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Asian J Endosc Surg ISSN 1758-5902
O R I G I N A L A RT I C L E
Triple-incision laparoscopic distal gastrectomy for the resection of gastric cancer: Comparison with conventional laparoscopy-assisted distal gastrectomy Shinsuke Usui, Masaki Tashiro, Shigeo Haruki & Akiyo Matsumoto Department of Surgery, Tsuchiura Kyodo General Hospital, Tsuchiura, Japan
Keywords LADG; laparoscopy-assisted distal gastrectomy; reduced port surgery Correspondence Shinsuke Usui, Department of Surgery, Tsuchiura Kyodo General Hospital, Manabe-shin-machi 11-7, Tsuchiura, Ibaragi 300-0053, Japan. Tel: +81 29 823 3111 Fax: +81 29 823 1160 Email: [email protected] Received: 15 October 2013; revised 21 February 2014; accepted 16 March 2014 DOI:10.1111/ases.12109
Abstract Introduction: Reduced port surgery and single-port surgery are currently in the spotlight as next-generation, minimally invasive surgical techniques. We performed a triple-incision laparoscopic distal gastrectomy (TIL-DG) for gastric cancer as a reduced port surgery. Method: A total of 76 patients underwent a TIL-DG. A D1+ or D2 lymph node dissection was performed, and the Roux-en-Y method was used for reconstruction. The short-term patient outcomes of the TIL-DG group were compared with those of the conventional laparoscopy-assisted distal gastrectomy group (59 cases) to evaluate the feasibility of TIL-DG. Results: No significant differences were observed between the TIL-DG group and the laparoscopy-assisted distal gastrectomy group in terms of mean operative time, blood loss, and the length of the postoperative hospital stay. The mean number of retrieved regional lymph nodes in the TIL-DG group was slightly higher than that in the laparoscopy-assisted distal gastrectomy group. Conclusion: A triple-incision laparoscopic distal gastrectomy is a feasible and safe procedure.
Introduction Since laparoscopy-assisted distal gastrectomy (LADG) for early gastric cancer was first introduced by Kitano et al. in 1994 (1), LADG has spread widely throughout Japan, and many reports regarding laparoscopic gastrectomy for gastric cancer have been published. Initially, LADG required a 5–7-cm mini-laparotomy at the epigastrium for reconstruction after the gastrectomy. Recently, several techniques for intracorporeal anastomosis have been developed for reconstruction using the Billroth I–II method and the Roux-en-Y method (2,3). Consequently, the required size of the mini-laparotomy has been reduced, thereby minimizing the invasiveness of the procedure and improving cosmesis. More recently, reduced port surgery (RPS) and single-port surgery (SPS) have been in the spotlight as next-generation, minimally invasive surgical techniques. Cholecystectomy and appendectomy have been the most prevalent applications of the SPS technique (4,5). RPS and SPS for LADG have also been described in several publications (6). However, the
techniques required to perform a conventional LADG are complex and difficult to perform using a reduced port gastrectomy because of interference between the forceps and the laparoscope. RPS or SPS for gastric cancer should be a safe and reliable procedure, and the oncological safety should also be guaranteed. Accordingly, we introduced a triple-incision laparoscopic distal gastrectomy (TIL-DG) as a reduced port surgery; this procedure combines the techniques used for single-incision laparoscopic surgery with the techniques used for a conventional laparoscopic distal gastrectomy. To assess the feasibility of this new approach, the outcomes of TIL-DG were compared with those of conventional LADG.
Materials and Methods Patients Between April 2010 and December 2012, 76 patients (47 men and 29 women) underwent a TIL-DG. Based on preoperative evaluations including barium radiography,
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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tied with a 2-0 polypropylene straight needle line, were inserted into the abdominal cavity through the trocar, and the straight needle was forced out the abdominal wall. The hanging forceps were suspended from the abdominal wall by a thread (Figure 2a). After the tissue was grasped, the thread was pulled and clamped. An optimal surgical field was thus created by adjusting the grasping point for the hanging forceps and by adjusting the force of traction on the thread (Figure 2b).
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Operative technique for TIL-DG
Figure 1 (a) The newly developed Minimini trocar sleeve (MMT) is a reusable 5-mm trocar. (b) A multichannel trocar was set up by attaching a conventional 12-mm trocar and a MMT to a path saver. A hole was made in the cap, and then the MMT was inserted into the hole. A conventional 12-mm trocar was inserted into the ready-made hole.
an upper gastrointestinal endoscopy, and CT, all the patients were diagnosed as having gastric cancer (cT1-T3, cN0-1, cStage I–II) according to the Japanese Classification of Gastric Carcinoma (7). In all the patients, the cancer was located in the lower third or middle third of the stomach. Informed consent was obtained from each patient before TIL-DG was performed. To assess the oncologic safety and feasibility of TIL-DG, 59 patients who had undergone conventional LADG between May 2008 and January 2010 were retrospectively selected. All TIL-DG and LADG procedures were performed by a single surgeon who had previous experience performing more than 300 laparoscopic gastrectomy procedures. Materials A new trocar, the Minimini trocar sleeve, was used for the TIL-DG. The Minimini trocar sleeve is a 5-mm reusable trocar that was developed in cooperation with Hope Electronics (Kamagaya, Japan) for single-incision and reduced port surgery (Figure 1a). A multichannel trocar was set up by attaching one Minimini trocar sleeve and a 12-mm trocar to a path saver (Sumitomo Bakelite Co Ltd, Tokyo, Japan) for performing the TIL-DG (Figure 1b). Assistant forceps, also known as hanging forceps, were used to create the surgical field during the TIL-DG procedure. These forceps are based on the ready-made detachable forceps (B Braun Aesculap, Tuttingen, Germany) that are used to close blood vessels during laparoscopic surgery. The hanging forceps, which were
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After the induction of general anesthesia, the patient was placed in Fowler’s position with his or her legs apart. Initially, a 3-cm incision was made at the umbilicus, and a multichannel port was attached to the wound. Thereafter, pneumoperitoneum was established, and the remaining two ports were put in place: a 5-mm right subcostal port and a 5-mm right mid-abdominal port (Figure 3a). The operator performed all the procedures from the right side of the patient using two 5-mm trocars. The assistant operator stood between the patient’s legs and manipulated a 5-mm flexible scope and rigid forceps through a multichannel port located at the umbilicus (Figure 3b). Finally, the hanging forceps were suspended from the mid-upper abdominal wall. To elevate the liver, a suture was placed around the right crus of the diaphragm and the falciform ligament, and the suture was then pulled out of the abdomen and tied. The greater omentum was dissected toward the splenic flexure with a Harmonic scalpel (Ethicon Endo-Surgery, Cincinnati, USA), and the left gastroepiploic vessels were exposed and divided with a clip and the Harmonic scalpel. The lymph nodes along the left gastroepiploic vessels (no. 4Sb) were dissected. Then, the same plane of the greater omentum was dissected toward the hepatic flexure. The pedicle of the right gastroepiploic vessels was hung using the hanging forceps (Figure 4a), the right gastroepiploic vessels were exposed, and the infrapyloric lymph nodes (no. 6) were dissected. In cases requiring a D2 lymph node dissection, the lymph nodes around the superior mesenteric vein (no. 14v) were also dissected (Figure 4b). A 45-mm endoscopic linear stapler (ETS45; Ethicon Endo-Surgery) was inserted into the abdominal cavity through the multichannel port, and the duodenum was transected. In this situation, the laparoscope was inserted into the abdominal cavity through the 5-mm right midabdominal port. After the duodenum was transected, the proper hepatic artery was identified, and the right gastric artery was divided with a clip and the Harmonic scalpel at its origin. The suprapyloric lymph nodes (no. 5) were then dissected.
