doi:10.1111/codi.12922

Original Article

The impact of a dedicated multidisciplinary team on the management of early rectal cancer P. G. Vaughan-Shaw, J. M. D. Wheeler and N. R. Borley Department of Colorectal Surgery, Cheltenham General Hospital, Cheltenham, UK Received 14 July 2014; accepted 31 December 2014; Accepted Article online 20 February 2015

Abstract Aim Local excision of early rectal cancer (ERCa) offers comparable survival and reduced operative morbidity compared with radical surgery, yet it risks an adverse oncological outcome if performed in the wrong setting. This retrospective review considers the impact of the introduction of a specialist early rectal cancer multidisciplinary team (ERCa MDT) on the investigation and management of ERCa. Method A retrospective comparative cohort study was undertaken. Patients with a final diagnosis of pT1 rectal cancer at our unit were identified for two 12-month periods before and after the introduction of the specialist ERCa MDT. Data on investigations and therapeutic interventions were compared. Results Nineteen patients from 2006 and 24 from 2011 were included. In 2006, 12 patients underwent MRI and four transrectal ultrasound (TRUS) examination, while in 2011, 18 and 20, respectively, received MRI and TRUS. In 2006 four patients underwent incidental ERCa polypectomy, with all having a positive resection margin leading to anterior resection. In 2011 only one case with a positive margin following extended endoscopic mucosal resection was identified. Definitive

Introduction The outcome of patients with rectal cancer has improved through total mesorectal excision [1] and neoadjuvant and adjuvant therapy. Radical surgery, however, carries a significant risk of mortality, morbidity and poor function [2,3]. For early rectal cancer (ERCa), including lesions confined to the submucosa Correspondence to: Mr N. Borley, Department of Colorectal Surgery, Cheltenham General Hospital, Sandford Road, Cheltenham GL53 7AN, UK. E-mail: [email protected] Previous communications: Abstract presented at the Association of Coloproctology of GB & Ireland Annual Meeting July 2013 and British Society of Gastroenterology Annual Meeting, June 2013.

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local excision without subsequent resection occurred in two patients in 2006 and in 16 in 2011. Conclusion The study demonstrates an improvement in preoperative ERCa staging, a reduction in margin positivity and an increase in the use of local excision following the implementation of a specialist ERCa MDT. The increased detection of rectal neoplasms through screening and surveillance programmes requires further investigation and management. A specialist ERCa MDT will improve management and should be available to all practitioners involved with patients with ERCa. Keywords Adenocarcinoma/diagnosis, adenomatous polyps/surgery, rectal neoplasms/diagnosis, rectal neoplasms/surgery, microsurgery/methods What does this paper add to the literature? This is the first published study to analyse the impact of a specialist early rectal cancer multidisciplinary team (ERCa MDT) on the extent and suitability of investigation and management of ERCa. We report an improvement in preoperative staging and an increase in the use of local excision for ERCa coinciding with the introduction of the ERCa MDT.

without locoregional lymphovascular spread, local excision may offer similar survival without the associated morbidity and mortality. Transanal endoscopic microsurgery (TEMS) [4,5] is now widely used for large benign rectal neoplasms and ERCa, but risks an adverse outcome if the indications are not adhered to [6–8]. The first step is to distinguish malignant from benign lesions. Rectal lesions which cannot be excised completely by conventional endoscopic polypectomy or endoscopic mucosal resection (EMR) or which are either proven or suspicious of ERCa have been given the term ‘significant rectal neoplasms’ (SRNs) [9]. Significant rectal neoplasms are increasingly seen through the National Bowel Cancer Screening Pro-

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gramme, and diagnostic accuracy is clearly central to their management. Determining suitability for local excision is a multifactorial decision that must consider pathological factors of local and regional stage, comorbidity and the desires of the patient and local expertise [10]. Such an assessment is becoming increasingly complex and an ERCa and significant rectal neoplasm multidisciplinary team (MDT) was formed by the local cancer network to advise on potential ERCa, uncertain rectal neoplasms and ‘unexpected’ polyp cancers of the rectum. The hope was that this would increase the use of local excision and reduce the incidence of ‘unexpected’ ERCa and the use of radical surgery in patients who were otherwise appropriate for local excision. The present study aimed, therefore, to analyse the impact of the introduction of a specialist ERCa MDT on the extent and suitability of investigation and management of ERCa.

