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Total versus subtotal gastrectomy for distal gastric

cancer: meta-analysis of randomized clinical trials
This article was published in the following Dove Press journal:
OncoTargets and Therapy
7 November 2016
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Lingling Kong* Objectives: This meta-analysis of randomized controlled trials was conducted to give a more
Nianzhao Yang* precise estimation of the efficacy and drawbacks of total gastrectomy (TG) versus subtotal
Lianghui Shi gastrectomy (SG) for proven distal gastric cancer.
Guohai Zhao Methods: The electronic databases Cochrane and PubMed (updated on April 10, 2016) were
Minghai Wang searched for randomized controlled trials comparing TG with SG as surgical procedures for distal
gastric cancer. Five outcome variables were analyzed, including postoperative complications,
Yisheng Zhang
anastomotic fistula rate, hospital mortality rate, mortality rate of recurrence (the patient’s death
Department of General Surgery,
is caused by the recurrence of gastric cancer, rather than caused by other diseases), and 5-year
The First Affiliated Yijishan Hospital
of Wannan Medical College, Wuhu, survival rate. Random or fixed effect model was used to perform this meta-analysis.
People’s Republic of China Results: Six trials, including 573 cases treated with TG and 791 cases treated with SG, were
*These authors contributed equally included. Compared with patients in the SG group, patients in the TG group did not show a
to this work higher rate of postoperative complications (odds ratio [OR]: 1.46, 95% confidence interval
[CI]: 0.71–3.03, P=0.30). However, patients in the TG group showed a significantly higher rate
of anastomotic fistula than patients in the SG group (OR: 3.78, 95% CI: 1.97–7.27, P,0.0001).
Hospital mortality rate, which was analyzed in four trials, including 510 TG versus 729 SG
patients, showed no significant difference between the two groups (OR: 1.80, 95% CI: 0.85–3.78,
P=0.12). Importantly, there was no significant difference in the 5-year survival between the
two groups (OR: 0.68, 95% CI: 0.39–1.19, P=0.18). Mortality rate of recurrence, which was
also analyzed in three trials, including 396 TG versus 407 SG patients, showed a significantly
higher rate in the TG group (OR: 0.07, 95% CI: 0.01–0.13, P=0.03).
Conclusion: This meta-analysis demonstrated that postoperative complications, hospital
mortality rate, and 5-year survival rate in TG patients was similar to the SG group. Furthermore,
SG was associated with significantly fewer anastomotic fistula and lower mortality rate of
recurrence compared with TG. However, lower mortality rate of recurrence was probably related
to the criteria of these two procedures.
Keywords: total gastrectomy, subtotal gastrectomy, gastric cancer, randomized controlled trials

Introduction
Gastric cancer is one of the most common digestive tract malignancies worldwide,
and surgical resection is the only therapeutic modality for cure.1 The resection method
Correspondence: Minghai Wang; includes total gastrectomy (TG) and subtotal gastrectomy (SG). Since Billroth
Yisheng Zhang performed the first SG in 1881 and Schlatter the first TG in 1897, the best surgical
Department of General Surgery, The
First Affiliated Yijishan Hospital of procedure for adenocarcinoma of the distal stomach has been a subject of debate for
Wannan Medical College, No 92, more than a century.2–4
Zheshan Road, Wuhu, Anhui
241001, People’s Republic of China
The routine use of TG was accepted for three main reasons:5–7 1) TG could reduce
Tel +86 553 138 6665 8218; the likelihood of recurrence due to possible inadequate lymph nodes removal; 2) it could
+86 553 138 5530 0038
Email wangmh0410@sina.com;
remove all multicentric carcinoma foci in the gastric remnant; and 3) it could eliminate
zhangys0109@hotmail.com the risk of metachronous adenocarcinoma that may develop in the gastric remnant.
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Dovepress © 2016 Kong et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php
http://dx.doi.org/10.2147/OTT.S110828
and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you
hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission
for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php).
Kong et al Dovepress

