Endoscopy-Assisted Laparoscopic Resections for Gastric Gastrointestinal Stromal Tumors: A Retrospective Study

Abstract

Objective:

To explore the safety, feasibility, and clinical curative effect of endoscopy-assisted laparoscopic resections for gastric gastrointestinal stromal tumors (GISTs).

Materials and Methods:

We retrospectively compared the general condition of 41 GIST patients undergoing endoscopy-assisted laparoscopic resections (n = 41, combined group) with those undergoing traditional open gastrectomy (n = 43, open surgery group).

Results:

All patients survived during the surgery. The average operation time of the combined group and the open surgery group was 90 ± 40 minutes and 120 ± 60 minutes, respectively, and no significant difference (P = .088) was observed. Bleeding volume during operation was significantly lower [(50 ± 20 versus 150 ± 40) mL, P < .001] and recovery time of the gastrointestinal function was significantly shorter in the combined group [(2.02 ± 0.99) days versus (3.02 ± 1) days, P < .001]. No statistical difference was found in the postoperative complications (5% versus 12%, P = .442) or GIST recurrence (2.44% versus 2.33%, P = 1.000) between the two groups. Follow-up visit showed no death.

Conclusion:

For GIST patients who attempted to receive gastrectomy, endoscopy-assisted laparoscopic resections showed advantages on the operation time, bleeding volume, and recovery time and are suggested as a better alternative for GISTs.

Introduction

Gastrointestinal stromal tumors (GISTs),with the incidence of 0.1%–2% worldwide, are the most common mesenchymal tumors of the gastrointestinal (GI) tract and represent ∼80% of all stromal tumors.¹ A great majority of the GISTs occur in the stomach, with rare occurrence in the small intestine, omentum, colon, and rectum or esophagus.^2–5 Curative treatment of GISTs involves surgical resection and laparoscopic technique, which can be divided into different subtypes: transgastric resections, endoscopy-assisted laparoscopic resections, wedge resections, partial gastrectomy, and hand-assisted laparoscopic resections.⁶ However, there is still debate regarding the most appropriate operative approach for larger GISTs. Laparoscopic resection combined with gastroscope management (or endoscopy-assisted laparoscopic resections) has gained improvement in GIST surgery in clinical practice. Increasing evidence has proved the feasibility and safety of laparoscopic resection of GISTs. The benefit of the combined management for oncologic results, however, has not been reported widely.^7–12

In our study, we retrospectively compared the general information, benefit of operation, perioperative outcome, and oncologic outcome between the 41 patients undergoing endoscopy-assisted laparoscopic resections for GISTs and 43 patients undergoing traditional open gastrectomy for GISTs. We aimed to observe whether the endoscopy-assisted laparoscopic resections have better outcomes compared with open surgical resection in Chinese GIST patients.

Materials and Methods

Study subject

A total of 84 patients with GISTs were all retrospectively reviewed from the GI surgery department of the third affiliated hospital of Sun Yat-sen University from January 2011 to December 2014. The GISTs were pathologically diagnosed and localized endoscopically. We carefully excluded patients with upper GI hemorrhage, perforation or obstruction, tumor size >10 cm by image or biopsy, tumors located outside the stomach, and distant metastasis. Among all these patients, 41 underwent endoscopy-assisted laparoscopic resections for GISTs (combined group), while 43 underwent traditional open gastrectomy (open surgery group). All the surgeries for the GIST patients were performed by the same senior surgeons with working experience longer than 8 years. This study and the protocol were approved by the Ethics Committee of the Third Affiliated Hospital of Sun Yat-sen University.

Anesthesia and surgical preparation

For the endoscopy-assisted laparoscopic resections, after induction of general anesthesia, the patient was placed in a supine position with both legs abducted. The surgeon stood on the left side of the patient and the first assistant stood on the right side. The second assistant holding a laparoscopic lens stood between the expanded legs. Pneumoperitoneum was established to an insufflation pressure of 1.60–1.86 kPa. Generally, there were five laparoscopic ports: camera port with 30° inclined lens in the infra-umbilical region and four additional ports in left upper, left lower, right upper, and right lower quadrants, respectively. The endoscopist was placed on the left side of the patients while the assistant stood beside the patient's head. The endoscope was guided into the fore gut through the pharynx into the esophagus. The mucosa of the esophagus and stomach was observed and the lesion characteristics were determined.

