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Outcomes of enhanced recovery after surgery in lung cancer: A systematic review and meta-analysis

  • Wenhui Zhang
    Affiliations
    Department of Thoracic Surgery, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China

    Department of Thoracic Surgery, Nantong Key Laboratory of Translational Medicine in Cardiothoracic Diseases, and Research Institution of Translational Medicine in Cardiothoracic Diseases in Affiliated Hospital of Nantong University, Nantong, China
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  • Yuting Zhang
    Affiliations
    Department of Thoracic Surgery, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China

    Department of Thoracic Surgery, Nantong Key Laboratory of Translational Medicine in Cardiothoracic Diseases, and Research Institution of Translational Medicine in Cardiothoracic Diseases in Affiliated Hospital of Nantong University, Nantong, China
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  • Yi Qin
    Affiliations
    Department of Nursing, Affiliated Hospital of Nantong University, Nantong, China
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  • Jiahai Shi
    Correspondence
    Corresponding author.
    Affiliations
    Department of Thoracic Surgery, Nantong Key Laboratory of Translational Medicine in Cardiothoracic Diseases, and Research Institution of Translational Medicine in Cardiothoracic Diseases in Affiliated Hospital of Nantong University, Nantong, China
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Open AccessPublished:June 29, 2022DOI:https://doi.org/10.1016/j.apjon.2022.100110

      Abstract

      Objective

      To assess the effect of ERAS on clinical prognosis in perioperative patients following lung cancer surgery.

      Methods

      PubMed, Web of Science, MEDLINE, EMBASE, and other databases were systematically searched from inception to December 2021. Randomized controlled trials and peer-reviewed cohort studies on the use of ERAS in lung cancer surgery patients were included. Primary outcomes comprised visual analog scale scores after treatment and quality of life. Secondary outcomes comprised complication rate, function-related outcomes (chest tube indwelling time and first ambulation), and length of stay. Statistical analysis was performed using RevMan 5.4.1 software.

      Results

      Finally, 23 studies were included (12 cohort studies and 11 randomized controlled trials) with a total of 8094 patients. Meta-analysis showed that ERAS significantly reduced visual analog scale scores (mean difference [MD] = −1.99, 95% confidence interval [CI] = −2.45, −1.54, P < 0.01), reduced the incidence of complications (odds ratio = 0.48, 95% CI = 0.37, 0.61, P < 0.01), shortened chest tube indwelling time (MD = −2.20, 95% CI = −2.75, −1.64, P < 0.01), accelerated first ambulation (MD = −1.48, 95% CI = −1.77, −1.19, P < 0.01), shortened length of stay (MD = −2.70, 95% CI = −3.05, −2.36, P < 0.01), and improved quality of life (MD = 10.3, 95% CI = 9.59, 11.02, P < 0.01).

      Conclusions

      ERAS can accelerate postoperative recovery and improve quality of life. These findings support the use of ERAS as a standard of care for lung cancer surgery patients. However, the evidence quality was moderate and there were significant differences among studies. More high-quality studies incorporating relevant outcomes are needed for confirmation.

      Keywords

      Introduction

      The morbidity and mortality of lung cancer are high worldwide.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Surgical resection is the preferred treatment for patients with stage I–IIIA lung cancer.
      • Nasim F.
      • Sabath B.F.
      • Eapen G.A.
      Lung cancer.
      To improve the treatment effect, a minimally invasive technique was introduced in the field of lung cancer several years ago.
      • Flores R.M.
      • Alam N.
      Video-assisted thoracic surgery lobectomy (VATS), open thoracotomy, and the robot for lung cancer.
      Concomitant with economic development, research on minimally invasive surgery continues to progress, the technology continues to mature, and video-assisted thoracoscopic surgery (VATS) is becoming increasingly popular. VATS is a non-rib-spreading thoracic procedure. It enables the real-time observation of the surgical procedure in the chest cavity via TV screen and thoracoscope. The VATS incision is approximately 5–8 ​cm. It comprises a true anatomic lobectomy with the individual dissection of lobar vessels and bronchus, as well as standard lymph node dissection or sampling.
      • Swanson S.J.
      • Herndon 2nd, J.E.
      • D'Amico T.A.
      • et al.
      Video-assisted thoracic surgery lobectomy: report of CALGB 39802--a prospective, multi-institution feasibility study.
      ,
      • Yan T.D.
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      • D'Amico T.A.
      • et al.
      Video-assisted thoracoscopic surgery lobectomy at 20 years: a consensus statement.
      Despite the acceptance of VATS, it is associated with several serious postoperative complications, such as pleural effusion and pneumothorax.
      • Manerikar A.
      • Querrey M.
      • Cerier E.
      • et al.
      Comparative effectiveness of surgical approaches for lung cancer.
      Poor lung function before the operation, incorrect intraoperative procedure, and postoperative sputum accumulation are some of the factors that cause complications. Complications can have many negative effects on patients and can increase the risk of cancer recurrence.
      • Lerut T.
      • Moons J.
      • Coosemans W.
      • et al.
      Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification.
      Patients who have had technical surgical complications are more likely to experience dyspnea, fatigue, and vomiting, which can substantially affect their overall quality of life.
      • Derogar M.
      • Orsini N.
      • Sadr-Azodi O.
      • Lagergren P.
      Influence of major postoperative complications on health-related quality of life among long-term survivors of esophageal cancer surgery.
      Therefore, perioperative management must be strengthened to reduce adverse clinical outcomes.
      Enhanced recovery after surgery (ERAS) is a multidisciplinary perioperative care program that includes strategies such as preoperative education, shortening of fasting time, optimization of anesthesia protocols, and early mobilization.
      • Ljungqvist O.
      • Scott M.
      • Fearon K.C.
      Enhanced recovery after surgery: a review.
      By implementing these strategies, it is possible to accelerate recovery and improve quality of life.
      • Ljungqvist O.
      • Hubner M.
      Enhanced recovery after surgery-ERAS-principles, practice and feasibility in the elderly.
      ,
      • Keil D.S.
      • Schiff L.D.
      • Carey E.T.
      • et al.
      Predictors of admission after the implementation of an enhanced recovery after surgery pathway for minimally invasive gynecologic surgery.
      ERAS was originally implemented in patients with colorectal cancer and has been widely used in various disciplines in recent years.
      • Gustafsson U.O.
      • Scott M.J.
      • Schwenk W.
      • et al.
      Guidelines for perioperative care in elective colonic surgery: enhanced Recovery after Surgery (ERAS((R))) Society recommendations.
      Meta-analyses have shown that ERAS has substantial positive effects in colorectal, liver, and pancreatic surgery.
      • Visioni A.
      • Shah R.
      • Gabriel E.
      • Attwood K.
      • Kukar M.
      • Nurkin S.
      Enhanced recovery after surgery for noncolorectal surgery?: a systematic review and meta-analysis of major abdominal surgery.
      In recent years, ERAS has been used in lung cancer surgery; however, its safety and effectiveness remain controversial.
      • Huang L.
      • Kehlet H.
      • Petersen R.H.
      Reasons for staying in hospital after video-assisted thoracoscopic surgery lobectomy.
      ,
      • Kehlet H.
      Enhanced postoperative recovery: good from Afar, but far from good?.
      The number of systematic reviews of ERAS is limited. Three systematic reviews of patients undergoing lung cancer surgery concluded that ERAS can substantially accelerate postoperative recovery; however, the overall reliability of the evidence is poor.
      • Fiore Jr., J.F.
      • Bejjani J.
      • Conrad K.
      • et al.
      Systematic review of the influence of enhanced recovery pathways in elective lung resection.
      • Li S.
      • Zhou K.
      • Che G.
      • et al.
      Enhanced recovery programs in lung cancer surgery: systematic review and meta-analysis of randomized controlled trials.
      • Li R.
      • Wang K.
      • Qu C.
      • et al.
      The effect of the enhanced recovery after surgery program on lung cancer surgery: a systematic review and meta-analysis.
      The effect of ERAS on postoperative pain and quality of life had not been examined. Therefore, this meta-analysis aimed to further investigate the effect of ERAS on clinical outcomes, comprising postoperative pain, quality of life, complication rate, function-related outcomes, and length of stay (LOS) in patients who had undergone lung cancer surgery.

