Abstract
Objective:
The objective is to investigate if laparoscopic-dominant abdominoperineal resection (LDAPR) with individualised levator ani resection inhibits local recurrence (LR) and prolongs survival as compared to laparoscopic abdominoperineal resection (APR).
Materials and Methods:
Rectal cancer surgery cases were retrospectively identified from September 2014 to December 2019. LDAPR-treated group (55 patients) and the APR-treated group (71 patients) were included in the study. The operation time, circumferential resection margin (CRM), intraoperative tumor surgery (ITP), post-operative complications, the 2-year overall survival (OS) and LR were compared in the two groups.
Results:
The CRM and ITP were significantly reduced in the LDAPR as compared to the APR group (3.6% vs. 16.9%, t = 5.522, P = 0.019; 3.6% vs. 14.1%, t = 3.926, P = 0.048). In terms of post-operative complications, the incidence of urinary retention in LDAPR was significantly reduced than the APR group (10.9% vs. 25.4%, χ2 = 4.139, P = 0.041). Similarly, perineal pain at 6 months or 1 year after surgery was significantly down-regulated in LDAPR than in the APR group (72.7% vs. 88.7%, χ2 = 5.320, P = 0.021; 18.2% vs. 43.2%, χ2 = 8.288, P = 0.004). However, there was no statistically significant difference in the post-operative complications between the LDAPR and APR groups. Finally, LDAPR led to a significantly improved 2-year OS and a reduced LR compared to APR.
Conclusion:
LDAPR reduces CMR, ITP and LR and simplified the perineum operation, subsequently protecting the pelvic autonomic nerves. Compared to the conventional APR, LDAPR is a promising procedure worth adopting for rectal cancer treatment.
Keywords: Abdominoperineal resection, individualised levator ani resection, local recurrence, low rectal cancer, overall survival
INTRODUCTION
Low rectal cancer refers to malignant rectal tumours within 5 cm from the anal verge. Currently, surgery remains the main treatment method for common rectal cancer, with abdominoperineal resection (APR)[1,2] being the standard surgical procedure. The use of the APR lies in the ability to remove the low tumour, related lymphoid tissue and elaborate structures from the deep pelvis.[3] The APR indications include ultra-low rectal cancer growths with the inability to obtain a negative distal margin, external sphincter involvement or the levator ani complex invasion.[4] The patients with poor baseline function of the sphincter with rectal cancer are also well-suited to receive abdominoperineal resection.
However, despite the major progress in the multidisciplinary treatment approach to rectal cancer, about 40% of rectal cancer patients will undergo an abdominoperineal resection, resulting in a permanent colostomy.[5] In recent years, Holm et al.[6] have also reported a new surgical method for treating low rectal cancer, namely extralevator abdominoperineal excision (ELAPE) combined with different levator ani. The surgical confluence plane is at the origin of the levator ani muscle. The levator ani muscle is completely removed, making the surgical specimen columnar, avoiding the formation of surgical waste and reducing the positive rate of circumferential resection margin (CRM) and intraoperative perforation.[7] Nevertheless, due to extended resection, ELAPE surgery may lead to more complications such as sexual dysfunction, urination dysfunction, chronic perineal pain and perineal hernia.[8,9] Due to the disadvantages of APR and ELAPE surgery, new technology is needed to avoid adverse surgical effects and complications.
Here, we propose a new method of combined abdominal and perineal resection, as an alternative to the conventional APR, that is, individualised resection of the levator ani muscle guided by laparoscopy to reduce the positive rate of CMR and ITP, reduce local recurrence (LR) and simplify the operation of the perineum. In addition, we provide evidence that laparoscopic-dominant abdominoperineal resection (LDAPR) is a safe technology for rectal cancer. The primary endpoints were CRM (+), ITP, 2-year overall survival (2-year OS) and 2-year LR. The secondary endpoints were the post-operative complications.
