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5 - Perioperative Lung Resection Outcomes After Implementation of A Multidisciplinary, Evidence-Based Thoracic ERAS Program.
5 - Perioperative Lung Resection Outcomes After Implementation of A Multidisciplinary, Evidence-Based Thoracic ERAS Program.
5 - Perioperative Lung Resection Outcomes After Implementation of A Multidisciplinary, Evidence-Based Thoracic ERAS Program.
ANNSURG-D-19-01144
ORIGINAL ARTICLE
METHODS
From the Department of Surgery, Division of Cardiothoracic Surgery, University Study Design
of California, San Francisco, San Francisco, CA; yDepartment of Surgery,
Division of General Surgery, University of California, San Francisco, San
This is a prospective, cohort study of 295 patients who
Francisco, CA; and zDepartment of Anesthesia and Perioperative Care, underwent elective lobectomy or sublobar resection for primary lung
University of California, San Francisco, San Francisco, CA. cancer or pulmonary metastasis before (PRE n ¼ 169) and after
Y johannes.kratz@ucsf.edu. (POST n ¼ 126) implementation of the Thoracic ERAS Program at
Author contributions: G.J.H. designed the study, acquired, analyzed, and inter-
preted the data, drafted the manuscript, and gave final approval for submission.
UCSF from October, 2015 to March, 2019, which includes 2 years
B.S. and S.M. acquired the data, critically revised the manuscript, and gave before and 1.5 years after implementation. The Thoracic ERAS
final approval for submission. A.S., L.C., and D.M.J. interpreted the data, Program (Table 1) for lung resection is multidisciplinary, evi-
critically revised the manuscript, and gave final approval for submission. dence-based, addresses all facets of perioperative care, and contains
J.R.K. designed the study, interpreted the data, critically revised the manu-
script, and gave final approval for submission.
all major ERAS Society guidelines.12 The Thoracic ERAS Program
The authors report no conflicts of interest. was applied to all patients regardless of stage or number of lesions;
Supplemental digital content is available for this article. Direct URL citations however, the program was not utilized on patients with extended
appear in the printed text and are provided in the HTML and PDF versions of resections, such as chest wall resection. In addition, patients with
this article on the journal’s Web site (www.annalsofsurgery.com).
Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
length of stay 3 weeks were excluded before analysis (PRE n ¼ 1,
ISSN: 0003-4932/16/XXXX-0001 POST n ¼ 1). The UCSF Institutional Review Board approved
DOI: 10.1097/SLA.0000000000003719 the study and informed consent was waived as de-identified data
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ANNSURG-D-19-01144
were prospectively collected by chart review (Protocol # 18–26431, operating room, operative supplies, room and board, doctors, nurs-
Expiration 10/23/2019). This study was not supported by an external ing, therapy, pharmacy, laboratory assessment, and imaging. They do
funding source. not represent indirect costs, such as building maintenance or admin-
istration, and they do not represent patient charges.
Operative Technique
Open cases were approached through a standard muscle- Statistical Methods
sparing, posterolateral thoracotomy. Video-assisted thoracoscopic Descriptive statistics were used to assess baseline character-
surgery (VATS) cases were approached though a 3-port technique istics and crude perioperative outcomes PRE and POST. Outcomes
for sublobar resection or 3-port technique plus a 5th intercostal space were also evaluated in a subcohort of elderly patients defined as >73
4 to 8 cm utility incision for lobectomy. Robotic-assisted VATS (RA- years old (upper quartile). A propensity score-matched analysis was
VATS) cases were performed using a completely portal 4-arm utilized to estimate the average treatment effect of the ERAS
technique with all ports placed in the 8th interspace. Rib spreading program.14 Propensity scores were based upon the following cova-
was not utilized in VATS or RA-VATS. riates: age-adjusted Charlson comorbidity index,15 sex, race, diag-
nosis (primary lung cancer or pulmonary metastasis), and procedure
Outcomes (lobectomy or sublobar resection). In additional analyses, propensity
The primary outcome was length of stay, and the secondary scores were also based upon minimally invasive surgery, preopera-
outcomes were program adherence, overall morbidity, daily opioid tive opioid history, and epidural analgesia.