Endoscopy-assisted laparoscopic resections

Endoscopy-assisted laparoscopic resections, including laparoscopic wedge resection (LWR), laparoscopic-assisted proximal gastrectomy (LAPG), and laparoscopic-assisted distal gastrectomy (LADG) were determined according to the tumor size and location.

LWR was performed as follows: (1) Anterior wall: ligaments adjacent to the tumor were dissected, the endoscope was reintroduced into the stomach with a little air inflation, pressure was applied to the stomach with biopsy forceps about 2–4 cm around the lesion, and the serosal surface of the tented-out stomach was grasped through the laparoscope. Subsequently, the stomach was desufflated, and an endo-GIA stapler containing the gastric mass was placed across the stomach. To confirm that the mass was successfully captured within the portion of the stomach, the endoscope was advanced back into the stomach, followed by deploying the stapler. The stapler was used to ligate and transect the stomach portion containing the mass. (2) Posterior wall: gastrocolic and gastrosplenic ligaments were dissected using harmonic scalpel and the entire greater curvature and posterior wall of stomach was reflected. Localization and resection were performed accordingly. (3) Lesser curvature of stomach: hepatogastric ligament was gently dissected; the endoscopist should be more careful when the tumor is closer to the pylorus.

LAPG or LADG was conducted for GIST, which was close to the cardia or pylorus and difficult for local excision. The stomach specimen was then removed through the umbilical port and submitted to pathology. After the resection, the endoscopist ensured the absence of remnant tumor lesion on the gastric mucosa, absolute closure of the wedge resection, and absence of active bleeding.

Laparotomy

Wedge resection, proximal gastrectomy, or distal gastrectomy was performed according to the tumor size and location. Total gastrectomy was avoided unless GIST was relatively larger or had malignant potential.

Postoperative observation

The tumor tissue samples and lymph nodes were carefully checked and subjected to pathological examination after the operation. Timely rehydration, nutrition, and symptomatic therapy were given postoperatively. Moreover, the operation time, intraoperative blood loss, postoperative use of analgesics (days of analgesic usage), transfer laparotomy cases, GI function recovery time (time of the first anal aerofluxus after surgery), postoperative hospitalization days, and complications were recorded as well. Follow-up visits to all the cases were consecutively done by telephone, mail, or outpatient follow-up.

Statistical analysis

In this study, the Statistical Package for Social Sciences, version 13.0, was used for statistical analysis. Student's t-test was used to assess significant differences in the patients' demography data and general condition during operation between the combined group and the open surgery group. Pearson's χ² test was used to compare postoperative complications between the two groups (if expected values were below 5, Fisher's exact test was used). P values <.05 were regarded as statistically significant.

Results

General information

Among the 84 patients, 41 patients (14 males, 27 females) with a mean age of 54.85 ± 10.19 years in the combined group underwent endoscopy-assisted laparoscopic resections, while in the open surgery group, 43 patients (18 males, 25 females) with a mean age of 53.19 ± 9.95 years experienced traditional open transgastric resections. The patients' demography data were recorded and the age (P = .450), gender (P = .467), body–mass index (P = .234), and past operation history (P = 1.000) were all matched without statistic difference between the two groups (Table 1).

Table 1.

Characteristics of the Gastrointestinal Stromal Tumor Patients in the Combined Group and the Open Surgery Group

		Gender
	n	Female	Male	Mean age (year)	BMI	Past operation history (%)
Combined group	41	27	14	54.85 ± 10.19	21.09 ± 3.37	2 (4.88%)
Open surgery group	43	25	18	53.19 ± 9.95	21.90 ± 2.82	3 (6.98%)
P		.467		.450	.234	1.000

BMI, body–mass index.

General surgery situation of the two groups for GIST patients

The two groups showed no difference in tumor size with compatible tumor locations and operation ways (P = .383 for tumor location; P = .331 for tumor size; P = .268 for operation ways) (Table 2). For the combined group, 38 cases (92.68%) underwent the endoscopy-assisted laparoscopic GIST resections or LWR, one case underwent LAPG (2.44%), and two cases underwent LADG (4.88%). No patient suffered the total gastrectomy (Table 2). For the open surgery group, 33 cases (76.74%) underwent GIST resections or LWR, while three cases underwent LAPG (6.98%), and six cases underwent LADG (13.95%). Besides, 1 patient underwent total gastrectomy because of a massive tumor next to the cardia (Table 2).The local resection rate of the combined group (92.68%) was obviously significantly higher (P = .043) than that of the open surgery group (76.74%), which could be viewed in Table 2.

