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The impact of enhanced recovery after surgery (ERAS) protocol compliance on morbidity from resection for primary lung cancer

Open ArchivePublished:December 19, 2017DOI:https://doi.org/10.1016/j.jtcvs.2017.10.151

      Abstract

      Objective

      The adoption of Enhanced Recovery After Surgery programs in thoracic surgery is relatively recent with limited outcome data. This study aimed to determine the impact of an Enhanced Recovery After Surgery pathway on morbidity and length of stay in patients undergoing lung resection for primary lung cancer.

      Methods

      This prospective cohort study collected data on consecutive patients undergoing lung resection for primary lung cancer between April 2012 and June 2014 at a regional referral center in the United Kingdom. All patients followed a standardized, 15-element Enhanced Recovery After Surgery protocol. Key data fields included protocol compliance with individual elements, pathophysiology, and operative factors. Thirty-day morbidity was taken as the primary outcome measure and classified a priori according to the Clavien-Dindo system. Logistic regression models were devised to identify independent risk factors for morbidity and length of stay.

      Results

      A total of 422 consecutive patients underwent lung resection over a 2-year period, of whom 302 (71.6%) underwent video-assisted thoracoscopic surgery. Lobectomy was performed in 297 patients (70.4%). Complications were experienced by 159 patients (37.6%). The median length of stay was 5 days (range, 1-67), and 6 patients (1.4%) died within 30 days of surgery. There was a significant inverse relationship between protocol compliance and morbidity after adjustment for confounding factors (odds ratio, 0.72; 95% confidence interval, 0.57-0.91; P < .01). Age, lobectomy or pneumonectomy, more than 1 resection, and delayed mobilization were independent predictors of morbidity. Age, lack of preoperative carbohydrate drinks, planned high dependency unit/intensive therapy unit admission, delayed mobilization, and open approach were independent predictors of delayed discharge (length of stay >5 days).

      Conclusions

      Increased compliance with an Enhanced Recovery After Surgery pathway is associated with improved clinical outcomes after resection for primary lung cancer. Several elements, including early mobilization, appear to be more influential than others.

      Key Words

      Abbreviations and Acronyms:

      ERAS (Enhanced Recovery After Surgery), LOS (length of stay), OR (odds ratio), PONV (postoperative nausea and vomiting), VATS (video-assisted thoracoscopic surgery)
      Figure thumbnail fx1
      Compliance with number of ERAS protocols and (A) morbidity and (B) delayed discharge.
      Increasing overall compliance with an ERAS pathway in patients undergoing lung cancer resection is associated with a reduction in postoperative morbidity and a shorter LOS.
      ERAS protocols have been described in thoracic surgery, but there remains a paucity of evidence reporting clinical outcomes. In this study, we have demonstrated that increased overall compliance with ERAS protocols reduces morbidity and LOS. In addition, several independent factors that seem more influential than other elements of the pathway have been identified.
      See Editorial Commentary page 1853.
      Lung cancer is the leading cause of cancer deaths worldwide, accounting for 13% and 14% of all new cancers in the United Kingdom and United States, respectively.

      Cancer Research UK. Lung cancer mortality statistics. 2014. Available at: http://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/lung-cancer#heading-Zero. Accessed January 1, 2018.

      American Cancer Society. Lung and bronchus cancer at a glance. 2017. Available at: https://cancerstatisticscenter.cancer.org/#!/. Accessed January 1, 2018.

