The authors have declared that no competing interests exist.
Conceived and designed the experiments: ZX BW. Performed the experiments: WW X. Zhang. Analyzed the data: WW CS. Contributed reagents/materials/analysis tools: X. Zhi. Wrote the paper: WW.
To expand the current knowledge on the feasibility and safety of laparoscopic total gastrectomy (LTG) for gastric cancer in comparison with open total gastrectomy (OTG).
Additional studies comparing laparoscopic versus open total gastric resection have been published, and it is necessary to update the meta-analysis of this subject.
Original articles compared LTG and OTG for gastric cancer, which published in English from January 1990 to July 2013 were searched in PubMed, Embase, and Web of Knowledge by two reviewers independently. Operative time, blood loss, harvested lymph nodes, proximal resection margin, analgesic medication, first flatus day, first oral intake, postoperative hospital stay, postoperative complications, hospital mortality, 5-year overall survival (OS) and disease-free survival (DFS) were compared using STATA version 10.1.
17 studies were selected in this analysis, which included a total of 2313 patients (955 in LTG and 1358 in OTG). LTG showed longer operative time, less blood loss, fewer analgesic uses, earlier passage of flatus, quicker resumption of oral intake, earlier hospital discharge, and reduced postoperative morbidity. The number of harvested lymph nodes, proximal resection margin, hospital mortality, 5-year OS and DFS were similar.
LTG had the benefits of less blood loss, less postoperative pain, quicker bowel function recovery, shorter hospital stay and lower postoperative morbidity, at the price of longer operative time. There were no statistical differences in lymph node dissection, resection margin, hospital mortality, and long-term outcomes, which indicated the similar oncological safety with OTG. A positive trend was indicated towards LTG. So LTG can be performed as an alternative to OTG by the experienced surgeons in high-volume centers. Whereas, due to the relative small sample size of long-term outcomes and lack of randomized control trials, more studies are required.
Since the first laparoscopic gastrectomy for gastric caner was performed by Japanese surgeons in 1991
Literatures that published in English from January 1990 to July 2013 were searched in the following database: PubMed, Embase, and Web of Knowledge. The keywords “laparoscopic”, “total gastrectomy”, “gastric cancer”, “randomized controlled trial”, “prospective study”, and “comparative study” were used. Then, all titles, abstracts, or related citations were scanned and reviewed.
Inclusion criteria were described as follow: (1) studies that compared LTG with OTG for gastric cancer; (2) LTG that was performed with either laparoscopy-assisted or total laparoscopic approach; (3) any type of comparative study; (4) studies with any size.
Exclusion criteria were used as follows: (1) studies including other types of gastric resection, unless the data were presented separately; (2) studies in which <3 interested indexes were reported, or the indexes were difficult to calculate from the results; (3) overlapping data.
Newcastle–Ottawa Quality Assessment Scale for cohort studies (NOS) (
(1) Representativeness of the exposed cohort |
(a) Truly representative of the average |
(b) Somewhat representative of the average |
(c) Selected group of users (e.g. nurses, volunteers) |
(d) No description of the derivation of the cohort |
(2) Selection of the non-exposed cohort |
(a) Drawn from the same community as the exposed cohort (1 star) |
(b) Drawn from a different source |
(c) No description of the derivation of the non-exposed cohort |
(3) Ascertainment of exposure |
(a) Secure record (e.g. surgical records) (1 star) |
(b) Structured interview (1 star) |
(c) Written self-report |
(d) No description |
(4) Demonstration that outcome of interest was not present at start of study |
(a) Yes (1 star)o |
(b) No |
(1) Comparability of cohorts on the basis of the design or analysis |
(a) Study controls for |
(b) Study controls for any additional factor (1 star) (ASA, tumor size, stage etc.) |
(1) Assessment of outcome |
(a) Independent blind assessment (1 star) |
(b) Record linkage (1 star) |
(c) Self-report |
(d) No description |
(2) Was follow-up long enough for outcomes to occur? |
(a) Yes ( |
(b) No |
(3) Adequacy of follow-up of cohorts |
(a) Complete follow-up – all subjects accounted for (1 star) |
(b) Subjects lost to follow-up unlikely to introduce bias – small number lost |
(c) Follow-up rate |
(d) No statement |
*A study can be awarded a maximum of one star for each numbered item within the Selection and Outcome categories. A maximum of two stars can be given for Comparability. Underlined and quoted phrases are provided in the scale to allow for adjustment to particular studies. Italicized phrases indicate our interpretation of the question relevant to this study.
