Chinese clinical practice guidelines for super minimally invasive surgery of digestive tract tumors

Background

Digestive tract tumors (DTTs) represent a major clinical challenge due to their high incidence and mortality, as well as the substantial physical and psychological burden associated with surgical treatment. At present, curative resection remains the standard and preferred approach for the radical treatment of DTTs. However, surgical strategies based on organ removal and anatomical reconstruction inevitably lead to significant short-term complications and long-term impairments in quality of life. For example, total gastrectomy often results in nutrient malabsorption, leading to anemia and osteoporosis; patients undergoing subtotal gastrectomy may suffer from postural intolerance (inability to lie flat), diarrhea, gastroparesis, and dumping syndrome. Esophageal or colorectal resections are frequently associated with anastomotic leakage and anastomotic stricture, while rectal surgery often necessitates loss of anal preservation. Similarly, pancreaticoduodenectomy (Whipple procedure) alters the physiological route of food digestion, and may induce complications such as biliary fistula and pancreatic fistula^[1]. Notably, organ resection and anatomical reconstruction also pose potential drawbacks. A study on post-gastrectomy patients revealed that the surgery significantly affects the activity of the posterior cingulate cortex, suggesting an impact beyond local anatomical changes^[2]. In contrast, SMIS, organ-preserving curative procedures, which maintain the integrity of normal anatomical structures, can effectively avoid these complications. By achieving radical disease eradication while preserving organ function, this approach represents a new paradigm in surgical oncology.

The Super Minimally Invasive Surgery (SMIS) paradigm was first proposed by professor Enqiang Linghu in 2016 as a revolutionary surgical concept that redefines traditional approaches based on organ resection and anatomical reconstruction^[3]. This innovative model utilizes four principal access channels—via the natural cavity channel, the tunnel channel, the puncture channel, and the multi-cavity channel, and encompasses dozens of surgical techniques and nearly a hundred procedural variations, all aimed at achieving the ultimate goal of “curing disease while restoring the organ to its original integrity”^[4]. Guided by the philosophy of SMIS, therapeutic interventions strive for near-perfect outcomes, enabling patients to retain their preoperative quality of life and ensuring that survival remains unaffected by the disease itself. The SMIS paradigm promotes a treatment philosophy grounded in the body’s natural anatomical order, emphasizing organ preservation, functional restoration, and minimal disruption to physiological structures. Moreover, the underlying principles of SMIS are universally applicable across all domains of invasive medical therapy, representing the ultimate goal and future direction of surgical innovation and practice.

Since it was first proposed, the concept of SMIS has received official recognition from both national and international academic organizations. In 2019, the SMIS Collaborative Group was established under the Chinese Society of Digestive Endoscopy (CSDE). In 2021, the World Endoscopy Organization (WEO) founded the SMIS Committee, and in the same year, the National Committee for Terms in Sciences and Technologies of China officially included SMIS in the Terminology of Digestive Endoscopy, thereby standardizing its nomenclature within the professional community^[5]. In 2022, the 14th Five-Year National Key R&D Program funded the “Establishment and Application Model Research of the SMIS Efficacy Evaluation System for Digestive Tract Tumors.” Building on these milestones, SMIS has played an increasingly important role in the treatment of DTTs, showing rapid progress and widespread clinical adoption worldwide (Table 1, 2). Consequently, the development of a scientific and standardized clinical practice guideline has become both necessary and urgent. This guideline aims to provide evidence-based and expert consensus-driven recommendations for the clinical application of SMIS in the management of esophageal, gastric, colorectal, and duodenal tumors, through a systematic evaluation of current literature and multidisciplinary expert collaboration.

At different stages of DTTs, the SMIS treatment mode encompasses a spectrum of progressively advanced approaches. For intramucosal cancer with an extremely low risk of LNM, local non-FTR—achieved through endoscopic submucosal dissection (ESD) or endoscopic mucosal resection (EMR)—can provide radical removal with minimal invasion, followed by close surveillance. For lesions invading the submucosal layer, local progressive FTR may be performed via endoscopy or laparoscopy to achieve en bloc removal of the lesion and the full-thickness, which is suitable for selected high-risk early cancer(EC). In cases where LNM risk exists, local progressive FTR combined with precise lymph node.