      Surgical resection offers the best chance of cure for early-stage lung cancer and therefore represents the first choice treatment.
      Royal College of Physicians
      Lung Cancer Clinical Outcomes Publication 2016 (for the 2014 Audit Period).
      However, lung cancer is associated with significant complications in up to 50% of cases, which can lead to delayed recovery, poorer long-term outcomes, and higher costs.
      • Chen F.F.
      • Zhang D.
      • Wang Y.L.
      • Xiong B.
      Video-assisted thoracoscopic surgery lobectomy versus open lobectomy in patients with clinical stage non-small cell lung cancer: a meta-analysis.
      • Phillips J.D.
      • Merkow R.P.
      • Sherman K.L.
      • DeCamp M.M.
      • Bentrem D.J.
      • Bilimoria K.Y.
      Factors affecting selection of operative approach and subsequent short-term outcomes after anatomic resection for lung cancer.
      Enhanced Recovery After Surgery (ERAS) pathways were initially developed in colorectal surgery in an effort to improve the postoperative recovery of patients undergoing colonic resection, based largely on the work of Kehlet and others.
      • Kehlet H.
      Multimodal approach to control postoperative pathophysiology and rehabilitation.
      • Wilmore D.W.
      • Kehlet H.
      Management of patients in fast track surgery.
      • Kehlet H.
      • Wimore D.W.
      Multimodal strategies to improve surgical outcome.
      • Fearon K.C.H.
      • Lljungqvist O.
      • Von Meyenfeldt M.
      • Revhaug A.
      • Dejong C.H.C.
      • Lassen K.
      • et al.
      Enhanced recovery after surgery: a consensus review of clinical care for patients undergoing colonic resection.
      ERAS pathways consist of multimodal, evidence-based protocols targeting the entire patient pathway from referral to discharge. The stress response to surgery is reduced and results in improved patient outcomes.
      • Kehlet H.
      • Wimore D.W.
      Multimodal strategies to improve surgical outcome.
      Furthermore, variations in treatment are reduced, earlier hospital discharge is facilitated, and hospital costs are lowered.
      • Kehlet H.
      Multimodal approach to control postoperative pathophysiology and rehabilitation.
      • Nicholson A.
      • Lowe M.C.
      • Parker J.
      • Lewis S.R.
      • Alderson P.
      • Smith A.F.
      Systematic review and meta-analysis of enhanced recovery programmes in surgical patients.
      • Paton F.
      • Chambers D.
      • Wilson P.
      • Eastwood A.
      • Craig D.
      • Fox D.
      • et al.
      Effectiveness and implementation of enhanced recovery after surgery programmes: a rapid evidence synthesis.
      • Lee L.
      • Mata J.
      • Ghitulescu G.A.
      • Boutros M.
      • Charlebois P.
      • Stein B.
      • et al.
      Cost-effectiveness of enhanced recovery versus conventional perioperative management for colorectal surgery.
      Fast-track, multimodal pathways have been described in thoracic surgery. Cerfolio and colleagues
      • Cerfolio R.J.
      • Pickens A.
      • Bass C.
      • Katholi C.
      Fast-tracking pulmonary resections.
      demonstrated that preoperative patient education and standardized removal of catheters and chest drains postoperatively facilitated earlier discharge without adversely affecting morbidity or mortality. Other groups have demonstrated a reduction in complications and a reduced length of stay (LOS).
      • 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.
      • Padilla Alarcón J.
      • Peñalver Cuesta J.C.
      Experience with lung resection in a fast-track surgery program.
      • Muehling B.M.
      • Halter G.L.
      • Schelzig H.
      • Meirerhenrich R.
      • Steffen P.
      • Sunder-Plassman L.
      • et al.
      Reduction of postoperative pulmonary complications after lung surgery using fast track clinical pathway.
      • Das-Neves-Pereira J.C.
      Fast-track rehabilitation for lung cancer lobectomy: a five-year experience.
      More recently, specific ERAS pathways for thoracic surgery have been described.
      • Madani A.
      • Fiore J.F.
      • Wang Y.
      • Bejjani J.
      • Sivakumaran L.
      • Mata J.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      • Scarci M.
      • Solli P.
      • Bedetti B.
      Enhanced recovery pathway for thoracic surgery in the UK.
      • Giménez-Milà M.
      • Klein A.A.
      • Martinez G.
      Design and implementation of an enhanced recovery program in thoracic surgery.
      Nevertheless, there remains a paucity of evidence regarding ERAS in lung resection surgery, particularly in terms of clinical outcomes and in combination with a predominantly minimally invasive video-assisted thoracoscopic surgery (VATS) technique.
      It remains unclear whether the benefits obtained from ERAS pathways are a consequence of a significant improvement in 1 or 2 individual elements of care or whether they are the aggregation of marginal gains throughout the pathway. In this study, we present findings from a large institutional database of an ERAS program that includes all patients undergoing primary lung resection during the study period. Our primary aim was to identify the individual elements of an ERAS protocol predictive of 30-day morbidity and delayed discharge in patients undergoing resection for lung cancer.

      Material and Methods

      This study was reported according to the STROBE criteria for observational studies.
      • Elm von E.
      • Altman D.G.
      • Egger M.
      • Pocock S.J.
      • Gøtzsche P.C.
      • Vandenbroucke J.P.
      STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guideline for reporting observational studies.
      Institutional approval was obtained for the conduct of the study as an audit of practice.

      Patient Selection

      In this cohort study, patients undergoing lung resection for primary lung cancer at a single UK regional referral center between April 2012 and June 2014 were prospectively identified and entered into an electronic database. All adult patients (aged >18 years) were included if they underwent a sublobar resection (anatomic segmentectomy or nonanatomic wedge resection), lobectomy, or pneumonectomy for primary lung cancer regardless of surgical approach. Elective and expedited operations were included. Those undergoing thoracic surgical operations for benign disease or metastatic disease, and individuals aged less than 18 years were excluded.
      Key data fields collected included patient demographics, pathophysiology, protocol compliance with individual elements of an ERAS protocol, and operative factors. The primary outcome measure was any 30-day morbidity, which was classified a priori according to the Clavien-Dindo system specific to thoracic surgery. Minor morbidity was defined as the occurrence of a Clavien-Dindo grade I or II complication, and major morbidity was defined as the occurrence of a grade III or IV complication. Postoperative LOS was considered a secondary outcome measure and dichotomized around the median LOS and thus treated as a categoric variable. Other secondary outcome measures included 30-day readmission, reoperation, and 30-day mortality.