Table 2.

General Surgery Situation of the Gastrointestinal Stromal Tumor Patients in the Two Groups

		Tumor location				Operation method
	n	Fundus	Corpus	Antrum	Tumor size	Local resections	Proximal gastrectomy	Distal gastrectomy	Total gastrectomy
Combined group	41	11	25	5	3.33 ± 1.61	38	1	2	0
Open surgery group	43	15	26	2	3.66 ± 1.51	33	3	6	1
P		.383			.331	.268

General condition during operation and postoperative conditions of the surgery

The operation time of the combined group was 103.66 ± 37.17 minutes, while the operation time of the open surgery group was significantly shorter (136.74 ± 50.81 minutes, P = .001) (Table 3). The combined group showed shorter lesion lengths (P = .001) than the open surgery group. The estimated blood loss was 50.73 ± 26.11 versus 114.19 ± 78.47 mL in the combined group and the open surgery group, respectively, which showed a statistic difference (P < .001). Postoperatively, there were significant differences in flatus passage days and analgesic duration as well (P < .001 for flatus passage days; P < .001 for analgesic duration). Moreover, the combined group showed shorter days to resume diet (P < .001) and shorter postoperative hospital stays compared with the open surgery group (P < .001) (Table 3).

Table 3.

General Condition During Operation and Postoperative Conditions of the Surgery

	Combined group (n = 41)	Open surgery group (n = 43)	P
Operation time (minutes)	103.66 ± 37.17	136.74 ± 50.81	.001
Incision lengths (cm)	48.54 ± 16.63	145.79 ± 57.08	.000
Bleeding volume (mL)	50.73 ± 26.11	114.19 ± 78.47	.000
Analgesic duration (days)	2.60 ± 1.43	4.52 ± 2.08	.000
Flatus passage days (days)	2.38 ± 1.23	3.76 ± 1.51	.000
Time for liquid diet (days)	3.09 ± 1.01	5.28 ± 1.74	.000
Duration of hospitalization (days)	8.05 ± 3.14	12.98 ± 3.85	.000

Postoperative complication and recurrence of the two groups

There was no death in both groups, while there was one case of hemorrhage from the incision site and 1 patient with pulmonary infection in the combined group, both of whom were conservatively treated and cured completely. As for the postoperative complication in the open surgery group, there were one case of hemorrhage of the incision, two cases of pulmonary infection, and one case of incision infection, which were treated conservatively as well. The incidence of postoperative complication showed no difference between the two groups (4.88% for the combined group and 9.30% for the open surgery group) (P = .716, Table 4).

Table 4.

Postoperative Complications and Recurrence of the Two Groups

	Combined group (%)	Open surgery group (%)	P
N	41	43
Postoperative complications	2 (4.88%)	4 (9.30%)	.716
Postoperative recurrence	1 (2.44%)	1 (2.33%)	1.000

We did a follow-up visit of 5–36 months after the surgery to all of the patients, and no death was noted during the follow-up. As shown in Table 4, in the combined group, 1 patient suffered from recurrence 11 months after surgery (2.44%), while 1 patient in the open surgery group suffered from recurrence 15 months after surgery as well (2.33%), which showed no statistic difference (P = 1.000). The other patients in the two groups were in complete recovery without recurrence.

Discussion

Most mesenchymal tumors arising from the GI musculature in humans are GISTs, which originate from interstitial Cajal cells, as discovered by Isozaki and Hirota in 1998.¹³ Although surgery remains the standard initial treatment for nonmetastatic GISTs, the preferred operative approach and the extent of resection are still not well established. Most of the GISTs are localized with a distinct boundary to the normal tissue and are with a tendency to grow in an exophytic manner. For the GISTs, lymphatic spread is quite uncommon and, as such, systemic lymphadenectomy has been deemed unnecessary,^14,15 thus reducing the need for large-scale lymph node dissection and making the surgery schedule easier with the local removal of the primary lesion.^11,16,17 The most important step during the laparoscopic resections for GISTs is the tumor-free principle because the rupture of pseudocapsule would not only induce local hemorrhage but also increase the incidence of dissemination of the tumor to a great extent. Thereby, once the rupture happened, the optimal way is the excision of the whole lump in or around the tumor, including the normal tissue. Therefore, wedge resection is considered to be the preferred method for treatment of the majority of GISTs.

