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Comparison of long-term results between laparoscopy-assisted gastrectomy and open gastrectomy with D2 lymphadenectomy for advanced gastric cancer Cheng Fang, M.D.1, Jin Hua, M.D.1, Jipeng Li, M.D., Jianyong Zhen, M.D., Fei Wang, M.D., Qingchuan Zhao, M.D., Jianbo Shuang, M.D., Jianjun Du, M.D.* Department of Surgery, Xijing Hospital of Digestive Diseases, The Fourth Military Medical University, No. 127 Changle West Road, Xian 710032, China

KEYWORDS: Laparoscopy-assisted gastrectomy; Advanced gastric cancer; Case–control study

Abstract BACKGROUND: The aim of this study was to compare surgical outcomes and oncologic efficacy of laparoscopy-assisted gastrectomy (LAG) versus open gastrectomy (OG) for advanced gastric cancer. METHODS: For this study, 87 consecutive advanced gastric cancer (AGC) patients who underwent LAG with D2 lymph node dissection between April 2005 and October 2009 were enrolled, compared with 87 AGC patients who underwent OG during the same period. RESULTS: Operative procedure and surgical margin were similar between the 2 groups. The operative time was significantly longer in the LAG group than the OG group, while the estimated blood loss was significantly less in the LAG group. There were no significant differences in postoperative complications and in the number of lymph nodes retrieved. The use of analgesic drugs was significantly less after LAG. Length of postoperative stay was significantly shorter in the LAG group. The 5-year overall survival rate and recurrence-free survival rate were comparative between the 2 groups. CONCLUSION: This 5-year case–control study presented that laparoscopy-assisted gastrectomy may be a safe and acceptable procedure in terms of long-term results for AGC. Ó 2014 Elsevier Inc. All rights reserved.

Since Kitano et al1 first performed laparoscopy-assisted gastrectomy (LAG) for gastric cancer, it has gained acceptance widely. Numerous reports have indicated that LAG for early gastric cancer is feasible and equivalent to open gastrectomy (OG) in terms of oncologic parameters, with less blood loss and fewer complications. Despite the clear The authors declare no conflicts of interest. * Corresponding author. Tel.: 186-29-8477-1533; fax: 186-29-82539041. E-mail address: [email protected] Manuscript received June 25, 2013; revised manuscript September 18, 2013 1 These authors contributed equally to this work and are considered to be co-first authors. 0002-9610/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2013.09.028

benefits of laparoscopic gastrectomy in early stage cancers demonstrated in the literature, the application of laparoscopic techniques for advanced gastric cancer (AGC) remains controversial. Several concerns exist mainly about the technical feasibility and curability of laparoscopic D2 gastrectomy for AGC. In recent decades, preliminary works2–5 have demonstrated that LAG for AGC is technically feasible with comparable survival rate to open D2 gastrectomy. Moreover, 3 recent 5-year case–control studies6–8 showed that LAG can achieve an oncologically equivalent resection and the 5-year survival rate did not differ between LAG and OG groups. The aim of this case–control study is to provide our evidence for the safety and feasibility of LAG with D2

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lymphadenectomy for AGC, in terms of surgical results and 5-year survival rate.