Methods

Results

Section 1: Application, implementation rules, and nomenclature of SMIS in DTTs

Question 1: Surgical models of SMIS for DTTs

SMIS is defined as a surgical approach applied to diseases that require operative intervention or those with unsatisfactory outcomes from long-term pharmacological treatment. The fundamental principle is to remove or eradicate pathological lesions while preserving the integrity of the body’s natural anatomical structure, thereby achieving curative treatment.^[10] Throughout this development process, endoscopic diagnosis and treatment technologies have achieved breakthroughs in applications from within the digestive tract lumen to beyond the lumen, gradually expanding from the treatment of internal medicine diseases to surgical diseases, thus aligning more closely with the scope of surgical treatments. To better implement the concept of SMIS, deep multidisciplinary integration between the fields of digestive endoscopy and surgery is required, in which SMIS that extends beyond endoscopy is performed to ensure the maximum preservation of anatomical integrity while eradicating the disease.^[1,10,11]

Question 2: Access routes for SMIS in DTTs

The direction of SMIS development is focused on surgical improvements related to the four types of channels, which include the continuous implementation and promotion of procedures with high safety and efficacy, efforts to improve procedures with high efficacy but low safety, and the continuous expansion of new SMIS techniques, methods, and therapeutic indications.^[4,12] The SMIS surgical techniques for DTTs are as follows:

1. SMIS via natural cavity channels. This refers to surgery performed through a naturally open passage of the human body that meets the super minimally invasive requirements. This includes non-FTR and FTR of the digestive tract, which are the preferred treatments for early DTTs. Active exploration and refinement of SMIS resection techniques for super indications and methods for closing large wound areas are under development. Procedures such as laser lithotripsy and stone removal while preserving the duodenal papilla, and endoscopic resection of precancerous lesions in pancreaticobiliary cancers under direct visualization, are also included in this category.

2. SMIS via tunnel channel. This refers to surgery performed through an artificially created tunnel in tissue, with the procedure taking place within the created space and meeting the super minimally invasive criteria. This includes mucosal-side nonFTR of extensive early DTTs, resection of tumors in the submucosal layer via a tunnel channel, and full-thickness incisions from the muscularis propria side of the digestive tract for treating conditions such as achalasia and gastroparesis, and tumor removal from the digestive tract lumen through the muscularis propria.

3. SMIS via puncture channel. This refers to surgery performed through a puncture channel into a cavity or lumen that meets the super minimally invasive criteria. Examples include endoscopic ultrasound (EUS)-guided percutaneous puncture, sclerotherapy for pancreatic cystic lesions, and percutaneous abdominal puncture FTR of DTTs, with or without LN dissection or removal.

4. SMIS via multi-cavity channel. This refers to surgery performed through more than one channel and/or using more than one endoscope within a cavity, in which access through all channels meets the super minimally invasive requirements. This approach may be used for accessing difficult-to-reach areas where a single endoscopic approach might fail, offering an alternative approach for challenging locations. For example, combined endoscopy and laparoscopy may be used to resect DTTs with or without LN dissection or removal.

Question 3: Principles for selecting the SMIS access route

The implementation of SMIS follows a set of core principles aimed at ensuring the safety and efficacy of the surgical procedure through a comprehensive preoperative lesion assessment, precise selection of surgical techniques, and the prevention and management of complications. This approach seeks to provide patients with treatment outcomes and a quality of life consistent with the concept of SMIS.^[12,13] These core principles are as follows:

1. Principle of organ preservation, anatomical integrity, and unchanged organ function: The surgery focuses on removing the diseased tissue without damaging surrounding organs and tissues. Due to limitations, such as the depth and extent of the lesion, it may not be possible to remove only the diseased tissue. Efforts should be made to maximally preserve the surrounding organs and tissues while ensuring complete lesion excision, with anatomical structure and function maintained.

2. Principle of cavity consistency: The entry point, approach, and target location of the surgical procedure should ideally be within a single cavity, minimizing the need for multi-cavity incisions to reduce trauma and recovery time. In SMIS treatment, the use of four-channel access should be considered as the primary approach.

3. Principle of aseptic technique: Aseptic conditions should be the first priority, particularly in surgeries involving multi-cavity channels or percutaneous abdominal or thoracic puncture approaches. Strict adherence to aseptic principles is required.

4. Principle of avoiding chemical irritant release: In SMIS procedures involving punctures or multi-cavity channels, it is essential to avoid puncturing through ductal systems, such as blood vessels, lymphatic vessels, bile ducts, the gallbladder, and pancreatic ducts, to prevent the introduction of chemical irritants into the abdominal cavity, which could cause infection.

5. Principle of natural cavity channel preference: If there is an option to use a natural orifice, preference should be given to natural orifice routes, provided they comply with the first four principles.

6. Principle of substitution under natural cavity channel contraindications: When access through a natural orifice is contraindicated due to factors such as obstruction or narrowing, a puncture channel should be chosen, ensuring adherence to the first four principles.

