International Journal of Surgery 53 (2018) 163–170

Contents lists available at ScienceDirect

International Journal of Surgery

journal homepage: www.elsevier.com/locate/ijsu

Review

Distal versus total gastrectomy for middle and lower-third gastric cancer: A T
systematic review and meta-analysis
Zhengyan Li, Bin Bai, Fengni Xie, Qingchuan Zhao∗
Department of Surgery, Xijing Hospital of Digestive Diseases, The Fourth Military Medical University, No. 127 Changle West Road, Xi'an 710032, China

A R T I C LE I N FO A B S T R A C T

Keywords: Background: The optimal resection extent for middle or lower-third gastric cancer still remains controversial.
Distal gastrectomy This study was aim to compare the safety and long-term prognosis of distal gastrectomy (DG) with total gas-
Total gastrectomy trectomy (TG) for middle and lower-third gastric cancer.
Gastric cancer Methods: Pubmed, EMBASE, the Cochrane Library, and Web of Science were searched from inception to October
Meta-analysis
2017 for comparative studies comparing DG with TG for middle or lower-third gastric cancer. We performed the
meta-analysis using RevMan 5.3 software.
Results: Overall, 11 comparative studies with 3554 patients, including 4 randomized controlled trials and 7
retrospective cohort studies, were analyzed. Compared with DG, TG showed a higher rate of overall post-
operative complication, anastomosis leakage, wound complication, peritoneal abscess, and mortality. There
were no significant differences between the two groups in rate of recurrence and cancer–related death. The 5-
year overall survival is better in the DG group than in the TG group, but no significant differences were found in
stage-specific analysis.
Conclusions: Compared with TG, DG is an optimal surgical procedure for middle or lower-third gastric cancer in
early and locally advanced stages with better short-term outcomes and comparable long-term prognosis under
the precondition of negative proximal resection margin.

1. Introduction
Gastric cancer is a worldwide health concern and is the second
leading cause of cancer-related deaths in China [1]. Surgical resection
with proper perigastric lymphadenectomy remains the cornerstone of
radical resection of potentially curable gastric cancer [2,3]. The extent
of gastrectomy for curative treatment of gastric cancer depends on the
comprehensive consideration of tumor location, tumor size and surgeon
experience [4].However, there still remains controversy for the choice
of optimal resection extent for gastric cancer involving the middle or
lower-third of the stomach. Some studies have recommended total
gastrectomy (TG) as the standard procedure because of its potential
advantage of improved long-term survival and lower the incidence of
gastric remnant cancer [5,6].However, some studies reported that distal
gastrectomy (DG) is superior to TG when intraoperative and short-term
outcomes and quality of life (QOL) were taken into consideration [7,8].
During the recent years, two meta-analyses [9,10] have been published
to compare the feasibility and safety between DG and TG for distal
gastric cancer, but conflicting results were found between these studies
for postoperative complication and survival outcomes. Meanwhile,
several included studies in previous meta-analyses did not state the
tumor location clearly and some cases with tumor located in the upper
third of the stomach may also be included in these meta-analyses. The
aforementioned problems may lower the persuasion of their article.
Moreover, a series of reports on DG versus TG for the treatment of
middle and lower-third gastric cancer have been published this year.
Therefore, it is necessary to carry out a comprehensive systematic re-
view and meta-analysis with more reasonable inclusion criteria by
pooling data from all of the currently available articles. The aim of this
study was to provide an updated meta-analysis with more sufficient
evidence to compare the safety and long-term prognosis of DG with TG
for middle and lower-third gastric cancer.

Abbreviations: OS, Overall survival; OR, odds risk; CI, Confidence interval; DG, Distal gastrectomy; TG, Total gastrectomy; LADG, laparoscopy-assisted distal gastrectomy; LATG,
laparoscopy-assisted total gastrectomy; PRM, Proximal resection margin; QoL, Quality of life; RCT, Randomized control trail; nRCT, Non-randomized control trail; WMD, Weighted mean
difference
∗
Corresponding author. Department of Digestive Surgery, Xijing Hospital of Digestive Diseases, The Fourth Military Medical University, No. 127 Changle West Road, Xian 710032,
China.
E-mail address: zhaoqc62@yahoo.com (Q. Zhao).

