Influence of enhanced recovery after surgery programs on laparoscopy-assisted gastrectomy for gastric cancer: a systematic review and meta-analysis of randomized control trials
Li et al. World Journal of Surgical Oncology
Influence of enhanced recovery after surgery programs on laparoscopy-assisted gastrectomy for gastric cancer: a systematic review and meta-analysis of randomized control trials
Zhengyan Li 0
Qian Wang 0
Bofei Li 0
Bin Bai 0
Qingchuan Zhao 0
0 Department of Surgery, Xijing Hospital of Digestive Diseases, The Fourth Military Medical University , No. 127 Changle West Road, Xian 710032 , China
Background: This meta-analysis is aimed to evaluate the feasibility and safety of enhanced recovery after surgery (ERAS) programs in gastric cancer patients undergoing laparoscopy-assisted gastrectomy (LAG). Methods: We performed a meta-analysis of randomized control trials involving either enhanced recovery after surgery (ERAS)/fast track surgery (FTS) for patients underwent LAG. EMBASE, Pubmed, Web of science, and Cochrane Library were searched. Primary outcomes included the length of postoperative hospital stay, cost of hospitalization, postoperative complications, and readmission rate. Results: Five randomized control trials were eligible for analysis. There were 159 cases in FTS group and 156 cases in conventional care group. Compared with conventional care group, FTS group relates to shorter postoperative hospital stay (WMD − 2.16; 95% CI − 3.05 to − 1.26, P < 0.00001), less cost of hospitalization (WMD − 4.72; 95% CI − 6.88 to − 2.55, P < 0.00001), shorter time to first flatus (WMD − 9.72; 95% CI − 13.75 to − 5.81, P < 0.00001), lower level of C-reaction protein on postoperative days 3 or 4 (WMD − 19.66; 95% CI − 28.98 to − 10.34, P < 0.00001), higher level of albumin on postoperative day 4 (WMD 3.45; 95% CI 2.01 to 4.89, P < 0.00001), and postoperative day 7 (WMD 5.63; 95% CI 1.01 to 10.24, P = 0.02). Regarding postoperative complications, no significant differences were observed between FTS group and conventional care group (OR 0.63, 95% CI 0.37 to 1.09, P = 0.10). The readmission rate of FTS group was comparable to conventional care group (WMD 3.14; 95% CI 0.12 to 81.35, P = 0.49). Conclusions: Among patients undergoing LAG, FTS is associated with shorter postoperative hospital stay, rapid postoperative recovery, and decreased cost without increasing complications or readmission rate. The combined effects of the two methods could further accelerate clinical recovery of gastric cancer patients.
Fast track surgery; Enhanced recovery after surgery; Gastric cancer; Laparoscopy-assisted gastrectomy
Gastric cancer is a worldwide health concern and is the
second leading cause of cancer-related deaths in China
]. In recent years, the use of laparoscopy-assisted
gastrectomy (LAG) was developed and clinically
implemented to treat gastric cancer with the advantage of
better short-term outcomes [
]. Fast track surgery
(FTS)/enhanced recovery after surgery (ERAS) was first
introduced by Kehlet in the 1990s and has gained
satisfactory curative effect in many fields of surgery [
ERAS guidelines have been established in many kinds of
surgeries, such as colectomy, cystectomy, and stomach
surgery. Recent meta-analyses have demonstrated that
ERAS is safe and effective after laparoscopic
hepatectomy and colorectal surgery [
]. Previous studies
have demonstrated that ERAS could accelerate the
postoperative recovery in open gastrectomy for gastric
]. However, the role of ERAS in LAG is still
unclear. To date, several studies have reported the value
of FTS in LAG [
]. But they are all based on
singlecenter studies with small sample size which may
influence the credibility of the results. Therefore, we conduct
this meta-analysis to assess the effects of ERAS protocol
in gastric cancer patients undergoing LAG.