GC, gastric cancer; ASA, American Society of Anesthesiology classification; BMI, body mass index.
selection | comparability | outcome | |||||||
References | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | score |
Dulucq et al |
* | * | * | * | * | * | * | 7 | |
Usui et al |
* | * | * | * | ** | * | 7 | ||
Mochiki et al |
* | * | * | * | * | * | * | 7 | |
Kim et al |
* | * | * | * | * | * | 6 | ||
Topal et al |
* | * | * | * | ** | * | 7 | ||
Kawamura et al |
* | * | * | * | ** | 6 | |||
Sakuramoto et al |
* | * | * | * | * | * | * | * | 8 |
Du et al |
* | * | * | * | ** | * | * | * | 9 |
Kim et al |
* | * | * | * | ** | * | 7 | ||
Eom et al |
* | * | * | * | * | * | * | * | 8 |
Amanda K. et al |
* | * | * | * | * | 5 | |||
Kunisaki et al |
* | * | * | * | ** | * | * | 7 | |
Siani et al |
* | * | * | * | * | * | 6 | ||
Jeong et al |
* | * | * | * | ** | * | 7 | ||
Guan et al |
* | * | * | * | * | * | 6 | ||
Lee et al |
* | * | * | * | ** | * | * | * | 9 |
Kim et al |
* | * | * | * | ** | * | 7 | ||
Bo et al |
* | * | * | * | ** | * | * | * | 9 |
The data was extracted and critically appraised independently by two authors. We extracted operative time, blood loss, number of harvested lymph nodes, and proximal resection margin to assess the effectiveness of the procedures. The analgesic medication, first flatus day, first oral intake and hospital stay were used to compare the postoperative recovery of the procedures. The postoperative complications including wound infection, anastomotic leakage, anastomotic stenosis, postoperative ileus, pneumonia, pancreatitis, intra-abdominal abscess and adhesive bowel obstruction were compared. The hospital mortality, 5-year overall survival (OS) and disease free survival (DFS) were used to estimate the postoperative safety of LTG.
We used weighted mean differences (WMD) with 95% confidence intervals (CI) to analyze continuous variables presented in the same scale (i.e., operative time, blood loss, postoperative hospital stay). When a study reported a range instead of standard deviation (SD), a quarter of the range amplitude was equivalent to the estimated SD
The electronic search strategy identified 195 articles that mentioned laparoscopic gastrectomy and open gastrectomy for gastric cancer. After screening the titles, abstracts, full texts, or a combination of these, we selected articles based on the inclusion and exclusion criteria (
Sample size | ||||||
References | Year | Country | Journal | LTG | OTG | Type of the study |
Dulucq et al |
2005 | France | Surg Endosc | 8 | 11 | Prospective Cohort study |
Usui et al |
2005 | Japan | SURG LAPARO ENDO PER | 20 | 19 | Cohort study |
Mochiki et al |
2008 | Japan | Surg Endosc | 20 | 18 | Cohort study |
Kim et al |
2008 | South Korea | J LAPAROENDOSC ADV S | 27 | 33 | Prospective Cohort study |
Topal et al |
2008 | Belgium | Surg Endosc | 38 | 22 | Prospective Cohort study |
Kawamura et al |
2009 | Japan | World J Surg | 46 | 35 | Cohort study |
Sakuramoto et al |
2009 | Japan | Surg Endosc | 30 | 44 | Cohort study |
Du et al |
2010 | China | Hepato-Gastroenterology | 82 | 94 | Retrospective Cohort study |
Kim et al |
2011 | South Korea | J Korean Surg Soc | 63 | 127 | Retrospective Cohort study |
Eom et al |
2012 | South Korea | Surg Endosc | 100 | 348 | Case-control Cohort study |
Kunisaki et al |
2012 | Japan | Surg Endosc | 27 | 30 | Prospective Cohort study |
Siani et al |
2012 | Italy | MINERVA CHIR | 25 | 25 | Retrospective Cohort study |
Jeong et al |
2012 | South Korea | J Am Coll Surg | 122 | 122 | Prospective Cohort study |
Guan et al |
2012 | China | Surg Endosc | 41 | 56 | Case-control Cohort study |
Lee et al |
2013 | South Korea | Surg Endosc | 50 | 50 | Prospective Cohort study |
Kim et al |
2013 | South Korea | J LAPAROENDOSC ADV S | 139 | 207 | Prospective Cohort study |
Bo et al |
2013 | China | J Gastrointest Surg | 117 | 117 | Case-control Cohort study |
LTG, laparoscopic total gastrectomy; OTG, open total gastrectomy.
