Diseases of the Colon & Rectum:
Original Contributions: Colorectal/Anal Neoplasia
Multicenter Study of Outcome in Relation to the Type of Resection in Rectal Cancer
Ortiz, Hector M.D., Ph.D.1; Wibe, Arne M.D., Ph.D.2,3; Ciga, Miguel Angel M.D.4; Kreisler, Esther M.D., Ph.D.5; Garcia-Granero, Eduardo M.D., Ph.D.6; Roig, Jose Vicente M.D., Ph.D.7; Biondo, Sebastiano M.D., Ph.D.5; on behalf of the Spanish Rectal Cancer Project
1Department of Surgery, Public University of Navarra, Pamplona, Spain
2Department of Surgery, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway
3Department of Cancer Research and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway
4Department of Surgery, Complejo Hospitalario de Navarra, Pamplona, Spain
5Department of General and Digestive Surgery, Colorectal Unit, Bellvitge University Hospital, University of Barcelona, Barcelona, Spain
6Department of Surgery, Colorectal Unit, Hospital la Fe, Universidad de Valencia, Valencia, Spain
7Department of Surgery, Hospital General Universitario, Valencia, Spain
Funding/Support: This work was support by grants from the Ministry of Health, Social Services and Equality of Spain (FIS number PI11/00010) and the health authorities of the government of Navarra, Spain (20/11).
Financial Disclosure: None reported.
Correspondence: Sebastiano Biondo, M.D., Ph.D., Bellvitge University Hospital, Department of General and Digestive Surgery, c/o Feixa Llarga s/n, L’Hospitalet de Llobregat, 08907 Barcelona, Spain. E-mail: email@example.com
BACKGROUND: A surgical teaching and auditing program has been implemented to improve the results of treatment for patients with rectal cancer.
OBJECTIVE: The aim of this study was to assess the treatment and outcome in patients resected for rectal cancer, focusing on differences relating to the type of resection.
DESIGN: This was an observational study.
SETTINGS: The study took place throughout the network of hospitals that compose the National Health Service in Spain.
PATIENTS: This study included a consecutive cohort of 3355 patients from the Spanish Rectal Cancer Project. The data of patients who were operated on electively, with curative intent, by anterior resection (n = 2333 [69.5%]), abdominoperineal excision (n = 774 [23.1%]), and Hartmann procedure (n = 248 [7.4%]) between March 2006 and May 2010 were analyzed.
MAIN OUTCOME MEASURES: Clinical, pathologic, and outcome results were analyzed in relation to the type of surgery performed.
RESULTS: After a median follow-up time of 37 months (interquartile range, 30–48 months), bowel perforations were found to be more common in the Hartmann procedure (12.6%) and abdominoperineal groups (10.1%) than in the anterior resection group (2.3%; p < 0.001). Involvement of the circumferential resection margin was also more common in the Hartmann (16.6%) and abdominoperineal groups (14.3%) than in the anterior resection group (6.6%; p < 0.001). Multivariate analysis showed a negative influence on local recurrence, metastasis, survival for advanced stage, intraoperative perforation, invaded circumferential margin, and Hartmann procedure. However, abdominoperineal excision did not significantly influence local recurrence (HR, 0.945; 95% CI, 0.571–1.563; p = 0.825).
LIMITATIONS: The main weakness of this study was the voluntary nature of registration in the Spanish Rectal Cancer Project.
CONCLUSIONS: Although bowel perforation and involvement of the circumferential resection margin were more common after abdominoperineal excision than after anterior resection, this study did not identify abdominoperineal excision as a determinant of local recurrence in the context of 3 years of median follow-up.
The types of bowel resection in rectal cancer include anterior resection (AR), abdominoperineal excision (APE), and Hartmann procedure. Although sphincter-sparing techniques are currently the most common operations, there are still patients in whom a restorative operation is not an option because of a bulky, tethered, locally advanced or very low tumor or in whom function is likely to be poor if a restorative operation is performed.
Although surgical procedures are not directly comparable, some studies have shown inferior outcomes after APE.1–6 However, others either do not report differences between operations7–9 or showed no differences in the rates of local recurrence (LR) between both procedures.10
Differences in outcome can have a multifactor interpretation, including patient and tumor characteristics,11 as well as surgical technique,12 especially if the APE is performed as a synchronous combined procedure.13 Therefore, it is still not clear whether APE, per se, has a worse outcome than AR.
