Association of Preoperative Patient Frailty and Operative Stress With Postoperative Mortality | Geriatrics | JAMA Surgery | JAMA Network
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Figure 1.  Mortality at 30, 90, and 180 Days Stratified by Risk Analysis Index (RAI)
Mortality at 30, 90, and 180 Days Stratified by Risk Analysis Index (RAI)

The categories of Operative Stress Score are defined as follows: 1, very low stress; 2, low stress; 3, moderate stress; 4, high stress; and 5, very high stress. The RAI is based on the accumulation of deficits model of frailty and uses 14 variables to generate a score from 0 to 81, with higher scores indicating more frailty.

Figure 2.  Mortality at 30, 90, and 180 Days Stratified by Frailty and Number of Complications
Mortality at 30, 90, and 180 Days Stratified by Frailty and Number of Complications

The categories of Operative Stress Score are defined as follows: 1, very low stress; 2, low stress; 3, moderate stress; 4, high stress; and 5, very high stress. The Risk Analysis Index (RAI) is based on the accumulation of deficits model of frailty and uses 14 variables to generate a score from 0 to 81, with higher scores indicating more frailty.

Table 1.  Demographic Characteristics
Demographic Characteristics
Table 2.  Most Prevalent Procedures by OSS
Most Prevalent Procedures by OSS
Table 3.  The 30-, 90-, and 180-Day Mortality by OSSa
The 30-, 90-, and 180-Day Mortality by OSSa
1.
Makary  MA, Segev  DL, Pronovost  PJ,  et al.  Frailty as a predictor of surgical outcomes in older patients.  J Am Coll Surg. 2010;210(6):901-908. doi:10.1016/j.jamcollsurg.2010.01.028PubMedGoogle ScholarCrossref
2.
Robinson  TN, Wu  DS, Pointer  L, Dunn  CL, Cleveland  JC  Jr, Moss  M.  Simple frailty score predicts postoperative complications across surgical specialties.  Am J Surg. 2013;206(4):544-550. doi:10.1016/j.amjsurg.2013.03.012PubMedGoogle ScholarCrossref
3.
Lin  HS, Watts  JN, Peel  NM, Hubbard  RE.  Frailty and post-operative outcomes in older surgical patients: a systematic review.  BMC Geriatr. 2016;16(1):157. doi:10.1186/s12877-016-0329-8PubMedGoogle ScholarCrossref
4.
Robinson  TN, Wallace  JI, Wu  DS,  et al.  Accumulated frailty characteristics predict postoperative discharge institutionalization in the geriatric patient.  J Am Coll Surg. 2011;213(1):37-42. doi:10.1016/j.jamcollsurg.2011.01.056PubMedGoogle ScholarCrossref
5.
Kim  SW, Han  HS, Jung  HW,  et al.  Multidimensional frailty score for the prediction of postoperative mortality risk.  JAMA Surg. 2014;149(7):633-640. doi:10.1001/jamasurg.2014.241PubMedGoogle ScholarCrossref
6.
McIsaac  DI, Bryson  GL, van Walraven  C.  Association of frailty and 1-year postoperative mortality following major elective noncardiac surgery: a population-based cohort study.  JAMA Surg. 2016;151(6):538-545. doi:10.1001/jamasurg.2015.5085PubMedGoogle ScholarCrossref
7.
McIsaac  DI, Taljaard  M, Bryson  GL,  et al.  Frailty as a predictor of death or new disability after surgery: a prospective cohort study  [published ahead of print July 24, 2018].  Ann Surg. 2018. doi:10.1097/SLA.0000000000002967PubMedGoogle Scholar
8.
Shah  R, Attwood  K, Arya  S,  et al.  Association of frailty with failure to rescue after low-risk and high-risk inpatient surgery.  JAMA Surg. 2018;153(5):e180214. doi:10.1001/jamasurg.2018.0214PubMedGoogle Scholar
9.
Joseph  B, Phelan  H, Hassan  A,  et al.  The impact of frailty on failure-to-rescue in geriatric trauma patients: a prospective study.  J Trauma Acute Care Surg. 2016;81(6):1150-1155. doi:10.1097/TA.0000000000001250PubMedGoogle ScholarCrossref
10.
Arya  S, Kim  SI, Duwayri  Y,  et al.  Frailty increases the risk of 30-day mortality, morbidity, and failure to rescue after elective abdominal aortic aneurysm repair independent of age and comorbidities.  J Vasc Surg. 2015;61(2):324-331. doi:10.1016/j.jvs.2014.08.115PubMedGoogle ScholarCrossref
11.
Saxton  A, Velanovich  V.  Preoperative frailty and quality of life as predictors of postoperative complications.  Ann Surg. 2011;253(6):1223-1229. doi:10.1097/SLA.0b013e318214bce7PubMedGoogle ScholarCrossref
12.
Augustin  T, Burstein  MD, Schneider  EB,  et al.  Frailty predicts risk of life-threatening complications and mortality after pancreatic resections.  Surgery. 2016;160(4):987-996. doi:10.1016/j.surg.2016.07.010PubMedGoogle ScholarCrossref
13.
Farhat  JS, Velanovich  V, Falvo  AJ,  et al.  Are the frail destined to fail? frailty index as predictor of surgical morbidity and mortality in the elderly.  J Trauma Acute Care Surg. 2012;72(6):1526-1530. doi:10.1097/TA.0b013e3182542fabPubMedGoogle ScholarCrossref
