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Review
Colorectal cancer
 Essential knowledge and technical tips for total mesorectal excision and related procedures for rectal cancer
Min Soo Choorcid, Hyeon Woo Baeorcid, Nam Kyu Kimorcid
Annals of Coloproctology 2024;40(4):384-411.
DOI: https://doi.org/10.3393/ac.2024.00388.0055
Published online: August 30, 2024

Division of Colon and Rectal Surgery, Department of Surgery, Yonsei University College of Medicine, Seoul, Korea

Correspondence to: Nam Kyu Kim, MD, PhD, FRCS, FACS, FASCRS (Hon), FRSCRS (Hon) Division of Colon and Rectal Surgery, Department of Surgery, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea Email: namkyuk@yuhs.ac
This manuscript was written based on memorial lecture honoring the late Professor Kim Kwang-Yeon.
• Received: June 28, 2024   • Revised: July 13, 2024   • Accepted: July 24, 2024

© 2024 The Korean Society of Coloproctology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Total mesorectal excision (TME) has greatly improved rectal cancer surgery outcomes by reducing local recurrence and enhancing patient survival. This review outlines essential knowledge and techniques for performing TME. TME emphasizes the complete resection of the mesorectum along embryologic planes to minimize recurrence. Key anatomical insights include understanding the rectal proper fascia, Denonvilliers fascia, rectosacral fascia, and the pelvic autonomic nerves. Technical tips cover a step-by-step approach to pelvic dissection, the Gate approach, and tailored excision of Denonvilliers fascia, focusing on preserving pelvic autonomic nerves and ensuring negative circumferential resection margins. In Korea, TME has led to significant improvements in local recurrence rates and survival with well-adopted multidisciplinary approaches. Surgical techniques of TME have been optimized and standardized over several decades in Korea, and minimally invasive surgery for TME has been rapidly and successfully adopted. The review emphasizes the need for continuous research on tumor biology and precise surgical techniques to further improve rectal cancer management. The ultimate goal of TME is to achieve curative resection and function preservation, thereby enhancing the patient’s quality of life. Accurate TME, multidisciplinary-based neoadjuvant therapy, refined sphincter-preserving techniques, and ongoing tumor research are essential for optimal treatment outcomes.
  • Keywords: Total mesorectal excision; Rectal cancer; Pelvic anatomy
According to a World Health Organization (WHO) report, colorectal cancer ranks as the third most common cancer globally, accounting for about 10% of all cancer cases and is the second leading cause of cancer-related deaths worldwide [1]. In the United States, the incidence of rectal cancer was reported to be 44,180 cases annually in 2019 [2]. In Korea, rectal cancer is the third most common cancer and has the second highest incidence rate among all cancers. As of 2018, the annual incidence rate of rectal cancer was reported to be 44.5 cases per 100,000 people [3], which is considered high on a global scale, particularly in the age group of 50 to 69 years. Data analysis from 1990 to 2019 indicates that the incidence rate of rectal cancer has steadily increased. This rising trend is linked to the introduction of centralized screening programs, which have led to increased cancer detection through early diagnosis. The incidence rate of rectal cancer is expected to continue rising until 2024, due to the aging population and lifestyle changes. However, with effective prevention and early screening programs, the long-term incidence rate may decrease [4]
Historically, the treatment of rectal cancer was linked to low rates of anal sphincter preservation, along with substantial morbidity and mortality. Another significant challenge was the high rate of local recurrence, which drastically affected patients' quality of life until their death. The limited surgical field often resulted in blunt pelvic dissection, causing tears in the mesorectal fascia (MRF) and leaving behind parts of the mesorectum that could contain residual disease. These factors were major contributors to recurrence and diminished quality of life postsurgery.
The introduction of total mesorectal excision (TME) by Dr. Heald significantly transformed the surgical approach to treating rectal cancer. Before this development, local recurrence rates of rectal cancer were notably high, ranging from 30% to 38%, and were frequently accompanied by considerable rates of voiding and sexual dysfunction. In 1982, Heald et al. [5] identified that local recurrences were often due to residual tumor cell nests in the distal mesorectum. Heald underscored the importance of performing TME, which entails the complete removal of the distal mesorectum, to mitigate the risk of local recurrence.
One of our studies supports this hypothesis. Joh et al. [6] analyzed 72 rectal cancer patients to determine the presence of tumor deposits and metastatic lymph nodes in the distal mesorectum. They found metastatic lymph nodes in 7 patients and tumor deposits in 4 patients within the distal mesorectum, located 2 to 5 cm below the lower margin of the tumor. This finding was particularly significant in stage III patients, highlighting the importance of removing the distal mesorectum at least 5 cm below the tumor margin in cases of locally advanced rectal cancer.
Heald's theory, based on observations from 5 patients, identified small foci of adenocarcinoma in the mesorectum, several centimeters distal to the lower edge of the primary rectal cancer. He hypothesized that these residual tumor nests could lead to recurrences at the pelvic or suture line. In 1 case, a microscopic deposit was discovered in a lymphatic vessel 4 cm below the lower edge of the rectal cancer, even though there was no nodal involvement. Heald further observed that cutting the mesorectum too close to the tumor might result in the spillage of viable cancer cells. He also noted that the deep sacral curve could cause surgeons to cut obliquely across the mesorectum, potentially leaving behind tissue not only distal but also posterior to the tumor. This tendency to angle the dissection plane towards the rectal wall, both posteriorly and laterally, could increase the risk of local recurrence. To reduce these risks, Heald recommended routinely flushing the lumen below the clamp with water to prevent the implantation of viable cancer cells from the lumen. Following these practices in TME for rectal cancer, Heald reported a significant reduction in the local recurrence rate to 3.7% at 5 years. Additionally, the 5-year disease-free survival (DFS) rate reached 80%. These results were unprecedented, demonstrating a significantly lower local recurrence rate and improved survival outcomes [7].
These reports focused exclusively on surgical outcomes without incorporating adjuvant therapies. Heald highlighted the significance of precise pelvic dissection along anatomical planes, which led to a high rate of preserving sexual and voiding functions after rectal cancer surgery. In the United States, Enker et al. [8] also underscored the importance of meticulous anatomical pelvic dissection to improve oncologic outcomes and preserve the pelvic autonomic nervous system. They presented data on the safety and efficacy of low anterior resection in 681 consecutive cases at the Memorial Sloan Kettering Cancer Center (MSKCC). They reported an overall local recurrence rate of 7%, an actuarial 5-year overall survival (OS) rate of 81%, and a DFS rate of 75%. Furthermore, they analyzed oncologic outcomes based on whether patients received preoperative, postoperative, or no radiotherapy.
Subsequent studies on oncologic outcomes from Western countries, based on the TME principle, have shown local recurrence rates ranging from 4.5% to 7%. Cecil et al. [9] reported that TME leads to low local recurrence rates in lymph node-positive rectal cancer. Similarly, Wibe et al. [10] highlighted the effectiveness of TME in reducing local recurrence based on a national audit.
Heald emphasized the importance of completely removing the mesorectum and retracting it posteriorly to leave a muscle tube 2 to 3 cm above the pelvic floor. This technique results in a rectal reservoir that is entirely free of visceral tissue. Initially, there were concerns that TME might result in a high rate of anastomotic leakage. Although the concept has since evolved, it was a significant topic of debate in the academic literature at the time. In 1994, Karanjia et al. [11] reported on the leakage rates from stapled anastomoses after TME in a series of 276 consecutive patients treated between 1978 and 1992. Most leakage occurred in patients whose anastomotic sites were less than 6 cm from the anal verge, with a leakage rate leading to peritonitis of 17.4% (38 cases). Of these, 24 cases (11.0%) involved major leakage, and 14 cases (6.4%) involved minor leakage. They provided deep insights into the high rate of anastomotic leakage, noting that the reduced viability of the remaining anorectal tissue after TME was a contributing factor. He also observed instances of necrosis in the remaining rectum. We believe that the concern for local recurrence led to the complete removal of the distal mesorectum, regardless of tumor level, which might have been the original concept of TME several decades ago.
In contrast, several colorectal surgeons at MSKCC recommended transecting the rectum just above the levator ani muscles after completely removing the mesorectum in cases of low rectal cancer [12]. This was followed by a low pelvic anastomosis after the splenic flexure had been fully mobilized. For mid-rectal cancers, they preserved 2 to 3 cm of the rectal muscular tube. In cases of upper rectal cancer, the mesorectum and rectum were divided at right angles approximately 5 to 6 cm distal to the primary tumor, leaving the lowest part of the mesorectum as a vascular pedicle for the remaining rectum. They reported a local recurrence rate of less than 10% and an anastomotic leakage rate of less than 5%. The researchers recommended a tailored excision of the mesorectum based on the tumor's location, which has been shown to be safe in terms of oncological and postoperative outcomes.
Subsequently, Law and Chu [13] implemented a tailored excision of the mesorectum based on the tumor level. They reported that partial mesorectal excision for upper rectal cancer, maintaining a 4 to 5 cm mesorectal margin, could achieve oncologic outcomes comparable to those of TME, while also reducing the rate of anastomotic leakage.
At present, tailored mesorectal excision is regarded as the standard treatment, rather than the complete removal of the mesorectum. This method involves selectively removing the mesorectum depending on the tumor's proximity to the anal verge. In cases of upper rectal cancer, partial mesorectal excision is sufficient and does not compromise oncologic outcomes. For middle and low rectal cancers, however, complete excision of the mesorectum is necessary. This tailored approach is widely accepted and emphasizes the importance of precise dissection along the embryonic plane and achieving a negative circumferential resection margin (CRM).
Martling et al. [14] reported that surgical training through TME workshops significantly improved the quality of surgery and oncologic outcomes. Their study demonstrated that implementing a structured surgical training program led to better outcomes for rectal cancer patients.
Dr. Heald trained young surgeons worldwide through workshops and live demonstrations. In 2009, we invited him to Korea for the first time to deliver a lecture and conduct a live demonstration at our hospital during a TME workshop. Dr. Heald traveled globally, akin to an evangelist, conducting live TME workshops to improve rectal cancer surgical techniques and educate numerous surgeons.
We have hosted numerous expert surgeons, including Dr. Heald, for live TME demonstrations and discussions with young colleagues in Korea. We hope these efforts have contributed to the improvement of rectal cancer treatment in Korea.
In 1986, Quirke et al. [15] published a study that involved 52 patients with rectal cancer, using whole-mount sections. They found that 27% of these patients had positive CRM. Furthermore, among those with CRM involvement, 83% experienced local recurrence.
Nagtegaal and Quirke [16] conducted a comprehensive review of the role of CRM in the treatment of rectal cancer. They emphasized the significant prognostic impact of CRM, analyzing data from 17,500 patients. Their findings indicated that CRM involvement is a strong predictor of survival, distant metastasis, and local recurrence. CRM is typically considered positive if the margin is less than 1 mm. The study also detailed various types of CRM involvement, including direct tumor spread (28% to 29%), discontinuous tumor spread (14% to 67%), lymph node metastasis (12% to 14%), and venous or lymphatic invasion. They emphasized the importance of assessing CRM during the local staging of rectal cancer. In situations where the CRM is threatened, neoadjuvant therapy should be considered, requiring collaboration among radiation oncologists, medical oncologists, and radiologists.
At Severance Hospital (Seoul, Korea), rectal cancer patients with positive CRM experienced a local recurrence rate of 23.5%, which is more than double the rate of 11.3% observed in those with negative CRM. Additionally, the 5-year cancer-specific survival rate was significantly lower in the group with positive margins. Positive CRM was identified as an independent prognostic factor for recurrence [17].
To date, CRM is recognized as an independent prognostic factor for local recurrence and survival in rectal cancer. CRM is defined as the shortest distance between the tumor and the resection plane. To measure this accurately, many centers adopt Quirke’s protocol, which involves using whole-mount sections for TME specimens. This technique requires microtomes equipped with mega cassette clamps and specialized technical training [15]. This method has also been implemented in collaboration with the pathologist Hoguen Kim [18]. The study evaluated the predictive accuracy of CRM measurements using preoperative magnetic resonance imaging (MRI) and whole-mount sections in mid-rectal cancer, highlighting the importance of different scan planes.
In Korea, most hospitals assess CRM using conventional sections. This technique involves arranging small tissue blocks oriented as anterior, posterior, right/left lateral, or in square configurations. Recently, Giner et al. [19] reported intriguing results from a comparison of CRM assessment accuracy between whole-mount and conventional sections. Their study found no difference in CRM values between the 2 methods.