trocars were placed in the right hypochondral and bilateral abdominal regions. The stomach resection pathway was selected according to the location of the tumor. Distal gastrectomy was the common procedure for tumor located in the middle and lower third of the stomach, total gastrectomy was performed for proximal gastric cancer. First, the left gastroepiploic vessels were divided to dissect lymph node 4sb. Then, the division was continued toward the inferior border of the pancreas neck portion while identifying the middle colic vessels, and lymph node 14v around the superior mesenteric vein were removed. The right gastroepiploic vessels and gastric artery were divided at their origin to clear lymph nodes 6 and 5. The duodenum was transected about 2 cm distal from the pylorus, using an endoscopic linear stapler (Endo-GIA, US Surgical Corporation, Norwalk, CT). The lymph nodes along the common hepatic (group 8a) and proper hepatic (group 12a) arteries were removed. The lymph node dissection was continued toward the celiac axis, and the left gastric vein and artery were exposed and divided individually at their roots with the removal of lymph nodes 7 and 9. The right cardiac nodes (group 1) and group 3 were dissected, following the lymph node 11p along the proximal splenic artery were removed. During laparoscopy-assisted total gastrectomy, lymph nodes around the distal splenic artery (group 11d) and splenic hilum (group 10) were also dissected. Pancreaticosplenectomy was not performed routinely, but only when necessitated by tumor invasion. Finally, lymph nodes 2 and 4sa were dissected. After lymphadenectomy and gastrectomy, a 5 to 7 cm laparotomy was made under the xyphoid to remove the specimen and perform gastrointestinal anastomosis or esophagojejunostomy. Open operations were performed in a standard fashion as previously reported. Approximately 15- to 20-cm length incision was made from falciform process to periumbilical area. Gastrectomy and D2 lymph node dissection were performed basically. All gastrectomies were performed by a single surgeon experienced both in laparoscopic gastrectomy and OG in our institution.

Patients and Methods This study was a retrospective case–control study that includes 87 patients who underwent LAG for AGC with D2 lymph node dissection in our institution from April 2005 to October 2009. This group was compared with 87 matched patients who underwent the same procedure in an open fashion during the same period of time. The criteria for inclusion were the patients who underwent laparoscopic or open D2 gastrectomy for local T2 to T4a AGC, with no evidence of distant metastasis or invasion to adjacent organs. Patients in both groups were matched for stage, age, sex, American Society of Anesthesiology risk class (ASA), body mass index (BMI), and operative procedure. Clinical and pathological data were obtained from operative and pathological reports from our institution. In this study, both the procedures (LAG and OG) were suitable for all patients who met our inclusion criteria. After a sufficient explanation of the surgical and oncologic risks for both procedures, the surgical procedure (LAG or OG) was chosen by the patients themselves when a written informed consent was signed preoperatively. Postoperative complications were classified using a therapy-oriented severity grading system (TOSGS), which simplified the definition of postoperative complications and graded the severity of these events.9,10 Since first reported by Clavien,11 this system had been modified by several studies. The modified classification in this study is presented as follows: grade 1, no need for speciflc intervention; grade 2, need for drug therapy such as antibiotics; grade 3, need for invasive therapy; grade 4, organ dysfunction with intensive care unit stay; and grade 5, death.12 Data regarding follow-up were obtained from our institutional outpatient clinical database. All patients were subjected to follow-up and no patients were lost in both groups. Patients follow-up were scheduled to perform abdominopelvic computed tomography scan and abdominal ultrasound every 6 months after surgery. Endoscopy is suggested every 6 months to closely monitor recurrence for patients with T4a depth or significant positive lymph node metastasis, and once a year for other patients with AGC after surgery. The statistical analysis was performed using Student t test or chi-square test, and P value ,.05 was considered to indicate statistical significance. Cumulative survival was estimated using Kaplan–Meier method and compared with log-rank test. Analyses were performed with the use of SPSS Version 17.0 (SPSS Inc, Chicago, IL).

Surgical procedure Under general anesthesia, the patients were placed in a supine position with legs apart. One initial 10-mm camera port was introduced below the umbilicus. A 12-mm port was inserted in the left hypochondral region. And three 5-mm

Results Patient demographics One hundred seventy-four case-matched patients were evaluated (87 laparoscopy vs 87 open), with a median age of 57 years (range, 33 to 82 years) in laparoscopy group and 56 years (range, 33 to 79 years) in open group. There were no significant differences in clinical features between LAG and OG groups, including sex ratio, median BMI, ASA, and comorbidity disease (Table 1).

