Summary

There has been a recent increase in the use of totally laparoscopic total gastrectomy (TLTG) for gastric cancer. However, there is no scientific evidence to determine which esophagojejunostomy (EJS) technique is the best. In addition, both short- and long-term oncological results of TLTG are inconsistent. We reviewed 25 articles about TLTG for gastric cancer in which at least 10 cases were included. We analyzed the short-term results, relationships between EJS techniques and complications, long-term oncological results, and comparative study results of TLTG. TLTG was performed in a total of 1170 patients. The mortality rate was 0.7%, and the short-term results were satisfactory. Regarding EJS techniques and complications, circular staplers (CSs) methods were significantly associated with leakage (4.7% vs. 1.1%, p < 0.001) and stenosis (8.3% vs. 1.8%, p < 0.001) of the EJS as compared with the linear stapler method. The long-term oncological prognosis was acceptable in patients with early gastric cancers and without metastases to lymph nodes. Although TLTG tended to increase surgical time compared with open total gastrectomy and laparoscopy-assisted total gastrectomy, it reduced intraoperative blood loss and was expected to shorten postoperative hospital stay. TLTG is found to be safer and more feasible than open total gastrectomy and laparoscopy-assisted total gastrectomy. At present, there is no evidence to encourage performing TLTG for patients with advanced gastric cancer from the viewpoint of long-term oncological prognosis. Although the current major EJS techniques are CS and linear stapler methods, in this review, CS methods are significantly associated with leakage and stenosis of the EJS.

Keywords

circular stapler;esophagojejunostomy;gastric cancer;linear stapler;totally laparoscopic total gastrectomy

1. Introduction

Laparoscopy-assisted distal gastrectomy (LADG) for gastric cancer was first performed by Kitano et al1 in 1994 and showed satisfying short-term results.2 The long-term results of LADG for early gastric cancer were also favorable,3 and LADG was reported to be surgically less invasive and lead to an earlier recovery than open surgery.4 ;  5

The number of reports on laparoscopy-assisted total gastrectomy (LATG) for gastric cancer has increased with the advancement of techniques for lymphadenectomy and reconstructive procedures for the upper stomach.6; 7; 8; 9 ;  10 However, esophagojejunostomy (EJS) via minilaparotomy in LATG is relatively difficult because of the limited angle of the direct view, depending on the patients somatotype and obesity index, and totally laparoscopic total gastrectomy (TLTG) has become more commonly used for intracorporeal anastomosis performed under pneumoperitoneum. As surgical techniques progressed from LATG to TLTG, new EJS techniques have been devised for TLTG.11; 12; 13; 14 ;  15 TLTG has been widely performed in Japan and Korea and has shown favorable short-term performance results.16; 17; 18 ;  19

EJS in TLTG is a very important surgical procedure because it is associated with the risk of anastomotic leakage, bleeding, and stenosis.20 ;  21 No scientific conclusion can be drawn at present regarding which procedure reduces the postoperative complications of EJS in TLTG because no clear evidence is available based on well-designed randomized controlled trials (RCTs). We retrospectively reviewed reports on various techniques for EJS in TLTG, compared various EJS techniques and complications, and investigated short- and long-term oncological results and comparative study results of TLTG.

2. Methods

2.1. Definition and surgical techniques

This review included TLTG or totally laparoscopic degastrectomy for gastric or remnant gastric cancer, using Roux-en Y reconstruction. As with surgical procedures via minilaparotomy, the removal of resected specimens and performing jejunojejunostomy were permitted. EJS had to be performed intracorporeally under pneumoperitoneum to satisfy the determination of TLTG. Regarding EJS techniques, this review targeted the so-called single stapling technique (SST), double stapling technique (DST), and hemidouble stapling technique (HDST) using circular staplers (CSs), as well as the functional end-to-end anastomosis (FETEA) and overlap methods using linear staplers (LSs), and the hand-sewn (HS) method, and classified procedures into these six types. Reports that did not meet the above criteria or those using several or unknown EJS techniques were excluded from the analyses of EJS techniques.

We analyzed short-term results, relationships between EJS techniques and complications, as well as long-term oncological results and comparative study results of TLTG.

2.2. Search strategy

This review included only English articles identified by the term “totally laparoscopic” or a combination of “laparoscopic” and “total gastrectomy” in the PubMed online database. On July 15, 2013, a final search of PubMed was performed, and we selected and reviewed original articles describing the clinical results of TLTG performed in at least 10 cases. Reports using animal data or those including robotic surgeries were excluded.

2.3. Statistical analyses

Data were collected and analyzed using StatMate IV for Windows (ATMS Co., Ltd., Tokyo, Japan). The Student t test was used to compare the continuous variable, and the Chi-square test was used to compare the categorical variable. A p value < 0.05 was considered significant.