14.
Suskind  AM, Walter  LC, Jin  C,  et al.  Impact of frailty on complications in patients undergoing common urological procedures: a study from the American College of Surgeons National Surgical Quality Improvement database.  BJU Int. 2016;117(5):836-842. doi:10.1111/bju.13399PubMedGoogle ScholarCrossref
15.
Adams  P, Ghanem  T, Stachler  R, Hall  F, Velanovich  V, Rubinfeld  I.  Frailty as a predictor of morbidity and mortality in inpatient head and neck surgery.  JAMA Otolaryngol Head Neck Surg. 2013;139(8):783-789. doi:10.1001/jamaoto.2013.3969PubMedGoogle ScholarCrossref
16.
George  EM, Burke  WM, Hou  JY,  et al.  Measurement and validation of frailty as a predictor of outcomes in women undergoing major gynaecological surgery.  BJOG. 2016;123(3):455-461. doi:10.1111/1471-0528.13598PubMedGoogle ScholarCrossref
17.
Seib  CD, Rochefort  H, Chomsky-Higgins  K,  et al.  Association of patient frailty with increased morbidity after common ambulatory general surgery operations.  JAMA Surg. 2018;153(2):160-168. doi:10.1001/jamasurg.2017.4007PubMedGoogle ScholarCrossref
18.
Rumer  KK, Saraswathula  A, Melcher  ML.  Prehabilitation in our most frail surgical patients: are wearable fitness devices the next frontier?  Curr Opin Organ Transplant. 2016;21(2):188-193. doi:10.1097/MOT.0000000000000295PubMedGoogle ScholarCrossref
19.
Halloway  S, Buchholz  SW, Wilbur  J, Schoeny  ME.  Prehabilitation interventions for older adults: an integrative review.  West J Nurs Res. 2015;37(1):103-123. doi:10.1177/0193945914551006PubMedGoogle ScholarCrossref
20.
Gillis  C, Li  C, Lee  L,  et al.  Prehabilitation versus rehabilitation: a randomized control trial in patients undergoing colorectal resection for cancer.  Anesthesiology. 2014;121(5):937-947. doi:10.1097/ALN.0000000000000393PubMedGoogle ScholarCrossref
21.
Carli  F, Awasthi  R, Gillis  C, Kassouf  W.  Optimizing a frail elderly patient for radical cystectomy with a prehabilitation program.  Can Urol Assoc J. 2014;8(11-12):E884-E887. doi:10.5489/cuaj.2025PubMedGoogle ScholarCrossref
22.
Hall  DE, Arya  S, Schmid  KK,  et al.  Development and initial validation of the Risk Analysis Index for measuring frailty in surgical populations.  JAMA Surg. 2017;152(2):175-182. doi:10.1001/jamasurg.2016.4202PubMedGoogle ScholarCrossref
23.
Arya  S, Varley  P, Youk  A,  et al.  Recalibration and external validation of the Risk Analysis Index: a surgical frailty assessment tool  [published online March 19, 2019].  Ann Surg. 2019. doi:10.1097/SLA.0000000000003276PubMedGoogle Scholar
24.
Schwarze  ML, Barnato  AE, Rathouz  PJ,  et al.  Development of a list of high-risk operations for patients 65 years and older.  JAMA Surg. 2015;150(4):325-331. doi:10.1001/jamasurg.2014.1819PubMedGoogle ScholarCrossref
25.
Massarweh  NN, Kaji  AH, Itani  KMF.  Practical guide to surgical data sets: Veterans Affairs Surgical Quality Improvement Program (VASQIP).  JAMA Surg. 2018;153(8):768-769. doi:10.1001/jamasurg.2018.0504PubMedGoogle ScholarCrossref
26.
Powell  C.  The Delphi technique: myths and realities.  J Adv Nurs. 2003;41(4):376-382. doi:10.1046/j.1365-2648.2003.02537.xPubMedGoogle ScholarCrossref
27.
Jones  J, Hunter  D.  Consensus methods for medical and health services research.  BMJ. 1995;311(7001):376-380. doi:10.1136/bmj.311.7001.376PubMedGoogle ScholarCrossref
28.
Harris  PA, Taylor  R, Thielke  R, Payne  J, Gonzalez  N, Conde  JG.  Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.  J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010PubMedGoogle ScholarCrossref
29.
Copeland  GP, Jones  D, Walters  M.  POSSUM: a scoring system for surgical audit.  Br J Surg. 1991;78(3):355-360. doi:10.1002/bjs.1800780327PubMedGoogle ScholarCrossref
30.
Scott  S, Lund  JN, Gold  S,  et al.  An evaluation of POSSUM and P-POSSUM scoring in predicting post-operative mortality in a level 1 critical care setting.  BMC Anesthesiol. 2014;14:104. doi:10.1186/1471-2253-14-104PubMedGoogle ScholarCrossref
31.
Haga  Y, Ikei  S, Ogawa  M.  Estimation of Physiologic Ability and Surgical Stress (E-PASS) as a new prediction scoring system for postoperative morbidity and mortality following elective gastrointestinal surgery.  Surg Today. 1999;29(3):219-225. doi:10.1007/BF02483010PubMedGoogle ScholarCrossref
32.
Haga  Y, Ikejiri  K, Wada  Y,  et al.  A multicenter prospective study of surgical audit systems.  Ann Surg. 2011;253(1):194-201. doi:10.1097/SLA.0b013e3181f66199PubMedGoogle ScholarCrossref
33.