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Figure 2 (a) The hanging forceps was suspended from the abdominal wall using a thread. (b) After the tissue was grasped, the thread was pulled and clamped. In this manner, the organ was hung from the abdominal wall.
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5mm 5mm Multi channel port Figure 3 (a) Trocar placement for a triple-incision laparoscopic distal gastrectomy. (b) The operator stood on the right side of the patient and used two 5-mm trocars. The assistant stands between the patient’s legs and manipulates a 5-mm flexible scope and a rigid forceps through a multichannel port.
a
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GDA ASPDV
RGEA
GCT SMV
The pedicle of the left gastric vessels was hung using the hanging forceps (Figure 5a), and the lymph nodes along the common hepatic artery (no. 8a) and the celiac artery (no. 9) were dissected using the Harmonic scalpel. The left gastric vessels were divided at their origins with a clip and the Harmonic scalpel. In cases requiring a D2 lymph node dissection, the lymph nodes along the proper hepatic artery (no. 12a) and the splenic artery (no. 11p) were also dissected (Figure 5b). For the no. 12a and the
Figure 4 (a) The hanging forceps was attached to the pedicle of the right gastroepiploic vessels. (b) Dissection of no. 6 and 14v lymph nodes was completed. ASPDV, anterior superior pancreoduodenal vein; GCT, gastrocolic trunk; GDA, gastroduodenal artery; RGEA, right gastroepiploic artery; SMV, superior mesenteric vein.
no. 11p lymph node dissections, the portal vein and the splenic vein were identified as a landmark of the dorsal plane. The lymph nodes along the lesser curvature (nos. 1 and 3) were also dissected. The distal two-thirds of the stomach were intracorporeally dissected using a 60-mm endoscopic linear stapler (Echelon; Ethicon Endo Surgery), which was inserted into the abdominal cavity through the
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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CHA PV
SV
Figure 5 (a) The hanging forceps was attached to the pedicle of the left gastric vessels. (b) A D2 lymph node dissection (no. 8a, 9, 11p, and 12a) was completed. CHA, common hepatic artery; PV, portal vein; SA, splenic artery; SV, splenic vein.
SA
5mm
12mm
5mm
12mm 12mm
Figure 7 Trocar placement in a conventional laparoscopy-assisted distal gastrectomy. In cases requiring an intracorporeal gastroenteral anastomosis, a 4–5-cm mini-laparotomy was made below the xiphoid process. Figure 6 Reconstruction was performed using the Roux-en-Y method in all the triple-incision laparoscopic distal gastrectomy cases.
multichannel port. To confirm the transection line, an intraoperative endoscopy examination was also performed. The dissected stomach was pulled out through the mini-laparotomy at the umbilical incision. Reconstruction was performed using the Roux-en-Y method (Figure 6). The jejunum was intracorporeally transected at a point 30 cm distal to the ligament of Treitz with an ETS45 endoscopic linear stapler. The Y-limb anastomosis was performed under direct vision through the mini-laparotomy at the umbilicus. The gastrojejuno anastomosis was performed intracorporeally using a 45-mm endoscopic linear stapler (ETS45). The common entry hole of the endoscopic linear stapler was closed using hand suturing.
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Operative technique for conventional LADG In the conventional LADG group, five ports were used: two bilateral subcostal ports, two bilateral mid-abdominal ports, and an umbilical port (Figure 7). The method used for the lymph node dissection was the same as that used for the TIL-DG. Reconstruction was performed using an extracorporeal Billroth-I method or the Roux-en-Y method, including an intracorporeal gastrojejunotomy or an extracorporeal gastrojejunostomy. In cases requiring an extracorporeal gastroduodenal anastomosis and an extracorporeal gastrojejunal anastomosis, a 4–5-cm minilaparotomy was performed below the xiphoid process. Clinical pathway In both the TIL-DG group and LADG group, the same clinical pathway was implemented for postoperative care.
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Figure 8 (a) Appearance of the wound 14 days after triple-incision laparoscopic distal gastrectomy. (b) Appearance of the wound 14 days after conventional laparoscopy-assisted distal gastrectomy.