3. Results

3.1. Literature overview

In 2005, Dulucq et al22 reported the first case series of TLTG for gastric cancer (n = 8), which was a prospective single-center study of TLTG and other surgical procedures. Since then, TLTG has become a more commonly used surgical procedure for gastric cancer, and many reports focusing on reconstruction techniques in EJS and short-term results have been published in recent years. Our initial literature search found 629 articles; however, only 25 of them satisfied the conditions described above. 11; 12; 13; 14; 15; 16; 17; 18; 19; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33; 34; 35; 36; 37 ;  38

Table 111; 12; 13; 14; 15; 16; 17; 18; 19; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33; 34; 35 ;  36 summarizes the reports cited in this review. Of the 25 articles cited in this review, only two were prospective studies and the remaining 23 were retrospective studies. Three articles described comparative studies of TLTG and open total gastrectomy (OTG),16; 17 ;  19 including one comparing TLTG versus LATG.18 Sixteen articles focused on surgical and short-term results only, and nine articles described long-term oncological results.13; 17; 23; 25; 27; 29; 35; 36 ;  37

Table 1. Outline of the cited articles.
Author Publication year Study design Comparative study Total number EJS method
Huscher et al23 2007 Retrospective No 11 FETEA
Topal et al16 2008 Prospective TLTG vs. OTG 38 SST/DST
Usui et al11 2008 Retrospective TLTG vs. TLTG with J pouch 23 SST
Ziqiang et al24 2008 Retrospective No 14 FETEA
Okabe et al12 2009 Retrospective No 16 FETEA
Jeong and Park13 2009 Retrospective No 16 DST
Shinohara et al25 2009 Retrospective No 55 FETEA
Kinoshita et al14 2010 Retrospective No 10 SST
Bracale et al26 2010 Retrospective No 67 FETEA
Inaba et al15 2010 Retrospective No 53 Overlap
Marangoni et al27 2012 Retrospective No 53 DST
Moisan et al17 2012 Prospective TLTG vs. OTG 31 HS
Nunobe et al28 2011 Retrospective No 41 DST
Tsujimoto et al29 2012 Retrospective TLTG vs. LPG 15 Overlap
Jeong et al30 2012 Retrospective TLTG vs. LDG 118 SST/DST
Lee et al31 2012 Retrospective No 27 FETEA
Shim et al32 2013 Retrospective SST vs. DST vs. HDST vs. Overlap 48 SST/DST/HDST/Overlap
Kim et al33 2012 Retrospective No 124 FETEA
Yoshikawa et al34 2013 Retrospective No 20 SST
Kim et al18 2013 Retrospective TLTG vs. LATG 90 FETEA
Kim et al19 2013 Retrospective TLTG vs. OTG 139 FETEA
Ebihara et al35 2013 Retrospective No 65 FETEA
Lafemina et al36 2013 Retrospective No 17 DST
Kim et al37 2013 Retrospective No 36 SST
Nagai et al38 2013 Retrospective Early group vs. recent group 94 Overlap

DST = double stapling technique; EJS = esophagojejunostomy; FETEA = functional end-to-end anastomosis; HDST = hemidouble stapling technique; HS = hand-sewn; LATG = laparoscopy assisted total gastrectomy; LDG = laparoscopic distal gastrectomy; LPG = laparoscopic proximal gastrectomy; OTG = open total gastrectomy; SST = single stapling technique; TLTG = totally laparoscopic total gastrectomy.

As for EJS techniques, SST, DST, HDST, FETEA, overlap, and HS methods were used in seven, seven, one, 10, four, and one articles, respectively.

3.2. Patient demographics

Table 21; 2; 3; 4; 5; 6; 7; 8; 9; 10; 11; 12; 13; 14; 15; 16; 17; 18; 19; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33; 34; 35; 36; 37 ;  38 summarizes the backgrounds of patients reported in the articles cited in this review. TLTG was performed in a total of 1170 patients, and of the 1094 with data on sex ratios, TLTG was more often performed on men (760 men vs. 334 women). Some studies reported mean values, and the others used median values for age and body mass index; when mean values were used, the mean age and mean body mass index were calculated to be 62.2 years and 23.2 kg/m2, respectively. A history of open abdominal surgery was described in seven articles, and 92 patients (92/559, 16.5%) had a history of open abdominal surgery. In 462 patients with data on clinical stage, the numbers of patients in each of the TNM classification (7th edition) by the Union for International Cancer Control were 1/317/65/54/25 in the order of clinical stages 0/I/II/III/IV, respectively.