      Enhanced Recovery After Surgery

      ERAS protocols were established in 2010 to improve patient outcomes, reduce variation in practice, and provide more cost-effective care. All patients followed the institution's generic, standardized 15-element ERAS protocol, against which protocol compliance was determined (Table 1 and Video 1). Patients were reviewed daily, including weekends, by an attending thoracic surgeon.
      Figure thumbnail fx3
      Video 1The concept of ERAS and protocols for patients undergoing thoracic surgery. Video available at: http://www.jtcvsonline.org/article/S0022-5223(17)32855-6/fulltext.
      Table 1Elements of the generic Enhanced Recovery After Surgery pathway
      • 1.
        Preoperative visit
      • 2.
        Preoperative assessment
      • 3.
        Patient education and explanation of ERAS
      • 4.
        Admission on day of surgery
      • 5.
        Preoperative carbohydrate drink
      • 6.
        Avoidance of sedation
      • 7.
        Prophylactic antibiotics
      • 8.
        Regional anesthesia
      • 9.
        Goal-directed fluid therapy
      • 10.
        Intraoperative warming
      • 11.
        Avoidance of postoperative intravenous fluids
      • 12.
        Avoidance of opiate analgesia
      • 13.
        Early feeding
      • 14.
        Targeted PONV therapy
      • 15.
        Mobilization within 24 h
      ERAS, Enhanced Recovery After Surgery; PONV, postoperative nausea and vomiting.
      The standard multimodal approach can be divided into preoperative, perioperative, and postoperative phases. Further elements specific to lung resection surgery were included to form our institution's thoracic surgery ERAS pathway, as detailed next and in Table 2.
      Table 2Thoracic surgery Enhanced Recovery After Surgery pathway
      Preoperative phase
       1. Preoperative visit and assessment
       2. Patient education and explanation of ERAS
       3. Smoking cessation
       4. Preoperative rehabilitation
       5. Admission on day of surgery
       6. Preoperative carbohydrate drink
       7. Avoidance of sedative preanesthetic medication
      Perioperative phase
       1. Prophylactic antibiotics
       2. Regional anesthesia with paravertebral catheters
       3. Avoidance of crystalloid overload
       4. Intraoperative warming
       5. Venous thromboembolism prophylaxis
       6. Avoidance of urinary catheter
       7. Minimally invasive surgery (VATS) where possible
       8. Single chest drain
      Postoperative phase
       1. Avoidance of postoperative intravenous fluids
       2. Avoidance of opiate analgesia
       3. Early feeding
       4. Targeted PONV therapy
       5. Mobilization within 24 h
       6. Early chest drain and catheter removal
      ERAS, Enhanced Recovery After Surgery; VATS, video-assisted thoracoscopic surgery; PONV, postoperative nausea and vomiting.

      Preoperative Phase

      All patients attended a multidisciplinary 1-stop clinic for preoperative assessment. They were assessed by a surgeon, an anesthesiologist, and a nurse skilled in the preoperative preparation of patients. This enabled the early identification and management of comorbidities and facilitated subsequent day-of-surgery admission. Patients received an ERAS diary that outlined the protocol, provided daily targets and milestones, and introduced the concept of a planned date of discharge after elective surgery. The diary was then completed during their admission. Smoking-cessation counseling was provided when necessary, but smoking status did not delay admission. If patients were deemed unfit for surgery, they were enrolled in a preoperative rehabilitation program consisting of 4 elements: patient education, smoking cessation, nutritional advice, and exercise (based on chronic obstructive pulmonary disease rehabilitation programs).
      All patients were admitted to hospital on the day of their surgery. Two hours before induction of anesthesia, patients were given complex carbohydrate drinks to prevent dehydration, reduce postoperative insulin resistance, and improve preoperative well-being.
      • Gianotti L.
      • Biffi R.
      • Sandini M.
      • Marrelli D.
      • Vignali A.
      • Caccialanza R.
      • et al.
      Preoperative Oral Carbohydrate Load Versus Placebo in Major Elective Abdominal Surgery (PROCY).
      Routine administration of preanesthetic sedative medication was not given, and patients walked from the preoperative department to the operating room.

      Perioperative Phase

      Prophylactic antibiotics were given at induction. General anesthesia with lung-protective strategies during 1-lung ventilation was used in combination with regional anesthesia (normally a paravertebral catheter with additional intercostal blocks). Epidural anesthesia was not routinely used. Balanced crystalloid solutions were infused intravenously, and vasopressors were administered to avoid intraoperative hypoperfusion. Goal-directed fluid therapy and the use of noninvasive cardiac output monitors were not found to be useful. Instead, anesthesiologists avoided restrictive or liberal fluid regimens.
      Ketamine and intravenous steroids were used as adjuncts to pain relief and postoperative nausea and vomiting (PONV). Normothermia was maintained throughout using convective active warming devices. Venous thromboembolism prophylaxis consisted of compression stockings and pneumatic compression devices intraoperatively, with chemoprophylaxis in the form of subcutaneous low-molecular-weight heparin started on the evening of surgery. Urinary catheters were not routinely placed.
      Minimally invasive (VATS) surgery was used wherever possible. A single chest drain was placed at the end of each procedure and connected to a Thopaz digital chest drainage system (Medela, Switzerland).