Table 1 Patient and treatment characteristics
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2) Reconstruction Billroth I Roux-en-Y (extracorporeal) Roux-en-Y (intracorporeal)
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2)
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2)
TIL-DG group (n = 76)
LADG group (n = 59)
P-value
47/29 66.8 ± 10.3 22.1 ± 2.9
34/25 65.1 ± 13.1 22.3 ± 2.6
0.61 0.79 0.29
0 0 76
24 23 12
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
23/10 69.4 ± 9.8 21.4 ± 2.4
17/18 70.1 ± 10.3 22.8 ± 2.5
0.91 0.38 0.02 (P < 0.05)
TIL-DG (D2) group (n = 33)
LADG (D2) group (n = 35)
P-value
24/19 64.8 ± 10.3 22.6 ± 3.1
17/7 57.8 ± 13.4 21.7 ± 2.8
0.22 0.98 0.23
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
The nasogastric tube was removed soon after the operation. Clear liquids were restarted on postoperative day (POD) 1, and a liquid diet was restarted on POD 2. Nonsteroidal anti-inflammatory drugs were routinely administered on POD 1, and epidural catheters were routinely removed on POD 4. The peripheral intravenous drip was ended on POD 5, and the patients were discharged on POD 7 or POD 8. Figure 8a shows the wound 14 days after a TIL-DG. Figure 8 shows the wound 14 days after a conventional LADG. Statistical analysis All the data were analyzed using Statcel3 (the Useful Add-in Forms on Excel, 3rd ed.) for Windows (Tokorozawa, Japan). The χ2 test or the Fisher’s exact test was used to compare the patient characteristics and the postoperative outcome between the treatment groups. Continuous variables were compared using the Student’s
t-test and were expressed as the mean ± SD. P-values less than 0.05 were considered statistically significant.
Results The patient characteristics of the TIL-DG group and the LADG group are shown in Table 1. The mean age, sex, and BMI of the patients were similar between the two groups. The BMI in the TIL-DG (D1+) group was slightly less than that in the LADG (D1+) group. The types of reconstruction are also listed in Table 1. In the TIL-DG group, a Roux-en-Y reconstruction with an intracorporeal gastrojejunostomy was performed in all the cases. In the LADG group, a Roux-en-Y reconstruction with an intracorporeal gastrojejunostomy was performed in 12 cases. In the remaining 47 LADG cases (79.6%), either a Billroth I reconstruction via a 4–5-cm epigastric mini-laparotomy or a Roux-en-Y reconstruction with an extracorporeal gastrojejunostomy via a 4–5-cm epigastric mini-laparotomy was performed.
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Table 2 Short-term clinical outcomes
Operation time, mean ± SD (min) Blood loss, mean ± SD (mL) Number of dissected lymph nodes, mean ± SD (n) Postoperative hospital stay, mean ± SD (days) Intraoperative complication (n) Postoperative complication (n)
Operation time, mean ± SD (min) Blood loss, mean ± SD (mL) Number of dissected lymph nodes, mean ± SD (n) Postoperative hospital stay, mean ± SD (days) Intraoperative complication (n) Postoperative complication (n)
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
247.8 ± 54.9 48.8 ± 56.7 35.3 ± 12.1 7.5 ± 1.6 0 1 (pseudomonas colitis)
240.7 ± 62.1 70.0 ± 60.5 22.9 ± 13.3 8.7 ± 4.0 0 1 (pancreatic fistula)
0.62 0.14 0.00016(P < 0.05) 0.10
TIL-DG (D2) group (n = 43)
LADG (D2) group (n = 24)
P-value
268.9 ± 48.1 52.0 ± 80.2 43.9 ± 14.2 7.3 ± 1.3 0 1 (pancreatitis)
262.3 ± 52.6 61.5 ± 67.1 31.6 ± 12.5 8.0 ± 3.0 0 1 (anastomotic bleeding)
0.60 0.63 0.00071(P < 0.05) 0.21
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
The short-term outcomes of both groups are shown in Table 2. The TIL-DG group and the LADG group were each classified into two subgroups according to the level of the lymph node dissection (D1+ and D2). No significant differences in operation time, volume of blood loss, or postoperative hospital stay were observed between the two groups. The number of retrieved lymph nodes in the TIL-DG (D1+) group was higher than that in the LADG (D1+) group, and the number of retrieved lymph nodes in the TIL-DG (D2) group was also higher than that in the LADG (D2) group. No cases of intraoperative complications or conversion to open surgery occurred in either group. Postoperative complications occurred in two cases in the TIL-DG group (2.6%) and in two cases in the LADG group (3.4%). The complications in the TIL-DG group consisted of one case with pancreatitis and one case with pseudomembranous colitis. The patient with pancreatitis was treated conservatively and was discharged on POD 11. The patient with pseudomembranous colitis was also treated conservatively and was discharged on POD 14. The complications in the LADG group consisted of one case of pancreatic fistula and one case of anastomotic bleeding. The pancreatic fistula was diagnosed as Grade A according to the criteria of the International Study Group of Postoperative Pancreatic Fistula, and the patient was treated conservatively and was discharged on POD 13. The anastomotic bleeding occurred in a case that underwent Billroth I reconstruction using a circular stapler. The bleeding was stopped conservatively without requiring endoscopic clipping, and the patient was discharged on POD 21. The histopathological findings are listed in Table 3. No significant difference in the histological type, pT, pN, or pStage was seen between the treatment groups.
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The operation times for the consecutive TIL-DG cases are shown in Figure 9. A comparison of the mean operative time of the first five cases and the last five cases is also shown in Table 4. No significant differences in the mean operation times of the first five cases and the last five cases were observed when the patients were compared according to the D1+ and D2 lymphadenectomy subgroups.
Discussion The use of LADG has spread widely throughout Japan and other Asian nations since Kitano et al. first reported its application for early gastric cancer in 1994. In recent years, laparoscopic total gastrectomy and laparoscopic proximal gastrectomy for the upper third of the stomach have been performed at many medical institutions (8–11), and the long-term outcomes of laparoscopic gastrectomy for advanced gastric cancer have been reported in several studies (12,13). In contrast, SPS and RPS for gastroenterological surgery are presently in the spotlight as next-generation laparoscopic surgical techniques. The number of reports on the use of SPS for cholecystectomy or appendectomy has increased rapidly, and SPS for gastric cancer has also been recently reported in several studies. In many reports, SPS has been reported to offer an advantage over conventional laparoscopic surgery with regard to cosmesis. However, no reports have confirmed the minimal invasiveness of SPS compared with conventional laparoscopic surgery. SPS for gastrectomy requires a higher level of expertise than a conventional laparoscopic gastrectomy because of the complexity of the associated lymph node dissection and intracorporeal anastomosis. Generally, the operator manipulates the trocar through a multichannel port
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Table 3 Histopathological findings of the resected specimens
Location (L/M) Histological Type Differenciated Undifferenciated pT (1/2/3/4a) pN (0/1/2/3) pStage (1A/1B/2A/2B/3A)
Location (L/M) Histological type Differenciated Undifferenciated pT (1/2/3/4a) pN (0/1/2/3) pStage (1A/1B/2A/2B/3A/3B/3C)
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
13/20
12/23
0.66
22 11 27/3/3/0 29/2/1/1 26/3/1/1/2
18 17 34/0/1/0 29/6/0/0 30/4/0/1/0
0.09 0.26 0.50
TIL-DG (D2) group (n = 43)
LADG (D2) group (n = 24)
P-value
17/26
16/8
0.03
20 23 31/4/3/5 30/9/2/2 24/8/4/4/1/2
10 14 17/5/2/0 15/7/2/0 13/6/2/2/1/0
0.23 0.56 0.89
L, lower third of the stomach ; LADG, laparoscopy-assisted distal gastrectomy; M, middle third of the stomach; TIL-DG, triple-incision laparoscopic distal gastrectomy.
