Abstract
Background: This study aimed to examine the effect of hospital volume on long-term outcomes of patients who underwent laparoscopic gastrectomy for clinical stage I gastric cancer. Patients and Methods: A total of 420 patients with clinical stage I gastric cancer who underwent laparoscopic gastrectomy at our university hospital (high-volume group) and affiliated hospitals (low-volume group) were included in this study. Overall survival (OS) and cause-specific survival (CSS) rates were analyzed. Results: No significant differences were observed in the number of lymph nodes retrieved (29.9 vs. 27.7, p=0.21) and CSS between the high- and low-volume groups (p=0.92), although the OS rate in the low-volume group was significantly less than that in the high-volume group (p=0.045). Conclusion: These results indicate no clinical impact of hospital volume on prognosis of patients who underwent laparoscopic gastrectomy for clinical stage I gastric cancer when performed by surgeons with sufficient experience in open gastrectomy.
Although the incidence of gastric cancer has remained constant, it is still the second most common cause of cancer-related death worldwide (1). Surgical treatments are regarded as the primary choice among various treatments. However, improvements in endoscopic and laparoscopic surgical devices have led to new treatment options for patients with gastric cancer. Stereotyped laparoscopic procedure established by pioneers and the development of innovative surgical devices have made it possible to safely introduce these new procedures (2-4).
A number of studies have reported favorable short-term results following laparoscopic gastrectomy (5, 6). Moreover, several recent reports have shown that laparoscopic gastrectomy provides not only with better early postoperative outcomes, but also with equivalent oncological outcomes (7-11).
The present study aimed to examine the effect of hospital volume on long-term outcomes of patients who underwent laparoscopic gastrectomy for clinical stage I gastric cancer in our group, and also to validate the appropriateness of the rapid spread of laparoscopic procedures for surgeons with sufficient experience in open gastrectomy.
Patients and Methods
Patients. Between 2002 and 2012, 420 patients with gastric cancer who underwent laparoscopic gastrectomy for adenocarcinoma at the Kyoto Prefectural University of Medicine Hospital and affiliated hospitals (provided in the Acknowledgements section) were included in this retrospective study. The annual average number of gastrectomies was over 100 at our university hospital, which was defined as the high-volume group. On the other hand, the average numbers of gastrectomy were less than 30 at most of the affiliated hospitals, which defined this as the low-volume group.
Preoperative clinical diagnoses of tumor invasion and metastasis were generally made based on the findings of endoscopy, ultrasound endoscopy, barium study, and computed tomography (CT). Indication for laparoscopic gastrectomy at our hospital was gastric cancer clinically-diagnosed as stage I (T1N0, T1N1, and T2N0). Written informed consent was obtained from all patients prior to surgery. Laparoscopic gastrectomy was performed or guided by two surgeons (DI and AH) at our hospital. After DI performed the procedure on 100 cases as an operating surgeon, laparoscopic gastrectomy was then performed in affiliated hospitals at their request, in which doctors who had performed open gastrectomy on at least 30 cases performed laparoscopic gastrectomy while DI guided the operation as an assistant. The macroscopic and microscopic classification of gastric cancer was based on the Japanese Classification of Gastric Carcinoma (12).
Surgical procedures. The type of gastrectomy was determined based on tumor location, and the degree of lymph node dissection was determined based on the tumor size and depth of invasion. Indication for laparoscopic proximal gastrectomy (LPG) was gastric cancer located in the upper third of the stomach, with a preoperative clinical stage of T1N0, for which the resection line was at least 5 cm apart from the gastric angle. Laparoscopic distal gastrectomy (LDG) was performed for gastric cancer located at the lower or middle third of the stomach, with a preoperative clinical stage I.Laparoscopic total gastrectomy (LTG) was performed for superficial spreading gastric cancer involving the upper third of the stomach or multiple gastric lesions.
Our surgical procedures have been described previously (13, 14). In brief, the greater omentum was divided with laparoscopic coagulating shears (LCS) (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH, USA). The right gastroepiploic vessels were clipped and divided. The greater omentum was then divided to the lower pole of the spleen with LCS, and the left gastroepiploic vessels were clipped and divided. After retracting the left lobe of the liver using a Snake Retractor (Stryker, San Jose, CA, USA), the right gastric vessels were clipped and divided. The gastro-pancreatic ligament was then lifted toward the ventral side with the assistant's right hand grasper, and the supra-pancreatic lymph nodes were dissected. The left gastric vein was then exposed and dissected. The left gastric artery was exposed from the left side, double clipped, and divided. Lymph nodes along the lesser curvature were finally dissected. The short gastric vessels and posterior gastric vessels were divided in LPG or LTG, and the regional lymph nodes (right and left cardial, along the short gastric arteries) were also dissected. Lymph node dissections were performed based on the Guidelines of the Japanese Gastric Cancer Association (15). The first choice of reconstruction in LDG was Billroth-I, and Roux-en Y reconstruction was performed if the remnant stomach was small. Esophago-gastrostomy and esophago-jejunostomy were performed intracorporeally in LPG and LTG, respectively.