McIsaac  DI, Moloo  H, Bryson  GL, van Walraven  C.  The association of frailty with outcomes and resource use after emergency general surgery: a population-based cohort study.  Anesth Analg. 2017;124(5):1653-1661. doi:10.1213/ANE.0000000000001960PubMedGoogle ScholarCrossref
34.
Fried  TR, Bradley  EH, Towle  VR, Allore  H.  Understanding the treatment preferences of seriously ill patients.  N Engl J Med. 2002;346(14):1061-1066. doi:10.1056/NEJMsa012528PubMedGoogle ScholarCrossref
35.
van der Windt  DJ, Bou-Samra  P, Dadashzadeh  ER, Chen  X, Varley  PR, Tsung  A.  Preoperative Risk Analysis Index for frailty predicts short-term outcomes after hepatopancreatobiliary surgery.  HPB (Oxford). 2018;20(12):1181-1188. doi:10.1016/j.hpb.2018.05.016PubMedGoogle ScholarCrossref
36.
Esses  G, Andreopoulos  E, Lin  HM, Arya  S, Deiner  S.  A comparison of three frailty indices in predicting morbidity and mortality after on-pump aortic valve replacement.  Anesth Analg. 2018;126(1):39-45. doi:10.1213/ANE.0000000000002411PubMedGoogle ScholarCrossref
37.
Hall  DE, Arya  S, Schmid  KK,  et al.  Association of a frailty screening initiative with postoperative survival at 30, 180, and 365 days.  JAMA Surg. 2017;152(3):233-240. doi:10.1001/jamasurg.2016.4219PubMedGoogle ScholarCrossref
38.
Isharwal  S, Johanning  JM, Dwyer  JG, Schimid  KK, LaGrange  CA.  Preoperative frailty predicts postoperative complications and mortality in urology patients.  World J Urol. 2017;35(1):21-26. doi:10.1007/s00345-016-1845-zPubMedGoogle ScholarCrossref
39.
Ernst  KF, Hall  DE, Schmid  KK,  et al.  Surgical palliative care consultations over time in relationship to systemwide frailty screening.  JAMA Surg. 2014;149(11):1121-1126. doi:10.1001/jamasurg.2014.1393PubMedGoogle ScholarCrossref
40.
Berian  JR, Mohanty  S, Ko  CY, Rosenthal  RA, Robinson  TN.  Association of loss of independence with readmission and death after discharge in older patients after surgical procedures.  JAMA Surg. 2016;151(9):e161689. doi:10.1001/jamasurg.2016.1689PubMedGoogle Scholar
41.
VanderWeele  TJ.  On the promotion of human flourishing.  Proc Natl Acad Sci U S A. 2017;114(31):8148-8156. doi:10.1073/pnas.1702996114PubMedGoogle ScholarCrossref
42.
VanderWeele  TJ, McNeely  E, Koh  HK.  Reimagining health-flourishing.  JAMA. 2019;321(17):1667-1668. doi:10.1001/jama.2019.3035PubMedGoogle ScholarCrossref
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    2 Comments for this article
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    Differentiation between emergency and elective surgery for operative stress assessment
    Rahul Gupta, MBBS, MS, MCh | Synergy Institute of Medical Sciences
    I read with interest the article by Shinall et al on the association between patient fraility and operative stress. But on reading the details about the operative stress score, I did not understand how the stress associated with emergency surgery was taken in to account. For example, a given patient undergoing emergency open colectomy for intestinal obstruction or perforation is obviously having higher operative stress compared to a patient undergoing elective open colectomy. The authors need to clarify whether this aspect was taken in to consideration while preparing operative risk score.
    CONFLICT OF INTEREST: None Reported
    Response to Dr. Gupta on behalf of the authors
    Amalia Cochran, MD | The Ohio State University
    We thank the reader for this perceptive comment, and we agree that the emergent vs. elective status of the surgical procedure is of paramount importance. In developing the Operative Stress Score, the raters were asked to consider the stress associated with the procedure in an elective setting. The dataset used for the published analysis included all surgeries included in VASQIP for the specified years, both elective and emergent. Our intention was to provide an analysis that was generalizable to the broadest sample of surgery as actually performed across the VA. However, this reader is not the first to inquire about the relative impact of emergency status on our analysis, and thus we have just completed subgroup analyses that examine the relationship of operative stress, frailty and mortality in elective and emergent contexts. In brief, although mortality is higher among emergent surgeries, the same pattern of mortality and frailty across all ranges of operative stress is observed in both the emergent and elective sub-samples. We have submitted these findings for consideration as a peer-reviewed publication.
    CONFLICT OF INTEREST: None Reported
    READ MORE
    Original Investigation
    November 13, 2019

