Originally published as JCO Early Release 10.1200/JCO.2007.14.5961 on June 9 2008

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by West, N. P. Articles by Quirke, P. Search for Related Content PubMed PubMed Citation Articles by West, N. P. Articles by Quirke, P. Related Articles Related Editorial Social Bookmarking                            What's this?

Evidence of the Oncologic Superiority of Cylindrical Abdominoperineal Excision for Low Rectal Cancer

Nicholas P. West, Paul J. Finan, Claes Anderin, Johan Lindholm, Torbjorn Holm, Philip Quirke

From Pathology and Tumour Biology, Leeds Institute of Molecular Medicine, University of Leeds; and Department of Colorectal Surgery, Leeds General Infirmary, Leeds, United Kingdom; and Department of Coloproctology; and Department of Pathology, Karolinska University Hospital, Stockholm, Sweden

Corresponding author: Phillip Quirke, PhD FRCPath, Gastrointestinal Cancer Research Group, Pathology and Tumour Biology, Yorkshire Cancer Research and Liz Dawn Translational Science Centre, Leeds Institute of Molecular Medicine, Wellcome Trust Brenner Building, Level 4, Room 4.20a, St James's University Hospital, Beckett St Leeds, LS9 7TF, United Kingdom; e-mail: patpq{at}leeds.ac.uk

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Purpose Abdominoperineal excision (APE) of the rectum and anus for rectal cancer continues to have greater local recurrence and poorer survival than that seen following anterior resection. Changing to an extended prone perineal dissection results in a more cylindrical specimen and should improve outcomes.

Patients and Methods One hundred twenty-eight specimens from patients who underwent APE that was performed for potentially curable primary rectal adenocarcinoma were dissected according to standard protocol in Leeds and Stockholm between 1997 and 2007 and were studied. Tissue morphometry was performed on the cross sectional photographs of 93 patient cases.

Results The cylindrical technique removed more tissue in the distal rectum and in all slices that contained tumor compared with the standard operation (both P < .0001). Greater distance was observed from the muscularis propria or internal sphincter to the anterior, posterior, and lateral resection margins (all P < .0001). This was associated with lower circumferential resection margin (CRM) involvement (14.8% v 40.6%; P = .013) and intraoperative perforations (3.7% v 22.8%; P = .0255). An increase in the amount of tissue removed in the distal rectum (P < .0001) was demonstrated by a single surgeon who changed from the standard to the cylindrical technique during the study period; the change was associated with a reduction in CRM positivity (from 36.2% to 12.5%) and in perforations (from 12.8% to 0.0%).

Conclusion Cylindrical APE performed in the prone position for low rectal cancer removes more tissue around the tumor that leads to a reduction in CRM involvement and intraoperative perforations, which should reduce local disease recurrence. The cylindrical technique has the potential to improve patient outcomes substantially if appropriate surgical education programs are developed.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Despite the introduction of total mesorectal excision (TME) for the surgical treatment of rectal cancer, local recurrence and survival after abdominoperineal excision (APE) of the rectum and anus have not improved to the same degree as that seen with anterior resection (AR).^1,2 The difference in outcome may be explained by a combination of the anatomic and surgical difficulties associated with standard APE surgery. In the lower rectum, the mesorectum reduces in size and disappears at the top of the sphincters. Below this level, the sphincter muscle forms the circumferential resection margin (CRM). Tumors of the distal rectum, therefore, will have less distance to traverse to reach the CRM than higher tumors, in which the CRM is protected by a thicker mesorectum. We have demonstrated previously a significant reduction in tissue volume around the tumor in APEs compared with ARs by using tissue morphometry.¹ This was associated with greater CRM positivity (41% v 12%), greater local recurrence (23.8% v 13.5%) and poorer 5-year cancer-specific survival (52.3% v 65.8%). Other groups from Norway and Holland have reported similar findings.^2,3 A further complicating factor is the technical difficulty associated with operating deep in the pelvis via an abdominal approach. This is reflected by a greater intraoperative perforation rate in APEs compared with ARs, which is well recognized to increase the chances of local recurrence and death.²