MATERIALS AND METHODS
This study retrospectively used medical records of rectal cancer surgery cases from September 2014 to December 2019. The experimental group included patients who had undergone laparoscopic-led individualised levator ani resection from January 2017 to December 2019, while the control group included patients who had received laparoscopic conventional APR surgery from September 2014 to December 2016. The ethics committee of Zhangzhou Municipal Hospital Affiliated of Fujian Medical University approved this retrospective investigation and waived the regulations of informed consent due to the design of the study.
Inclusion criteria
Solitary rectal adenocarcinoma or carcinoma diagnosed by colonoscopy and biopsy, and the anus could not be preserved; the high-resolution magnetic resonance imaging (MRI) staging below T3a, and some T3b and T3c patients were reduced after neoadjuvant chemoradiotherapy; age <75 years old; no local infection such as anal fistula and perianal abscess; no severe cardiopulmonary, liver and kidney dysfunction; laparoscopic surgery and no sexual dysfunction and urination prior to surgery.
Exclusion criteria
Post-operative pathological findings of non-adenocarcinoma such as signet-ring cell carcinoma and malignant melanoma; medical records of T4 stage; patients with distant metastasis or local inability to undergo R0 resection, but palliative resection is performed; transition to laparotomy.
Surgical methods
Abdominoperineal resection
The operation is divided into two phases: the abdominal and perineal phases.
The abdominal phase is done according to the conventional surgical procedures that target the total mesorectal excision (TME) plane. It follows the principle of low anterior resection in laparoscopic anterior rectotomy that ensures the separation of the left Toldt space. The lymph nodes at the inferior mesenteric artery and the root of the vein are dissected at a high position and ligated. The mesorectum is later freed to the sacral promontory, separated along with the retrorectal space to the level of the levator ani hiatus, and the separation is confirmed by touching the bony sense of the tip of the coccyx using an ultrasonic knife. Next, both sides of the mesorectum are further separated along the holy plane. The separation reaches the starting point of the levator ani fissure (both sides).
The peritoneum is incised in an arc at 0.5 cm on the peritoneal reflex line to ensure the integrity of Denonvillier’s fascia. In male patients, Denonvillier’s fascia needs to be transected when the sharp separation reaches the upper border of the prostate. In women, the strong separation can be performed directly along the Denonvillier fascia’s surface to the levator hiatus’s upper edge. The procedure results in complete separation of the terminal mesentery of the rectum. The sigmoid colon, located 15 cm from the proximal end of the tumour, is cut off with a laparoscopic linear incision and a closure device. The proximal colon is finally pulled out of the left lower abdomen for a permanent stoma.
Perineal phase
The anus is closed with a double purse suture. An oval incision is made at the key point of the perineal body in front of the anus, the tip of the coccyx at the rear and on both sides of the medial border of the ischial tubercle. The subcutaneous tissue is incised layer by layer. The anococcygeal ligament is then cut in front of the tip of the coccyx, and the abdominal group is joined. The anterior wall of the anal rectal canal is then separated from the rectus muscle, the urethra and the prostate (posterior vaginal wall in women). This also enables the removal of the distal sigmoid colon and an eventual anal tissue perineal incision. The wound surface is let to undergo hemostasis and then flushed. The perineal incision is finally sutured in a layer-by-layer pattern without closing the pelvic floor peritoneum.
Laparoscopic-dominant abdominoperineal resection with individualised levator ani resection
In the abdominal phase, the mesorectum is surgically freed to the levator ani muscle insertion level similar to the APR group. The coccygeal anus ligament is removed under laparoscopic direct vision, and then, the extent of levator ani muscle resection is determined according to the tumour location and degree of invasion. The tumour is confined to T2, and the levator ani muscle is cut and dissociated from a distance of 1.5 cm from the insertion point of the levator ani muscle. The levator ani muscle on the healthy side is preserved if there is no invasion on the contralateral side. All the levator ani muscles on the affected side are resected in case the tumour invaded more than T3.
The healthy levator ani muscle is preserved on the opposite side without invasion. If the tumour invades both sides, the scope of resection of the levator ani muscle on both sides is determined according to the above method, and the depth of tumour invasion is also assessed. Part of the prostate and vagina could be removed if the anterior rectal wall tumour involved the anterior pelvic fascia. The coccyx tip would be removed together if the posterior wall tumour invaded the presacral fascia. There is no need to change the patient’s position in the perineal group.