Operative characteristics The surgical outcomes of both cohorts are shown in Table 2. In total, 46 patients underwent a distal gastrectomy

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Table 1 Patient demographics for patients who underwent laparoscopy-assisted and open gastrectomy

Age (range, y) Sex Male Female BMI (range, kg/m2)

Laparoscopic (n 5 87)

Open (n 5 87)

P value

57 (33–82)

56 (33–79)

NS

78 78 9 9 23.3 22.9 NS (18.3–31.6) (18.3–31.6) ASA NS 1 38 31 2 39 42 3 10 14 Comorbidity disease NS Hypertension 4 4 Cardiovascular 3 5 Diabetes 5 5 Liver 3 2 Cholecyst 3 4 Pulmonary 2 2 ASA 5 American Society of Anesthesiology risk class; BMI 5 body mass index; NS 5 not significant.

Pathological characteristics

1 2 3

2

The pathological characteristics are presented in Table 3. Pathological analysis was performed by a pathologist specialized in our institution. The clinicopathological factors affecting the recurrence are the presence of lymph node metastasis, depth of invasion, and tumor size.13 According to the 7th International Union Against Cancer classification of gastric cancer,14 our data presented no significant differences in tumor node metastasis (TNM) stages, extent of tumor invasion, and nodal status (P , .05). In the LAG group, 23, 42, and 22 patients were T2, T3, and T4a depth of invasion, respectively. In the OG group, 25, 39, and 23 patients were T2, T3, and T4a depth of invasion, respectively. In total, almost one fourth of all patients were T4a depth of invasion. The median tumor size was 4.4 cm (range, 2.0 to 13.5 cm) for the LAG group and 4.8 cm (range, 1.0 to 10.2 cm) for the OG group. The median number of resected lymph nodes following D2 dissection for LAG was 32 (range, 8 to 65) compared with 36 (range, 12 to 72) for OG (P , .05). The number of patients with positive lymph node metastasis did not differ significantly between the laparoscopy group (49 patients) and the open group (55 patients). No significant difference was shown in tumor differentiation. No positive resection margin was obtained in either group.

2 1

Follow-up results

6 0

5 0

and 41 patients underwent a total gastrectomy both in the LAG group and the OG group. The median operative time for laparoscopic procedure was 337 min (range, 240 to 650 min) compared with 224 min (range, 145 to 500 min) for open procedure. The median blood loss was Table 2 Surgical outcomes of laparoscopy-assisted and open gastrectomy Laparoscopic (n 5 87) Operative procedure Distal Total Operating time (min) Blood loss (mL) Use of analgesic drugs (d) Postoperative stay (d) Early complications TOSGS 1 TOSGS 2 TOSGS 3 TOSGS 4 TOSGS 5 Total Late complications

less after laparoscopy surgery (220 mL; range, 50 to 400 mL) than that after open surgery (310 mL; range, 100 to 600 mL), which presented the advantage of laparoscopic surgery. The use of analgesic drugs was significantly less after LAG, and the length of postoperative stay in the 2 groups was 12 days (range, 5 to 36 days) and 18 days (range, 7 to 45 days), respectively. In this study, postoperative complications occurred in 6 LAG patients and 5 OG patients. In the laparoscopic group, 1 patient (incision infection) experienced TOSGS grade 1, 2 patients (lung infection) experienced grade 2, 3 patients (1 lung infection needed closed drainage of pleural cavity and 2 duodenal stump leakage) experienced grade 3; in the open group, 2 patients (incision infection) experienced TOSGS grade 1, 2 patients (1 intestinal obstruction and 1 wound dehiscence) experienced grade 3, and 1 patient (heart dysfunction with intensive care unit stay) experienced grade 4. No inhospital mortality was observed. Similarly, there were no late complications identified in either group.

Open (n 5 87)

P value

NS 46 46 41 41 337 (240–650) 224 (145–500) ,.01 220 (50–400) 3 (0–5)

310 (100–600) ,.05 4 (1–6) ,.01

12 (5–36)

18 (7–45)

,.01 NS

NS 5 not significant; TOSGS 5 therapy-oriented severity grading system (grade 1: no need for speciflc intervention; grade 2: need for drug therapy such as antibiotics; grade 3: need for invasive therapy; grade 4: organ dysfunction with intensive care unit stay; grade 5: death).