use, direct costs, 30-day readmission, and 30-day mortality. The propensity scores utilized had appropriate overlap and
Overall morbidity was defined as the presence of 1 or more in- balance between the covariates PRE and POST (Supplementary
hospital postoperative complications comprising all organ systems Digital Content—Evaluation of Propensity Scores and Matching,
(Supplementary Digital Content—Morbidity Definition, http://link- http://links.lww.com/SLA/B848). Patients were then matched using
s.lww.com/SLA/B848). In addition, morbidity was subclassified into their propensity score by nearest neighbor 1:1 matching with replace-
minor and major morbidity based upon Clavien-Dindo Class I to II or ment and caliper 0.2. The adequacy of matching was verified by a
III to IV, respectively.13 balance of matching, which appropriately reduced the predictive
Daily opioid use was defined as the total in-hospital oral value of the covariates. Overall, the propensity scores and matching
morphine equivalent (OME) use divided by the length of stay if the did not violate any model assumptions.
length of stay was 7 days. Patients with hospitalizations >7 days Missing data were found to be missing at random, and no deletion
were excluded from this analysis (excluded PRE n ¼ 11; POST n ¼ 3). or imputation methods were used. A predetermined 2-sided alpha of 0.05
Direct costs represent the total direct costs incurred to the was considered statistically significant. All analyses were performed in
medical center in providing patient care associated with surgery and Stata 15.1 (StataCorp LP; College Station, TX) using the following
subsequent hospitalization, and includes, but not limited to, the packages: pscore; psmatch2; pstest; pbalchk; teffects; psmatch.
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CE: ; ANNSURG-D-19-01144; Total nos of Pages: 6;
ANNSURG-D-19-01144
Annals of Surgery Volume XX, Number XX, Month 2019 Thoracic ERAS Lung Resection Outcomes
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ANNSURG-D-19-01144
FIGURE 1. Thoracic ERAS Program Adherence. Core components of the Thoracic ERAS Program were measured to evaluate PRE and
POST program adherence. The Thoracic ERAS Program altered clinical practice patterns, and there was appropriate adherence with
increased minimally invasive surgery, line removal, ambulation, and goal discharge as well as reduced ICU admission and epidural
analgesia for minimally invasive surgery. D/C indicates discontinue; ICU, intensive care unit; POD1, postoperative day 1.
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ANNSURG-D-19-01144
Annals of Surgery Volume XX, Number XX, Month 2019 Thoracic ERAS Lung Resection Outcomes
TABLE 4. Propensity Score-matched Analysis Accounting for Age, Sex, Race, Charlson Comorbidity Index, Diagnosis, and
Procedure.
Overall Thoracic ERAS Program
Outcomes PRE (n ¼ 466) POST (n ¼ 492) ATE (95% CI) P
Length of stay (d) 4.5 3.1 1.4 (1.9, 0.9) <0.01
Overall morbidity 36.0% 22.4% 13.6% (25.1%, 2.1%) 0.02
Direct costs ($) 23,100 19,100 4000 (6000, 2000) <0.01
30-d readmission 5.1% 7.5% 2.4% (2.7, 7.6%) 0.35
Propensity scores: age, sex, race, Charlson comorbidity index, diagnosis (primary lung cancer vs pulmonary metastasis), and procedure performed (lobectomy vs sublobar
resection).
ATE indicates average treatment effect.
TABLE 5. Propensity Score-matched Analysis Additionally Accounting for Minimally Invasive Surgery
Accounting for Minimally Invasive Surgery
Outcomes PRE (n ¼ 332) POST (n ¼ 339) ATE (95% CI) P
Length of stay (d) 4.4 3.2 1.2 (1.7, 0.7) <0.01
Overall morbidity 32.0% 20.0% 12.0% (22.5%, 1.6%) 0.02
Direct costs ($) 23,000 19,500 3500 (5900, 1100) <0.01
Readmission 6.3% 6.6% 0.3% (7.5%, 8.1%) 0.94
Propensity scores: age, sex, race, Charlson comorbidity index, diagnosis (primary lung cancer vs pulmonary metastasis), procedure performed (lobectomy vs sublobar resection),
and minimally invasive surgery.
