Application of enhanced recovery after surgery in perioperative patients undergoing laparoscopic surgery for gastric cancer: A meta-analysis : Medicine

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Research Article: Systematic Review and Meta-Analysis

Application of enhanced recovery after surgery in perioperative patients undergoing laparoscopic surgery for gastric cancer: A meta-analysis

Yuan, Wei BDa; Huang, Guigui BDb; Dai, Peng BDa; Zhong, You MDa; Ai, Qiubao MDa; Liao, Qinghui BDc,*

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Medicine 102(11):p e32962, March 17, 2023. | DOI: 10.1097/MD.0000000000032962
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1. Introduction

Gastric cancer (GC), a malignancy derived from gastric epithelial cells, is currently 1 of the most common malignancies.[1] According to statistics, there were over 700,000 new GC cases in China in 2020, accounting for about half of the new cases globally.[2] In addition, due to the strong concealment of early-stage GC without special clinical symptoms as well as the lack of medical knowledge, patients often ignore or treat GC incorrectly, which also leads to the fact that GC has reached the middle and late stage in most cases by the time of diagnosis.[3] Surgery or/and chemoradiotherapy remains the mainstay of clinical treatment for GC, which contributes to relatively ideal therapeutic effects for early-stage GC, but no curative effect for advanced GC.[4] Although early-stage GC is highly likely to be cured, the diseased gastric tissue still needs to be excised during surgical treatment, which greatly affects the normal life of patients.[5] Therefore, when no new clinical treatment options for GC therapy have been identified, how to more effectively ensure the efficacy and safety of radical GC resection has also become critical in determining the prognosis of patients.

In modern clinical research, researchers can effectively address the negative effects caused by radical surgery for GC through targeted care strategies. For example, Wen et al[6] showed that holistic nursing under the social medical model can improve the quality of life of GC patients, while Yin et al believed that information-knowledge-attitude-practice nursing intervention can enhance the self-management ability of GC patients,[7] which fully demonstrated that modern nursing services with more characteristics gradually became a breakthrough to improve clinical treatment effect. Among all kinds of characteristic nursing strategies, enhanced recovery after surgery (ERAS) puts forward a nursing strategy that uses a series of optimized treatment measures proven effective by evidence-based medical evidence to intervene in order to make patients recover quickly, which has achieved extremely remarkable clinical application results at present.[8–10] ERAS protocols, which have lower rates of complication, faster postoperative recovery, lower costs, shorter postoperative hospital stays, and lower surgical morbidity, were first used in colorectal surgery, expanding gradually to obstetrics and gynecology, urology, and pelvic surgery.[11–16] For GC, there is also relevant research showing the excellent application effect of ERAS.[17] However, the application of ERAS in GC is controversial because it needs to shorten the postoperative bed time of patients and force them to complete rehabilitation exercises, and some researchers hold that it will aggravate the postoperative injuries of patients.[18]

Consequently, this study will systematically analyze the application of ERAS in perioperative patients undergoing laparoscopic radical surgery for GC, so as to provide a reliable reference for the subsequent application of ERAS in GC and ensure the safety and the prognosis of GC patients.

2. Materials and methods

2.1. Search strategy

We searched the literature databases of PubMed ( and Web of Science ( for studies related to ERAS and laparoscopic surgery for GC from their inception till October 2022.

2.2. Selection criteria

The inclusion criteria were as follows: the nature of the study was set as a clinical cohort study or randomized controlled trial; The research participants were GC patients undergoing laparoscopic surgery; The research content was a comparison of clinical application effects between ERAS and other care approaches. The exclusion criteria were as follows: Articles with obvious logic errors or design defects, lack of objective reference criteria for evaluation indicators, follow-up success rate < 80%, or conflicts of interest were excluded.

2.3. Quality evaluation

Literature quality was assessed from the following dimensions by referring to the Cochrane risk of bias tool:[19] random sequence generation; allocation concealment; blinding; nonselective reporting; other bias. The literature quality was defined as low, medium or high risk depending on the actual situation of the article, with lower risk representing higher reference value of the literature. The quality assessment was independently completed by 2 members of the research team.