Lukaszczyk and Preletz¹⁸ in 1992 were the first to report a successful laparoscopic resection of a gastric GIST, and later in 1994, Kitano et al.¹⁹ reported the first case of LADG in Japan when laparoscopy began to gain improvement and roles for surgery for GISTs. Theoretically, GIST of any size can be operated by laparoscopy, but there is still debate on the standard size for the laparoscopic resection. In 2005, the National Comprehensive Cancer Network and the European Society of Medical Oncology released consensus statements that recommended that a laparoscopic resection may be acceptable for small intramural tumors (<2 cm), but otherwise should be avoided.²⁰ However, the guidelines were modified in 2007 that tumors up to 5 cm can be safely approached laparoscopically, and even larger tumors could be considered through a laparoscopic hand-assisted approach.²¹ Besides, according to Mochizuki's team, LWR was a feasible treatment option for GISTs of the stomach if the lesion is <5 cm in diameter as well.²² On the appropriate tumor size for laparoscope surgery, we think that it should not be the absolute indication as the operative successful rate was closely related to operator's skill and experiences. If careful observations on integrity of the tumor peplos, the presence of adjacent organ invasion, and peritoneal metastasis are combined with the proficient skills and the disease-free principle strictly, the undesirable outcomes would be largely avoided. On the other hand, withdrawing the tumors under protection with plastic covering to avoid incision planting and taking out a larger tumor after another small incision can reduce the surgical trauma as well.

For GISTs with a diameter <2 cm, localization of the tumors becomes a difficulty as hand touch is impossible during laparoscopic exploration. Thus, endoscopic tumor location showed its crucial role in increasing accuracy and safety of the surgery. Endoscopy-assisted laparoscopic resections for GISTs have become a popular technique⁶ as endoscopy could localize the tumor accurately and help the surgeon to choose the appropriate operation method and the excision extent. Especially when the tumor is closely located next to the cardiac or pyloric, the excision extent could be precisely calculated by gastroscopy, thus avoiding cardiac or pyloric stenosis and reducing the possibility of subtotal gastric resection or total gastric resection.

In 2002, Matthews et al. conducted a retrospective review and showed that laparoscopic resection of gastric GISTs offered a decreased length of stay, a trend to decreased blood loss, and comparable oncologic outcomes.²³ In 2013, Koh's group²⁴ published a systematic review of 11 observational studies comparing laparoscopic with open resection for evaluation of short- and long-term outcomes, which showed that the laparoscopic approach had a lower frequency of minor complications, lower length of stay, shorter time to initiation of oral diet, and lower intraoperative bleeding. However, they did not find any statistically differences in reoperation rate, operative time, positive margins, local recurrence, cancer-free survival, and overall survival. While in the same year, Shu et al.²⁵ divided 36 GIST cases into the laparoscopic surgical treatment group (laparoscopy group, n = 15) and the open resection treatment group (open resection group, n = 21) and drew the conclusion that laparoscopic resection of gastric GISTs offered the advantages of less trauma, faster recovery, and shorter hospital stay. In our study of 41 patients in the combined group and 43 patients in the open surgery group, no difference was noted on the general surgery situation, including tumor size, tumor locations, and the operation ways. Similar to previous studies, our result showed that the laparoscopic approach offered the advantages of a shorter lesion length, lower intraoperative bleeding, shorter time to initiation of oral diet, faster recovery, and shorter hospital stay than the open surgery group. Besides, the result in our study also showed a shorter operation time and analgesic duration of the surgery. With regard to postoperative complications and recurrence, there was no difference between the two groups, which indicates that the endoscopy-assisted laparoscopic excision was as good as the traditional open surgery on the operative prognosis for GISTs.

Conclusion

Our data demonstrate that the endoscopy-assisted laparoscopic excision technique is a safe, feasible, and minimally invasive alternative approach for local or segmental resections of gastric GISTs.

Footnotes

Acknowledgments

Our study was supported by the Medical Scientific Research Foundation of Guangdong Province (B2013127) and the Major Project of Production, Teaching, and Research Collaborative Innovation of Guangzhou City (2060404).

Disclosure Statement

No competing financial interests exist.

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