      Methods

      Eligibility criteria

      Inclusion criteria

      Participants

      The review included studies of patients with lung cancer undergoing surgery whose clinical diagnosis complied with the guidelines for the diagnosis and treatment of non-small cell lung cancer.

      NCCN clinical practice guidelines in oncology: non-small cell lung cancer. Available from: https://www.nccn.org/professionals/physician_gls/.

      Interventions

      Studies in which the ERAS measures included at least one strategy before, during, and after the surgery compared with standard care were included.

      Outcomes

      We assessed the following outcomes: visual analog scale (VAS) score, quality of life (36-item Short-Form, SF-36), complication rate, function-related outcomes (chest tube indwelling time and first ambulation), and LOS. All included studies reported on at least one of the outcome measures.

      Study design

      We included peer-reviewed cohort studies and randomized controlled trials (RCTs).

      Exclusion criteria

      Participants

      Studies with a sample size of < 30 cases were excluded.
      • Triantafyllou T.
      • Olson M.T.
      • Theodorou D.
      • Schizas D.
      • Singhal S.
      Enhanced recovery pathways vs standard care pathways in esophageal cancer surgery: systematic review and meta-analysis.
      Smaller sample sizes introduce greater random error coupled with publication bias, which may exaggerate the effectiveness of interventions.
      • Dechartres A.
      • Trinquart L.
      • Boutron I.
      • Ravaud P.
      Influence of trial sample size on treatment effect estimates: meta-epidemiological study.

      Studies

      The following study types were excluded: studies in languages other than Chinese and English, conference abstracts, reviews, studies for which the full text was not available, and studies lacking sufficient data.

      Data sources and search strategy

      We searched PubMed, Cochrane Library, Web of Science, MEDLINE, EMBASE, CNKI, WanFang, and VIP from database inception to December 2021. The focus of the review was lung cancer and ERAS. Details of the Web of Science search strategies are shown in Table 1; the other databases were searched using the same strategies. We also manually searched the gray literature to ensure that no relevant sources were omitted.
      Table 1Details of the Web of Science search strategies.
      Web of ScienceSearch strategy
      #1(((((((((((((((((TS = (Lung neoplasms)) OR TS = (Pulmonary Neoplasms)) OR TS = (Neoplasms, Lung)) OR TS = (Lung Neoplasm)) OR TS = (Neoplasm, Lung)) OR TS = (Neoplasms, Pulmonary)) OR TS = (Neoplasm, Pulmonary)) OR TS = (Pulmonary Neoplasm)) OR TS = (Lung Cancer)) OR TS = (Cancer, Lung)) OR TS = (Cancers, Lung)) OR TS = (Lung Cancers)) OR TS = (Pulmonary Cancer)) OR TS = (Cancer, Pulmonary)) OR TS = (Cancers, Pulmonary)) OR TS = (Pulmonary Cancers)) OR TS = (Cancer of the Lung)) OR TS = (Cancer of Lung)
      #2(((((((((TS = (enhanced recovery after surgery)) OR TS = (fast-track surgery)) OR TS = (fast-track rehabilitation)) OR TS = (enhanced recovery)) OR TS = (enhanced recovery after surgery program)) OR TS = (ERAS)) OR TS = (FTS)) OR TS = (Early recovery)) OR TS = (clinical pathway)) OR TS = (critical pathways)
      #3(TS = (Randomized controlled trial)) OR TS = (cohort study)
      #4((#1) AND #2) AND #3

      Data extraction

      Data extraction followed the principles of Hozo et al
      • Hozo S.P.
      • Djulbegovic B.
      • Hozo I.
      Estimating the mean and variance from the median, range, and the size of a sample.
      It was important to obtain detailed data for each study to address the purpose of this review. The main data extracted were study characteristics (first author, country, year, and study design), patient characteristics (age, sample size per arm, and percentage of male participants), interventions, and outcome measures. Two evaluators (ZW and ZYT) independently selected studies and extracted data from each study, then jointly compared the collected data. Any disagreements about the results were resolved through consensus or consultation with a third evaluator.

      Risk of bias assessment

      The Newcastle–Ottawa Quality Assessment Scale (NOS)
      • Stang A.
      Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses.
      and the Cochrane risk of bias tool
      • Cumpston M.
      • Li T.
      • Page M.J.
      • et al.
      Updated guidance for trusted systematic reviews: a new edition of the Cochrane Handbook for Systematic Reviews of Interventions.
      was used for the quality assessment of cohort studies and RCTs. The NOS assesses three quality parameters: selection, comparability, and outcome. A cohort study with a NOS score of ≥ 7 is regarded as having low risk of bias; low NOS scores indicate high risk of bias. The risk of bias tool assesses the following domains: selection bias, performance bias, detection bias, attrition bias, reporting bias, and other risks of bias. Studies were judged on each domain as showing high, low, or unclear risk of bias. Two evaluators jointly checked all studies and reached a consensus.