Method A retrospective comparative cohort study was performed of all patients with a final diagnosis of pT1 rectal cancer identified during two 12-month periods, 2006 and 2011, from the histopathological records in the hospital. Biopsy and resection histopathology reports were searched to ensure that all cases of ERCa, including patients undergoing polypectomy only, were identified. Referrals from other trusts were included in the cohort but patients with an incomplete dataset were excluded. Data relating to preoperative diagnostic and staging investigations including endoscopy, transrectal ultrasound (TRUS), MRI, and CT scan reports were collected. MDT reports and clinic letters were analysed and data on management, including radiotherapy, endoscopic and surgical procedures, were collected. Postoperative histology was compared with preoperative clinical and radiological staging where available. Data on the clinical outcomes were available but not analysed in the study. Demographics, preoperative staging and management were compared between the 2006 and 2011 cohorts. End-points

The end-points of interest included the presence of a recorded MDT discussion and the preoperative stage before first management, the incidence of ‘unexpected’ adenocarcinoma after polypectomy, the proportion of patients undergoing local excision as definitive treatment, the incidence of an R1 (positive) resection margin with local excision and the accuracy of preoperative staging.

Impact of a dedicated early rectal cancer MDT

Transanal endoscopic microsurgery

Transanal endoscopic microsurgery was carried out by two surgeons using the standard Richard Wolf Transanal Endoscopic Microsurgery Instrument System (Richard Wolf UK Ltd, Wimbledon, UK). For ERCa for which local excision was agreed as primary treatment, excision was full thickness with suturing as standard technique whilst for all other lesions mucosectomy or, where necessary because of previous scar tissue, partial thickness excision was used. The early rectal cancer multidisciplinary team

The ERCa MDT was developed as part of the regional cancer network in 2008 in response to the need to evaluate the ‘difficult rectal polyp’ or SRN and any proven ERCa considered for local excision [9]. It now takes referrals from what was the Three Counties Cancer Network (four colorectal MDTs) and up to 12 other MDTs from outside. Members include two consultant surgeons with an interest in SRN, ERCa and TEMS, two interventional colonoscopists (gastroenterologists), a specialist gastrointestinal pathologist, two radiologists specializing in rectal cancer imaging, a clinical oncologist, cancer nurse specialists and a trials nurse. In addition to conventional imaging, TRUS images and endoscopic stills were used to aid decisionmaking. Statistical analysis

Unless otherwise stated, results are presented as median (interquartile range, IQR). Data were stored in ExcelTM (Microsoft Inc., Seattle, Washington, USA). No comparative statistics were applied due to the small numbers of included cases. The audit was registered with both the local audit department and those of the relevant referring trusts.

Results In 2006, 20 patients with a final histology of pT1 rectal cancer were identified. One was excluded as all preoperative investigations and an endoscopic biopsy has been performed privately elsewhere and the results were unavailable. The 19 included patients had a median age of 65 (60–73) years, six were referred from outside. In 2011, 24 patients with a pT1 cancer were included of median age 67 (62–74) years. Fifteen patients were referral from outside the referral area of the unit. Demographics, management and pathological staging are given in Table 1.

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Impact of a dedicated early rectal cancer MDT

Table 1 Demographics, management and histology.