The surgical incision is made in a similar manner as described for the APR (control) group. Because the space between the levator ani muscle and the perianal fat has been removed in the abdominal group, only the subcutaneous tissue and the perianal fat area need to be incised (the ischiorectal fossa fat tissue is not completely removed) because it is very easy to join the abdominal group. The specimen is then held in one hand, and the rectourethral muscle and puborectalis muscle are cut off under the guidance of the fingers and separated from the urethra and prostate (the posterior wall of the vagina in women). For reconstruction, the perineal incision is finally reconstructed through layer-by-layer suturing without closing the pelvic floor peritoneum. The perineal defect closure was done through biological mesh (Biodesign, Cook Medical, IN, USA).
The general data of the patients in these two groups were compared, including gender, age, BMI, distance from the inferior tumour to the anal verge (cm), tumour location, neoadjuvant therapy, American Society of Anaesthesiologist (ASA) grading, pathological differentiation and p-T\N staging. In addition, these two groups’ operation conditions and post-operative recovery indicators were also compared, including operation time, intraoperative blood loss, post-operative to discharge time, positive ITP and CRM (+). The post-operative complications of the two groups were also analysed, including abdominal bleeding, chylous leakage, surgical-site infection (SSI), perineal incision healing, intestinal obstruction, pulmonary infection, deep-vein thrombosis, urinary retention, perineal pain and discomfort. Finally, the 2-year OS and 2-year LR were determined.
Statistical analysis
Data were analysed using SPSS 25.0 (SPSS Inc., Chicago, IL, USA). The normal distribution of the continuous data was tested by Shapiro–Wilk normality test and evaluated through an unpaired Student’s t-test. Qualitative data were expressed by rate, and the comparison between groups was analysed by the Chi-square test. Survival was determined using Kaplan–Meier analysis. P < 0.05 was defined as a statistically significant difference.
RESULTS
According to the inclusion and exclusion criteria, 55 LDAPR and 71 APR cases were selected. There were 55 males and 71 females. The average age of LDAPR and APR was 58.07 ± 12.19 and 58.11 ± 12.74 years, respectively. The median follow-up time was 36 months (range, 2–98 months). There was no significant difference in general data including the tumour location, distance from the anal verge, ASA scoring, pre-operative-T staging and pre-operative-N staging between the LDAPR and the APR groups [P > 0.05, Table 1].
Table 1.
General patient’s information
| LDAPR, n (%) | APR, n (%) | t/χ2 | P | |
|---|---|---|---|---|
| Gender, male | 20 (46.4) | 35 (49.3) | 2.110 | 0.147 |
| Age (year) | 58.07±12.19 | 58.11±12.74 | −0.018 | 0.986 |
| BMI (kg/m2) | 21.23±2.65 | 21.08±3.14 | 0.278 | 0.782 |
| Tumour location | ||||
| Back | 9 (16.4) | 8 (11.3) | 0.421 | 0.240 |
| Front | 8 (14.5) | 8 (11.3) | ||
| Right | 25 (45.5) | 26 (36.6) | ||
| Left | 13 (23.6) | 29 (40.8) | ||
| Distance from anal verge (cm) | 2.28±0.94 | 2.01±1.08 | 1.232 | 0.220 |
| Neoadjuvant therapy | ||||
| No | 45 (81.8) | 63 (88.7) | 1.210 | 0.271 |
| Yes | 10 (18.2) | 8 (11.3) | ||
| ASA scoring | ||||
| I | 29 (52.7) | 33 (46.5) | 0.508 | 0.776 |
| II | 18 (32.7) | 27 (38.0) | ||
| III | 8 (14.6) | 11 (15.5) | ||
| Pre-operative-T staging | ||||
| T1 | 15 (27.3) | 19 (26.7) | 3.690 | 0.158 |
| T2 | 15 (27.3) | 30 (42.3) | ||
| T3 | 25 (45.4) | 22 (31.0) | ||
| Pre-operative-N staging | ||||
| N0 | 27 (49.1) | 30 (42.3) | 2.580 | 0.275 |
| N1 | 25 (45.5) | 31 (43.7) | ||
| N2 | 3 (5.4) | 10 (14.0) |
APR: Abdominoperineal resection, LDAPR: Laparoscopic-dominant abdominoperineal resection, BMI: Body mass index, ASA: American Society of Anaesthesiologists
Only two patients in the LDAPR group had CRM (+), which was significantly lower than that in the APR group, as shown in Table 2. The number of positive ITP in the LDAPR group was also significantly lower than that in the APR group. There was no statistically significant difference in the operation time, intraoperative blood loss and post-operative hospital stay between the LDAPR and the APR group (P > 0.05).
