An update on minimally invasive treatment of colorectal cancer: a narrative review

Introduction

Background

Colorectal cancer (CRC) is a major source of morbidity and mortality in the United States and throughout the world. The American Cancer Society (ACS) estimates that in 2024, 106,590 new patients will be diagnosed with colon cancer and 46,220 with rectal cancer, making CRC the fourth most commonly diagnosed form of cancer behind breast, prostate, and lung cancers (1,2). The National Cancer Institute (NCI) estimates that 53,010 patients will succumb to their CRC this year, making it the second deadliest form of cancer behind lung cancer (3). Although its overall incidence in adults over the age of 55 years has decreased, particularly due to a focus on screening, the incidence of CRC in adults younger than 55 years has steadily increased by 1–2% annually since the 1990s for reasons that are still unclear (2). Virostko et al. assessed the trend in age at diagnosis of CRCs. In 2004, 10% of cancer diagnoses occurred in patients under the age of 50 years, increasing to 12.2% by 2015. Additionally, 51.6% of patients diagnosed before age 50 years had stage III or IV disease, compared to 40% of those diagnosed after age 50 years (4). There has been an increasing amount of focus regarding the optimal medical and surgical approach to treating CRC. In 2022 alone, the NCI appropriated over $257 million for CRC research (5). While rapid advances in our understanding of tumor biology and consequent discoveries of new anti-tumor agents offer promising results, surgical resection remains the backbone of curative CRC therapy. In this narrative review, we will explore recent advances in the surgical management of CRC with a focus on minimally invasive techniques.

Rationale and knowledge gap

The advent of new technology and surgical techniques has only added to the surgical armamentarium available to treat colon and rectal cancer. This updated review of the literature aims to both highlight the available therapies and address gaps in the literature for surgeons to provide the highest level of care to patients with CRC.

Objective

In this updated review, we aim to explore the existing evidence, highlight novel developments, and suggest potential areas for future research regarding minimally invasive techniques in colorectal surgery, that may further improve our care of patients with CRC. We present this article in accordance with the Narrative Review reporting checklist (available at https://asj.amegroups.com/article/view/10.21037/asj-24-39/rc).

Methods

A literature review was carried out using the PubMed database (Table 1). Search terms of “colorectal cancer”, “minimally invasive surgery”, “laparoscopic surgery”, “robotic surgery”, and “endoscopic surgery” were used. Papers published between January 1993 and December 2023 were eligible for review. Papers were excluded if not written in English and if the referenced procedure was not related to colon and rectal cancer. The authors further reviewed what were considered landmark papers at the time of publication and selected 55 papers ranging from case series to meta-analysis studies to be included in the updated review of the literature (Table 2).

Discussion

Laparoscopic surgery (LS) for CRC

In September 1983, Dr. Semm performed the first laparoscopic appendectomy at the University of Kiel (59). Since then, the use of laparoscopy has been adopted across various surgical specialties as an alternative to traditional, open techniques. There have been numerous studies aimed at examining the short- and long-term benefits of laparoscopy for the treatment of CRC. In a prospective randomized controlled trial (RCT), Schwenk et al. found that the use of LS for colorectal resections decreased postoperative analgesic requirements (6). In a separate Cochrane meta-analysis of 25 RCTs, Schwenk et al. reported that patients undergoing laparoscopic colorectal resection on average experience less blood loss, postoperative pain, and time to return of bowel function with reduction in overall length of stay by 1.5 days compared to open surgery (OS) (7). Other investigators have found that despite an objective improvement in surrogate measures for pain in patients receiving LS, the difference between subjective pain perception in patients receiving LS or OS is murkier. Weeks et al. found statistically significant but clinically modest decreases in duration of postoperative analgesia in LS patients compared to OS patients; however, they did not find any statistically significant difference in subjective pain perception scores of the 428 patients analyzed (8).