Table 2. Patients' demographic characteristics.
Author Publication year Total number Sex M/F Age (y) Mean ± SD or median (range) BMI (kg/m2) Mean ± SD or median (range) Previous abdominal surgery TNM classification UICC, 7th edition (0/I/II/III/IV) Surgical indication
Huscher et al23 2007 11 ND ND ND ND 0/4/1/2/4 Advanced included
Topal et al16 2008 38 23/15 68.0 (37–85) 24.0 (17–30) ND 0/17/7/10/4 Advanced included
Usui et al11 2008 23 18/5 67.7 ± 11.5 23.7 ± 11.5 ND ND Under T2 and N1
Ziqiang et al24 2008 14 9/5 57.4 ± ND ND ND ND Advanced included
Okabe et al12 2009 16 11/5 70.0 (39–81) 20.8 (16.7–27.6) ND ND Any T and N0
Jeong and Park13 2009 16 10/6 59.0 ± ND 23.0 ± ND 0 ND Under T2 and N0
Shinohara et al25 2009 55 41/14 59.0 (29–80) ND ND 0/17/12/16/10 Advanced included
Kinoshita et al14 2010 10 9/1 63.7 (45–80) 22.4 (18.0–26.0) ND ND Any T and N0
Bracale et al26 2010 67 45/22 66.9 ± ND ND ND 0/35/15/12/5 Advanced included
Inaba et al15 2010 53 40/13 59.4 (30–82) 22.0 (15.0–32.4) ND ND Advanced included
Marangoni et al27 2012 13 ND ND ND ND 1/3/4/5/0 Advanced included
Moisan et al17 2012 22 ND 67.0 (29–83)a 26.0 (19–30)a 10a ND Advanced included
Nunobe et al28 2011 41 31/10 65.8 ± 1.6 23.8 ± 0.6 9 0/41/0/0/0 Under T1 and N0
Tsujimoto et al29 2012 15 10/5 65.8 ± 14.3 20.8 ± 3.8 ND 0/10/2/1/2 Under T3 and N1
Jeong et al30 2012 118 77/41 63.7 ± 11.0 23.2 ± 3.6 2 ND Under T2 and N0
Lee et al31 2012 27 16/11 59.1 ± ND 24.6 ± ND ND 0/23/4/0/0 ND
Shim et al32 2013 48 33/15 56.7 ± ND 24.3 ± ND ND ND ND
Kim et al33 2012 124 77/47 57.4 ± ND 23.6 ± ND 27 ND Advanced included
Yoshikawa et al34 2013 20 ND ND ND ND ND ND
Kim et al18 2013 90 61/29 58.0 ± 10.8 23.2 ± 2.9 21 ND Advanced included
Kim et al19 2013 139 86/53 58.0 (30–84) 23.6 (13.6–32.4) 23 ND Advanced included
Ebihara et al35 2013 65 45/20 65.9 ± 10.2 23.5 ± 4.0 ND 0/65/0/0/0 Stage I
Lafemina et al36 2013 17 40/8 64.0 (55–70)b 27.1 (24.0–30.5)b ND ND Advanced included
Nagai et al38 2013 94 64/30 66.0 ± ND 21.6 ± ND ND 0/71/19/4/0 Advanced included
Kim et al37 2013 36 24/12 60.9 ± 11.4 23.4 ± 3.4 ND 0/31/1/4/0 Under T1 and N0
Total or mean 1170 760/334 62.2 c 23.2 d 92 1/317/65/54/25

BMI = body mass index; ND = not described in the article; OTG = open total gastrectomy; SD = standard deviation; TLTG = totally laparoscopic total gastrectomy; UICC = Union for International Cancer Control.

a. Nine laparoscopic subtotal gastrectomy cases were included in these data.17

b. Thirty-one OTG cases were included in these data.36

c. Mean age of the TLTG cases was calculated using every data of the articles, except for median value.

d. Mean BMI of the TLTG cases was also calculated using every data of the articles, except for median value.

Table 2 also presents data containing clear surgical indication of TLTG. Thirteen reports had no limitations on the indication of TLTG for advanced gastric cancer, and the others limited indication to cases of T3 or less and N1 or less gastric cancer.

3.3. Surgical data

Table 311; 12; 13; 14; 15; 16; 17; 18; 19; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33; 34; 35; 36; 37 ;  38 provides the surgical results of TLTG. Some studies used median values, and others used mean values to report the surgical results. The mean surgical time and mean blood loss calculated from reported mean values were 254.2 minutes and 114.0 mL, respectively. For lymphadenectomy, the numbers of patients classified as D0/D1/D1+/D2 in the 14th edition of the Japanese Classification of Gastric Carcinoma by the Japan Gastric Cancer Association were 0/13/238/270, respectively, and some of the patients with advanced gastric cancer concomitantly underwent pancreatosplenectomy or splenectomy. Twenty-three patients were converted to OTG, mostly owing to intraoperative accidental symptoms as well as uncontrollable bleeding and difficulties in EJS techniques. The mean number of dissected lymph nodes calculated from the reported mean values was 39.5.