Table 2.
Surgery data
| LDAPR, n (%) | APR, n (%) | t/χ2 | P | |
|---|---|---|---|---|
| CRM | ||||
| Positive | 2 (3.6) | 12 (16.9) | 5.522 | 0.019 |
| Negative | 53 (96.4) | 59 (83.1) | ||
| ITP | ||||
| Negative | 53 (96.4) | 61 (85.9) | 3.926 | 0.048 |
| Positive | 2 (3.6) | 10 (14.1) | ||
| Surgery time (min) | 138.53±15 | 147.82±30.31 | −1.785 | 0.077 |
| Blood loss (mL) | 51.45±25.49 | 56.62±28.63 | −1.053 | 0.294 |
| Post-operative hospital stay (day) | 6.45±1.21 | 6.66±1.25 | −0.934 | 0.352 |
APR: Abdominoperineal resection, LDAPR: Laparoscopic-dominant abdominoperineal resection, CRM: Circumferential resection margin, ITP: Intraoperative tumour perforation
In addition, all patients in both groups had a smooth recovery after the operation, and no deaths were reported, as shown in Table 3. There was no statistically significant difference in SSI, poor healing of the perineal incision, intestinal obstruction, pulmonary infection and deep-vein thrombosis between the LDAPR and APR groups (all P > 0.05). However, the LDAPR group had significantly lower urine retention and perineal pain compared to APR group (χ2 = 4.193, P = 0.041). We later made a 2-year analysis of OS and LR in both the LDAPR and the APR groups. According to our results, the LDAPR group demonstrated a significantly higher OS and LR than the APR group. (P < 0.05), as shown in Figures 1 and 2.
Table 3.
Post-operative complications
| LDAPR, n (%) | APR, n (%) | χ 2 | P | |
|---|---|---|---|---|
| SSI | ||||
| No | 44 (80.0) | 57 (80.3) | 0.002 | 0.969 |
| Yes | 11 (20.0) | 14 (19.7) | ||
| Perineal incision infection | ||||
| No | 50 (90.9) | 63 (88.7) | 0.159 | 0.690 |
| Yes | 5 (9.1) | 8 (11.3) | ||
| Intestinal obstruction | ||||
| No | 49 (89.1) | 65 (91.5) | 0.217 | 0.641 |
| Yes | 6 (10.9) | 6 (8.5) | ||
| Lung infection | ||||
| No | 52 (94.5) | 67 (94.4) | 0.002 | 0.965 |
| Yes | 3 (5.5) | 4 (5.6) | ||
| Deep-vein thrombosis | ||||
| No | 52 (94.5) | 66 (93.0) | 0.131 | 0.717 |
| Yes | 3 (5.5) | 5 (7.0) | ||
| Urinary retention | ||||
| No | 49 (89.1) | 53 (74.6) | 4.193 | 0.041 |
| Yes | 6 (10.9) | 18 (25.4) | ||
| Perineal pain (6 months after surgery) | ||||
| No | 15 (27.3) | 8 (11.3) | 5.320 | 0.021 |
| Yes | 40 (72.7) | 63 (88.7) | ||
| Perineal pain (1 year after surgery) | ||||
| No | 45 (81.8) | 41 (57.7) | 8.288 | 0.004 |
| Yes | 10 (18.2) | 30 (42.3) |
APR: Abdominoperineal resection, LDAPR: Laparoscopic-dominant abdominoperineal resection, SSI: Surgical-site infection
Figure 1.