Figure 9 Operation times (min) for consecutive triple-incision laparoscopic distal gastrectomy (TIL-DG) cases.
during SPS and even in RPS. The complexity of the manipulation consequently arises from the conflict between the forceps and the laparoscope. The operator’s trocar, especially the operator’s dominant trocar, should be free for movement. In our procedure, the operator
manipulates the trocars located at the right subcostal and right mid-abdomen. This trocar placement is the same as in conventional LADG. The processes of lymph node dissection and reconstruction are also the same as in conventional LADG. The special instruments required for
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Table 4 Mean operation time of TIL-DG (first five cases vs last five cases) TIL-DG (D1+)
First five cases (n = 5)
Last five cases (n = 5)
P-value
Operation time, mean ± SD (min) TIL-DG (D2)
306.6 ± 51.3
278.0 ± 48.5
0.39
First five cases (n = 5)
Last five cases (n = 5)
Operation time, mean ± SD (min)
273.0 ± 68.3
285.6 ± 34.3
0.72
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
RPS and SPS, such as flexible forceps and multi-degree forceps, are not used to maintain triangulation and retraction of the organs. Instead, the assistant operator manipulates a forceps and a laparoscope through a multichannel port. Conflict between the forceps and the laparoscope is rare because the angle of approach to the target organ is different between the forceps and the 5-mm flexible laparoscope. Consequently, no significant differences in the mean operation time or the volume of blood loss were observed between the TIL-DG group and a conventional LADG group. As shown in Figure 3 and Table 4, no learning curve for the performance of a TIL-DG was observed, and there was no significant difference in the mean operation time between the first five and the last five cases that underwent TIL-DG. In the present study, all the operations were performed by one expert surgeon who had previously performed more than 300 laparoscopic gastrectomies. Similar results can be expected when other expert surgeons with experience performing LADG attempt to perform TIL-DG. However, the results would likely differ for beginner operators and trainees. Because the operator’s role is larger in a TIL-DG procedure than in an LADG procedure, the operator should take the initiative in the progress of the operation, similar to a solo surgery. In the present study, the average number of retrieved lymph nodes in the TIL-DG group was higher than that in the conventional LADG group. However, the period required to perform TIL-DG differed from that required to perform LADG. The data for the TIL-DG group were newer than for the LADG group by about 2 years. In recent years, high-definition laparoscope systems have undergone remarkable advances. Advancements in knowledge of microscopic anatomy, which have been facilitated by the images from these systems, have also been remarkable. As a result, laparoscopic techniques for lymph node dissection have improved and the number of retrieved lymph nodes has increased. Although there were no significant differences in the histopathological findings between the TIL-DG group and the LADG group, the pT, pN, and pStage were slightly higher in the TIL-DG group than in the LADG group. Consequently, these differences could have influenced the difference in the
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number of retrieved lymph nodes. At the least, the TIL-DG procedure is not inferior to conventional LADG with regard to oncological safety. Nevertheless, further randomized controlled trials comparing TIL-DG with LADG should be conducted to obtain accurate evidence regarding the oncological outcomes of TIL-DG. At present, several kinds of thin forceps with a diameter of 2–3 mm, such as the MiniLap (Stryker, Kalamazoo, USA) and the BJneedle (Nichion, Funabashi, Japan), have been developed. With these forceps and a thin trocar, a conventional LADG could obtain better cosmesis. Additionally, the advantages of TIL-DG include the efficient utilization of surgical staff. In conventional LADG, the procedure is conducted by three surgical staff members consisting of an operator, an assistant operator, and a laparoscopist. In TIL-DG, the procedure is conducted by only two surgical staff members, an operator and an assistant operator. Reducing the number of surgical staff required leads to cost savings for the operation. Generally, the assistant operator manipulates two forceps to create the surgical field in conventional LADG. In TIL-DG, the assistant operator manipulates only one pair of forceps. Accordingly, the shortage of forceps is compensated for by the use of assistant forceps, or hanging forceps. The method of towing internal organs, such as the gallbladder or liver, using threads has been described as a “marionette trick.” (14–16) Our method of using the hanging forceps is a modification of the marionette trick, and the hanging forceps have the advantage that the traction point can be easily changed by altering the grasping point. Throughout all the steps of the TILDG, the hanging forceps were only required twice: for the no. 6 lymph node dissection and for the no. 8a and no. 9 lymph node dissection. The other steps could be completed without using the hanging forceps. Thus, the creation of the surgical field throughout the entire TIL-DG was not complicated. The TIL-DG has superior cosmesis compared with a conventional LADG, and this technique has the potential to become a technically and oncologically accepted alternative to LADG. However, the indications for conventional LADG for advanced gastric cancer remain controversial, as do the safety and feasibility of reduced port surgery (or single-incision surgery) for gastric
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cancer. Further examination is required to evaluate the benefits of TIL-DG.
Acknowledgments The authors have no conflict of interest to report. The authors wish to thank Shigeyuki Sakaguchi for preparing the schema.