Despite these short-term advantages, the adoption of laparoscopy in the treatment of CRC had initially been slow, in part due to fear of an inferior oncologic resection and increased recurrence rates, especially amid isolated case reports of abdominal wall recurrence along trocar sites (9-12). Until recently, few studies had examined long-term oncological outcomes of LS compared to traditional open approaches for CRC (7,13). There is now an abundance of data showing equivalent outcomes between laparoscopic and open interventions. Between 1997 and 2003, the COlon cancer Laparoscopic or Open Resection (COLOR) trial randomized 1,248 patients across 29 centers in eight countries with solitary left or right non-metastatic colon cancer to LS or OS. Three-year results published in 2009 reported that there was a slight difference in disease-free survival in favor of open colectomy [2.0%; 95% confidence interval (CI): −3.2% to 7.2%] (14). However, the authors concluded that the difference was minute and that a laparoscopic approach was still viable. Subsequently, in 2017, Deijen et al. published 10-year outcomes for 256 Dutch patients enrolled in the study. They reported comparable disease-free (45.2% vs. 43.2%, P=0.96), overall (48.4 vs. 46.7%, P=0.83), and stage-specific survival rates for LS and OS groups, as well as comparable overall recurrence rates (29.4% vs. 28.2%, P=0.73) and incidence of port- or wound-site recurrences (laparoscopic =3 vs. open =4) (15). However, it is important to note that this study only examines the Dutch cohort of the original COLOR trial, representing only a quarter of the entire study population. Similarly, the 10-year outcomes of the Medical Research Council Conventional vs. Laparoscopic-Assisted Surgery In Colorectal Cancer (MRC CLASICC) trial, a multicenter analysis of 794 patients who were randomized to either LS or OS between 1996 and 2002, showed no significant difference in long-term overall and disease-free survival for colon or rectal cancer (16,17). This trial also showed no significant difference in local and distant recurrence rates for LS compared to OS. The Clinical Outcomes of Surgical Therapy (COST) Study Group also demonstrated non-inferiority of LS compared to OS for colon cancer. In 2007, long-term results of 872 patients across 48 institutions demonstrated that 5-year disease-free survival (69.2% vs. 68.4%, P=0.94) and 5-year overall survival (76.4% vs. 74.6%, P=0.93) were similar for LS or OS groups (18). Long-term data from these trials have also shown that port-site recurrence along the abdominal wall following LS for CRC is a relatively rare entity, and its incidence is comparable to surgical site recurrence along the abdominal wall following OS. In the COLOR trial, 7 patients (1.3%) in the LS group developed recurrence at the trocar or extraction site along the abdominal wall, compared to 2 patients (0.4%) in the OS group (14). In the COST trial, 2 patients (0.5%) in the LS group and 1 patient (0.2%) in the OS experienced recurrence in surgical wounds (19). In the CLASICC trial, 10 patients (1.9%) in the LS group and 2 patients (0.7%) in the OS group experienced wound or port-site recurrence, without a statistically significant difference between the two groups (18). In 2008, a Cochrane systematic review and meta-analysis of 12 RCTs including 3,346 patients found no difference in recurrence rates at either the primary site or distant sites, or in port-site, wound, and peritoneal recurrences (20). With regards to rectal cancer, two RCTs published in 2015 initially called into question the equivalence of laparoscopy compared to OS. The ACOSOG Z6051 trial randomized 486 patients [2008–2013] with stage II/III rectal cancer within 12 cm of the anal verge to laparoscopic vs. open resection (60). The primary outcome was a surgical success composite of circumferential radial margin greater than 1 mm, distal margin without tumor, and completeness of total mesorectal excision (TME). Conversion to open was required in 11.3% of cases, and operative time was significantly prolonged by an average of 45 minutes with a laparoscopic compared to an open approach (60). Whereas secondary outcomes such as complication and readmission rates were similar, overall surgical success was lower in the laparoscopic (81.7%) compared to the open resection arm (86.9%) and did not meet criteria for non-inferiority (P=0.41) (60). Similarly, the Australasian Laparoscopic Cancer of the Rectum (ALaCaRT) trial randomized 475 patients across 24 sites in Australia and New Zealand [2010–2014] with T1–T3 rectal adenocarcinoma less than 15 cm from the anal verge to either laparoscopic or open resection (61). The primary endpoint was a composite of assessing adequate surgical resection, including complete TME, a clear circumferential margin (≥1 mm), and a clear distal resection margin (≥1 mm). Successful resection was achieved in 194 patients (82%) in the LS group and 208 patients (89%) in the OS group, which also did not meet criteria for non-inferiority (P=0.38) (61). Whereas both ACOSOG Z6051 and ALaCaRT failed to show non-inferiority of laparoscopic compared to OS in terms of pathological outcomes, longer-term oncologic outcomes were evaluated in follow-up studies published in 2019. At median follow-up of 47.9 months, ACOSOG Z6051 found no statistically significant difference between laparoscopic and open resection in terms of 2-year disease-free survival (79.5% vs. 83.2%), local and regional recurrence (4.6% vs. 4.5%, and distant recurrence (14.6% vs. 16.7%) (21). Similarly, at a median follow-up of 3.2 years in the ALaCaRT trial, cumulative incidence of locoregional recurrence at 2 years (5.4% vs. 3.1%), disease-free survival (80% vs. 82%), and overall survival (94% vs. 93%) were not statistically different in the laparoscopic compared to open groups (22). Additional RCTs have further supported these findings of equivalent disease-free and overall survival rates (21,23).