Additionally, some studies demonstrated that TG was of recurrence of the two groups, and 5-year survival rate
preferable to SG, because patients treated with TG had of the two groups. The extracted data were discussed until
longer 5-year survival than patients treated with SG.8–10 consensus was achieved.
On the other hand, advocates of SG claimed that routine use
of TG increased operative morbidity and hospital mortality, Statistical analysis
and had no advantage over SG in terms of 5-year oncologi- The odds ratios (ORs) and 95% confidence intervals (CIs)
cal results.11–13 were used to assess all outcomes.13 We assessed the het-
The debate over the type of curative resection for distal erogeneity between studies by using the Q statistic, which
gastric cancer based on a number of retrospective published indicates the presence of heterogeneity when P,0.10.
studies, and patients’ criteria of eligibility were different. If the results of studies had no heterogeneity, the fixed-
Therefore, with respect to the trials comparing TG versus effects model (the Mantel–Haenszel method) was used
SG, well-designed randomized controlled trials (RCTs) are to calculate the pooled ORs. Otherwise, a random-effects
necessary. Until now, only a few RCTs3,8,14,15 have reported model (the DerSimonian and Laird method) was used for
the data on the short- and long-term outcomes of TG for distal meta-analysis. Statistical significance was considered when
gastric cancer in comparison to SG, and the results reported P,0.05. All statistical analyses were conducted using the
in these RCTs were discordant. Review Manager version 5.1.6 (Cochrane Collaboration,
Therefore, a more precise estimation of the outcomes of Oxford, UK) software package.
TG in comparison to SG is necessary. To our knowledge,
there is no meta-analysis of the evidence gathered from the Results
outcomes of TG and SG surgery for distal gastric cancer. Description of eligible trials
This meta-analysis may give the answer in terms of the Six clinical trials8,14–18 published in four articles were con-
best available scientific evidence to date. The postoperative sidered suitable for this meta-analysis. The study size in two
complication rate, anastomotic fistula rate, hospital mortality RCTs from Europe was larger than 100 patients except for
rate, mortality rate of recurrence, and 5-year survival rate of the Asian trial (including 54 patients). All trials reported an
TG in comparison to SG were estimated in this study. appropriated method of randomization. None of the stud-
ies reported the method of blinding. Six studies contained
Methods 1,364 pooled patients, of whom 573 were allocated to the
Search strategy TG group, 791 to the SG group. The detailed information of
The electronic literature searches were conducted using each included study is shown in Table 1.
Cochrane and PubMed (updated on April 10, 2016). Search The patients were excluded from the study if: 1) cura-
terms included: “total gastrectomy”, “subtotal gastrectomy”, tive resection could not be performed and thus conservative
“gastric cancer”, and “Randomized controlled trials”. All surgery was performed; 2) curative resection could not be
titles, abstracts, and full-text articles were evaluated by performed for macroscopic lymph node involvement of the
two reviewers independently. To be eligible, the studies cardioesophageal junction or splenopancreatic region; 3) lini-
had to meet the following criteria: 1) RCTs of any size that tis plastica; 4) lymphoma; 5) suspected superficial carcinoma;
investigated TG versus SG in patients with cancer in distal and 6) patients with heart failure, renal insufficiency, severe
stomach; 2) reported on relevant short- or long-term out- diabetes or arteritis, obesity (.20% of normal body weight),
comes of trial; and 3) published in peer-reviewed journals recent myocardial infarction, and liver cirrhosis, patients
in English language. who underwent laparoscopic surgery, and patients who died
within 30 days after surgery. The inclusion criteria were: 1)
Data extraction cancer of the distal half of the stomach; 2) absence of hepatic
The data extraction and critical appraisal from all the eligible or peritoneal spread of the tumor or metastatic deposits in the
studies was carried out independently by two investigators. third nodal level, according to the Japanese classification; and
The following variables were extracted from the included 3) absence of unresectable infiltration of contiguous organs.
studies if available: first author’s name, publication year, the The reconstructive methods vary from trial to trial.
number of patients in TG and SG groups, overall complica- In Gouzi’s paper, TG repair was performed by a standard
tion rate of the two groups, anastomotic fistula rate of the Roux-en-Y esophagojejunostomy.8 Reconstruction of SG
two groups, mortality rate of the two groups, mortality rate was performed by a Billroth II gastrojejunostomy. Whereas,

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Dovepress TG versus SG for distal gastric cancer

Table 1 Characteristics of included studies

Authors Year Country Patients (N) Design Randomization Blinding
Gouzi et al 8
1989 France SG:93 RCT Adequate Not stated
TG:76
Robertson et al14 1994 People’s Republic SG:25 RCT Adequate Not stated
of China TG:29
Bozzetti et al3,15 1997, 1999 Italy SG:320 RCT Adequate Not stated
TG:304
De Manzoni et al16 2003 Italy SG:77 RCT Adequate Not stated
TG:40
Lee et al18 2010 Korea SG:62 RCT Adequate Not stated
TG:63
Park et al17 2014 Korea SG:214 RCT Adequate Not stated
TG:61
Abbreviations: N, numbers; RCT, randomized controlled trial; SG, subtotal gastrectomy; TG, total gastrectomy.