This meta-analysis was conducted on the basis of the
preferred reporting items for systematic reviews and
meta-analyses (PRISMA) guidelines [
Pubmed, Web of science, and Cochrane Library were
searched from January 1995 to July 2017. Studies were
limited to English and Chinese. We used the following
key words: “fast track,” “enhanced recovery,” “FTS,”
“ERAS,” “gastric cancer,” “laparoscopy-assisted
gastrectomy,” and “laparoscopic gastrectomy.” Additionally, the
reference lists of all included studies were also searched
to retrieve related articles.
Inclusion and exclusion criteria
Inclusion criteria categories included (1) patients
undergoing LAG for gastric cancer (2) perioperative care using
either ERAS or FTS protocols compared with standard
or conventional care, (3) randomized controlled trials
(RCTs)(4) clearly state the ERAS program, and at
least one or more of the primary outcomes was reported.
Studies were excluded if they (1) included less than 6
interventions items in the FTS group according to the
ERAS guidelines [
] (2) unable to provide one of the
primary outcome mentioned above.
The primary outcomes were the length of postoperative
hospital stay, cost of hospitalization, postoperative
complications, and readmission rate. The secondary
outcomes were time to first flatus, level of C-reaction
protein, albumin, and Interleukin-6.
Quality assessment and data extraction
The quality of each included RCT was assessed
according to the Cochrane methodology, which included the
following evaluation domains: random sequence
generation, allocation concealment, blinding of participants
and personnel, blinding of outcome assessment,
incomplete outcome data, selective reporting, and other biases
]. The data was extracted from each eligible trial by
two authors (Q Wang and Bin Bai). From each study, we
extracted the general information of included studies,
including the author, publication year, type of studies,
sample size, surgery method, follow-up duration, and
some other details.
The data pooling was carried out using the Review
Manager software (version 5.3, Nordic Cochrane Centre).
The pooled results were expressed as the mean
difference (MD) with 95% confidence interval (CI).
Continuous variables were assessed using weighted mean
difference (WMD). Dichotomous variables was analyzed
using odds ratios (OR) and 95% CI.
Statistical heterogeneity among studies was
evaluated by using the Cochran Q statistic and quantified
by I2 statistics. The random-effects model was used in
this meta-analysis. Due to the limited number of
studies (less than 10), the funnel plot was not
performed to test the publication bias. P < 0.05 was
considered statistically significant.
Characteristics of trials
Figure 1 summarizes the flow chart for the selection
of eligible studies. Eventually, five studies [
] were considered eligible for this meta-analysis. In
all, data from 315 patients were recorded, of which
159 in the FTS group and 156 in the conventional
care group. All included studies were conducted in
Asia (4 in China and 1 in Korea), and their studies
were published between 2012 and 2016. Table 1
shows the general characteristics of included studies.
The EARS items applied in the included studies are
presented in Table 2. Regarding the methodological
quality, all included studies showed low to moderate
overall risks of bias (Fig. 2).
Postoperative hospital stay and hospitalization expenditure
The data of postoperative hospital stay could be
obtained from four included studies. The result showed
that FTS group is associated with a significant
reduction in postoperative hospital stay when compared to
the conventional care group (WMD − 2.16; 95% CI −
3.05 to − 1.26, P < 0.00001) (Fig. 3a). High
heterogeneity was observed among the studies (P = 0.04, I2 =
65%), and a random-effects model was used. Three
included studies reported the cost of hospitalization.
Results showed that FTS group had a less cost of
hospitalization compared to the conventional care
Postoperative complications and readmission rate
Postoperative complications were described in all five
studies. The results of this meta-analysis did not show a
significant difference between the two groups (OR =
0.63, 95% CI 0.37 to 1.09, P = 0.10) (Fig. 3c). Two studies
reported readmission rate of patients. No statistical
RCT randomized controlled trials, FTS fast track surgery, CC conventional care, NR not reported, 1 time to first flatus, 2 C-reaction protein, 3 interleukin-6, 4 length
of postoperative hospital stay, 5 hospitalization expenditure, 6 readmission rate, 7 postoperative complications, 8 albumin
Kim et al.
Hu et al.
Abdikarim et al.
Li et al.
Liu et al.
difference was found between the two groups (WMD =
3.14; 95% CI 0.12 to 81.35; P = 0.49) (Fig. 3d).