https://doi.org/10.1016/j.ijsu.2018.03.047
Received 25 January 2018; Received in revised form 7 February 2018; Accepted 23 March 2018
Available online 27 March 2018
1743-9191/ © 2018 IJS Publishing Group Ltd. Published by Elsevier Ltd. All rights reserved.
Z. Li et al.
Fig. 1. The PRISMA flow diagram of the meta-analysis.
2. Methods
2.1. Literature search
A systematic literature search of PubMed, EMBASE, the Cochrane
Library, and Web of Science published up until October 2017 was un-
dertaken with restriction to English. Search terms “gastric carcinoma”,
“gastric cancer”, “distal gastrectmoy”, “total gastrectomy”and “subtotal
gastrectomy” were used in combination with the Boolean operators
AND or OR. The reference lists of articles obtained were also reviewed
to find relevant literature. Two investigators performed the literature
search independently.
2.2. Study selection
Studies met all the following criteria were included for meta-ana-
lysis: (1) comparative studies that compared DG with TG in patients
with gastric cancer; (2) studies that reported at least one outcome of
interest, including postoperative complication, mortality, recurrence,
cancer-related death rate, and 5-year overall survival (OS) rate; (3)
tumor location should be clearly stated and restricted to middle or
lower-third of the stomach. Studies were excluded if they met any of the
following criteria: (1) studies such as reviews, comments, letters, case
reports or cohort studies including fewer than ten patients; (2) studies
included recurrent gastric cancer, gastrointestinal stromal tumors, or
benign gastric diseases; (3) studies published in language other than
English. We included the latest one if the same author or center pub-
lished more than one article.
164
International Journal of Surgery 53 (2018) 163–170
2.3. Data extraction and quality assessment
Data were extracted independently by 2 reviewers, and discrepancies
were adjudicated by a third reviewer.The following data were extracted
from each study: first author, publication year, country, study design,
study period, lymph node dissection, tumor stage, median follow-up,
postoperative morbidity (overall postoperative complications, wound
problem, anastomotic leakage, bleeding, peritoneal abscess, and mor-
tality), and long-term prognosis (recurrence, cancer–related death, 5-
year OS, and stage-specific survival outcome).Randomized control trails
(RCTs) were methodologically assessed by Jadad scale. Other studies
were methodologically assessed using the Newcastle–Ottawa Scale
(NOS), which has been widely used for the assessment of the quality of
non-randomized studies in meta-analyses [11].
2.4. Statistical analysis
The odds ratio (OR) was used to analyze the dichotomous variables.
The weighted mean difference (WMD) was used for continuous vari-
ables, and both were reported with 95% confidence intervals (CIs).
Statistical heterogeneity among studies was evaluated by using the
Cochran Q statistic and quantified by I2 statistics. Heterogeneity was
graded as low (I2 < 25%), moderate (I2 25% to 75%), or high
(I2 > 75%).Fixed-effects model was applied when heterogeneity was
low (I2 < 25%).Otherwise random-effects model was used. The results
were regarded as statistically significant at two-sided P < 0.05.The
data were collected and extracted using SPSS 21.0(SPSS Inc., Chicago
IL, USA).All statistical analyses for meta-analyses were performed using
the dedicated Cochrane tool of Review Manager software (RevMan
version 5.3; Cochrane Collaboration).
Z. Li et al. International Journal of Surgery 53 (2018) 163–170

Table 1
Characteristics of included studies.
Study Publication year Country Study Design Study period Patients Lymph node Tumor stage Median follow-up
dissection (months)
TG DG

Gouzi et al. [13] 1989 France Randomized control trail 1980–1985 76 93 NR NR NR

Robertson et al. [14] 1994 China Randomized control trail 1987–1991 25 29 NR T1-T4 28.5
Bozzetti et al. [15] 1997,1999 Italy Randomized control trail 1982–1993 304 320 NR NR 72
De Manzoni et al. [16] 2003 Italy Randomized control trail 1988–1998 40 77 D2 T3 39.7
Moghimi et al. [17] 2008 Iran Retrospective cohort study 2001–2006 35 31 D2 NR 20
Jang et al. [18] 2010 Korea Retrospective cohort study 1993–2005 178 148 D1,D2 I-IV NR
Lee et al. [19] 2010 Korea Retrospective cohort study 2000–2006 63 62 NR I-IV NR
Mocan et al. [20] 2013 Romania Retrospective cohort study 2002–2005 89 91 D1,D2 I-III NR
Ji et al. [21] 2017 China Retrospective cohort study 2005–2011 195 144 D1,D2 I-IV 41.8
Liu et al. [22] 2017 China Retrospective cohort study 2008–2015 105 1157 D1,D2 I-III 25.83
Li et al. [23] 2017 China Retrospective cohort study 2005–2014 146 146 D2 I-III 54

TG, total gastrectomy; DG, distal gastrectomy; NR, no reported.