Table 3. Surgical data.
Author Publication year Surgical time (min) Mean ± SD or median (range) Blood loss (mL) Mean ± SD or median (range) Lymphadenectomy (D0/D1/D1+/D2) Conversion to OTG Harvested lymph nodes Mean ± SD or median (range)
Huscher et al23 2007 304.0 ± 83.0 ND 0/2/0/9 3 a 35.0 ± 18.0 a
Topal et al16 2008 187.0 (120–360) 10.0 (5–400) 0/0/0/38 0 17.0 (0–90)
Usui et al11 2008 305.9 ± 57.6 77.5 ± 71.7 0/0/22/1 0 ND
Ziqiang et al24 2008 255.1 ± ND 107.5 ± ND 0/0/0/14 0 ND
Okabe et al12 2009 325.0 ± 68.0 195.0 ± 197.0 ND 0 47.0 ± 13.0
Jeong and Park13 2009 194.0 ± ND 170.0 ± ND 0/0/16/0 0 33.0 ± ND
Shinohara et al25 2009 406.0 (200–865) 102.0 (20–694) 0/0/0/55 0 46 (17–106)
Kinoshita et al14 2010 257.0 ± ND 69.0 ± ND ND 0 43.3 ± ND
Bracale et al26 2010 249.0 ± ND ND 0/5/0/62 7 ND
Inaba et al15 2010 373.4 ± 105.0 146.5 ± 325.3 ND 0 ND
Marangoni et al27 2012 260.0 ± ND 125.0 ± ND ND 1 26.0 ± ND
Moisan et al17 2012 250.0 (160–240) b 100.0 (50–500) b 0/3/5/23 b 1 b 35 (9–68) b
Nunobe et al28 2011 298.6 ± 10.1 85.9 ± 15.2 0/0/0/41 0 42.8 ± 2.3
Tsujimoto et al29 2012 236.4 ± 43.4 51.2 ± 58.0 0/3/7/5 0 38.6 ± 15.4
Jeong et al30 2012 292.0 ± 88.0 256.0 ± 207.0 0/0/99/19 1 41.0 ± 16.0
Lee et al31 2012 126.2 ± 21.3 ND 0/0/27/0 0 33.7 ± 16.2
Shim et al32 2013 A:229.1 ± 45.7 c ND ND 0 ND
B:226.5 ± 51.4 c
C:209.0 ± 39.4 c
D:205.5 ± 33.1 c
Kim et al33 2012 F:189.0 ± 46.3 d ND ND 0 42.6 ± 15.5 d
S:148.3 ± 51.9 d 37.4 ± 15.7 d
Yoshikawa et al34 2013 297.1 ± ND ND ND 0 ND
Kim et al18 2013 166.4 ± 47.5 ND ND 0 43.1 ± 17.2
Kim et al19 2013 144.0 (72–345) ND ND 0 37 (2–94)
Ebihara et al35 2013 271.5 ± 64.7 85.2 ± 143.2 0/0/62/3 1 30.2 ± 12.4
Lafemina et al36 2013 230 (190–277) 250 (150–450) ND 9 22 (17–28)
Nagai et al38 2013 E:341.4 ± 75.7e 70.2 ± 77.3e ND 0 53.4 ± 21.0e
R:368.0 ± 94.6e 80.4 ± 115.0e 47.0 ± 18.8e
Kim et al37 2013 227.1 ± 57.6 77.1 ± 71.7 ND 0 37.9 ± 10.9
Total or mean 254.2 f 114.0 g 0/13/238/270 23 39.5 h

DST = double stapling technique; HDST = hemidouble stapling technique; ND = not described in the article; OTG = open total gastrectomy; SD = standard deviation; SST = single stapling technique; TLTG = totally laparoscopic gastrectomy.

a. Eighty-nine laparoscopic subtotal gastrectomy cases were included in these data.23

b. Nine laparoscopic subtotal gastrectomy cases were included in these data.17

c. Shim et al32 reported four types of EJS techniques: types A, B, C, and D denote SST, DST, HDST, and overlap methods, respectively.

d. Kim et al33 reported the comparison of TLTG cases between first 70 cases (F) and subsequent 54 cases (S).

e. Nagai et al38 reported the comparison of TLTG cases between early period (E) and recent period (R).

f. Mean surgical time was calculated using every data of the articles, except for median value.

g. Mean blood loss was calculated using every data of the articles, except for median value.

h. Average of harvested lymph nodes was also calculated using every data of the articles, except for median value.

3.4. Postoperative data

Table 411; 12; 13; 14; 15; 16; 17; 18; 19; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33; 34; 35; 36; 37 ;  38 provides the postoperative results of TLTG. Postoperative complications included leakage of the EJS (n = 33), leakage of the duodenal stump (n = 19), anastomotic bleeding (n = 33), postoperative pancreatic fistula (n = 16), and stenosis of the EJS (n = 38). The mortality rate was only 0.7% (8/1170). Based on articles with mean values, the time to the first flatus and time to restart oral intake were 3.3 days and 5.0 days, respectively, and the mean postoperative hospital stay was 12.0 days.