ATE indicates average treatment effect.
thoracic surgery in an effort to improve care for our core components of the program likely contributed to these reduc-
collective patients. tions, such as patient education of the importance of ambulation and
The Thoracic ERAS Program reduced length of stay by at least breathing exercises, standardization of rehabilitation services, spe-
1 day for all patients regardless of surgical technique or procedure. cialized delirium prevention measures, and increased utilization of
Importantly, in the setting of expedited hospitalizations, readmission minimally invasive surgery. We may see further reduction in mor-
remained unchanged and nominal. Moreover, as 47% were dis- bidity with increased adherence to our analgesia, line management,
charged within program goal, we expect to further reduce length and ambulation goals.
of stay through continued management of patient expectations, and In light of the ongoing opioid epidemic, a core component of
also utilizing the momentum gained from our significant cultural the program was reduction in opioid use through utilization of
shift at the provider level. Of note, not all centers have found multimodality analgesia. The Thoracic ERAS Program reduced
improved length of stay for patients undergoing minimally invasive opioid use by 19 oral morphine equivalents daily. This finding
surgery within their ERAS programs.5,9 The discordance in findings highlights the importance of patient expectations, alignment with
is likely due to differences in the historical control, and also the nursing care, and opioid-sparing medications. We are currently
ambitiousness of the program goals. conducting a randomized, triple-blinded clinical trial evaluating
After implementation of the program, patients experienced intercostal nerve blockade with liposomal versus standard bupiva-
fewer complications with an absolute reduction in overall morbidity caine, and we may further reduce opioid use by this approach.16
by at least 12%. This finding was driven by reduction in minor From a financial perspective, the Thoracic ERAS Program
morbidity and its most prevalent complications (pneumonia, atrial reduced direct costs by at least $3500 per patient. This corresponds
fibrillation, and delirium). Importantly, we found a reduction in to a program cost savings of at least $350,000 per 100 patients
overall morbidity for our elderly patients. A combination of the undergoing lung resection annually. Not unexpectedly, reduced length
of stay and ICU utilization were the main drivers of cost savings, which
offset the intraoperative costs associated with increased minimally
TABLE 6. Propensity Score-matched Analysis of Opiod Use invasive surgery. Further cost savings from the program may have been
Accounting for Age, Sex, Race, Charlson Comorbidity Index, demonstrated by showing an improvement in available bed days and
Preoperative Opioid Use, Minimally Invasive Surgery, and the opportunity costs by freeing up hospital resources, but our study was
Use of Epidural Analgesia. limited in scope to direct costs only.
Daily Opioid Usage Our program was developed before the ERAS Society thoracic
PRE POST ATE surgery formalization, but contains all of the major guidelines and 42
Outcomes (n ¼ 239) (n ¼ 249) (95% CI) P of the 45 individual content measures.12 The 3 individual content
measures that are different pertain to preoperative fasting and chest
Daily OME 101 82 19 (36, 1) 0.04 tube drainage systems. The ERAS Society recommends preoperative
Propensity scores: age, sex, race, Charlson comorbidity index, preoperative opioid oral carbohydrate loading (Evidence Low, Recommendation Strong),
use, minimally invasive surgery, epidural analgesia; daily OME: total oral morphine fasting only 2 hours before anesthesia (Evidence High, Recommen-
equivalent (OME) per length of stay if length of stay <7 days.
ATE indicates average treatment effect.
dation Strong), and use of chest tube digital drainage systems
(Evidence Low, Recommendation Strong). The UCSF Thoracic
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ANNSURG-D-19-01144
ERAS Program utilized fasting at midnight without carbohydrate 2. Ljungqvist O, Scott M, Fearon KC. Enhanced recovery after surgery: a review.