Evaluation of long-term outcomes. Adjuvant chemotherapy using S-1, an oral fluoropyrimidine, was administered for one year to patients with stage II/III after 2007. Follow-up consisted of blood examinations, radiological examinations of the gastrointestinal tract, endoscopic procedures, CT, and ultrasonography. Blood chemistry and tumor markers [carcinoembryonic antigen (CEA) and carbohydrate antigen 19-9 (CA19-9)] were examined every three months for at least two years, and thereafter every six months for at least five years. Endoscopic and CT examinations were performed annually for at least five years.
Overall survival (OS) and cause-specific survival (CSS) rates were analyzed based on follow-up data as of July 2013. The OS and CSS were compared between the high- and low-volume groups. Statistical analysis. Survival rates were calculated by the Kaplan-Meier method, with the date of gastrectomy as the starting point. Only deaths from postoperative complications and gastric cancer recurrences were considered for the analysis of CSS, and patients who were alive or had died of a cause other than gastric cancer were defined as censored cases. Differences in survival were examined by the log-rank test. The significance of differences was accepted at p<0.05.
Results
Patient and tumor characteristics. The mean patient age was 65.5 years (range: 32 to 92 years), and the male:female ratio was 2.1:1. Of the 420 patients, 321 patients underwent LDG, 26 patients LPG, and 73 patients LTG. Nine patients were converted to open surgery because of uncontrollable hemorrhage in two patients, intraoperative identification of advanced-stage disease in six patients, and severe adhesion in one patient. Most patients underwent laparoscopy-assisted gastrectomy, in which resection and/or anastomosis were performed extra-corporeally through a small incision, as previously described (13). Concomitant resections of other organs were performed in 24 patients, and consisted of 17 cholecystectomies and seven colorectal resections for synchronous diseases.
Some patients had pathologically-advanced gastric cancer, in which the tumor invaded to or beyond the muscle layer. Details of the clinicopathological characteristics are summarized in Table I. The final stage was stage IA in 341 patients (81.3%), stage IB in 35 (8.3%), stageIIA in 19 (4.5%), stage IIB in 11 (2.6%), stage IIIA in five (1.2%), stage IIIB in five (1.2%), stage IIIC in one (0.2%), and stage IV in three patients (0.7%).
Postoperative outcomes. The most frequently reported complication was wound infection (12 patients; 2.9%), followed by anastomotic stenosis (six patients; 1.4%), and pancreatic fistula (two patients; 0.5%). No anastomotic leakage was encountered in this study, except for duodenal stump leakage in one patient. Anastomotic stenosis was more frequently found in LPG (three patients; 11.5%) than in LDG (one patient; 0.3%) and LTG (two patients; 2.7%). However, all patients were successfully treated with endoscopic balloon dilatation. Three patients, two patients due to pancreatic leakage and one patient due to duodenal stump leakage, were classified as more than grade 3 with the Clavien-Dindo classification. Two patients required reoperations, and one patient died from severe pneumonia following reoperation.
Long-term prognosis. The mean follow-up after surgery was 30 months (range 4-124 months). During the follow-up period, 13 deaths occurred, including eight without apparent findings of recurrence. Five patients in this laparoscopic gastrectomy study developed tumor recurrence. Recurrence patterns were peritoneal dissemination in two patients, para-aortic lymph node metastasis in two, and hematogenous metastasis in two (one patient developed both peritoneal and lymph node recurrence). The detailed clinicopathological data of recurrent cases are shown in Table II. The 5-year OS and CSS rates were 97.2% and 100.0% for stage IA, 92.9% and 92.9% for stage IB, 75.0% and 75.0% for stage IIA, and 100.0% and 100.0% for stage IIB, respectively (Figure 1).
Clinicopathological characteristics.
Clinicopathological characteristics of recurrent cases.
In comparison between the high- and low-volume groups, patients in the high-volume group were slightly older, with a higher ratio of males: females, and also had a greater number of histologically diffuse-type tumors than patients in the low-volume group. However, no significant differences were observed regarding the type of performed operation, the number of lymph nodes retrieved, or pathological T and N categories between the two groups. Regarding prognoses, CSS rates in the two groups were similar (p=0.92), whereas the OS rate in the low-volume group was significantly less than that in the high-volume group (p=0.045) (Figure 2).
Discussion
Many reports have already demonstrated favorable early postoperative outcomes following laparoscopic gastrectomy, such as better cosmesis, less intraoperative blood loss, the rapid return of bowel function, less postoperative fever and pain, and also a shorter hospital stay (5, 6). However, the Japanese Gastric Cancer Treatment Guidelines 2010 classified laparoscopic gastrectomy as an investigational treatment because of a lack of definitive long-term survival results (15).
Survival curves for patients with gastric cancer who underwent laparoscopic gastrectomy. A: Overall survival. B: Cause-specific survival. Survival curves are not shown for patients with more than stage III disease due to the small number of patients.