With the implementation of any novel technology or procedure, there is also a learning curve that can affect individual surgeon performance and patient outcomes. Assessment of learning curves for laparoscopic right and left hemicolectomies and low anterior resections for rectal cancer have been evaluated. Tekkis et al. and Park et al. used similar models evaluating surgical time, conversion to OS, readmission rates, and complications for left and right hemicolectomies and low anterior resections (24,25). Optimal proficiency was reached after 55 cases for right hemicolectomy, 62 cases for left hemicolectomy, and 92 cases for low anterior resections (24,25). In addition to surgeon proficiency, overall hospital case volume can also affect surgical outcomes. The COLOR study group compared a variety of outcomes among participating centers assigned to either low, medium, or high case volume groups. Surgeons at high case volume hospital reported shorter skin-to-skin times compared to medium and low volume hospitals (188 vs. 210 vs. 240 min, P<0.001) (26). Surgeons at high case volume hospitals also harvested more lymph nodes (12 vs. 9 vs. 9, P<0.001) and had lower rates of conversion to OS (9% vs. 24% vs. 24%, P<0.001) when compared to medium and low volume hospitals (26). Enhanced recovery after surgery (ERAS) protocols were first established in the early 2000s, with the goal of accelerating recovery of patients through minimizing physiologic stressors. Components of the ERAS protocol include carbohydrate loading, judicious fluid management, and early nutrition in the postoperative period. These interventions significantly impacted the length of stay, complication rates, and readmission rates. Length of hospital stay (LOS) and complication rates are often the primary outcomes assessed when evaluating ERAS protocols and have been successfully reproduced in multiple healthcare settings regardless of resource status. Ban et al. reviewed compliance with ERAS protocols demonstrating it had significant impact on shorter LOS, reduced postoperative complications, and decreased admission rates (27). Thiele et al. also found that ERAS protocols positively impacted the LOS and postoperative complication rates for both OS and LS and increased patient satisfaction (28).

Robotic surgery (RS) for CRC

RS has been increasingly used across various surgical disciplines, including for the treatment of non-cancerous colorectal pathology. With the advent of tremor-free instruments, three-dimensional video, multiple degrees of motion with improved ergonomics and wrist articulation, and, more recently, tactile feedback, robotic technology is undoubtedly a valuable surgical tool. There has been a significant amount of research as to whether this cutting-edge technology leads to improved oncologic outcomes. Lorenzon et al. examined 22 studies including 1,652 laparoscopic and 1,120 robotic-assisted resections and further stratified their analysis into right, left, and pelvic resections of the rectum. They found that LS was associated with quicker operative time and lower costs [standardized mean difference (SMD) =0.686 and 0.493] while RS had better morbidity outcomes [odds ratio (OR) =0.763], although these differences were not significant when examining solely the randomized trials (29). With further stratification, the authors also demonstrated that a laparoscopic approach was associated with a statistically significant decreased operating time in left-sided and pelvic disease (SMD =0.609 and 0.529) and blood loss in pelvic disease (SMD =0.339) (29). In overall studies, the morbidity rate range was 10.3% to 33.3% in the LS group and 5.9% to 30.6% in the RS group (29). However, these findings were not replicated in the randomized trial analysis group.

A more recent meta-analysis by Solaini et al. examined 11 studies that included 52,589 patients (LS group 39,083, RS group 13,506) who underwent left-sided colectomy for either benign or malignant disease. They demonstrated that RS, despite being associated with a longer operative time, was also associated with a decreased rate of overall complications, anastomotic leaks, and superficial wound infection for the treatment of benign disease (30). However, in their subgroup analysis on malignant disease (LS group 452, RS group 259), the only trend that remained significant was an increased operating time in the RS group [pooled weighted mean difference (WMD) 30.1; 95% CI: 23.4–36.8; P=0.002] (30). The authors did note that there may have been a selection bias present, given that patients undergoing oncologic resection who were noted to be at higher risk underwent LS.

The Robotic vs. Laparoscopic Resection for Rectal Cancer (ROLARR) trial, which compared the two approaches for curative management of rectal cancer, assessed whether a robotic approach was associated with a decreased conversion to laparotomy when compared with a laparoscopic approach (31). The authors demonstrated that there was no statistically significant benefit with regards to this endpoint with 10.1% in the robotic assisted group required conversion vs. 12.2% in standard laparoscopic group [unadjusted risk difference =4.1% (95% CI: −1.4% to 9.6%); adjusted OR =0.61 (95% CI: 0.31 to 1.21); P=0.16] (31). There was also no demonstrated statistically significant benefit with regards to the secondary end-points that were examined in this study, such as intraoperative and postoperative complications, circumferential resection margin (CRM) positivity, quality of life, bladder and sexual dysfunction, and 30-day mortality. Although the authors did enforce a minimum level of experience for participating surgeons, operations in this trial were performed by a surgeon who was an expert in LS, but still in the learning phase for robotic-assisted LS. As the authors note, it may be that a robotic approach may yield some benefit as surgeon experience level increases.

Overall, these results show that RS is likely associated with decreased short-term postoperative complications, an association that may be especially more impactful in benign disease. However, these benefits must be balanced with an increased cost to the patient and a longer operative time. These trade-offs could likely be mitigated with an enhanced focus on robotic surgical training and simulation-based education across all training levels.