The aim of this observational study was to report the results of a national audit program on rectal cancer surgery that analyzed the outcomes of the operations performed and focused on differences between AR and APE. Moreover, an assessment of whether the type of surgery could be a prognostic factor in outcome was studied.
This study is part of the Spanish Rectal Cancer Project, the objective of which was to improve rectal cancer treatment at a national level in the National Health Service. This initiative, which started in 2006, aimed to introduce total mesorectal excision (TME) surgery to multidisciplinary teams of surgeons, pathologists, and radiologists to establish a network of hospitals in the National Health Service in Spain. There are 47 million inhabitants covered by the Spanish National Health Service. It includes 247 public hospitals, 88 of which participate in the Spanish Rectal Cancer Project, accounting for a population of 19,329,992 inhabitants. Requisites for a hospital to be accepted into the project include serving a population area of 150,000 to 800,000 inhabitants and operating on more than 20 patients per year for rectal cancer. Surgeons in our participating hospitals have full-time dedication to coloproctology in elective surgery; however, emergency surgery can be performed by general or colorectal surgeons.
The majority of patients are managed by the public network for rectal cancer and are mandatorily referred to the local hospital. Therefore, within the geographic area and centers participating in the study, there is no selection of patients.
Imitating the Norwegian Colon and Rectal Cancer Project, the effectiveness of the training program was measured by a central registry with feedback to participating institutions of their own results compared with the national average. A more detailed description has been published previously.14
The entire present cohort consists of 3994 patients who had a TME rectal cancer resection between March 2006 and May 2010 by the first 51 hospitals with surgeons who were taught by Prof Arne Wibe during 2006 to 2009. Surgery was considered curative in 3355 patients and defined as a local radical procedure (R0 and R1) with negative or with microscopic invasion margins in the absence of distant metastases. Follow-up was continued until May 1, 2013.
All patients had a tumor located between 0 and 15 cm from the anal verge and were undergoing AR, APE, or a Hartmann procedure. APE was not performed as a synchronous combined procedure. At APE operation, the TME plane was dissected to the prostate or below the cervix. The perineal approach was used for wide excision of the anus and distal rectum. If there was evidence of macroscopic tumor spread outside the plane of dissection, a wider excision was performed locally.
Although a Hartmann procedure was indicated based on clinical features that were different from AR and APE (eg, older patients, comorbidity, or impairment of defecation function), patients undergoing this operation were included to represent the entire cohort of patients who underwent elective surgery. Moreover, some surgeons working on this project believe that the postoperative course is easier after a Hartmann procedure than after abdominoperineal resection and Hartmann is preferred if oncologic resection of the sphincters is not necessary and bowel continuity is not to be restored because of impairment of defecation function or severe concomitant disease.
LR, metastasis, and overall survival (OS) were the main outcome measures. LR rates were analyzed both in the entire cohort (including patients with R2 resection) and in the group of patients who underwent curative operations. Incidences of metastasis and survival were studied only in the curative surgery cohort. Because of the small number and to avoid bias, patients who were operated on in an emergency setting were excluded from the multivariate analysis.
Decisions on whether to use neoadjuvant treatment (long-cycle chemoradiotherapy) were made on an individual basis according to recommendations issued by the Spanish Clinical Cancer Guidelines.15 Preoperative chemotherapy and radiotherapy were considered the treatments of choice for stage II and stage III rectal cancer. Contraindications for preoperative radiotherapy were advanced age, symptomatic ischemic cardiovascular disease, and previous radiotherapy to the pelvis.
According to the national guidelines,15 patients were followed every 3 months for the first 2 years and then every 6 months until 5 years after surgery. However, the individual follow-up planning was left to the discretion of surgeons at the participating hospital. General blood tests, CEA, abdominal CT, and chest CT were performed. If LR was suspected, its diagnosis was confirmed by pelvic MRI and positron emission tomography-CT.
After any hospital consultation, a specific follow-up registration form including data on LR, metastases, second tumors, and death/survival was completed. Follow-up information was reported yearly to the central database by the surgeon responsible for rectal cancer registration at each hospital.
Intraoperative bowel perforation (IOP) was defined as any surgical defect from the rectal lumen to the surface. Tumor perforation to another organ and intraoperative perforation were included. Circumferential resection margin was considered invaded if cancer cells were found ≤1 mm from the margin.
