Maximizing how minimal we can go: a narrative review of minimally invasive surgery for gastric gastrointestinal stromal tumors

Introduction

Background

Minimally invasive surgery (MIS) has been adopted for resection of gastrointestinal cancers with equivalent oncologic outcomes and the benefit of reduced postoperative pain, decreased hospital stay, and earlier recovery of bowel function (1,2).

Gastrointestinal stromal tumors (GISTs) are the most common sarcoma (3). These tumors arise from the interstitial cells of Cajal, and are identified most commonly in the stomach, followed by small intestine, colon and rectum, and esophagus. The cornerstone of management of localized GIST is complete surgical resection without routine lymphadenectomy (4,5). For patients with advanced GIST, tyrosine kinase inhibitors (TKIs), such as imatinib, are effective targeted therapies, as the majority of GISTs express gain-of-function mutations in KIT (~70%) or PDGFRA (~10%) receptor tyrosine kinases (3).

Rationale

The goal of surgical resection of GISTs is to obtain histologically negative (R0) margins without tumor rupture (6). Tumor rupture is a dreaded complication as it is a negative prognostic factor associated with a high risk of relapse (7-9). Thus, surgical approach must take into consideration tumor characteristics such as location and size in planning for R0 resection. Unlike gastric adenocarcinoma, gastric GISTs are typically well-defined and rarely metastasize to lymph nodes. Therefore, 5 cm resection margins and D2 lymphadenectomy are unnecessary, and simple wedge gastrectomy may be sufficient for some gastric GISTs (6).

For smaller (≤5 cm) gastric GISTs located in favorable locations, such as the gastric body or fundus, wedge gastrectomy has become increasingly common (10). The procedure begins with inspection of the abdomen for metastatic disease, followed by mobilization of the stomach. The GIST may be excised with a linear stapler, which concomitantly closes the stomach defect. Alternatively, the GIST can be excised sharply, and the gastric defect can be closed with a linear stapler or with suture closure. MIS approaches have been adopted for wedge gastrectomy, as the literature has demonstrated improved post-operative outcomes compared to open surgery with equivalent oncologic outcomes (11-13).

For GISTs located in anatomically unfavorable locations, such as the gastroesophageal junction (GEJ) or pylorus, laparoscopic wedge gastrectomy may be technically challenging as there is a risk of postoperative stenosis, and formal distal gastrectomy or total gastrectomy may be needed for complete surgical resection (14). Laparoscopic wedge gastrectomy is also more difficult for large GISTs, as they are difficult to manipulate laparoscopically. Given these challenges, open resection is commonly utilized for larger tumors or those located in unfavorable areas. However with further advances in MIS techniques and the proliferation of robotic surgery, there is a growing body of literature exploring MIS approaches for GISTs that are larger or in anatomically unfavorable locations.

While laparoscopic and robotic techniques have made considerable advances in the past two decades, one concern is that wedge gastrectomy may be removing an excessive margin of tissue, leading to gastric deformity and compromise of function. Laparoscopic and endoscopic cooperative techniques have evolved in parallel to traditional MIS surgical approaches in the past two decades as a method to improve precision given direct endoscopic visualization. There is now growing evidence that these cooperative techniques are also safe and feasible with equivalent oncologic outcomes compared to traditional surgical approaches.

Objective

The goal of this narrative review is to provide a timely analysis of MIS surgical techniques for gastric GIST resections. The analysis will address safety, feasibility, and clinical outcomes for gastric GIST ≤5 and >5 cm, and those tumors located in unfavorable anatomic locations. We will also evaluate advancements in laparoscopic-endoscopic cooperative surgical techniques, which have evolved in parallel to conventional MIS approaches. We present this article in accordance with the Narrative Review reporting checklist (available at https://ales.amegroups.com/article/view/10.21037/ales-23-67/rc).