7. Principle of shortest surgical approach: When selecting the surgical access route, consideration should be given to the distance between the entry point and the surgical site. The shortest possible path should be chosen to minimize damage to surrounding organs or tissues, reduce surgical difficulty, and shorten the procedure time.

8. Principle of bleeding prevention and control: Preoperative assessment of bleeding risk should be thorough, and effective preventative and hemostatic contingency measures should be used to ensure an almost 100% hemostasis success rate. This principle is essential in the application of the four-channel access in SMIS procedures.

9. Principle of perforation prevention and closure: Prior to surgery, perforation risk should be thoroughly assessed, and appropriate techniques for prevention and closure should be applied to restore the integrity and closure of the body’s natural cavities. This principle must be considered in the application of the four-channel access in SMIS procedures.

10. Principle of tumor treatment: For SMIS treatment of benign and malignant tumors, principles such as not cutting through the tumor, en bloc resection, tumor-free techniques, and prevention of metastasis should be followed.

Question 4: Nomenclature for SMIS in DTTs

To succinctly and comprehensively summarize the disease and its treatment method in a manner reflecting its application that is easily recognized, the currently established SMIS nomenclature convention is as follows. The nomenclature must include the lesion location, lesion nature, surgical channel, and treatment method.^[5] The following nomenclature convention is recommended for adoption: “lesion location + lesion nature + channel + super minimally invasive excision/incision/removal/drainage/ ablation”. This convention represents the final diagnosis after the surgery is completed and pathological results are integrated. Previously used endoscopic techniques, such as endoscopic mucosal resection (EMR) and endoscopic submucosal dissection (ESD), which are SMIS methods, are not included in the surgical nomenclature but should be described in detail in the surgical record, including the treatment process and specific techniques applied. For example, the natural cavity channel (per-oral SMIS-FTR for GC on the greater curvature of gastric body), the tunnel channel (per-tunnel SMIS-non FTR for GC on the greater curvature of gastric antrum), the puncture channel (per-puncture SMIS-FTR for appendiceal adenoma), and the multi-cavity channel (per-multi-cavity SMIS for GC on the anterior wall of gastric body).

Section 2: The application of SMIS in treating early esophageal cancer (EEC) and precancerous lesions, along with strategies for stricture prevention

Question 5: For patients with esophageal dysplasia or early stage, well-differentiated, non-ulcerative EEC, it is recommended to select super minimally invasive non-full-thickness resection (nft-SMIR).

In the treatment of EEC and precancerous lesions, SMIS provides a treatment option that preserves organ integrity. Key factors influencing the selection of the resection method include the tumor size, depth of invasion, histological grading, and presence of ulcers. The American Society for Gastrointestinal Endoscopy (ASGE) guidelines for ESD in the treatment of early esophageal and GC recommend a lesion size of 15 mm as the cutoff to decide between ESD and EMR. However, this should not be seen as a strict threshold, as there is no upper limit established for lesion size with ESD.^[14] Additionally, determining the depth of invasion before resection is essential. The Japanese Esophageal Society’s guidelines for EC treatment define absolute indications for ESD as flat lesions (Paris 0–II), invasion into M1 to M2, and no more than two-thirds circumferential involvement, while relative indications are M3 to SM1 lesions, in which endoscopic resection would leave a more than 75% circumferential mucosal defect.^[15] Ensuring the resection of an entire specimen is crucial for assessing cure rates, accurate staging, guiding further treatment decisions, and managing recurrence after resection.

ESTD has been shown to be highly effective and safe for treating large early-stage esophageal cancers. Compared to traditional ESD, ESTD has a higher complete resection rate, faster dissection speed, and lower postoperative recurrence rate. Therefore, ESTD can be considered the first choice of SMIS for large early-stage EC. The decision to use SMIS resection should also be based on several other factors, including local expertise, availability, the judgment of the endoscopist, and patient preferences.

Question 6: Postoperative stricture prevention in esophageal SMIS

Currently, methods for preventing esophageal stricture include the following: (1) Prophylactic balloon dilation (EBD): EBD can reduce the incidence of post-ESD esophageal stricture and shorten the treatment time required after stricture occurs. However, EBD requires repeated endoscopic procedures, causing significant discomfort and an economic burden for patients, and is therefore not recommended for standalone use. (2) Esophageal stents: Esophageal stents can be used as a preventive measure, but care must be taken to avoid potential complications such as stent displacement and restenosis. (3) Corticosteroids: The local use of corticosteroids can suppress inflammatory responses and the synthesis of collagen fibers and promote collagen breakdown, thereby reducing the incidence of post-ESD stricture. (4) Scar inhibitors and wound coverage: The use of scar inhibitors and wound coverage techniques can reduce scar formation and prevent stricture.