      Postoperative Phase

      Intravenous fluids were replaced by oral fluids and diet at the earliest opportunity, typically by the morning after surgery. A standardized analgesic regimen was used consisting of regular acetaminophen, and nonsteroidal anti-inflammatory drugs where appropriate. Opiates were avoided if possible and used only for breakthrough pain if required. Paravertebral blockade continued until postoperative day 2. PONV was addressed with a multimodal approach consisting of both nonpharmacologic (preoperative carbohydrate drinks, avoidance of crystalloid overload) and pharmacologic (avoidance of opiates, steroids, and regular postoperative ondansetron) components.
      Patients were mobilized within 24 hours of surgery and had milestones to achieve each day. Thoracic surgery physiotherapists provided daily sessions with all patients to improve ventilation, aid clearance of secretions, and encourage mobilization.
      Chest drains were removed early according to permissive protocols. This required the absence of an air leak for the previous 6 hours and the drainage of less than 500 mL fluid for the previous 24 hours.

      Statistical Methods

      Continuous variables are expressed as median and interquartile range, and normality was assessed with the Shapiro–Wilk test. Categoric variables are expressed as count and percentages. Patients were divided in 2 groups according to the presence of any morbidity event at 30 days from surgery; 159 patients had such an event, and the remaining 263 patients did not.
      The analysis between groups was conducted using the Mann–Whitney U test for continuous variables that were not normally distributed. Categoric variables were compared with Pearson's chi-square test or Fisher exact test as appropriate. Predictors for morbidity at 30 days, as defined by a P value less than .10 on univariate analysis, were tested using a parsimonious multiple logistic regression model. A stepwise approach was conducted by backward and forward selection methods using Akaike information criterion as discrimination criterion between models. The predictive ability of the model was tested with the Hosmer–Lemeshow goodness of fit test. The same method of analysis was used to define the independent predictors of prolonged postoperative LOS. This was defined as a LOS equal to or greater than 5 postoperative days. Alpha error was set at 0.05, and all tests were 2 tailed. Statistical analysis was performed with R version 3.4.0 (R Foundation for Statistical Computing, Vienna, Austria).

      Results

      A total of 422 patients underwent lung resection for primary lung cancer between April 2012 and June 2014. A total of 302 (71.6%) of these resections were performed using a VATS approach. Forty-one (9.7%) VATS procedures were converted to open, and 77 (18.2%) were performed as a planned open procedure. Elective procedures accounted for 416 cases (98.6%), and the remaining cases were made up of expedited cases brought forward from their originally planned day of surgery because of clinical deterioration. Multiple resections were performed in 47 patients (11.1%). Lobectomy was the most frequently performed procedure and accounted for 297 (70.4%) of cases. Sublobar resections and pneumonectomies accounted for 111 cases (26.3%) and 14 cases (3.3%), respectively.
      A total of 154 patients (36.5%) had a Thoracoscore of 2 or greater, and 118 patients (28.0%) had an American Society of Anesthesiologists of III or greater. A total of 356 patients (84.4%) had a World Health Organization performance status of 0 or 1, with 343 patients (81.3%) having a Medical Research Council dyspnea score of 0 or 1. There were 7 (1.6%) unplanned reoperations and 23 (5.5%) readmissions within 30 days of the primary operation (Table 3). Complications were experienced by 159 patients (37.6%). Of these, 55 (13%) were major complications (Clavien-Dindo III and IV).
      Table 3Patient outcomes
      LOS, median (range)5 (1-67)
      HDU LOS, median (range)0 (0-10) [2 (1-10)]
      Median and range for the entire population.
      Median and range for patients admitted in HDU.
      ITU LOS, median (range)0 (0-36) [3 (1-36)]
      Median and range for the entire population.
      Media and range for patients admitted to the ITU.
      30-d readmission, n (%)23 (5.5)
      30-d reoperation, n (%)7 (1.6)
      30-d morbidity, n (%)
       None259 (61.4)
       Minor (Clavien-Dindo I and II)104 (24.6)
       Major (Clavien-Dindo III and IV)55 (13.0)
       Missing4 (0.9)
      Mortality, n (%)
       30 d6 (1.4)
       60 d7 (1.7)
       90 d9 (2.1)
      LOS, Length of stay; HDU, high dependency unit; ITU, intensive therapy unit.
      Median and range for the entire population.
      Median and range for patients admitted in HDU.
      Media and range for patients admitted to the ITU.

