Hybrid laparo-endoscopic techniques for challenging colorectal lesions: a systematic review

Vol:.(1234567890) Surgical Endoscopy (2025) 39:7160–7171 https://doi.org/10.1007/s00464-025-12243-w REVIEW ARTICLE Hybrid laparo‑endoscopic techniques forchallenging colorectal lesions: asystematic review GiovanniDistefano1,3· CarloAlbertoAmmirati1· MicheleBarbiero1· RobertoPassera2· AlbertoArezzo1 Received: 4 August 2025 / Accepted: 13 September 2025 / Published online: 29 September 2025 © The Author(s) 2025 Abstract Background Colorectal cancer screening has increased the detection of polyps requiring resection, but standard endoscopic techniques such as endoscopic mucosal resection (EMR) or endoscopic submucosal dissection (ESD) are often unsuitable for large, fibrotic, or anatomically challenging lesions. Segmental colectomy remains definitive but carries substantial morbidity, particularly for benign disease. Laparo-endoscopic cooperative surgery (LECS) and related hybrid techniques have emerged as minimally invasive alternatives bridging the gap between endoscopic and surgical resection. Methods A systematic review was performed according to PRISMA guidelines, querying PubMed, Embase, and Cochrane databases (1985–2024). Studies reporting combined laparoscopic-endoscopic resections for colorectal lesions unsuitable for standard endoscopic treatment were included. Outcomes assessed included additional surgery, adenocarcinoma detection, complication rates, surgery for complications, conversion to open surgery, and recurrence. Random-effects models were used to calculate pooled proportions and 95% confidence intervals (CIs). Results Twenty-seven studies encompassing 1112 patients were included. The pooled rate of additional surgery was 5% (95% CI 3–8%; I2 = 0%), including 7% (95% CI 5–9%) for oncologic indications. Adenocarcinoma was identified in 12% of resected lesions (95% CI 8–16%), underscoring limitations of preoperative staging. Overall complications occurred in 7% (95% CI 5–10%), with surgery for complications required in only 1% (95% CI 0–2%). Conversion to open surgery occurred in 2% (95% CI 1–3%). Long-term follow-up demonstrated a local recurrence rate of 3% (95% CI 2–6%; I2 = 0%). Conclusions Hybrid laparoscopic–endoscopic resections are safe, effective, and reproducible options for complex colorectal lesions not amenable to standard endoscopic resection. These techniques achieve low complication and recurrence rates while preserving bowel and minimizing morbidity associated with colectomy. Given the 12% incidence of unexpected adenocarcinoma, intraoperative adaptability and multidisciplinary expertise are essential. Prospective multicenter studies with standardized reporting are needed to refine patient selection and confirm long-term oncologic safety. Keywords Colorectal polyps· Laparo-endoscopic cooperative surgery· Hybrid resection· Minimally invasive surgery· Organ-preserving surgery Colorectal cancer (CRC) is the third most diagnosed malignancy and the second leading cause of cancer-related death globally. Worldwide, over 1.920.000 new CRC cases were reported in 2022 with approximately 904.000 deaths attributed to the disease [1]. Despite an overall decline in both incidence and mortality due to increased screening and improved management, regional disparities persist, largely reflecting unequal implementation of screening programs and differences in risk factor profiles [2]. The adenoma–carcinoma sequence remains the fundamental model for CRC development, with the majority of cancers arising from pre-existing adenomatous polyps or sessile serrated lesions [3]. Accordingly, early detection and endoscopic removal of these lesions represents the most effective strategy to reduce CRC incidence and mortality [4]. Large-scale colonoscopy screening programs have significantly increased the detection rate of colorectal polyps, and Other Interventional Te chniques * Alberto Arezzo alber[email protected] 1 Department ofSurgical Sciences, University ofTurin, Città della Salute e della Scienza di Torino, Turin, Italy 2 Department ofMedical Sciences, University ofTurin, Turin, Italy 3 Doctoral School ofBioengineering andMedico-Surgical Sciences, Politecnico di Torino, Turin, Italy 7161Surgical Endoscopy (2025) 39:7160–7171 leading to widespread adoption of endoscopic resection techniques such as polypectomy, endoscopic mucosal resection (EMR), and endoscopic submucosal dissection (ESD). These