(5) Autologous mucosal grafting: Autologous mucosal grafting is an innovative method that has been used to prevent stricture after endoscopic treatment of esophageal circumferential lesions with good results.

Section 3: Surgical selection and curative assessment of SMIS for EGC and precancerous lesions

Question 7: For patients with EGC or gastric epithelial dysplasia or HGIN, SMIS can be performed.

With the increasing detection rate of EGC, its proportion in the overall cases of GC has approached 20%.^[16] Radical gastrectomy combined with systematic lymph node dissection remains the preferred surgical approach in some regional hospitals. However, the regional LN status in the surgical scope is a key factor and crucial component in determining both the surgical approach and prognosis.^[17] Previous studies have shown that this type of surgery can effectively control cancer recurrence; however, many patients without LNM unnecessarily suffer from complications and sequelae caused by organ resection. Moreover, the extent of necessary LN dissection remains a subject of ongoing debate.^{[18, 19, 20]} The removal of non-metastatic LNs may disrupt the immune system, potentially causing secondary effects on the primary tumor or latent metastatic foci.^{[17, 18, 19, 20, 21]} Given that excessive organ and LN resection can cause irreversible harm to the body, it is of great significance to choose and perform less invasive, more individualized, and precise surgical strategies.^[22]

In recent years, the concept of SMIS has significantly transformed the treatment approach and surgical paradigms of EGC to become the first-line treatment option for both EGC and precancerous lesions. The surgical techniques include the following: (1) nft-SMIR, which includes treatments that have been widely developed and used for decades, such as ESD, ESTD, EMR, and endoscopic intermuscular dissection (EID), with the dissection layer extending from the mucosal layer to the muscularis propria, and the recently developed stepwise super minimally invasive non-full-thickness resection (snft-SMIR); (2) super minimally invasive full-thickness resection (ft-SMIR) using endoscopy, including stepwise super minimally invasive full-thickness resection (sft-SMIR), endoscopic full-thickness resection(EFTR), and hybrid EFTR; and (3) super minimally invasive multi-cavity channel gastrectomy, which involves performing full-thickness lesion resection combined with LN dissection using an endoscope via natural cavity channels and a laparoscope through a percutaneous abdominal puncture channel. These three surgical methods must be chosen based on the strict T-stage classification of gastric cancer, ensuring maximal patient safety and quality of life while maintaining curative intent.^[22]

A preliminary exploration of the LN dissection range of EGC in different tumor locations for super minimally invasive multi-cavity channel gastric conserving surgery, and the clinical practice experience obtained from the original clinical guidelines are summarized as follows.

1. Lower middle GC (distal GC) : (1) The original guidelines recommend D1 dissection, i.e., No. 1 (right cardia), 3 (lesser curvature side), 4sb (left gastric omentum vascular side), 4 d (right gastric omentum vascular side), 5 (upper pylorus), and 6 (lower pylorus). (2) Local FTR with regional LN dissection was classified according to specific location (ultimately based on the actual location of the tumor) as follows: ① antrum of the stomach, No. 3 (lesser curvature side), 4sb (adjacent to the left vessel of the gastric omentum), 4 d (adjacent to the right vessel of the gastric omentum), 5 (above the pylorus), 6 (below the pylorus), and 7 (adjacent to the left gastric artery); ② small curvature side of gastric body, No. 1 (right cardia), 3 (small curvature side), 5 (upper pylorus), and 7 (adjacent to left gastric artery); and ③ on the greater curvature side of the gastric body, No. 4sb (adjacent to the left vessel of the gastric omentum) and 4 d (adjacent to the right vessel of the gastric omentum).

2. Upper GC (proximal GC): (1) The original guidelines recommend D1 dissection, i.e., No. 1 (right cardia), 2 (left cardia), 3a (upper part of lesser curvature), 4sa (adjacent to short gastric vessels), 4sb (adjacent to left gastric omentum vessels), and 7 (adjacent to left gastric artery). (2) Local FTR with regional LN dissection was classified according to specific locations (ultimately based on the actual location of the tumor) as follows: ① lesser curvature side of the gastric fundus, No. 1 (right of the cardia), 2 (left of the cardia), 3 (lesser curvature side), and 7 (adjacent to the left gastric artery); and ② gastric fundus vault, No. 1 (right cardia), 2 (left cardia), and 4sa (near the short blood vessels of the greater curvature of the stomach).

