Abstract
Background
At present, abdominoperineal excision with neoadjuvant chemoradiotherapy (nCRT) is one of the treatment modalities of distal rectal cancer. Our study analyzed the effects of laparoscopic extralevator abdominoperineal resection (ELAPE) compared with laparoscopic conventional abdominoperineal resection(cAPR) in the treatment of distal rectal cancer.
Methods
Retrospective analysis was conducted on the clinicopathological data of 177 distal rectal cancer patients treated with a laparoscopic abdominoperineal resection between 2011 and 2018. The patients were divided into four groups as follows: ELAPE without nCRT (group A), cAPR without nCRT (group B), ELAPE with long-course nCRT (group C) and cAPR with long-course nCRT (group D).
Results
Positive circumferential resection margin (CRM), local recurrence rate, 3-year disease-free survival (DFS) and 3-year overall survival (OS) did not differ between group A and group B. The rate of positive CRM in group C was lower than group D (4.4% vs. 11.9%, respectively), although the difference was not significant (P = 0.377). The 3-year local recurrence rate in group C was lower compared with group D (6.6% vs. 16.7%, respectively), although the difference was not significant (P = 0.135). Three-year DFS and 3-year OS were not different between groups C and D.
Conclusions
This study showed that the effect of laparoscopic ELAPE in patients with low-risk rectal cancer is similar to laparoscopic cAPR, revealing that laparoscopic cAPR can be routinely selected for patients with low-risk rectal cancer. Furthermore, laparoscopic ELAPE has a tendency to reduce the rate of positive CRM and local recurrence in patients with high-risk rectal cancer. Laparoscopic ELAPE can be routinely considered for patients with high-risk rectal cancer.
Keywords: Laparoscope, Extralevator abdominoperineal resection, Conventional abdominoperineal excision, Distal rectal cancer
Background
Laparoscopic surgery can achieve less postoperative complications and faster postoperative recovery in patients with distal rectal cancer [1]. Moreover, laparoscopic surgery can be performed safely in the elderly population, and reduce their pain and convalescence [2]. Therefore, laparoscopic technology has been routinely used in abdominoperineal excision (APE) in patients with distal rectal cancer [3–6].
During conventional abdominoperineal resection (cAPR) the mesorectum is mobilized along the surface of mesorectal fascia from the levator muscles down to the top of anorectal ring. Incision of the gap between mesorectum and levator muscles close to levator hiatus increases the risk of positive circumferential resection margin (CRM). To decrease the risk of positive CRM the mesorectum is not mobilized from the levator muscles and the gap between mesorectum and levator muscles is not incised in extralevator abdominoperineal resection (ELAPE). Compared with cAPR, ELAPE was considered to be able to reduce risk for intraoperative perforation (IOP), and positive CRM, which may induce local recurrence of tumor [7, 8]. At present, ELAPE has been suggested to be selectively performed in patients with advance stage distal rectal cancer [9].
Similarly, the incision of the gap between mesorectum and levator muscles much closer to rectal muscle tube in cAPR might increase the risk of positive CRM in early stage distal rectal cancer, too. Therefore, we speculate that ELAPE can also decrease the risk of positive CRM and influence the survival of the patient with early stage distal rectal cancer. In this study the data of patients undergoing cAPR and ELAPE were analyzed to evaluate the efficacy of ELAPE in patients with early stage distal rectal cancer.
In order to reduce tumor mass and local recurrence rate, neoadjuvant chemoradiotherapy (nCRT) is routinely applied to the treatment of patients with advance stage distal rectal cancer [10–13]. For patients with early stage distal rectal cancer, which includes T1-3bN0 determined by magnetic resonance imaging (MRI), surgery can be delivered directly [14]. For patients with advance stage distal rectal cancer, which includes T3c-3dN0, T1-3N1-2 and T4b, nCRT should be delivered before surgery [15].
In previous studies, patients with distal rectal cancer who received laparoscopic cAPR directly and those who underwent nCRT and then laparoscopic cAPR were seldom distinguished [16, 17]. To investigate the effect of laparoscopic ELAPE with or without nCRT, we divided patients into four groups according to whether they received long-course nCRT. The effects of laparoscopic ELAPE were analyzed using a stratified method compared with laparoscopic cAPR.
Methods
Patients
A total of 177 patients with distal rectal cancer treated with a curative laparoscopic ELAPE or laparoscopic cAPR at the Second Hospital of Tianjin Medical University (Tianjin, China) and the First Affiliated Hospital of Kunming Medical University (Kunming, China) were retrospectively reviewed between June 2011 and June 2018.