techniques are generally safe and effective; however, they may not be feasible for all lesions. Large-scale colonoscopy screening programs have significantly increased the detection rate of colorectal polyps, leading to widespread adoption of endoscopic resection techniques such as endoscopic mucosal resection (EMR), and endoscopic submucosal dissection (ESD). These techniques are generally safe and effective; however, they may not be feasible for all lesions. Large or “complex” polyps—typically defined as lesions > 20mm, involving multiple folds or more than onethird of the colonic circumference, or located in anatomically challenging sites such as the right colon or near the ileocecal valve—are often associated with fibrosis due to prior resection attempts or are morphologically flat (e.g., lateral spreading tumors, LSTs). Such features substantially increase the technical difficulty and risk of complications during standard endoscopic resection. Additionally, piecemeal resection of large lesions often results in uncertain histopathological assessment and may compromise oncologic adequacy. Although traditional surgical resection remains a definitive option for such difficult lesions, it is associated with increased morbidity and mortality, particularly in elderly patients or those with significant comorbidities. Segmental colectomy, while radical, is often unwarranted in cases of benign pathology. To bridge this gap, combined laparoendoscopic approaches have been developed with the aim of minimizing surgical invasiveness while ensuring complete and safe resection of difficult colorectal lesions. LaparoEndoscopic Cooperative Surgery (LECS) and similar collaborative procedures, including laparoscopically assisted endoscopic resection and endoscopic-assisted laparoscopic wedge or full-thickness resections, have gained attention in recent years. These techniques allow for intraoperative endoscopic localization and assessment of the lesion, laparoscopic control of the bowel wall, and selective full-thickness or transmural resection when needed. They offer the potential to preserve more bowel, avoid major colectomies, and enable immediate surgical management in the case of unexpected malignancy or perforation [5, 6]. Several retrospective and prospective series, as well as systematic reviews, have shown promising results in terms of efficacy, complication rates, and oncologic adequacy [7]. This evolving body of evidence highlights the potential role of laparo-endoscopic approaches in the management of complex colorectal neoplasia. However, considerable heterogeneity remains in terms of technique, indications, and reported outcomes. The present systematic review aims to assess the updated safety and efficacy profile of laparo-endoscopic resections for colorectal lesions that are considered unsuitable for standard endoscopic treatment, with a particular focus on recurrence, complications, oncologic outcomes, and the need for further interventions. Material andmethods This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and MetaAnalyses (PRISMA) guidelines [8]. Eligibility criteria All studies published between January 1985 and December 2024 were eligible for inclusion if they reported on patients undergoing combined laparoscopic-endoscopic local resection of colorectal lesions. Eligible procedures included laparoscopically assisted endoscopic polypectomy, endoscopicassisted laparoscopic wedge or full-thickness resection, and other minimally invasive techniques aimed at removing colorectal lesions unsuitable for standard endoscopic treatment. Studies were excluded if they involved extended colorectal resections (e.g., segmental colectomies or hemicolectomies), included fewer than 10 patients, were animal studies, reviews, editorials, position papers, conference abstracts, or book chapters. In cases of suspected patient cohort overlap, only the most recent or complete publication was included. Search strategy A comprehensive literature search was conducted in May 2025 using Embase, PubMed, and the Cochrane Central Register of Controlled Trials. The search string was specifically developed for this review and included terms related to laparoscopy, endoscopy, polypectomy, and colorectal lesions. The complete search strategy is provided as an appendix to this manuscript (Appendix 1). Study selection anddata extraction Two reviewers (GD, MB) independently screened all studies in a three-step