      Predictors of Morbidity

      Multiple logistic regression identified sublobar resection (odds ratio [OR], 0.45; 95% confidence interval [CI], 0.27-0.75; P < .01) as an independent predictor of reduced morbidity at 30 days (Table 4), whereas increased age (OR, 1.02 per year; 95% CI, 1.00-1.02, P = .04) and more than 1 resection (OR, 2.21; 95% CI, 1.13-4.36; P = .02) were predictive of increased morbidity. There was a significant inverse relationship between protocol compliance and morbidity (OR, 0.72; 95% CI, 0.57-0.91; P < .01) (Figure 1, A).
      Table 4Predictors of morbidity at 30 days
      Univariable analysisMultivariable analysis
      OR95% CIP valueOR95% CIP value
      Age1.031.01-1.05.011.021.001-1.05.04
      Gender (male)0.660.44-0.98.04
      Sublobar resection0.540.33-0.86.010.450.27-0.75<.01
      >1 resection2.041.11-3.79.022.211.13-4.36.02
      VATS procedure0.960.62-1.49.87
      Thoracoscore0.970.86-1.09.68
      Preoperative visitNANANA
      Preoperative assessmentNANANA
      Explanation ERAS1.280.65-2.64.48
      Day of surgery admission0.300.04-1.54.16
      Carbohydrate drink0.620.41-0.98.04
      Avoidance of sedationNANANA
      Prophylactic antibiotic0.520.19-1.4.19
      Regional anesthesia0.740.34-1.66.45
      Intraoperative warmingNANANA
      Avoidance of IV fluid0.300.01-3.15.33
      Avoidance of opiate analgesia1.340.38-3.72.61
      Early feeding0.490.22-1.11.08
      Targeted PONV treatment1.320.57-3.32.52
      Early mobilization0.470.31-0.72<.01
      Preoperative creatinine1.011.002-1.2.021.010.99-1.01.07
      Preoperative hemoglobin1.010.99-1.02.09
      Compliance score0.680.54-0.84<.010.720.57-0.91<.01
      HDU stay4.953.03-8.36<.01
      ITU stay6.513.35-14<.012.001.18-3.6.02
      OR, Odds ratio; CI, confidence interval; VATS, video-assisted thoracic surgery; NA, not available; ERAS, Enhanced Recovery After Surgery; IV, intravenous; PONV, postoperative nausea and vomiting; HDU, high dependency unit; ITU, intensive care unit.
      Figure thumbnail gr1
      Figure 1Association between compliance with number of ERAS protocol elements and (A) morbidity and (B) delayed discharge. ERAS, Enhanced Recovery After Surgery.

      Predictors of Length of Stay

      Planned admission to the high dependency unit (OR, 2.86; 95% CI, 1.64-5.03; P < .01) or intensive therapy unit (OR, 3.81; 95% CI, 1.82-8.61; P < .01) was an independent predictor of delayed discharge (LOS >5 days), whereas surgery via a VATS approach (OR, 0.54; 95% CI, 0.32-0.89; P = .01), preoperative carbohydrate drinks (OR, 0.57; 95% CI, 0.36-0.96; P = .01), and early mobilization (OR, 0.25; 95% CI, 0.16-0.40; P < .01) were associated with reduced LOS (Table 5).
      Table 5Predictors of prolonged length of stay
      Univariable analysisMultivariable analysis
      OR95% CIP valueOR95% CIP value
      Age1.031.01-1.05<.011.031.01-1.06<.01
      Gender (male)0.780.53-1.15.21
      Sublobar resection0.660.43-1.03.07
      >1 resection1.230.67-2.29.50
      VATS procedure0.390.25-0.61<.010.540.32-0.89.01
      Thoracoscore1.050.94-1.18.38
      Preoperative visitNANANA
      Preoperative assessmentNANANA
      Explanation ERAS1.160.84-3.19.16
      Day of surgery admission0.200.01-1.27.15
      Carbohydrate drink0.570.36-0.89.010.590.36-0.96.04
      Avoidance of sedationNANANA
      Prophylactic antibiotic0.540.19-1.47.25
      Regional anesthesia2.160.97-5.14.07
      Intraoperative warmingNANANA
      Avoidance of IV fluidNANANA
      Avoidance of opiate analgesia1.050.47-2.39.90
      Early feeding0.740.33-1.65.47
      Targeted PONV treatment1.590.70-3.73.27
      Early mobilization0.250.16-0.40<.010.430.26-0.71<.01
      Preoperative creatinine1.011.001-1.02.04
      Preoperative hemoglobin0.990.98-1.01.38
      Compliance score0.670.53-0.83<.01
      HDU admission4.953.02-8.36<.012.861.64-5.03<.01
      ITU admission6.513.35-14<.013.811.82-8.61<.01
      OR, Odds ratio; CI, confidence interval; VATS, video-assisted thoracic surgery; NA, not available; ERAS, enhanced recovery after surgery; IV, intravenous; PONV, postoperative nausea and vomiting; HDU, high dependency unit; ITU, intensive therapy unit.