It remains critically important to report the status of the CRM in the final histopathology of TME specimens in rectal cancer. This information is crucial for assessing the completeness of the surgical resection and for predicting the patient's prognosis, as a positive CRM significantly predicts local recurrence and OS. Accurate assessment of the CRM can inform subsequent treatment decisions, including whether adjuvant therapy is necessary.
We once attended a pathology lecture at our university given by Professor Nagtegaal. She was the first to report the importance of TME completeness. She established the criteria for complete, nearly complete, and incomplete resections, explaining that patient prognosis varies according to these criteria.
A complete TME is characterized by an intact mesorectum with only minor irregularities and no narrowing toward the distal resection margin. A nearly complete TME exhibits irregularities on the mesorectal surface and slight conning down, but no visible muscle layer is exposed. An incomplete TME, however, has defects that extend deep to the muscle layer and a very irregular mesorectal surface. Although there were no significant differences in overall recurrence between complete and nearly complete TME procedure, there was a significantly higher risk of overall recurrence after incomplete TME [20]. Nagtegaal et al. [20] also highlighted the clinical significance of the pathologist in quality control through the macroscopic evaluation of rectal cancer resection specimens. Their study emphasized the importance of this assessment in ensuring the completeness of TME, presenting criteria for complete, nearly complete, and incomplete resections. In 2009, Enker and Levi [21] further underscored the importance of macroscopic assessment of TME specimens and stressed the need for standardized descriptions that allow for the comparison of clinical outcomes across centers and trials. Additionally, García-Granero et al. [22] assessed 359 rectal cancer TME specimens and classified them as complete, nearly complete, and incomplete. Their study found a statistically significant difference in local recurrence rates between complete and non-complete TME, with the worst prognosis observed in cases with positive CRM and non-complete TME.
Over time, TME, along with autonomic nerve preservation and anal sphincter preservation, has become widely accepted and is now considered the standard surgical management for rectal cancer in Korea. Consequently, both oncologic and functional outcomes have improved dramatically, including a significant increase in sphincter preservation rates.
Update on treatment strategy
The management landscape of rectal cancer has undergone significant evolution, marked by the integration of total neoadjuvant therapy (TNT) and advancements in imaging technologies. These developments have transformed preoperative planning by improving the visualization of the rectum and surrounding structures, thereby enabling more accurate assessments of CRM involvement. As a result, alternative treatment strategies are being explored, aiming to standardize rectal cancer management. The goal is to achieve exceptionally high tumor control while minimizing surgical interventions or adopting nonoperative management approaches.
At the National Cancer Institute Consensus Conference in 1990, postoperative chemoradiotherapy (CRT) was recommended for patients with stage II and III rectal cancer to reduce local recurrence. Subsequently, the German Rectal Cancer Study Group demonstrated that preoperative CRT yielded superior outcomes compared to postoperative CRT in advanced rectal cancer. Sauer et al. [23] reported that preoperative CRT not only resulted in a lower rate of local recurrence (6% vs. 13%) but also reduced the rate of acute toxicity; however, it did not improve OS. Additionally, preoperative CRT enhanced the rate of anal sphincter preservation. Nevertheless, there were no differences in rates of distant metastasis and 5-year survival between the preoperative and postoperative CRT groups. Preoperative CRT also proved superior to postoperative CRT in terms of treatment compliance, toxicity, downstaging, and sphincter preservation in patients who were candidates for abdominoperineal resection (APR), as well as in achieving 5-year local control. In 2012, a follow-up study on the same patient cohort over an 11-year period was published. Sauer et al. [24] found that the significant improvement in local control with preoperative CRT compared to postoperative CRT persisted, but it still had no effect on OS.
However, we have observed that some patients with locally advanced rectal cancer, despite showing a positive response in the primary tumor, experienced disease progression after receiving preoperative long-course CRT. The liver and/or lungs were the most common sites of metastasis. These findings suggest that such patients may not be suitable candidates for upfront TME or conventional preoperative CRT [25].
The case involved locally advanced rectal cancer with invasion into adjacent structures, including the seminal vesicle and levator ani muscle. High-risk factors, such as extramural vascular invasion, were also noted. Additionally, the patient exhibited an elevated serum carcinoembryonic antigen level. Given these circumstances, conventional preoperative CRT may not be sufficient for adequate treatment (Fig. 1).
TNT has received increasing attention for the treatment of advanced rectal cancer. Clinical trials, including RAPIDO (Rectal Cancer and Preoperative Induction Therapy Followed by Dedicated Operation) and PRODIGE 23 (Partenariat de Recherche en Oncologie Digestive 23), have demonstrated enhanced local control and improved survival rates in patients with locally advanced rectal cancer. The RAPIDO trial revealed that a regimen of short-course radiotherapy followed by chemotherapy before TME significantly enhanced local control compared to the conventional method of preoperative CRT, TME, and optional adjuvant chemotherapy [26]. Although the RAPIDO trial initially reported significant improvements, such as a notable reduction in disease-related treatment failure at the 3-year follow-up and a doubling of the pathologic complete response rate, the subsequent 5-year follow-up data were less encouraging. Dijkstra et al. [27] noted that the experimental arm, which involved short-course radiotherapy followed by chemotherapy, was linked to an increased risk of local recurrence, reaching up to 10%, versus 6% in the standard long-course CRT. The predominant patterns of local recurrence occurred in the presacral and anastomotic areas. Riou et al. [28] suggested that these outcomes could be attributed to suboptimal radiotherapy in the experimental arm. The PRODIGE 23 trial showed that neoadjuvant chemotherapy with FOLFIRINOX (oxaliplatin 85 mg/m2, irinotecan 180 mg/m2, leucovorin 400 mg/m2, and fluorouracil 2,400 mg/m2 intravenously every 14 days for 6 cycles) followed by preoperative CRT led to better patient outcomes than the standard treatment protocol [29].
Fokas et al. [30] reported long-term results from a randomized phase 2 trial of CAO/ARO/AIO-12 (Chemoradiotherapy Plus Induction or Consolidation Chemotherapy as Total Neoadjuvant Therapy) trial, which investigated CRT in combination with either induction or consolidation chemotherapy as TNT for locally advanced rectal cancer. The chemotherapy regimen included 3 cycles of fluorouracil, leucovorin, and oxaliplatin administered before and after fluorouracil/oxaliplatin CRT (50.4 Gy). The findings indicated that CRT followed by chemotherapy led to a higher pathologic complete response, without adversely affecting DFS, toxicity, quality of life, or stool incontinence. The authors recommended this sequence as the preferred approach for TNT when organ preservation is a priority.
While neoadjuvant and adjuvant therapies have evolved, it is crucial to emphasize that curative surgical treatment remains the cornerstone of managing rectal cancer. The responsibility of performing curative surgeries while preserving function rests heavily on surgeons. Although TME is the most critical surgical principle, it is equally important to identify factors that may lead to postoperative recurrence and to initiate various neoadjuvant treatments when these factors are present. The concepts of preoperative CRT and the currently emerging TNT stem from this understanding. Currently, numerous risk factors identified through preoperative rectal MRI are being extensively studied. Recognizing these risks is vital for developing effective treatment strategies.
High-resolution rectal MRI has been shown to correlate with pathological and oncologic outcomes, facilitating risk stratification in the selection of high-risk rectal cancer patients. Key features assessed include MR CRM involvement, extramural tumor spread, mesorectal nodal status, lateral pelvic lymph node metastasis, and extramural vascular invasion [31].
The risk stratification system has been a cornerstone for minimizing the morbidity associated with overtreatment and for planning aggressive interventions for high-risk patients. Preoperative CRT and TNT have been implemented based on this MRI-based risk stratification approach.
Basic anatomy
In a review article, the critical importance of sharp pelvic dissection for rectal cancer surgery was emphasized, particularly in the context of TME, while ensuring the preservation of the pelvic autonomic nerve system [32]. The deep pelvis is a concave, curved tunnel characterized by a narrow bony space and is surrounded by urogenital structures and a neurovascular bundle (NVB). Achieving a complete cylindrical-shaped TME specimen while preserving the pelvic autonomic nerve system poses significant challenges due to the narrow confines, surrounding organ structures, and limited visibility. Key technical tips include implementing space-making procedures and following a precise sequence of operative steps. Just as maritime navigation has transitioned from relying on astronomical observations to utilizing global positioning system (GPS), our goal is to refine surgical navigation methods to achieve optimal outcomes in rectal cancer surgery. Advances in imaging and individualized treatment strategies are reshaping rectal cancer surgery. Concepts such as customized Denonvilliers fascia (DVF) excision, navigating the complexities of the lower rectum, and employing techniques such as the Gate approach enable surgeons to tailor the surgical approach more effectively.
The anatomy of the mesorectum
The mesorectum contains blood vessels, lymphatics, and lymph nodes, and is enveloped by the thin, shiny MRF, which is composed of collagen fibers. The posterolateral part of the mesorectum is the thickest, while the anterior part is the thinnest (Fig. 2). Approximately 2 cm above the levator ani muscle, the mesorectum is nearly absent, leaving only the rectal wall at this level (Fig. 3). Although numerous effective combined upfront treatments have been established, achieving curative resection remains the most critical goal in the treatment of locally advanced rectal cancer. In this context, we describe the anatomical structures necessary for safe and effective oncologic and functional surgery for rectal cancer. The rectum and mesorectum are located in the curved, concave pelvic cavity within the retroperitoneal space, except for the anterior part of the upper rectum. For curative resection of rectal cancer, achieving clear proximal and distal margins is essential, similar to resections of other solid organ cancers. In rectal cancer, the CRM is particularly important. A positive resection margin is strongly associated with local and systemic recurrence, leading to poor oncologic outcomes.
Gimbap, a popular takeaway food in Korea, serves as a useful analogy to illustrate the importance of complete TME. Gimbap consists of rice and vegetables wrapped in seaweed, which is then sliced. Mishandling the outer seaweed can cause the inner contents to spill out, just as incomplete TME can lead to the spread of cancer cells and recurrence (Fig. 4) [33]. This analogy highlights the critical need to maintain the integrity of the MRF to prevent the dissemination of cancer cells and ensure successful surgical outcomes.
The pelvic fascia
Understanding and identifying the fascial planes around the rectum and adjacent organs is crucial for achieving sharp pelvic dissection along embryological planes. Proper dissection along these planes enables a bloodless operation and is essential for optimal oncologic outcomes while preserving anal, urinary, and sexual functions. Recognizing the perirectal fascia and their corresponding interfaces is mandatory for successful TME. This knowledge is also fundamental for procedures such as APR, intersphincteric resection (ISR), transanal TME (TaTME), and lower anterior resections for rectal cancer.
Bisset and Hill [34] described a fibrous envelope surrounding the perirectal fat, known as the mesorectum, and named it the fascia propria. Typically, nerve structures are not visible unless the fascia covering bony structures and muscles is opened. At the S4 level, relatively dense connective tissue is encountered between the presacral fascia and the rectal proper fascia [35].
This fascia is referred to as the rectosacral fascia or Waldeyer fascia. Crapp and Cuthbertson [36] emphasized its clinical importance, stating that not recognizing and dividing it may lead to hemorrhage from the presacral venous plexus.
The thickness of this fascia varies among individuals. In cases where it is thick, blunt dissection by hand may lead to avulsion injuries of the presacral venous system. After sharp division of this fascia, posterior dissection can proceed down to the coccyx and pelvic floor. DVF, a dense connective tissue layer, is located at the anterior part of the rectum and becomes visible after the anterior peritoneal reflection near the seminal vesicle is opened. Denonvilliers originally described it as a membrane positioned behind the seminal vesicle and in front of the rectum. Its texture can vary from a thin, transparent layer to a tough, thick membrane. It tends to be more pronounced in young male patients and consists of dense collagen fibers and coarse elastic fibers. There is ongoing debate about whether to perform anterior or posterior dissection of DVF, concerning both oncologic and functional safety. In this discussion, we will describe each aspect of the individual pelvic fascia in detail (Fig. 5) [34].