3. Results Table 3
Newcastle-Ottawa Scale assessment of non-randomized studies.
3.1. Study selection
Study Selection Comparability Outcome Total

We conduct this systematic review and meta-analysis in accordance 1 2 3 4 5 6 7 8

with the Preferred Reporting Items for Systematic Reviews and Meta-
Analysis (PRISMA) guidelines [12]. Finally, 11 studies [13–23] were Moghimi et al., 2008 * * – * ** – – * 6
Jang et al., 2010 * * * * * * * – 7
eligibly included in the pooled analysis, which contained 4 randomized
Lee et al., 2010 * * * * * * – * 7
controlled studies [13–16] and 7 retrospective cohort studies [17–23]. Mocan et al., 2013 * * * * * * * – 7
The detailed search steps are illustrated in Fig. 1. Ji et al., 2017 * * * * * * * * 8
Liu et al., 2017 * * * * * * – – 6
Li et al., 2017 * * * * ** * * * 9
3.2. Study characteristics and quality assessment
1.Representativeness of exposed cohort; 2.Selection of non-exposed cohort;
Table 1 summarizes the characteristics of included studies, which 3.Ascertainment of exposure; 4. Outcome of interest was not present at start of
were published from 1989 to 2017 with sample size ranged from 54 to study; 5. Comparability of cohorts on the basis of the design or analysis;
1262. A total of 3554 patients were included in the meta-analysis with 6.Assessment of outcomes; 7.Follow-up long enough for outcomes to occur;
1256 in the TG group and 2298 in the DG group. The 4 RCTs included 8.Adequacy of follow-up.
964 patients: 445 in the DG group and 519 in the TG group. The 7
retrospective cohort studies included 2590 patients: 811 in the TG
group and 1779 in the DG group. Methodological assessment outcomes groups in terms of the incidence of bleeding (OR, 1.65; 95%CI, 0.61 to
for RCTs are listed in Table 2. The quality assessment outcomes of 4.51; P = 0.32) (Fig. 2C). 7 studies totaling 2745 patients reported data
retrospective cohort studies are summarized in Table 3. on mortality. Compared with DG, TG was associated with a higher
mortality (OR, 2.75; 95%CI, 1.33 to 5.70; P = 0.006) (Fig. 2F).
3.3. Postoperative complication and mortality
3.4. Recurrence and cancer–related death rate
Overall postoperative complication was mentioned in 9 studies.
Overall postoperative complication rate for TG was 21.9%, significantly Among all included studies, 3 studies reported recurrence results, and
higher than the rate of 15.5% of TG (OR, 1.61; 95% CI, 1.03 to 2.51; 4 studies reported cancer–related deaths. The pooled data based on these
P = 0.04) (Fig. 2A).Regarding to specific postoperative complication, studies identified no significant in the recurrence (OR, 1.08; 95% CI, 0.19
TG was associated with a higher incidence of anastomosis leakage to 6.08; P = 0.93) (Fig. 3A) or gastric cancer–related death rates (OR,
(OR,2.14; 95%CI, 1.24 to 3.69; P = 0.006) (Fig. 2B), wound compli- 1.39; 95% CI, 0.63 to 3.05; P = 0.41) (Fig. 3B) between the two groups.
cation (OR,2.00; 95%CI, 1.15 to 3.49; P = 0.01) (Fig. 2D), and peri-
toneal abscess compared with DG (OR,4.00; 95%CI, 2.01 to 7.93;
3.5. Overall survival and stage-specific survival
P < 0.0001) (Fig. 2E). There was no difference between TG and DG
In all, 10 studies with median follow-up ranging from 20 to 72
Table 2 months reported 5-year OS.The result showed that the 5-year OS is
Jadad Scale assessment of randomized studies. better in the DG group than in the TG group group (OR, 0.62; 95% CI,
0.43 to 0.89; P = 0.009) (Fig. 3C). In consideration of the clin-
Study Randomization Allocation Blinding Withdrawal Total
icopathological differences between the two groups, stage-specific
concealment
analyses were carried out on the 5-year OS. The result demonstrate that
Gouzi et al., 1989 2 1 0 1 4 the 5-year OS rates are comparable between the DG and TG groups in
[13] stage I, II, or III (P > 0.05; Fig. 3D).
Robertson et al., 2 1 0 1 4
1994 [14]
Bozzetti et al., 2 1 0 1 4 4. Discussion
1999 [15]
De Manzoni et al., 2 1 0 1 4
Surgical resection with proper perigastric lymph node dissection is
2003 [16]
the mainstay of the curative treatment for potentially curable gastric

165
Z. Li et al. International Journal of Surgery 53 (2018) 163–170

Fig. 2. Forest plot of pooled odds ratio of postoperative morbidity.A Overall postoperative complication; B Anastomotic leakage; C Bleeding; D Wound problem; E
Peritoneal abscess; F Mortality.