      Data analysis

      Statistical analysis was performed using Review Manager 5.4.1 (The Cochrane Collaboration, London, United Kingdom). The combined effect size was obtained by calculating the mean difference (MD) for continuous variables and the odds ratio (OR) for dichotomous variables. The effect size was calculated using the 95% confidence interval (CI). Moreover, for studies that expressed data using interquartile ranges or medians, the data were transformed using the estimation method proposed by Wan et al
      • Luo D.
      • Wan X.
      • Liu J.
      • Tong T.
      Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range.
      Heterogeneity was inevitable because the setting of each study was different and was assessed using the Q test and I2. The random-effects model was used if the heterogeneity was significant (I2 > 50% or P < 0.10). Otherwise, the fixed-effects model was used.
      • DerSimonian R.
      • Laird N.
      Meta-analysis in clinical trials.
      ,
      • Mantel N.
      • Haenszel W.
      Statistical aspects of the analysis of data from retrospective studies of disease.
      Subgroup analysis was used to confirm the robustness of the meta-analysis. Sensitivity analysis was performed by excluding one study at a time. We also re-analyzed the data using a fixed-effects model. P < 0.05 was considered statistically significant. Publication bias was assessed using Egger's test; values of P < 0.05 indicate publication bias.
      • Sterne J.A.
      • Sutton A.J.
      • Ioannidis J.P.
      • et al.
      Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials.

      Results

      Study characteristics

      In total, 3654 studies were retrieved. After removing duplicates, we reviewed 2351 titles and abstracts. We read the full text of 115 studies and finally included 23 studies according to the inclusion criteria.
      • Brunelli A.
      • Thomas C.
      • Dinesh P.
      • Lumb A.
      Enhanced recovery pathway versus standard care in patients undergoing video-assisted thoracoscopic lobectomy.
      • Madani A.
      • Fiore Jr., J.F.
      • Wang Y.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      • Cai Q.
      Multidisciplinary enhanced recovery after surgery in video-assisted thoracoscopic surgery for lung cancer.
      • Che Q.
      • Wang H.
      • Li Y.
      • Xia H.
      Application of rapid rehabilitation in perioperative nursing of early non- small cell lung cancer.
      • Fan X.
      • Jiao J.
      • Zhu W.
      • Yin J.
      Application of enhanced recovery after surgery in perioperative nursing of patients undergoing radical resection of lung cancer.
      • Forster C.
      • Doucet V.
      • Perentes J.Y.
      • et al.
      Impact of an enhanced recovery after surgery pathway on thoracoscopic lobectomy outcomes in non-small cell lung cancer patients: a propensity score-matched study.
      • Haro G.J.
      • Sheu B.
      • Marcus S.G.
      • et al.
      Perioperative lung resection outcomes after implementation of a multidisciplinary, evidence-based thoracic ERAS program.
      • Huang H.
      • Ma H.
      • Chen S.
      Enhanced recovery after surgery using uniportal video-assisted thoracic surgery for lung cancer: a preliminary study.
      • Li Y.
      • Yi H.
      • Xiao Y.
      • Chen X.
      • Guo L.
      Fast rehabilitation surgery in application of radical operation for lung cancer under thoracoscope.
      • Li L.
      • Zhao R.
      • Wang H.
      • Zheng X.
      • Zhao R.
      Interventional effect of fast track suegery concept on lung cancer patients during perioperative period.
      • Li J.
      The effect of rapid rehabilitation surgical nursing on postoperative lung function recovery and quality of life in patients undergoing thoracoscopic radical resection of lung cancer.
      • Salati M.
      • Brunelli A.
      • Xiume F.
      • Refai M.
      • Pompili C.
      • Sabbatini A.
      Does fast-tracking increase the readmission rate after pulmonary resection? A case-matched study.
      • Van Haren R.M.
      • Mehran R.J.
      • Mena G.E.
      • et al.
      Enhanced recovery decreases pulmonary and cardiac complications after thoracotomy for lung cancer.
      • Shiono S.
      • Endo M.
      • Suzuki K.
      • Hayasaka K.
      Impact of enhanced recovery after surgery on outcomes of elderly patients undergoing open thoracic surgery.
      • Tahiri M.
      • Goudie E.
      • Jouquan A.
      • Martin J.
      • Ferraro P.
      • Liberman M.
      Enhanced recovery after video-assisted thoracoscopic surgery lobectomy: a prospective, historically controlled, propensity-matched clinical study.
      • Wang J.
      • Ni B.
      • Ma H.
      The application of fast- track surgery in thoracoscopic lung cancer operation for the aged patients.
      • Wang T.
      Clinical study of perioperative and serum indexex variation and prognostic relevance in the application of FTS in treatment of stage Ⅰ~Ⅱ non-small cell lung cancer.
      • Wang C.
      • Lai Y.
      • Li P.
      • Su J.
      • Che G.
      Influence of enhanced recovery after surgery (ERAS) on patients receiving lung resection: a retrospective study of 1749 cases.
      • Xu F.
      Application of Rapid Rehabilitation (ERAS) in Thoracoscopy for Radical Lung Cancer Surgery.
      • Zhang X.
      • Xie D.
      • Chen C.
      • Lin J.
      Investigation on the application of the concept of rapid rehabilitation surgery in the perioperative period of thoracoscopic lung cancer radical surgery.
      • Zhang Z.
      Application of the concept of enhanced recovery after surgery in thoracoscopic radical resection of lung cancer.
      • Zhao G.
      • Huang Y.
      • Chen X.
      • et al.
      Research on fast track surgery application in lung cancer surgery.
      • Zheng C.
      Effect of enhanced recovery after surgery on postoperative rehabilitation and quality of life of elderly patients undergoing thoracoscopic radical resection of lung cancer.
      A flow chart outlining the search strategy is shown in Fig. 1. The 23 studies involved a total of 8094 patients, 3151 in the ERAS group and 4943 in the control group. Of the included studies, 12 were cohort studies and 11 were RCTs. The average age of the study population ranged from 55 to 80 years, and approximately 65% of participants were men. Table 2 summarizes the baseline characteristics of each included study. Each study used different ERAS measures; details of the perioperative measures are shown in Table 2.
      Fig. 1
      Fig. 1Study selection flowchart. Transparent reporting outline of the search strategy results from initial search to included studies.
      Table 2Basic characteristics of included studies.
      StudyCountryStudy designCases ERAS/control%