The MRF, also referred to as the rectal proper fascia, encapsulates the mesorectum. It is crucial for establishing a dissection plane that separates the rectum from surrounding tissues, which helps preserve oncological margins and prevents damage to adjacent structures. The presacral fascia, another significant anatomical structure, covers the sacrum and serves as a barrier. During dissection, careful navigation is required to avoid damaging critical nerves and to minimize hemorrhage. A thorough understanding of these fascial planes is essential for effective surgical dissection. Waldeyer fascia, a dense connective tissue, is located between the rectal proper fascia and the presacral fascia at the S3 and S4 vertebral levels (Fig. 6) [35]. In the deep, concave, and narrow pelvic cavity, the presacral fascia not only covers the sacrum and the presacral venous system but also fuses with the MRF. Tearing this fascia can lead to the avulsion of the presacral fascia and significant presacral venous bleeding. During open TME, manual dissection in this area often results in severe bleeding, requiring the use of surgical tape packing and compression to achieve hemostasis. Additionally, Waldeyer fascia may be absent in a small percentage of patients. In one study, Waldeyer fascia was observed at the S2 level in 15% of cases, at the S3 level in 38% of cases, and at the S4 level in 46% of cases [37].
DVF is encountered during anterior pelvic dissection in males at the level of the seminal vesicles. This fascia serves as an important landmark to ensure both oncologic and functional safety. It has an apron-like shape, forming an inverted triangle. At the level of the seminal vesicles and prostate, NVBs from the pelvic plexus run to the genitalia at the 10 and 2 o’clock positions outside the DVF. These bundles, which are critical to sexual function, are located posterolaterally to the seminal vesicles and prostate and posteri­or to the DVF. He et al. [38] noted that the DVF consists of numerous fibers that merge with the connective tissue of the pelvic wall and partially insert into nerve branches emerging from the pelvic plexus. Additionally, Muraoka et al. [39] reported that the lateral extension of the DVF varies, sometimes connecting with the lateral pelvic fascia and NVB or moving anteriorly along the prostate capsule. This indicates that its anatomical presentation varies both among sites and individuals.
There is ongoing debate about whether the DVF is a monolayer or a multilayer structure. Based on my observations and perspectives, we argue that it consists of multiple tissue layers. Supporting this view, previous histological studies on cadaver specimens have shown that the DVF is not a single layer but comprises multiple layers. These studies also reveal that the DVF is loosely connected to the seminal vesicles, yet it has a dense attachment to the prostate, extending down to the perineal body. The NVBs, which are crucial for sexual function, run alongside the seminal vesicles and prostate, positioned at the 10 and 2 o’clock directions outside the DVF. This anatomical configuration highlights the importance of recognizing the multilayered structure of the DVF for ensuring both oncologic and functional safety during pelvic dissection (Fig. 7) [40, 41].
Pelvic autonomic nervous system
The superior hypogastric nerve descends to form a plexus near the origin of the inferior mesenteric artery. This plexus forms a dense network around the artery. Therefore, there is a risk of damaging the superior hypogastric nerve during lymph node dissection or ligation at the root of the inferior mesenteric artery. The inferior hypogastric nerve descends into the pelvis, crossing the left common iliac artery at the level of the first sacral vertebra, and continues along the pelvic sidewall. It is essential to preserve the superior hypogastric nerve plexus when separating the rectosigmoid colon from the gonadal vessels and ureters. Pelvic dissection should adhere to the plane between the inferior hypogastric nerve fibers and the rectal proper fascia within the pelvic cavity. The inferior hypogastric nerve joins with the parasympathetic sacral nerves originating from the 2nd, 3rd, and 4th sacral foramina to form the pelvic plexus at the lateral pelvic wall. Numerous small NVBs, extending from the pelvic plexus to the genitalia, cross the seminal vesicles at the 10 and 2 o’clock positions. During cadaveric dissection, Y-shaped pelvic autonomic nerve structures are clearly visible in the hemipelvis, underscoring the complex anatomy and the necessity for precise surgical navigation to preserve these vital nerve pathways (Fig. 8) [35, 41].
The inferior hypogastric nerves descend along each side of the pelvic wall, forming mesh-like structures that are densely attached to the lateral part of the MRF, historically known as the lateral ligament. Gentle mobilization of the rectum's lateral wall and preservation of the pelvic plexus are crucial for maintaining voiding and sexual functions after surgery. Proper management of these nerves and structures is essential for the success of pelvic dissections, ensuring both oncologic safety and the preservation of vital functions.
Pelvic floor
The pelvic floor is a wide sheet of muscle that stretches across the inner surfaces of the bony pelvis. It comprises the ischiococcygeus muscle, the iliococcygeus muscle, and the pubococcygeus muscle (Fig. 9).
The well-known puborectalis muscle, part of the pubococcygeus muscle, plays a crucial role in reinforcing the external anal sphincter (EAS) and forming the anorectal angle, both of which are vital for fecal continence. The levator ani muscle, an essential component of the pelvic floor, receives innervation from the levator ani nerve, which originates from the 3rd and 4th sacral nerves, as well as branches from the pudendal nerve. Variations in the structure and function of the pelvic floor can be observed in coronal axis views from rectal MRI, influenced by factors such as sex and body mass index. In dissections, the U-shaped puborectalis muscle is clearly visible, recognized for its role in maintaining fecal continence by creating a sharp anorectal angle. This funnel-shaped structure typically attaches to the mesorectum and its surrounding fascia. When the mesorectum is completely mobilized from the pelvic floor, structures such as the anococcygeal raphe and the anal hiatus are revealed. During TME, a thorough understanding of pelvic floor anatomy is imperative. This knowledge becomes particularly crucial when the resection involves the levator ani muscle, as it is essential for ensuring a successful surgical outcome (Fig. 10) [42].
Even with successful TME, achieving a curative resection for rectal cancer within the surgical anal canal requires careful consideration of several factors. It is also crucial to accurately determine the indications for APR and ISR to ensure a truly curative resection. If a tumor is located below the anorectal ring, as determined by transrectal ultrasound, sigmoidoscopy, and rectal MRI, and is confined to the internal anal sphincter (IAS) without extending beyond it or invading the EAS, combined excision of the involved IAS can achieve an R0 resection while preserving the EAS and levator ani muscle. However, if the low-lying rectal cancer involves the EAS and/or the levator ani muscle, APR is indicated (Fig. 11). One reason for the historically poor prognosis of APR was the high rate of positive CRM. Therefore, if distal rectal cancer involves the levator ani muscle, this muscle must be excised to avoid a positive CRM. A thorough understanding of pelvic floor anatomy is essential for this procedure. En bloc resection of the pelvic floor and MRF is necessary to obtain a cylindrically shaped specimen. Without a complete understanding of pelvic floor anatomy, excision of the levator ani muscle and its origin can be challenging, potentially leading to inadequate resection. This aspect of the procedure goes beyond standard TME; instead, it involves complete TME along with total excision of the pelvic floor, which is vital for achieving an R0 resection in cases of distal rectal cancer involving the pelvic floor. Performing the procedure with the patient in the jackknife position can improve visibility and facilitate access to the expanded levator ani muscle, which is why some surgeons prefer this position during the perineal dissection of APR. However, I believe that transabdominal division of the levator ani muscle can be effectively accomplished through a robotic approach after TME, even with the patient in the lithotomy position. This technique enables complete excision of the levator ani muscle.
During ISR and coloanal anastomosis (CAA), it is essential to ensure that the longitudinal muscle of the rectum is well separated from the surrounding levator ani muscle. Additionally, a thorough understanding of the intersphincteric groove and intersphincteric plane is crucial. The anal canal features a cylindrical double-layered structure. The inner layer is composed of the IAS and the conjoined longitudinal muscle, both of which are innervated by the autonomic nervous system. The outer layer includes the puborectalis muscle and the EAS, innervated by somatic nerves. The groove between the IAS and EAS is easily palpable and serves as an important landmark for ISR (Fig. 12).
The intersphincteric approach involves accessing the transanal area and proceeding to the surgical anal ring, where the puborectalis muscle is situated. My histological observations indicate that the attachment of the rectum to the levator ani muscle consists of intermingled smooth and skeletal muscle fibers. The conjoined longitudinal muscle, outer longitudinal muscle, and puborectalis muscle are intertwined, requiring a comprehensive understanding of the topographic anatomy for effective detachment (Fig. 13).
Tsukada et al. [43] observed variations in the length of the attachment of the longitudinal muscle to the levator ani muscle, noting that the anterolateral attachment is longer than the posterior attachment, which is the shortest. Typically, an ISR specimen includes the IAS and conjoined longitudinal muscle, which are separated from the levator ani. The detachment process starts posteriorly, proceeds laterally, and finishes with the most extensive anterolateral detachment from the levator ani muscle and adjacent structures. During this procedure, it is critical to carefully separate the rectum from anterior structures such as the urethra, rectourethralis muscle, vagina, or prostate. A thorough understanding of these anatomical relationships is essential for the successful execution of ISR (Fig. 14) [44].
During APR, once the TME is completed through a transabdominal approach, the perineal dissection can begin. This phase of the procedure is associated with several risks, including the possibility of rectal perforation and urethral injury. Planellas et al. [45] found that urethral injuries occurred in 0.73% of cases in their clinical series. This incidence rose to 1.64% among high-risk patients, particularly men with middle and distal rectal cancer. A technique-specific analysis showed that urethral injuries occurred in 3.2% of cases undergoing TaTME and in 4% of cases undergoing APR. To minimize the risk of urethral injuries, a thorough understanding of anatomical landmarks is imperative.
The rectourethralis muscle serves as an important anatomical landmark for avoiding complications such as urethral injury, especially during procedures like APR and ISR. This muscle originates on the anterior surface of the rectum and inserts into the perineal body. Positioned posterior to the urethra, anterior to the rectal wall, and lateral to the levator ani muscle, the rectourethralis muscle has a Y-shaped appearance. Its arms extend into the rectal wall and attach to both the levator ani and the perineal body. The urethral sphincter and the rectourethralis muscle are approximately 1 cm apart, and the muscle's thickness varies from 2 to 10 mm [46]. Previous anatomical studies have traced the path of the DVF to the perineum, ending at the rectourethralis muscle. Understanding these anatomical relationships is essential for minimizing the risk of urethral injury during pelvic surgery [47].
During APR or ISR procedures, the most effective way to prevent urethral injury is to identify and meticulously dissect around the rectourethralis muscle. By carefully dissecting posterior to the DVF until reaching the prostate level (via the transabdominal approach), the integrity of the rectourethralis muscle is preserved, keeping it separate from both the urethra and rectum (via the transperineal approach). This precise dissection delineates the DVF's pathway to the perineum and its endpoint at the rectourethralis muscle. Soga et al. noted that the DVF concludes at the rhabdosphincter and the apical portion of the rectourethralis muscle, indicating that the DVF acts as a landmark for a safe pelvic dissection plane [48]. This termination point significantly increases the chances of preserving the NVB during transabdominal pelvic dissection in the lower pelvis. Additionally, it facilitates the preservation of the urethra and urethral sphincter muscle during ISR or APR via the transanal approach, as the dissection remains posterior to the DVF. Understanding these anatomical relationships is essential for minimizing the risk of urethral injury and achieving successful outcomes in pelvic surgery (Fig. 15).
The management of tumors within the surgical anal canal and the preservation of the rectourethralis muscle are complex aspects of rectal cancer surgery. These procedures demand a careful balance of the tumor's location, size, and its relationship with adjacent structures to determine the most suitable surgical approach. Achieving optimal oncologic outcomes while preserving the patient's quality of life requires meticulous surgical planning and execution.
The sequence of pelvic dissection
We believe that the sequence of pelvic dissection is crucial for obtaining a complete TME specimen in the deep, concave, and narrow pelvis. This task is not akin to driving on a long, straight road; it is more comparable to navigating a winding path with numerous elevations and depressions. Just as careful attention to signposts and safe driving are necessary to reach a destination, it is equally important to meticulously follow anatomical landmarks to ensure successful surgical outcomes. For a complete TME, understanding how to access the embryologic plane using these landmarks is essential. It is also critical to recognize potential danger zones that could lead to nerve damage or inadvertent breaches of the MRF. Therefore, we propose a step-by-step pelvic dissection procedure. Given the limited space, a systematic and sequential approach is necessary to create sufficient room for the subsequent steps of deep pelvic dissection. This method is the most effective way to avoid tearing the MRF, damaging adjacent structures, including the nervous system, and preventing positive CRM. We have outlined a 7-step approach for proper rectal mobilization (Fig. 16) [49–51].
The mesosigmoid colon and sigmoid vascular pedicles were retracted to expose the underlying retroperitoneal structures. Subsequently, the inferior mesenteric vein was retracted, and an incision was made to separate the inferior mesenteric vein and mesentery from these structures while preserving the gonadal vein and ureter. My preferred approach for dissection is medial to lateral. Following the mobilization of the sigmoid colon and mesentery, a dissection from lateral to medial was carried out to fully mobilize the mesosigmoid colon.