166
Z. Li et al.
Fig. 3. Forest plot of pooled odds ratio of long-term prognosis.A Recurrence; B Cancer–related death; C 5-year OS; D Stage-specific analyses of 5-year OS.
cancer. The optimal surgery method should be based on the curative
resection of the tumor with minimal complication and mortality, re-
sulting in better long-term prognosis and ideal quality of life for the
patient [8,21,24]. At the moment, D2 lymph node dissection has been
accepted as the standard [4].However, there is still no consensus re-
garding the best extent of gastrectomy for middle and lower-third
gastric cancer. Previous meta-analysis is in relatively small sample size
167
International Journal of Surgery 53 (2018) 163–170
and the included studies in this study have been published several years
[9]. Some conclusions in that study also inconsistent with several latest
articles.The present meta-analysis includes comparative studies of the
safety and long-term survival outcomes of DG and TG for patients with
middle or lower-third gastric cancer from 1989 to 2017.Although not
all the studies included were RCTs, the majority of the included studies
were of moderate to high quality. Our study included 11 publications
Z. Li et al.
with 3554 patients and reflects the updated outcomes, and would
provide a more objective and comprehensive evaluation on this topic.
Postoperative complication is an important factor to evaluate the
safety and technical feasibility of surgical procedure. The postoperative
complications always associated with longer hospital stays and in-
creased cost of hospitalization, and even resulted in perioperative death
or poor long-term prognosis [25–27]. In this meta-analysis, the com-
parison results about postoperative complication are not consistent in
all trials. Ji et al. [21] reported that the postoperative complications
was higher in the TG group than the DG group. We conducted a well-
matched study recently to evaluate the postoperative complications
according to the Clavien-Dindo classification system and found no
statistically significant differences in overall and major complication
rates between the DG and TG groups [23]. Compared to DG, TG is
considered to be more complicated and technically demanding in terms
of lymph node dissection and reconstruction after gastrectomy
[28,29].Our meta-analysis revealed that the overall postoperative
complication rate and mortality in the TG group are higher than that in
the DG group. In addition, a study conducted by Lee et al. [30] reported
that TG was a significant independent risk factor for overall and severe
complication (grade ≥ IIIa).Despite improvements in surgical tech-
nique and perioperative management, anastomotic leakage still remains
one of the most serious and sometimes life-threatening complication,
with reported incidence of 0%–15% [31–34].Regarding specific com-
plication, previous studies demonstrated that TG is associated with
higher anastomotic leakage rate compared with DG [21,30,35].In the
present study, analyses of specified complications revealed that the rate
of anastomosis leakage, wound problem, and peritoneal abscess are
higher in the TG group than in the DG group.
In recent years, increasing numbers of studies have shown that the
minimally invasive surgery procedure is a well-established and ac-
cepted practice for the treatment of early and locally advanced gastric
cancer [36–38].Compared with laparoscopy-assisted distal gastrectomy
(LADG), laparoscopy-assisted total gastrectomy (LATG) still remains a
challenging procedure due to its technical difficulties, especially in the
procedure of esophagojejunostomy [39–41].Additionally, it is more
difficult to perform intracorporeal esophagojejunostomy through a
limited operating room and the deep anastomosis location, especially in
obese patients [42,43].Kim et al. [35] reported that the incidence of
anastomotic leakage was significantly higher for LATG as compared
with LADG. Lin et al. [44] and Li et al. [23] found that the anastomotic
leakage tended to be more frequent, though not significant, for LATG.
Long-term survival and cancer recurrence rate are two key in-
dicators for assessing patients' prognosis. Based on the available data,
our result showed that the 5-year OS rate of all patients in the DG group
was superior to those in the TG group. A previous meta-analysis also
revealed a favoring trend to DG when 5-year OS rate was compared
[10].But this result is inconsistent in included studies. Gouzi et al. [13]
and Bozzetti et al. [15] reported a similar long-term survival outcome