All the articles were published between 2005 and 2013. A total of 2313 patients were involved in the meta-analysis, which contained 955 people undergoing LTG and 1358 people receiving OTG. Fourteen studies were published by Asian investigators, and only three were reported by the western scholars. This result can be explained by the high incidence of gastric cancer in eastern countries. And the conclusions might bias to the Asians. As shown in
References | Approach | Age (years) | Male(No.) | BMI (kg/m2) | Tumor diameters (cm) | Lymph nodes dissection | Population | ASA (No.) | Stage (No.) | |||||
1 | 2 | 3 | I | II | III | IV | ||||||||
Dulucq et al |
LTG | 75±8 | 3 | 5.5±2 | D1 | EGC+AGC | ||||||||
OTG | 67±14 | 5 | 6.1±0.4 | |||||||||||
Usui et al |
LTG | 66.0±10.4 | 13 | 21.3±3.1 | D1 | EGC | ||||||||
OTG | 66.2±10.2 | 14 | 22.1±2.4 | |||||||||||
Mochiki et al |
LTG | 66±2.4 | 16 | 3.6±0.5 | D1 | EGC | ||||||||
OTG | 63±2.2 | 16 | 5.7±0.8 | |||||||||||
Kim et al |
LTG | 57.3±14.2 | 16 | 22.6±3.1 | D1, D2 | EGC+AGC | ||||||||
OTG | 61.6±9.2 | 23 | 22.4±2.1 | |||||||||||
Topal et al |
LTG | 68.0±12 | 23 | 24.0±3 | 4.7±4.3 | D2 | EGC+AGC | 17 | 7 | 10 | 4 | |||
OTG | 69.0±12 | 17 | 24.0±3 | 3.0±4.3 | 7 | 7 | 6 | 2 | ||||||
Kawamura et al |
LTG | 64.0±10.4 | 36 | 22.8±3.0 | D2 | EGC | 15 | 27 | 4 | |||||
OTG | 65.2±10.7 | 25 | 22.9±2.4 | 14 | 15 | 6 | ||||||||
Sakuramoto et al |
LTG | 63.7±9.2 | 12 | 21.9±2.7 | 4.0±2.9 | D1, D2 | EGC+AGC | 9 | 20 | 1 | 25 | 2 | 3 | 0 |
OTG | 67.2±9.9 | 10 | 22.5±3.6 | 6.1±3.7 | 8 | 28 | 8 | 15 | 17 | 12 | 0 | |||
Du et al |
LTG | 60.4±18.5 | 54 | 22.3±2.6 | 5.4±1.4 | D2 | AGC | 3 | 36 | 42 | 0 | |||
OTG | 57.8±17.2 | 61 | 22.5±2.4 | 5.9±1.9 | 6 | 31 | 57 | 0 | ||||||
Kim et al |
LTG | 55.9±12.2 | 43 | 22.7±2.5 | 3.8±2.1 | D2 | EGC | 45 | 15 | 3 | ||||
OTG | 57.3±11.1 | 81 | 23.0±2.9 | 3.9±2.7 | 86 | 39 | 2 | |||||||
Eom et al |
LTG | 54.9±13.5 | 57 | 22.7±2.8 | 4.3±2.9 | D2 | EGC | 100 | 0 | 0 | 0 | |||
OTG | 58.7±11.5 | 254 | 23.8±2.9 | 4.4±3.0 | 348 | 0 | 0 | 0 | ||||||
Kunisaki et al |
LTG | 67.4±11.0 | 21 | 23.5±2.5 | D1, D2 | EGC+AGC | 11 | 14 | 2 | |||||
OTG | 67.1±6.6 | 20 | 24.3±4.3 | 9 | 16 | 5 | ||||||||
Siani et al |
LTG | 65±8.5 | 15 | D1, D2 | EGC+AGC | 6 | 5 | 14 | 0 | |||||
OTG | 66±7.8 | 18 | 4 | 5 | 16 | 0 | ||||||||
Jeong et al |
LTG | 63.2±11.2 | 89 | 23.1±3.4 | D1, D2 | EGC+AGC | 33 | 80 | 9 | 105 | 13 | 4 | 0 | |
OTG | 62.6±11.7 | 93 | 23.5±3.2 | 43 | 67 | 12 | 99 | 16 | 7 | 0 | ||||
Guan et al |
LTG | 60.7±9.1 | 33 | D2 | EGC+AGC | 18 | 20 | 3 | 0 | |||||
OTG | 57.8±9.9 | 40 | 25 | 25 | 6 | 0 | ||||||||
Lee et al |
LTG | 50.6±22.1 | 32 | 23.2±3.7 | D2 | EGC+AGC | 85 | 46 | 8 | 24 | 13 | 9 | 4 | |