      Discussion

      In this study, it has been shown that overall compliance with an ERAS pathway is important for patients undergoing lung resection for primary lung cancer. Increased compliance was associated with reduced morbidity. At the same time, several independent factors emerged as being more influential than other elements of the pathway. Early mobilization and preoperative carbohydrate drinks were the only individual protocol elements that were predictive of reduced morbidity or LOS. Use of the VATS approach was associated with a reduction in LOS, but not morbidity. Other factors associated with increased morbidity were more than 1 resection, lobectomy or pneumonectomy, and age. Planned admission to the high dependency unit/intensive therapy unit was an important institutional factor associated with delayed discharge, although it had no impact on morbidity. Earlier work by Madani and colleagues
      • Madani A.
      • Fiore J.F.
      • Wang Y.
      • Bejjani J.
      • Sivakumaran L.
      • Mata J.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      also noted that the whole pathway was likely to be more important than individual elements, but did demonstrate that early chest drain and urinary catheter removal were independent predictors of a shorter hospital stay.
      ERAS describes multimodal protocols designed to optimize patients preoperatively, reduce and limit the stress response to surgery perioperatively, and improve postoperative recovery, facilitating a more timely return to a patient's normal activities of daily living. Sometimes referred to as “Enhanced Recovery Programs” or “fast-track surgery,” these pathways have revolutionized the care of surgical patients across a number of surgical specialties since their introduction in gastrointestinal surgery in the late 1990s.
      • Kehlet H.
      Multimodal approach to control postoperative pathophysiology and rehabilitation.
      Patient outcomes are optimized, morbidity is reduced, and variations in care are minimized. These efficiencies then translate into a shorter length in hospital stay and reduced costs without affecting readmission rates.
      • Nicholson A.
      • Lowe M.C.
      • Parker J.
      • Lewis S.R.
      • Alderson P.
      • Smith A.F.
      Systematic review and meta-analysis of enhanced recovery programmes in surgical patients.
      • Paton F.
      • Chambers D.
      • Wilson P.
      • Eastwood A.
      • Craig D.
      • Fox D.
      • et al.
      Effectiveness and implementation of enhanced recovery after surgery programmes: a rapid evidence synthesis.
      • Lee L.
      • Mata J.
      • Ghitulescu G.A.
      • Boutros M.
      • Charlebois P.
      • Stein B.
      • et al.
      Cost-effectiveness of enhanced recovery versus conventional perioperative management for colorectal surgery.
      There is little, strong level 1 evidence to suggest ERAS pathways are superior to conventional care in thoracic surgery, although this study appears to demonstrate that increased compliance with the protocol improves clinical outcomes.
      The adoption of the ERAS concept in thoracic surgery is relatively recent. Evidence for the benefit of ERAS protocols is limited, and few, if any, have addressed the impact of VATS on outcome within their program. Cerfolio and colleagues
      • Cerfolio R.J.
      • Pickens A.
      • Bass C.
      • Katholi C.
      Fast-tracking pulmonary resections.
      implemented a fast-track program for open lung resections with a particular focus on preoperative patient education, epidural use, standardized aggressive removal of catheters and chest drains postoperatively, early mobilization, and a daily plan with an estimated day of discharge on the fourth postoperative day. These interventions facilitated early discharge without adversely affecting morbidity or mortality.
      • Cerfolio R.J.
      • Pickens A.
      • Bass C.
      • Katholi C.
      Fast-tracking pulmonary resections.
      Other groups have demonstrated a reduction in complications and a reduced LOS using fast-track protocols.
      • 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.
      • Padilla Alarcón J.
      • Peñalver Cuesta J.C.
      Experience with lung resection in a fast-track surgery program.
      • Muehling B.M.
      • Halter G.L.
      • Schelzig H.
      • Meirerhenrich R.
      • Steffen P.
      • Sunder-Plassman L.
      • et al.
      Reduction of postoperative pulmonary complications after lung surgery using fast track clinical pathway.
      • Das-Neves-Pereira J.C.
      Fast-track rehabilitation for lung cancer lobectomy: a five-year experience.
      In one small, randomized controlled trial, a pathway involving the avoidance of preoperative fasting, regional analgesia, early enteral feeding, and early ambulation resulted in a significant reduction in pulmonary complications.
      • Muehling B.M.
      • Halter G.L.
      • Schelzig H.
      • Meirerhenrich R.
      • Steffen P.
      • Sunder-Plassman L.
      • et al.
      Reduction of postoperative pulmonary complications after lung surgery using fast track clinical pathway.
      With the use of propensity matching, Salati and colleagues
      • 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.
      were able to show that the introduction of a fast-track pathway resulted in a reduced LOS. Their protocols focused on preoperative patient education, standardizing postoperative care, and aggressive chest drain management.
      More recently, specific ERAS pathways for thoracic surgery have been described.
      • Madani A.
      • Fiore J.F.
      • Wang Y.
      • Bejjani J.
      • Sivakumaran L.
      • Mata J.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      • Scarci M.
      • Solli P.
      • Bedetti B.
      Enhanced recovery pathway for thoracic surgery in the UK.
      • Giménez-Milà M.
      • Klein A.A.
      • Martinez G.
      Design and implementation of an enhanced recovery program in thoracic surgery.
      Madani and colleagues
      • Madani A.
      • Fiore J.F.
      • Wang Y.
      • Bejjani J.
      • Sivakumaran L.
      • Mata J.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      introduced an ERAS program for open lobectomy, standardizing care and addressing preoperative, intraoperative, and postoperative elements of the patient pathway. They were able to demonstrate a reduction in LOS and a reduced number of complications without an increase in readmission rates. However, their protocols were relatively conservative. A move away from epidural analgesia to paravertebral blockade and more aggressive chest drain protocols may have allowed them to demonstrate even greater benefits.
      • Yeung J.H.
      • Gates S.
      • Naidu B.V.
      • Wilson M.J.
      • Gao Smith F.
      Paravertebral block versus thoracic epidural for patients undergoing thoracotomy.
      • Baidya D.K.
      • Khanna P.
      • Maitra S.
      Analgesic efficacy and safety of thoracic paravertebral and epidural analgesia for thoracic surgery: a systematic review and meta-analysis.
      • Cerfolio R.J.
      • Bryant A.S.
      Results of a prospective algorithm to remove chest tubes after pulmonary resection with high output.