Robertson et al14 restored the intestinal continuity by an end- (Figure 5), with no between-study heterogeneity (P=0.14,
to-side esophagojejunostomy, using a circular stapler, with I2=49%) (Figure 5). The detailed information of the pooled
a 40 cm jejunal Roux limb. data is shown in Table 2.

Pooled efficacy of TG versus SG Discussion

Six clinical trials containing 1,364 patients (TG =573, Six trials8,14–18 have been undertaken to investigate the issues
SG  =791) were analyzed. Compared with patients in the of efficacy and drawbacks of TG versus SG. This meta-
SG group, patients in the TG group did not show a higher analysis showed that the anastomotic fistula rate and mortality
rate of postoperative complications (OR: 1.46, 95% CI: rate of recurrence was higher in the TG group than the SG
0.71–3.03, P=0.30) (Figure 1). However, patients in the group. In addition, there was no difference in postoperative
TG group showed a significantly higher rate of anastomotic complication rate, hospital mortality rate, and 5-year survival
fistula than patients in the SG group (OR: 3.78, 95% CI: rate between TG and SG groups.
1.97–7.27, P,0.0001) (Figure 2). Furthermore, there was no Both TG and SG are surgical procedures performed with
significant difference in the hospital mortality rate between curative intent. These two surgical procedures are quite
the two groups (OR: 1.80, 95% CI: 0.85–3.78, P=0.12) effective curative treatments, but also bring a great number
(Figure 3). Importantly, there was no significant difference of postoperative complications, which include surgical and
in the 5-year survival between the two groups (OR: 0.68, nonsurgical complications. Two RCTs from Hong Kong14
95% CI: 0.39–1.19, P=0.18) (Figure 4). and Italy15 revealed that the risk of postoperative complica-
Mortality rate of recurrence, which was analyzed in tions was found to be higher in the TG group than the SG
three trials14,15,18 that included 803 pooled patients, of whom group. But RCTs from France8 and Italy16 demonstrated
396 TG versus 407 SG patients, showed a significantly higher that TG did not increase postoperative complications in
rate in the TG group (OR: 0.07, 95% CI: 0.01–0.13, P=0.03) comparison with SG. Our meta-analysis showed that there

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Figure 1 Meta-analysis of postoperative complications in randomized trials of total gastrectomy versus subtotal gastrectomy.
Abbreviations: CI, confidence interval; M–H, Mantel–Haenszel.

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6797
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Kong et al Dovepress

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Figure 2 Meta-analysis of anastomotic fistula in randomized trials of total gastrectomy versus subtotal gastrectomy.
Abbreviations: CI, confidence interval; M–H, Mantel–Haenszel.

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Figure 3 Meta-analysis of hospital mortality rate of total gastrectomy versus subtotal gastrectomy.
Abbreviations: CI, confidence interval; M–H, Mantel–Haenszel.

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Figure 4 Meta-analysis of 5-year survival rate of total gastrectomy versus subtotal gastrectomy.
Abbreviations: CI, confidence interval; M–H, Mantel–Haenszel.

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Figure 5 Meta-analysis of mortality of recurrence in randomized trials of total gastrectomy versus subtotal gastrectomy.
Abbreviations: CI, confidence interval; M–H, Mantel–Haenszel.