OTG | 51.0±22.6 | 32 | 23.0±3.4 | 137 | 52 | 18 | 24 | 13 | 9 | 4 | ||||
Kim et al |
LTG | 58.0±13.5 | 86 | 23.6±4.7 | 3.2±3.7 | D2 | AGC | 0 | 0 | 139 | 0 | |||
OTG | 56.0±13.3 | 134 | 24.1±4.6 | 4.0±5.4 | 0 | 0 | 207 | 0 | ||||||
Bo et al |
LTG | 54.5±10.6 | 82 | 21.1±3.0 | D2 | AGC | 6 | 40 | 52 | 19 | ||||
OTG | 52.6±13.6 | 80 | 21.7±3.8 | 4 | 38 | 55 | 20 |
LTG, laparoscopic total gastrectomy; OTG, open total gastrectomy; EGC, early gastic cancer; AGC, advanced gastric cancer; BMI, body mass index; ASA, American Society of Anesthesiology classification.
D1 lymph node dissection of total gastrectomy, which requires the retrieval of lymph nodes along the left gastric artery and the common hepatic artery, around the celiac artery, was performed in three articles
There was a longer duration of operative time in the LTG group than that in the OTG group (WMD, 47.00; 95% CI, 31.67, 62.33;
The postoperative pain patients suffered was evaluated by counting the times of the analgesics use. Patients receiving the laparoscopic procedure used fewer analgesics (WMD, −2.46; 95% CI, −2.71, −2.22;
In the subcategory analysis of postoperative complications, patients in LTG group showed less wound infection (RR, 0.35; 95% CI, 0.20, 0.61;
Test for Overall Effect | Test for Heterogeneity | ||||
Items | RR 95% CI | ||||
Anastomotic leakage | 1.18 (0.61, 2.26) | 0.48 | 0.629 | <0.1% | 0.656 |
Anastomotic stenosis | 1.29 (0.72, 2.30) | 0.85 | 0.394 | <0.1% | 0.839 |
Wound infection | 0.35 (0.20, 0.61) | 3.70 | <0.1% | 0.822 | |
Postoperative ileus | 0.71 (0.28, 1.78) | 0.73 | 0.463 | <0.1% | 0.949 |
Postoperative pneumonia | 0.59 (0.29, 1.18) | 1.50 | 0.133 | <0.1% | 0.955 |
Pancreatitis | 0.56 (0.18, 1.70) | 1.02 | 0.310 | <0.1% | 0.968 |
Intra-abdominal abscess | 0.55 (0.29, 1.03) | 1.87 | 0.062 | 7.4% | 0.369 |
Adhesive bowel obstructions | 0.73 (0.36, 1.48) | 0.86 | 0.388 | <0.1% | 0.681 |
CI, confidence interval; LTG, laparoscopic total gastrectomy; OTG, open total gastrectomy; RR, relative risks; WMD, weighed mean difference; data in bold, significant
According to Cochrane Handbook, when a meta-analysis contains fewer than ten studies, meta-regression should generally not be considered. Therefore, we just examined the outcome variables with high heterogeneity, which included more than ten studies, in a meta-regression model. The analyses indicated that study quality, country of patients, sample size, and lymph nodes dissection were significant sources of heterogeneity (
Variable | Coefficient | Standard error | 95% CI | |
Study quality | 24.784 | 27.306 | 0.388 | −36.986 to 86.553 |