All patients were diagnosed with colonoscopy and pathological biopsy proved distal rectal adenocarcinoma. Clinical staging was evaluated by enhanced computed tomography (CT) and no distal metastasis was confirmed. T and N stages of rectal lesions were evaluated by magnetic resonance imaging (MRI) before surgery. Results of MRI evaluation in all patients showed that a safe distal margin could not be achieved using a sphincter sparing technique or tumor invasion in the anal sphincter.
For patients with low-risk rectal cancer, which included T1-3bN0 determined by MRI imaging, laparoscopic ELAPE (group A) or cAPR (group B) were delivered directly. Postoperative chemotherapy (mfolfox6 or Xelox) was recommended according to the final pathology report.
For patients with high-risk rectal cancer, which include T3c-3bN0, T1-3N1-2 and T4b with MRF invasion, long-course nCRT was delivered before surgery. A total of 50.4–54.0 Gy of radiation and 5-FU-based chemotherapy (capecitabine) were given to patients. Laparoscopic ELAPE (group C) or cAPR (group D) were performed 8–10 weeks following nCRT. During the interval between nCRT and surgery, the patient received Xelox (2 times) or mfolfox6 (3 times) chemotherapy. Postoperative chemotherapy (mfolfox6 or Xelox) was recommended for 2–3 months.
Operation procedure
The procedure of laparoscopic ELAPE and cAPR was conducted according to the principle of total mesorectal excision.
In laparoscopic ELAPE the mesorectum is not mobilized from the levator ani muscles, and the potential space between the mesorectum and levator ani muscle was not incised (Fig. 1). Therefore, after mobilizing the mesorectum along the surface of mesorectal fascia down to the beginning of the levator ani muscles the mobilization is stopped at the upper border of the coccyx posteriorly, just at the starting point of the levator ani muscle laterally and anteriorly. The rest of procedure was conducted as described in the previous literature [16, 18].
Fig. 1.
a Specimen of ELAPE The proper fascia of rectum is intact and the anorectal junction is completely covered by the levator ani muscle. b Specimen of cAPR The anorectal junction is not covered by the levator ani muscle
In laparoscopic cAPR the mesorectum is mobilized from the levator ani muscles, the potential space between the mesorectum and levator ani muscle was incised. Therefore, the mesorectum is mobilized along the surface of mesorectal fascia from the levator muscles down to the top of anorectal ring. The rest of procedure was conducted as described in the previous literature [16, 18].
Outcome measures
Patient demographics, preoperative MRI-stage, neoadjuvant treatment, intraoperative perforation, pathologic stage, positive CRM, postoperative complications, local recurrence, 3-year disease-free survival (DFS) and 3-year overall survival (OS) were collected and analyzed.
Follow-up
All patients were followed up in the two hospitals for an average of 36 months postoperatively. CEA, CT, MRI and Colonoscopy was conducted as described in the literature [19].
Statistics
SPSS software (version 23.0; IBM Corp., Armonk, NY, USA) was applied for statistical analysis. Categorical data were analyzed using the Chi-square test. The Kaplan Meier method were used to calculate cumulative rates for local recurrence and survival. P < 0.05 was considered to be statistically significant.
Results
The study included 177 patients; 90 patients did not receive nCRT, of which 49 cases underwent laparoscopic ELAPE (group A) and 41 cases underwent laparoscopic cAPR (group B). Characteristics of patients were listed in Tables 1 and 2. Gender, age and preoperative MRI-stage were not significantly different between group A and group B (Table 2). A total of 87 patients received nCRT before surgery, of which 45 cases underwent laparoscopic ELAPE (group C) and 42 cases underwent laparoscopic cAPR (group D). Gender, age, preoperative MRI-stage and neoadjuvant treatment were not significantly different between group C and group D (Table 2).
Table 1.
Characteristics of patients after ELAPE and cAPR regardless of nCRT
| ELAPE (94) | cAPR (83) | P values | |
|---|---|---|---|
| Age (years) | 59.61 ± 11.93 | 58.33 ± 10.86 | 0.585 |
| Gender | |||
| Male | 52 | 46 | 0.989 |
| Female | 42 | 37 | |
| MRI-stage | |||
| I | 20 | 16 | 0.742 |
| II | 48 | 39 | 0.588 |
| III | 26 | 28 | 0.381 |
| Neoadjuvant treatment | 45 | 42 | 0.717 |
Table 2.