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Asian J Endosc Surg ISSN 1758-5902
O R I G I N A L A RT I C L E
Triple-incision laparoscopic distal gastrectomy for the resection of gastric cancer: Comparison with conventional laparoscopy-assisted distal gastrectomy Shinsuke Usui, Masaki Tashiro, Shigeo Haruki & Akiyo Matsumoto Department of Surgery, Tsuchiura Kyodo General Hospital, Tsuchiura, Japan
Keywords LADG; laparoscopy-assisted distal gastrectomy; reduced port surgery Correspondence Shinsuke Usui, Department of Surgery, Tsuchiura Kyodo General Hospital, Manabe-shin-machi 11-7, Tsuchiura, Ibaragi 300-0053, Japan. Tel: +81 29 823 3111 Fax: +81 29 823 1160 Email: [email protected] Received: 15 October 2013; revised 21 February 2014; accepted 16 March 2014 DOI:10.1111/ases.12109
Abstract Introduction: Reduced port surgery and single-port surgery are currently in the spotlight as next-generation, minimally invasive surgical techniques. We performed a triple-incision laparoscopic distal gastrectomy (TIL-DG) for gastric cancer as a reduced port surgery. Method: A total of 76 patients underwent a TIL-DG. A D1+ or D2 lymph node dissection was performed, and the Roux-en-Y method was used for reconstruction. The short-term patient outcomes of the TIL-DG group were compared with those of the conventional laparoscopy-assisted distal gastrectomy group (59 cases) to evaluate the feasibility of TIL-DG. Results: No significant differences were observed between the TIL-DG group and the laparoscopy-assisted distal gastrectomy group in terms of mean operative time, blood loss, and the length of the postoperative hospital stay. The mean number of retrieved regional lymph nodes in the TIL-DG group was slightly higher than that in the laparoscopy-assisted distal gastrectomy group. Conclusion: A triple-incision laparoscopic distal gastrectomy is a feasible and safe procedure.
Introduction Since laparoscopy-assisted distal gastrectomy (LADG) for early gastric cancer was first introduced by Kitano et al. in 1994 (1), LADG has spread widely throughout Japan, and many reports regarding laparoscopic gastrectomy for gastric cancer have been published. Initially, LADG required a 5–7-cm mini-laparotomy at the epigastrium for reconstruction after the gastrectomy. Recently, several techniques for intracorporeal anastomosis have been developed for reconstruction using the Billroth I–II method and the Roux-en-Y method (2,3). Consequently, the required size of the mini-laparotomy has been reduced, thereby minimizing the invasiveness of the procedure and improving cosmesis. More recently, reduced port surgery (RPS) and single-port surgery (SPS) have been in the spotlight as next-generation, minimally invasive surgical techniques. Cholecystectomy and appendectomy have been the most prevalent applications of the SPS technique (4,5). RPS and SPS for LADG have also been described in several publications (6). However, the
techniques required to perform a conventional LADG are complex and difficult to perform using a reduced port gastrectomy because of interference between the forceps and the laparoscope. RPS or SPS for gastric cancer should be a safe and reliable procedure, and the oncological safety should also be guaranteed. Accordingly, we introduced a triple-incision laparoscopic distal gastrectomy (TIL-DG) as a reduced port surgery; this procedure combines the techniques used for single-incision laparoscopic surgery with the techniques used for a conventional laparoscopic distal gastrectomy. To assess the feasibility of this new approach, the outcomes of TIL-DG were compared with those of conventional LADG.
Materials and Methods Patients Between April 2010 and December 2012, 76 patients (47 men and 29 women) underwent a TIL-DG. Based on preoperative evaluations including barium radiography,
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tied with a 2-0 polypropylene straight needle line, were inserted into the abdominal cavity through the trocar, and the straight needle was forced out the abdominal wall. The hanging forceps were suspended from the abdominal wall by a thread (Figure 2a). After the tissue was grasped, the thread was pulled and clamped. An optimal surgical field was thus created by adjusting the grasping point for the hanging forceps and by adjusting the force of traction on the thread (Figure 2b).
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Operative technique for TIL-DG
Figure 1 (a) The newly developed Minimini trocar sleeve (MMT) is a reusable 5-mm trocar. (b) A multichannel trocar was set up by attaching a conventional 12-mm trocar and a MMT to a path saver. A hole was made in the cap, and then the MMT was inserted into the hole. A conventional 12-mm trocar was inserted into the ready-made hole.
an upper gastrointestinal endoscopy, and CT, all the patients were diagnosed as having gastric cancer (cT1-T3, cN0-1, cStage I–II) according to the Japanese Classification of Gastric Carcinoma (7). In all the patients, the cancer was located in the lower third or middle third of the stomach. Informed consent was obtained from each patient before TIL-DG was performed. To assess the oncologic safety and feasibility of TIL-DG, 59 patients who had undergone conventional LADG between May 2008 and January 2010 were retrospectively selected. All TIL-DG and LADG procedures were performed by a single surgeon who had previous experience performing more than 300 laparoscopic gastrectomy procedures. Materials A new trocar, the Minimini trocar sleeve, was used for the TIL-DG. The Minimini trocar sleeve is a 5-mm reusable trocar that was developed in cooperation with Hope Electronics (Kamagaya, Japan) for single-incision and reduced port surgery (Figure 1a). A multichannel trocar was set up by attaching one Minimini trocar sleeve and a 12-mm trocar to a path saver (Sumitomo Bakelite Co Ltd, Tokyo, Japan) for performing the TIL-DG (Figure 1b). Assistant forceps, also known as hanging forceps, were used to create the surgical field during the TIL-DG procedure. These forceps are based on the ready-made detachable forceps (B Braun Aesculap, Tuttingen, Germany) that are used to close blood vessels during laparoscopic surgery. The hanging forceps, which were
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After the induction of general anesthesia, the patient was placed in Fowler’s position with his or her legs apart. Initially, a 3-cm incision was made at the umbilicus, and a multichannel port was attached to the wound. Thereafter, pneumoperitoneum was established, and the remaining two ports were put in place: a 5-mm right subcostal port and a 5-mm right mid-abdominal port (Figure 3a). The operator performed all the procedures from the right side of the patient using two 5-mm trocars. The assistant operator stood between the patient’s legs and manipulated a 5-mm flexible scope and rigid forceps through a multichannel port located at the umbilicus (Figure 3b). Finally, the hanging forceps were suspended from the mid-upper abdominal wall. To elevate the liver, a suture was placed around the right crus of the diaphragm and the falciform ligament, and the suture was then pulled out of the abdomen and tied. The greater omentum was dissected toward the splenic flexure with a Harmonic scalpel (Ethicon Endo-Surgery, Cincinnati, USA), and the left gastroepiploic vessels were exposed and divided with a clip and the Harmonic scalpel. The lymph nodes along the left gastroepiploic vessels (no. 4Sb) were dissected. Then, the same plane of the greater omentum was dissected toward the hepatic flexure. The pedicle of the right gastroepiploic vessels was hung using the hanging forceps (Figure 4a), the right gastroepiploic vessels were exposed, and the infrapyloric lymph nodes (no. 6) were dissected. In cases requiring a D2 lymph node dissection, the lymph nodes around the superior mesenteric vein (no. 14v) were also dissected (Figure 4b). A 45-mm endoscopic linear stapler (ETS45; Ethicon Endo-Surgery) was inserted into the abdominal cavity through the multichannel port, and the duodenum was transected. In this situation, the laparoscope was inserted into the abdominal cavity through the 5-mm right midabdominal port. After the duodenum was transected, the proper hepatic artery was identified, and the right gastric artery was divided with a clip and the Harmonic scalpel at its origin. The suprapyloric lymph nodes (no. 5) were then dissected.