Although there is analysis of short-term data comparing RS and LS, there are relatively few studies that have examined whether there is a difference in overall survival. Park et al., in their RCT of 71 patients (LS group 36, RS group 35) who underwent robot-assisted colectomy vs. laparoscopic-assisted colectomy for right-sided colon cancer, demonstrated that there was no significant difference in 3- or 5-year disease-free survival or overall survival (24). In fact, when analyzing prognostic factors, their analysis revealed similar disease-free surgical (P=0.24) (24). Like prior studies, the authors also demonstrated that RS was associated with a longer operative time (195 vs. 129 min, P<0.001) and higher cost ($12,235 vs. $10,319, P=0.013) (24). Similarly, Cuk et al., in their retrospective analysis of 7,565 patients (LS group 6,905, RS group 660) undergoing resection for stage I–III colon cancer demonstrated no significant difference in all-cause (hazard ratio =0.98; 95% CI: 0.82–1.17; P=0.78) or colon cancer-specific morality (hazard ratio =0.89; 95% CI: 0.67–1.18; P=0.41) at the 3-year mark (32). However, the authors did show that patients undergoing LS had an increased risk of recurrence (LS =1,178, RS =82, P=0.002) and decreased recurrence-free survival (hazard ratio =0.80; 95% CI: 0.64–1.00; P=0.049) (32). Notably, a prior systematic review by Cuk et al. with 55 studies and 5,357 patients (LS group 4,617, RS group 740) had actually demonstrated an improved 3-year overall and disease-free survival for patients undergoing robotic resection of right-sided colon cancer (62). In a separate study that randomized patients undergoing TME for rectal cancer to RS or LS, Lei et al. determined that RS did not confer an overall or disease-free-survival benefit to patients. Furthermore, the authors demonstrated a statistically significant decrease in overall complications in the RS group (33). However, of the fifteen short- and long-term complications that were analyzed, only urinary retention was significantly decreased in the RS group.

As these results show, although there are short-term benefits to a robotic approach, it is unclear whether RS provides an increased survival benefit when compared to a laparoscopic approach. Given the relative novelty of RS, further research is needed to definitively delineate which patient population, if any, would benefit. Cost effectiveness is determined by comparing the cost relative to the outcome. Kim et al. reviewed the cost-effectiveness of RS vs. LS for rectal cancer based on short-term outcomes in a Korean population. They determined that there was no difference in short-term outcomes, but RS was associated with a significantly higher cost (34). These elevated costs were due to increased operating times and the cost of operating equipment. The group notes that given the robot is a surgical tool that continues to be refined these costs will continue to change and will require reassessment. Hancock et al. also sought to assess cost-effectiveness of RS in the elective setting and compared it to laparoscopic and open colectomies. During their study period, a standardized surgical procedure was adopted. This protocol called for a dedicated robotic operating room team, standard instrument use, and routine use of sequential operative steps. This significantly reduced the total cost of RS via decreased operative use time 279 vs. 431 minutes (35). They also found that that low anterior resections performed robotically were significantly less expensive $14,093 vs. $17,314 (35).

Variations on LS

Variations on traditional LS, such as single-incision and hand-assisted LS (HALS), have become increasingly popular in an attempt to expand on the use and outcomes of LS.

Single-incision laparoscopic colectomy (SILC), a variation on traditional multiport laparoscopic colectomy (TMLC), was first reported by Bucher et al. and Remzi et al. in 2008 for right hemicolectomy through a single umbilical port for two patients with ascending colon polyps (36,37). Since then, the SILC technique has been adequately used for various indications, including complete oncologic resection for CRC (38).

Data show that SILC is a feasible and safe variation on TMLC. In a case series of over 400 SILC, only 17 cases required the placement of additional ports, and 7 cases required conversion to an open procedure (39). Further, Huscher et al. found no difference in operative time, morbidity, or mortality between SILC and TMLC in a prospective randomized clinical trial (40).

In SILC, forgoing the lateral ports utilized in TMLC improves cosmesis by reducing the number of incisions. However, SILC has been shown to improve postoperative outcomes beyond cosmetic, specifically length of stay and postoperative pain. Papaconstantinou et al. found SILC was associated with a significantly shorter length of stay (>1 hospital day) and decreased maximum pain score on postoperative days 1 and 2, when compared to TMLC (41). Similarly, in an RCT of 50 patients, those who underwent SILC had significantly lower median pain scores and shorter median hospital stays compared to those who underwent TMLC (42).