Step 1. Incision of the parietal pelvic peritoneum

The first step involves making an incision in the parietal pelvic peritoneum at the sacral promontory. This area provides visibility of the iliac vessels, ureter, and superior hypogastric nerve plexus. Careful dissection of the superior hypogastric nerve from the mesosigmoid is performed, followed by retraction toward the iliac vessels and retroperitoneal structures. Sharp dissection continues to the left side, exposing the left common iliac vessel, gonadal vessel, and left ureter. The approach is then directed toward the root of the inferior mesenteric artery, with careful efforts to preserve the superior hypogastric nerve plexus, which originates from the preaortic sympathetic trunk (T10–L3).

Step 2. Posterior dissection

Posterior pelvic dissection is conducted along the rectal proper fascia, which encases the mesorectum and rectum, while preserving the inferior hypogastric nerve adjacent to the pelvic sidewall. This dissection generally follows an avascular plane and extends to the rectosacral fascia. In situations where there is a prominent promontory, the laparoscopic instruments inserted through the standard working port may not reach the end of the pelvic floor.

Step 3. Anterior dissection

When dissecting the anterior region, the seminal vesicle in men or the vaginal wall in women is typically encountered first. At this point, a white, membrane-like structure known as the DVF becomes visible. The preferred plane for dissection is posterior to the DVF, unless the tumor is situated anteriorly. It is crucial to avoid a positive CRM, as the mesorectum anteriorly is notably thin.

Step 4. Deep posterior dissection

At this point, the rectum is anatomically positioned concavely along the curve of the sacrum, bordered by the ischial tuberosity and iliac wing, which define the limits of the pelvic cavity. The space at the anorectal junction is restricted, complicating the acquisition of an adequate surgical view. A curvilinear transverse incision is made close to the rectal proper fascia in the rectosacral fascia, while the mesorectum is held under upward traction. Continuing the dissection after the division of the rectosacral fascia exposes the presacral venous plexus, which is shielded by the parietal pelvic fascia. Constant and careful traction is essential, and blunt dissection should be avoided to prevent partial tears and bleeding from the presacral venous plexus.

Step 5. Deep anterolateral dissection

Deep anterolateral dissection presents significant challenges in a narrow pelvis. When the DVF is encountered, dissection should continue posterior to the DVF to reveal the NVB at the anterolateral aspect of the seminal vesicle. Further dissection facilitates the creation of an avascular plane between the MRF and the NVB, achieved under gentle traction of the rectum and seminal vesicle. At the 2 o’clock position on the right side, the NVB is located, providing access to the anterolateral portion of the lower rectum, which serves as the entry point to the deep pelvic floor. As the deep anterolateral dissection progresses to the pelvic floor muscles, complete separation of the MRF from the underlying pelvic floor is achieved. On the lateral aspect of the pelvic wall, both the pelvic plexus and the NVB should be considered. Further deep anterior dissection posterior to the DVF, extending beyond the seminal vesicle, facilitates easy separation from the DVF covering the prostate gland, minimizing the risk of bleeding.

Step 6. Deep posterolateral dissection

Following the deep anterolateral dissection, the next step involves a deep posterolateral dissection, which exposes the anococcygeal ligament and pelvic floor. This region includes connections between the pelvic plexus and the MRF, necessitating gentle traction. Once the step-by-step procedure is completed, this area is well exposed, allowing for the safe dissection of the MRF from the pelvic plexus. Occasionally, the middle rectal artery may be encountered and can be managed appropriately. The NVB, which was retracted at the 11 and 2 o’clock positions following the deep anterolateral dissection, is already exposed. The exposure of the anococcygeal ligament is now complete. Although the division of the anococcygeal ligament is sometimes debated, it may be necessary for the complete mobilization of the rectum and facilitates the transection of the rectum flush with the anal canal.