Recently, surgeons in Stockholm have described a more radical approach to APE surgery,⁴ which closely mirrors the original Miles operation.⁵ The procedure involves careful mobilization of the mesorectum only as far down as the origins of the levator muscle. After stoma formation, the abdomen is closed, the patient is rotated into the prone position, and an extended perineal dissection is performed. This includes the sphincter complex and follows the inferior surface of the levators to a point laterally where they originate on the pelvic sidewall. This point should be just inferior to the level where the abdominal procedure was terminated. The coccyx is often removed in continuity with the main specimen to improve direct visualization of the dissection. In the case of anterior tumors, in which the CRM is frequently threatened, a portion of prostate or vaginal wall may be removed also. If the resulting pelvic floor defect is too large for primary closure, a gluteus maximus flap reconstruction or insertion of a prosthetic mesh may be performed. This modified procedure has two distinct advantages. First, because the levator muscles are removed in continuity with the anal canal and mesorectum en bloc, a more cylindrical specimen is created, which should increase the amount of tissue removed around the tumor and, therefore, reduce CRM positivity. Second it enables better visualization for the traditionally difficult perineal dissection, which should reduce the chances of entering the wrong surgical plane and perforating the specimen. Early reports suggest that the cylindrical method of excision can improve patient prognosis without a significant increase in morbidity.⁴

After the recent calls for a change in approach to APE surgery,^1,2,6 we devised a retrospective study to review a series of cylindrical and standard APE specimens that were resected in Leeds and Stockholm over the last 10 years. One of the authors (P.J.F.) is a specialist colorectal cancer surgeon from Leeds who underwent training in the cylindrical technique during the study period and who has performed this procedure since December 2005. We aimed to evaluate the advantages of the cylindrical compared with the standard method and to assess the significance of a change in surgical approach to a single surgeon's practice. In addition to clinical and pathologic data, we aimed to use precise tissue morphometry to accurately determine the amount of tissue removed around the tumor with both surgical techniques.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Leeds Patient Cases
All APEs performed between January 1, 1997 and June 30, 2007, at the Leeds General Infirmary were identified by a search of the Northern and Yorkshire Cancer Registry Information Service database and the pathology archives. A total of 148 patient cases were identified initially before the following were excluded: 13 patients with squamous cell carcinomas, eight with unresectable disease at operation, seven with distant metastases, four with previous attempts at removal in other hospitals, four with recurrent rectal cancers, two with benign lesions, and one with pelvic exenteration. One hundred nine patient cases of potentially curable primary adenocarcinoma, therefore, were entered into the study, which included 99 standard and 10 cylindrical operations. One author (P.J.F.) performed 47 of the standard and eight of the cylindrical procedures.

Karolinska Patient Cases
The photographic images of 19 APEs for potentially curable primary rectal adenocarcinoma that were performed between 2001 and 2006 were obtained from the Karolinska University Hospital in Stockholm. They included two standard and 17 cylindrical operations.

Clinical and Pathologic Data
Details of CRM involvement and surgical perforation rates were obtained from a combination of the surgical notes, pathology reports, and specimen photographs. Any tumor located less than 1 mm from the CRM was considered to represent margin involvement, according to previous evidence.⁷ Any visible defect into the rectal lumen noted at specimen cut-up was classified as an intraoperative perforation. This included three patient cases in which initial attempts at AR had cut through the tumor before completion of proctectomy.