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Figure 2 (a) The hanging forceps was suspended from the abdominal wall using a thread. (b) After the tissue was grasped, the thread was pulled and clamped. In this manner, the organ was hung from the abdominal wall.
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5mm 5mm Multi channel port Figure 3 (a) Trocar placement for a triple-incision laparoscopic distal gastrectomy. (b) The operator stood on the right side of the patient and used two 5-mm trocars. The assistant stands between the patient’s legs and manipulates a 5-mm flexible scope and a rigid forceps through a multichannel port.
a
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GDA ASPDV
RGEA
GCT SMV
The pedicle of the left gastric vessels was hung using the hanging forceps (Figure 5a), and the lymph nodes along the common hepatic artery (no. 8a) and the celiac artery (no. 9) were dissected using the Harmonic scalpel. The left gastric vessels were divided at their origins with a clip and the Harmonic scalpel. In cases requiring a D2 lymph node dissection, the lymph nodes along the proper hepatic artery (no. 12a) and the splenic artery (no. 11p) were also dissected (Figure 5b). For the no. 12a and the
Figure 4 (a) The hanging forceps was attached to the pedicle of the right gastroepiploic vessels. (b) Dissection of no. 6 and 14v lymph nodes was completed. ASPDV, anterior superior pancreoduodenal vein; GCT, gastrocolic trunk; GDA, gastroduodenal artery; RGEA, right gastroepiploic artery; SMV, superior mesenteric vein.
no. 11p lymph node dissections, the portal vein and the splenic vein were identified as a landmark of the dorsal plane. The lymph nodes along the lesser curvature (nos. 1 and 3) were also dissected. The distal two-thirds of the stomach were intracorporeally dissected using a 60-mm endoscopic linear stapler (Echelon; Ethicon Endo Surgery), which was inserted into the abdominal cavity through the
Asian J Endosc Surg •• (2014) ••–•• © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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CHA PV
SV
Figure 5 (a) The hanging forceps was attached to the pedicle of the left gastric vessels. (b) A D2 lymph node dissection (no. 8a, 9, 11p, and 12a) was completed. CHA, common hepatic artery; PV, portal vein; SA, splenic artery; SV, splenic vein.
SA
5mm
12mm
5mm
12mm 12mm
Figure 7 Trocar placement in a conventional laparoscopy-assisted distal gastrectomy. In cases requiring an intracorporeal gastroenteral anastomosis, a 4–5-cm mini-laparotomy was made below the xiphoid process. Figure 6 Reconstruction was performed using the Roux-en-Y method in all the triple-incision laparoscopic distal gastrectomy cases.
multichannel port. To confirm the transection line, an intraoperative endoscopy examination was also performed. The dissected stomach was pulled out through the mini-laparotomy at the umbilical incision. Reconstruction was performed using the Roux-en-Y method (Figure 6). The jejunum was intracorporeally transected at a point 30 cm distal to the ligament of Treitz with an ETS45 endoscopic linear stapler. The Y-limb anastomosis was performed under direct vision through the mini-laparotomy at the umbilicus. The gastrojejuno anastomosis was performed intracorporeally using a 45-mm endoscopic linear stapler (ETS45). The common entry hole of the endoscopic linear stapler was closed using hand suturing.
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Operative technique for conventional LADG In the conventional LADG group, five ports were used: two bilateral subcostal ports, two bilateral mid-abdominal ports, and an umbilical port (Figure 7). The method used for the lymph node dissection was the same as that used for the TIL-DG. Reconstruction was performed using an extracorporeal Billroth-I method or the Roux-en-Y method, including an intracorporeal gastrojejunotomy or an extracorporeal gastrojejunostomy. In cases requiring an extracorporeal gastroduodenal anastomosis and an extracorporeal gastrojejunal anastomosis, a 4–5-cm minilaparotomy was performed below the xiphoid process. Clinical pathway In both the TIL-DG group and LADG group, the same clinical pathway was implemented for postoperative care.
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Figure 8 (a) Appearance of the wound 14 days after triple-incision laparoscopic distal gastrectomy. (b) Appearance of the wound 14 days after conventional laparoscopy-assisted distal gastrectomy.