Characteristics of patients
| Group A (49) | Group B (41) | P values | Group C (45) | Group D (42) | P values | |
|---|---|---|---|---|---|---|
| Age (years) | 60.22 ± 12.84 | 62.22 ± 12.07 | 0.453 | 59.28 ± 11.02 | 54.50 ± 10.21 | 0.537 |
| Gender | 0.921 | 0.894 | ||||
| Male | 28 | 23 | 24 | 23 | ||
| Female | 21 | 18 | 21 | 19 | ||
| MRI-stage | 0.863 | 0.393 | ||||
| I | 20 | 16 | 0 | 0 | ||
| II | 29 | 25 | 19 | 14 | ||
| III | 0 | 0 | 26 | 28 | ||
| Neoadjuvant Treatment | 0 | 0 | 1.0 | 45 | 42 | 1.0 |
Perioperative data
Perioperative data of the patients including intraoperative perforation, pathologic stage, positive CRM and postoperative complications collected from patient chart notes were listed in Tables 3 and 4.
Table 3.
Perioperative data of patients after ELAPE and cAPR regardless of nCRT
| ELAPE (94) | cAPR (83) | P values | |
|---|---|---|---|
| Intraoperative perforation | 1 | 4 | 0.294 |
| Pathologic stage | |||
| pT0 | 0 | 0 | 1.0 |
| pT1 | 12 | 6 | 0.224 |
| pT2 | 37 | 35 | 0.704 |
| pT3 | 0 | 0 | 1.0 |
| pT4 | 0 | 0 | |
| pN0 | 0 | 0 | |
| pN1 | 0 | 0 | |
| pN2 | 0 | 0 | |
| ypT0 | 3 | 4 | 0.867 |
| ypT1 | 7 | 6 | 0.956 |
| ypT2 | 9 | 8 | 0.988 |
| ypT3 | 21 | 17 | 0.764 |
| ypT4 | 5 | 7 | 0.411 |
| ypN0 | 21 | 19 | 0.930 |
| ypN1 | 15 | 16 | 0.562 |
| ypN2 | 9 | 7 | 0.792 |
| Positive CRM | 2 | 5 | 0.347 |
| Postoperative complications | |||
| Urinary retention | 6 | 6 | 0.823 |
| Intestinal obstruction | 3 | 5 | 0.587 |
| Perineal wound dehiscence | 8 | 7 | 0.985 |
Table 4.
Comparison of perioperative data from patients with distal rectal cancer
| Group A (49) | Group B (41) | P values | Group C (45) | Group D (42) | P values | ||
|---|---|---|---|---|---|---|---|
| Intraoperative perforation | 0 | 0 | 1.0 | 1 | 4 | 0.317 | |
| Pathologic stage | |||||||
| pT0 | ypT0 | 3 | 4 | 0.924 | |||
| pT1 | 12 | 6 | 0.244 | ypT1 | 7 | 6 | 0.868 |
| pT2 | 37 | 35 | 0.244 | ypT2 | 9 | 8 | 0.911 |
| pT3 | ypT3 | 21 | 17 | 0.561 | |||
| pT4 | ypT4 | 5 | 7 | 0.453 | |||
| pN0 | ypN0 | 21 | 19 | 0.894 | |||
| pN1 | 0 | 0 | 1.0 | ypN1 | 15 | 16 | 0.643 |
| pN2 | 0 | 0 | 0.244 | ypN2 | 9 | 7 | 0.688 |
| Positive CRM | 0 | 0 | 1.0 | 2 | 5 | 0.377 | |
| Postoperative complications | |||||||
| Urinary retention | 3 | 1 | 0.742 | 3 | 5 | 0.636 | |
| Intestinal obstruction | 1 | 2 | 0.875 | 2 | 3 | 0.937 | |
| Perineal wound dehiscence | 3 | 4 | 0.806 | 5 | 3 | 0.788 | |
No intraoperative perforation or positive CRM were observed in both group A and group B (P = 1.0). Pathologic stage was not significantly different between group A and group B. No unplanned reoperations or deaths were seen in group A or group B. The rate of intraoperative perforation in group C was lower compared with group D (1/45 vs. 4/42, respectively), although the difference was not significant (P = 0.317). The rate of positive CRM in group C was lower compared with group D (2/45 vs. 5/42, respectively), although the difference was not significant (P = 0.377). Pathological stage was not significantly different between group C and group D. No unplanned reoperations and deaths were seen in group C or group D (Table 4).