between DG and TG. However, Lee et al. [19] and Mocan et al. [20]
found that the 5-year OS rates were significantly higher for the DG than
for the TG. Liu et al. [22] also found that the 5-year OS rate of TG was
lower than those of DG in a large scale case-control trial. Many surgeons
tended to perform TG for relatively later-stage gastric cancer to ensure
the curativeness of the surgery. So, cases in TG groups are always as-
sociated with more advanced tumor stages. Considering the imbalance
in tumor staging between the two groups, we perform stage-specific
analysis and found the long-term survival outcome is comparable be-
tween the two groups. Regarding cancer recurrence and cancer-related
death rate, no significant differences were observed between the two
groups.
With respect to surgical outcomes, extensive studies indicated that
the operating time and postoperative hospital stay were significantly
longer in the TG than that in DG. Kim et al. [35] and Lee et al. [45]
reported the longer operation time were revealed as risk factor for the
occurrence of complication. It means that patients who underwent TG
168
International Journal of Surgery 53 (2018) 163–170
may at higher risk of complications compared with DG. Compared with
the standard D2 lymph dissection of DG, TG should perform the lymph
node dissection of No 10 and No 11d.So, patients who underwent TG
are always had more harvested lymph nodes. But this should not be
regard as superiority of TG because they all meet the requirement of
Japanese gastric cancer treatment guidelines [4]. In addition, DG is
associated with less blood loss as compared with TG and this advantage
still exists with the use and development of minimally invasive tech-
nique [23,44].
Many studies have confirmed that positive resection margin had a
definite negative influence on the prognosis of gastric cancer patients
[46–50]. Several studies stated that the advanced tumor stage, large
tumor size, and diffuse histologic type were significantly independent
predictors for a positive margin [46,47].Given the above reasons, many
surgeons prefer to perform TG for patients with middle or lower-third
gastric cancer to ensure a safe proximal resection margin (PRM),
especially for the cases in advanced stage. In the present meta-analysis,
7 studies [16,18–23] preform multivariate analyses to investigated in-
dependent factors for OS. Interestingly, the analyses revealed a con-
sistent result that the resection extent is not an independent factor for
survival of patients. For patients with middle or lower-third gastric
cancer, PRM is a most important factor to be taken in consideration for
the chosen of resection extent. NCCN guidelines and Japanese guide-
lines recommend a 3–5 cm resection margin [4,51]. However, Post-
lewait et al. [52]found that the extensive PRM distances for proximal
gastric cancer is not associated with decreased tumor recurrence or
improved survival and therefore imply that a grossly negative PRM is
sufficient for gastric cancer. In terms of middle or lower-third gastric
cancer, studies have also proved that the length of proximal resection
margin is not associated with long-term prognosis of patients after
curative resection [18,19,21,52,53].
QOL after surgery is often used to assess the subjective of illness and
its treatment which should also be taken into consideration for the
chosen of resection extent [7,54]. Studies have demonstrated that pa-
tients who underwent DG always have a better QoL than those who
underwent TG during postoperative short-term follow-up period
[8,55].Lee et al. [7] evaluated the long-term QOLafter DG and TG found
that five-year survivors after TG were still experiencing worse QOLthan
those who underwent DG in terms of symptoms and dietary limitations.
Previous studies indicated that hospital cost may also a factor in
driving the selection of surgery type [56,57]. At present, the cost-ef-
fectiveness of DG compared with TG is seldom reported. A recent study
conducted by us assessing cost-effectiveness of the LADG and LATG and
found a financial advantage of 5404RMB in favor of LADG [23]. We
attributed this to that TG always associated with more material costs,
longer operating time, and longer postoperative hospital stay. This may
the same for present study as most research reported a longer operating
time, higher complication rate, and longer postoperative hospital stay
in TG, which could be the major factors of increased hospital cost.
Although our meta-analysis included all the RCTs and nRCTs with