Step 7. Identification of the pelvic floor

After the anococcygeal ligament is divided, the levator ani muscle becomes visible. The MRF is connected to the underlying pelvic floor, necessitating meticulous dissection. Following the separation of the mesorectum from the pelvic floor, and elevating the rectum, the lower rectum can be seen clearly without the mesorectum. Dissecting down to the pelvic floor is crucial for achieving an adequate distal resection margin in cases of middle and distal rectal cancer. An endostapler may then be used along the predetermined transection line of the rectum. At this point, the rectum and mesorectum have been fully mobilized circumferentially from the surrounding pelvic anatomical structures and associated fascia.
In summary, to preserve voiding and sexual function while achieving optimal TME, it is essential to adopt a sequential approach that includes posterior, anterior, and lateral dissections, with a deep understanding of the fascial structures involved. The most effective technique for achieving a cylindrical-shaped complete TME is to dissect along the embryonic fascia-to-fascia plane. We want to highlight the significance of deep anterolateral dissection. Once the posterior and anterior dissections are complete, the deep anterolateral dissection should commence from the previously established plane of the DVF. Below the prostate, the rectal wall, DVF, and the fascia covering the NVBs are fused together. Employing the Gate approach allows for clear visualization of the pelvic plexus, thus providing ample space for the surgical procedure. We strongly believe that initiating the procedure with posterior and anterior dissections, followed by deep anterolateral dissection, not only simplifies the separation from the surrounding fascial structures but also creates the necessary space for complete rectal mobilization.
Gate approach
The proposed Gate approach is defined by anatomical boundaries, specifically where the MRF that surrounds the distal mesorectum attaches to the pelvic floor. It is essential to perform a careful and meticulous dissection of the MRF from the funnel-shaped pelvic floor to ensure the integrity of the mesorectum. The technique involves dissection in the anterolateral part of the TME, starting either at the seminal vesicle or the lateral side of the vagina, and extending to the lateral part of the mesorectum. The dissection continues deeply until it reaches the pelvic floor, effectively creating a clear and accessible gateway between the MRF and the pelvic floor. Additionally, this method includes a posterolateral dissection that leaves the lateral part of the mesorectum suspended like a bridge. This configuration facilitates the dissection process while preserving the integrity of the pelvic plexus (Fig. 17) [51, 52]
Based on our observations, we suggest that the Gate approach could be particularly beneficial in cases where a rectal MRI sagittal view shows an extended anterior dissection line, along with a narrow pelvic outlet (short distance between the pubic bone and coccyx), or in cases where posterolaterally located rectal cancer is fixed to the MRF and surrounding parietal pelvic fascia.
Customized DVF excision
During anterior pelvic dissection, encountering the DVF is significant for 2 main reasons: preserving sexual function and ensuring a curative resection. In cases of anterior rectal wall cancer, the mesorectum is thin, which increases the risk of a positive CRM. Therefore, careful dissection in this area is crucial for avoiding complications and achieving optimal surgical outcomes. If a tumor invades the anterior rectal wall and penetrates the mesorectum, exposing the anterior part of the rectum after incising the anterior peritoneum is challenging due to the acute angle involved. Another concern is the high incidence of positive CRM because the anterior mesorectum is usually thin. Understanding the topographic anatomy of the DVF is clinically important for both oncologic and functional outcomes in the surgical treatment of rectal cancer. After incising the anterior peritoneal reflection and exposing the seminal vesicle or vagina—particularly near the seminal vesicle in men—the DVF can be identified. It is crucial to determine whether anterior or posterior dissection of the DVF is more optimal for rectal cancer surgery to ensure better oncologic and functional outcomes. Anteriorly located rectal cancer tends to have poorer oncologic outcomes than laterally or posteriorly located rectal cancer. Lee et al. [53] reported that locally advanced anteriorly located rectal cancer in men exhibited a higher risk of recurrence than rectal cancer in other directions (lateral or posterior quadrants). In a subsequent study, Kang et al. [54] also reported that the rate of positive CRM was higher for anteriorly located rectal cancer compared to nonanteriorly located rectal cancer. Furthermore, multivariate analysis showed that an anterior tumor was the only independent risk factor for a positive CRM [53, 54].
Achieving a negative CRM during anterior pelvic dissection near the DVF continues to be a contentious issue. Heald and Moran [55] have recommended dissection anterior to the DVF to ensure the completeness of TME and to lower the rate of local recurrence. Kraima et al. [56] supported this approach, likening the DVF to the MRF and recommending its inclusion in TME to improve oncologic outcomes. In contrast, some studies suggest a dissection plane posterior to the DVF. Sugihara et al. [57] found numerous communicating branches from the bilateral pelvic plexus on the ventral side of the DVF, which are closely linked to urogenital function. Muraoka et al. [39] described the DVF as consisting of multiple layers, not adhering to the prostate capsule, particularly towards the posterolateral aspect of the prostate. This nonadherence indicates that the space between the DVF and the prostatic capsule, filled with loose areolar tissue and the NVB, could provide a safer dissection plane, minimizing damage to neural structures. Muraoka et al. [39] also noted that the lateral extension of the DVF connects with the lateral pelvic fascia and NVB. He et al. [38] observed that the lateral border of the DVF macroscopically runs posterolateral to the seminal vesicle, attaching to and crossing the pelvic plexus. These studies support a posterior approach to the DVF for preserving the NVB and pelvic plexus during anterior pelvic dissection. Additionally, Kourambas et al. [58] conducted a histologic study that suggests neural damage as a potential cause for the high incidence of erectile dysfunction, even with nerve-sparing techniques during radical prostatectomy. They observed scattered connections of NVBs in both the posterolateral and medial aspects of the DVF. Although the NVB is preserved at the posterolateral edge of the prostate during radical prostatectomy, the combined excision of the DVF might lead to the removal of these connecting neural fibers. Given these findings, anterior pelvic dissection should generally be performed posterior to the DVF. Even if the tumor is located anteriorly and there is a risk of positive CRM, the simultaneous resection of the DVF may be necessary to preserve the NVB, the small communicating branches, and ultimately, the pelvic plexus. For tumors that are cT2 and located anteriorly, or cT3 and located laterally or posteriorly, it is advisable to perform anterior pelvic dissection posterior to the DVF until reaching the pelvic floor. For cT3 or cT4 tumors located anteriorly, optimal anterior pelvic dissection should be performed anterior to the DVF to achieve a negative CRM. For cT3 tumors at the level of the prostate gland, dissection should be performed posterior to the DVF at the seminal vesicle level, but switched to anterior to the DVF at the level of the prostate gland. However, if there is a long segment of cT3 tumor extending from the seminal vesicle to the prostate, proper anterior pelvic dissection should be performed anterior to the DVF (Fig. 18). This tailored approach to DVF excision, based on tumor location, level, and depth of invasion, is crucial for achieving optimal oncologic and functional outcomes.
Safe mobilization of the lateral wall of the rectum
After completing deep posterior and anterior pelvic dissection, the next critical step is the mobilization of the lateral wall of the rectum. It is crucial to safely mobilize the lateral part of the rectum to prevent injury to the pelvic plexus and to ensure the preservation of the mesorectum's integrity, thus avoiding a positive CRM. Anatomically, the MRF in this region is attached to the pelvic plexus and related endopelvic fascia. This area, which was previously referred to as the lateral ligament, often poses difficulties in delivering the rectum from the deep pelvic cavity. Dissection proceeds to the deep pelvic floor, leaving the lateral attachment and connective tissue layer hanging like a bridge between the parietal and MRF, allowing the middle rectal artery (MRA) to be ligated while preserving the pelvic plexus under gentle traction. It is important to note that the traditionally recognized lateral ligament is not actually present; rather, it is the adhesion point where the MRF attaches to the pelvic plexus (Fig. 19). These ligamentous structures between the mesorectum and the inferior hypogastric or pelvic plexus consist of rectal branches from the pelvic plexus, connective tissue, and the MRA. Sato and Sato [59] emphasized that the pelvic splanchnic nerves, arising posteromedially from the 3rd and 4th sacral nerves, are components of this lateral attachment. It is crucial to perform step-by-step dissection and exposure of this area. Following deep posterior and anterior pelvic dissection posterior to DVF, the lateral part of the mesorectum is exposed. Properly handling the MRA is essential for ensuring proper dissection and nerve-sparing TME. The MRA has been regarded as an important anatomical structure in complete TME, as it is the only vessel that penetrates the proper rectal fascia and enters the pelvic cavity, threatening the integrity of TME. Additionally, it is closely related to the lateral lymphatic drainage route. In the past, open TME procedures with poor visual fields in a narrow pelvis often involved rough traction and mass ligation, leading to frequent pelvic plexus injury and incomplete TME. This, combined with laterally located metastatic lymph nodes within the mesorectal fascial envelope, could result in local recurrence. In the era of minimally invasive surgery (MIS) TME, vascular clips can be used to safely manage the MRA, or it can be cauterized with an energy device, preserving the MRF and pelvic plexus. The Gate approach is 1 potential method for exposing the MRA and pelvic plexus. Kiyomatsu et al. [60] reviewed the anatomy of the MRA and noted that its frequency varies widely in the literature, ranging from 12% to 97%. The MRA's trajectory is typically lateral and anterolateral, with the lateral type being present in 20% to 30% of cases. The anterolateral type, which is more frequent and smaller, usually penetrates the NVB from the anterolateral direction. Heinze et al. [61] studied the anatomy of the MRA using 37 formalin-fixed hemipelvis specimens. They found that the MRA was present in 71.4% of cases (21.4% bilaterally and 50% unilaterally) and originated from the anterior division of the internal iliac artery, branching from either the internal pudendal artery or the inferior gluteal artery. They also noted the complex course of the MRA, moving from the pelvic wall through the pelvic nerve plexus and parietal pelvic fascia into the mesorectum. Its diameter varies from 0.5 to 3.5 mm, with an average of approximately 2 mm. They observed that the MRA consistently traverses the inferior hypogastric plexus, meaning that surgical transection of the MRA risks autonomic pelvic plexus injury, either mechanically or thermally. Therefore, it should be performed at a sufficient distance from the autonomic nerves. Precise anatomical knowledge of the trajectory of the MRA is essential for nerve-sparing TME surgery. They additionally showed the presence of lymphatic vessels accompanying the MRA. The presence of the MRA can predict lateral pelvic lymph node metastasis, supporting their observations. Contrast-enhanced MRI detected the MRA in 65.7% of cases (31.4% bilateral, 34.3% unilateral). Iwasa et al. [62] argued that the presence of the MRA functions as a robust predictor of lateral pelvic lymph node metastasis in patients with lower rectal cancer. We are confident that precise anatomical knowledge and experience are crucial for achieving success in rectal surgery.