    Association of Preoperative Patient Frailty and Operative Stress With Postoperative Mortality

    Author Affiliations
    • 1Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee
    • 2Division of Vascular Surgery, Stanford University School of Medicine, Stanford, California
    • 3Surgical Service Line, Veterans Affairs Palo Alto Healthcare System, Palo Alto, California
    • 4Center for Health Equity Research and Promotion, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, Pennsylvania
    • 5Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 6Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 7Department of Surgery, Henry Ford Health System, Detroit, Michigan
    • 8Center for Innovations in Quality, Effectiveness, and Safety, Michael E. DeBakey Veterans Affairs Medical Center, Houston, Texas
    • 9Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas
    • 10Department of Surgery, University of Texas Health San Antonio, San Antonio
    • 11South Texas Veterans Health Care System, San Antonio
    • 12Department of Surgery, University of Nebraska Medical Center, Omaha
    • 13Nebraska Western Iowa Veterans Affairs Health System, Omaha
    • 14Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Vanderbilt University Medical Center, Nashville, Tennessee
    • 15Department of Cardiothoracic Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 16Department of Surgery, Stanford University, Palo Alto, California
    • 17Deparment of Plastic Surgery, Vanderbilt University Medical Center, Nashville, Tennessee
    • 18Department of Obstetrics and Gynecology, University of Nebraska Medical Center, Omaha
    • 19Department of Anesthesiology and Perioperative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 20Department of Otolaryngology, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 21Division of Urology, University of Nebraska Medical Center, Omaha
    • 22Department of Otolaryngology, Vanderbilt University Medical Center, Nashville, Tennessee
    • 23Perioperative Surgical Home, Henry Ford Health System, Detroit, Michigan
    • 24Department of Orthopedic Surgery, Henry Ford Health System, Detroit, Michigan
    • 25Department of Anesthesiology, Henry Ford Health System, Detroit, Michigan
    • 26Department of Orthopaedic Surgery and Rehabilitation, University of Nebraska Medical Center, Omaha
    • 27Department of Urology, Vanderbilt University Medical Center, Nashville, Tennessee
    • 28Department of Neurosurgery, University of Nebraska Medical Center, Omaha
    • 29Wolff Center, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
    JAMA Surg. 2020;155(1):e194620. doi:10.1001/jamasurg.2019.4620
    Key Points