HALS is a fusion of OS and LS that includes a small laparotomy incision with the traditional laparoscopic ports which allows the surgeon’s hand to enter the abdominal cavity without disrupting pneumoperitoneum. This technique allows for tactile sensation and is favored for its potential to provide the benefits of LS, such as decreased postoperative pain and shorter hospital stay, while mitigating some of the drawbacks, such as longer operative time. A meta-analysis comparing HALS and OS for CRC found that HALS was associated with longer operative time, less blood loss, fewer total and postoperative hospital days, less wound infection, and less postoperative complications but was not associated with differences in reoperation, anastomotic leak, or mortality (43). A meta-analysis comparing HALS and LS for benign and malignant colorectal disease found no difference in operating time or perioperative complication rates (44). A query of the National Surgical Quality Improvement Program (NSQIP) demonstrated that when comparing HALS and LS for elective colectomies, HALS was associated with higher risk of wound complications and readmission but was not associated with shorter operative time (45). These findings suggest that HALS preserves some of the advantages of LS over OS regarding blood loss and postoperative recovery. However, it does not significantly shorten operative time and may increase risk of wound infection compared to LS, and therefore should be reserved as a favorable alternative to OS for patients and pathologies not amenable to a purely laparoscopic approach.

Endoscopic resection of CRC

Whereas screening colonoscopy has long played a critical role in detection of CRC, advances in endoscopic skills and technologies now allow for resection of not only benign polyps but also small malignant lesions. Endoscopic full-thickness resection (EFTR) can be offered to patients with T1 cancers less than 2 cm in size. EFTR is particularly useful in patients with low-risk and benign lesions as the procedure does not require hospitalization and helps patients to avoid unnecessary surgical intervention. Fahmawi et al. performed a meta-analysis of EFTR evaluating primary outcomes of technical success, R0 resection and complications. Data demonstrated a technical success rate of 89.25% (95% CI: 86.4–91.7%) (46). An R0 resection was achieved in 82.4% (95% CI: 79.0–85.5%) (46). Complications which included minor and major bleeding, post-polypectomy syndrome and perforation occurred in 10.2% of all procedures (46,47). With the continued advancements made in artificial intelligence (AI), its uses in society and medicine will continue to grow. Its application to pattern recognition has shown promise in the assistance of colon polyp detection. Adenoma detection rate (ADR) is one of the key metrics to ensure endoscopists are adequately assessing the colon. With the use of real-time AI technology, Wang et al. found an ADR increase from 20.3% to 29.1% which was statistically significant (48). This statistically significant change was largely due to increased identification of diminutive adenomas and hyperplastic polyps with no difference in large adenoma detection. Hassan et al. performed a meta-analysis of computer-aided detection vs. standard colonoscopy. Twenty-one studies included 18,232 patients and found that while ADR was increased, more non-neoplastic polyps were removed, and the inspection time was only marginally increased (49).

Transanal resection of rectal cancer

The standard of care for resection of rectal cancer involves mesorectal excision with a clear CRM. Tumors in the upper third of the rectum can typically be treated with TME, whereas tumors in the mid- to lower-third of the rectum are more amenable to TME. There has been extensive research into the oncologic efficacy of trans-anal resection, including transanal excision (TAE), transanal endoscopic microsurgery (TEM), and transanal minimally invasive surgery (TAMIS) as an alternative to radical resection, specifically in patients with favorable tumor morphology (such as <3 cm in size, well- to moderately-differentiated, and without perineural or perivascular invasion) (50). Importantly, patients that undergo TAE must subsequently be carefully monitored for recurrence of disease. Additionally, even in carefully selected groups of patients, transanal resection has been shown to have increased rates of local recurrence (50-52).

In fact, some studies demonstrating decreased disease-free survival for the treatment of early-stage rectal cancer with subsequent, aggressive monitoring for recurrence of disease (53-55). Numerous studies have demonstrated that transanal resection of early-stage rectal cancers may be a viable option in a select group of patients with favorable tumor biology. Patients who have tumors <3 cm in size that are well- to moderately-differentiated and without perineural or lymphovascular invasion. However, these patients need to be adequately counseled that they are at higher risk for local recurrence (50,56).

Intraoperative adjuncts

It is well documented that many factors, both surgeon-dependent and independent, affect anastomotic leaks. These include tension at the site, type of anastomosis, nutritional status, immune status, stump perfusion, and various others. While many of these factors can be objectively or subjectively measured, vascular perfusion of the anastomotic site is a much more elusive entity. Indocyanine green (ICG), a cyanine-based fluorescent dye that tightly binds plasma proteins, can be used along with infrared cameras to visualize perfusion intra-operatively and provide feedback to the surgeon regarding stump viability in real time. Safiejko et al. describe the use of ICG as an adjunct to determine whether there is adequate blood supply at the anastomotic site, with the intent to reduce anastomotic leaks (57). With minimal change to the well-established laparoscopic and robotic surgical procedure, it provides real-time indicator of blood supply. This adjunct provides a statistically significant reduction in anastomotic leak rate from 7.6% to 3.7% (57). In a single-center randomized trial of 252 patients, De Nardi et al. demonstrated that while ICG can be used to assess the degree of colic stump perfusion, even in visually normal stumps, its use as an adjunct in surgery has not been demonstrated to have a meaningful reduction in rates of anastomotic leakage, even when ICG demonstrates inadequate stump perfusion requiring additional stump resection (58).