2.4. Data extraction

After identifying eligible studies, the members of the research team read the full text and extracted relevant information such as the authors, research years, grouping methods, basic information of the research subjects, intervention measures, endpoints, and statistical methods of the literature.

2.5. Endpoints

First postoperative exhaust time: the interval between the completion of surgery and the first gastrointestinal exhaust time was recorded; First postoperative bowel movement: the time from the completion of the operation and the first defecation of the patient was recorded; length of stay (LOS): the time between the completion of surgery and patient discharge was counted; Complications: complications (incision infection, fever, lung infection, etc.) that occurred postoperatively were observed, and the incidence of complications was calculated; Hospitalization expenses: all expenses spent on hospitalization and treatment were calculated.

2.6. Statistical analyses

EndNote X9 software was employed for literature arrangement and preservation, and RevMan 5.4 software for meta-analysis and graphic drawing. The mean differences test and odds ratio test were utilized for comparisons of measurement data and counting data, respectively. In case of heterogeneity among studies, the random-effects model was used for analysis, and a funnel plot was drawn for verification (basic symmetry on both sides indicates low bias of results); in the absence of heterogeneity, a fixed-effects model was applied for analysis. P < .05 was considered statistically significant.

2.7. Ethics statement

The ethical approval was not required for this study, because this study is a meta-analysis.

3. Results

3.1. Literature retrieval results

A total of 197 papers related to ERAS and laparoscopic surgery for GC were retrieved from PubMed and Web of Science databases. After software deduplication, manual reading and retrieval criteria screening, and 11 papers were finally included for meta-analysis (the literature retrieval process is shown in Fig. 1).[20–30] The quality of the included literature was mainly of low and medium risk, with high reference value (Fig. 2).

Figure 1.:
Literature retrieval process.
Figure 2.:
Literature quality evaluation.

3.2. Basic characteristics of research subjects

Among the 11 articles, a total of 2039 subjects were enrolled, of which 998 patients receiving ERAS were regarded as the experimental group (e.g.,), and another 1041 patients receiving routine care were set as the control group (CG). Patients basic characteristics and endpoints are presented in Table 1.

Table 1 - Basic characteristics of research subjects.
Author e.g. CG Endpoints
n Age M/F n Age M/F
Wang Y 2021[20] 44 54.5 ± 5.4 25/19 44 55.2 ± 6.0 20/24 (1) (2) (3) (4)
Kang SH 2018[21] 46 56.3 ± 10.4 33/13 51 54.5 ± 12.6 38/13 (1) (3)
Weindelmayer J 2021[22] 248 60–76 154/94 103 60–78 55/48 (3) (4)
Jeong O 2021[23] 219 61.9 ± 11.4 146/73 219 61.2 ± 10.8 145/74 (3) (4)
Tian Y 2022[24] 186 58.3 ± 10.5 129/57 184 58.6 ± 10.9 124/60 (1) (2) (3) (4) (5)
Xiao SM 2022[25] 50 72.7 ± 2.7 36/14 50 72.3 ± 2.3 38/12 (3) (4) (5)
Desiderio J 2018[26] 20 61.0 ± 16.0 8/12 40 63.0 ± 14.0 19/21 (1) (2) (3) (4)
Chen JX 2022[27] 23 67.6 ± 8.7 17/6 26 66.2 ± 8.4 17/9 (1) (2) (3)
Wang WK 2019[28] 30 58.22 ± 4.31 25/5 30 59.26 ± 5.35 23/7 (1) (2) (3) (4) (5)
Zhou J 2017[29] 30 63.2 ± 9.8 16/14 30 60.5 ± 11.6 18/12 (1) (2) (4)
Ji W 2018[30] 102 34–79 62/40 264 37–79 133/131 (1) (3) (5)
(1) First postoperative exhaust time; (2) First postoperative bowel movement; (3) LOS; (4) Complications; (5) Hospitalization expenses.

3.3. Meta-analysis results

3.3.1. First postoperative exhaust time.

As shown in Table 2, 8 papers reported the first postoperative exhaust time of patients, with heterogeneity among them (I2 = 89%), so the random-effects model was used for analysis. As shown in Figure 3, the first postoperative exhaust time was shorter in for example than in CG (P < .05). Subsequently, a funnel plot of the first postoperative exhaust time was drawn (Fig. 4), and it can be seen that both sides of the plot were basically symmetrical, confirming that the results were less biased.