process: first by title, then by abstract, and finally through full-text review of potentially eligible articles. Screening and selection were conducted using the Rayyan platform. Any discrepancies were resolved by consensus with a third reviewer (CAA). Data extraction was independently performed by the same two reviewers using pre-defined data collection forms. Extracted variables included study design, country, sample size, patient demographics, lesion characteristics, surgical technique, recurrence, complications, conversion to open 7162 Surgical Endoscopy (2025) 39:7160–7171 surgery, adenocarcinoma detection, and need for additional surgery (either for complications or oncologic reasons). Outcomes The primary outcome of interest was the rate of additional surgery following combined laparoscopic–endoscopic resection. This included both reoperations for postoperative complications and surgeries performed to achieve oncologic radicality. Secondary outcomes included: • Incidence of adenocarcinoma in the resected specimens • Rate of additional oncologic surgery • Overall complication rate • Rate of surgery due to complications • Conversion rate to open surgery • Recurrence rate after local resection Each outcome was calculated as the proportion of lesions or patients meeting the criteria relative to the total included in the corresponding category. Quality assessment andstatistical analysis Risk of bias within individual studies was assessed using the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) tool. Specifically, we evaluated the availability of histological reference standards, completeness of data regarding technical success, and reporting on oncologic adequacy. Following a conservative approach, all outcomes were analysed by a random-effects model, where the proportions of single studies were used to calculate an overall proportion. This model incorporates heterogeneity among studies and takes into account differences in sample size by which proportions were measured in each study; this within-study variation was accountedfor using the exact binomial distribution. Individual and pooled estimates of these proportions together with 95% confidence intervals (CIs) were presented in the Forest plots. Publication bias was assessed by generating a funnelplot and performing the rank correlation test of funnel plot asymmetry. Heterogeneity was assessed by the I2measure of inconsistency, statistically significant if I2 > 50%. Potential sources of heterogeneity wereexplored by two sensitivity analyses: checking the results of cumulative (sequentially including studiesby date of publication) and influence analyses (calculating pooled estimates by omitting one study at atime). All analyses were performed using R 4.5.1 package meta (R Foundation for Statistical Computing, Vienna, Austria). Results A total of 27 studies encompassing 1112 patients were included. A flow diagram of this systematic review, with the number of papers retrieved, included and excluded, as well as the reasons for exclusion, is shown in Fig.1. A developed summary table (Table1) includes the core characteristics of all studies included in this review. The characteristics of the studies and detailed QUADAS quality assessment are also summarized in Table1 and Supplementary Table1, respectively. QUADAS evaluation showed generally high methodological quality: 100% of studies met core criteria such as appropriate patient spectrum, adequate reference standard, short test-reference interval, and blinded interpretation of results. Some variability was observed in reporting of selection criteria and procedural details (items 2, 8, 9), with 8 studies showing partial or unclear reporting. Reporting of outcomes by specific hybrid technique was inconsistent across studies. For example, SerraAracil et al. [31] described different variants of combined endoscopic-laparoscopic surgery, including full-thickness resections and laparoscopically assisted resections, but did not provide stratified complication or recurrence rates. Similarly, Suzuki et al. [25] and Tamegai et al. [23] reported on LECS-CR procedures but presented results in aggregated form without separation by technique. This variability precluded meaningful subgroup analysis and limited the possibility of comparing outcomes across different hybrid approaches. For conceptual clarity, however, the hybrid procedures can be broadly categorized into three groups: (a) laparoscopically assisted EMR, (b) endoscopic-assisted laparoscopic wedge/full-thickness resections, and (c) endoscopic-assisted segmental resections. Primary outcome—additional surgery The overall rate of additional surgery, including both oncologic and complication-related interventions, was5%(95% CI 3–8%; I2 = 0%), indicating excellent inter-study consistency. This represents a substantial reduction compared to standard segmental resections and supports the feasibility of the combined approach (Fig.2). Secondary outcomes Table2 summarizes the proportion of lesions or patients meeting each outcome relative to the total included in the corresponding category. 