Kaplan-Meier curve of two-year overall survival in the LDAPR and APR groups
Figure 2.
Kaplan-Meier curve of local recurrence in both the LDAPR and APR groups
DISCUSSION
Since the abdominal perineum combined with rectal resection (APR) was proposed in 1908, it has been used for 100 years as a standard surgical method to treat low rectal cancer.[10] The confluent plane of the abdominal perineum in APR surgery is at the levator ani hiatus, and the mesorectum is cut at the insertion point of the levator ani muscle so that the surgical specimen presents a narrow wasp waist shape in the lower part of the rectum [Figure 3a-c], which is called the surgical waist. The surgical waist is precisely the high incidence area of surgical perforation and CRM positive rate.[11,12] According to a previous report, an analysis of 373 APR surgical samples in the Dutch TME trial found 13.7% of ITP and a 30.4% rate of CRM (+) cases.[5] Almost similar observations were made by Marr[13] and Wibe et al.[14] These findings showed that positive CRM and high ITP are the independent risk factors for LR after APR.
Figure 3.
Demonstration of the APR surgery cut line. (a) MRI image (b) surgery picture (c) surgical specimen
In recent years, Holm et al.[6] reported a new surgical method for treating low rectal cancer, namely ELAPE combined with different levator ani. The surgical confluence plane is at the origin of the levator ani muscle. The levator ani muscle is completely removed, making the surgical specimen columnar, avoiding the formation of surgical waste, and reducing the positive rate of CRM and intraoperative perforation.[7] However, due to the extensive resection range, the complete resection of the levator ani muscle and the ischiorectal fossa fat makes perineal complications such as sexual dysfunction, urination dysfunction and chronic perineal pain and perineal hernia more complex than traditional APR surgery.[15] In addition, this combination surgery procedure involves a complex pelvic floor reconstruction technology and expensive an acellular dermal matrix patch, thus cannot be easily adopted in primary hospitals.
Our team evaluated the relevant evidence-based medical records and assessed the advantages and disadvantages of traditional APR and ELAPE surgery. We propose a new combined abdominal and perineal resection method, LDAPR with personalised levator ani resection. Different stages and positions are used to determine the resection range of the levator ani muscle, reducing the amount of perineal tissue resection while ensuring the safety of the incision margin [Figure 4a-c]. We retrospectively compared the clinical data of LDAPR and APR. The CRM (+) of the two groups was 3.6% versus 16.9%, (t = 5.522, P = 0.019), and the ITP was 3.6% versus 14.1%, (t = 3.926, P = 0.048), with statistical significance of P < 0.05. On the 2-year LR rate, LDAPR significantly reduced the LR rate compared to the APR treatment. Further, compared with APR, the LDAPR has obvious advantages in CRM (+) and ITP, similar to the results of several ELAPE studies.[7] LDAPR reduced CRM (+), ITP, 2-year LR and increased 2-year OS.
Figure 4.
Demonstration of the LDAPR surgery cut line. (a) MRI image (b) surgery picture (c) surgical specimen
The confluent plane of APR is at the insertion point of the levator ani muscle, and the operation of the perineum has a poor visual field. Once the bleeding is blindly clamped, it is easy to damage the pelvic nerve, resulting in urinary retention, perineal pain, sexual dysfunction and other related symptoms of pelvic nerve injury. ELAPE achieves oncological safety through extended resection, but its damage to the pelvic nerve is huge. Several studies have found that ELAPE can increase sexual dysfunction and urinary retention.[15,16,17] The symptoms of pelvic nerve injury are complex and diverse, and common manifestations include urinary retention, perineal pain and sexual dysfunction.