Year of publication | −39.016 | 26.020 | 0.168 | −97.877 to 19.846 |
Country of patients | −31.149 | 35.156 | 0.399 | −110.678 to 48.379 |
Sample size | 7.435 | 30.133 | 0.811 | −60.732 to 75.601 |
Stage of gastric cancer | 15.702 | 18.197 | 0.411 | −25.463 to 56.868 |
Lymph node dissection | 34.537 | 21.836 | 0.148 | −14.861 to 83.936 |
Study quality | −118.080 | 58.824 | 0.091 | −262.017 to 25.858 |
Year of publication | −44.325 | 61.162 | 0.496 | −193.983 to 105.332 |
Country of patients | −2.482 | 76.190 | 0.975 | −188.911 to 183.947 |
Sample size | 220.280 | 56.992 | 0.008 | 80.827 to 359.734 |
Stage of gastric cancer | 77.672 | 43.096 | 0.122 | −27.780 to 183.125 |
Lymph node dissection | −61.135 | 41.344 | 0.190 | −162.300 to 40.030 |
Study quality | 4.231 | 1.620 | 0.031 | 0.496 to 7.965 |
Year of publication | −0.933 | 1.687 | 0.595 | −4.823 to 2.956 |
Country of patients | −1.116 | 3.720 | 0.772 | −9.694 to 7.462 |
Sample size | −1.677 | 1.963 | 0.418 | −6.203 to 2.850 |
Stage of gastric cancer | 1.402 | 1.251 | 0.295 | −1.482 to 4.287 |
Lymph node dissection | 3.421 | 1.763 | 0.088 | −0.643 to 7.486 |
Study quality | −0.450 | 0.435 | 0.336 | −1.480 to 0.579 |
Year of publication | 0.025 | 0.439 | 0.956 | −1.013 to 1.063 |
Country of patients | −1.169 | 0.621 | 0.102 | −2.637 to 0.299 |
Sample size | 0.109 | 0.437 | 0.810 | −0.925 to 1.143 |
Stage of gastric cancer | 0.198 | 0.334 | 0.572 | −0.592 to 0.988 |
Lymph node dissection | −0.107 | 0.336 | 0.759 | −0.901 to 0.687 |
Study quality | −2.116 | 0.659 | 0.015 | −3.675 to −0.557 |
Year of publication | 0.224 | 0.911 | 0.813 | −1.931 to 2.379 |
Country of patients | −2.529 | 0.942 | 0.031 | −4.757 to −0.301 |
Sample size | 2.744 | 0.817 | 0.012 | 0.811 to 4.676 |
Stage of gastric cancer | 0.036 | 0.624 | 0.956 | −1.440 to 1.512 |
Lymph node dissection | 2.480 | 0.715 | 0.010 | 0.790 to 4.170 |
Data in bold, significant
As shown in
Sample Size | Test for Overall Effect | Test for Heterogeneity | ||||||
Items | n |
LTG | OTG | RR or WMD 95% CI | ||||
EGC | 5 | 249 | 547 | 29.06 (4.32, 53.79) | 2.30 | 94.0% | ||
AGC | 3 | 338 | 418 | 39.93 (7.46, 72.41) | 2.41 | 92.4% | ||
<8 scores | 12 | 576 | 705 | 36.15 (19.99, 52.32) | 4.38 | 91.4% | ||
≥8 scores | 5 | 379 | 653 | 68.38 (52.40, 84.37) | 8.38 | 70.4% | ||
<50 cases | 10 | 282 | 293 | 42.97 (21.69, 64.25) | 3.96 | 91.6% | ||
≥50 cases | 7 | 673 | 1065 | 52.34 (29.69, 75.08) | 4.51 | 93.7% | ||
Western patients | 3 | 71 | 58 | 28.02 (17.94, 38.09) | 5.45 | <0.1% | 0.627 | |
EGC | 4 | 149 | 199 | −242.79 (−445.19, −40.39) | 2.35 | 97.8% | ||
AGC | 2 | 199 | 211 | −169.87 (−195.48, −144.27) | 13.00 | <0.1% | 0.417 | |