7163Surgical Endoscopy (2025) 39:7160–7171 • Adenocarcinoma detection rate: adenocarcinoma was identified in 12% of resected lesions (95% CI 8–16%; I2 = 68.8%), highlighting significant heterogeneity in preoperative diagnostic accuracy across studies (Fig.3). • Oncologic surgery requirement: following local resection, 7% of patients (95% CI 5–9%; I2 = 0%) required radical oncologic surgery, primarily due to invasive histology (Fig.4). • Overall complication rate: complications occurred in 7% of patients (95% CI 5–10%; I2 = 25.6%), mainly bleeding, perforation, and localized infections (Fig.5). • Surgery for complications: surgical management was necessary in 1% of cases (95% CI 0–2%; I2 = 0%) (Fig.6). • Conversion to open surgery: conversion was required in 2% of procedures (95% CI 1–3%; I2 = 0%), confirming good intraoperative control even in technically challenging situations (Fig.7). • Local recurrence: long-term follow-up of 992 patients showed a local recurrence rate of 3% (95% CI 2–6%; I2 = 0%), indicating durable local control (Fig.8). Follow-up duration was reported in 18 out of 27 studies, with a median of 20months (range 1–196months). Although reporting methods varied across studies, a sensitivity analysis restricted to studies with at least 12months of follow-up yielded recurrence rates comparable to the overall analysis, thereby confirming the robustness of our results. Discussion This systematic review confirms that combined laparoscopic-endoscopic techniques, such as LECS and its variants, are safe and effective for the treatment of complex colorectal lesions that are not suitable for standard endoscopic Fig. 1 Flow-chart of the literature search in this systematic review 7164 Surgical Endoscopy (2025) 39:7160–7171 Table 1 Core characteristics of all included studies Reference Study design Country Inclusion period Mono/multicentric Patients, n Mean age (years) Male (%) Le Picard (1997) [9] Prospective France 1994–1996 Monocentric 16 56–80 56 Mal (1998) [10] Retrospective France 1990–1997 Monocentric 65 62 58 Ommer (2003) [11] Retrospective Germany 1995–2002 Monocentric 23 70.7 47.8 H. Winter (2007) [12] Prospective Germany 1998–2007 Monocentric 38 66 55 Wilhelm (2009) [13] Prospective Germany 1997–2006 Monocentric 146 64 47 Franklin (2009) [14] Prospective USA 1990–2008 Monocentric 160 74.7 51 DJ. Grunhagen (2011) [15] Prospective The Netherlands 2006–2009 Monocentric 11 73.2 63 Wood (2011) [16] Prospective UK 2008–2009 Monocentric 13 66 33 Yan (2011) [17] Retrospective USA 2003–2008 Monocentric 23 70 61 Jang (2012) [5] Retrospective USA / Monocentric 26 60.7 39 Sang W. Lee (2014) [18] Retrospective USA 2003–2012 Monocentric 75 69 43 C. Goh (2014) [19] Retrospective Ireland 2010–2013 Monocentric 30 65.4 60 Crawford (2015) [20] Retrospective Canada 2009–2013 Monocentric 30 64 66 Lascarides (2016) [21] Prospective USA / Monocentric 17 63 52 Račkauskas (2017) [22] Retrospective Lithuania 2010–2016 Monocentric 21 65.33 33 Tamegai (2018) [23] Retrospective Japan 2012–2018 Monocentric 17 66.5 58 Bulut (2019) [24] Retrospective New Zealand 2016–2017 Monocentric 25 71 52 S Suzuki (2019) [25] Retrospective Singapore 2004–2017 Monocentric 15 64 66 ES Huang (2020) [26] Retrospective USA 2013–2017 Monocentric 9 59.7 66.6 Parker (2021) [27] Retrospective UK 2008–2018 Monocentric 55 65 69 Kasim L Mirza (2021) [28] Retrospective California 2015–2020 Monocentric 22 64 81.8 Kolosov (2022) [29] Prospective Russia 2019–2020 Monocentric 31 67.8 93 Golda (2022) [30] Retrospective Spain 2010–2020 Monocentric 23 69.9 82.6 Serra-Aracil (2022) [31] Retrospective Spain 2018–2020 Monocentric 17 69 58 L W Leicher (2022) [32] Prospective The Netherland 2017–2019 Multicentric 110 66 56 Austin T Jones (2021) [33] Retrospective USA 2018–2019 Monocentric 37 67 