Methods

A narrative review was performed using PubMed, Medline, and Cochrane Review databases using different combinations of the following search terms: “minimally invasive”, “laparoscopic surgery”, “robotic surgery”, “endoscopy”, “laparoscopic-endoscopic cooperative surgery”, “gastrointestinal stromal tumors”, “GIST”.

Studies published in English between January 1, 2006 and August 1, 2023 were included for review. The references of acquired sources were reviewed in order to identify other possibly missed studies (Table 1).

Discussion

MIS approaches for GISTs ≤5 cm

National Comprehensive Cancer Network (NCCN) recommendations for MIS resection of GIST were revised in 2007 to include tumors ≤5 cm, an update from 2 cm (10,11). These guideline updates were based on small retrospective series, which demonstrated the safety and feasibility of laparoscopic surgical resection. While these studies did not exclusively evaluate tumors ≤5 cm, the majority of the studies reported resections of small tumors (12-15). Otani et al. reported outcomes of 60 individuals who underwent GIST resections from 1993–2004. The group excluded tumors ≥5 cm from laparoscopic resection. In total, 35 patients underwent laparoscopic resections, all of whom had negative margins (12). While the other early studies used to guide these recommendations did not limit tumor size for the analysis, all studies included small GISTs (median tumor size 3.8–5 cm) (13,16). Across all of these early studies, there were no local recurrences at the surgical margins noted with the laparoscopic approach, supporting the oncologic safety of an MIS approach. With median follow-up of 53 months, Otani et al. reported 96.1% disease free survival rate (12). Additionally, Nakamori et al. and Otani et al. found that tumor size did not independently predict disease-free survival or overall survival (12,15).

Since the 2017 updated NCCN recommendations, laparoscopic GIST resection has become more common. A National Cancer Database (NCDB) review of GIST resections between 2010–2016 noted a 23% increase in the rate of laparoscopic resections (26% in 2010 compared to 49% in 2016) (2). Despite the increasing use of MIS techniques, prospective studies are lacking. While retrospective series and meta-analysis present significantly larger samples for comparison, they do not specifically limit analysis to GIST ≤5 cm. Therefore, results evaluating the efficacy of laparoscopic resection for small GISTs are extrapolated from heterogeneous datasets.

A meta-analysis of 11 retrospective studies evaluating 381 laparoscopic and 384 open GIST resections found no difference in overall complications (21% vs. 40%, P=0.51), margin positivity (4% vs. 8%, P=0.24), local recurrence (4 % vs. 9%, P=0.51), and overall survival (P=0.29) between the two surgical approaches (1). While this review did not specifically evaluate outcomes based on size, laparoscopically-resected tumors were generally smaller (median tumor size ranging from 2.9–6 cm in the laparoscopic group and 2–9.2 cm in the open group) (1).

Similarly, in a retrospective study evaluating 666 gastric GIST resections from 61 European countries from 2001–2013, there was a higher proportion of patients with tumors <5 cm in the laparoscopic group (67% laparoscopic vs. 45% open), while larger tumors (5–10 cm) were more prevalent in the open group (29% laparoscopic vs. 42% open). In this study, shorter operative time (130±70 vs. 150±70 min, P=0.003), reduced operative blood loss (48±128 vs. 159±424 mL, P<0.001), and shorter length of stay (7 vs. 11 days, P<0.001) were reported in the laparoscopic group. There was no difference in R0 resection rates between the laparoscopic and open groups (96% vs. 93%, P=0.10) (17).

Park et al. reported the results of a multicenter retrospective study comparing laparoscopic and open GIST resections at multiple Korean and Japanese centers. The laparoscopic group had a higher rate of tumors ≤5 cm (83% laparoscopic vs. 80% open, P<0.001). In a sub-analysis of tumors ≤5 cm resected using a laparoscopic (N=254) or open (N=244) surgical approach, postoperative complication and 30-day mortality rates were similar, and the laparoscopic group had a shorter length of stay (6.5 vs. 8.8 days, P<0.001) (18).