Table 4. Postoperative data.
Author Publication year EJS leakage Stump leakage Bleeding Pancreatic fistula EJS stenosis Mortality Time to flatus (d) Mean ± SD or median (range) Time to intake (d) Mean ± SD or median (range) Hospital stay (d) Mean ± SD or median (range)
Huscher et al23 2007 0 2 2 0 0 2 3.4 ± 1.0 a 5.9 ± 4.5a 11.4 ± 4.5a
Topal et al16 2008 2 0 0 0 0 1 ND ND 11.0 (6–73)
Usui et al11 2008 0 0 0 0 0 0 ND ND 11.2 ± 5.3
Ziqiang et al24 2008 0 0 0 1 0 0 3.9 ± ND 4.9 ± 1.0 ND
Okabe et al12 2009 0 0 0 0 1 0 ND 3.0 (ND) 11.0 (ND)
Jeong and Park13 2009 0 0 0 0 0 0 ND ND (3–5) 11.0 (8–14)
Shinohara et al25 2009 2 0 0 7 0 0 ND 3.0 (3–6) 14.0 (9–25)
Kinoshita et al14 2010 0 0 0 0 0 0 ND 4.0 (2–10) 13.0 (8–24)
Bracale et al26 2010 4 3 5 0 2 1 4.7 ± ND ND 12.4 (8–45)
Inaba et al15 2010 2 1 0 3 1 0 ND ND 14.4 ± ND
Marangoni et al27 2012 0 0 0 0 0 1 ND ND 11.0 (ND)
Moisan et al17 2012 2 2 1 0 0 0 ND 4.0 (2–13) 7.0 (4–59)
Nunobe et al28 2011 2 0 0 3 3 0 ND 2.7 ± 0.5 16.9 ± 1.5
Tsujimoto et al29 2012 0 0 0 0 0 0 3.0 ± 1.3 4.1 ± 2.2 13.5 ± 9.1
Jeong et al30 2012 9 1 11 0 4 2 2.9 ± 0.8 3.5 ± 4.5 11.9 ± 11.9
Lee et al31 2012 0 0 3 0 0 0 ND ND 8.1 ± ND
Shim et al32 2013 A:2 b 1 b 0 b 0 b 5 b 0 b ND ND 10.3 ± ND b
B:2 b 0 b 0 b 0 b 4 b 0 b 8.4 ± ND b
C:1 b 1 b 1 b 0 b 1 b 0 b 9.3 ± ND b
D:0 b 0 b 0 b 0 b 0 b 0 b 8.8 ± ND b
Kim et al33 2012 F:2 c 1 c 1 c 0 c 5 c 0 c 3.2 ± 0.9 c 8.6 ± 9.6 c 12.7 ± 11.5 c
S:0 c 0 c 3 c 0 c 1 c 0 c 3.3 ± 0.9 c 5.6 ± 4.6 c 8.8 ± 5.8 c
Yoshikawa et al34 2013 0 0 0 0 0 0 ND ND ND
Kim et al18 2013 0 1 2 0 4 0 3.4 ± 1.0 4.5 ± 1.8 7.9 ± 4.3
Kim et al19 2013 0 1 3 0 2 0 3.0 (2–6) 3.0 (3–46) 7.0 (5–72)
Ebihara et al35 2013 0 1 0 1 3 1 1.9 ± 0.7 4.6 ± 1.8 21.4 ± 13.5
Lafemina et al36 2013 1 2 1 0 1 0 ND ND 8.0 (6–9)
Nagai et al38 2013 E:2 d 0 d 0 d 0 d 0 d 0 d ND 5.5 ± 2.5 d 16.7 ± 9.5 d
R:0 d 1 d 0 d 1 d 0 d 0 d 4.9 ± 4.7 d 14.2 ± 12.1 d
Kim et al37 2013 0 1 0 0 0 0 3.1 ± 0.7 ND 9.2 ± 8.7
 Total or Mean 33 19 33 16 38 8 3.3 e 5.0 f 12.0 g

DST = double stapling technique; EJS = esophagojejunostomy; HDST = hemidouble stapling technique; ND = not described in the article; SD = standard deviation; SST = single stapling technique; TLTG = totally laparoscopic gastrectomy.

a. Eighty-nine laparoscopic subtotal gastrectomy cases were included in these data.23

b. Shim et al32 reported four types of EJS techniques: types A, B, C, and D denote SST, DST, HDST, and overlap methods, respectively.

c. Kim et al33 reported the comparison of TLTG cases between first 70 cases (F) and subsequent 54 cases (S).

d. Nagai et al38 reported the comparison of TLTG cases between early period (E) and recent period (R).

e. Mean time to first flatus was calculated using every data of the articles, except for median value.

f. Mean time to oral intake was calculated using every data of the articles, except for median value.

g. Average of postoperative hospital stay was also calculated using every data of the articles, except for median value.

3.5. EJS techniques: Overview

Table 5 summarizes the EJS techniques used in the cited articles. For methods of anvil insertion and purse-string suture placement, only representative methods are listed in Table 5. With EJS techniques using LSs, disruption of the esophageal hiatus and slippage of the EJS site into the lower mediastinum are possible. The HS method is highly feasible to use for intracorporeal anastomosis, providing a sufficient view under pneumoperitoneum, and has the advantage of not requiring an entry hole closure. EJS techniques used in 101 patients, 139 patients, 14 patients, 553 patients, 176 patients, 31 patients, and 156 patients were SST, DST, HDST, FETEA, overlap, HS, and unknown methods, respectively.