LR was defined as recurrent disease in the pelvis, including recurrence at the site of the anastomosis and in the perineal wound. Isolated recurrence in the ovaries was recorded as distant metastasis. All LR rates were given as the sum of LR occurring in isolation and concomitant with distant metastases. The Spanish Death Registry provided information on time of death. Consequently, survival data are given as OS.
Stage classification for pathologic specimen followed the TNM classification from the American Joint Committee on Cancer (stages I–IV; 5th edition). A circumferential resection margin was considered invaded if cancer cells were found ≤1 mm from the margin.
The ethical committees of all involved centers approved this project. Informed consent was obtained from all patients included in the study. No patient refused the collection of his or her data.
Continuous variables are presented as mean (SD) or median interquartile range (quartile 1 to quartile 3). Categorical variables are presented as absolute numbers and percentages. A χ2 test or ANOVA test was used for intergroup comparisons.
Results regarding LR, distant metastasis, and mortality were presented as total number of events (patients were considered to be at risk of the studied event until death, emigration, or end of follow-up). Crude cumulative incidence rates were estimated by the Kaplan-Meier method. After assessing proportionality and linearity of the HRs, event-specific HR modeling was performed using a Cox proportional-hazards regression model.
Potential confounding factors such as age, sex, tumor level, tumor stage, neoadjuvant treatment, surgical procedures, intraoperative bowel perforation, invasion of the circumferential resection margin (CRM), presence of residual tumor, laparoscopic approach, hospital categories (general or academic), and elective or emergency surgery were included in the models. HR was given with 95% CI. All of the significant variables were included in the final analyses. Confounding variables with a marginal association (p < 0.15) were included in the model and removed when they failed to significantly change the likelihood of the model, as well as the estimates of the remaining variables in the model. If one variable was significant in the analysis of LR but not survival rate and metastasis, or vice versa, that variable was included in both regression models. Data were analyzed using the R statistical package version 3.0.1 (A Language and Environment for Statistical Computing, Vienna, Austria).
Table 1 shows the characteristics of the entire cohort of patients (including those who underwent palliative surgeries) who underwent surgery for rectal cancer. A total of 920 (23.0%) underwent an APE, 2687 (67.3%) an AR, and 387 (9.7%) a Hartmann operation. Table 2 reports the characteristics of patients who underwent only curative operations. A total of 700 patients (23.1%) had an APE, 2333 (69.5%) an AR, and 248 (7.4%) a Hartmann procedure. The median follow-up time was 37 months (interquartile range, 30–48 months).
Median age was significantly higher in patients with a Hartmann or APE procedure compared with those after AR (p < 0.001). Patients who underwent a Hartmann operation presented with a significantly higher ASA III to IV grade. No differences were observed in the distribution of sex after each procedure in the series or its subgroups.
Tumors of patients after a Hartmann procedure had a more advanced stage (T and TNM) both in the entire cohort (p = 0.004) and in the curative surgery patients (p< 0.001). Infiltration to neighboring structures (p < 0.001), as well as bowel perforation and positive CRM (p< 0.001), was more frequent in patients who underwent Hartmann procedure or APE.
Neoadjuvant treatment was indicated in a significant percentage of patients who had undergone an APE (p < 0.001). A Hartmann procedure was more frequently performed in the emergency setting (p < 0.001) and less frequently approached by laparoscopy (p < 0.001). No differences were observed concerning technique performed and academic hospitals.
Postoperative mortality occurred more frequently among patients who underwent a Hartmann operation (p < 0.001). Patients who underwent APE or Hartmann procedure presented with higher postoperative morbidity rates than patients with AR (p < 0.001). The need for postoperative reoperation was similar in all groups of patients (p = 0.560).
The cumulative incidence at 5 years of LR, metastases, and OS of the 3355 patients who underwent curative resection is shown in Table 3. The overall estimated LR rate was 6.81% (95% CI, 5.53–8.08); distant metastases were observed in 21.54% (95% CI, 19.44–23.59) of patients, and OS was 74.69% (95% CI, 72.48–76.97).