Postoperative intestinal obstruction, urinary retention, and perineal wound dehiscence were all comparable between group A and group B (P > 0.05). In addition, postoperative intestinal obstruction, urinary retention, and perineal wound dehiscence were all comparable between group C and group D (P > 0.05).
Local recurrence
A total of 47 patients were alive without local recurrence at last follow-up in group A. Two patients developed local recurrence, and the 3-year local recurrence rate was 4.1% (2/49). Thirty-nine patients were alive without local recurrence at last follow-up in group B. Two patients developed local recurrence, and the 3-year local recurrence rate was 4.8% (2/41). The local recurrence rate was not significantly different between group A and group B (P = 0.856). The cumulative incidence curves are shown in Fig. 2.
Fig. 2.
a Cumulative local recurrence rate of patients without nCRT. b Cumulative local recurrence rate of patients with nCRT. c Comparative analysis of cumulative local recurrence rate between ELAPE and cAPR patients regardless of nCRT. Dotted lines represent Kapan–Meier analysis. a P = 0.856, b P = 0.135, c P = 0.169
A total of 41 patients were alive without local recurrence at last follow-up in group C. Three patients developed local recurrence, the local recurrence rate was 6.6% (3/45). Thirty-four patients were alive without local recurrence at last follow-up in group D. Seven patients developed local recurrence, and the local recurrence rate was 16.7% (7/42). The local recurrence rate was not significantly different between group C and group D (P = 0.135). The cumulative incidence curves are shown in Fig. 2.
DFS
In group A, two patients had local recurrence, four had liver metastasis, five had lung metastasis and two had liver and lung metastasis. The 3-year DFS rate was 73.5% (36/49) in group A. In group B, two patients had local recurrence, three had liver metastasis, six had lung metastasis and one had bone metastasis. The 3-year DFS rate was 70.7% (29/41) in group B. No difference in 3-year DFS was observed between groups A and B (P = 0.820) (Fig. 3).
Fig. 3.
a 3-year DFS of patients without nCRT. b 3-year DFS of patients with nCRT. c Comparative analysis of 3-year DFS between ELAPE and cAPR patients regardless of nCRT. Dotted lines represent Kapan–Meier analysis. a P = 0.820, b P = 0.759, c = 0.642
In group C, three patients had local recurrence, five had liver metastasis, six had lung metastasis, three had liver and lung metastasis and one had bone metastasis. The 3-year DFS rate was 59.2% (27/45) in group C. In group D, five patients had local recurrence, two had local recurrence and liver metastasis, four had liver metastasis, five had lung metastasis, one had liver and lung metastasis and two had bone metastasis. The 3-year DFS rate was 54.8% (23/42) in group D. No difference in 3-year DFS was observed between groups C and D (P = 0.759) (Fig. 3).
OS
At 36 months follow-up, the median OS was not reached in either groups A or B. The 3-year OS survival rates were 81.6% (40/49) in group A and 75.6% (31/41) in group B, and the 3-year OS was not significantly different (P = 0.545) (Fig. 4).
Fig. 4.
a 3-year OS of patients without nCRT. b 3-year OS of patients with nCRT. c Comparative analysis of 3-year OS between ELAPE and cAPR patients regardless of nCRT. Dotted lines represent Kapan-Meier analysis. a P = 0.545, b P = 0.864, c = 0.564
In addition, the median OS was not reached in either groups C or D. The 3-year OS survival rates were 64.4% (29/45) in group C and 61.9% (26/42) in group D, and the 3-year OS was not significantly different (P = 0.864) (Fig. 4).
Discussion
The extralevator abdominoperineal resection (ELAPE) lays emphasis on precise anatomy and complies with the radical resection of tumors principle. ELAPE has provided higher quality LN harvests and reduced the rate of intraoperative perforation, positive CRM and local recurrence compared with the conventional abdominoperineal resection(cAPR) procedure [20–25].
During the abdominal laparoscopic ELAPE procedure, the anterior space of the rectum does not require an incision to the hiatus in the levator ani muscle. However, the anterior lobe of the Denonvilliers fascia should be incised, otherwise the neurovascular bundles (NVB) on both sides of the seminal vesicle gland may be pulled and deformed during perineum operation. The NVB can be easily injured, which can lead to postoperative autonomic nerve dysfunction. In this study, the NVB in all patients within each of the four groups were effectively protected and no severe urinary or sexual function-related adverse events were observed.