      Male
      Intervention measuresOutcomes
      Alessan 2017United KingdomRCS235/36542.1/40A, B, C, E, H, J, I, MComplication
      Amin 2015CanadaRCS107/12761/45A, F, H, I, J, KComplication, LOS, chest tube indwelling time
      Cai 2018ChinaPCS62/5966.1/66.1A, C, E, F, H, I, J, KVAS, LOS, first ambulation, complication
      Che 2018ChinaRCT75/7566.7/64A, E, F, H, IVAS, chest tube indwelling time, LOS, first ambulation, complication
      Fan 2019ChinaRCT100/8063/63.8A, C, E, F, H, I, J, LLOS, chest tube indwelling time, first ambulation, complication
      Forster 2021SwitzerlandRCS140/16747.1/58.7A, E, F, H, I, JComplication, LOS, chest tube indwelling time
      Greg 2019USAPCS126/16931/43.8C, E, F, H, ILOS
      Huang 2018ChinaRCS38/4542.1/55.6A, B, C, F, H, I, JComplication, VAS, chest tube indwelling time, LOS
      Li 2017ChinaRCT80/8066.3/61.3A, F, H, J, KVAS, LOS, complication, chest tube indwelling time, first ambulation
      Li 2018ChinaRCT50/5060/62A, B, F, H, I, J, KVAS, LOS, complication, chest tube indwelling time
      Li 2020ChinaRCT40/4067.5/62.5A, C, E, F, H, I, J, KQoL, complication
      Michele 2012ItalyRCS232/232NRA, B, C, D, E, F, H, I, J, K, MComplication, LOS
      Robert 2018USARCS342/161547.4/50A, B, E, F, H, I, J, K, LComplication, LOS, chest tube indwelling time
      Satoshi 2019JapanRCS130/40566.2/57A, B, C, D, E, F, G, H, I, J, K, L, MComplication
      Tahiri 2020CanadaRCS98/9836.7/29.6A, C, E, F, H, I, J, KComplication, LOS, chest tube indwelling time, first ambulation
      Wang 2015ChinaRCT54/5468.5/64.8A, B, C, E, F, H, I, J, K, LVAS, chest tube indwelling time, first ambulation, LOS, complication
      Wang 2019ChinaRCT45/4568.9/64.4A, E, H, I, J, K, LVAS, LOS, first ambulation, complication, chest tube indwelling time
      Wang 2021ChinaRCS691/105850.8/49.8A, C, D, E, F, H, J, KComplication, LOS, chest tube indwelling time
      Xu 2020ChinaPCS60/6046.7/55A, B, C, E, F, H, I, J, KVAS, LOS, complication
      Zhang 2017ChinaRCT50/5052/50A, B, C, E, F, H, I, J, KVAS, chest tube indwelling time, QoL, complication, LOS
      Zhang 2019ChinaRCT106/10665.1/51.9A, B, D, E, F, H, I, J, K, LVAS, chest tube indwelling time, LOS, first ambulation, complication
      Zhao 2010ChinaRCT38/3663.2/69.4C, D, E, F, H, IVAS, LOS, complication
      Zheng 2019ChinaRCT43/4367.4/72.1A, E, F, G, H, I, J, KVAS, LOS, chest tube indwelling time, QoL, complication
      ERAS, enhanced recovery after surgery; RCT, randomized controlled trial; PCS, prospective cohort study; RCS, retrospective cohort study; VAS, visual analog scale; QoL, quality of life; LOS, length of stay.
      Intervention measures. Preoperative (A) Patient education, the importance of smoking and alcohol reduction, and nutritional supplements (B) Respiratory function exercise and incentive spirometer instruction (C) Shortened fasting and water period (D) Psychological care, good communication through understanding needs. Intraoperative (E) Intraoperative warming, such as controlling the temperature of the operating room, applying warm water bags and other devices (F) Optimizing the anesthesia method, selecting the appropriate anesthetic drugs (G) Avoidance of fluid overload. Postoperative (H) Multimodal analgesia (I) Restriction of use/early removal of surgical drains (J) Early mobilization, basic activities in bed after awakening, and getting out of bed 1 day after surgery (K) Early feeding (L) Respiratory function exercise (M) Fluid therapy targeting euvolemia.

      Risk of bias

      Fig. 2 and Table 3 summarize the risk of bias in the RCTs and cohort studies. The overall quality of the included studies was good. All studies compared the baseline characteristics of the two groups and found that these were consistent. The included studies also showed consistent findings regarding the promotion of patient recovery by the ERAS program. The NOS scores of the included cohort studies were all ≥ 6, and most studies showed a low risk of bias. Studies showed comprehensive selection and comparability parameters, but most studies ignored the adequacy of cohort follow-up in relation to the outcome parameters. Most of the included RCTs had moderate selection bias; no other serious bias was found. However, the risk of bias was increased owing to the lack of allocation concealment.
      • Guyatt G.H.
      • Oxman A.D.
      • Sultan S.
      • et al.
      GRADE guidelines: 9. Rating up the quality of evidence.
      Fig. 2
      Fig. 2The risk of bias of randomized controlled trials. Green represents low risk; yellow represents unclear risk; red represents high risk. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
      Table 3Risk of bias assessment: NOS scores for cohort studies.
      Items of NOSStudies
      Alessa

      2017
      Amin 2015Cai

      2018
      Forster

      2021
      Greg 2019Huang 2018Michele

      2012
      Robert 2018Satoshi 2019Tahiri 2020Wang 2021Xu

      2020
      Selection
      Representativeness of the exposed cohort
      Selection of the non-exposed cohort
      Ascertainment of exposure
      Demonstration that outcome of interest was not present at start of study
      Comparability
      Comparability of cohorts on basis of the design or analysis∗∗∗∗∗∗∗∗∗∗∗∗∗∗∗∗∗∗
      Outcome
      Assessment of outcome
      Was follow-up long enough for outcomes to occur
      Adequacy of follow-up of cohorts
      Total678686767677
      NOS, Newcastle–Ottawa Quality Assessment Scale.