moderate to high quality and in relatively large sample size to draw a
reasonable conclusion, there were still several limitations. Because the
published year of included studies varied greatly, the patients may be
influenced by varied staging standard and different treatment guide-
lines. Moreover, limited data was available on disease free survival rate,
recurrence rate, hospital costs, and QoL associated with DG and TG,
especially when we limited the tumor location to middle or lower-third
of the stomach. Finally, considerable heterogeneity across studies
cannot be neglected due to the inherent differences of regional, char-
acteristics of patients, surgeon experience, and length of follow-up
period.
5. Conclusions
In conclusion, the current available evidence indicated that DG is an
alternative surgical procedure for middle or lower-third gastric cancer
Z. Li et al.
with better short-term outcomes and comparable long-term prognosis
as compared with TG. We suggest that DG should be the first surgical
option for middle or lower-third gastric cancer in early and locally
advanced stages under the precondition of negative PRM.
Ethical approval
No need Ethical Approval.
Sources of funding
This study was supported by the National Key Basic Research
Program of China (No. 2014CBA02002).
Disclosures
The authors declare that they have no conflict of interest.
Research registration Unique Identifying Number (UIN)
reviewregistry438.
Author contribution
Zhengyan Li and Qingchuan Zhao performed the experiment con-
ception and design. Zhengyan Li and Bin Bai performed the research
and retrieved the data. Zhengyan Zhengyan Li and Fengni Xie, per-
formed the data analysis. Zhengyan Li did the paper writing. All authors
read and approved the final manuscript.
Guarantor
Qingchuan Zhao.
References
[1] W. Chen, R. Zheng, P.D. Baade, et al., Cancer statistics in China, CA A Cancer J.
Clin. 2016 (66) (2015) 115–132.
[2] D. Shin, S.S. Park, Clinical importance and surgical decision-making regarding
proximal resection margin for gastric cancer, World J. Gastrointest. Oncol. 5 (2013)
4–11.
[3] I.P.H. Songun, E.M. Kranenbarg, M. Sasako, C.J. van de Velde, Surgical treatment of
gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2
trial, Lancet Oncol. 11 (2010) 439–449.
[4] Japanese Gastric Cancer A, Japanese gastric cancer treatment guidelines 2014 (ver.
4), Gastric Cancer: Off. J. Int. Gastric Cancer Assoc. Jpn Gastric Cancer Assoc. 20
(2017) 1–19.
[5] C.J.T.R. Clark, V. Picozzi Jr., D.B. Schembre, F.P. Cummings, E. Lin, Current pro-
blems in surgery: gastric cancer, Curr. Probl. Surg. 43 (2006) 566–670.
[6] H.J.S.A. Stein, J.R. Siewert, Site-dependent resection techniques for gastric cancer,
Surg. Oncol. Clin. 11 (2002) 405–414.
[7] S.S. Lee, H.Y. Chung, O.K. Kwon, W. Yu, Long-term quality of life after distal
subtotal and total gastrectomy: symptom- and behavior-oriented consequences,
Ann. Surg. 263 (2016) 738–744.
[8] S. Park, H.Y. Chung, S.S. Lee, et al., Serial comparisons of quality of life after distal
subtotal or total gastrectomy: what are the rational approaches for quality of life
management? J. Gastric Cancer 14 (2014) 32–38.
[9] L.Y.N. Kong, L. Shi, G. Zhao, M. Wang, Y. Zhang, Total versus subtotal gastrectomy
for distal gastric cancer: meta-analysis of randomized clinical trials, OncoTargets
Ther. (2016) 6795–6800.
[10] J. Qi, P. Zhang, Y. Wang, et al., Does total gastrectomy provide better outcomes
than distal subtotal gastrectomy for distal gastric Cancer? A systematic review and
meta-analysis, PLoS One 11 (2016) e0165179.
[11] A. Stang, Critical evaluation of the Newcastle-Ottawa scale for the assessment of the
quality of nonrandomized studies in meta-analyses, Eur. J. Epidemiol. 25 (2010)
603–605.
[12] D. Moher, A. Liberati, J. Tetzlaff, et al., Preferred reporting items for systematic
reviews and meta-analyses: the PRISMA statement, Bmj 339 (2009) b2535.
[13] J.L.H.M. Gouzi, P.L. Fagniez, B. Launois, Y. Flamant, F. Lacaine, J.C. Paquet,
J.M. Hay, Total versus subtotal gastrectomy for adenocarcinoma of the gastric
antrum. A French prospective controlled study, Ann. Surg. 209 (1989) 162–166.
[14] C.S.C.S. Robertson, S.D. Woods, S.M. Griffin, S.A. Raimes, J.T. Lau, A.K. Li, A
prospective randomized trial comparing R1 subtotal gastrectomy with R3 total
gastrectomy for antral cancer, Ann. Surg. 220 (1994) 176–182.
[15] F.M.E. Bozzetti, G. Bonfanti, R. Miceli, C. Piano, L. Gennari, Subtotal versus total
169
International Journal of Surgery 53 (2018) 163–170
gastrectomy for gastric cancer: five-year survival rates in a multicenter randomized