Tissue Morphometry
All APE specimens underwent routine pathologic processing, which included fixation in 10% formalin, painting of the CRM, and serial slicing from the distal margin at 3 to 5 mm intervals, as described previously.⁸ Digital photographic images of the whole specimen and of serial cross sectional slices alongside a metric scale were taken and were stored on the i-Base digital database (Department of Histopathology, Leeds General Infirmary, Leeds, United Kingdom) or at the Karolinska University Hospital. The following patient cases were excluded from morphometric analysis: 14 that did not show all the slices from the distal margin of the specimen, eight with poor quality photographs, six with no photographs, three with no cross sectional slices, two with no metric scale, and two in which the specimen had been opened before slicing. Ninety-three patient cases, which included 27 cylindrical and 66 standard operations, had at least one adequate photographic image of the cross sectional slices. Precise tissue quantitation was performed with the QWin image analyzer (Leica Microsystems, Wetzlar, Germany) on the distal 12 slices of the specimen by using a method described previously.¹ The cross sectional area of the tissue outside the internal sphincter or muscularis propria (IS/MP), depending on the level of the slice, was obtained, as were measurements from the IS/MP to the anterior, posterior, and lateral painted resection margins. The position of the IS/MP was estimated for those slices in which the tumor caused significant anatomic distortion.

Statistical Analyses
Statistical analyses were performed by using either a two-tailed t test for unpaired samples (continuous variables) or a two-tailed Fisher's exact test (categoric variables), and a significance level was set as less than .05.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Clinical and Pathologic Data
Clinical and pathologic characteristics of the patient population are presented in Table 1. Microscopic CRM involvement by tumor cells was demonstrated in 35.2% of patient cases, and the intraoperative perforation rate was 18.8%. In Leeds, there was considerable variation in CRM positivity and perforation rates among the higher volume surgeons when using the standard operation technique. CRM positivity varied from 27.3% to 55.6%, and perforation rates from 10.0% to 36.4%, among those surgeons who had performed at least 10 APEs during the study period. Specimens that had an intraoperative perforation had a significantly greater rate of CRM involvement compared with those that were intact (70.8% v 26.9%; P < .0001). Of the perforated specimens, 81.8% showed an anterior defect, and the remainder were located at the left lateral aspect; 82.6% of all the perforations were at the level of the tumor. CRM positivity and surgical perforation rates both strongly correlated with the depth of tumor invasion.

View larger version (10K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Differential circumferential resection margin positivity (P = .013) and intraoperative surgical perforation (P = .0255) rates according to the method of abdominoperineal excision used.

View larger version (26K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Mean cross sectional tissue area outside the internal sphincter or muscularis propria in the distal 12 slices of the specimen according to operation type, with 95% confidence intervals, (A) by slice number from the distal aspect of the specimen. (B) Overall means, including all slices that contained macroscopically evident tumor (both P < .0001).

View larger version (13K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 3. Mean distance per slice from the internal sphincter or muscularis propria to the anterior, posterior and lateral painted circumferential resection margins according to operation type for the distal 12 slices of the specimen (all P < .0001), with 95% confidence intervals.

View larger version (29K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 4. Mean cross sectional tissue area outside the internal sphincter or muscularis propria in the distal 12 slices according to institution and operation type, with 95% confidence intervals. Leeds patient cases include only those performed by P.J.F. (A) by slice number from the distal aspect of the specimen. (B) Overall means, including all slices that contained macroscopic tumor.

There was a 10% difference in CRM involvement between males and females (37.3% v 47.1%) in specimens removed via the standard technique, although this difference was not statistically significant. Specimens from males that were excised with the cylindrical method had approximately 25% more tissue removed outside the IS/MP in the distal rectum compared with those from females (P < .0001), but this did not result in a significantly lower CRM positivity or perforation rate. The increased tissue was demonstrated at both the anterior and posterior aspects, which each had approximately 4 mm extra tissue (P < .0001 and P = .02, respectively).