After a median follow-up period of 44 months (range, 1 to 82 months), the 5-year cumulative overall survival rate in the laparoscopic group was 59%, compared to 54% in the open group. The overall survival analysis shown in Fig. 1A indicated no significant difference in the overall survival rate between the 2 groups (P 5 .525). As shown in Fig. 1B, the recurrence-free survival rate was 59% in the LAG group

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4 Table 3 Pathological characteristics of laparoscopy-assisted and open gastrectomy

Differentiation Well Well–Moderately Moderately Moderately–Poorly Poorly Depth of invasion pT2 pT3 pT4a Nodal category pN0 pN1 pN2 pN3 Stage IB IIA IIB IIIA IIIB IIIC Tumor size (range, cm) No. resected lymph nodes (range) Positive lymph node metastasis Positive resection margin

Laparoscopic (n 5 87)

Open (n 5 87)

17 10 13 20 27

12 10 22 13 30

23 42 22

25 39 23

38 21 17 11

32 23 22 10

19 15 23 14 8 8 4.4 (2.0–13.5)

NS 19 14 15 24 9 6 4.8 (1.0–10.2) NS

32 (8–65)

36 (12–72)

NS

49

55

NS

0

0

P value NS

NS

NS

of the technical difficulty in extraperigastric lymphadenectomy and the sparse data available on the procedure’s oncologic adequacy. Although the application of laparoscopic surgery for AGC is still debated, from 2000 to 2012, many reports have indicated similar long-term results between LAG and OG. Lee and Kim2 showed acceptable long-term outcomes of 106 patients with gastric cancer who underwent LAG with D2 lymphadenectomy between January 2004 and February 2009. Recently, the studies in Japan3 and Korea4 have reported that LAG with D2 lymph node dissection can provide an acceptable prognosis and may be applicable for AGC treatment, involving a total of 186 LAG cases and 239 LAG cases, respectively. In this study, we compared long-term survival rate between the 2 groups with a median follow-up of 44 months. We demonstrated that there was no evidence that differences exist regarding 5-year survival for LAG group vs OG group and this is consistent with most published reports.

All comparisons were not significantly different. NS 5 not significant.

and 48% in the OG group, respectively, with no significant differences between the 2 groups (P 5 .205). Recurrences occurred in 36 patients in the LAG group compared to 45 patients in the OG group (Table 4), no significant differences in recurrence were observed of T stages.

Comments With the improvement in laparoscopic technology, LAG has gained great popularity. In Japan and Korea, it has become a standard therapy for early gastric cancer.15 Many reports16–19 have presented advantages of LAG over OG for early gastric cancer, such as less blood loss, less incisional pain, shorter hospital stay, and better postoperative pulmonary function. With regards to AGC, since Uyama et al20 reported laparoscopic total gastrectomy with distal pancreatosplenectomy and D2 lymphadenectomy for AGC in 1999, the attempt to perform LAG for AGC has increased rapidly. Nevertheless, LAG for AGC is not very common because

Figure 1 (A) Kaplan–Meier overall survival curves of the LAG group and the OG group. No significant difference was observed (P 5 .525). (B) Comparison of recurrence-free survival rate. There was no significant difference between the 2 groups (P 5 .205).

C. Fang et al. Table 4

A 5-year case–control study

5

Recurrence according to depth of invasion Recurrence

T-stage

LAG

OG

P value

T2 T3 T4a Total

2 20 14 36

4 25 16 45

NS NS NS

LAG 5 laparoscopy-assisted gastrectomy; NS 5 not significant; OG 5 open gastrectomy.