Italian trial. Italian Gastrointestinal Tumor Study Group, Ann. Surg. 230 (1999)
170–178.
[16] G. De Manzoni, G. Verlato, F. Roviello, et al., Subtotal versus total gastrectomy for
T3 adenocarcinoma of the antrum, Gastric Cancer: Off. J. Int. Gastric Cancer Assoc.
Jpn Gastric Cancer Assoc. 6 (2003) 237–242.
[17] S.A.M.T.S. Mehrdad Moghimi, Peirovi Habibollah, Faezeh sodagari surgical out-
comes and local recurrence following total or subtotal gastrectomy for early ade-
nocarcinoma of antrum, Chin. J. Canc. Res. (2008) 279–285.
[18] Y.J. Jang, M.S. Park, J.H. Kim, et al., Advanced gastric cancer in the middle one-
third of the stomach: should surgeons perform total gastrectomy? J. Surg. Oncol.
101 (2010) 451–456.
[19] J.H. Lee, Y.I. Kim, Which is the optimal extent of resection in middle third gastric
cancer between total gastrectomy and subtotal gastrectomy? J. Gastric Cancer 10
(2010) 226–233.
[20] L.T.C. Mocan, D. Bartos, F. Zaharie, I. Ioana, A. Bartos, C. Puia, A. Necula, T. Mocan,
C. Iancu, Long term outcome following surgical treatment for distal gastric cancer,
J. Gastrointestin Liver Dis. 22 (2013) 53–58.
[21] X. Ji, Y. Yan, Z.D. Bu, et al., The optimal extent of gastrectomy for middle-third
gastric cancer: distal subtotal gastrectomy is superior to total gastrectomy in short-
term effect without sacrificing long-term survival, BMC Canc. 17 (2017) 345.
[22] Z.F.F. Liu, M. Guo, S. Liu, G. Zheng, G. Xu, X. Lian, D. Fan, H. Zhang, Distal gas-
trectomy versus total gastrectomy for distal gastric cancer, Medicine 96 (2017)
e6003.
[23] Z. Li, G. Ji, B. Bai, et al., Laparoscopy-assisted distal gastrectomy versus laparo-
scopy-assisted total gastrectomy with D2 lymph node dissection for middle-third
advanced gastric cancer, Surg. Endosc. (2017), https://doi.org/10.1007/s00464-
017-5919-9.
[24] R.W. Randle, D.S. Swords, E.A. Levine, et al., Optimal extent of lymphadenectomy
for gastric adenocarcinoma: a 7-institution study of the U.S. gastric cancer colla-
borative, J. Surg. Oncol. 113 (2016) 750–755.
[25] J. Zhou, P. Yu, Y. Shi, et al., Evaluation of Clavien-Dindo classification in patients
undergoing total gastrectomy for gastric cancer, Med. Oncol. 32 (2015) 120.
[26] M. Tokunaga, Y. Tanizawa, E. Bando, et al., Poor survival rate in patients with
postoperative intra-abdominal infectious complications following curative gas-
trectomy for gastric cancer, Ann. Surg Oncol. 20 (2013) 1575–1583.
[27] T. Kubota, N. Hiki, T. Sano, et al., Prognostic significance of complications after
curative surgery for gastric cancer, Ann. Surg Oncol. 21 (2014) 891–898.
[28] S.E. Lee, K.W. Ryu, B.H. Nam, et al., Technical feasibility and safety of laparoscopy-
assisted total gastrectomy in gastric cancer: a comparative study with laparoscopy-
assisted distal gastrectomy, J. Surg. Oncol. 100 (2009) 392–395.
[29] T. Etoh, M. Honda, H. Kumamaru, et al., Morbidity and mortality from a propensity
score-matched, prospective cohort study of laparoscopic versus open total gas-
trectomy for gastric cancer: data from a nationwide web-based database, Surg.
Endosc. (2017), https://doi.org/10.1007/s00464-017-5976-0.
[30] K.G. Lee, H.J. Lee, J.Y. Yang, et al., Risk factors associated with complication fol-
lowing gastrectomy for gastric cancer: retrospective analysis of prospectively col-
lected data based on the Clavien-Dindo system, J. Gastrointest. Surg. 18 (2014)
1269–1277.
[31] M. Inokuchi, S. Otsuki, Y. Fujimori, et al., Systematic review of anastomotic com-
plications of esophagojejunostomy after laparoscopic total gastrectomy, World J.
Gastroenterol. 21 (2015) 9656–9665.
[32] M. Schietroma, E.M. Cecilia, F. Carlei, et al., Prevention of anastomotic leakage
after total gastrectomy with perioperative supplemental oxygen administration: a
prospective randomized, double-blind, controlled, single-center trial, Ann. Surg
Oncol. 20 (2013) 1584–1590.
[33] Y. Haga, Y. Wada, H. Takeuchi, et al., Prediction of anastomotic leak and its
prognosis in digestive surgery, World J. Surg. 35 (2011) 716–722.
[34] W. Gong, J. Li, Combat with esophagojejunal anastomotic leakage after total gas-
trectomy for gastric cancer: a critical review of the literature, Int. J. Surg. 47 (2017)
18–24.
[35] D.J. Kim, J.H. Lee, W. Kim, Comparison of the major postoperative complications
between laparoscopic distal and total gastrectomies for gastric cancer using
Clavien-Dindo classification, Surg. Endosc. 29 (2015) 3196–3204.
[36] K.H. Pak, W.J. Hyung, T. Son, et al., Long-term oncologic outcomes of 714 con-