Overall, 73.4% of patients received preoperative treatment that included radiotherapy in 46.1% and combination chemoradiotherapy in 27.3%. Patients who had been treated showed a significantly lower rate of CRM positivity (27.7% v 55.9%; P = .0058). Patients who received radiotherapy alone showed the lowest rate of CRM involvement (22.0% v 55.9%; P = .0014) despite approximately half of the patients having only 5 x 5 short-course radiotherapy. Preoperative therapy appeared to have no effect on the rate of intraoperative perforation.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
We and others^1-3 have shown previously that, when using the standard APE operation, there is a major problem caused by a higher rate of CRM involvement, tumor perforation, and local recurrence, which leads to an approximately 10% reduction in survival compared with that seen after AR. We have shown that less tissue is removed around the tumor with an APE compared with an AR,¹ and, in the Dutch TME trial, we reported that the surgical plane achieved was wholly inadequate. In one third of patient cases, the plane was in the lumen, submucosa, or sphincter; in two thirds, it was on the sphincter surface.² Holm et al⁴ recently reported the experience of a new cylindrical technique that led to a large reduction in CRM involvement and perforation. Surgeons at the Hospital Saint-Antoine in Paris reported their results for APE surgery in 2003 that showed low, 10%, local recurrence rates, an overall survival of 67%, and an overall survival in curative cases of 76%.¹⁰ They also used a cylindrical technique (E. Tiret, personal communication, August 2007; Fig 5). In this article, we demonstrated that the reported superiority of the Holm cylindrical APE is caused by the removal of more tissue around the tumor compared with standard APEs. We have shown further that the intervention of a change in surgical technique by a single surgeon increases the amount of tissue removed, reduces CRM involvement, and lowers intraoperative perforation rates.

View larger version (57K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 5. Anterior and posterior surfaces of specimens from abdominoperineal excisions with serial cross sectional slices. (A) Standard specimen with surgical waist. (B-D) Cylindrical specimens from Karolinska (T.H.), Paris (E.T.) and Leeds (P.J.F.). (E-F) Cross sectional slices of standard and cylindrical specimens.

We were able to demonstrate significant variability in the rates of CRM involvement, intraoperative perforations, and the amount of tissue removed in the distal rectum among surgeons who performed standard APE operations in Leeds. During the study, one surgeon (P.J.F.) was trained in the cylindrical technique by watching a video of the procedure and by personally discussing the operation with one of the expert cylindrical surgeons from the Karolinska (T.H.). This enabled us to demonstrate at the individual surgeon level that a switch to the cylindrical method resulted in more tissue being removed in the distal rectum and around the tumor, which led to a drop in CRM positivity and perforations. The Leeds cylindrical APE removed slightly less tissue than the Karolinska procedure, which may reflect a higher rate of coccygeal amputation in Stockholm, a lesser degree of experience in Leeds, or the need for more intensive education.

Tumor perforation must be avoided, as it has been shown in many series to increase local recurrence and to reduce survival.^2,11 We have shown that approximately 71% of perforated specimens demonstrate microscopic CRM involvement, which partly explains why these patients fare so badly. As noted in the Dutch TME study,² the majority of perforations occurred through the tumor, but—in contrast to their findings—more than 80% occurred at the anterior, not the posterior, aspect. The Dutch trial reported that the frequency of CRM positivity was greater in anteriorly placed tumors than in those in other locations (P < .001).¹² Our morphometry data supports the theory that the anterior aspect of the specimen is the one most likely to be perforated or to be involved by tumor, as the mean distance to this margin is much less than to the posterior or lateral aspects. The cylindrical technique appears to go some way towards rectifying this by almost doubling the amount of tissue present anteriorly beyond the IS/MP.