CAA after ultralow anterior resection, whether stapled or hand-sewn, can completely preserve the levator ani muscle. ISR also preserves this muscle. Although these procedures involve detaching the rectum from the levator ani muscle sheet, the muscle remains intact. When rectal cancer involves the levator ani muscle without invading the EAS complex, TME with partial excision of the levator ani muscle can achieve a negative CRM and R0 resection. This approach is technically feasible, and the functional and long-term oncologic outcomes should be closely monitored. This technique is indicated for rectal cancer involving the levator ani muscle, which is typically located at the anorectal ring level. While APR is the most common procedure for this situation, some surgeons prefer partial or hemilevator excision if the IAS and EAS are not involved. Involvement of the levator ani muscle plate can typically be identified via high-resolution MRI and rectal examination (e.g., a palpable tumor at the anorectal ring 4 cm above the anal verge). Tumors at the anorectal ring level often spare the EAS and IAS, so complete excision of the involved levator ani muscle is crucial for achieving a negative CRM. However, this approach presents 2 challenges: first, ensuring favorable functional outcomes after the combined excision of the levator ani muscle, given its role in continence and bowel function; and second, accurately performing the technically demanding customized excision to avoid a positive CRM [63]. For lower rectal cancer involving the levator ani muscle, APR with total levator excision (referred to as extralevator APR or extralevator abdominoperineal excision [ELAPE]) can be performed to avoid a positive CRM and reduce local recurrence. Understanding the complex anatomical relationships among the rectum, levator ani muscle (a funnel-shaped group of thin, striated muscles forming the pelvic floor), and the surrounding structures is crucial for surgical planning. ELAPE aims to achieve a cylindrical specimen shape by excising the levator ani muscle while keeping it attached to the rectum, thus preventing "waisting" of the specimen. Optimal visualization during ELAPE is often achieved by positioning patients in the jackknife position, which facilitates better access and visibility for the surgeon.
Historically, APR was the only way to achieve R0 resection with total levator excision for tumors at the anorectal ring level exhibiting partial invasion of the levator muscle plate. However, since 2013, partial excision of the involved levator ani muscle has been introduced [63]. This technique, which can be applied to patients with tumors at the anorectal junction that exhibit partial levator ani muscle invasion, involves TME dissection toward the levator ani muscle and unilateral excision of the involved levator ani muscle via the intersphincteric plane (Figs. 20, 21) [44, 64, 65]. Preoperative CRT has facilitated sphincter-preserving procedures like partial excision of the levator ani muscle by achieving significant downsizing and downstaging in patients with unilateral levator ani muscle plate involvement in whom the EAS remains intact.
In a series of 23 consecutive cases involving partial excision of the levator ani muscle (PELM), Yang et al. [66] reported the following outcomes: a 3-year local recurrence rate of 14.4% over a median follow-up period of 44 months, a 3-year OS rate of 95%, and a DFS rate of 72.4%. Among the local recurrences, 66% (2 out of 3) were anastomotic and 33% (1 out of 3) were presacral. All patients experiencing local recurrence underwent salvage APR. Systemic recurrence occurred in 3 out of the 23 patients, with the liver, lungs, and paraaortic lymph nodes identified as the sites of recurrence. One year after ileostomy closure, the mean scores were as follows: frequency subscale, 30.3; dietary subscale, 16.6; MSKCC Bowel Function Instrument total, 68.3; urgency and soilage, 10.5; and Wexner, 10.7. They concluded that robotic PELM can be effectively performed with minimal CRM involvement and acceptable functional outcomes in patients with tumors invading the ipsilateral levator ani muscle at the anorectal ring level.
In the context of TME for tumors at the anorectal ring level, it is recommended to adopt a tailored approach for excising the levator ani muscle. Although the role of the levator ani muscle is significant, its full implications are not yet completely understood. The following are the proposed classifications for levator ani muscle excision:
1. Total levator excision with combined EAS resection (APR): This involves the complete removal of the levator ani muscle along with the EAS.
2. Total levator excision with CAA or ISR: This approach preserves only the EAS, with complete excision of the levator ani muscle.
3. PELM with ISR: This method involves partial excision of the levator ani muscle only in areas invaded by the tumor, preserving portions of both the EAS and the levator ani muscle.
This classification offers a structured method for managing tumors at the level of the anorectal ring that involve the levator ani muscle. However, it is essential to accumulate more case experiences and conduct long-term follow-ups to assess the long-term efficacy and safety of the PELM approach, considering both oncologic and functional outcomes.
Even with the best efforts to perform TME, the patient's pelvic shape and tumor location can pose significant challenges. In such cases, we believe TaTME might be a more suitable option. Incomplete TME and poor-quality TME specimens can lead to recurrence, often due to inexperience or challenging pelvic anatomy. The primary reasons for incomplete TME are typically associated with male patients, preoperative CRT, and large tumors. Additionally, a narrow and deep pelvic anatomy complicates pelvic dissection. Previous studies have shown that the bony structures of the pelvis, such as the depth and length of the sacrum and the dimensions of the pelvic inlet and outlet, affect the difficulty of TME [67–69]. In a previous study, we determined that surgical outcomes were influenced by clinical and anatomical factors identified through pelvic MRI [70]. This study revealed that challenging pelvic anatomies, characterized by a long sacral length, shallow sacral angle, and narrow intertuberous diameter, were significantly associated with prolonged pelvic dissection times. We discovered that pelvic MRI-based pelvimetry could reflect the anatomical challenges of the pelvis, resulting in increased operation time. Subsequently, Baek et al. [71] analyzed 183 patients who underwent robotic surgery for rectal cancer and identified high body mass index, preoperative CRT, and lower tumor level as factors contributing to extended operation times. However, pelvimetric parameters did not correlate with operation time, leading to the conclusion that the robotic system might mitigate the challenges posed by difficult pelvic anatomy. Lee et al. [69] hypothesized that the angle of the pelvic floor might influence TME difficulty. They suggested that the configuration of the pelvic floor muscles impacts TME difficulty and could predict challenges in transabdominal TME. Their data indicated that the incline of the pelvic floor muscle is the sole anatomical parameter that can predict TME difficulty. Therefore, TaTME presents a viable alternative for patients with challenging pelvic anatomy to achieve a complete TME specimen. The International TaTME Consensus Conference suggested that a deep, narrow pelvis could indicate the need for TaTME [72].
Park et al. [73] reported on 117,320 patients who underwent surgical resection for colorectal cancer from 2013 to 2018. During this period, the proportion of laparoscopic resections rose from 64.7% in 2013 to 77.4% in 2018. Notably, the rate of laparoscopic surgery for rectal cancer reached 81.6% in 2018. We now estimate that the rate of laparoscopic resection for rectal cancer may have surpassed 95%. The Korean Association of Robotic Surgeons (KAROS) study group examined the trend of robotic surgery for colorectal, stomach, and hepatobiliary cancers from 2005 to 2014 [74]. During the study period, the number of robotic colorectal surgeries saw a significant increase, totaling 505 cases by 2014. However, the proportion of robotic surgeries relative to laparoscopic surgeries remained unchanged. While the rates of ISR and APR steadily increased, the number of low anterior resection cases stayed consistent. The high cost of robotic surgery, which is not covered by national medical insurance, appears to be a significant obstacle to the broader adoption of this technology in colorectal surgery.
The KAROS study group analyzed data from a nationwide registry on robotic rectal surgery in Korea [75]. Baek et al. [75] examined 4 types of operative procedures between 2006 and 2014: anterior resection, low anterior resection, ISR, and APR. Since 2006, the number of robotic procedures in Korea has increased, with more than 500 operations performed in 2014. Low anterior resection was the most common robotic procedure, accounting for 67.2% of operations, followed by ISR at 22.6% since 2010. Additionally, the frequency of APR has progressively increased to 12.4%. With the increasing prevalence of laparoscopic surgery for rectal cancer, randomized clinical trials began in the late 1990s. Among these, the ALaCaRT (Australasian Laparoscopic Cancer of the Rectum) trial and the American College of Surgeons Oncology Group (ACOSOG) Z6051 trial failed to demonstrate that laparoscopic TME specimens are not inferior to open TME specimens for rectal cancer. Stevenson et al. [76] conducted a randomized noninferiority phase 3 trial (ALaCaRT) comparing open and laparoscopic resection for rectal cancer. This trial showed that the noninferiority of laparoscopic surgery compared with open surgery for R0 resection was not established. CRM was clear in 93% of laparoscopic cases and 97% of open cases, with a conversion rate to open surgery of 9%. Later, Stevenson et al. [77] also reported on DFS and local recurrence after laparoscopic-assisted resection or open resection for rectal cancer. This study showed that laparoscopic surgery for rectal cancer did not differ significantly from open surgery in terms of 2-year recurrence, DFS, or OS. Fleshman et al. [78] conducted a multicenter, noninferiority, randomized clinical trial in the United States. The open conversion rate was 11.3%, and a negative CRM was observed in 90% of cases (87.9% in the laparoscopic group and 92.3% in the open group). However, they concluded that for stage II and III rectal cancer, laparoscopic resection failed to meet the criteria for noninferiority in terms of pathologic outcomes compared to open resection. Subsequently, they reported follow-up results of this clinical trial, which showed that laparoscopic resection of rectal cancer was not significantly different from open resection in terms of DFS and recurrence [79]. Despite some concerns raised by the 2 aforementioned studies about the oncological safety of laparoscopic surgery for rectal cancer, subsequent research has provided favorable data demonstrating its oncological stability. Clinical studies conducted in Korea, although carried out in a different patient population, offer meaningful and valuable insights. The COREAN (Comparison of Open Versus Laparoscopic Surgery for Mid and Low Rectal Cancer After Neoadjuvant Chemoradiotherapy) trial, which compared open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy, showed a conversion rate of 1.5% and a low rate of CRM involvement (3%) [80]. These results indicate that while laparoscopic surgery for rectal cancer requires thorough training and experience, it demonstrates treatment outcomes equivalent to open surgery. Given the additional advantages of laparoscopic surgery, it is not an exaggeration to say that laparoscopic rectal cancer surgery has become nearly universal in Korea. Multicenter prospective randomized clinical trials, such as the MRC CLASSIC (Medical Research Council Conventional Versus Laparoscopic-Assisted Surgery in Colorectal Cancer), COLOR II (Colorectal Cancer Laparoscopic or Open Resection II), and COREAN trials, have evaluated the oncologic outcomes of laparoscopic surgery for rectal cancer. These trials found no significant differences in local recurrence or DFS rates between laparoscopic and open surgery [81–83]. Although the ACOSOG Z6051 and ALaCaRT trials did not establish the noninferiority of laparoscopic surgery compared to open surgery for rectal cancer through their statistical analyses, the 10-year follow-up of the COREAN trial confirmed the long-term oncological safety of laparoscopic surgery in patients with rectal cancer treated with preoperative CRT [84]. Furthermore, the superiority of robotic surgery over laparoscopic surgery was not proven in the ROLARR (Robotic Versus Laparoscopic Resection for Rectal Cancer) trial. Advanced surgical techniques alone do not ensure better oncological outcomes. Instead, it is more important how well surgeons adhere to the principles of TME and perform the surgery, regardless of the modality chosen. Jayne et al. [85] conducted a randomized clinical trial comparing robotic-assisted versus laparoscopic surgery among 471 patients with rectal cancer. The open conversion rate was 8.1% for robotic surgery and 12.2% for laparoscopy. No statistically significant difference was found between the 2 surgical modalities in terms of the rate of CRM involvement, which was 6% for robotic surgery and 5.1% for laparoscopy. However, the conversion rate was lower in selected groups of male patients and those with obesity who underwent robotic TME compared to laparoscopic TME. In Korea, Park et al. [86] conducted a multicenter randomized clinical trial, COLRAR (Comparison of Laparoscopic Versus Robot-Assisted Surgery for Rectal Cancer), to assess the safety and efficacy of robotic surgery for mid or low rectal cancer compared with laparoscopic surgery. Patients were prospectively enrolled between 