Sample size Age (interquartile range) (years) Male gender Initial management Polypectomy Biopsy Definitive management Local excision only Resection Declined surgery Staging on histopathology Kikuchi level recorded pT1 Sm1 pT1 Sm2 pT1 Sm3 Nodal status recorded pN0 pN1

2006

2011

19 65 (60–73)

24 67 (61.75–74.5)

14

11

4 15

4 20

3 15 1

20 4 0

4 1 1 2 10 7 3

21 6 3 12 9 8 1

Local excision as definitive treatment and local excision margin positivity

In 2006, eight patients underwent local excision, including one conventional per-anal excision and seven TEMS excisions (three full-thickness). Of these five had positive resection margins on histology and all but one patient (patient choice) preceded to anterior resection. Therefore, in 2006, 10 (53%) patients underwent primary resection without a prior attempt at local excision, of whom eight were for a T1 N0 cancer, while only two (11%) underwent definitive local excision. In 2011, 20 patients underwent local excision (all TEMS, 15 full thickness) with no positive margins. Four patients underwent subsequent resection following unfavourable histology (Kikuchi stage Sm3, n = 3) or patient choice (n = 1), while two patients declined radical surgery but received adjuvant radiotherapy. Therefore in 2011 only two (8%) patients underwent primary resection (of which one was for a T1 N0 cancer), while 16 (67%) underwent local excision as the definitive surgical treatment.

Discussion MDT discussion and staging

Records of MDT discussion were identified for 17 of the 19 patients in 2006. In 2011, following implementation of the specialist ERCa MDT, 22 of the 24 patients were discussed in this arena. The remaining two patients were discussed at the generic colorectal MDT on the neighbouring site within the trust. In 2011, more patients underwent appropriate preprocedure imaging than in 2006 (MRI 18 vs 12, TRUS 20 vs 4, CT 22 vs 15; Figs. 1 and 2). The rT and rN stage was more commonly reported on MRI in 2011 compared with 2006 (18 vs 9 and 13 vs 8) while Kickuchi or Haggit substaging was more commonly reported in histology reports in 2011 (21 vs 11). Incidental adenocarcinoma polypectomy

In 2006, four of the pT1 cases were identified following polypectomy. All were incomplete, with positive resection margins, and anterior resection was carried out in these four patients. In 2011 four pT1 cases were identified following polypectomy, of which three were documented as being an extended endoscopic mucosal resection (eEMR; i.e. a piecemeal EMR resulting in a multiply fragmented pathological specimen) with one positive resection margin. Two of these patients proceeded to full-thickness TEMS following complete preoperative staging.

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This study demonstrates an improvement in the preoperative investigation of ERCa and an appropriate decrease in the use of radical surgery following the implementation of a specialist ERCa MDT. The investigation and management of rectal cancer has changed considerably in the last two decades with the increasing use of neoadjuvant therapy for advanced cases and local excision of early cancers with a view to cure. The diagnosis of ERCa is set to increase with the National Bowel Cancer Screening Programme while the increasing age and comorbidity of the patient population may favour local excision over radical surgery. Several colorectal surgeons have developed a specialist interest in ERCa, undertaking TRUS and precise local excision using TEMS, while radiologists, oncologists and pathologists are becoming equally subspecialized in some centres. National Institute of Health and Care Excellence (NICE) guidelines now recommend that patients with Stage 1 rectal cancer are discussed within an ERCa MDT [11] and a number of such regional specialist MDTs now exists across the country. MDT discussion and preoperative staging investigations

A number of studies have demonstrated improvement in completeness (margin positivity), operative mortality, 5-year survival and patient satisfaction after the implementation of an ERCa MDT [12–15], yet this is the

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Impact of a dedicated early rectal cancer MDT

20 rectal lesions with final pathology pT1

Complete dataset unavailable n = 1 15 lesions biopsied 4 polypectomy

Investigations 12 MRI (63%), 4 TRUS (21%)

Declined surgery n = 1

8 local excision (1 per-anal, 7 TEMS)

10 straight to resection

+v e

m

gi

n

=

3

M

1S

pT

ar

4

= 1

3 local excision only

Figure 1 Investigation and management of early rectal cancer in 2006 (TRUS, transrectal ultrasound; TEMS, transanal endoscopic microsurgery, MRI, magnetic resonance imaging).