JAMA Surg. 2017;152:292–298.
loading and standard dry suction drainage systems. Nevertheless, this
3. Nicholson A, Lowe MC, Parker J, et al. Systematic review and meta-analysis
study represents an external validation of the ERAS Society major of enhanced recovery programmes in surgical patients. Br J Surg. 2014;101:
guidelines and that these additional components can be studied as we 172–188.
continue to evaluate our program. 4. Sarin A, Litonius ES, Naidu R, et al. Successful implementation of an
This study does have limitations. A high proportion of our Enhanced Recovery After Surgery program shortens length of stay and
patients had stage I disease, and extended lung resections were improves postoperative pain, and bowel and bladder function after colorectal
surgery. BMC Anesthesiol. 2016;16:55.
excluded from this study. We suspect that other institutions may be
5. Van Haren RM, Mehran RJ, Mena GE, et al. Enhanced recovery decreases
experiencing similar upward trends in patients who present with stage I pulmonary and cardiac complications after thoracotomy for lung cancer. Ann
disease due to the steady increase in lung cancer screening adoption. In Thorac Surg. 2018;106:272–279.
addition, although the propensity score-matched analysis helped 6. Rogers LJ, Bleetman D, Messenger DE, et al. The impact of enhanced
reduce the bias of nonrandomization, there may still be unmeasured recovery after surgery (ERAS) protocol compliance on morbidity from
variables that could alter the findings. Furthermore, the Hawthorne resection for primary lung cancer. J Thorac Cardiovasc Surg. 2018;155:
1843–1852.
effect could have played a role as patients and providers were aware of
7. Madani A, Fiore JF Jr, Wang Y, et al. An enhanced recovery pathway reduces
the program and its goals. Finally, some components of the program, duration of stay and complications after open pulmonary lobectomy. Surgery.
such as patient education, do not have validated metrics that would aid 2015;158:899–908.
their evaluation. Despite these limitations, this study represents the first 8. McKenna RJ, Mahtabifard A, Pickens A, et al. Fast-tracking after video-
external validation of the ERAS Society guidelines and demonstrates assisted thoracoscopic surgery lobectomy, segmentectomy, and pneumonec-
its safety and effectiveness for patients undergoing lung resection at a tomy. Ann Thorac Surg. 2007;84:1663–1668.
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CONCLUSIONS 10. Paci P, Madani A, Lee L, et al. Economic impact of an enhanced
Use of a multidisciplinary, evidence-based Thoracic ERAS recovery pathway for lung resection. Ann Thorac Surg. 2017;104:
Program improves perioperative outcomes for patients undergoing 950–957.
lung resection. Our study demonstrates the value of a thoughtfully 11. Fiore JF, Bejjani J, Conrad K, et al. Systematic review of the influence of
enhanced recovery pathways in elective lung resection. J Thorac Cardiovasc
planned program to reduce patient morbidity and healthcare costs. Surg. 2016;151:708–715.
Adoption of such programs in the care of thoracic surgery patients 12. Batchelor TJ, Rasburn NJ, Abdelnour-Berchtold E, et al. Guidelines for
should be encouraged. enhanced recovery after lung surgery: recommendations of the
Enhanced Recovery After Surgery (ERAS) Society and the European
ACKNOWLEDGMENTS Society of Thoracic Surgeons (ESTS). Euro J Cardiothorac Surg.
2019;55:91– 115.
The authors would like to thank Christina Cheng, Courtney
13. Dindo D, Demartines N, Clavien PA. Classification of surgical complications:
Cook, Shayne Cordoza, Lisa Hayes, Jane Lee, Catherine McDo- a new proposal with evaluation in a cohort of 6336 patients and results of a
nough, Quynh Nguyen, Sean O’Keefe, and Samantha Scott for their survey. Ann Surg. 2004;240:205–213.
assistance in the implementation of the Thoracic ERAS Program, and 14. Staffa SJ, Zurakowski D. Five steps to successfully implement and evaluate
also Claudia Hermann for enabling access and assessment of our propensity score matching in clinical research studies. Anesth Analg.
institution’s financial data. 2018;127:1066–1073.
15. Charlson M, Szatrowski TP, Peterson J, et al. Validation of a combined
comorbidity index. J Clin Epidemiol. 1994;47:1245–1251.
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Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.