59.5 Julia Hanevelt (2023) [34] Retrospective The Netherlands 2015–2022 Monocentric 57 69.5 61.4 Fig. 2 Forest plot for additional surgery 7165Surgical Endoscopy (2025) 39:7160–7171 resection. Hybrid laparo-endoscopic approaches encompass a wide spectrum of techniques, ranging from laparoscopically assisted EMR to wedge or full-thickness resections and more limited segmental resections. Although some recent reports, such as Serra-Aracil etal. [31], have highlighted these variants, outcome measures were usually presented in aggregated form without stratification by technique. This lack of granularity precluded reliable meta-analytic comparison between procedural subtypes, and our pooled estimates should therefore be interpreted as representative of hybrid approaches as a whole rather than of individual procedures. With a pooled additional surgery rate of just 5% and consistent results across studies, this approach appears to provide a reliable organ-preserving alternative to traditional segmental colectomy, particularly when complete endoscopic resection is either infeasible or carries high risk. Recent technological advancements and growing expertise in the field of endoscopic resection of large superficial colorectal lesions are progressively reducing the need for surgical intervention. According to recent data from high-volume European centers, endoscopic submucosal dissection (ESD) achieves en bloc resection rates exceeding 85% even for lesions larger than 20mm, although the true oncologic benefit is realized in only a limited subset of patients. Endoscopic Submucosal Dissection (ESD) has been widely adopted for en bloc resection of superficial colorectal neoplasms; however, its clinical benefit is often undermined by the relatively high incidence of incomplete (R1) resections. Reported R1 rates in colorectal ESD range from 8 to 15%, largely due to technical challenges, fibrosis, and lesion morphology in the colon and rectum, which differ substantially from gastric ESD where en bloc R0 rates exceed 90% [35–37]. Incomplete resection not only negates the oncologic advantage of ESD by leaving positive margins but also necessitates additional interventions, either repeat endoscopic procedures or radical surgery, thereby increasing morbidity [38]. Moreover, several studies have shown that R1 resections are associated with a significantly higher risk of local recurrence compared to R0 resections [39]. These limitations underscore the need for careful patient selection and technical refinement, as well as the potential role of hybrid laparoscopic-endoscopic approaches to ensure complete full-thickness resection in anatomically or technically challenging lesions [40]. Specifically, the primary oncologic advantage of ESD over endoscopic mucosal resection (EMR) is seen in cases of well-differentiated adenocarcinomas with superficial submucosal invasion and no lymphovascular involvement. However, due to its technical complexity and higher risk of adverse events, ESD Table 2 Main results of the analyzed outcomes Analyzed variables Value (%) 95% CI I2 (%) Recurrence rate 3 2–6 0 Adenocarcinoma detection rate 12 8–16 68.8 Overall complications rate 7 5–10 25.6 Surgery for complications 1 0–2 0 Conversion to open surgery 2 1–3 0 Oncologic surgery requirement 7 5–9 0 Fig. 3 Forest plot for adenocarcinoma detection rate 7166 Surgical Endoscopy (2025) 39:7160–7171 should be reserved for lesions with a high suspicion of early submucosal invasion [41]. In most other cases, piecemeal EMR remains a safe and sufficient option for removing large (> 2cm), sessile or flat colonic lesions. If histology reveals invasive adenocarcinoma beyond the mucosal layer, radical surgery is recommended. Conversely, the presence of dysplasia at the resection margin does not justify surgery but rather calls for close endoscopic follow-up. The findings also highlight that a significant proportion of lesions presumed benign—approximately 12%—were found to harbor adenocarcinoma on final pathology. The heterogeneity observed in the pooled incidence of adenocarcinoma is mainly attributable to differences in diagnostic accuracy and patient selection across studies. In most series, adenocarcinoma was diagnosed only a posteriori on the final resection specimen, whereas preoperative biopsies rarely guided Fig. 4 Forest plot for surgery for oncological reason Fig. 5 Forest plot for overall complications rate 7167Surgical Endoscopy (2025) 