15 underwent resection

19 cases pT1 rectal cancer Abbreviations: MRI Magnetic Resonance lmaging, TRUS Trans-rectal ultrasound, TEMS Trans-anal Endoscopic Microsurgery

first published study to consider staging investigations before and after its implementation. A study reporting the UK TEM database (to which our unit submits cases) revealed, however, a TRUS rate of only 33% in patients undergoing TEMS over the period 1992–2008 [16]. In our study there was a substantial increase in the use of TRUS in ERCa between 2006 and 2011, and in particular before local excision by TEMS, demonstrating a high rate of use during the latter part of the period, which is likely to reflect a national increase in the use of TRUS. Unexpected malignant invasion after polypectomy

The present study reports eight cases of unexpected malignancy, with no significant change in such occurrences between the 2006 and 2011 cohorts, but EMR

was more commonly used in the later cohort with complete excision more commonly achieved. Despite the technical advance in the methods of removing polyps, such cases should arguably have undergone a discussion in the ERCa MDT rather than going directly to a ‘trial EMR or polypectomy’ as this may not provide a complete specimen, possibly limiting and complicating future management options. The need to be selective when referring uncertain rectal polyps (SRNs) to the ERCa MDT is obvious to limit the workload for the MDT and diagnostic services. Under these circumstances, a small incidence of truly unexpected malignancy may be inevitable, but experience from the National Bowel Cancer Screening Programme indicates that by using the criteria of size and sessile morphology as risk factors for malignancy this can be minimized, as shown in the present study.

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24 rectal lesions with final pathology pT1

20 lesions biopsied 4 polypectomy

20 lesions biopsied

4 polyps removed by eEMR 1 polyp with +ve margin 3 polyps fully excised

Investigations 3 had MRI (post-EMR), 3 TRUS

No further treatment n = 2

Investigations 15 had MRI, 17 TRUS

R0 TEMS n=2

Resection n=2

TEMS n = 18 1 ice 3 = cho SM tient Pa =1

20 local excision only

4 underwent resection

24 cases pT1 rectal cancer Abbreviations: MRI Magnetic Resonance lmaging, TRUS Trans-rectal ultrasound, TEMS Trans-anal Endoscopic Microsurgery

Local excision as definitive treatment and diminishing margin positivity

The present study demonstrates an increase in 2011 in the definitive use of local excision accompanied by a reduction in the rate of margin positivity, which implies that case selection and referral to a specialist ERCa MDT improves the technical outcome. The results support the role of the specialist ERCa MDT in selecting the appropriate investigations and allowing all management options to be considered. In demonstrating the effectiveness of the ERCa MDT on the investigation and management of ERCa, we nevertheless acknowledge that the numbers of

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Figure 2 Investigation and management of early rectal cancer in 2011 (TRUS, transrectal ultrasound; TEMS, transanal endoscopic microsurgery; EMR, endoscopic mucosal resection; eEMR, extended EMR; MRI, magnetic resonance imaging).

patients are too small to permit the use of statistical comparison. Despite this there is every indication that the results demonstrate improvement in preoperative staging with more refined case selection for local excision over radical surgery. It is also the case that the differences observed between the two periods cannot be solely a direct result of the ERCa MDT – they are likely to be partly due to other factors including increasing acceptance of local excision for ERCa and improved surgical technique to reduce margin positivity. A specialist ERCa MDT ensures that all relevant surgical techniques, including local excision, are discussed and considered while careful case selection ensures optimal surgical and oncological results.

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The present study demonstrates an improvement in the accuracy of preoperative staging of ERCa, a reduction in margin positivity after local excision and an increase in the use of local excision following the implementation of a specialist ERCa MDT. The increased detection of significant rectal neoplasms by screening and surveillance necessitates a robust and consistent pathway for the investigation, discussion and management of such tumours. A specialist ERCa MDT should be available to all colorectal surgeons and physicians.

Acknowledgement The authors would like to thank Lisa Richardson for her administrative assistance in undertaking this study.

Funding None.

Author contributions PGV-S: Study conception and design, analysis and interpretation of data, writing manuscript. JMDW: Writing manuscript. NRB: Study conception and design, acquisition of data, writing manuscript.

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The impact of a dedicated multidisciplinary team on the management of early rectal cancer.

Local excision of early rectal cancer (ERCa) offers comparable survival and reduced operative morbidity compared with radical surgery, yet it risks an...
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