The cumulative incidence of LR in the 3355 curative resections is shown in Figure 1. The estimated LR rate at 5 years was 5.45% (95% CI, 3.99–6.89) after AR, 9.0% (95% CI, 6.07–12.00) after APE, and 13.06% (95% CI, 8.27–17.6) after Hartmann procedure. Significant differences were found in the log-rank test (p < 0.001). The estimated LR rate at 5 years in the entire cohort was 6.0% (95% CI, 5.08–6.92) after AR, 9.50% (95% CI, 7.54–11.46) after APE, and 14.20% (95% CI, 10.48–17.92) after Hartmann procedure. Significant differences were found in the log-rank test (p < 0.001).
The estimated cumulative incidence of metastases is shown in Figure 2. At 5 years, it was 18.51% (95% CI, 16.18–20.78) in the AR group, 27.22 (95% CI, 22.23–31.88) in the APE group, and 36.74% (95% CI, 23.73–47.54) in the Hartmann procedure group. The log-rank test indicates a significant difference comparing AR with the APE and Hartmann groups (p < 0.001); however, there was no significant difference between the APE and Hartmann procedure groups.
The OS in relation to the type of resection is shown in Figure 3. The estimated survival at 5 years was 80.29% (95% CI, 77.85–82.81) in the AR group, 64.08% (95% CI, 58.97–69.64) in the APR group, and 52.55% (95% CI, 43.56–63.39) in the Hartmann procedure group. The log-rank test indicates a significant difference (p < 0.001).
The estimated specific disease survival at 5 years was 88.4% (95% CI, 87.11–89.69) in the AR group, 78.1% (95% CI, 75.16–81.04) in the APE group, and 66.8% (95% CI, 61.04–72.56) in the Hartmann procedure group. The log-rank test indicates a significant difference (p < 0.001).
The estimated HRs for LR in relation to different prognostic variables are shown in Tables 4 and 5. Multivariate analysis of the entire cohort and of the curative surgery group show that the lower level of the tumor, advanced pathologic TNM stage, Hartmann procedure, IOP, and invaded CRM negatively influenced LR. However, APE did not significantly influence LR rates of the entire cohort (HR, 0.87; 95% CI, 0.55–1.38; p = 0.557) or of patients with curative operations (HR, 0.945; 95% CI, 0.571–1.560; p = 0.825).
Tables 6 and 7 show the relation between variables considered in the curative surgery group and metastasis, and death (OS) after a Cox regression model.
The risk of distant metastases increased in advanced pathologic TNM-stage tumors, APE (HR, 1.494; 95% CI, 1.119–1.195; p = 0.006) and Hartmann procedures, and in specimens with IOP or invaded CRM. OS was significantly related to older age, male sex, lower level of the tumor, advanced pathologic TNM stage, APE (HR, 1.433; 95% CI, 1.085–1.891; p = 0.013), Hartmann procedures, IOP, and invaded CRM.
This study could not confirm that APE, per se, influenced the rates of LR. However, it shows that the relationship between outcome and quality of surgery, measured by IOP and invaded CRM, was as important as the pathologic stage of the tumor. Furthermore, as expected, the Hartmann procedure had a negative influence on all outcomes.
The main weakness of this study deals with the voluntary nature of registration in the Spanish Rectal Cancer Project as opposed to other studies, where registration is either compulsory9,10 or in the context of randomized trials.3,5 However, several actions have been set up to guarantee the validity of registered data, including the audit of results by the health authorities.16 Moreover, to control for inclusion bias during the process of acceptance in the project, each candidate hospital was asked to provide data on their rectal cancer operations from the previous 5 years. The presence of a deviation of 10% in annual case mix was reviewed with the surgeon responsible for each hospital.
Another weakness of the study is the short period of follow-up. The introduction of neoadjuvant therapy could influence a delay in terms of LR. However, most of the recurrences in rectal cancer surgery are diagnosed in the first 3 to 5 postoperative years.17
When assessing results from different techniques, the participation of 51 hospitals has also been of concern because of the variability in practice that it can imply.12 However, all the centers participating in the project and having registered the data analyzed in the study were initially taught uniformly by the director of the Norwegian Colorectal Cancer Project.18 It has also been observed how results of this study reproduce those of the Norwegian Colorectal Cancer Project.10 Although some institutions have observed equal outcomes after APE and AR,7,8 results from randomized trials show that LR and survival are worse after APR than after AR.3,5
Other than the technical difficulties of surgery for low rectum tumors, particularly in patients with a narrow pelvis, the impairment of outcomes after APE has been related to the waist that it creates in the specimen. The rationale of this explanation is that resections producing these specimens do not include the levator ani.11
Technical difficulty and waisted specimens are considered the causes for higher rates of invaded CRM and IOP after APE than after AR. Taking into account that involved CRM19,20 and IOP21,22 are thought to be surrogates for oncologic outcomes, those should be worse after APE compared with AR. Reported invaded CRM rates after APE vary in the literature between 11% and 52%2–5,9,10,20–22 and those of IOP between 10% and 19%.3,9,10,13,21–23
National registries of Norway and Denmark, as well as the Stockholm Colorectal Cancer Study Group, where the Spanish project sought inspiration, report a 12% to 18% rate for invaded CRM and a 10% to 16% rate for IOP,9,10,23 which is more homogenously distributed and comparable with those of the present series at 14% and 10%.