Table 2 - The results of meta-analysis.
Factors Patients Effect (95% CI) Heterogeneity test Statistical model
First postoperative exhaust time 1148 MD = −2.15, 95%CI [−3.41; −0.89] 89% Random
First postoperative bowel movement 685 MD = −4.49, 95%CI [−7.13; −1.86] 91% Random
 LOS 1977 MD = −2.20, 95%CI [−2.86; −1.54] 93% Random
 Complications 221 OR = 0.57, 95%CI [0.43;0.78] 2% Fixed
 Hospitalization expenses 894 MD = −601.53, 95%CI [−858.75; −344.31] 87% Random
CI = confidence interval, LOS = length of stay, MD = mean differences, OR = odds ratio.

Figure 3.:
Forest plots of first postoperative exhaust time.
Figure 4.:
Funnel plot of first postoperative exhaust time.

3.3.2. First postoperative bowel movement.

As shown in Table 2, the first postoperative bowel movement was reported in 6 papers with heterogeneity among them (I2 = 92%), so the random-effects model was used for analysis. As shown in Figure 5, for example had shorter time of the first postoperative bowel movement than CG (P < .05). A funnel plot of the first postoperative bowel movement was drawn (Fig. 6), it can be seen that both sides of the plot were basically symmetrical.

Figure 5.:
Forest plots of first postoperative bowel movement.
Figure 6.:
Funnel plot of first postoperative bowel movement.

3.3.3. LOS.

As shown in Table 2, given the presence of heterogeneity among the 10 articles reporting the LOS of patients (I2 = 93%), the random-effects model was employed for analysis, with the results (Fig. 7) indicating shorter LOS in for example as compared to CG (P < .05). Similarly, a funnel plot plotting the LOS (Fig. 8) showed that the 2 sides of the graph were symmetrical, suggesting little results bias.

Figure 7.:
Forest plots of LOS. LOS = length of stay.
Figure 8.:
Funnel plot of LOS. LOS = length of stay.

3.3.4. Complications.

As shown in Table 2, heterogeneity was no present in the 8 articles that analyzed complications in patients (I2 = 2%). The fixed-effects model analysis (Fig. 9) revealed a lower incidence of complications in for example compared with CG (P < .05).

Figure 9.:
Forest plots of complications.

3.3.5. Hospitalization expenses.

As shown in Table 2, 4 papers investigated hospitalization expenses, with heterogeneity among them. The results of the random-effects model analysis (Fig. 10) identified that the hospitalization expenses were lower in for example than in CG (P < .05). The funnel plot of Hospitalization expenses shows that the figure is basically symmetrical (Fig. 11).

Figure 10.:
Forest plots of hospitalization expenses.
Figure 11.:
Funnel plot hospitalization expenses.

4. Discussion

At present, the incidence of GC continues to rise worldwide, and surgery, as the most effective and direct treatment for GC, is increasingly used in clinical practice.[31] Due to the possibility of surgical resection of part of gastric tissue and the inevitable stress injury caused by invasive mechanical operation, how to improve the safety of GC surgery more effectively has become 1 of the key links affecting patient outcomes.[32] ERAS is a model of multidisciplinary collaboration in modern clinical care, integrating surgery, anesthesiology, nursing and nutrition.[33] Among them, nursing is 1 of the most critical and important links, which has been proved to have excellent application effects in mitigating patients bad psychology, improving overall surgical outcomes, and reducing postoperative complications.[34,35] However, for GC, the application of ERAS is still controversial due to the lack of reliable clinical guidelines. Thus, this study focuses on the application value of ERAS in GC patients undergoing laparoscopic surgery, which is of important clinical implications.