Table 5. EJS techniques overview and comparison of postoperative complications.
SST DST HDST FETEA Overlap HS p
Anvil insertion Endo PSI EndoStitch Hand-sewn, etc. Orvil EST, etc. Orvil, etc.
Double stapling + +
Hiatus destroy + +
Anastomosis in mediastinum + +
Necessity of entry hole closure + + + + +
Diameter of anastomosis (mm) < 30 < 30 mm < 30 > 30 > 30 20–30
Number (n) a 101 139 14 553 176 31
Duration of anastomosis Mean ± SD or median (range) 6.0 ± ND d 43.2 ± 11.5 f P: 8.9 ± 5.1 g A: 6.4 ± 3.6 g 54.0 ± ND c 42.8 ± 11.3 f 37.0 ± 7.1 f 42.5 ± ND b 44.0 ± ND e 34.3 ± 6.4 f 0.041f
Complications (n, %)
 EJS leakage 6, 5.9 5, 3.6 1, 7.1 6, 1.1 2, 2.3 2, 6.5 0.009
 Bleeding 4, 4.0 1, 0.7 1, 7.1 15, 2.7 0, 0 1, 3.2 0.110
 EJS stenosis 12, 11.9 8, 5.8 1, 7.1 12, 2.2 1, 0.6 0, 0 < 0.001
 Stump leakage 3, 3.0 2, 1.4 1, 7.1 8, 1.4 2, 1.1 2, 6.5 0.198
 Pancreatic fistula 0, 0 3, 2.2 0, 0 9, 1.6 4, 2.3 0, 0 0.680
Mortality (n, %) 0, 0 1, 0.7 0, 0 4, 0.7 0, 0 0, 0 0.803

DST = double stapling technique; EJS = esophagojejunostomy; EST = efficient purse-string stapling technique; FETEA = functional end-to-end anastomosis; HDST = hemidouble stapling technique; HS = hand-sewn; ND = not described in the article; SD = standard deviation; SST = single stapling technique.

a. A total of 156 cases were excluded from these series, because descriptions of EJS techniques and breakdown of methods were unclear.

b. Ziqiang et al24 reported these data; the range was 32–66 minutes.

c. Jeong and Park13 reported these data; the range was 38–75 minutes.

d. Kinoshita et al14 reported these data, but this was the mean time for purse-string by hand-sewn suturing. Its range was 5–7 minutes.

e. Bracale et al26 reported these data; the range was 38–54 minutes.

f. Shim et al32 reported four types of EJS techniques: types A, B, C, and D denote SST, DST, HDST, and overlap methods, respectively.

g. Kim et al37 reported time for purse-string suture (P) and time for anvil placement (A).

For the time required to perform EJS, Kinoshita et al14 reported 6 minutes on average from purse-string suture placement using the HS method to the insertion of the anvil using the SST method. Kim et al37 also reported that the mean times for purse-string suture and for anvil placement in the SST method were 8.9 minutes and 6.4 minutes, respectively. Jeong and Park13 reported that EJS using the DST method took 54 minutes on average. Ziqiang et al24 reported that EJS using the FETEA method took 42.5 minutes on average, and Bracale et al26 also reported that it took 44.0 minutes on average, accounting for 17.7% of the entire surgical time. Shim et al32 compared four EJS techniques (SST, DST, HDST, and overlap methods) and showed that EJS took 43.2 ± 11.5 minutes, 42.8 ± 11.3 minutes, 37.0 ± 7.1 minutes, and 34.3 ± 6.4 minutes, respectively, with a significantly shorter time required for the overlap method (p = 0.041).

Regarding the major postoperative complications associated with each method, the incidence rates of leakage of the EJS were 5.9% (6/101), 3.6% (5/139), 7.1% (1/14), 1.1% (6/553), 2.3% (2/176), and 6.5% (2/31) using the SST, DST, HDST, FETEA, overlap, and HS methods, respectively, showing high rates with HDST, HS, and SST methods (p = 0.009). The incidence rates of anastomotic bleeding were also 4.0% (4/101), 0.7% (1/139), 7.1% (1/14), 2.7% (15/553), 0%, and 3.2% (1/31) using the SST, DST, HDST, FETEA, overlap, and HS methods, respectively, with no significant difference between the six methods (p = 0.110). The incidence rates of stenosis of the EJS were 11.9% (12/101), 5.8% (8/139), 7.1% (1/14), 2.2% (12/553), 0.6% (1/176), and 0%, using SST, DST, HDST, FETEA, overlap, and HS methods, respectively, showing the highest rate with the SST method (p < 0.001). No significant difference was detected for the incidences of leakage of the duodenal stump, postoperative pancreatic fistula, and mortality.

In the analysis using the stapling device (Table 6), the incidence of leakage of the EJS was significantly higher in the CS methods than in the LS methods (4.7% vs. 1.1%, p < 0.001). The incidence of stenosis of the EJS was also significantly higher in the CS methods than in the LS methods (8.3% vs. 1.8%, p < 0.001). No significant difference was detected for the incidence of anastomotic bleeding.