Table 1 Patient and treatment characteristics
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2) Reconstruction Billroth I Roux-en-Y (extracorporeal) Roux-en-Y (intracorporeal)
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2)
Gender, male/female (n) Age, mean ± SD (years) BMI, mean ± SD (kg/m2)
TIL-DG group (n = 76)
LADG group (n = 59)
P-value
47/29 66.8 ± 10.3 22.1 ± 2.9
34/25 65.1 ± 13.1 22.3 ± 2.6
0.61 0.79 0.29
0 0 76
24 23 12
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
23/10 69.4 ± 9.8 21.4 ± 2.4
17/18 70.1 ± 10.3 22.8 ± 2.5
0.91 0.38 0.02 (P < 0.05)
TIL-DG (D2) group (n = 33)
LADG (D2) group (n = 35)
P-value
24/19 64.8 ± 10.3 22.6 ± 3.1
17/7 57.8 ± 13.4 21.7 ± 2.8
0.22 0.98 0.23
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
The nasogastric tube was removed soon after the operation. Clear liquids were restarted on postoperative day (POD) 1, and a liquid diet was restarted on POD 2. Nonsteroidal anti-inflammatory drugs were routinely administered on POD 1, and epidural catheters were routinely removed on POD 4. The peripheral intravenous drip was ended on POD 5, and the patients were discharged on POD 7 or POD 8. Figure 8a shows the wound 14 days after a TIL-DG. Figure 8 shows the wound 14 days after a conventional LADG. Statistical analysis All the data were analyzed using Statcel3 (the Useful Add-in Forms on Excel, 3rd ed.) for Windows (Tokorozawa, Japan). The χ2 test or the Fisher’s exact test was used to compare the patient characteristics and the postoperative outcome between the treatment groups. Continuous variables were compared using the Student’s
t-test and were expressed as the mean ± SD. P-values less than 0.05 were considered statistically significant.
Results The patient characteristics of the TIL-DG group and the LADG group are shown in Table 1. The mean age, sex, and BMI of the patients were similar between the two groups. The BMI in the TIL-DG (D1+) group was slightly less than that in the LADG (D1+) group. The types of reconstruction are also listed in Table 1. In the TIL-DG group, a Roux-en-Y reconstruction with an intracorporeal gastrojejunostomy was performed in all the cases. In the LADG group, a Roux-en-Y reconstruction with an intracorporeal gastrojejunostomy was performed in 12 cases. In the remaining 47 LADG cases (79.6%), either a Billroth I reconstruction via a 4–5-cm epigastric mini-laparotomy or a Roux-en-Y reconstruction with an extracorporeal gastrojejunostomy via a 4–5-cm epigastric mini-laparotomy was performed.
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Table 2 Short-term clinical outcomes
Operation time, mean ± SD (min) Blood loss, mean ± SD (mL) Number of dissected lymph nodes, mean ± SD (n) Postoperative hospital stay, mean ± SD (days) Intraoperative complication (n) Postoperative complication (n)
Operation time, mean ± SD (min) Blood loss, mean ± SD (mL) Number of dissected lymph nodes, mean ± SD (n) Postoperative hospital stay, mean ± SD (days) Intraoperative complication (n) Postoperative complication (n)
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
247.8 ± 54.9 48.8 ± 56.7 35.3 ± 12.1 7.5 ± 1.6 0 1 (pseudomonas colitis)
240.7 ± 62.1 70.0 ± 60.5 22.9 ± 13.3 8.7 ± 4.0 0 1 (pancreatic fistula)
0.62 0.14 0.00016(P < 0.05) 0.10
TIL-DG (D2) group (n = 43)
LADG (D2) group (n = 24)
P-value
268.9 ± 48.1 52.0 ± 80.2 43.9 ± 14.2 7.3 ± 1.3 0 1 (pancreatitis)
262.3 ± 52.6 61.5 ± 67.1 31.6 ± 12.5 8.0 ± 3.0 0 1 (anastomotic bleeding)
0.60 0.63 0.00071(P < 0.05) 0.21
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
The short-term outcomes of both groups are shown in Table 2. The TIL-DG group and the LADG group were each classified into two subgroups according to the level of the lymph node dissection (D1+ and D2). No significant differences in operation time, volume of blood loss, or postoperative hospital stay were observed between the two groups. The number of retrieved lymph nodes in the TIL-DG (D1+) group was higher than that in the LADG (D1+) group, and the number of retrieved lymph nodes in the TIL-DG (D2) group was also higher than that in the LADG (D2) group. No cases of intraoperative complications or conversion to open surgery occurred in either group. Postoperative complications occurred in two cases in the TIL-DG group (2.6%) and in two cases in the LADG group (3.4%). The complications in the TIL-DG group consisted of one case with pancreatitis and one case with pseudomembranous colitis. The patient with pancreatitis was treated conservatively and was discharged on POD 11. The patient with pseudomembranous colitis was also treated conservatively and was discharged on POD 14. The complications in the LADG group consisted of one case of pancreatic fistula and one case of anastomotic bleeding. The pancreatic fistula was diagnosed as Grade A according to the criteria of the International Study Group of Postoperative Pancreatic Fistula, and the patient was treated conservatively and was discharged on POD 13. The anastomotic bleeding occurred in a case that underwent Billroth I reconstruction using a circular stapler. The bleeding was stopped conservatively without requiring endoscopic clipping, and the patient was discharged on POD 21. The histopathological findings are listed in Table 3. No significant difference in the histological type, pT, pN, or pStage was seen between the treatment groups.
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The operation times for the consecutive TIL-DG cases are shown in Figure 9. A comparison of the mean operative time of the first five cases and the last five cases is also shown in Table 4. No significant differences in the mean operation times of the first five cases and the last five cases were observed when the patients were compared according to the D1+ and D2 lymphadenectomy subgroups.
Discussion The use of LADG has spread widely throughout Japan and other Asian nations since Kitano et al. first reported its application for early gastric cancer in 1994. In recent years, laparoscopic total gastrectomy and laparoscopic proximal gastrectomy for the upper third of the stomach have been performed at many medical institutions (8–11), and the long-term outcomes of laparoscopic gastrectomy for advanced gastric cancer have been reported in several studies (12,13). In contrast, SPS and RPS for gastroenterological surgery are presently in the spotlight as next-generation laparoscopic surgical techniques. The number of reports on the use of SPS for cholecystectomy or appendectomy has increased rapidly, and SPS for gastric cancer has also been recently reported in several studies. In many reports, SPS has been reported to offer an advantage over conventional laparoscopic surgery with regard to cosmesis. However, no reports have confirmed the minimal invasiveness of SPS compared with conventional laparoscopic surgery. SPS for gastrectomy requires a higher level of expertise than a conventional laparoscopic gastrectomy because of the complexity of the associated lymph node dissection and intracorporeal anastomosis. Generally, the operator manipulates the trocar through a multichannel port
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Table 3 Histopathological findings of the resected specimens
Location (L/M) Histological Type Differenciated Undifferenciated pT (1/2/3/4a) pN (0/1/2/3) pStage (1A/1B/2A/2B/3A)
Location (L/M) Histological type Differenciated Undifferenciated pT (1/2/3/4a) pN (0/1/2/3) pStage (1A/1B/2A/2B/3A/3B/3C)
TIL-DG (D1+) group (n = 33)
LADG (D1+) group (n = 35)
P-value
13/20
12/23
0.66
22 11 27/3/3/0 29/2/1/1 26/3/1/1/2
18 17 34/0/1/0 29/6/0/0 30/4/0/1/0
0.09 0.26 0.50
TIL-DG (D2) group (n = 43)
LADG (D2) group (n = 24)
P-value
17/26
16/8
0.03
20 23 31/4/3/5 30/9/2/2 24/8/4/4/1/2
10 14 17/5/2/0 15/7/2/0 13/6/2/2/1/0
0.23 0.56 0.89
L, lower third of the stomach ; LADG, laparoscopy-assisted distal gastrectomy; M, middle third of the stomach; TIL-DG, triple-incision laparoscopic distal gastrectomy.