Taken together, these studies support MIS resection of selected GISTs ≤5 cm, with similar oncologic outcomes to the open approach, with the potential benefit of shorter length of stay. As such, MIS approaches have commonly become a preferred approach for smaller GISTs in anatomically favorable locations. However, guidelines remain cautious about applying MIS techniques for larger GIST given the risk of tumor rupture, which increases the risk of dissemination and recurrence (19,20).

MIS approaches in large gastric GIST

In the past decade, there has been a growing body of literature assessing the feasibility, safety, and outcomes of MIS resection of gastric GISTs >5 cm.

Intraoperative outcomes

Reported differences in operative time between MIS and open approaches are mixed. In a meta-analysis of 7 Asian and European studies performed by Lian et al., operative times were shown to be comparable between the laparoscopic and open groups [weighted mean difference (WMD) =−0.87 min; 95% CI: −47.50 to 47.75; P=0.97] (21). However, subsequent retrospective studies found that operative times for laparoscopic cases were longer than the conventional open approach (22,23). As Khoo et al. noted, laparoscopic resections may be more challenging given increased tumor size and care needed to avoid excessive manipulation and rupture (22).

Despite the conflicting evidence on operative time, intraoperative blood loss seems to be equivalent, if not improved, for MIS approaches compared to open resection. A meta-analysis performed by Lian et al. reported no difference in volume of intraoperative blood loss between groups (WMD =−34.38 mL; 95% CI: −79.60 to 10.84; P=0.14) (21). Other subsequent retrospective studies also reported no difference in blood loss between these approaches (22,24). However a retrospective study of 44 patients found significantly decreased blood loss in the laparoscopic group (73±36 vs. 105±51 mL, P=0.02) (23). This latter finding is consistent with other larger retrospective studies investigating the safety and feasibility of laparoscopic resections, although these prior studies were not exclusive to larger GISTs (25-27). Lower blood loss in the laparoscopic group may be attributable to better visualization of anatomy and vasculature through laparoscopic cameras. Additionally laparoscopic wounds are smaller compared to open incisions, minimizing blood loss.

Postoperative outcomes

One benefit of a MIS approach reported in many oncologic populations is shorter length of stay and recovery times. One of the earliest comparative studies reported by De Vogelaere et al. demonstrated superior postoperative outcomes in the laparoscopic group (28). This study, while not limited to patients with GISTs >5 cm, reported earlier nasogastric tube removal (mean 3 vs. 5.5 days, P<0.001) and initiation of feeds (mean 4 vs. 6.4 days, P=0.002) in the laparoscopic group. The median length of hospital stay was also significantly shorter (7 vs. 14 days, P=0.007) (28).

In subsequent studies focusing primarily on large gastric GISTs, similar findings were demonstrated. A retrospective study of 3,765 American patients found that an MIS approach was associated with significantly shorter hospital stays (4.7 vs. 6.3 days, P<0.001) (29). This finding was also reflected in a meta-analysis of several Asian and European retrospective studies comparing overall lengths of stay between laparoscopic and open groups (WMD =−2.38 days, 95% CI: −3.09 to −1.66, P<0.05) (30). Smaller studies have found that patients undergoing MIS resection had equivalent or faster time to flatus and diet tolerance compared to conventional open resection (31,32).

MIS approaches have demonstrated comparable rates of postoperative morbidity and mortality. The prior meta-analysis found no significant differences in the rate of postoperative complications between open and laparoscopic groups (OR =0.54, 95% CI: 0.30–0.99, P=0.05) (30). A retrospective American cohort study reported that MIS resection had improved 30-day mortality (0.5% vs. 1.2%, P=0.03) and 90-day mortality (0.9% vs. 2.1%, P=0.04) (29). Stanek et al. evaluated postoperative complications rates after laparoscopic resection and found no differences between patients with GIST ≤5 and >5 cm (33). Similar studies by Milone et al. and Severino et al. also found comparable complication rates between size groups (34,35).