Only 2 previous studies9,10 have assessed the operation, per se, as a potential independent prognostic factor. Wibe et al10 showed similar LR rates after both techniques and worse OS rates after APE. Anderin et al9 could not confirm in the multivariate analysis that APE, per se, was an independent prognostic factor for LR, metastasis, and OS.
It is difficult to explain the almost similar LR rates reported by the Norwegian Rectal Cancer Project (8%),24 the Stockholm Colorectal Cancer Study Group (5%),9 and the observed 7% in this study, because the use of neoadjuvant treatment differed considerably. In the Norwegian Rectal Cancer Project,24 20% of patients underwent neoadjuvant treatment compared with 71% in the Stockholm Colorectal Cancer Study9 and 60% in the Spanish Rectal Cancer Project. It seems like the optimal use of neoadjuvant treatment is still to be defined. This study also shows that training multidisciplinary teams and offering feedback of results improve surgical competence, which has become an essential tool in the management of rectal cancer toward optimizing surgery and diminishing the invaded CRM and IOP rates.14,18,25
It has been suggested that oncologic results after APE can be improved by the extralevator technique13,26 as one way of controlling correct planes of dissection. Unfortunately, results of this operation have not been reported. Whether a change in technique for APE in the centers participating in the Spanish project could be a way of improving results should be evaluated in the future.
We stress that the aim of this study was not to demonstrate the superiority of any one surgical approach. Instead, we transmit the experience of a national audit program on rectal cancer surgery highlighting the message that rectal cancer presents different results according to the different operations performed. The procedure chosen depends on the characteristics of the patient, tumor level, fecal incontinence before surgery, and preoperative findings like perforated tumors with abscesses. Thus, the purpose of this article is to report the details of different outcomes from different procedures.
Although bowel perforation and involvement of the circumferential resection margin were more common after APE than after AR, this study did not identify APE as a determinant of LR in the context of 3 years of median follow-up.
The authors thank all the involved specialists at the participating hospitals for their efforts toward improving standards of rectal cancer treatment in Spain. On behalf of the patients, we also thank the Ministry of Health for funding this project.
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Hospitals included in the Spanish Rectal Cancer Project are as follows: Virgen de la Arrixaca (Juan Lujan, M.D.), Bellvitge (Doménico Fraccalvieri, M.D.; Sebastiano Biondo), Complejo Hospitalario de Navarra (Pedro Armendáriz, M.D.; Mario de Miguel, M.D.), Clínico de Valencia (Alejandro Espí, M.D.), Josep Trueta (Antonio Codina, M.D.), Sagunto (María D. Ruiz, M.D.), Vall de Hebrón (Eloy Espin, M.D.), La Fe (Rosana Palasí, M.D.), Complejo Hospitalario Ourense (Alberto Parajo, M.D.), Germans Trias i Pujol (Ignasi Camps, M.D.; Marta Piñol, M.D.), Morales Meseguer (Enrique Pellicer, M.D.), Lluis Alcanyis (Vicent Viciano, M.D.), Complejo Asistencial Burgos (Evelio Alonso, M.D.), del Mar (Miguel Pera, M.D.), Meixoeiro (Teresa