Question 8: For patients with EGC undergoing SMIS, a precise assessment of LNM risk should be performed, and targeted LN dissection may be conducted when feasible.

Due to the complex and multidirectional lymphatic drainage pattern of the stomach, SLN detection, which targets the first station (D1) of the primary tumor’s lymphatic drainage pathway, can yield false negatives. This presents a clinical challenge in digestive tract LN tracing. However, researchers have proposed various methods to predict LNM in multiple studies. Currently, non-invasive preoperative detection methods, including PET-CT and CT of the chest, abdomen, and pelvis combined with ultrasound of superficial human LNs, are effective approaches for assessing the systemic status of the tumor and LNM.^[23] Patients with EGC carry a risk of LNM, though reported rates vary across centers. The incidence of LNM in intramucosal cancer is relatively low, ranging from approximately 2% to 5.9%, while the rate increases in submucosal cancer (T1b stage), ranging from about 2.5% to 20.3%.^{[24, 25, 26, 27]} The submucosal layer is rich in lymphatic vessels, and once cancer infiltrates this layer, the likelihood of LNM via lymphatic reflux rises significantly. Therefore, greater attention is given to the LNM rate in T1b EGC. For example, Abdelfatah ^[26] reported an LNM rate of only 2.5% in T1b cases, whereas the General Surgery Department of the PLA General Hospital reported a rate as high as 20.3%.^[27] In its second edition of the endoscopic treatment guidelines for EGC, the Japan Gastroenterological Endoscopy Society (JGES)^[28] proposed a stratified evaluation of LNM rates based on tumor size, histological type, and the presence or absence of ulceration, which estimated the risk to range from 1% to 10.6% (Table 4).

For Tis, T1a-M1, and T1a-M2 EGC, non-full-layer resection or full-layer resection is used. For some T1a-M3 and T1b EGC, full-thickness resection surgery or multi-cavity SMIS gastric preservation surgery is considered. For T1b with high risk factors of LNM or T2 with a low risk of LNM, multi-cavity SMIS gastric conserving surgery should be considered (Figure 1).

Figure 1

SMIS surgical selection strategy for early gastric cancer. SMIS, super minimally invasive surgery.

Question 9: Evaluation of curative effect for SMIS in EGC

The evaluation of post-EGC cure has significant clinical value, as evidenced by the following: (1) guiding subsequent treatment, where the correct selection of chemotherapy, radiotherapy, or targeted therapy reduces the risk of recurrence; (2) assessing recurrence risk, where formulation of more targeted follow-up plans and monitoring strategies; (3) improving patient quality of life, in that for patients with a higher cure rate, unnecessary subsequent treatments can be reduced, thus minimizing treatment-related side effects; (4) psychological support, in that a cure evaluation provides patients with a clear treatment outcome, thus helping alleviate anxiety and uncertainty and boosting their confidence in the future; (5) health economic considerations, where a cure evaluation helps patients and doctors assess the economic benefits of treatment, avoiding unnecessary treatment costs and alleviating the patient’s financial burden; (6) prognostic communication, that is, a cure evaluation offers a quantifiable prognostic indicator, facilitating more effective communication between doctors, patients, and their families, thus helping them gain a clearer understanding of the treatment outcome; (7) health decision-making, in that patients can make more informed health decisions based on the cure evaluation results, such as whether to modify their lifestyle or dietary habits to reduce the risk of recurrence; (8) research participation, in that patients with unsatisfactory cure evaluation results may be more motivated to participate in clinical studies to seek new treatment methods; and (9) legal and insurance matters, where, in some cases, the cure evaluation result may affect the patient’s legal rights and insurance claims.

With the expansion of treatment indications for EGC and the iterative innovations in related SMIS surgical techniques, the limitations of the traditional eCura evaluation system in clinical applications have become increasingly apparent. To address this, Professor Enqiang Linghu’s team introduced the SMIS-Cure evaluation system in 2025 (Table 5). By integrating key factors, such as surgical method selection, tumor size, depth of invasion, differentiation type, ulceration status, vascular and nerve invasion, and residual lesions in the surgical specimen, the system forms a three-level dynamic evaluation standard: SMIS-Cure A (cured), SMIS-Cure B (clinically cured), and SMIS-Cure C (surgical reassessment). The evaluation also includes LNM risk assessment prior to the preoperative evaluation to create a more systematic evaluation framework that aligns with the characteristics of SMIS surgery.