Conclusions

The treatment of CRC has typically involved surgical resection in conjunction with a combination of chemotherapy and radiation. Over time, the use of LS and RS has become the preferred option given similar oncologic outcomes and improved pain, hospital length of stay, and decreased complication rates. The advancement in robotic technology, medical devices, and pharmaceuticals will continue to push the boundary on the minimally invasive approach that can provide safe oncologic outcomes in the management of CRC.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at: https://asj.amegroups.com/article/view/10.21037/asj-24-39/rc

Peer Review File: Available at: https://asj.amegroups.com/article/view/10.21037/asj-24-39/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://asj.amegroups.com/article/view/10.21037/asj-24-39/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. SEER. Cancer Stat Facts: Colorectal Cancer. [Cited 2024 Oct 7]. Available online: https://seer.cancer.gov/statfacts/html/colorect.html
2. American Cancer Society. Colorectal Cancer Statistics. Key Statistics for Colorectal Cancer. [Cited 2024 Oct 7]. Available online: https://www.cancer.org/cancer/types/colon-rectal-cancer/about/key-statistics.html
3. SEER. Cancer Stat Facts: Cancer of Any Site. [Cited 2024 Sep 7]. Available online: https://seer.cancer.gov/statfacts/html/all.html
4. Virostko J, Capasso A, Yankeelov TE, et al. Recent trends in the age at diagnosis of colorectal cancer in the US National Cancer Data Base, 2004–2015. Cancer 2019;125:3828-35. [Crossref] [PubMed]
5. NCI. NCI Budget Fact Book. Funding for Research Areas. 2022 [cited 2024 Oct 9]. Available online: https://www.cancer.gov/about-nci/budget/fact-book/data/research-funding
6. Schwenk W, Böhm B, Müller JM. Postoperative pain and fatigue after laparoscopic or conventional colorectal resections. A prospective randomized trial. Surg Endosc 1998;12:1131-6.
7. Schwenk W, Haase O, Neudecker J, et al. Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev 2005;2005:CD003145. [Crossref] [PubMed]
8. Weeks JC, Nelson H, Gelber S, et al. Short-term quality-of-life outcomes following laparoscopic-assisted colectomy vs open colectomy for colon cancer: a randomized trial. JAMA 2002;287:321-8. [Crossref] [PubMed]
9. Fusco MA, Paluzzi MW. Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon. Report of a case. Dis Colon Rectum 1993;36:858-61. [Crossref] [PubMed]
10. Berends FJ, Kazemier G, Bonjer HJ, et al. Subcutaneous metastases after laparoscopic colectomy. Lancet 1994;344:58. [Crossref] [PubMed]
11. Cirocco WC, Schwartzman A, Golub RW. Abdominal wall recurrence after laparoscopic colectomy for colon cancer. Surgery 1994;116:842-6.
12. Koea JB, Lanouette N, Paty PB, et al. Abdominal wall recurrence after colorectal resection for cancer. Dis Colon Rectum 2000;43:628-32. [Crossref] [PubMed]
13. Reza MM, Blasco JA, Andradas E, et al. Systematic review of laparoscopic versus open surgery for colorectal cancer. Br J Surg 2006;93:921-8. [Crossref] [PubMed]
14. Colon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 2009;10:44-52.
15. Deijen CL, Vasmel JE, de Lange-de Klerk ESM, et al. Ten-year outcomes of a randomised trial of laparoscopic versus open surgery for colon cancer. Surg Endosc 2017;31:2607-15. [Crossref] [PubMed]
16. Jayne DG, Thorpe HC, Copeland J, et al. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 2010;97:1638-45. [Crossref] [PubMed]
17. Green BL, Marshall HC, Collinson F, et al. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 2013;100:75-82. [Crossref] [PubMed]
18. Fleshman J, Sargent DJ, Green E, et al. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 2007;246:655-62; discussion 662-4. [Crossref] [PubMed]
19. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350:2050-9. [Crossref] [PubMed]
20. Kuhry E, Schwenk WF, Gaupset R, et al. Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev 2008;2008:CD003432. [Crossref] [PubMed]
21. Fleshman J, Branda ME, Sargent DJ, et al. Disease-free Survival and Local Recurrence for Laparoscopic Resection Compared With Open Resection of Stage II to III Rectal Cancer: Follow-up Results of the ACOSOG Z6051 Randomized Controlled Trial. Ann Surg 2019;269:589-95. [Crossref] [PubMed]