2.01 to 4.89, P < 0.00001) and postoperative day 7
(WMD 5.63; 95% CI 1.01 to 10.24, P = 0.02) (Fig. 4e).
Time to first flatus, ambulation time, and time to start diet
The results of this meta-analysis revealed that FTS
group was associated with a shorter time to first flatus
(WMD − 9.78; 95% CI − 13.75 to − 5.81, P < 0.00001)
(Fig. 4a). No significant differences were found between
the two groups in terms of ambulation time (WMD −
0.97; 95% CI − 2.27 to 0.33, P = 0.14) (Fig. 4b) and time
to start diet (WMD − 1.30; 95% CI − 2.87 to 0.26, P =
0.10) (Fig. 4c).
C-reaction protein, albumin, and Interleukin-6
Three studies reported the C-reaction protein level on
postoperative day 1. There was no significant
difference between the two groups (WMD = − 8.34; 95% CI
− 25.05 to 8.37, P = 0.33) (Fig. 4d). Results suggested
that FTS group was associated with a lower level of
C-reaction protein on postoperative days (PODs) 3
and 4 (WMD − 19.66; 95% CI − 28.98 to − 10.34, P <
0.00001), and there was no significant difference
between the two groups on postoperative day 7 (WMD
− 18.65; 95% CI − 38.75 to 1.46, P = 0.07) (Fig. 4d).
Two studies reported the albumin level on
postoperative day 1. No significant difference was observed
between the two groups (WMD = 0.36; 95% CI − 0.56 to
1.27, P = 0.45) (Fig. 4e). However, the results showed
that FTS group was associated with a higher level of
albumin on postoperative day 4 (WMD 3.45; 95% CI
ERAS was first proposed by the Danish physician
Kehlet, with the aim of reducing surgical trauma and
facilitating postoperative recovery by the use of a
series of perioperative management [
laparoscopic surgery have garnered tremendous
popularity over open surgery with better short-term
outcomes, such as less operative bleeding, earlier bowel
movement, reduced pain, fewer overall complications,
and shorter postoperative hospital stays [
date, ERAS and laparoscopic technique have been
widely applied. However, the benefit of ERAS in
patients undergoing laparoscopic gastrectomy is still
unclear. To the best of our knowledge, this is the first
meta-analysis focus on this topic. Comparing with
previous meta-analyses mainly focus on open
gastrectomy, the surgical procedure of our study was limited
The results of the meta-analysis suggest that the
FTS group is associated with a significant reduction
in postoperative hospital stay, time to first flatus,
postoperative CRP, IL-6, and hospital charge as
compared with conventional care group. Additionally, no
difference in postoperative complications and
readmission rate was observed when comparing ERAS
and conventional care within LAG.
A shorter hospital stay was the advantage of
laparoscopic surgery. Our results showed that ERAS
combined with LAG could shorten the length of
postoperative hospital stay as compared with
conventional care. Meanwhile, we also found that all
included studies showed a consistent tendency favoring
the FTS group. A previous meta-analysis suggested
that ERAS combined with LAG are associated with a
significant reduction in postoperative hospital stay of
2.68 days as compared with conventional care. Our
meta-analysis showed that FTS group was associated
with a reduction in postoperative hospital stay of
2.16 days. Secondly, we found in the present study
that FTS group are associated with a significant
reduction in time to first flatus. Four included studies
with appropriate data that reported this outcome
showed a result favoring FTS group. It has been
widely accepted that both LAG and ERAS can reduce
surgical trauma and facilitating postoperative recovery.
Our results revealed that the combined effects of the
two methods can further accelerate clinical recovery
of the patients undergoing LAG.
Postoperative complication is the key indicator for
assessing the safety and feasibility of surgical procedure.