    Question  Is frailty associated with increased risk of postoperative mortality across all levels of operative stress?

    Findings  In this cohort study of 432 828 unique patients, frailty was associated with increased 30-, 90-, and 180-day mortality across all levels of operative stress. Mortality among patients with frailty after low- and moderate-stress procedures was substantially higher than mortality rates usually associated with high-risk surgical procedures.

    Meaning  The findings suggest that even minor surgical procedures are associated with high risk for patients with frailty and that surgeons and referring physicians should consider whether the potential benefits of surgery warrant the increased risk.

    Abstract

    Importance  Patients with frailty have higher risk for postoperative mortality and complications; however, most research has focused on small groups of high-risk procedures. The associations among frailty, operative stress, and mortality are poorly understood.

    Objective  To assess the association between frailty and mortality at varying levels of operative stress as measured by the Operative Stress Score, a novel measure created for this study.

    Design, Setting, and Participants  This retrospective cohort study included veterans in the Veterans Administration Surgical Quality Improvement Program from April 1, 2010, through March 31, 2014, who underwent a noncardiac surgical procedure at Veterans Health Administration Hospitals and had information available on vital status (whether the patient was alive or deceased) at 1 year postoperatively. A Delphi consensus method was used to stratify surgical procedures into 5 categories of physiologic stress.

    Exposures  Frailty as measured by the Risk Analysis Index and operative stress as measured by the Operative Stress Score.

    Main Outcomes and Measures  Postoperative mortality at 30, 90, and 180 days.

    Results  Of 432 828 unique patients (401 453 males [92.8%]; mean (SD) age, 61.0 [12.9] years), 36 579 (8.5%) were frail and 9113 (2.1%) were very frail. The 30-day mortality rate among patients who were frail and underwent the lowest-stress surgical procedures (eg, cystoscopy) was 1.55% (95% CI, 1.20%-1.97%) and among patients with frailty who underwent the moderate-stress surgical procedures (eg, laparoscopic cholecystectomy) was 5.13% (95% CI, 4.79%-5.48%); these rates exceeded the 1% mortality rate often used to define high-risk surgery. Among patients who were very frail, 30-day mortality rates were higher after the lowest-stress surgical procedures (10.34%; 95% CI, 7.73%-13.48%) and after the moderate-stress surgical procedures (18.74%; 95% CI, 17.72%-19.80%). For patients who were frail and very frail, mortality continued to increase at 90 and 180 days, reaching 43.00% (95% CI, 41.69%-44.32%) for very frail patients at 180 days after moderate-stress surgical procedures.

    Conclusions and Relevance  We developed a novel operative stress score to quantify physiologic stress for surgical procedures. Patients who were frail and very frail had high rates of postoperative mortality across all levels of the Operative Stress Score. These findings suggest that frailty screening should be applied universally because low- and moderate-stress procedures may be high risk among patients who are frail.