      Meta-analysis of VAS scores after treatment

      Of the 23 included studies, 12 studies
      • Cai Q.
      Multidisciplinary enhanced recovery after surgery in video-assisted thoracoscopic surgery for lung cancer.
      ,
      • Che Q.
      • Wang H.
      • Li Y.
      • Xia H.
      Application of rapid rehabilitation in perioperative nursing of early non- small cell lung cancer.
      ,
      • Huang H.
      • Ma H.
      • Chen S.
      Enhanced recovery after surgery using uniportal video-assisted thoracic surgery for lung cancer: a preliminary study.
      • Li Y.
      • Yi H.
      • Xiao Y.
      • Chen X.
      • Guo L.
      Fast rehabilitation surgery in application of radical operation for lung cancer under thoracoscope.
      • Li L.
      • Zhao R.
      • Wang H.
      • Zheng X.
      • Zhao R.
      Interventional effect of fast track suegery concept on lung cancer patients during perioperative period.
      ,
      • Wang J.
      • Ni B.
      • Ma H.
      The application of fast- track surgery in thoracoscopic lung cancer operation for the aged patients.
      ,
      • Wang T.
      Clinical study of perioperative and serum indexex variation and prognostic relevance in the application of FTS in treatment of stage Ⅰ~Ⅱ non-small cell lung cancer.
      ,
      • Xu F.
      Application of Rapid Rehabilitation (ERAS) in Thoracoscopy for Radical Lung Cancer Surgery.
      • Zhang X.
      • Xie D.
      • Chen C.
      • Lin J.
      Investigation on the application of the concept of rapid rehabilitation surgery in the perioperative period of thoracoscopic lung cancer radical surgery.
      • Zhang Z.
      Application of the concept of enhanced recovery after surgery in thoracoscopic radical resection of lung cancer.
      • Zhao G.
      • Huang Y.
      • Chen X.
      • et al.
      Research on fast track surgery application in lung cancer surgery.
      • Zheng C.
      Effect of enhanced recovery after surgery on postoperative rehabilitation and quality of life of elderly patients undergoing thoracoscopic radical resection of lung cancer.
      with 3170 patients (1589 ERAS and 1581 control) were included in the meta-analysis of VAS scores after treatment. The heterogeneity test showed significant heterogeneity (P < 0.01, I2 = 99%), so the random-effects model was used. ERAS significantly improved postoperative pain in patients with lung cancer (MD = −1.99, 95% CI [−2.45, −1.54], P < 0.01) (Fig. 3). The subgroup analysis of VAS at 1 h, 6 h, 12 h, 24 h, 48 h, 72 h, and 7 days after surgery showed that the heterogeneity was reduced (P > 0.05 and I2 < 50%) and the results of the meta-analysis were robust. As shown in Fig. 3, compared with the control group, the ERAS group experienced a significant improvement in postoperative pain at 6 h (MD = −3.81, 95% CI [−7.12, −0.49], P < 0.05), 12 h (MD = −3.32, 95% CI [−4.60, −2.03], P < 0.01), 24 h (MD = −1.63, 95% CI [−2.44, −0.81], P < 0.01), 72 h (MD = −1.12, 95% CI [−1.68, −0.55], P < 0.01), 7 days (MD = −1.50, 95% CI [−2.70, −0.30], P < 0.05). However, there was no significant difference in pain at 1 h (MD = −2.81, 95% CI [−7.48, 1.85], P > 0.05) and 48 h (MD = −2.71, 95% CI [−6.51, 1.10], P > 0.05) after surgery. Considering the significant heterogeneity among studies, sensitivity analysis was performed to identify the source of the difference. However, the heterogeneity did not change.
      Fig. 3
      Fig. 3Forest plot of VAS scores after treatment. Meta-analysis comparing ERAS versus standard recovery for postoperative pain after lung cancer surgery. ERAS, enhanced recovery after surgery; VAS, visual analog scale.

      Meta-analysis of quality of life

      Three studies
      • Li J.
      The effect of rapid rehabilitation surgical nursing on postoperative lung function recovery and quality of life in patients undergoing thoracoscopic radical resection of lung cancer.
      ,
      • Zhang X.
      • Xie D.
      • Chen C.
      • Lin J.
      Investigation on the application of the concept of rapid rehabilitation surgery in the perioperative period of thoracoscopic lung cancer radical surgery.
      ,
      • Zheng C.
      Effect of enhanced recovery after surgery on postoperative rehabilitation and quality of life of elderly patients undergoing thoracoscopic radical resection of lung cancer.
      with 1064 patients (532 ERAS and 532 control) were included in the meta-analysis of quality of life. The heterogeneity test showed no significant heterogeneity (P ​= ​0.04, I2 ​= ​46%), so the fixed-effects model was used. The results showed that ERAS significantly improved quality of life in patients with lung cancer (MD ​= ​10.3, 95% CI [9.59, 11.02], P ​< ​0.01) (Fig. 4). Subgroup analysis was performed on the four dimensions of quality of life: physiological, psychological, role, and social function. The results were robust (P ​= ​0.77 and I2 ​= ​0%).
      Fig. 4
      Fig. 4Forest plot of quality of life. Meta-analysis comparing ERAS versus standard recovery for quality of life after lung cancer surgery. ERAS, enhanced recovery after surgery.

      Meta-analysis of complication rate

      Except for Greg et al,
      • Haro G.J.
      • Sheu B.
      • Marcus S.G.
      • et al.
      Perioperative lung resection outcomes after implementation of a multidisciplinary, evidence-based thoracic ERAS program.
      22 RCTs with 7423 patients (2812 ERAS and 4611 control) analyzed postoperative complications, and the incidence of complications was described using a binary variable. There was heterogeneity among studies (P ​< ​0.01, I2 ​= ​62%), so the random-effects model was used. As shown in Fig. 5, ERAS significantly reduced the incidence of complications in patients with lung cancer (OR ​= ​0.48, 95% CI [0.37, 0.61], P ​< ​0.01). After excluding the study by Alessandro et al, the heterogeneity was significantly reduced, and the result was stable. However, the incidence of specific complications, such as reoperation, readmission, and mortality, was very low. We performed a subgroup analysis, which showed that there was no significant difference in reoperation rate (OR ​= ​0.87, 95% CI [0.49, 1.55], P ​> ​0.05), readmission rate (OR ​= ​1.03, 95% CI [0.75, 1.40], P ​> ​0.05), and mortality rate (OR ​= ​1.15, 95% CI [0.60, 2.22], P ​> ​0.05).
      Fig. 5
      Fig. 5Forest plot of the complication rate. Meta-analysis comparing ERAS versus standard recovery for the complication rate after lung cancer surgery. ERAS, enhanced recovery after surgery.