Within the preoperative stratification assessment, the LNM risk is divided into three levels based on multimodal imaging diagnostic results. (1) No evidence of LNM metastasis: no tumor-related LNs are found using PET-CT, abdominal enhanced CT, or magnetic resonance imaging (MRI) combined with whole-body superficial LN ultrasound. (2) Suspicious LNM risk: abdominal CT, MRI, or whole-body superficial lymph node ultrasound suggests the presence of lymph nodes but cannot confirm whether they are tumor-related, requiring combined PET-CT examination, which still cannot completely rule out the possibility of tumor-related LN. (3) Clear evidence of LNM: through one or more imaging modalities, such as abdominal CT, MRI, whole-body superficial LN ultrasound, or PET-CT, the presence of tumor-related LNs is confirmed. Compared with the eCura grading system, the innovative breakthrough of SMIS-Cure lies in the introduction of new surgical evaluation standards, such as ft-SMIR and SMIS multi-cavity gastric preservation surgery, which cover the entire process from preoperative assessment to postoperative follow-up in an evidence-based decision-making framework, and retain the eCura A evaluation standard of the eCura system as the radical cure standard. The SMIS-Cure evaluation system aims to shift GC diagnosis and treatment from a “radical priority” model to a “radical and functional balance” paradigm.

Question 10: Postoperative follow-up strategy for SMIS in EGC

For patients with EGC and HGIN of the stomach, it is recommended that the characteristics of the three levels of cure degrees [SMIS-Cure A (cured), B (clinically cured), and C (surgical reassessment)] are systematically evaluated using the SMIS-Cure evaluation system, and additional individualized treatment and follow-up plans are formulated based on the grading results (Figure 2). Specifically, patients assessed as SMIS-Cure A can undergo standardized follow-up (endoscopic monitoring at intervals of 6–12 months), those at the SMIS-Cure B level require intensified and close follow-up (imaging combined with endoscopic evaluation every 3 months), and those at the SMIS-Cure C level require a multidisciplinary consultation to determine a secondary intervention strategy, while dynamically monitoring the risk of LNM and the effect of organ function preservation.^[119,120] For special populations who cannot tolerate surgery due to advanced age or severe complications, clinically, it is necessary to focus on evaluating the risk of LNM and the possibility of local recurrence and distant metastasis. It is essential to fully inform the patient that recurrent GC is usually incurable and has an extremely poor prognosis. This stratified decision-making process needs to take into account the individual situation of each patient to strike a balance between risk control and quality of life, and also give consideration to the rational utilization of medical resources.

Figure 2

Supplementary treatment status after surgery evaluated by the SMIS-Cure system. SMIS, super minimally invasive surgery.

Section 4: SMIS treatment for early colorectal cancer (ECRC) and precancerous lesions

Question 11: For patients with ECRC or high-grade colorectal intraepithelial neoplasia, SMIS can be performed.

In the past 15 years, there has been a tremendous transformation in the treatment model of colorectal tumors, with a gradual shift from traditional surgery to minimally invasive endoscopic techniques. With the application of new technologies and concepts, such as preoperative precise diagnoses, adjuvant chemoradiotherapy, immunotherapy, transanal endoscopic microsurgery (TEM), transanal endoscopic operations (TEO), transanal minimally invasive surgery (TAMIS), EFTR, and EID, the treatment model of CRC has gradually shifted towards preserving organ function.^[29] In recent years, a new treatment strategy concept referred to as “resection and analysis” has emerged for CRC stages T1 and T2. The resection and analysis strategy requires endoscopic resection, followed by pathological evaluation to assess the risk of LNM and the necessity of additional intestinal resection. Its use has provided further evidence of the oncological and endoscopic technical safety requirements for practical implementation.^[30,31]

In recent years, surgical projects based on the concept of SMIS have included the following. (1) nft-SMIR surgery: treatments such as ESD, ESTD, EMR, and EID, which have been widely performed and developed for decades, have expanded the peeling layer from the mucosal layer to the muscularis propria. Furthermore, a new SMIS procedure, nsft-SMIR, enables the implementation of a progressive resection strategy that conforms to the growth characteristics of tumors. (2) ft-SMIR of digestive endoscopic lesions: a new SMIS procedure, the sft-SMIR, and the SMIS closure method of cutting and closing simultaneously provide a means of safe and effective FTR surgery performed through a single colonoscope via a natural body cavity. In addition, transanal local excision (LE) surgeries such as TEM, TEO, and TAMIS also conform to the concept of SMIS. (3) ft-SMIR of lesions combined with LN resection surgery: SMIS is carried out by combining the natural body cavity channel of the digestive endoscope with the percutaneous abdominal puncture channel of the laparoscope. These three surgical methods must be selected based on the strict T staging of CRC to ensure the patient’s safety and quality of life to the greatest extent.^{[32, 33, 34, 35, 36]}

Question 12: For patients with CRC, preoperative assessment of LNM is an essential prerequisite for performing SMIS.