Comparison of survival curves for patients who underwent laparoscopic gastrectomy between the high- and low-volume groups. A: Overall survival. B: Cause-specific survival. No significant difference was observed in the cause-specific survival rate between the two groups, whereas the overall survival rate in the low-volume group was significantly less than that in the high-volume group.
Nevertheless, laparoscopic gastrectomy has been spreading mainly rapidly for stage I gastric cancer worldwide. The present study aimed to investigate the long-term outcomes of laparoscopic gastrectomy for patients with clinical stage I gastric cancer in our group, and to examine the effect of hospital volume on the outcomes, and the appropriateness of the rapid spread of laparoscopic procedures for experienced open surgeons was evaluated.
In the early phase of developing this new therapeutic modality, laparoscopic procedures were considered to have definite disadvantages for precise lymph node dissections. However, development of pioneering equipment and the standardization of procedures has enabled for lymph node dissections to be safely and securely performed with laparoscopic gastric surgery (2-4). In fact, the mean number of lymph nodes retrieved was 29.4 in this study, which was not significantly different from that with open gastrectomy for stage I gastric cancer in our hospital (data not shown). This finding indicates that lymph node dissection performed laparoscopically-achieved equivalent results to open surgery. Previous reports also demonstrated that laparoscopic gastrectomy with lymph node dissection for early gastric cancer was safe and oncologically-equivalent to open gastrectomy. However, only a limited number of surgeons performed laparoscopic surgeries in these reports (7-11, 16). In this study, we also examined the quality of lymph node dissection between the high- and low-volume centers. Our university hospital is a high-volume academic center, and laparoscopic gastrectomy was introduced after DI learned the procedures at an advanced specialized hospital. On the other hand, most affiliated hospitals are low-volume centers, and it was difficult to introduce the new procedure in the same manner due to the small number of surgical staff members. Therefore, the surgeons of the affiliated hospitals applied a different approach to introducing the new procedures, which entailed understanding the details of the laparoscopic procedures and the assistants' roles in each scene through a in-house manual and full-length video of our standardized laparoscopic gastrectomy. After they fully-understood the procedure, the doctors in charge of patients performed laparoscopic gastrectomy at the affiliated hospitals under the mentorship of DI. Our present findings show no significant difference in the number of lymph nodes retrieved between the high- and low-volume groups, which indicates that adequate lymph node dissection was performed by doctors at the low-volume hospitals.
Regarding the prognosis of patients, survival rates in this study were similar to those in an open surgery-group reported previously (17). The pattern of recurrence was not significantly different from that of conventional open gastrectomy (17), and there was no incidence of port-site recurrence in this study. The laparoscopic group included only cases that were diagnosed preoperatively with stage I disease, which may have had an effect on survival differences. Therefore further studies are needed to evaluate the exact survival effect of laparoscopic approach for patients with advanced gastric cancer. Regarding the effect of hospital volume on prognosis, the OS rate of the low-volume group was significantly less than that of the high-volume group. The reason for this remains unknown; however, the significantly higher age and proportion of males in the low-volume group may have had a negative effect on the overall survival rate. All four patients who died from other diseases unrelated to gastric cancer in the low-volume group were male, of whom three were more than 78 years old (78, 80, and 80 years old), and the CSS rate in the low-volume group was similar to that in the high volume group.
Conclusion
These findings indicate that laparoscopic gastrectomy with lymph node dissection is a safe and oncologically-feasible procedure, at least for clinical stage I gastric cancer, and there is no impact of hospital volume on the prognosis when performed by surgeons with sufficient experience in open gastrectomy.
Acknowledgements
We would like to thank all our colleagues for giving us the opportunity to teach laparoscopic gastrectomy procedures. Our colleagues were the following: Kyoto Kizugawa Hospital: Drs. T Obayashi and K Deguchi, and T Daido; Midorigaoka Hospital: Drs. H Tamai and T Imanishi; Kyoto Kujo Hospital: Drs. K Suchi and K Kitagawa; Shirahama Hamayu Hospital: Dr. K Soga; Ayabe City Hospital: Drs. K Inoue; Rakusai Newtown Hospital: Drs. K Imura and N Yamaoka; Kyoto First Red Cross Hospital: Dr. Y Itokawa; Saiseikai Shiga Hospital: Drs. M Masuyama and K Fukuda, Kanai Hospital: Dr. K Taniguchi; Nishijin Hospital: Drs. K Fukumoto and T Miyagaki; Nantan Hospital: Drs. A Iwamoto and S Nishida; Nara City Hospital: Dr. H Nagata; Osaka JR Hospital: Dr. M Takemura; Panasonic Hospital: Dr. T Shimizu; Marutamachi Hospital: Dr. M Tokui; Horikawa Hospital: Dr. N Yamaoka; and Minase Hospital: Dr. H Minato.
Footnotes
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Conflicts of interest
None.
- Received September 22, 2013.
- Revision received October 17, 2013.
- Accepted October 18, 2013.
- Copyright© 2013 International Institute of Anticancer Research (Dr. John G. Delinassios), All rights reserved
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