      Meta-analysis of function-related outcomes

      Postoperative recovery mainly includes chest tube indwelling time and first ambulation. Fifteen studies
      • Madani A.
      • Fiore Jr., J.F.
      • Wang Y.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      ,
      • Che Q.
      • Wang H.
      • Li Y.
      • Xia H.
      Application of rapid rehabilitation in perioperative nursing of early non- small cell lung cancer.
      • Fan X.
      • Jiao J.
      • Zhu W.
      • Yin J.
      Application of enhanced recovery after surgery in perioperative nursing of patients undergoing radical resection of lung cancer.
      • Forster C.
      • Doucet V.
      • Perentes J.Y.
      • et al.
      Impact of an enhanced recovery after surgery pathway on thoracoscopic lobectomy outcomes in non-small cell lung cancer patients: a propensity score-matched study.
      ,
      • Huang H.
      • Ma H.
      • Chen S.
      Enhanced recovery after surgery using uniportal video-assisted thoracic surgery for lung cancer: a preliminary study.
      • Li Y.
      • Yi H.
      • Xiao Y.
      • Chen X.
      • Guo L.
      Fast rehabilitation surgery in application of radical operation for lung cancer under thoracoscope.
      • Li L.
      • Zhao R.
      • Wang H.
      • Zheng X.
      • Zhao R.
      Interventional effect of fast track suegery concept on lung cancer patients during perioperative period.
      ,
      • Van Haren R.M.
      • Mehran R.J.
      • Mena G.E.
      • et al.
      Enhanced recovery decreases pulmonary and cardiac complications after thoracotomy for lung cancer.
      ,
      • Tahiri M.
      • Goudie E.
      • Jouquan A.
      • Martin J.
      • Ferraro P.
      • Liberman M.
      Enhanced recovery after video-assisted thoracoscopic surgery lobectomy: a prospective, historically controlled, propensity-matched clinical study.
      • Wang J.
      • Ni B.
      • Ma H.
      The application of fast- track surgery in thoracoscopic lung cancer operation for the aged patients.
      • Wang T.
      Clinical study of perioperative and serum indexex variation and prognostic relevance in the application of FTS in treatment of stage Ⅰ~Ⅱ non-small cell lung cancer.
      • Wang C.
      • Lai Y.
      • Li P.
      • Su J.
      • Che G.
      Influence of enhanced recovery after surgery (ERAS) on patients receiving lung resection: a retrospective study of 1749 cases.
      ,
      • Zhang X.
      • Xie D.
      • Chen C.
      • Lin J.
      Investigation on the application of the concept of rapid rehabilitation surgery in the perioperative period of thoracoscopic lung cancer radical surgery.
      ,
      • Zhang Z.
      Application of the concept of enhanced recovery after surgery in thoracoscopic radical resection of lung cancer.
      ,
      • Zheng C.
      Effect of enhanced recovery after surgery on postoperative rehabilitation and quality of life of elderly patients undergoing thoracoscopic radical resection of lung cancer.
      and eight studies
      • Cai Q.
      Multidisciplinary enhanced recovery after surgery in video-assisted thoracoscopic surgery for lung cancer.
      • Che Q.
      • Wang H.
      • Li Y.
      • Xia H.
      Application of rapid rehabilitation in perioperative nursing of early non- small cell lung cancer.
      • Fan X.
      • Jiao J.
      • Zhu W.
      • Yin J.
      Application of enhanced recovery after surgery in perioperative nursing of patients undergoing radical resection of lung cancer.
      ,
      • Li Y.
      • Yi H.
      • Xiao Y.
      • Chen X.
      • Guo L.
      Fast rehabilitation surgery in application of radical operation for lung cancer under thoracoscope.
      ,
      • Tahiri M.
      • Goudie E.
      • Jouquan A.
      • Martin J.
      • Ferraro P.
      • Liberman M.
      Enhanced recovery after video-assisted thoracoscopic surgery lobectomy: a prospective, historically controlled, propensity-matched clinical study.
      • Wang J.
      • Ni B.
      • Ma H.
      The application of fast- track surgery in thoracoscopic lung cancer operation for the aged patients.
      • Wang T.
      Clinical study of perioperative and serum indexex variation and prognostic relevance in the application of FTS in treatment of stage Ⅰ~Ⅱ non-small cell lung cancer.
      ,
      • Zhang Z.
      Application of the concept of enhanced recovery after surgery in thoracoscopic radical resection of lung cancer.
      analyzed the effect of ERAS on chest tube indwelling time and first ambulation, respectively. The heterogeneity test indicated high heterogeneity among studies regarding chest tube indwelling time (P ​< ​0.01, I2 ​= ​98%). The random-effects model was used, and the combined effect size was statistically significant (MD ​= ​−2.20, 95% CI [−2.75, −1.64], P ​< ​0.01) (Fig. 6). There was significant heterogeneity among studies for first ambulation data (P ​< ​0.01, I2 ​= ​98%), so the random-effects model was used. The combined effect size was significant (MD ​= ​−1.48, 95% CI [−1.77, −1.19], P ​< ​0.01) (Fig. 7). ERAS significantly accelerated recovery after surgery.
      Fig. 6
      Fig. 6Forest plot of chest tube indwelling time. Meta-analysis comparing ERAS versus standard recovery for chest tube indwelling time after lung cancer surgery. ERAS, enhanced recovery after surgery.
      Fig. 7
      Fig. 7Forest plot of first ambulation. Meta-analysis comparing ERAS versus standard recovery for first ambulation after lung cancer surgery. ERAS: enhanced recovery after surgery.

      Meta-analysis of LOS

      As shown in Fig. 8, 20 studies
      • Madani A.
      • Fiore Jr., J.F.
      • Wang Y.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      • Cai Q.
      Multidisciplinary enhanced recovery after surgery in video-assisted thoracoscopic surgery for lung cancer.
      • Che Q.
      • Wang H.
      • Li Y.
      • Xia H.
      Application of rapid rehabilitation in perioperative nursing of early non- small cell lung cancer.
      • Fan X.
      • Jiao J.
      • Zhu W.
      • Yin J.
      Application of enhanced recovery after surgery in perioperative nursing of patients undergoing radical resection of lung cancer.
      • Forster C.
      • Doucet V.
      • Perentes J.Y.
      • et al.
      Impact of an enhanced recovery after surgery pathway on thoracoscopic lobectomy outcomes in non-small cell lung cancer patients: a propensity score-matched study.
      • Haro G.J.
      • Sheu B.
      • Marcus S.G.
      • et al.
      Perioperative lung resection outcomes after implementation of a multidisciplinary, evidence-based thoracic ERAS program.
      • Huang H.
      • Ma H.
      • Chen S.
      Enhanced recovery after surgery using uniportal video-assisted thoracic surgery for lung cancer: a preliminary study.
      • Li Y.
      • Yi H.
      • Xiao Y.
      • Chen X.
      • Guo L.
      Fast rehabilitation surgery in application of radical operation for lung cancer under thoracoscope.
      • Li L.
      • Zhao R.
      • Wang H.
      • Zheng X.
      • Zhao R.
      Interventional effect of fast track suegery concept on lung cancer patients during perioperative period.
      ,
      • Salati M.
      • Brunelli A.
      • Xiume F.
      • Refai M.
      • Pompili C.
      • Sabbatini A.
      Does fast-tracking increase the readmission rate after pulmonary resection? A case-matched study.
      ,
      • Van Haren R.M.
      • Mehran R.J.
      • Mena G.E.
      • et al.
      Enhanced recovery decreases pulmonary and cardiac complications after thoracotomy for lung cancer.
      ,
      • Tahiri M.
      • Goudie E.
      • Jouquan A.
      • Martin J.
      • Ferraro P.
      • Liberman M.
      Enhanced recovery after video-assisted thoracoscopic surgery lobectomy: a prospective, historically controlled, propensity-matched clinical study.
      • Wang J.
      • Ni B.
      • Ma H.
      The application of fast- track surgery in thoracoscopic lung cancer operation for the aged patients.
      • Wang T.
      Clinical study of perioperative and serum indexex variation and prognostic relevance in the application of FTS in treatment of stage Ⅰ~Ⅱ non-small cell lung cancer.
      • Wang C.
      • Lai Y.
      • Li P.
      • Su J.
      • Che G.
      Influence of enhanced recovery after surgery (ERAS) on patients receiving lung resection: a retrospective study of 1749 cases.
      • Xu F.
      Application of Rapid Rehabilitation (ERAS) in Thoracoscopy for Radical Lung Cancer Surgery.
      • Zhang X.
      • Xie D.
      • Chen C.
      • Lin J.
      Investigation on the application of the concept of rapid rehabilitation surgery in the perioperative period of thoracoscopic lung cancer radical surgery.
      • Zhang Z.
      Application of the concept of enhanced recovery after surgery in thoracoscopic radical resection of lung cancer.
      • Zhao G.
      • Huang Y.
      • Chen X.
      • et al.
      Research on fast track surgery application in lung cancer surgery.
      • Zheng C.
      Effect of enhanced recovery after surgery on postoperative rehabilitation and quality of life of elderly patients undergoing thoracoscopic radical resection of lung cancer.
      with 6780 patients (2534 ERAS and 4246 control) were included in the meta-analysis for LOS. The heterogeneity test showed high heterogeneity among studies (P ​< ​0.01, I2 ​= ​97%), and the random-effects model was used. LOS reduced after the implementation of ERAS (MD ​= ​−2.70, 95% CI [−3.05, −2.36], P ​< ​0.01).
      Fig. 8
      Fig. 8Forest plot of length of stay. Meta-analysis comparing ERAS versus standard recovery for length of stay after lung cancer surgery. ERAS, enhanced recovery after surgery.