Approximately 30% of patients initially present with CRC at Tis and T1 stages without LN involvement or metastasis, and surgery remains the standard treatment method for these patients. Currently, non-invasive preoperative detection methods, including PET-CT and enhanced CT of the chest, abdomen and pelvis combined with ultrasound examination of superficial LNs of the human body, are effective means of assessing the systemic status of tumors and LNM.^[23,35] In addition, rectal EUS and enhanced MRI are accurate tools for preoperative staging of rectal cancer (RC).^[37,38] Approximately 10% of T1 colorectal patients have LNM, among which the proportion of patients with pedunculated tumors (3–7%) is lower than that of those with sessile tumors (up to 28%).^[39,40] The risk of LNM can be stratified according to various histopathological factors, such as the depth of invasion, lymphovascular invasion, histological grade, and tumor budding.^[41,42]

T1 CRC patients with a low risk of LNM can be cured by LE through SMIS, while high-risk T1 CRC requires radical surgery with lymph node dissection.^[43] Currently, many patients still undergo unnecessary radical surgery. Although most patients achieve radical cure, their quality of life in the later stage is sacrificed. New diagnostic techniques for LNM have been recently developed, such as nomograms, artificial intelligence systems, and genomic analysis, which can identify more low-risk T1 CRC cases.^[44,45] In addition, studies based on LE show that the curability and necessity of additional treatments (including postoperative chemoradiotherapy and preoperative neoadjuvant therapy) are becoming an acceptable strategy for T1 CRC, particularly for RC.^[46]

When formulating the SMIS treatment plan, in addition to weighing the advantages and disadvantages of the treatment strategy based on the LNM risk stratification, the best SMIS surgical method should also be selected according to the LNM risk, as well as the patient’s life expectancy, physical condition, social characteristics, and personal wishes. According to the data from a multi-center study in the United States, the postoperative mortality rate of patients who received radical resection of rectal cancer increased significantly with age: it was only 1.5% for those aged 69 and below, but climbed to 8.0% for patients over 85 years old. A cross-national data comparison further showed regional differences in the postoperative mortality rate of surgery, with 1.3% reported in a Japanese cohort and 2.4% in a Dutch cohort. Therefore, for patients with a risk percentage equal to or lower than these reported risks, the risk of LNM is acceptable, and it is feasible to perform SMIS local resection surgery.

Question 13: Evaluation of curative outcomes and follow-up strategy for SMIS in CRC or high-grade intraepithelial neoplasia

The cure rate of early colorectal cancer is relatively high, usually ranging from 60 to 80%. Some studies even indicate that the cure rate of early colorectal cancer (particularly stage I or II) after surgical resection can exceed 90%. For extremely early intramucosal cancer, an almost 100% cure rate can be achieved.^[47]

The purpose of follow-up after SMIS for ECRC is to detect local residual tumor, recurrence, metastasis, and ectopic lesions at an early stage. The formulation of the follow-up plan should comprehensively consider various factors, such as the SMIS treatment techniques employed (such as en bloc resection or piecemeal resection), the assessment of resection integrity based on the pathological results of the specimens, the presence of recurrence risk factors, and the patient’s underlying diseases ^[48] (Figure 3). Currently, there is a lack of high-quality evidence-based medicine regarding the optimal follow-up interval after endoscopic resection of early CRC. According to the expert consensus, it is recommended that colonoscopy be performed 3, 6, and 12 months after curative endoscopic resection of early CRC. Imaging examinations (chest and abdominal CT) should also be performed to rule out the possibility of LNM and other conditions. If all reexamination results are normal, the follow-up interval can be extended to 1 or 3 years, with attention paid to combining tumor marker testing, fecal occult blood testing, and relevant imaging examinations. For lesions resected through piecemeal resection, it is advisable to conduct the first reexamination within 3 to 6 months according to different recurrence risks, and care should be taken to avoid a missed diagnosis of the lesion during follow-up. More detailed and effective follow-up plans require the support of more high-quality clinical studies in the future.^[49,50]

Figure 3

SMIS strategy selection, prognosis, and follow-up for early colorectal cancer and high-grade intraepithelial neoplasia. SMIS, super minimally invasive surgery.

Question 14: For selected patients with LARC who achieve tumor regression after neoadjuvant therapy, SMIS local excision may be considered.