Approximately two thirds of APEs were performed on male patients, which is similar to earlier studies.¹² The Dutch TME trial reported a significantly higher rate of CRM involvement in females compared with males (39.5% v 24.3%).² In this study, we were able to demonstrate a 10% greater CRM positivity rate in specimens from female patients that were removed by the standard method, but this difference was not statistically significant. Our morphometry data suggest that, with cylindrical surgery, males have approximately 25% more tissue outside the IS/MP in the distal rectum. Previous studies performed in Leeds have demonstrated that male patients have a statistically larger area of overall mesorectal package and of mesorectal fat and a higher ratio of transverse to anteroposterior diameters of the mesorectal package compared with females.¹³ Another contributory factor may be anatomic differences in the female bony pelvis. It has been shown previously that a shorter interspinous distance in the female pelvis leads to greater CRM positivity by increasing the technical difficulty of excision,¹⁴ although other groups have reported a smaller interspinous distance in males.¹⁵

The cylindrical technique has been used routinely at the Karolinska since 2000, mainly for locally advanced rectal cancer. An audit of results showed a reduction in intraoperative perforations and CRM involvement, so the cylindrical method is now standard for all low-lying rectal tumors that require an APE. Postoperative morbidity and mortality are not increased, and the experience so far shows no adverse effects from the prone jackknife position. The risks of intraoperative complications during the perineal phase probably are reduced because of the improved visualization of the operative field. As the risk of perforations and involved margins are reduced, the local recurrence rate appears to be lower than that seen with the standard APE operation. At Karolinska, neoadjuvant radiotherapy or radiochemotherapy has been standard treatment for all patients with low rectal cancer who require an APE. In combination with the cylindrical operation, the local recurrence rate was 6% in patients who were operated on until 2005, as measured with a minimal follow-up of 22 months.

We have demonstrated that adoption of the cylindrical technique can lead to an immediate improvement in CRM positivity and perforation rates for an individual surgeon. It is likely that further improvements will occur as there is more experience with the modified perineal phase; however, to obtain the full benefit of this operation immediately, it may be necessary for surgeons to undergo a formal educational program. It is hoped that the results of this study will encourage all specialist rectal cancer surgeons to undergo training in the cylindrical technique to improve patient survival for low rectal cancer, as with that seen for AR for tumors of the upper and middle rectum. The use of this operation in combination with newer preoperative neoadjuvant therapies should further improve results without the risk of increased perforation rates.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
The authors indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Conception and design: Nicholas P. West, Paul J. Finan, Torbjorn Holm, Philip Quirke

Financial support: Philip Quirke

Administrative support: Nicholas P. West, Philip Quirke

Provision of study materials or patients: Nicholas P. West, Paul J. Finan, Claes Anderin, Johan Lindholm, Torbjorn Holm

Collection and assembly of data: Nicholas P. West, Paul J. Finan, Claes Anderin, Johan Lindholm, Torbjorn Holm

Data analysis and interpretation: Nicholas P. West, Paul J. Finan, Torbjorn Holm, Philip Quirke

Manuscript writing: Nicholas P. West, Paul J. Finan, Torbjorn Holm, Philip Quirke

Final approval of manuscript: Nicholas P. West, Paul J. Finan, Claes Anderin, Johan Lindholm, Torbjorn Holm, Philip Quirke

	NOTES

 
published online ahead of print at www.jco.org on June 9, 2008.

N.W. is supported by the United Kingdom Department of Health Academic Clinical Fellowship program, and P.Q. is supported by grants from Yorkshire Cancer Research and the Experimental Cancer Medicine Centre Initiative.

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
1. Marr R, Birbeck K, Garvican J, et al: The modern abdominoperineal excision: The next challenge after total mesorectal excision. Ann Surg 242:74-82, 2005[CrossRef][Medline]

2. Nagtegaal ID, Van de Velde CJH, Marijnen CAM, et al: Low rectal cancer: A call for a change of approach in abdominoperineal resection. J Clin Oncol 23:9257-9264, 2005[Abstract/Free Full Text]

3. Wibe A, Syse A, Anderson E, et al: Oncological outcomes after total Mesorectal excision for cure for cancer of the lower rectum: Anterior vs. abdominoperineal resection. Dis Colon Rectum 47:48-58, 2004[CrossRef][Medline]