      Discussion

      The ERAS research group has published specific perioperative care pathways for thoracic surgery.
      • Batchelor T.J.P.
      • Rasburn N.J.
      • Abdelnour-Berchtold E.
      • et al.
      Guidelines for enhanced recovery after lung surgery: recommendations of the enhanced recovery after surgery (ERAS(R)) society and the European society of thoracic surgeons (ESTS).
      The presentation of a consensus may facilitate an understanding of the priorities for applying ERAS principles in clinical practice. However, implementing an ERAS program in a specific institution remains a daunting task because of the influence of historical practices, resource challenges, and other factors.
      • Batchelor T.J.P.
      Implementing enhanced recovery after thoracic surgery-no easy task.
      Overall adherence to the ERAS program improved patient outcomes.
      • Group E.C.
      The impact of enhanced recovery protocol compliance on elective colorectal cancer resection: results from an international registry.
      As technology develops, the ERAS program could incorporate more care elements at each stage of the perioperative period. Synergy of these elements may reduce stress response and catabolism.
      • Schatz C.
      Enhanced recovery in a minimally invasive thoracic surgery program.
      Some elements (such as preoperative respiratory function exercise and early postoperative mobilization) are more effective than others.
      • Rogers L.J.
      • Bleetman D.
      • Messenger D.E.
      • et al.
      The impact of enhanced recovery after surgery (ERAS) protocol compliance on morbidity from resection for primary lung cancer.
      Preoperative respiratory function exercise benefits the physiology of surgical patients and may reduce the incidence of pulmonary complications.
      • Sebio Garcia R.
      • Yanez Brage M.I.
      • Gimenez Moolhuyzen E.
      • Granger C.L.
      • Denehy L.
      Functional and postoperative outcomes after preoperative exercise training in patients with lung cancer: a systematic review and meta-analysis.
      The present review found consistent reports of such effects. Furthermore, postoperative immunosuppression caused by surgery
      • Kadosawa T.
      • Watabe A.
      The effects of surgery-induced immunosuppression and angiogenesis on tumour growth.
      may prolong wound healing time and hast cancer cell development. ERAS may reduce postoperative infection in patients and accelerate postoperative recovery by reducing inflammation,
      • Grant M.C.
      • Yang D.
      • Wu C.L.
      • Makary M.A.
      • Wick E.C.
      Impact of enhanced recovery after surgery and fast track surgery pathways on healthcare-associated infections: results from a systematic review and meta-analysis.
      which is consistent with our pooled estimates. Therefore, nurses should provide timely health education, such as multimedia playback, to increase patient awareness of the importance of measures such as early postoperative mobilization, thereby improving compliance.
      This meta-analysis showed that following ERAS, patients reported relief of postoperative pain, and the chest tube indwelling time was shortened, which indirectly reduced the incidence of postoperative complications. Pain is the most common postoperative problem in all types of surgery. Typically, the cause of patient-reported symptoms of pain is investigated and treated with appropriate drugs, such as Celecoxib
      • Ueda K.
      • Hayashi M.
      • Murakami J.
      • Tanaka T.
      • Utada K.
      • Hamano K.
      Intercostal block vs. epidural analgesia in thoracoscopic lung cancer surgery: a randomized trial.
      and Dezocine.
      • Huang X.
      • Cui Y.
      • Xiao Y.
      • Zhao X.
      • Xu J.
      • Yang L.
      Combined programmed intermittent bolus infusion with continuous infusion for the thoracic paravertebral block in patients undergoing thoracoscopic surgery: a prospective, randomized, and double-blinded study.
      However, some drugs have delayed effects. Because of this, most patients resist engaging in activities because of fear of pain, which leads to problems such as prolonged drainage, followed by an inflammatory response.
      • Grant M.C.
      • Sommer P.M.
      • He C.
      • et al.
      Preserved analgesia with reduction in opioids through the use of an acute pain protocol in enhanced recovery after surgery for open hepatectomy.
      Postoperative inflammatory responses are associated with the occurrence of complications.
      • Alazawi W.
      • Pirmadjid N.
      • Lahiri R.
      • Bhattacharya S.
      Inflammatory and immune responses to surgery and their clinical impact.
      The present study also showed that ERAS was directly related to a reduction in complications and improvement in quality of life. Improved life quality is a goal of humanistic care.
      • Ha D.M.
      • Prochazka A.V.
      • Bekelman D.B.
      • Stevens-Lapsley J.E.
      • Studts J.L.
      • Keith R.L.
      Modifiable factors associated with health-related quality of life among lung cancer survivors following curative intent therapy.
      The reported improvements in outcomes contribute toward ensuring the health and well-being of patients. Therefore, nurses should pay more attention to the ERAS program and implement appropriate ERAS measures for patients with lung cancer.
      Egger's test indicated publication bias among studies (P ​= ​0.001), possibly because several included studies did not account for potential confounders. After using the alternative approach described by Zwetsloot et al,
      • Zwetsloot P.P.
      • Van Der Naald M.
      • Sena E.S.
      • et al.
      Standardized mean differences cause funnel plot distortion in publication bias assessments.
      the risk of publication bias remained. For example, we found that the LOS improvement after the implementation of ERAS was conservative. This may be because LOS is affected by many factors in addition to readiness for discharge; non-medical factors such as surgeon habits and patient expectations
      • Fiore Jr., J.F.
      • Faragher I.G.
      • Bialocerkowski A.
      • Browning L.
      • Denehy L.
      Time to readiness for discharge is a valid and reliable measure of short-term recovery after colorectal surgery.
      may explain why some studies reported a lack of effect for ERAS. To some extent, the personal habits of surgeons affect ERAS outcomes. Surgeons in different research institutions use different ERAS measures, such as LOS criteria,
      • Leeds I.L.
      • Sadiraj V.
      • Cox J.C.
      • Schnier K.E.
      • Sweeney J.F.
      Assessing clinical discharge data preferences among practicing surgeons.
      based on their own experience. Additionally, most measures in the ERAS program require patient cooperation. High patient compliance may be needed to ensure the effectiveness of ERAS implementation.