      • Bjerregaard L.S.
      • Jensen K.
      • Petersen R.H.
      • Hansen H.J.
      Early chest tube removal after video-assisted thoracic surgery lobectomy with serous fluid production up to 500 ml/day.
      A number of different elements make up ERAS programs. It has not been possible to say whether some elements are more influential than others or whether adherence to the pathway in its entirety is more important. Experience in colorectal cancer surgery indicates that both options may hold true.
      • Gustafsson U.O.
      • Hausel J.
      • Thorell A.
      • Ljungqvist O.
      • Soop M.
      • Nygren J.
      Adherence to the enhanced recovery after surgery protocol and outcomes after colorectal cancer surgery.
      Increasing adherence to an ERAS pathway was associated with improved clinical outcomes, specifically reduced morbidity, symptoms, and readmissions. At the same time, restriction of intravenous fluids and the use of preoperative carbohydrate drinks were independent predictors of improved outcomes. Results from a large international registry on ERAS compliance in colorectal cancer surgery have corroborated these earlier results, while also demonstrating a reducing LOS with increasing compliance.
      ERAS Compliance Group
      The impact of enhanced recovery protocol compliance on elective colorectal cancer resection: results from an international registry.
      Furthermore, minimally invasive surgery was identified as an independent factor. Other independent factors for a shorter hospital stay included preoperative carbohydrate loading, total intravenous anesthesia, and avoidance of epidural analgesia, whereas restriction of perioperative intravenous fluids was associated with fewer complications.
      The feared consequence of introducing a fast-track program is that readmissions will increase. A readmission is harmful to patients with lung cancer and is associated with reduced short-term and long-term survival.
      • Puri V.
      • Patel A.P.
      • Crabtree T.D.
      • Bell J.M.
      • Broderick S.R.
      • Kreisel D.
      • et al.
      Unexpected readmission after lung cancer surgery: a benign event?.
      These concerns have not been realized in colorectal cancer surgery or other specialties.
      • Nicholson A.
      • Lowe M.C.
      • Parker J.
      • Lewis S.R.
      • Alderson P.
      • Smith A.F.
      Systematic review and meta-analysis of enhanced recovery programmes in surgical patients.
      • Paton F.
      • Chambers D.
      • Wilson P.
      • Eastwood A.
      • Craig D.
      • Fox D.
      • et al.
      Effectiveness and implementation of enhanced recovery after surgery programmes: a rapid evidence synthesis.
      Likewise, an increase in readmissions has not been demonstrated after lung cancer surgery within a fast-track or ERAS program.
      • 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.
      • Madani A.
      • Fiore J.F.
      • Wang Y.
      • Bejjani J.
      • Sivakumaran L.
      • Mata J.
      • et al.
      An enhanced recovery pathway reduces duration of stay and complications after open pulmonary lobectomy.
      In this study, our 30-day readmission rate was 5.5%. This is in keeping with other studies and registries.
      • 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.
      • Puri V.
      • Patel A.P.
      • Crabtree T.D.
      • Bell J.M.
      • Broderick S.R.
      • Kreisel D.
      • et al.
      Unexpected readmission after lung cancer surgery: a benign event?.
      However, one shortfall of this study is the inability to determine whether our ERAS pathway had an adverse effect on readmissions, because we have not included a comparator group before the introduction of the program.
      Minimally invasive surgery appears to be an independent predictor of a favorable outcome after colorectal cancer surgery within ERAS programs.
      ERAS Compliance Group
      The impact of enhanced recovery protocol compliance on elective colorectal cancer resection: results from an international registry.
      • Zhuang C.L.
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      • et al.
      Laparoscopic versus open colorectal surgery within enhanced recovery after surgery programs: a systematic review and meta-analysis of randomized controlled trials.
      VATS lung resection is increasing in popularity as evidence emerges of its efficacy in treating lung cancer while potentially improving outcomes.
      • Bendixen M.
      • Jørgensen O.D.
      • Kronberg C.
      • Andersen C.
      • Licht P.B.
      Postoperative pain and quality of life after lobectomy via video-assisted thoracoscopic surgery or anterolateral thoracotomy for early stage lung cancer: a randomised controlled trial.
      • Falcoz P.-E.
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      • Thomas P.-A.
      • Decaluwe H.
      • Hürtgen M.
      • Petersen R.H.
      • et al.
      Video-assisted thoracoscopic surgery versus open lobectomy for primary non-small-cell lung cancer: a propensity-matched analysis of outcome from the European Society of Thoracic Surgeon database.
      This study is the first to look at a well-established VATS program within an ERAS pathway. VATS lung resection was an independent predictor of LOS but not a predictor of morbidity.
      Immobility after thoracic surgery is common and largely due to modifiable factors, such as pain, nausea, drowsiness, continued chest drainage, and feeling light headed.
      • Agostini P.J.
      • Naidu B.
      • Rajesh P.
      • Steyn R.
      • Bishay E.
      • Kalkat M.
      • et al.
      Potentially modifiable factors contribute to limitation in physical activity following thoracotomy and lung resection: a prospective observational study.
      In this study, we have demonstrated that mobilization within the first 24 hours is beneficial in terms of LOS and morbidity. Early mobilization has been identified as a factor in reducing complications in a fast-track program,
      • Das-Neves-Pereira J.C.
      Fast-track rehabilitation for lung cancer lobectomy: a five-year experience.
      although a recent systematic review did not identify any benefits because of the poor quality of studies and conflicting results.
      • Caastelino T.
      • Fiore J.F.
      • Niculiseanu P.
      • Landry T.
      • Augustin B.
      • Feldman L.S.
      The effect of early mobilization protocols on postoperative outcomes following abdominal and thoracic surgery: a systematic review.
      Several elements of our ERAS pathway are likely to positively influence early mobilization. These include targeted PONV control, avoidance of epidural analgesia, a standardized analgesia regimen with avoidance of opiates where possible, and avoidance of fluid overload. The use of a digital chest drainage system with aggressive chest drain management may help.
      • Pompili C.
      • Detterbeck F.
      • Papagiannopoulos K.
      • Sihoe A.
      • Vachlas K.
      • Maxfield M.W.
      • et al.
      Multicenter international randomized comparison of objective and subjective outcomes between electronic and traditional chest drainage systems.