39:7160–7171 the indication for hybrid resection and were reserved for patients unfit for extended colectomy. As endoscopic biopsy usually samples only a fraction of the lesion, it may easily understage the true histology, explaining why invasive carcinoma was unexpectedly identified in lesions considered benign at endoscopy. For this reason, a reliable subgroup analysis stratifying lesions as benign versus malignant at baseline could not be performed, as such categories were not consistently available prior to resection. This diagnostic limitation must be acknowledged as a key contributor to the heterogeneity observed in the pooled analysis. This underscores the limitations of current diagnostic modalities in precisely staging complex colorectal polyps, despite advances in imaging and biopsy techniques. Fig. 6 Forest plot for surgery for complications Fig. 7 Forest plot for conversion to open surgery 7168 Surgical Endoscopy (2025) 39:7160–7171 Consequently, a second surgical procedure for oncologic radicality was necessary in 7% of cases. Intraoperative frozen section examination was not reported in any of the included studies. Consequently, adenocarcinoma was generally recognized only on final pathology of the hybrid resection specimen. Patients with such findings were then offered oncologic resection whenever clinically appropriate and acceptable. This highlights both the limits of current intraoperative decision-making and the potential for understaging with endoscopic biopsy, which samples only a small fraction of large or complex lesions. The absence of frozen section use in published series may have contributed to the proportion of patients requiring secondary oncologic surgery observed in this review. This outcome, while not negligible, remains acceptable in a clinical scenario where overtreatment through upfront colectomy can be avoided in the majority of patients. The long-term local recurrence rate of 3% (95% CI 2–6%; I2 = 0%) observed in this systematic review underscores the durability of local control achieved with these techniques. This exceptionally low rate, coupled with the absence of heterogeneity across included studies, highlights the oncologic reliability of these approaches when applied in appropriately selected patients. Such outcomes are comparable to, or even better than, those reported for standard surgical resections in early colorectal neoplasia, supporting their role as effective organ-preserving strategies. Moreover, the consistency of results across studies suggests that these techniques can deliver reproducible oncologic safety in different clinical settings, provided that meticulous patient selection and adherence to technical standards are ensured. Only relevant improvements in intraoperative staging of rectal cancer at the time of local excision, such as the use of fluorescence to better characterise tumour histology and invasiveness [42], or sampling of potential sentinel lymph nodes in the mesorectum [43–45], could significantly alter the perspective on organ-sparing techniques. Moreover, these techniques may take advantage of recent research in AI and computed tomography (CT) in assisting the preoperative localization of colorectal cancer resection surgery [46]. The complication rate observed in this review was low, with only 7% of patients experiencing adverse events and a mere 1% requiring surgical management of complications. These results compare favorably with those of standard surgical resection and suggest that laparo-endoscopic approaches maintain a favorable safety profile, even in anatomically challenging cases such as lesions located in the right colon, near the ileocecal valve, or involving previous fibrosis. Moreover, conversion to open surgery was required in only 2% of procedures, indicating that combined approaches are technically feasible and controllable when performed by adequately trained surgical and endoscopic teams. Perhaps most notably, the recurrence rate was just 3%, with excellent consistency across studies, suggesting durable local control and confirming the oncologic reliability of these techniques. The methodological quality of the included studies was assessed using the QUADAS tool, which revealed an overall high level of internal validity. All studies adequately described the patient spectrum and ensured the independence and reliability of the reference standard. However, Fig. 8 Forest plot for local recurrence rate