Table 6. Comparison of postoperative complications between CS methods and LS methods.
CS methods SST DST HDST LS methods FETEA Overlap p
Number (n) 254 729
Complication (n, %)
EJS leakage 12, 4.7 8, 1.1 < 0.001
Bleeding 6, 2.4 15, 2.1 0.777
Stenosis of EJS 21, 8.3 13, 1.8 < 0.001

CS = circular stapler; DST = double stapling technique; EJS = esophagojejunostomy; FETEA = functional end-to-end anastomosis; HDST = hemidouble stapling technique; LS = linear stapler; SST = single stapling technique.

3.6. Long-term outcome

Table 713; 17; 23; 25; 27; 29; 35; 36 ;  37 summarizes nine articles that followed the long-term oncological prognosis of patients who underwent TLTG. The use of various prognostic indexes in these articles made it difficult for us to appropriately evaluate the results. The observation periods varied widely (1–160 months) among reports, and several reports included many cases of advanced gastric cancer. For case series including advanced gastric cancer patients, the incidences of recurrence were 11 patients (20.0%) in the report by Shinohara et al,25 11 patients (22.0%) in the report by Marangoni et al,27 five patients (16.1%) in the report by Moisan et al,17 and 14 patients (29.2%) in the report by Lafemina et al.36 In the reports of Tsujimoto et al29 and Ebihara et al,35 in which strict conditions were established for the indication of TLTG, no recurrence was reported during the observation period.

Table 7. Long-term outcome.
Author Publication year Surgical indication Follow-up period Mean ± SD or median (range) Recurrence, n (%) Survival rates (%)
Huscher et al23 2007 Advanced included 57.6 ± 44.5a 31,a 31.0a OS = 59%,b DFS = 57%b
Jeong and Park13 2009 Under T2 and N0 6.4 ± ND ND ND
Shinohara et al25 2009 Advanced included 16.0 (7–130) 11, 20.0 ND
Marangoni et al27 2012 Advanced included 10.0 (3–26) 11, 22.0 ND
Moisan et al17 2012 Advanced included 28.0 (ND) 5, 16.1 OS = 82.3,c DFS = 79.4c
Tsujimoto et al29 2012 Under T3 and N1 18.9 ± ND 0, 0 ND
Ebihara et al35 2013 Stage I 37.0 (11–68) 0, 0 ND
Lafemina et al36 2013 Advanced included 18.0 (11–34) 14, 29.2 ND
Kim et al37 2013 Under T1 and N1 13.2 (ND) ND ND

DFS = disease-free survival; ND = not described in the article; OS = overall survival; SD = standard deviation.

a. Eighty-nine laparoscopic subtotal gastrectomy cases were included in these data.23

b. These were the 5-year OS and DFS rates.23

c. These were the 3-year OS and DFS rates.17

Regarding survival time, Moisan et al17 reported 3-year disease-free survival (DFS) and 3-year overall survival (OS) rates of 79.4% and 82.3%, respectively. When the analysis was limited to patients with early gastric cancer, the 3-year DFS and 3-year OS rates were pegged at 81.7% and 93.3%, respectively. Huscher et al23 reported 5-year DFS and 5-year OS rates of 57.0% and 59.0%, respectively.

3.7. Comparative studies between TLTG and OTG or LATG

Table 816; 17; 18 ;  19 provides the overview and conclusions of three TLTG versus OTG comparative studies and one TLTG versus LATG comparative study. The surgical time of TLTG was significantly longer than that of OTG in two articles (Topal et al16: 187.0 minutes vs. 150.0 minutes, p = 0.0003; Moisan et al 17: 250.0 minutes vs. 210.0 minutes, p = 0.007, mean). However, TLTG was associated with significantly less blood loss in two articles (Topal et al 16: 10.0 mL vs. 175.0 mL, p = 0.0001; Moisan et al 17: 100.0 mL vs. 300.0 mL, p = 0.001, median) and a significantly shorter postoperative hospital stay in two articles (Moisan et al 17: 7.0 days vs. 10.5 days, p = 0.001; Kim et al 19: 7.0 days vs. 8.0 days, p < 0.001, median), with no difference in postoperative complications compared to OTG. All articles concluded that TLTG was safe and feasible compared with OTG and LATG. 16; 17; 18 ;  19

Table 8. Comparative studies between TLTG and OTG or LATG.
Author Publication year Comparison Surgical time (min) Mean ± SD or median (range) Blood loss (ml) Mean ± SD or median (range) Postoperative complicationsn (%) Hospital stay Mean ± SD or median (range) Conclusion for TLTG
Topal et al16 2008 Prospective 187.0 (120–360) 10.0 (5–400) 15, 39.4 11.0 (6–73) Safe and feasible
TLTG vs. OTG 150.0 (120–360) 175.0 (50–1400) 9, 40.9 ND
(38 vs. 22) p = 0.0003 p < 0.0001 p = 0.913 p = 0.847
Moisan et al17 2012 Prospective 250.0 (160–420) 100.0 (50–500) 7, 22.5 7.0 (4–59) Safe and feasible
TLTG vs. OTG 210.0 (135–390) 300.0 (200–1400) 4, 12.9 10.5 (6–37)
(31 vs. 31) p = 0.007 p < 0.001 p = 0.506 p = 0.001
Kim et al19 2009 Retrospective 144.0 (72–345) ND 14, 10.0 7.0 (5–72) Safe and feasible
TLTG vs. OTG 137.0 (65–355) ND 45, 21.7 8.0 (2–34)
(139 vs. 207) p = 0.381 ND p = 0.005 p < 0.001
Kim et al18 2011 Retrospective 166.4 ± 47.5 ND 10, 11.1 7.9 ± 4.3 Safe and feasible
TLTG vs. LATG 158.5 ± 45.5 ND 4, 16.0 9.5 ± 7.5
(90 vs. 23) p = 0.461 ND p = 0.500 p = 0.198