<8 scores | 10 | 410 | 465 | −189.98 (−291.10, −88.86) | 3.68 | 97.0% | ||
≥8 scores | 4 | 279 | 305 | −152.87 (−240.92, −64.82) | 3.40 | 93.0% | ||
<50 cases | 9 | 255 | 260 | −240.34 (−320.75, −159.93) | 5.86 | 92.7% | ||
≥50 cases | 5 | 434 | 510 | −82.46 (−166.23, 1.31) | 1.93 | 0.054 | 94.9% | |
Western patients | 3 | 71 | 58 | −150.10 (−281.84, −18.37) | 2.23 | 77.4% | ||
EGC | 5 | 249 | 547 | 1.76 (−3.95, 7.46) | 0.60 | 0.546 | 87.0% | |
AGC | 3 | 338 | 418 | 0.86 (−1.44, 3.16) | 0.73 | 0.463 | 46.8% | 0.152 |
<8 scores | 11 | 538 | 683 | 1.75 (−1.72, 5.22) | 0.99 | 0.323 | 79.6% | |
≥8 scores | 5 | 379 | 653 | 2.56 (0.52, 4.59) | 2.46 | <0.1% | 0.640 | |
<50 cases | 9 | 244 | 271 | 3.44 (−0.38, 7.26) | 1.76 | 0.078 | 71.6% | |
≥50 cases | 7 | 673 | 1065 | 1.15 (−1.06, 3.36) | 1.02 | 0.308 | 43.9% | |
Western patients | 2 | 33 | 36 | 0.56 (−6.16, 7.28) | 0.16 | 0.870 | 42.0% | 0.189 |
EGC | 2 | 163 | 475 | −0.17 (−0.35, 0.01) | 1.85 | 0.064 | <0.1% | 0.793 |
AGC | 2 | 256 | 324 | −0.04 (−0.97, 0.89) | 0.09 | 0.932 | 64.3% | |
<8 scores | 3 | 243 | 390 | −0.04 (−0.32, 0.24) | 0.29 | 0.769 | 37.4% | 0.203 |
≥8 scores | 2 | 217 | 465 | −0.008 (−0.69, 0.67) | 0.02 | 0.982 | 80.0% | |
<50 cases | 1 | 41 | 56 | / | / | / | / | / |
≥50 cases | 4 | 419 | 799 | −0.19 (−0.69, 0.32) | 0.74 | 0.462 | 67.9% | |
Western patients | 0 | / | / | / | / | / | / | / |
EGC | 3 | 129 | 181 | −1.87 (−2.84, −0.91) | 3.80 | <0.1% | 0.519 | |
AGC | 2 | 256 | 324 | −2.50 (−2.75, −2.24) | 19.26 | <0.1% | 0.491 | |
<8 scores | 4 | 268 | 388 | −1.83 (−2.77, −0.89) | 3.81 | <0.1% | 0.691 | |
≥8 scores | 2 | 147 | 161 | −2.51 (−2.76, −2.26) | 19.38 | <0.1% | 0.219 | |
<50 cases | 3 | 98 | 96 | −2.44 (−3.81, −1.07) | 3.49 | 32.4% | 0.228 | |
≥50 cases | 3 | 419 | 451 | −2.47 (−2.71, −2.22) | 19.40 | <0.1% | 0.390 | |
Western patients | 0 | / | / | / | / | / | / | / |
EGC | 3 | 129 | 181 | −0.58 (−1.04, −0.12) | 2.49 | 65.1% | ||
AGC | 3 | 338 | 418 | −1.10 (−1.78, −0.42) | 3.17 | 93.6% | ||
<8 scores | 10 | 518 | 665 | −0.72 (−1.04, −0.41) | 4.56 | 85.7% | ||
≥8 scores | 4 | 279 | 305 | −0.94 (−1.64, −0.23) | 2.61 | 91.6% | ||
<50 cases | 8 | 224 | 253 | −0.87 (−1.28, −0.45) | 4.11 | 78.5% | ||
≥50 cases | 6 | 513 | 717 | −0.73 (−1.22, −0.25) | 2.97 | 94.5% | ||
Western patients | 2 | 33 | 36 | −1.75 (−2.33, −1.17) | 5.89 | 46.5% | 0.172 | |
EGC | 2 | 83 | 146 | −2.17 (−3.93, −0.41) | 2.41 | 84.3% | ||
AGC | 2 | 256 | 324 | −0.85 (−1.27, −0.43) | 3.94 | 14.7% | 0.279 | |
<8 scores | 5 | 385 | 531 | −1.30 (−2.23, −0.36) | 2.71 | 82.4% | ||
≥8 scores | 3 | 197 | 211 | −0.91 (−1.25, −0.57) | 5.28 | <0.1% | 0.703 | |