Through meta-analysis, we found that compared with routine care, the first postoperative exhaust time, first postoperative bowel movement and LOS of GC patients cared for by ERAS were obviously shortened, and the incidence of complications and the hospitalization expenses were obviously reduced, indicating that ERAS can effectively promote the recovery of patients undergoing laparoscopic surgery for GC, which is also in line with previous studies on the application of ERAS.[36–38] Combined with previous research findings, we believe that the application advantages of ERAS are mainly reflected in the following points: As we all know, due to the torment of the disease and the fear of surgery, patients usually have a serious adverse emotional burden before surgery, which may not only affect their postoperative recovery, but also increase their resistance to medical staff and reduce their treatment compliance.[39] In ERAS, it is required to strengthen patients health education and psychological nursing during perioperative period, which can effectively eliminate patients concerns about the disease and surgery, and improve their psychological state; Perioperative nutritional support and early rehabilitation training can speed up the recovery of patients gastrointestinal function, which facilitates their recovery on the 1 hand, and reduce the incidence of complications such as pulmonary infection and lower extremity deep venous thrombosis on the other.[40] This is of great significance to shorten the overall rehabilitation cycle of patients, improve the safety of laparoscopic surgery and reduce medical expenses; For medical staff, ERAS not only improves the quality of the overall medical service through multidisciplinary collaboration, but also reduces the workload of nurses, enabling nurses to provide more professional and meticulous services for patients, and significantly improving the treatment experience of patients. In the previous research, we also found that the patients’ satisfaction with treatment was obviously improved after the use of ERAS.[41] But this research did not analyze patient satisfaction, as this index is rarely reported in the articles included in this study.

Of course, improvements in various measures may not only be attributed to ERAS, but may also have some potential connection with laparoscopic surgery. Compared with traditional open surgery, laparoscopic surgery itself has the advantages of less trauma and faster postoperative recovery.[42] Besides, this procedure does not require preoperative bowel preparation and allows patients to eat liquid food and glucose to supplement nutrition, which also creates an ideal state for the postoperative rehabilitation of patients and reduces the adverse reactions caused by long-term fasting.[43] At present, laparoscopic surgery has been considered the first choice for GC radical surgery. Based on the results of the above experiments, we believe that in the future, ERAS can further improve surgical safety and provide a more reliable prognosis guarantee for perioperative patients undergoing laparoscopic surgery for GC.

However, there are some limitations to be improved in this study. For example, surgical techniques are also 1 of the keys to patients’ rehabilitation, and there are certainly some differences in surgical techniques across studies, which may also contribute to some bias in the results. In addition, there may be artificial statistical errors since data such as the time of first postoperative exhaust and defecation are subjective statistical results. In this regard, it is hoped that the sample size can be expanded in follow-up clinical research, the random method can be correctly adopted, the allocation concealment and blinding can be rationally used, and relevant indicators can be objectively evaluated, so as to reduce the occurrence of various biases and provide more reasonable and accurate reference opinions for clinical practice.

5. Conclusion

ERAS for perioperative patients undergoing laparoscopic surgery for GC can effectively shorten the postoperative rehabilitation cycle of patients, improve surgical safety and reduce treatment costs, with a very high clinical application value.

Author contributions

Conceptualization: Wei Yuan, Qinghui Liao.

Data curation: Wei Yuan, Guigui Huang, Peng Dai, You Zhong, Qiubao Ai, Qinghui Liao.

Formal analysis: Wei Yuan, Qinghui Liao.

Funding acquisition: Guigui Huang.

Investigation: Wei Yuan, Peng Dai, You Zhong, Qiubao Ai, Qinghui Liao.

Methodology: Guigui Huang, Peng Dai, Qinghui Liao.

Project administration: Wei Yuan, Peng Dai, Qinghui Liao.

Resources: Wei Yuan, Guigui Huang, You Zhong, Qiubao Ai, Qinghui Liao.

Software: Wei Yuan, Qinghui Liao.

Supervision: Peng Dai, You Zhong, Qiubao Ai, Qinghui Liao.

Validation: Wei Yuan, You Zhong, Qiubao Ai.

Visualization: Wei Yuan.

Writing – original draft: Wei Yuan.

Writing – review & editing: Qinghui Liao.


enhanced recovery after surgery
gastric cancer
length of stay


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enhanced recovery after surgery; gastric cancer; laparoscopic surgery; meta-analysis; postoperative rehabilitation

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