      Study Limitations

      A limitation of this study is the lack of a control group. This has been recognized as a potential problem in studies looking at the effects of ERAS and fast-track pathways in thoracic surgery.
      • Fiore J.F.
      • Bejjani J.
      • Conrad K.
      • Niculiseanu P.
      • Landry T.
      • Lee L.
      • et al.
      Systematic review of the influence of enhanced recovery pathways in elective lung resection.
      Indeed, there has only been 1 small and underpowered randomized controlled trial reported.
      • Muehling B.M.
      • Halter G.L.
      • Schelzig H.
      • Meirerhenrich R.
      • Steffen P.
      • Sunder-Plassman L.
      • et al.
      Reduction of postoperative pulmonary complications after lung surgery using fast track clinical pathway.
      Consequently, making statements about the ability of an ERAS pathway to reduce morbidity and shorten hospital stay when compared with traditional care is likely to introduce a number of biases, including selection, detection, and performance bias.
      • Fiore J.F.
      • Bejjani J.
      • Conrad K.
      • Niculiseanu P.
      • Landry T.
      • Lee L.
      • et al.
      Systematic review of the influence of enhanced recovery pathways in elective lung resection.
      In this study, we made no comparison with traditional care. All patients in our institution are on an ERAS pathway irrespective of procedure, comorbidities, or surgical approach, and this article reports consecutive patients admitted under our care over a 2-year period. A randomized controlled trial would be ideal but is likely to prove impossible to run because there would be considerable contamination between control and study groups managed in the same institution on the same ward by the same team. Another limitation of our study is the potential risk for postoperative ERAS compliance to be affected by the presence of early complications. However, in analysis of LOS in which morbidity was excluded and therefore the potential for reverse causality limited, a relationship of compliance with ERAS protocols remained even when including those patients admitted to the intensive therapy unit/high dependency unit (and therefore most likely to develop an early complication).

      Conclusions

      In patients undergoing lung cancer resection within an ERAS program, increased compliance with ERAS protocols is associated with a reduction in postoperative morbidity. Early mobilization after surgery is independently associated with reduced morbidity and LOS. In addition, VATS lung resection is associated with reduced LOS. Although it is clear that greater adherence to an ERAS pathway is associated with improved clinical outcomes, several elements appear to be more influential than others. ERAS pathways should be considered for care of all patients undergoing surgery for primary lung cancer.

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      Conflict of Interest Statement

      Authors have nothing to disclose with regard to commercial support.
      The authors thank V. D. Bruno of Wissenroad Ltd, for conducting the statistical review of the article.

      Supplementary Data

      References

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      Linked Article

      • How much can you “enhance” recovery after lung resection?
        The Journal of Thoracic and Cardiovascular SurgeryVol. 155Issue 4
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          The enhanced recovery after surgery movement is certainly gathering momentum. Origins can be traced as far back as the 1990s in colorectal surgery, where fast-track programs achieved a median postoperative hospital stay of 2 days in patients undergoing open colectomy compared with the accepted postoperative hospital stay of 5 to 10 days at the time.1 Since then, “enhanced recovery” (a more politically correct–sounding phrase compared with “fast track”) has been promoted across many Health Boards in Europe and the United Kingdom (National Health Service).
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