Figure 9 Operation times (min) for consecutive triple-incision laparoscopic distal gastrectomy (TIL-DG) cases.
during SPS and even in RPS. The complexity of the manipulation consequently arises from the conflict between the forceps and the laparoscope. The operator’s trocar, especially the operator’s dominant trocar, should be free for movement. In our procedure, the operator
manipulates the trocars located at the right subcostal and right mid-abdomen. This trocar placement is the same as in conventional LADG. The processes of lymph node dissection and reconstruction are also the same as in conventional LADG. The special instruments required for
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Table 4 Mean operation time of TIL-DG (first five cases vs last five cases) TIL-DG (D1+)
First five cases (n = 5)
Last five cases (n = 5)
P-value
Operation time, mean ± SD (min) TIL-DG (D2)
306.6 ± 51.3
278.0 ± 48.5
0.39
First five cases (n = 5)
Last five cases (n = 5)
Operation time, mean ± SD (min)
273.0 ± 68.3
285.6 ± 34.3
0.72
LADG, laparoscopy-assisted distal gastrectomy; TIL-DG, triple-incision laparoscopic distal gastrectomy.
RPS and SPS, such as flexible forceps and multi-degree forceps, are not used to maintain triangulation and retraction of the organs. Instead, the assistant operator manipulates a forceps and a laparoscope through a multichannel port. Conflict between the forceps and the laparoscope is rare because the angle of approach to the target organ is different between the forceps and the 5-mm flexible laparoscope. Consequently, no significant differences in the mean operation time or the volume of blood loss were observed between the TIL-DG group and a conventional LADG group. As shown in Figure 3 and Table 4, no learning curve for the performance of a TIL-DG was observed, and there was no significant difference in the mean operation time between the first five and the last five cases that underwent TIL-DG. In the present study, all the operations were performed by one expert surgeon who had previously performed more than 300 laparoscopic gastrectomies. Similar results can be expected when other expert surgeons with experience performing LADG attempt to perform TIL-DG. However, the results would likely differ for beginner operators and trainees. Because the operator’s role is larger in a TIL-DG procedure than in an LADG procedure, the operator should take the initiative in the progress of the operation, similar to a solo surgery. In the present study, the average number of retrieved lymph nodes in the TIL-DG group was higher than that in the conventional LADG group. However, the period required to perform TIL-DG differed from that required to perform LADG. The data for the TIL-DG group were newer than for the LADG group by about 2 years. In recent years, high-definition laparoscope systems have undergone remarkable advances. Advancements in knowledge of microscopic anatomy, which have been facilitated by the images from these systems, have also been remarkable. As a result, laparoscopic techniques for lymph node dissection have improved and the number of retrieved lymph nodes has increased. Although there were no significant differences in the histopathological findings between the TIL-DG group and the LADG group, the pT, pN, and pStage were slightly higher in the TIL-DG group than in the LADG group. Consequently, these differences could have influenced the difference in the
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number of retrieved lymph nodes. At the least, the TIL-DG procedure is not inferior to conventional LADG with regard to oncological safety. Nevertheless, further randomized controlled trials comparing TIL-DG with LADG should be conducted to obtain accurate evidence regarding the oncological outcomes of TIL-DG. At present, several kinds of thin forceps with a diameter of 2–3 mm, such as the MiniLap (Stryker, Kalamazoo, USA) and the BJneedle (Nichion, Funabashi, Japan), have been developed. With these forceps and a thin trocar, a conventional LADG could obtain better cosmesis. Additionally, the advantages of TIL-DG include the efficient utilization of surgical staff. In conventional LADG, the procedure is conducted by three surgical staff members consisting of an operator, an assistant operator, and a laparoscopist. In TIL-DG, the procedure is conducted by only two surgical staff members, an operator and an assistant operator. Reducing the number of surgical staff required leads to cost savings for the operation. Generally, the assistant operator manipulates two forceps to create the surgical field in conventional LADG. In TIL-DG, the assistant operator manipulates only one pair of forceps. Accordingly, the shortage of forceps is compensated for by the use of assistant forceps, or hanging forceps. The method of towing internal organs, such as the gallbladder or liver, using threads has been described as a “marionette trick.” (14–16) Our method of using the hanging forceps is a modification of the marionette trick, and the hanging forceps have the advantage that the traction point can be easily changed by altering the grasping point. Throughout all the steps of the TILDG, the hanging forceps were only required twice: for the no. 6 lymph node dissection and for the no. 8a and no. 9 lymph node dissection. The other steps could be completed without using the hanging forceps. Thus, the creation of the surgical field throughout the entire TIL-DG was not complicated. The TIL-DG has superior cosmesis compared with a conventional LADG, and this technique has the potential to become a technically and oncologically accepted alternative to LADG. However, the indications for conventional LADG for advanced gastric cancer remain controversial, as do the safety and feasibility of reduced port surgery (or single-incision surgery) for gastric
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cancer. Further examination is required to evaluate the benefits of TIL-DG.
Acknowledgments The authors have no conflict of interest to report. The authors wish to thank Shigeyuki Sakaguchi for preparing the schema.
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