groups compared the reports of PET-CT with those of staging investigations that occurred before and after the PET-CT was performed in the staging pathway, meaning that the impact of PET-CT itself was difficult to elicit. Last, although five groups were described within the methods, the results section classified the impact of PET-CT into 12 separate categories making replication of this methodology in this study difficult. A third study compared TNM staging from PET-CT with EUS and CTS results and linked this to post-operative histological reports (Salahudeen et al, 2008). However, only 25 patients were included meaning that the number of patients in each category was small. This classification system is also difficult to apply to diseases where neoadjuvant chemotherapy is used because of the impact of this on post-operative histology. These individual aspects of staging are perhaps less important because the main question being asked of PET-CT is whether the patient should undergo radical or palliative treatment, which was not addressed in these articles, and neither was the impact of PET-CT on treatment recommendations within the MDT.

Although it is thought that this is the first study to comprehensively categorise how PET-CT influences MDT decision making for patients with oesophageal cancer, it has some limitations. Although it was conducted in the context of a central meeting consisting of six referring hospitals, it was limited to a single MDT and it is possible that results are not widely generalisable; however, this MDT follows standard guidelines for oesophageal cancer treatment and staging (Allum et al, 2011). Second, although decision making was recorded prospectively, data were extracted retrospectively and therefore relied on accuracy of record keeping. It was not possible to calculate survival differences between the groups because of small patient numbers and the need for a longer follow-up period, and it is therefore suggested that future studies might address this issue. Last, although 22 of 23 patients in whom PET-CT prompted further investigations underwent biopsy, histological confirmation was not undertaken where PET-CT showed metastatic disease and the CTS did not. It is assumed, therefore, rather than certain, that the PET-CT findings were accurate and resulted in a correct change in MDT recommendation. Whereas this approach may be practiced by many centres, there is emerging evidence, although limited, that biopsy of metastases identified by PET-CT may be required and this warrants further investigation (Han et al, 2012; Bingham et al, 2013).

This study has demonstrated the importance of PET-CT in achieving more accurate selection of patients for radical treatment of oesophageal cancer. Avoiding radical treatment in those with previously undetected advanced disease offers direct benefits for patients by preventing the detrimental effects of these therapies on health-related quality of life (Avery et al, 2007; Abate et al, 2010), and also has financial implications for hospital trusts. This is exemplified by the recently published SCOPE-1 trial, which assessed the impact of the addition of cetuximab to definitive chemoradiotherapy in the treatment of oesophageal cancer (Crosby et al, 2013). In this study, 86% of patients were staged with PET-CT, which may explain why 2-year survival rates (56%) were higher than anticipated (35%). It is therefore recommended that national guidelines are followed by all UK cancer centres, such that patients considered for radical treatment of oesophageal and oesophago-gastric cancer always undergo PET-CT. Currently, such patients undergo CTS and PET-CT separately because the quality of the CT component of PET-CT is inferior to CTS alone. Future research and investment should address this issue and aim to amalgamate these investigations, meaning that patients need to undergo only one test. This will reduce hospital attendances, streamline the staging process, and provide patients with prompt access to the correct treatments, whether radical or palliative in nature.