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Dovepress TG versus SG for distal gastric cancer

Table 2 Summary statistics of pooled data comparing total gastrectomy versus subtotal gastrectomy
Outcome variables OR (95% CI) Test for overall effect Test for heterogeneity
Z P-value Q P-value I2 index
Complication 1.46 (0.71, 3.02) 1.03 0.30 8.18 0.04 63%
Anastomotic fistula 3.78 (1.97, 7.27) 4.00 ,0.0001 5.71 0.13 47%
Hospital mortality 1.80 (0.85, 3.78) 1.54 0.12 2.35 0.67 0%
Mortality rate of recurrence 0.07 (0.01, 0.13) 2.21 0.03 3.91 0.14 49%
Five-year survival 0.68 (0.39, 1.19) 1.35 0.18 9.34 0.03 68%
Abbreviations: CI, confidence interval; OR, odds ratio.

was no significant difference in postoperative complications complications in the RCT from Italy was not significantly dif-
between the TG and SG groups. The preoperative criteria of ferent between the TG and SG groups.15 Therefore, the pooled
eligibility, which excluded patients in poor condition from results showed that mortality rates in TG and SG groups were
randomization, might explain the lack of significant differ- not statistically significantly different, although pooled data
ences between TG and SG.15 showed a statistically significant higher anastomotic fistula
Anastomotic fistula rate was reported in three trials. rate in the TG group compared with the SG group.
The pooled data revealed a statistically significantly higher Recurrence rate was not reported in both TG and SG
anastomotic fistula rate in the TG group. In the Hong Kong groups. Mortality rate of recurrence in both surgical pro-
trial led by Robertson et al,14 three anastomotic fistulae were cedures was reported in two RCTs.3,14 Our meta-analysis
recorded in the TG group, which were at oesophagojejunal showed statistically significant lower mortality rate of recur-
junction. In the French trial led by Gouzi et al,8 12 anastomotic rence in the SG group than the TG group. To our knowledge,
fistulae were recorded, of which 7 were in the TG group the TG group has shown higher 5-year survival rate than
and 5 in SG group. In Italy, in a trial by De Manzoni et al,16 the SG group in two retrospective studies.9,10 However, this
three anastomotic fistulae were recorded, of which one was difference has not been observed in all trials. In contrast, the
recorded in the TG group and two in the SG group, and the RCT from Hong Kong14 showed that overall survival was
total numbers of two groups were 40 and 77, respectively. significantly better in the SG than the TG group (median
All these anastomotic fistulae were managed conservatively survival, 1,511 vs 922 days, P,0.05). For these inconsistent
with nutritional support with favorable outcome.8,14 In the conclusions, it is possible that some unknown prognostic
Italian trial led by Bozzetti et al,15 22 anastomotic fistulae were factors were not balanced between the TG and SG groups. In
recorded, of which 17 were in the TG and 5 in the SG groups. the present meta-analysis, no significant difference in 5-year
However, this trial did not provide any information about survival was observed between the TG and SG groups. How-
treatment. According to Gouzi and Robertson, the procedure ever, even early gastric cancer was associated with a high
of TG is more complicated and time consuming. Otherwise, frequency of second primaries.19 Therefore Bozzetti et al3,15
compared to TG, the reconstructive method of SG reflected suggested that with respect to the procedure of choice for dis-
richer blood supply to the stomach. Large clinical trials should tal gastric cancer, TG should not be rejected in principle.
be conducted to confirm this finding about significant differ- On the other hand, there are several limitations in this
ence in anastomotic fistula rate between TG and SG. meta-analysis. First, limited number of patients with cancer
There was no significant difference of hospital mortality of the middle one-third of the stomach were randomized to
rate between the two groups in all the trials, although TG either a TG or a SG group, although a majority of patients
surgical procedure was prolonged and more complex. in the Italian trial had cancer of the antrum. Second, the
All trials have revealed that there was a significantly SG group with D1 lymphadenectomy was not in line with
higher mortality rate in the TG group compared with the the TG group with D2 lymphadenectomy in the Hong
SG group. Lower mortality rate of recurrence was probably Kong trial. Third, the inclusion of studies published only
related to the criteria of these two procedures. In addition, in English is another potential limitation of this analysis.
high mortality rate in patients undergoing resection of the Fourth, only two trials mentioned the reconstructive method,
stomach was usually related to anastomotic fistula.8 How- so it is hard to assess whether or not the reconstructive
ever, all patients who suffered from anastomotic fistula in method influences the prognosis. Finally, only four RCTs
two RCTs from Hong Kong and France were medically were conducted in the 1990s in some countries, and the
treated and healed without mortality.8,14 Fatal complications sample is small. Further well-designed randomized clinical
may increase the mortality rate, but the proportion of fatal trials with larger sample size are still needed to get a more

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6799
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precise estimation of the efficacy and drawbacks of TG 2. Egli S, Schlatter K, Streule R, Lage D. A structure-based expert model
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