LATG = laparoscopy-assisted total gastrectomy; ND = not described in the article; OTG = open total gastrectomy; SD = standard deviation; TLTG = totally laparoscopic total gastrectomy.

4. Discussion

At present, low invasive treatments for gastric cancer include endoscopic procedures (such as endoscopic mucosal resection and endoscopic submucosal dissection) and laparoscopic gastrectomy (LG).39 As is the trend for laparoscopic surgery for various organs,40 ;  41 laparoscopic-assisted surgery has been switched to totally laparoscopic surgery in LG to allow greater magnification, a wider view, and practical use of more refined surgical techniques. As the noninferiority of LATG to OTG has been demonstrated,42; 43 ;  44 many reports about TLTG, as cited in this review, have been published. The critical point in TLTG is intracorporeal EJS techniques, if special techniques such as combined resection of adjacent organs45 and extended lymphadenectomy25 ;  46 are not taken into consideration.47 In this review, EJS techniques using CSs were significantly more associated with leakage and stenosis of the EJS, as compared with those using LSs. When SST and DST methods were used for esophageal cancer and colorectal cancer surgery, anastomotic stenosis was considered a relatively frequent complication and occurred in 2.4–10.0% of patients.48; 49 ;  50 As EJS is performed using longitudinally long devices in LS methods, a wider diameter of anastomosis can be secured, although there are concerns about the possible onset of gastroesophageal reflux disease owing to the disruption of the esophageal hiatus, slippage of the EJS site into the mediastinum, and severe consequences of leakage of the EJS.14; 34 ;  51 By contrast, the HS method is a simple and low-cost surgical technique, although currently not mainstream.17 ;  52 According to the time for anastomosis, it may not be a good comparative item in this study, as the devices used and the surgeons' experience and surgical technique cannot be at the same level. The current major EJS techniques of TLTG are obviously CS and LS methods, and which one is superior to the other remains to be determined. To correctly answer the question, analysis of clinical results from well-planned RCTs of EJS techniques in TLTG between CS and LS methods is warranted.

Based on the short-term results of comparative studies of TLTG versus OTG or LATG, it has been concluded that TLTG is, at present, safe and feasible.16; 17; 18 ;  19 The short-term results of TLTG from the 25 articles cited in the present review are substantially favorable and almost equivalent to the short-term results of OTG.30; 31; 32; 33; 34; 35; 36; 37 ;  38 Topal et al16 have suggested that the concomitance of splenectomy (p = 0.006) and the number of dissected lymph nodes (p = 0.042) are surgical factors related to the onset of postoperative complications of TLTG. Surgeons with only recent experience in performing TLTG more often encounter complications (p = 0.032), 16 and so even surgeons who are well experienced in LG should not readily switch to TLTG for advanced gastric cancer.

Regarding the long-term oncological prognosis investigated in this review, TLTG produced extremely satisfying results in patients with early gastric cancer and without metastases to lymph nodes.29 ;  35 However, the global effectiveness of LADG has been demonstrated only for early gastric cancer,3 ;  5 and therefore close attention should be paid to the long-term oncological results of LATG and TLTG in Japan. Most of the articles on TLTG were relatively new, and only a few articles included long-term results.17 ;  23 In addition, the disease stages of cases included in the survey varied widely, and variable prognostic factors specific to advanced gastric cancer, such as peritoneal dissemination, were not taken into consideration at all, and thus the data used in this review were insufficient for accurate analysis of the long-term oncological prognosis.36 In the future, long-term oncological effectiveness or noninferiority of TLTG for early gastric cancer should be demonstrated based on RCTs using the same method as that used for LADG.

5. Conclusion

We investigated various EJS techniques in TLTG, as well as short-term results, long-term oncological results, and comparative study results of TLTG. At present, TLTG is believed to be a safe and feasible surgical technique for surgeons with a steep learning curve, comparable to OTG and LATG.52; 53 ;  54 However, because of the difficulty of TLTG when applied to advanced gastric cancer requiring combined resection of adjacent organs and extended lymphadenectomy and its association with an increased risk of serious perioperative complications,25 the risks and benefits should be weighed prior to performing TLTG. The potential effects of TLTG on the long-term oncological prognosis have not been determined and warrant further investigation.55 For EJS techniques, leakage and stenosis of the EJS may occur more frequently in CS methods than in LS methods. Although CS and LS methods for EJS are the major techniques used in TLTG at present, further research is necessary to establish which reconstruction techniques are suitable for EJS.

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