Oncologic outcomes

Key principles of surgical resection are avoidance of tumor rupture and achievement of R0 resection. These have been concerns for utilizing MIS approaches for larger gastric GISTs, as increased size may make manipulation during resection more difficult thus increasing risk of tumor rupture. Tumor rupture has been associated with high locoregional recurrence rates.

There is increasing evidence demonstrating that MIS approaches have equivalent recurrence rates, disease-free survival, and overall survival compared to open surgical approaches. A meta-analysis of 7 Asian and European studies demonstrated similar recurrence rates between the laparoscopy and open resection groups (OR =0.54, 95% CI: 0.26–1.09, P=0.08) (30). Overall survival was similar between groups (OR =0.19, 95% CI: 0.03–1.17, P=0.07), but the laparoscopy group had higher disease-free survival rates (OR =0.52, 95% CI: 0.28–0.97, P=0.04) (30). A retrospective review of an American cohort also demonstrated similar overall survival rates (29).

These results have been replicated in several smaller cohort studies, with both laparoscopic and robotic approaches (24,32,36,37). In a cohort of patients with GISTs 5–8 cm who underwent laparoscopic (N=36) or open (N=30) resection, Lin et al. reported similar 5-year recurrence-free survival (94.2% vs. 100%, P=0.20) and 5-year overall survival (94.3% vs. 96.7%, P=0.67) (24). de’Angelis et al. reported outcomes of 36 patients who underwent laparoscopic or robotic resection of large gastric GISTs (32). R0 resections were achieved in their size- and location-matched 36-patient cohort. There was only one recurrence in the laparoscopic group and none in the robotic group (32). These studies report promising long-term oncologic outcomes of MIS resection of large gastric GISTs.

MIS approaches in unfavorable locations

Current guidelines support the use of MIS resection of gastric GIST in favorable anatomical locations, including the fundus, anterior wall of the gastric body, and greater curvature (19). There is currently no consensus supporting the routine use of MIS resection of tumors in less favorable anatomic locations, including the GEJ, lesser curvature, posterior wall of the gastric body, and antrum (Figure 1). However with advances in laparoscopic techniques and rapid development of robotic-assisted surgery, there is a growing body of evidence suggesting that MIS resection is feasible and safe (2,38,39).

Figure 1 Favorable and unfavorable anatomical locations for resection.

Intraoperative and postoperative outcomes

A study of 214 patients who underwent laparoscopic or open resection demonstrated that laparoscopic resection of GISTs located in unfavorable locations can be performed safely with shorter operative times (119±53.4 vs. 197.4±71.2 min, P<0.001) and lower blood loss (35.2±31.2 vs. 350.6±619.5 mL, P=0.001). Patients experienced faster time to first flatus (3.2±1.2 vs. 4.2±2.0 days, P=0.007), initiation of diet (4.2±1.9 vs. 5.5±2.5 days, P=0.012), shorter length of stay (9.5±5.3 vs. 14.9±7.8 days, P=0.001), and lower rates of postoperative complications (4.7% vs. 35.5%, P=0.001) (40). Similar results were reported in another multi-center retrospective study (18). Park et al. reported that patients with GISTs in unfavorable anatomic locations who underwent laparoscopic resection (N=173) had shorter length of stay (6.6±4.8 vs. 8.9±7.0 days, P<0.001) and fewer postoperative complications (4.0% vs. 10.1%, P=0.04) compared to patients who underwent open resection (N=188) (18).

MIS techniques now encompass robotic-assisted approaches. Robotic-assisted surgery offers numerous benefits compared to laparoscopic approaches, including improved 3-dimensional visualization and better articulation through wristed surgical instruments (1). These advantages facilitate access to locations deemed unfavorable and allow more precise dissection, suturing, and stapling (1).