García, M.D; Enrique Casal, M.D.), Complejo Asistencial Salamanca (Jacinto Garcia, M.D.), Gregorio Marañón (Marcos Rodríguez, M.D.),Torrecárdenas (Ángel Reina, M.D.), General de Valencia (José Roig, M.D.), Txagorritxu (José Errasti, M.D.), Donostia (José A. Múgica, M.D.), Reina Sofía (José Gomez, M.D.), Juan Ramón Jiménez (Ricardo Rada, M.D.; Mónica Orelogio) Arnau de Vilanova de Valencia (Natalia Uribe, M.D.), General de Jerez (Juan de Dios Franco, M.D.), General. Universitario de Elche (Antonio Arroyo, M.D.), Arnau de Vilanova de Lleida (José Enrique Sierra, M.D.), Santa Creu i Sant Pau (Pilar Hernandez, M.D.), Clínico de Santiago de Compostela (Jesús Paredes, M.D.), Universitario de Jaén (Gabriel Martínez, M.D.), Clínico San Carlos (Mauricio Garcia, M.D.), Cabueñes (Guillermo Carreño, M.D.), General de Albacete (Jesús Cifuentes, M.D.), Miguel Servet (José Monzón, M.D.), Xeral de Lugo (Olga Maseda, M.D.), Universitario de Fuenlabrada (Daniel Huerga, M.D.), Clínico y Provincial de Barcelona (Calin Pavel, M.D.), Joan XXIII (Fernando Gris, M.D.), Virgen de las Nieves (Inmaculada Segura, M.D.; Pablo Palma, M.D.), Nuestra Señora de la Candelaria (José Gregorio Díaz, M.D.), Complejo Hospitalario de Badajoz (José Luis Jiménez, M.D.), Clínico Universitario San Cecilio (Francisco Pérez, M.D.), Galdakao (Vicente Portugal, M.D.), Requena (Juan C. Bernal, M.D.), General Alicante (Félix Lluis, M.D.), Virgen Macarena (Luis Capitán, M.D.), Xeral-Cies De Vigo (Nieves Cáceres, M.D.), Infanta Sofía (Javier Martínez, M.D.), Povisa (Alfredo Estévez, M.D.), Virgen del Rocío (María Victoria Maestre, M.D.; José Manuel Díaz, M.D.), San Juan de Dios del Aljarafe (Mónica Reig, M.D.; Antonio Amaya, M.D.), Nuestra Señora de Sonsoles (José Antonio Carmona, M.D.), Getafe (Francisco J. Jiménez, M.D.), General de Granollers (Dídac Ribé i Serrat, M.D.), La Paz (Isabel Prieto, M.D.; Damian Garcia M.D.), Complejo Hospitalario de León (Tomas González de Francisco, M.D.; Amor Turienzo, M.D.), Dr. Peset (Manuel Martinez, M.D.). Rafael Méndez (Sergio del Valle, M.D.), General Reina Sofia (Pedro Parra, M.D.), San Pedro de Alcántara (Francisco Romero, M.D.), Torrevieja Salud (Alessandro Garcea, M.D.), Santa María de Lleida (Xavier Rodamilans de la O, M.D.), Virgen del Puerto (Alberto Pérez, M.D.), Segovia (Guillermo Ais, M.D.), Consorci Sanitari Integral (Luis Ortiz de Zarate, M.D.), Reus (Jesús Sánchez, M.D.), Instituto Valenciano de Oncologia (Rafael Estevan, M.D.), Viladecans (Albert Sueiras, M.D.), Cruces (Alberto Lamiquiz; Andoni Larzabal, M.D.), Ramón y Cajal (Javier Die, M.D.), Manises (Amparo Solana, M.D.), La Ribera Alzira (Francisco Javier Blanco, M.D.), Nuestra Señora del Rosell (Ana Mª Lage, M.D.), Mérida (José L. Domínguez, M.D.), Fundación Alcorcón (Paula Dujovne, M.D.), De Henares (Natividad Palencia, M.D.), General de Castellón (Rafael García, M.D.), De Vinaroz (Raul Adell, M.D.), Onkologikoa (Roberto Martínez, M.D.), Palencia (Ana Mª Huidobro, M.D.), Fundación Jiménez Díaz (Carlos Pastor, M.D.), Torrejón (Jesús Á. Garijo, M.D.), Universitario de Tenerife (Ángel Carrillo, M.D.), Puerto Real (Mª del Coral de la Vega, M.D.), Sta. Coloma De Gramenet (Manuel López, M.D.).
Abdominoperineal resection; Local recurrence; Metastases; Overall survival; Rectal cancer
© 2014 The American Society of Colon and Rectal Surgeons
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