<50 cases | 3 | 91 | 119 | −1.58 (−2.63, −0.53) | 2.95 | 86.2% | ||
≥50 cases | 5 | 491 | 623 | −0.84 (−1.38, −0.30) | 3.03 | 49.0% | ||
Western patients | 0 | / | / | / | / | / | / | / |
EGC | 5 | 249 | 547 | −4.87 (−8.60, −1.14) | 2.56 | 93.4% | ||
AGC | 2 | 256 | 324 | −3.23 (−3.77, −2.68) | 11.64 | 54.3% | 0.139 | |
<8 scores | 11 | 538 | 683 | −3.46 (−5.31, −1.62) | 3.68 | 88.6% | ||
≥8 scores | 4 | 297 | 559 | −3.26 (−3.79, −2.74) | 12.23 | <0.1% | 0.534 | |
<50 cases | 9 | 244 | 271 | −4.65 (−6.52, −2.75) | 4.80 | 84.9% | ||
≥50 cases | 6 | 591 | 971 | −1.70 (−3.08, −0.31) | 2.40 | 72.4% | ||
Western patients | 2 | 33 | 36 | −4.16 (−5.48, −2.85) | 6.21 | 6.7% | 0.300 | |
EGC | 4 | 229 | 538 | 0.94 (0.69, 1.28) | 0.40 | 0.689 | 38.8% | 0.179 |
AGC | 3 | 338 | 418 | 0.50 (0.35, 0.73) | 3.68 | <0.1% | 0.523 | |
<8 scores | 11 | 556 | 686 | 0.78 (0.61, 0.99) | 2.03 | 32.5% | 0.139 | |
≥8 scores | 5 | 379 | 653 | 0.79 (0.61, 1.03) | 1.78 | 0.076 | 46.6% | 0.112 |
<50 cases | 9 | 262 | 274 | 0.79 (0.55, 1.13) | 1.30 | 0.192 | 3.2% | 0.408 |
≥50 cases | 7 | 673 | 1065 | 0.75 (0.54, 1.04) | 1.72 | 0.085 | 57.3% | |
Western patients | 3 | 71 | 58 | 0.84 (0.48, 1.47) | 0.61 | 0.540 | <0.1% | 0.675 |
EGC | 3 | 166 | 401 | 1.60 (0.27, 9.64) | 0.51 | 0.609 | <0.1% | 0.665 |
AGC | 2 | 221 | 301 | 0.23 (0.01, 4.70) | 0.96 | 0.339 | / | / |
<8 scores | 6 | 360 | 418 | 1.42 (0.31, 6.46) | 0.46 | 0.649 | <0.1% | 0.674 |
≥8 scores | 4 | 262 | 536 | 0.57 (0.11, 3.09) | 0.65 | 0.513 | <0.1% | 0.392 |
<50 cases | 5 | 129 | 133 | 1.10 (0.15, 8.09) | 0.10 | 0.923 | <0.1% | 0.420 |
≥50 cases | 5 | 493 | 821 | 0.88 (0.23, 3.28) | 0.20 | 0.843 | <0.1% | 0.528 |
Western patients | 3 | 71 | 58 | 0.44 (0.02, 9.69) | 0.52 | 0.606 | / | / |
CI, confidence interval; LTG, laparoscopic total gastrectomy; OTG, open total gastrectomy; RR, relative risks; WMD, weighed mean difference; EGC, early gastric cancer; AGC; advanced gastric cancer; data in bold, significant
Number of comparisons.
We used the funnel plots and Egger's linear regression test to detect publication bias for each result. When the number of studies was small, there was a limitation in this test. So the funnel plots of proximal resection margin, analgesic medication, hospital mortality, 5-year OS and DFS, were not showed. Eventually, seven funnel plots were constructed for the outcomes we most cared about. The symmetry of most outcomes on the whole was observed. All the outcomes showed no significant publication bias (P>0.05) except operative time (t = 2.93;
A, operative time; B, blood loss; C, harvested lymph nodes; D, first flatus day; E, first oral intake; F, hospital stay; G, postoperative complications.