However these advantages need to be weighed against operative outcomes. Supsamutchai et al. reports that operative times in robotic-assisted surgery are longer than laparoscopic approaches (261±54 vs. 144±64 min, P<0.001) (41). This was attributed to the use of a hand-sewn repair in the robotic approach versus stapled resection and closure in the laparoscopic group. Patients also had longer time to resumption of normal diets in the robotic group (5.7±2.0 vs. 4.0±1.4 days, P=0.03). However there were no surgical site infections or anastomotic leakages in either robotic or laparoscopic groups (41). In a small case series of robotic wedge gastrectomy reported by Maggioni et al., there were no intraoperative or postoperative complications reported with all cases achieving R0 resection (42). Their cohort, consisting of 6 patients with 3 having tumors on the posterior gastric wall, had a mean operative time of 173±39 minutes and a mean hospital stay of 3±1 days (42). Another case series reported by Arseneaux et al. had similar results, in which R0 resection without any severe postoperative complications was achieved in all patients (43). In a series of 10 patients with GIST deemed difficult based on unfavorable locations and/or size criteria >5 cm, Furbetta et al. reported no cases of tumor rupture or intraoperative complications (44).

The small sample sizes in each of these studies must be considered when assessing robotic-assisted GIST resection. Taking the available evidence into account, robotic-assisted resections may take longer than laparoscopic resections, which may be attributable to device docking and differences in techniques, such as utilization of hand-sewn repairs.

Oncological outcomes

Several case series and retrospective studies focusing on MIS resection of tumors in unfavorable locations have found equivalent recurrence-free and overall survival rates compared to open surgery. In a study of 214 patients with gastric GIST located in favorable (N=140) or unfavorable (N=74) anatomic locations who underwent either open or laparoscopic resection, Huang et al. reported similar 5-year recurrence free survival and overall survival between the laparoscopic and open approaches when patients were analyzed by anatomic location (40). In a single-center series conducted by Lwin et al., 25 patients underwent robotic-assisted GIST resection. The majority of their cohort had tumors located in unfavorable locations (12 in GEJ, 7 in lesser curvature, 4 in posterior gastric wall) (45). The GEJ and pylorus were successfully preserved in all patients. Negative margins were obtained in 24/25 patients (96.3%)—the only tumor with a focally positive margin was located in the GEJ. However there was no recurrence detected at a median follow-up of 11.3 months (45).

Small case series and retrospective studies report that MIS resection of GIST located in anatomically unfavorable locations appears to be safe, feasible, and equivalent to open resection. Further research is still needed to investigate long-term oncologic outcomes; however large, prospective studies may be difficult to conduct due to the rarity of these tumors.

Approaching from above and below—exploring laparoscopic and endoscopic cooperative surgery (LECS)

As MIS techniques have improved rapidly in the past decade, collaborative techniques have also evolved in parallel in the form of LECS. Endoscopic resections have been commonly utilized for resection of small gastric GISTs with the benefits of less blood loss, less pain, and earlier recovery of bowel function (46,47). However common complications with endoscopic techniques are perforation with the possibility of tumor rupture and hemorrhage (46-48). As discussed previously, laparoscopic techniques have evolved to allow for more minimal resections with better functional outcomes and recovery. However depending on tumor characteristics, margins may still be more extensive than needed.

The hybrid LECS approach has the benefit of maximizing each technique’s strengths while overcoming their respective limitations. Since the development of the “classic” LECS procedure in 2008, it has been adapted into a multitude of approaches including inverted LECS, closed LECS, laparoscopic-assisted endoscopic full-thickness resection (LAEFR), the combination of laparoscopic and endoscopic approaches to neoplasia with a non-exposure technique (CLEAN-NET), and non-exposed endoscopic wall-inversion surgery (NEWS) (Figure 2) (49-51). The basic surgical principals remain constant. The endoscopic team defines the margins of the tumor by direct visualization. Both teams then simultaneously work to dissect the tumor free from their respective side. The laparoscopic team can subsequently close any remaining gastric wall defects. The specimen can be removed either transorally or transabdominally (50).