22. Stevenson ARL, Solomon MJ, Brown CSB, et al. Disease-free Survival and Local Recurrence After Laparoscopic-assisted Resection or Open Resection for Rectal Cancer: The Australasian Laparoscopic Cancer of the Rectum Randomized Clinical Trial. Ann Surg 2019;269:596-602. [Crossref] [PubMed]
23. Jeong SY, Park JW, Nam BH, et al. Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol 2014;15:767-74. [Crossref] [PubMed]
24. Park JS, Kang H, Park SY, et al. Long-term oncologic after robotic versus laparoscopic right colectomy: a prospective randomized study. Surg Endosc 2019;33:2975-81. [Crossref] [PubMed]
25. Tekkis PP, Senagore AJ, Delaney CP, et al. Evaluation of the learning curve in laparoscopic colorectal surgery: comparison of right-sided and left-sided resections. Ann Surg 2005;242:83-91. [Crossref] [PubMed]
26. Bonjer HJ, Deijen CL, Abis GA, et al. A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med 2015;372:1324-32. [Crossref] [PubMed]
27. Ban KA, Berian JR, Ko CY. Does Implementation of Enhanced Recovery after Surgery (ERAS) Protocols in Colorectal Surgery Improve Patient Outcomes? Clin Colon Rectal Surg 2019;32:109-13. [Crossref] [PubMed]
28. Thiele RH, Rea KM, Turrentine FE, et al. Standardization of care: impact of an enhanced recovery protocol on length of stay, complications, and direct costs after colorectal surgery. J Am Coll Surg 2015;220:430-43. [Crossref] [PubMed]
29. Lorenzon L, Bini F, Balducci G, et al. Laparoscopic versus robotic-assisted colectomy and rectal resection: a systematic review and meta-analysis. Int J Colorectal Dis 2016;31:161-73. [Crossref] [PubMed]
30. Solaini L, Bocchino A, Avanzolini A, et al. Robotic versus laparoscopic left colectomy: a systematic review and meta-analysis. Int J Colorectal Dis 2022;37:1497-507. [Crossref] [PubMed]
31. Jayne D, Pigazzi A, Marshall H, et al. Effect of Robotic-Assisted vs Conventional Laparoscopic Surgery on Risk of Conversion to Open Laparotomy Among Patients Undergoing Resection for Rectal Cancer: The ROLARR Randomized Clinical Trial. JAMA 2017;318:1569-80. [Crossref] [PubMed]
32. Cuk P, Kaalby L, Deding U, et al. Long-term Outcomes of Robot-assisted Versus Laparoscopic Surgery for Colon Cancer: A Nationwide Register-based Cohort Study. Ann Surg 2024;279:456-61. [Crossref] [PubMed]
33. Lei X, Yang L, Huang Z, et al. No beneficial effect on survival but a decrease in postoperative complications in patients with rectal cancer undergoing robotic surgery: a retrospective cohort study. BMC Surg 2021;21:355. [Crossref] [PubMed]
34. Kim CW, Baik SH, Roh YH, et al. Cost-effectiveness of robotic surgery for rectal cancer focusing on short-term outcomes: a propensity score-matching analysis. Medicine (Baltimore) 2015;94:e823. [Crossref] [PubMed]
35. Hancock KJ, Klimberg VS, Nunez-Lopez O, et al. Optimizing outcomes in colorectal surgery: cost and clinical analysis of robotic versus laparoscopic approaches to colon resection. J Robot Surg 2022;16:107-12. [Crossref] [PubMed]
36. Bucher P, Pugin F, Morel P. Single port access laparoscopic right hemicolectomy. Int J Colorectal Dis 2008;23:1013-6. [Crossref] [PubMed]
37. Remzi FH, Kirat HT, Kaouk JH, et al. Single-port laparoscopy in colorectal surgery. Colorectal Dis 2008;10:823-6. [Crossref] [PubMed]
38. Law WL, Fan JK, Poon JT. Single-incision laparoscopic colectomy: early experience. Dis Colon Rectum 2010;53:284-8. [Crossref] [PubMed]
39. Keller DS, Haas EM. Single-Incision Laparoscopic Colon and Rectal Surgery. Clin Colon Rectal Surg 2015;28:135-9. [Crossref] [PubMed]
40. Huscher CG, Mingoli A, Sgarzini G, et al. Standard laparoscopic versus single-incision laparoscopic colectomy for cancer: early results of a randomized prospective study. Am J Surg 2012;204:115-20. [Crossref] [PubMed]
41. Papaconstantinou HT, Sharp N, Thomas JS. Single-incision laparoscopic right colectomy: a case-matched comparison with standard laparoscopic and hand-assisted laparoscopic techniques. J Am Coll Surg 2011;213:72-80; discussion 80-2. [Crossref] [PubMed]