2011 and 2016. The rate of complete TME was 80.7% in the robotic TME group versus 77.1% in the laparoscopic TME group, showing no significant difference. Similarly, there was no difference in the rate of CRM positivity between the 2 groups. However, among patients who received preoperative CRT, the positive rate of CRM was 0% in the robotic TME group versus 6.1% in the laparoscopic TME group (P=0.034). They suggested that the robotic approach might have benefits in difficult cases, but concluded that robotic surgery did not significantly improve TME quality compared with conventional laparoscopic surgery. Subsequently, Kim et al. [87] reported the results of a phase II open-label prospective randomized controlled trial comparing robot-assisted (n=81) versus laparoscopic surgery (n=82) for rectal cancer. Complete TME was achieved in 80.3% of robotic operations and 78.1% of laparoscopic operations, showing no statistically significant difference. They demonstrated that robotic surgery for rectal cancer provided TME quality comparable to that of laparoscopic surgery, with similar postoperative morbidity, bowel function recovery, and quality of life. Based on the above results, there is still insufficient evidence to prove that robotic TME is superior to laparoscopic TME for rectal cancer. Some small-scale studies have reported that robotic surgery reduces surgeon fatigue and speeds up patient recovery, but these findings are not yet conclusive. Additionally, limited evidence supports the possibility that robotic surgery preserves sexual and urinary function significantly better than laparoscopic surgery. Many factors influence these outcomes, making it difficult to establish the superiority of robotic surgery definitively. The introduction of robotic surgery presents a new treatment method, and while initial feedback from surgeons who have used it is generally positive, further research is needed. Personally, we find robotic surgery to be convenient and precise for mid and low rectal cancer, which we believe are its main advantages.
The surgical approach for performing TME in mid or low rectal cancer within a deep, narrow pelvic cavity often presents significant challenges for surgeons. These challenges can lead to incomplete TME and a high rate of positive CRM. Ideal candidates for TaTME typically include patients with a narrow pelvis, a body mass index over 30 kg/m2, and a tumor diameter greater than 4 cm. Recently, international consensus guidelines have strongly recommended the adoption of TaTME for low rectal cancer [88]. The multicenter randomized controlled trial, COLOR III, compared TaTME with laparoscopic TME, focusing on oncologic safety in terms of CRM involvement and local recurrence rates, as well as postoperative morbidity and functional outcomes [89]. The results of this trial are critical for the broader adoption of TaTME for mid and low rectal cancer, and its oncologic outcomes have been reported.
Deijen et al. [90] reported that during a follow-up period of 18.9 months, the pooled local and distant recurrence rates were 4% and 8.1%, respectively. These rates are consistent with the oncologic outcomes previously reported in randomized controlled trials for laparoscopic TME. Lelong et al. [91] reported local recurrence rates of 5.3% for laparoscopic TME and 5.7% for TaTME, with a median follow-up period of 31.9 months. Kwon et al. [92] conducted a systematic review and meta-analysis comparing TaTME with laparoscopic TME for rectal cancer. The study revealed similar perioperative outcomes between the 2 groups but a significantly lower conversion rate for TaTME. The pathologic outcomes for TME were comparable between the groups, leading to the conclusion that TaTME can be adopted as a new health technology in Korea. Currently, robotic technology is also being used to perform TaTME and shows promise. To date, TaTME has demonstrated a low conversion rate, comparable perioperative outcomes to laparoscopic TME, similar pathologic outcomes, and promising oncologic results. However, some concerns arise from the fact that these results primarily come from high-volume centers and highly trained surgeons. For successful implementation of TaTME in Korea, it will be essential to establish a national training program through professional societies and academic institutions.
Regardless of the surgical treatment modality, the most crucial factor is the surgeon's competence in performing curative resection with precise dissection along the embryonic plane, while preserving the pelvic autonomic nervous system. Adherence to surgical principles is the most significant prognostic factor for oncologic outcomes. In 2008, we reported on the oncologic outcomes following TME for rectal cancer. A total of 1,276 patients were analyzed, with a mean follow-up period of 69.4 months. The 5-year overall local recurrence rates were 3.8% for stage I, 4.7% for stage II, and 8.4% for stage III. Additionally, the 5-year cancer-specific survival rates were 93.8% for stage I, 84.5% for stage II, and 64.5% for stage III [93]. In 2009, we also published an analysis of the operative safety and oncologic outcomes of anal sphincter-preserving surgery with mesorectal excision for rectal cancer, based on data from 931 patients [94]. Patients treated between 1989 and 2004 were analyzed; during the study period, a multidisciplinary team approach and tailored mesorectal excision became more popular between 1997 and 2004. We divided the patients into 2 groups (n=208 from 1989–1996, n=723 from 1997–2004). There were no significant differences between the 2 periods regarding anastomotic leakage (2.4% vs 3.6%), cancer-specific survival rates (79.1% vs 79.6%), and local recurrence rates (8.4% vs 8.6%). We further analyzed patients who underwent TME for rectal cancer, comparing MIS with open surgery [95]. This case-matched study included 633 patients (MIS, n=211; open, n=422) treated between 2003 and 2008, with a median follow-up period of 64 months. The anastomotic leakage rate was 4% for open surgery versus 6% for MIS. MIS consisted of laparoscopic (59%) and robotic approaches (41%). The CRM involvement (less than 1 mm) rate was 5% for open surgery and 4% for MIS. The 5-year OS, disease-specific survival, and DFS rates were 80.7%, 78.8%, and 84.0%, respectively, with local recurrence rates of 5.7% versus 5.1%. We found no significant differences in 5-year OS, disease-specific survival, DFS, or local recurrence rates between the open and MIS groups. MIS for TME, which includes laparoscopic and robotic approaches, showed no significant differences in oncologic outcomes compared to open surgery. This prompted us to suggest that MIS for rectal cancer is a safe option. The adoption of MIS for rectal cancer in Korea has been very successful, with the prevalence of MIS for TME for rectal cancer now approaching over 85%. However, MIS for rectal cancer is still regarded as a technically demanding procedure. In 2007, Jung et al. [96] analyzed 441 low rectal cancer patients at Asan Medical Center (Seoul, Korea). They reported a local recurrence rate of 12.8% for patients who underwent APR and 7.4% for those who underwent sphincter-saving resection (SSR). The 5-year cancer-specific survival rates were 73.2% for APR and 87.6% for SSR. Similarly, Kim et al. [97] reported oncologic outcomes after TME for rectal cancer at Asan Medical Center, revealing an overall local recurrence rate of 7.5% in stage II and 14.3% in stage III. The 5-year OS and DFS rates were 88.9% and 82.9%, respectively, for stage II, and 79% and 60%, respectively, for stage III. Subsequently, Yeom et al. [98] reported on the long-term outcomes of APR and LAR for low rectal cancer at Asan Medical Center. They analyzed 409 consecutive patients with low rectal cancer, among whom 335 (81.9%) underwent APR and 74 (18.1%) underwent SSR. The median follow-up period was 55.7 months. The local recurrence rate was 8.7% for SSR and 5.7% for APR. The systemic recurrence rate was 18.9% for SSR and 31.3% for APR. The 5-year recurrence-free survival rate was 70.2% for SSR and 84.2% for APR, and the rate of CRM involvement was 1.4% for SSR and 4.8% for APR.
A comparison of 2 studies conducted at the same hospital over a 10-year period reveals a significant reduction in the rate of local recurrence in the oncologic outcomes for low rectal cancer. This improvement highlights advancements in surgical techniques and postoperative care during this time. As previously mentioned, data from 2 hospitals indicate that the treatment outcomes for TME in rectal cancer, whether through open surgery or MIS, have a local recurrence rate ranging from 5% to 10%. The 5-year survival rates are quite favorable, comparable to or even better than global reports. In a separate study, Kim et al. [99] analyzed 111 patients with low rectal cancer at Inje University Busan Paik Hospital (Busan, Korea), with 65 undergoing APR and 46 receiving sphincter-saving operations. They found no significant difference in oncologic outcomes between the 2 surgical methods. The local recurrence rates were 20.1% for APR and 15.2% for sphincter-saving operations, while the 5-year DFS rates were 56.9% and 63%, respectively. When compared with data from Asan Medical Center in 2007, these results indicate a slightly higher incidence of local recurrence and lower survival rates. The volume of operations performed may contribute to these differences, although this is not definitively established. Nevertheless, these outcomes are still considered acceptable and represent improvements over previous results.
A collaborative study conducted by Keimyung University (Daegu, Korea) and Kyungpook National University (Daegu, Korea) examined the treatment outcomes of rectal cancer [100]. Cho et al. [100] conducted a retrospective study of 203 rectal cancer patients treated between 2006 and 2012 at 2 university hospitals. The patients were divided into 2 groups: those who underwent curative surgery alone (n=118) and those who received preoperative CRT followed by surgery (n=85). The 5-year local recurrence rates were 2% for both surgery-alone group and preoperative CRT plus surgery group. The 5-year DFS rates were 87% and 88%, respectively. Although the study showed that surgery alone in a selected group of patients was comparable to preoperative CRT followed by TME in terms of oncologic outcomes, the results were particularly remarkable for their low rate of local recurrence in patients with mid and low rectal cancer, T3, and CRM-negative status, highlighting the exceptional surgical technique of TME.
Advancements in anatomical and functional research, coupled with the widespread adoption of MIS, have enhanced the precision and accuracy of curative surgeries for rectal cancer. As a result, it is now more feasible to perform curative resections that also preserve function, leading to significantly improved treatment outcomes compared to those seen in the past. However, ongoing research is essential to identify the most effective preoperative treatments for reducing both systemic and local recurrences in advanced rectal cancer. Recent studies have shown that the TNT approach has increased clinical complete response rates. As surgeons, we envision a future where neoadjuvant treatment could achieve a 100% complete response rate in all patients, potentially eliminating the need for surgical intervention. In Korea, there has been a notable improvement in surgical outcomes for rectal cancer, including the successful implementation of minimally invasive techniques and the adoption of a multidisciplinary approach. However, continuing education on surgical techniques and the development of a national database remain crucial. These efforts are essential for the accurate evaluation and external reporting of TME specimen quality and CRM status. The success of TME ultimately benefits the patient, as achieving both curative resection and functional preservation significantly enhances the quality of daily life for those treated. Before concluding this review article, we would like to highlight several key points that should be conveyed to future generations:
1. Accurate TME to prevent local recurrence: Accurate TME is crucial for preventing recurrence near the anastomosis site within the 1st year after surgery. This underscores the importance of precision and completeness in surgery to reduce recurrence rates (Fig. 22).
2. A multidisciplinary approach for neoadjuvant therapy decisions: Preventing early recurrence after surgical treatment necessitates a multidisciplinary approach to determine the appropriate neoadjuvant therapy for locally advanced rectal cancer. Collaborating with radiation oncologists, medical oncologists, pathologists, and radiologists enhances the accuracy and effectiveness of the treatment plans.
3. Refinement of sphincter-preserving techniques: Sphincter preservation is a significant concern for patients. Therefore, refining surgical techniques for sphincter preservation is critical. This plays a vital role in improving patients' quality of life.
4. Research on biological characteristics of tumors and treatment direction: Ongoing research on the biological characteristics of tumors is necessary to suggest better treatment directions. This will aid in developing personalized treatment strategies and providing optimized care for each patient.