      • Seow-En I.
      • Wu J.
      • Yang L.W.Y.
      • et al.
      Results of a colorectal enhanced recovery after surgery (ERAS) programme and a qualitative analysis of healthcare workers' perspectives.
      Research shows that patient compliance before surgery is high. However, disease progression and psychological pressure lead to reduced compliance.
      • Rattray M.
      • Roberts S.
      • Desbrow B.
      • et al.
      A qualitative exploration of factors influencing medical staffs' decision-making around nutrition prescription after colorectal surgery.
      Therefore, nurses should pay more attention to the needs of patients and consider providing individualized ERAS measures for specific lung cancer disease sites or surgical interventions based on ERAS guidelines.
      Our results are partly consistent with previous studies
      • Li R.
      • Wang K.
      • Qu C.
      • et al.
      The effect of the enhanced recovery after surgery program on lung cancer surgery: a systematic review and meta-analysis.
      ; however, we included and analyzed more relevant outcome measures. Research by Huang et al
      • Huang H.
      • Ma H.
      • Chen S.
      Enhanced recovery after surgery using uniportal video-assisted thoracic surgery for lung cancer: a preliminary study.
      showed that compared with traditional perioperative care, ERAS reduced postoperative pain and shortened chest tube indwelling time. Furthermore, previous studies have found a substantial difference in quality of life between the ERAS program and standard care, which indicates that ERAS is beneficial.
      • Xu F.
      • Yu P.
      • Li L.
      Rapid rehabilitation nursing in postoperative patients with colorectal cancer and quality of life.
      ,
      • Zheng Y.
      • Mao M.
      • Ji M.
      • et al.
      Does a pulmonary rehabilitation based ERAS program (PREP) affect pulmonary complication incidence, pulmonary function and quality of life after lung cancer surgery? Study protocol for a multicenter randomized controlled trial.
      There is also evidence that the LOS of patients treated with the ERAS program is shorter.
      • Chau J.P.C.
      • Liu X.
      • Lo S.H.S.
      • et al.
      Perioperative enhanced recovery programmes for women with gynaecological cancers.
      This meta-analysis indicated significant heterogeneity among studies. During the study design process, we specified subgroup analyses of potential sources of heterogeneity in advance, including the number of ERAS measures, and risk of bias. However, these factors did not seem to explain the heterogeneity.
      • Schneider S.
      • Armbrust R.
      • Spies C.
      • du Bois A.
      • Sehouli J.
      Prehabilitation programs and ERAS protocols in gynecological oncology: a comprehensive review.
      A possible explanation is the differences in case mix among studies. The studies involved different patients in different countries. The diversity of patient types suggests the general applicability of our findings regarding the safety and efficacy of ERAS but inevitably led to heterogeneity. An in-depth analysis of sources of heterogeneity is required in the future.
      Teamwork is the basis for the success of the ERAS program. Some research
      • Wick E.C.
      • Hobson D.B.
      • Bennett J.L.
      • et al.
      Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections.
      has shown that good patient outcomes are inseparable from teamwork and effective communication. Many ERAS measures, such as multimodal analgesia, are not only relevant to nurses but also affect surgeon judgment.
      • Batchelor T.J.P.
      • Rasburn N.J.
      • Abdelnour-Berchtold E.
      • et al.
      Guidelines for enhanced recovery after lung surgery: recommendations of the enhanced recovery after surgery (ERAS(R)) society and the European society of thoracic surgeons (ESTS).
      Therefore, nurses should work collaboratively with surgeons and anesthesiologists to provide care throughout the perioperative period to ensure that patients receive optimal treatment.
      The main advantage of this meta-analysis was the inclusion of more studies and patients compared with previous analyses. It increased the focus on the needs of patients and postoperative recovery. However, this meta-analysis had several limitations. First, only Chinese and English articles were finally included. Because articles published in other languages were excluded, the findings do not reflect the status of these populations. Second, some studies did not satisfy the requirements for blinding or allocation concealment, resulting in biased results. Third, a unified ERAS guideline for lung cancer surgery remains to be developed, and indicators such as the inconsistency of chest tube removal criteria and discharge criteria may have affected the results. Moreover, the sample size of the included studies varied greatly, which may have introduced clinical heterogeneity. All these factors may limit the international application and generalizability of findings.

      Conclusions

      This systematic review indicated that ERAS may lead to significant reductions in pain conditions, postoperative complications, and LOS. Additionally, ERAS may accelerate postoperative recovery and improve quality of life. This analysis provides strong evidence for the efficacy and safety of ERAS for patients with lung cancer. Additional research is needed to investigate the effects of individual elements of the ERAS program. This would help identify important aspects of the program, gradually improve the program, and develop an ERAS application standard for with lung cancer.

      Acknowledgments

      The authors acknowledge the major medical databases for facilitating our research. We thank Diane Williams, PhD, from Liwen Bianji (Edanz) (www.liwenbianji.cn/), for editing the English text of a draft of this manuscript.

      Author contributions

      Wenhui Zhang: Study design, literature search, critical appraisal of included papers, extraction of data, data analysis, manuscript writing, and manuscript revision. Yuting Zhang: Critical appraisal of included papers, extraction of data, and data analysis. Yi Qin: Literature review and search, and study supervision. Jiahai Shi: Study design, study supervision, and manuscript revision.

      Declaration of competing interest

      None declared.

      Funding

      This work was supported by the National Natural Science Foundation of China (Grant No. 81770266 ); the China Postdoctoral Science Foundation (Grant No. 2019M661907 ); the Clinical Medical Research Center of Cardiothoracic Diseases in Nantong (Grant No. HS2019001 ); the Innovation Team of Cardiothoracic Disease at the Affiliated Hospital of Nantong University (Grant No. TECT-A04 ); and the Nantong Key Laboratory of Translational Medicine of Cardiothoracic Diseases .

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