Figure 2 Overview of LECS techniques. LECS, laparoscopic-endoscopic cooperative surgery; GIST, gastrointestinal stromal tumor; GEJ, gastroesophageal junction.

The use of LECS in resection of gastric GISTs <5 cm has been shown in several studies to be safe and feasible (52-56). A comparative study by Yin et al. reported that in patients with GISTs that underwent LECS, there were no differences in time to recovery of bowel function (2.07±0.59 vs. 2.83±0.95 days in laparoscopic group and 2.57±1.17 days in endoscopic group, P=0.28), length of hospital stay (6.33±2.53 vs. 6.53±2.00 days in laparoscopic group and 5.83±2.69 days in endoscopic group, P=0.45) and rate of postoperative complications (13% vs. 10% in laparoscopic group and 15% in endoscopic group, P=0.81) (52). Only one case had a positive margin, occurring with endoscopic resection only. There was only one recurrence overall in the laparoscopic group, with a median follow-up time of 69.5 months (52).

Harada et al. reported 213 patients who underwent LECS with all achieving R0 resections and no recurrences at a median follow-up time of 43 months (53). Operative times were comparable to those measured in laparoscopic resections, with a median time of 181 min. Hanayama et al. reported 40 patients who underwent LECS with an average tumor size of 25±9 mm, had an average estimated blood loss of 25±87 mL, zero conversions to open surgery, and only one severe postoperative complication (54). This singular case had postoperative hemorrhage which required subsequent hemostatic clipping, a known complication of endoscopy. There was no local or peritoneal recurrence, with a median follow-up of 31 months (range, 1–98 months).

A commonly cited benefit of LECS over traditional wedge resection is the ability to minimize margins. This allows for better anatomical and functional preservation of the remaining stomach. Komatsu et al. reported significantly shorter maximum margins in their LECS cohort compared to wedge resections (10 vs. 15 mm, P=0.02) (57). Kanehira et al. also reported significantly smaller margin widths in their CLEAN-NET group compared to wedge resections (5.4 vs. 33.1 mm, P<0.001) (58). Shoji et al. observed that the mean ratio of resected specimen area to tumor area was significantly higher in their laparoscopic group (449.7% vs. 261.2% in LECS and 191.0% in NEWS, P<0.001) (59).

For gastric GISTs >5 cm, there is a lack of literature describing the utilization of LECS and size remains a common exclusion criteria. There are few reported cases of larger GISTs safely resected using LECS. For example Kanehira et al. reported resection of a 9-cm tumor in their cohort using CLEAN-NET (58). However at the same time Mitsui et al. reported difficulty in retrieval of a 4-cm tumor utilizing NEWS, requiring retrieval through an umbilical incision instead of its usual transoral retrieval method (60). Additional difficulties in widely adapting LECS are the need for more proceduralists for the endoscopic and laparoscopic teams, and learning curve for these techniques.

Taken together, the current literature supports the safety and feasibility of LECS in resection of selected gastric GISTS, primarily those <5 cm. LECS allows for better identification of the tumor margins by direct endoscopic visualization, and postoperative outcomes are comparable to traditional MIS approaches. However further studies need to be conducted as much of the literature remains retrospective at this time with relatively small cohorts.

Conclusions

Advancements in MIS techniques have expanded the pool of candidates for MIS gastric GIST resection. There is a growing body of literature exploring the safety, feasibility, and oncologic outcomes of MIS gastric GIST resection; however, the majority of studies are small case series and retrospective reviews. Due to the rarity of gastric GIST there is a lack of prospective data and clinical trials comparing open and MIS gastric GIST resection. Despite this, the current data are promising, suggesting equivalent, if not improved, safety, feasibility, and oncologic outcomes compared to conventional open resection.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://ales.amegroups.com/article/view/10.21037/ales-23-67/rc

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