42. Poon JT, Cheung CW, Fan JK, et al. Single-incision versus conventional laparoscopic colectomy for colonic neoplasm: a randomized, controlled trial. Surg Endosc 2012;26:2729-34. [Crossref] [PubMed]
43. Zhang X, Wu Q, Gu C, et al. Hand-assisted laparoscopic surgery versus conventional open surgery in intraoperative and postoperative outcomes for colorectal cancer: An updated systematic review and meta-analysis. Medicine (Baltimore) 2017;96:e7794. [Crossref] [PubMed]
44. Moloo H, Haggar F, Coyle D, et al. Hand assisted laparoscopic surgery versus conventional laparoscopy for colorectal surgery. Cochrane Database Syst Rev 2010;CD006585. [Crossref] [PubMed]
45. Gilmore BF, Sun Z, Adam M, et al. Hand-Assisted Laparoscopic Versus Standard Laparoscopic Colectomy: Are Outcomes and Operative Time Different? J Gastrointest Surg 2016;20:1854-60. [Crossref] [PubMed]
46. Fahmawi Y, Hanjar A, Ahmed Y, et al. Efficacy and Safety of Full-thickness Resection Device (FTRD) for Colorectal Lesions Endoscopic Full-thickness Resection: A Systematic Review and Meta-Analysis. J Clin Gastroenterol 2021;55:e27-36. [Crossref] [PubMed]
47. Schmidt A, Beyna T, Schumacher B, et al. Colonoscopic full-thickness resection using an over-the-scope device: a prospective multicentre study in various indications. Gut 2018;67:1280-9. [Crossref] [PubMed]
48. Wang P, Berzin TM, Glissen Brown JR, et al. Real-time automatic detection system increases colonoscopic polyp and adenoma detection rates: a prospective randomised controlled study. Gut 2019;68:1813-9. [Crossref] [PubMed]
49. Hassan C, Spadaccini M, Mori Y, et al. Real-Time Computer-Aided Detection of Colorectal Neoplasia During Colonoscopy: A Systematic Review and Meta-analysis. Ann Intern Med 2023;176:1209-20. [Crossref] [PubMed]
50. Heafner TA, Glasgow SC. A critical review of the role of local excision in the treatment of early (T1 and T2) rectal tumors. J Gastrointest Oncol 2014;5:345-52. [Crossref] [PubMed]
51. Ptok H, Marusch F, Meyer F, et al. Oncological outcome of local vs radical resection of low-risk pT1 rectal cancer. Arch Surg 2007;142:649-55; discussion 656. [Crossref] [PubMed]
52. Hwang Y, Yoon YS, Bong JW, et al. Long-term Transanal Excision Outcomes in Patients With T1 Rectal Cancer: Comparative Analysis of Radical Resection. Ann Coloproctol 2019;35:194-201. [Crossref] [PubMed]
53. Nash GM, Weiser MR, Guillem JG, et al. Long-term survival after transanal excision of T1 rectal cancer. Dis Colon Rectum 2009;52:577-82. [Crossref] [PubMed]
54. Plummer JM, Leake PA, Albert MR. Recent advances in the management of rectal cancer: No surgery, minimal surgery or minimally invasive surgery. World J Gastrointest Surg 2017;9:139-48. [Crossref] [PubMed]
55. Endreseth BH, Myrvold HE, Romundstad P, et al. Transanal excision vs. major surgery for T1 rectal cancer. Dis Colon Rectum 2005;48:1380-8. [Crossref] [PubMed]
56. Verseveld M, Barendse RM, Gosselink MP, et al. Transanal minimally invasive surgery: impact on quality of life and functional outcome. Surg Endosc 2016;30:1184-7. [Crossref] [PubMed]
57. Safiejko K, Tarkowski R, Kozlowski TP, et al. Safety and Efficacy of Indocyanine Green in Colorectal Cancer Surgery: A Systematic Review and Meta-Analysis of 11,047 Patients. Cancers (Basel) 2022;14:1036. [Crossref] [PubMed]
58. De Nardi P, Elmore U, Maggi G, et al. Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc 2020;34:53-60. [Crossref] [PubMed]
59. Semm K. Endoscopic appendectomy. Endoscopy 1983;15:59-64. [Crossref] [PubMed]
60. Fleshman J, Branda M, Sargent DJ, et al. Effect of Laparoscopic-Assisted Resection vs Open Resection of Stage II or III Rectal Cancer on Pathologic Outcomes: The ACOSOG Z6051 Randomized Clinical Trial. JAMA 2015;314:1346-55. [Crossref] [PubMed]
61. Stevenson AR, Solomon MJ, Lumley JW, et al. Effect of Laparoscopic-Assisted Resection vs Open Resection on Pathological Outcomes in Rectal Cancer: The ALaCaRT Randomized Clinical Trial. JAMA 2015;314:1356-63. [Crossref] [PubMed]
62. Cuk P, Kjær MD, Mogensen CB, et al. Short-term outcomes in robot-assisted compared to laparoscopic colon cancer resections: a systematic review and meta-analysis. Surg Endosc 2022;36:32-46. [Crossref] [PubMed]