The incidence of urinary retention in LDAPR is significantly lower than that in APR (10.9% vs. 25.4%, χ2 = 4.139, P = 0.041), and perineal pain is significantly lower than APR at 6 months or 1 year after operation, with statistical significance of 72.7% versus 88.7%, (χ2 = 5.320, P = 0.021) and 18.2% versus 43.2%, (χ2 = 8.288, P = 0.004). LDAPR reduces the occurrence of urinary retention and perineal pain, which may be attributed to the reduction of levator ani muscle resection to avoid excessive resection and the protection of pelvic nerves under laparoscopic direct vision. International large-scale clinical trials have confirmed the application of the laparoscopic technique in rectal cancer in terms of the radical cure of the tumour and the safety of surgery.[18,19,20,21] Technically, laparoscopy requires less space for operation, enlarges the operative field and is more flexible in operating low rectal cancer radical resection. In addition, under laparoscopic direct vision, the levator ani muscle has a clear field of vision, blood vessels and nerves are visible, and the operation is accurate. Blind clamp resection of the perineal approach is avoided, which is more conducive to protecting pelvic vessels and autonomic nerves.
Since the implementation of LDAPR surgery in 2017, our team has found that individualised excision of the levator ani muscle under laparoscopic direct vision and avoiding the removal of the levator ani muscle through the perineal approach can reduce the damage to the nerve collateral caused by poor visual field.[22] Maximising the protection of the pelvic autonomic nerves related to urination and sexual function is also important in reducing the incidence of ITP and perineal complications. In addition, the confluent plane of the abdomen and perineum is reduced to the ischiorectal fossa fat, and the perineal surgery group can easily reach the same level as the abdominal group. In LDAPR, there is no need to change the surgical position.
The surgical process is simplified, and individualised excision of the levator ani can reduce the amount of perineal tissue resection, reduce the perineal defect and directly suture the pelvic floor to avoid pelvic floor reconstruction. Further, during the implementation of LDAPR, much attention should be paid to the following issues: There is no standard for how much the levator ani muscle should be removed, that is, the issue of safe incision margins. Our team cut off the tumour within T2 at 1.5 cm from the insertion point of the levator ani muscle. In the T3 stage, all the levator ani muscles are removed. Hence, it is unknown whether the scope can be further reduced.
Further studies should be done to clarify whether T0 tumour can further reduce the size of the levator, ani muscle resection. In this study, we did not close the pelvic floor peritoneum because of the risk of a hiatal hernia, but there may be a pelvic floor hernia if the pelvic floor peritoneum is not completed. Whether the pelvic floor peritoneum should be closed also deserves further investigation. Pre-operative accurate staging is the premise of individualised levator ani resection, which requires routine high-resolution MRI and intrarectal ultrasonography before LDAPR surgery is carried out to understand pre-operative staging and guide surgery accurately.
There are some limitations to this study. First, a single-centre retrospective study with a small number of cases in this study may affect the survey results to a certain degree. Second, this study only compared OS and LR 2 years after surgery and lacked long-term follow-up results. Further, we only studied perineal pain in pelvic autonomic dysfunction, which did not study sexual dysfunction.
CONCLUSION
LDAPR can effectively reduce the positive rate of CMR and ITP, minimise LR and simplify the operation of the perineum, which is beneficial to the protection of pelvic autonomic nerves. Consequently, adopting LDAPR is necessary for low rectal cancer surgery. However, more research remains necessary for the continuous improvement of LDAPR, and the long-term oncological effects require further follow-up exploration.
Ethics approval
The ethics committee of Zhangzhou Municipal Hospital Affiliated with Fujian Medical University approved this retrospective investigation.
Data availability
In the current investigation, if reasonably required, the corresponding author shall provide the data set and supporting materials generated and analysed during the study.
Consent for publication
All authors consent to the submission of this manuscript for consideration for publication.
Acknowledgement
Start-up funds for scientific research, Fujian Medical University (2018QH 1208).
Financial support and sponsorship
Start-up funds for scientific research, Fujian Medical University (2018QH 1208).
Conflicts of interest
There are no conflicts of interest.
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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
In the current investigation, if reasonably required, the corresponding author shall provide the data set and supporting materials generated and analysed during the study.