secutive laparoscopic gastrectomies for gastric cancer: results from the 7-year ex-
perience of a single institute, Surg. Endosc. 26 (2011) 130–136.
[37] C. Fang, J. Hua, J. Li, et al., Comparison of long-term results between laparoscopy-
assisted gastrectomy and open gastrectomy with D2 lymphadenectomy for ad-
vanced gastric cancer, Am. J. Surg. 208 (2014) 391–396.
[38] Y. Hu, C. Huang, Y. Sun, et al., Morbidity and mortality of laparoscopic versus open
D2 distal gastrectomy for advanced gastric cancer: a randomized controlled trial, J.
Clin. Oncol. : Off. J. Am. Soc. Clin. Oncol. 34 (2016) 1350–1357.
[39] W. Duan, K. Liu, X. Fu, et al., Semi-end-to-end esophagojejunostomy after laparo-
scopy-assisted total gastrectomy better reduces stricture and leakage than the
conventional end-to-side procedure: a retrospective study, J. Surg. Oncol. 116
(2017) 177–183.
[40] H. Kawamura, Y. Ohno, N. Ichikawa, et al., Anastomotic complications after la-
paroscopic total gastrectomy with esophagojejunostomy constructed by circular
stapler (OrVil( )) versus linear stapler (overlap method), Surg. Endosc. 31 (2017)
5175–5182.
[41] T. Bo, Y. Peiwu, Q. Feng, et al., Laparoscopy-assisted vs. Open total gastrectomy for
advanced gastric cancer: long-term outcomes and technical aspects of a case–-
control study, J. Gastrointest. Surg. 17 (2013) 1202–1208.
[42] H. Okabe, K. Obama, S. Tsunoda, et al., Advantage of completely laparoscopic
gastrectomy with linear stapled reconstruction: a long-term follow-up study, Ann.
Z. Li et al.
Surg. 259 (2014) 109–116.
[43] J.H. Shim, H.M. Yoo, S.I. Oh, et al., Various types of intracorporeal esophagojeju-
nostomy after laparoscopic total gastrectomy for gastric cancer, Gastric Cancer: Off.
J. Int. Gastric Cancer Assoc. Jpn. Gastric Cancer Assoc. 16 (2013) 420–427.
[44] J.X. Lin, C.M. Huang, C.H. Zheng, et al., Evaluation of laparoscopic total gas-
trectomy for advanced gastric cancer: results of a comparison with laparoscopic
distal gastrectomy, Surg. Endosc. 30 (2016) 1988–1998.
[45] J.H. Lee, D.J. Park, H.H. Kim, et al., Comparison of complications after laparoscopy-
assisted distal gastrectomy and open distal gastrectomy for gastric cancer using the
Clavien-Dindo classification, Surg. Endosc. 26 (2012) 1287–1295.
[46] S.Y. Wang, C.N. Yeh, H.L. Lee, et al., Clinical impact of positive surgical margin
status on gastric cancer patients undergoing gastrectomy, Ann. Surg Oncol. 16
(2009) 2738–2743.
[47] B.C. Cho, H.C. Jeung, H.J. Choi, et al., Prognostic impact of resection margin in-
volvement after extended (D2/D3) gastrectomy for advanced gastric cancer: a 15-
year experience at a single institute, J. Surg. Oncol. 95 (2007) 461–468.
[48] S.Y. Kim, Y.S. Hwang, T.S. Sohn, et al., The predictors and clinical impact of po-
sitive resection margins on frozen section in gastric cancer surgery, J. Gastric
Cancer 12 (2012) 113.
[49] S.C. Cunningham, F. Kamangar, M.P. Kim, et al., Survival after gastric adeno-
carcinoma resection: eighteen-year experience at a single institution, J.
Gastrointest. Surg. 9 (2005) 718–725.
170
International Journal of Surgery 53 (2018) 163–170
[50] T. Nagata, D. Ichikawa, S. Komatsu, et al., Prognostic impact of microscopic positive
margin in gastric cancer patients, J. Surg. Oncol. 104 (2011) 592–597.
[51] J.A.D.A.T. Ajani, K. Almhanna, D.J. Bentrem, J. Chao, P. Das, Gastric cancer, ver-
sion3.2016, NCCN clinical practice guidelines in oncology, J. Natl. Compr. Canc.
Netw. (2016) 1286–1312.
[52] L.M. Postlewait, M.H. Squires 3rd, D.A. Kooby, et al., The importance of the
proximal resection margin distance for proximal gastric adenocarcinoma: a multi-
institutional study of the US Gastric Cancer Collaborative, J. Surg. Oncol. 112
(2015) 203–207.
[53] C.M. Lee, Y.S. Jee, J.H. Lee, et al., Length of negative resection margin does not
affect local recurrence and survival in the patients with gastric cancer, World J.
Gastroenterol. 20 (2014) 10518–10524.
[54] A B, The cancer patient and quality of life, Oncol 7 (2002) 120–125.
[55] C.C. Huang, H.H. Lien, P.C. Wang, et al., Quality of life in disease-free gastric
adenocarcinoma survivors: impacts of clinical stages and reconstructive surgical
procedures, Dig. Surg. 24 (2007) 59–65.
[56] A. Silverstein, A. Costas-Chavarri, M.R. Gakwaya, et al., Laparoscopic versus open
cholecystectomy: a cost-effectiveness analysis at Rwanda military hospital, World J.
Surg. 41 (2017) 1225–1233.
[57] M.H. Gerber, D. Delitto, C.J. Crippen, et al., Analysis of the cost effectiveness of
laparoscopic pancreatoduodenectomy, J. Gastrointest. Surg. 21 (2017) 1404–1410.