Conflict of interest

Nam Kyu Kim is an Editor-in-Chief Emeritus of Annals of Coloproctology, but was not involved in the reviewing or decision process of this manuscript. No other potential conflict of interest relevant to this article was reported.

Funding

None.

Acknowledgments

This manuscript was based on the commemorative lecture given by the late Professor Kim Kwang-Yeon.

Author contributions

Conceptualization: NKK, MSC; Methodology: all authors; Validation: NKK, MSC; Supervision: NKK; Writing–original draft: all authors; Writing–review & editing: all authors. All authors read and approved the final manuscript.

Fig. 1.
Sagittal and coronal views of rectal magnetic resonance imaging. Sagittal view showed (A) a huge mass (cT3N2), (B) a large, bulky tumor in close proximity to the seminal vesicle (arrow), and (C) the left levator ani muscle (arrow). Additionally, numerous enlarged lymph nodes are identified within the mesorectum.
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Fig. 2.
A whole-mount section of a rectal specimen fixed in formalin reveals the detailed shape of the mesorectum, facilitating a clear understanding of the circumferential resection margin.
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Fig. 3.
The mesorectum is well-developed on the posterolateral side of the rectum. It tapers down, ending 2 to 3 cm above the level of the levator ani muscle. The arrow indicates a junction of the rectum and levator ani muscle. Adapted from Kim [35], available under the Creative Commons License.
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Fig. 4.
Gimbap, a popular takeaway food in Korea, can be likened to the anatomical structure of the rectum during total mesorectal excision. In this analogy, the outer layer of seaweed represents the rectal proper fascia. If the inner rice and vegetable contents push against or penetrate the outer seaweed layer (blue dotted circles), it threatens the circumferential resection margin (CRM). Similarly, during total mesorectal excision, if a surgeon accidentally tears the outer layer of fascia in the deep pelvic cavity, it could lead to tumor spillage, compromising the surgical outcome.
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Fig. 5.
A schematic sagittal view of the pelvis illustrating the various pelvic fasciae. The rectal proper fascia enveloped the mesorectum. Below the peritoneal reflection, the anterior Denonvilliers fascia, a dense membrane located between the rectum and seminal vesicle, is depicted. Posteriorly, the rectosacral fascia (Waldeyer fascia), a dense connective tissue between the posterior part of the rectal proper fascia and the presacral fascia at the S3 and S4 level, is shown. The presacral fascia covers the periosteum of the sacral bone. Adapted from Lee and Kim [34], available under the Creative Commons License.
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Fig. 6.
The surgical anatomy of rectosacral fascia. (A) Cadaveric dissection of a hemisectioned pelvis reveals the retrorectal space, displaying the rectosacral fascia at the level of the 4th sacral vertebra when the dissection follows the rectal proper fascia. Reprinted from Kim [35], available under the Creative Commons License. (B) The rectosacral fascia is encountered during deep posterior dissection in robotic surgery.
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Fig. 7.
Topographic anatomy of Denonvilliers fascia (DVF) and neurovascular bundle. (A) The apron-shaped DVF is located between the seminal vesicle (SV), prostate (P), and the rectum (R). It is attached to the prostate gland more densely, but loosely attached to the SV. (B) Each neurovascular bundle is found at the 10 and 2 o’clock direction. The neurovascular bundle is highlighted with a red box (Masson trichome stain, ×50). (C) A histological study of the cadaveric specimen revealed that the neurovascular bundle to the genitalia was located at the posterolateral side of the prostate gland, posterior to the DVF (Masson trichome stain, ×100). Panels B and C are reproduced from Yang et al. [40], available under the Creative Commons License.
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Fig. 8.
A cadaveric dissection of a hemisectioned pelvis shows the inferior hypogastric nerve descending along the pelvic sidewall. It converges with the sacral parasympathetic nerves, which arise from the 2nd, 3rd, and 4th sacral segments near the piriformis muscle. The inferior hypogastric nerve forms the pelvic plexus at the lateral pelvic wall after merging with these sacral parasympathetic nerves. Nerve bundles from the pelvic plexus then run to the genitourinary organs along the seminal vesicle in men. Reprinted from Kim [35], available under the Creative Commons License.
ac-2024-00388-0055f8.jpg
Fig. 9.
From the above, anterior to the ischial spine, the pelvic diaphragm includes the areas through which the vagina, rectum, and urethra pass. The pelvic floor consists of the pubococcygeus, puborectalis, and iliococcygeus muscles.
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Fig. 10.
After removal of the sacrum, the posterior midline view in a cadaveric study reveals the levator ani muscle. (A, B) The U-shaped puborectalis muscle encircles the rectum, and the pubococcygeus muscle is also clearly visible. (C) The levator ani muscle, attached to the pelvic sidewall, resembles a membranous sheet adhering to the rectal proper fascia, which envelops the mesorectum (reprinted from Kim [42], available under the Creative Commons License).
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Fig. 11.
Technical tips for abdominoperineal resection with negative circumferential resection margin. (A) A schematic coronal view of low rectal cancer invading the external anal sphincter (EAS) and levator ani muscle (LA). The red dotted line indicates the extralevator abdominoperineal excision (ELAPE) line. (B) Specimen after ELAPE for low rectal cancer invading the LA and EAS. The red arrow indicates excised portion of LA. IAS, internal anal sphincter.
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Fig. 12.
Histological study (hematoxylin–eosin, ×10) showed the internal anal sphincter (IAS; smooth muscle) and external anal sphincter (EAS; skeletal muscle) muscles, along with the longitudinal muscle between them.
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Fig. 13.
Histological study (hematoxylin–eosin, ×10) shows boundary between the rectum and levator ani muscle, where smooth and skeletal muscle intermingled. IAS, internal anal sphincter; EAS, external anal sphincter.
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Fig. 14.
Basic concept of intersphincteric resection and pathologic specimen. (A) Coronal view depicting the suggested dissection line (red dotted line) of the transanal approach for intersphincteric resection for T1/T2 low rectal cancer. (B) Completely resected low rectal cancer with intersphincteric resection. (C) A histological study (hematoxylin–eosin, ×50) shows the tumor confined to the rectal muscle propria, with pT2 staging and a sufficient circumferential resection margin obtained. (D) Cadaveric dissection shows a clear cleavage plane between the internal anal sphincter (IAS) and external anal sphincter (EAS); reprinted from Varela and Kim [44], available under the Creative Commons License. LA, levator ani muscle; R, rectum.
ac-2024-00388-0055f14.jpg
Fig. 15.
A schematic view of the relationship between the rectum (R) and rectourethralis muscle (RU) and suggested anterior dissection line. Sagittal view depicting the suggested dissection line (red dotted line) of intersphincteric resection (ISR) and abdominoperineal resection (APR) for low rectal cancer. Denonvilliers fascia (DVF) end to the RU. Identifying the RU is key for avoiding damage to the urethra. EAS, external anal sphincter; IAS, internal anal sphincter; LA, levator ani muscle; P, prostate.
ac-2024-00388-0055f15.jpg
Fig. 16.
Schematic images. (A) Red dotted lines depict anterolateral dissection behind the Denonvilliers fascia (DVF), and this dissection plane meets with posterolateral pelvic dissection along the parietal pelvic fascia (PPF), while preserving the hypogastric nerve (HGN) and division of rectosacral fascia. (B) The orange dotted line indicates the proposed dissection line. DVF and its lateral border meet with the PPF. Underneath this fascia, the neurovascular bundle (NVB) and HGN are present. IHN; inferior hypogastric nerve; MRF, mesorectal fascia; PP, pelvic plexus; R, rectum; MR, mesorectum; SV, seminal vesicle.
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Fig. 17.
A schematic image of the Gate approach illustrates one way to obtain a complete total mesorectal excision specimen in a deep narrow pelvic cavity. The red box area depicts a dissection area with the Gate approach. There will be a sharp pelvic dissection between the mesorectal fascia and pelvic floor. PP, pelvic plexus. Adapted and reproduced from Kim et al. [51], available under the Creative Commons License.
ac-2024-00388-0055f17.jpg
Fig. 18.
The concept of customized Denonvilliers fascia (DVF) excision. (A) A schematic sagittal view of the pelvis illustrating the anterior dissection plane. The red dotted line depicts the suggested dissection plane for early stage tumor (e.g., T1, T2), preserving the DVF and reducing the risk of nerve damage while ensuring circumferential margin negativity. (B) For more advanced tumor, especailly those anteriorly located, excising the DVF might be necessary to achieve circumferential resection margin negativity. (C) Under third robotic arm upward traction of the seminal vesicle, the whitish membrane-like DVF was exposed, robotic scissor incised it, and sharp dissection proceeded behind the DVF. MR, mesorectum; P, prostate; R, rectum; SV, seminal vesicle.
ac-2024-00388-0055f18.jpg
Fig. 19.
The rectal proper fascia adheres to the mesh-like pelvic plexus at the lateral pelvic wall. The fine branches from the pelvic plexus enter the rectal wall.
ac-2024-00388-0055f19.jpg
Fig. 20.
The blue dotted line depicts a division line of partial levator ani muscle. On the left side, the part of the levator ani muscle invaded by the tumor is excised; however, on the right side, the levator ani muscle is preserved. DL, dentate line; IAS, internal anal sphincter; EAS, external anal sphincter; ISS, intersphincteric space. Adapted from Varela and Kim [44], available under the Creative Commons License.
ac-2024-00388-0055f20.jpg
Fig. 21.
Comparison of rectal magnetic resonance imaging before and after partial excision of the involved levator ani muscle (PELM) shows an absence of right-side levator ani muscle plate. (A) Before PELM, tumor involved the right side of levator ani muscle partially. (B) After PELM, left side levator ani muscle can be identified, while right side of levator ani already excised.
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Fig. 22.
(A, B) Local recurrence near the anastomosis site after total mesorectal excision. Red arrows indicate recurrence near the anastomosis.
ac-2024-00388-0055f22.jpg
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    Essential knowledge and technical tips for total mesorectal excision and related procedures for rectal cancer
    Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image Image
    Fig. 1. Sagittal and coronal views of rectal magnetic resonance imaging. Sagittal view showed (A) a huge mass (cT3N2), (B) a large, bulky tumor in close proximity to the seminal vesicle (arrow), and (C) the left levator ani muscle (arrow). Additionally, numerous enlarged lymph nodes are identified within the mesorectum.
    Fig. 2. A whole-mount section of a rectal specimen fixed in formalin reveals the detailed shape of the mesorectum, facilitating a clear understanding of the circumferential resection margin.
    Fig. 3. The mesorectum is well-developed on the posterolateral side of the rectum. It tapers down, ending 2 to 3 cm above the level of the levator ani muscle. The arrow indicates a junction of the rectum and levator ani muscle. Adapted from Kim [35], available under the Creative Commons License.
    Fig. 4. Gimbap, a popular takeaway food in Korea, can be likened to the anatomical structure of the rectum during total mesorectal excision. In this analogy, the outer layer of seaweed represents the rectal proper fascia. If the inner rice and vegetable contents push against or penetrate the outer seaweed layer (blue dotted circles), it threatens the circumferential resection margin (CRM). Similarly, during total mesorectal excision, if a surgeon accidentally tears the outer layer of fascia in the deep pelvic cavity, it could lead to tumor spillage, compromising the surgical outcome.
    Fig. 5. A schematic sagittal view of the pelvis illustrating the various pelvic fasciae. The rectal proper fascia enveloped the mesorectum. Below the peritoneal reflection, the anterior Denonvilliers fascia, a dense membrane located between the rectum and seminal vesicle, is depicted. Posteriorly, the rectosacral fascia (Waldeyer fascia), a dense connective tissue between the posterior part of the rectal proper fascia and the presacral fascia at the S3 and S4 level, is shown. The presacral fascia covers the periosteum of the sacral bone. Adapted from Lee and Kim [34], available under the Creative Commons License.
    Fig. 6. The surgical anatomy of rectosacral fascia. (A) Cadaveric dissection of a hemisectioned pelvis reveals the retrorectal space, displaying the rectosacral fascia at the level of the 4th sacral vertebra when the dissection follows the rectal proper fascia. Reprinted from Kim [35], available under the Creative Commons License. (B) The rectosacral fascia is encountered during deep posterior dissection in robotic surgery.
    Fig. 7. Topographic anatomy of Denonvilliers fascia (DVF) and neurovascular bundle. (A) The apron-shaped DVF is located between the seminal vesicle (SV), prostate (P), and the rectum (R). It is attached to the prostate gland more densely, but loosely attached to the SV. (B) Each neurovascular bundle is found at the 10 and 2 o’clock direction. The neurovascular bundle is highlighted with a red box (Masson trichome stain, ×50). (C) A histological study of the cadaveric specimen revealed that the neurovascular bundle to the genitalia was located at the posterolateral side of the prostate gland, posterior to the DVF (Masson trichome stain, ×100). Panels B and C are reproduced from Yang et al. [40], available under the Creative Commons License.
    Fig. 8. A cadaveric dissection of a hemisectioned pelvis shows the inferior hypogastric nerve descending along the pelvic sidewall. It converges with the sacral parasympathetic nerves, which arise from the 2nd, 3rd, and 4th sacral segments near the piriformis muscle. The inferior hypogastric nerve forms the pelvic plexus at the lateral pelvic wall after merging with these sacral parasympathetic nerves. Nerve bundles from the pelvic plexus then run to the genitourinary organs along the seminal vesicle in men. Reprinted from Kim [35], available under the Creative Commons License.
    Fig. 9. From the above, anterior to the ischial spine, the pelvic diaphragm includes the areas through which the vagina, rectum, and urethra pass. The pelvic floor consists of the pubococcygeus, puborectalis, and iliococcygeus muscles.
    Fig. 10. After removal of the sacrum, the posterior midline view in a cadaveric study reveals the levator ani muscle. (A, B) The U-shaped puborectalis muscle encircles the rectum, and the pubococcygeus muscle is also clearly visible. (C) The levator ani muscle, attached to the pelvic sidewall, resembles a membranous sheet adhering to the rectal proper fascia, which envelops the mesorectum (reprinted from Kim [42], available under the Creative Commons License).
    Fig. 11. Technical tips for abdominoperineal resection with negative circumferential resection margin. (A) A schematic coronal view of low rectal cancer invading the external anal sphincter (EAS) and levator ani muscle (LA). The red dotted line indicates the extralevator abdominoperineal excision (ELAPE) line. (B) Specimen after ELAPE for low rectal cancer invading the LA and EAS. The red arrow indicates excised portion of LA. IAS, internal anal sphincter.
    Fig. 12. Histological study (hematoxylin–eosin, ×10) showed the internal anal sphincter (IAS; smooth muscle) and external anal sphincter (EAS; skeletal muscle) muscles, along with the longitudinal muscle between them.
    Fig. 13. Histological study (hematoxylin–eosin, ×10) shows boundary between the rectum and levator ani muscle, where smooth and skeletal muscle intermingled. IAS, internal anal sphincter; EAS, external anal sphincter.
    Fig. 14. Basic concept of intersphincteric resection and pathologic specimen. (A) Coronal view depicting the suggested dissection line (red dotted line) of the transanal approach for intersphincteric resection for T1/T2 low rectal cancer. (B) Completely resected low rectal cancer with intersphincteric resection. (C) A histological study (hematoxylin–eosin, ×50) shows the tumor confined to the rectal muscle propria, with pT2 staging and a sufficient circumferential resection margin obtained. (D) Cadaveric dissection shows a clear cleavage plane between the internal anal sphincter (IAS) and external anal sphincter (EAS); reprinted from Varela and Kim [44], available under the Creative Commons License. LA, levator ani muscle; R, rectum.
    Fig. 15. A schematic view of the relationship between the rectum (R) and rectourethralis muscle (RU) and suggested anterior dissection line. Sagittal view depicting the suggested dissection line (red dotted line) of intersphincteric resection (ISR) and abdominoperineal resection (APR) for low rectal cancer. Denonvilliers fascia (DVF) end to the RU. Identifying the RU is key for avoiding damage to the urethra. EAS, external anal sphincter; IAS, internal anal sphincter; LA, levator ani muscle; P, prostate.
    Fig. 16. Schematic images. (A) Red dotted lines depict anterolateral dissection behind the Denonvilliers fascia (DVF), and this dissection plane meets with posterolateral pelvic dissection along the parietal pelvic fascia (PPF), while preserving the hypogastric nerve (HGN) and division of rectosacral fascia. (B) The orange dotted line indicates the proposed dissection line. DVF and its lateral border meet with the PPF. Underneath this fascia, the neurovascular bundle (NVB) and HGN are present. IHN; inferior hypogastric nerve; MRF, mesorectal fascia; PP, pelvic plexus; R, rectum; MR, mesorectum; SV, seminal vesicle.
    Fig. 17. A schematic image of the Gate approach illustrates one way to obtain a complete total mesorectal excision specimen in a deep narrow pelvic cavity. The red box area depicts a dissection area with the Gate approach. There will be a sharp pelvic dissection between the mesorectal fascia and pelvic floor. PP, pelvic plexus. Adapted and reproduced from Kim et al. [51], available under the Creative Commons License.
    Fig. 18. The concept of customized Denonvilliers fascia (DVF) excision. (A) A schematic sagittal view of the pelvis illustrating the anterior dissection plane. The red dotted line depicts the suggested dissection plane for early stage tumor (e.g., T1, T2), preserving the DVF and reducing the risk of nerve damage while ensuring circumferential margin negativity. (B) For more advanced tumor, especailly those anteriorly located, excising the DVF might be necessary to achieve circumferential resection margin negativity. (C) Under third robotic arm upward traction of the seminal vesicle, the whitish membrane-like DVF was exposed, robotic scissor incised it, and sharp dissection proceeded behind the DVF. MR, mesorectum; P, prostate; R, rectum; SV, seminal vesicle.
    Fig. 19. The rectal proper fascia adheres to the mesh-like pelvic plexus at the lateral pelvic wall. The fine branches from the pelvic plexus enter the rectal wall.
    Fig. 20. The blue dotted line depicts a division line of partial levator ani muscle. On the left side, the part of the levator ani muscle invaded by the tumor is excised; however, on the right side, the levator ani muscle is preserved. DL, dentate line; IAS, internal anal sphincter; EAS, external anal sphincter; ISS, intersphincteric space. Adapted from Varela and Kim [44], available under the Creative Commons License.
    Fig. 21. Comparison of rectal magnetic resonance imaging before and after partial excision of the involved levator ani muscle (PELM) shows an absence of right-side levator ani muscle plate. (A) Before PELM, tumor involved the right side of levator ani muscle partially. (B) After PELM, left side levator ani muscle can be identified, while right side of levator ani already excised.
    Fig. 22. (A, B) Local recurrence near the anastomosis site after total mesorectal excision. Red arrows indicate recurrence near the anastomosis.

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    Essential knowledge and technical tips for total mesorectal excision and related procedures for rectal cancer
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