MRI is used to determine which surgery, with or without nCRT, is routinely suggested for patients with rectal cancer [26–28]. In the present study following MRI, the patients in group A and group B underwent surgery without nCRT, and no positive CRM or intraoperative perforations were observed in either group. These results indicated that both laparoscopic APR and laparoscopic ELAPE can achieve satisfactory CRM and intraoperative perforation results in patients with low-risk rectal cancer.
The rate of intraoperative perforations and positive CRM in group C was lower than group D, although the difference was not significant. These results indicated that laparoscopic ELAPE has a tendency to reduce the rate of intraoperative perforation and positive CRM in patients with high-risk rectal cancer.
Laparoscopic ELAPE did not reduce local recurrence rate in patients with low-risk rectal cancer compared with laparoscopic cAPR, which indicated that a decreased local recurrence rate can be obtained by choosing either laparoscopic cAPR or laparoscopic ELAPE in patients with low-risk rectal cancer. The rate of local recurrence in group C was significantly lower than group D, although the difference was not significant. These findings indicated that laparoscopic ELAPE has a tendency to reduce local recurrence rate of patients with high-risk rectal cancer.
Laparoscopic ELAPE did not improve 3-year DFS or 3-year OS in patients with low-risk rectal cancer compared with laparoscopic cAPR. These results indicated different laparoscopic surgery did not influence the outcome of DFS or OS in patients with low-risk rectal cancer.
Although the results of our study reveal that laparoscopic ELAPE has a tendency to reduce the rate of intraoperative perforation, positive CRM and local recurrence rate of patients with high-risk rectal cancer, laparoscopic ELAPE did not improve 3-year DFS or 3-year OS in patients with high-risk rectal cancer compared with laparoscopic cAPR. This finding may be related to the increased proportion of patients with distant metastasis. The treatment course before surgery is approximately 3 months, thus with the extension of the course of treatment, the risk of distant metastasis is increased. Therefore, the effect of ELAPE for improving DFS and OS of patients with high-risk rectal cancer was influenced by nCRT.
With the rapid development of laparoscopic technology, the number of distal rectal cancer patients who underwent abdominoperineal resection shows a downward trend.
In order to obtain a sufficient number of cases, we collected the date of the patients from two medical centers. Therefore, all the operations were not performed by the same surgeon, which may have an impact on our research results.
In conclusion, the effect of laparoscopic ELAPE in patients with low-risk rectal cancer is similar to laparoscopic cAPR, revealing that laparoscopic cAPR can be routinely selected for patients with low-risk rectal cancer. Furthermore, laparoscopic ELAPE has a tendency to reduce the rate of positive CRM and local recurrence in patients with high-risk rectal cancer. However, laparoscopic ELAPE did not achieve a higher 3-year DFS or 3-year OS in patients with high-risk rectal cancer, which was related to an increased risk of distant metastasis caused by long-term nCRT treatment before surgery. Our results revealed that laparoscopic ELAPE can be routinely considered for patients with high-risk rectal cancer.
Acknowledgements
Not applicable.
Abbreviations
- APE
Abdominoperineal excision
- cAPR
Conventional abdominoperineal resection
- CRM
Circumferential resection margin
- ELAPE
Extralevator abdominoperineal resection
- nCRT
Neoadjuvant chemoradiotherapy
- MRI
Magnetic resonance imaging
- MRF
Mesorectal fascia
- CT
Computed tomography
- MRI
Magnetic resonance imaging
Author contributions
ZQW: Designed the studies, interpretation of the data and writing of the manuscript. RL and DY: Performed studies and analysis. JY and WLL: prepared and edited the manuscript. ZYK: Conceived, designed and oversaw all of the studies, reviewed the manuscript, and responsible for the primary undertaking, completion, and supervision of all experiments. All authors read and approved the final manuscript.
Funding
This study was supported by Grants from Tianjin Natural Science Foundation (21JCYBJC01730) and the Youth Foundation of the second hospital of Tianjin Medical University (Grant No. 2019ydey02, 2020ydey20), which paid all editing and publication fees.
Availability of data and materials
The primary data analyzed during the current study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
This study was conducted in accordance with the Declaration of Helsinki, and with the approval of the Ethics Committee of the Second Hospital of Tianjin Medical University and the First Affiliated Hospital of Kunming Medical University. Written informed consent was obtained from all the participants.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Zhiqiang Wang and Rui Liang have contributed equally to this work and should be considered co-first authors
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The primary data analyzed during the current study are available from the corresponding author on reasonable request.