Extensive studies have shown that LAG is associated
with fewer complications, such as incision infection and
pneumonia as compared with OG. Meanwhile, one of
the main principles of the ERAS protocol is reducing
postoperative complications. Previous meta-analyses and
RCTs showed reduced postoperative complications and
readmission rate when ERAS was implemented in OG
14, 16, 28–30
]. A previous study in our department
demonstrated that the postoperative complication rate
in the FTS group was lower than that in the
conventional care group. They found that the ERAS protocol
could reduce the incidence of pneumonia. This benefit
may mainly attribute to the early ambulation of patients
]. Li et al. [
] also reported that the FTS group was
associated with a reduction in postoperative
complication rate following LAG. Our result also showed a
similar tendency favoring FTS, but there was no significant
difference between the two groups. The statistical
insignificance may be attributed to the reduction of some
common complications such as incision infection, and
pneumonia may have already been achieved by LAG,
leaving little room for improvement via the implement
of ERAS protocol. Additionally, it may also due to the
relative small sample size of the present study.
The use of abdominal drains following gastrectomy still
remains controversial. Prophylactic peritoneal drainage
has been widely used during gastrointestinal surgery
because of several advantages such as removing
intraperitoneal fluid and assisting the early detection of
postoperative hemorrhage or anastomotic leakage [
However, peritoneal drainage can cause uncomfortable
which may limit early mobilization and postoperative
recovery. There is evidence that abdominal drains do not
reduce the complication rate but increase intraperitoneal
fluid collection, infections, and risk of occurrence of
postoperative fistula [
]. Despite of these disadvantages,
peritoneal drainage is still commonly used for gastric cancer
surgery at most institutions. Only one of the included
studies in this meta-analysis did not use peritoneal
drainage as routine treatment [
]. Thus, the safety and efficacy
of no routine use of abdominal drainage tube need to be
assessed in further investigation.
It have been recognized widely that the advantages
of laparoscopic surgery such as alleviating surgical
stress and reducing respiratory interference could
accelerate postoperative recovery [
]. To date,
some authors have reported that ERAS protocol could
accelerate recovery by mitigating the inflammatory
14, 15, 38, 39
]. Our results suggest the
combination of the two methods can further alleviate the
inflammation and immune inhibition based on the
efficacy of a single method. Liu et al.  indicated
that FTS group showed lower C-reaction protein and
IL-6 levels (postoperative days 1, 4, and 7) compared
with the conventional care group. The level of serum
albumin is a nutritional status indicator. Our results
showed that the albumin in the FTS group was
higher than that in the conventional perioperative
care group on postoperative days 4 and 7. We
presumed that this difference may mainly attributed to
the early enteral nutrition (EN) improved
postoperative nutrition status in FTS group. In addition, several
meta-analyses have demonstrated that early EN may
decrease early occurrence of postoperative infections,
shorten the length of hospital stay and therefore
promote the postoperative recovery of paitents [
Researches have shown that laparoscopic surgery is
associated with better quality of life (QOL) as
compared with open surgery. Regarding the QOL
following ERAS combined with LAG, studies have been
seldom reported. Kim et al. [
] reported that the
ERAS protocol may have no negative effect on QOL
or patient satisfaction. Moreover, certain aspects of
QOL such as pain, fatigue, appetite loss, and financial
problems can be improved by the implement of ERAS
protocol. Our study has several limitations. First, the
included studies are all from Aisa and in relatively
small sample size, which may limited the
generalization of our results. Second, the differences
in patient characteristics is a source of bias that may
affect the stability of the results. Third, although time
to first flatus had low heterogeneity, other outcomes
had moderate or high heterogeneity. Moreover, the
compliance is varied among all included studies which
may reduce the benefits of ERAS protocol.
In conclusion, this meta-analysis indicates that ERAS
combined with laparoscopic technique is safe and
effective for gastric cancer and could significantly
decrease postoperative hospital stay, cost of
hospitalization, and time to first flatus without
increasing postoperative complication and readmission
rate. High-quality and larger-scale studies are needed
to provide more solid evidence.
This study was supported by the National Key Basic Research Program of
China (no. 2014CBA02002).
Availability of data and materials
All the data used in the study can be obtained from the original articles.
ZL and QZ performed the experiment conception and design. QW and BB
performed the research and retrieved the data. ZL and BL performed the
data analysis. ZL did the paper writing. All authors read and approved the
Ethics approval and consent to participate
All analyses were based on the previous published studies; thus, no ethical
approval and patient consent are required.
Consent for publication
All analyses were based on previous published studies; thus, no consent for
publication is required.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
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