The key points in the diagnosis of LARC include endoscopic or imaging findings of the primary rectal tumor, pathological confirmation of cancer, a tumor location within 12 cm of the anus, invasion beyond the muscular layer of the intestinal wall into the surrounding tissues or LNM, and the absence of distant metastasis.^[51] Low RC accounts for the majority of RC patients in China, and in its treatment, there are challenges in “saving lives, preserving the anus, and maintaining functions”.^[52] Currently, the standard treatment for LARC is the “sandwich” model, neoadjuvant chemoradiotherapy (nCRT) with total mesorectal excision (TME) and postoperative adjuvant chemotherapy.^[52,53] The Chinese diagnosis and treatment specifications ^[52] recommend neoadjuvant chemoradiotherapy for patients with stage II and III middle and low RC, including long-course chemoradiotherapy or short-course radiotherapy combined with chemotherapy, with chemotherapy regimens such as capecitabine being preferred.

TME is the gold standard for RC surgery. However, the surgery is technically difficult, may cause complications, and may also affect sexual function.^[52,53] For patients who achieve clinical complete response (cCR) or ncCR after neoadjuvant chemoradiotherapy, watch-and-wait (W& W) is a potential strategy and a current research direction. However, its local recurrence rate is relatively high, and the disease-free survival rate, overall survival rate, and disease-specific survival rate are not as high as those following total mesorectal excision. Although some studies have shown that a strict W& W strategy can detect local recurrence at an early stage without increasing the risk of systemic disease or resulting in poor survival outcomes,^[54] during the monitoring process, the uncertainty of clinical results can place a sizeable psychological and economic burden on patients and their families. From a pathological perspective, the W& W strategy does not completely eradicate the tumor tissue, and the remaining scar tissue provides conditions for local tumor recurrence.

LE, which involves resecting the tumor scar through transanal endoscopy, preserves the rectum, reduces the risk of local recurrence, and is helpful in determining a pathological complete response.^[55] SMIS with FTR may become a strong competitor to replace the standard of TEM in the treatment of LARC.^[56] However, while this technique resects the lesion, it can be accompanied by active perforations and defects in the intestinal wall. The closure of rectal wall defects remains a controversial issue. Clinical studies comparing the open and closed management of intestinal wall defects after local FTR of rectal tumors have found that there are no significant differences between the unclosed and closed groups in terms of the overall incidence rate, postoperative local infection rate, postoperative bleeding rate, and postoperative reintervention rate.^[57]

Section 5: SMIS treatment for duodenal papillary adenoma

Question 15: For patients with benign or high-grade neoplastic duodenal papillary tumors that do not involve the bile duct or pancreatic duct, SMIS can be performed.

Duodenal papillary adenoma is relatively rare clinically. Its incidence rate is less than 1 in 100,000, accounting for approximately 0.6%–0.8% of DTTs. It is commonly found in individuals aged 50 to 70 years old, and it is more prevalent in men (the male-to-female ratio is 1.5: 1).^[58,59] As a precancerous lesion, although duodenal adenoma is a benign disease, it follows the adenoma-adenocarcinoma pathway and has a certain risk of becoming cancerous (30%).^[60] Per-oral SMIS for duodenal papilla (SMIS-DP) or endoscopic papillectomy (EP) is the preferred treatment method for duodenal papillary adenoma without involvement of the pancreaticobiliary ducts. Its en bloc resection rate and radical resection rate are approximately 82.4% and 87.1% respectively, and it is particularly suitable for adenomas ≤ 3 cm. ^{[61, 62, 63]} Given the low risk of LNM, in patients with duodenal papillary adenocarcinoma confined to the mucosal layer and without local lymph node or distant metastasis (pTis and pT1a), endoscopic resection can be considered in cases in which surgical resection is not suitable or the patient refuses surgical resection.^[63,64] Compared with organ resection, anatomical reconstruction papillectomy, endoscopic SMIR has the advantages of less trauma, a faster recovery, and a lower incidence of adverse events. Moreover, there is no significant difference between the two methods in terms of long-term curative effect or recurrence rate.^[65,66]

After endoscopic resection, duodenoscopy [with biopsy) should be performed for reexamination and monitoring at 3, 6, and 12 months postoperatively, and then yearly (for at least 5 years) to prevent and detect recurrence.^{[62, 67]} If the specimen after resection indicates non-R0 resection, in consideration of the patient’s general condition, characteristics of the lesion, local technical conditions, and with full informed consent, pancreaticoduodenectomy, endoscopic re-resection, radiofrequency/APC ablation, or other treatments should be performed.^{[62,66,68,69]}

Supplementary Information

Supplementary materials are only available at the official site of the journal (www.intern-med.com).