Complete lymph node dissection is a crucial element for curative surgical treatment for AGC. The Japanese Gastric Cancer Association has presented complete D2 lymphadenectomy including lymph node station numbers 1 to 12 as the standard therapy.21 OG with D2 lymph node resection is considered to be a standard surgical approach for AGC. However, whether LAG with D2 lymphadenectomy is safe and feasible remains uncertain. The most objective index of lymphadenectomy is the comparison of the number of lymph nodes obtained between LAG and OG groups. Many publications5,22–26 have reported similar number of lymph nodes resected in LAG and OG with D2 dissection for AGC and the long-term results were also acceptable. In our series, the median number of resected lymph nodes was comparable to those experienced programs,6,12 32 (range, 8 to 65) in the LAG group compared with 36 (range, 12 to 72) in the OG group (P . .05). The number of patients with positive lymph node metastasis was 49 (56%) in the LAG group, compared with 55 (63%) in the OG group (P . .05). All these data show no significant differences between the 2 groups, indicating that a satisfactory lymph node dissection can be performed by LAG. It is universally accepted that depth of tumor invasion is considered to relate to the differences in clinical stages, which may influence the prognosis. Hwang et al13 reported that depth of invasion can affect the recurrence-free survival rate independently via a multivariate analysis of diseasespecial survival. The majority of previous studies about LAG mainly included cases with T2 or T3 depth. There is a general concern that laparoscopic surgery for AGC with T4a depth of invasion (serosa involved) may be accompanied by an increased incidence of peritoneal seeding of malignant cells and port site recurrence. Nevertheless, several authors have reported oncologically equivalent resection for T4a tumor using the laparoscopic approach, compared to the open procedure.27,28 Song et al29 analyzed the recurrence pattern following LAG for gastric cancer via a multicenter retrospective study of 1,417 patients. They showed that 8 of 45 serosa involved patients (18%) had a peritoneal recurrence, which was equivalent to that of open surgery, indicating that LAG for AGC patients with serosa involved was acceptable. In our study, about one fourth of all patients were diagnosed to have T4a depth of invasion. Recurrence of T4a depth of invasion occurred in 14 of LAG patients, compared with 16 of the OG group, which appeared to be

not significantly different (P . .05). Recurrence-free survival rates were also similar in the 2 groups (P 5 .205). Although LAG has several advantages over open surgery, such as less surgical trauma, reduced blood loss, less postoperative pain, and earlier return to normal bowel function,6,15,30,31 the complications after LAG remain one of the major concerns for surgical results. Many studies have reported acceptable rates for postoperative complications after LAG despite longer operative time, which is thought to be related to the morbidity and the mortality. In the literature,3,5,25 the operative time was reported to be between 261 and 479 min for LAG, compared to a range from 167 to 384 min for OG. However, the rate of postoperative complications was comparative between LAG and OG. As to our data, we observed a longer operative time in the LAG group but this did not affect the surgical outcomes. The complication rate of all patients is 6% (11 in 174) – 6 cases in the LAG group and 5 cases in the OG group. All of these patients recovered from these complications by appropriate management. No patient died during hospitalization. Nevertheless, it should be noted that our study had several limitations. Above all, this is a nonrandomized controlled study from a single center. The findings of this study may be limited to the retrospective nature of the analysis. For this reason, we included all consecutive patients who met the inclusion criteria between April 2005 and October 2009 to avoid any selective bias. Furthermore, although characteristics (age, sex, BMI, ASA, TNM) were well balanced between the 2 groups, several potential confounding factors have not been considered, such as histological type and tumor location, which are not expected to have significant role clinically in influencing the results of this study. Moreover, even though this case–control study presented acceptable prognosis of LAG with D2 dissection for AGC, our results only indicated the correlation between surgical procedures and survival rate, but not the actual influence of LAG on long-time results. A randomized controlled trail is required to further confirm the results reported in this article. Although this study was a nonrandomized trial with small number of patients, the 5-year survival rate and recurrence of LAG were shown to be comparable with OG for AGC. In conclusion, we consider LAG to be a safe and feasible procedure for AGC. However, a larger scale prospective trial is necessary to confirm the oncological safety of LAG for the treatment of AGC.

Acknowledgment We thank Christopher L. Wolfgang, Associate Professor of Surgery in Cameron Division of Surgical Oncology at Johns Hopkins University School of Medicine, for his reading and editing of the manuscript.

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Comparison of long-term results between laparoscopy-assisted gastrectomy and open gastrectomy with D2 lymphadenectomy for advanced gastric cancer.

The aim of this study was to compare surgical outcomes and oncologic efficacy of laparoscopy-assisted gastrectomy (LAG) versus open gastrectomy (OG) f...
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