4. Holm T, Ljung A, Haggmark T, et al: Extended abdominoperineal resection with gluteus maximus flap reconstruction of the pelvic floor for rectal cancer. Br J Surg 94:232-238, 2007[CrossRef][Medline]

5. Miles WE: A method of performing abdomino-perineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon. Lancet 2:1812-1813, 1908

6. Salerno G, Daniels IR, Brown G: Magnetic resonance imaging of the low rectum: Defining the radiological anatomy. Colorectal Dis 8:10-13, 2006 (suppl 3)

7. Adam IJ, Mohamdee MO, Martin IG, et al: Role of the circumferential margin involvement in the local recurrence of rectal cancer. Lancet 344:707-711, 1994[CrossRef][Medline]

8. Quirke P, Dixon MF: The prediction of local recurrence in rectal adenocarcinoma by histopathological examination. Int J Colorectal Dis 3:127-131, 1988[CrossRef][Medline]

9. Sobin LH, Wittekind CH (eds): TNM Classification of Malignant Tumours (ed 5). New York, NY, Wiley-Liss, 1997, pp 66-69

10. Dehni N, McFadden N, McNamara DA, et al: Oncologic results following abdominoperineal resection for adenocarcinoma of the low rectum. Dis Colon Rectum 46:867-874, 2003[CrossRef][Medline]

11. Eriksen MT, Wibe A, Syse A, et al: Inadvertent perforation during rectal cancer resection in Norway. Br J Surg 91:210-216, 2004[CrossRef][Medline]

12. den Dulk M, Marijnen AM, Putter H, et al: Risk factors for adverse outcome in patients with rectal cancer treated with an abdominoperineal resection in the total mesorectal excision trial. Ann Surg 246:83-90, 2007[CrossRef][Medline]

13. Boyle KM, Chalmers AG, Finan PJ, et al: The relationship between mesorectal morphology and gender in patients with primary rectal cancer. Colorectal Dis 7:23s, 2005 (suppl; abstr 068)

14. Boyle KM, Petty D, Chalmers AG, et al: MRI assessment of the bony pelvis may help predict respectability of rectal cancer. Colorectal Dis 7:232-240, 2005[CrossRef][Medline]

15. Salerno G, Daniels IR, Brown G, et al: Magnetic resonance imaging pelvimetry in 186 patients with rectal cancer confirms and overlap in pelvic size between males and females. Colorectal Dis 8:772-776, 2006[CrossRef][Medline]

Submitted September 26, 2007; accepted November 27, 2007.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

Related Editorial

• Extended Perineal Resection of Distal Rectal Cancers: Surgical Advance, Increased Utilization of Neoadjuvant Therapies, Proper Patient Selection or All of the Above?
  José G. Guillem and Bruce D. Minsky
  JCO 2008 26: 3481-3482 [Full Text]

This article has been cited by other articles:

				E Morris, P Quirke, J D Thomas, L Fairley, B Cottier, and D Forman Authors' response Gut, April 1, 2009; 58(4): 609 - 610. [Full Text] [PDF]

				C R Selvasekar, G David, D J Corless, A U Khan, and J P Slavin Rectal cancer surgery: is restoration of intestinal continuity the primary aim? Gut, February 1, 2009; 58(2): 311 - 311. [Full Text] [PDF]

				E Morris, P Quirke, J Thomas, L Fairley, B Cottier, and D Forman Authors' response Gut, January 1, 2009; 58(1): 150 - 152. [Full Text] [PDF]

				J. G. Guillem and B. D. Minsky Extended Perineal Resection of Distal Rectal Cancers: Surgical Advance, Increased Utilization of Neoadjuvant Therapies, Proper Patient Selection or All of the Above? J. Clin. Oncol., July 20, 2008; 26(21): 3481 - 3482. [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by West, N. P. Articles by Quirke, P. Search for Related Content PubMed PubMed Citation Articles by West, N. P. Articles by Quirke, P. Related Articles Related Editorial Social Bookmarking                            What's this?