According to “Gastric Cancer Treatment Guidelines in Japan, 2010”, total gastrectomy is used in radical resection of proximal and middle third gastric cancer. Laparoscopic surgery is recommended as a treatment for early gastric cancer and clinical research. Patient's preference and surgeon's suggestion may affect the choice of operation type. And cosmetic result, cost, recovery and pain are the major factors the patients care about
The randomized controlled trials (RCTs) are our first choice for the high quality of the outcomes. But no RCTs focusing on this subject were found. Eighteen non-randomized comparative cohort studies were selected. In order to get convincible results from articles, NOS was used to assess the quality of the studies and one low-quality study was excluded. Then, we compared the clinical characteristics between the two groups and no statistical differences were found in age, sex, ASA and pTNM stages except BMI which was lower in LTG groups. This finding indicated that selection bias might exist among the studies. Surgeons might prefer to perform LTG on thinner people and our conclusion might bias to laparoscopic procedures. Considering that more than half of the articles reported the gastrectomy with D2 dissection, which was preferred by Asian surgeons, the fact that most studies we collected were from eastern countries was reasonable. Compared with patients in western countries, Asian patients are younger, slimmer and healthier
Due to the lack of tactile sensation, narrow operating field, complicated vascular structure in the splenic hilum, and the advanced techniques for systemic lymph node dissection, LTG was regarded as a time-consuming procedure. Haverkamp
In spite of the longer operative time, a significant decrease of blood loss for laparoscopic approach was found compared with open procedure, which indicated fewer transfusions during the operation. The enlarged laparoscopic surgical field with the advantage of better vessel exposing and identifying contributed to this outcome, which is also attributed to the use of special instruments, such as the ultrasonic scalpel and ligatures
The length of resection margin can influence the rate of tumor-free margins. Thus, whether LTG can resect the similar length as OTG is very important for the oncological safety. Because the resection of proximal stomach is more difficult than the duodenal resection, most of the involved articles just provided the length of proximal resection margin. No statistical difference of this subject was found, which indicated the similar ability of proximal resection between LTG and OTG. This finding can also explain the similar positive rate of resection margin reported by three studies
The results were significantly favoring for LTG in the use of analgesics, first flatus day, first oral intake and the length of hospital stay. In this analysis, the times of the analgesics use were extracted to evaluate the postoperative pain, because pain-feeling is hard to measure for its subjectivity. Less pain during recovery is most likely caused by the minimal invasiveness of LTG and it suggests earlier recovery and better quality of life. Earlier passage of flatus represents a quicker recovery of bowel function, which has a direct impact on earlier resumption of oral intake and earlier discharge from hospital. Minimal gastrointestinal interference and the use of small incision can explain all the advantages above, and can also decrease surgical stress, therefore reduce the generalized inflammatory reaction, leading to a reduction of postoperative morbidity.
The extent of lymph node dissection is a critical factor for oncological adequacy. D1 dissection is now accepted as a standard treatment for selected patients with early gastric cancer. Debate about whether D2 dissection for curable advanced gastric cancer is superior to D1 dissection still exists. The more complexity and invasiveness of D2 dissection are thought to increase the postoperative complications and mortality. Whereas, D2 dissection is possible to remove more positive nodes than D1 dissection, which is necessary to minimize stage migration
The number of harvested lymph nodes is used to evaluate the oncological adequacy. According to UICC (Union for International Cancer Control), the removal of at least fifteen lymph nodes is beneficial for pathological examination. The mean number of lymph nodes retrieved by LTG was adequate in all studies. In Haverkamp
The postoperative morbidity is an important outcome to assess the safety of the operation type. In the subcategory analysis, reduced wound infection in LTG group was found due to the scattered trocar incisions and contractible sample-extraction incision. The same technique of digestive reconstruction in both procedures could explain the similar incidence of anastomotic leakage and stenosis. The minimal invasiveness of laparoscopic surgery could reduce the intervention to microenvironment of abdominal cavity and injury of intestinal serous membrane, which was thought being able to decrease the occurrence of postoperative ileus, pneumonia, pancreatitis, intra-abdominal abscess and adhesive bowel obstructions. In our analysis, we did not observe any statistical difference in these aspects, but a favorable trend in LTG was found. The relative small sample size in the subcategory might be the reason. When we pooled the data together, the patients undergoing LTG were associated with a significant reduction of total postoperative complications. And the same result was also found in the subgroup of D2 dissection. But in the other subgroups, only the studies of AGC or articles with <8 scores showed the fewer postoperative complications in LTG groups. Considering that low heterogeneity was found in the overall result and the rest subgroups showed a tendency towards LTG, this result can be explained by a relative small sample size in subgroups, which did not have enough volume to show the statistical difference. Therefore, the lower postoperative morbidity in LTG group should be reliable.
Our analysis revealed that there was no significant difference in hospital mortality between the two groups. And in the subgroup of D2 dissection, the same conclusion was found. These suggested the equivalent short-term prognosis between LTG and OTG. Long-term outcome is the most important factor used for evaluating the oncological safety of one surgery. The majority of recurrences occurs during the first two years after surgery
In conclusion, with the less blood loss, quicker postoperative recovery, reduced postoperative morbidity, and similar oncological safety, LTG is a feasible and safe surgery for gastric cancer. LTG can be performed as an alternative to OTG for selected patients by experienced surgeons in high-volume centers. However, well-designed RCTs in multicenter and the comparative studies of long-term outcomes are still needed for further validation.
PRISMA Checklist.
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