    Introduction

    Research shows that frailty among patients preoperatively is associated with postoperative outcomes.1-4 Patients who are frail have higher rates of morbidity, mortality, and failure to rescue after major procedures across surgical specialties.5-16 Patients who are frail also have higher rates of morbidity after ambulatory procedures typically considered to be minor.17 Thus, frailty is a salient, potentially modifiable patient characteristic in surgical practice.18-21

    Frailty is a global syndrome of decreased physiologic reserve accurately measured by the Risk Analysis Index (RAI).22,23 Surgical stress can exhaust the limited reserve of patients who are frail, leading to decompensation and death. Understanding of whether frailty’s association with poor outcomes varies with the physiologic stress of surgery is inadequate. Patients who undergo physiologically taxing, higher-stress surgical procedures may seem to be at greatest risk, and existing research on surgical risk assessment has focused on such high-risk inpatient surgical procedures.24 Previous work8 showed that frailty was associated with poor outcomes even after procedures with lower risk of mortality, which account for most procedures performed at most hospitals. Many surgical procedures are considered to be so minor that surgeons spend little time considering whether patients can endure the stress of the procedure. However, if frailty is associated with adverse outcomes after such low-risk, ambulatory surgical procedures, it is important to identify and counsel patients who are frail before these relatively minor procedures. Surgeons could then focus on preoperative interventions to mitigate frailty-associated risks. Patients and surgeons could also engage in more informed, shared decision-making to ensure that surgery aligns with patient values.

    To address this knowledge gap in the understanding of frailty, we designed this study to examine the association among operative stress, patient frailty, and postoperative mortality. We first used a modified Delphi consensus method to establish a measure of operative stress based on Current Procedural Terminology (CPT) codes (2017 Edition). We applied a score according to the amount of operative stress to a representative sample of surgical procedures across the Veterans Health Administration in which we also assessed frailty and postoperative mortality.

    Methods
    Patient Population and Measures

    This retrospective cohort study used data from the Veterans Affairs Surgical Quality Improvement Program (VASQIP). Case sampling methods, the robustness of the data, and available data within VASQIP have been described previously.25 We included all VASQIP records for noncardiac surgical cases between April 1, 2010, and March 31, 2014, for which 1-year postoperative vital status (whether the patient was alive or deceased) was available. The Veterans Affairs Pittsburgh Healthcare System institutional review board, Pittsburgh, Pennsylvania, approved the analysis of the VASQIP data and determined these retrospective, deidentified data to be exempt. The Vanderbilt University Medical Center institutional review board, Nashville, Tennessee, approved the process for the Delphi consensus methodology to generate the Operative Stress Score (OSS).

    We assessed patient frailty with the RAI, a validated tool with high predictive power for postoperative mortality that can be applied to quality improvement data sets.22 The RAI is based on the accumulation of deficits model of frailty and uses 14 variables to generate a score from 0 to 81, with higher scores indicating more frailty. The variables include demographic factors (age, sex), comorbidities (presence of disseminated cancer, unintentional weight loss, renal failure, congestive heart failure, poor appetite, and dyspnea at rest), cognitive decline, facility residence, and level of independence in 4 activities of daily living. Revised RAI scores were calculated from VASQIP variables according to procedures described elsewhere.23 The outcomes of interest were 30-day, 90-day, and 180-day all-cause mortality.

    Operative Stress Score

    We used a modified Delphi consensus method24,26,27 to rate common surgical procedures according to physiologic stress, naming the resulting scale the OSS. The categories are defined as follows: OSS 1, very low stress; OSS 2, low stress; OSS 3, moderate stress; OSS 4, high stress; and OSS 5, very high stress. For pragmatic feasibility, we chose a set of CPT codes comprising 90.0% of all procedures included in our VASQIP cohort. We then recruited a panel of staff-level surgeons and anesthesiologists across the specialty fields covered by these CPT codes. Specialty-specific subpanels included at least 3 surgeons (or anesthesiologists) who we purposively sampled to include early-, mid-, and late-career physicians practicing within 5 years, 5 to 10 years, and more than 10 years, respectively, from completion of residency. Anesthesiologists rated all CPT codes; surgical specialists rated only those CPT codes within their field of practice.

    Ratings were solicited and managed using REDCap.28 Survey instructions described the concept of physiologic stress and the purpose of the rating project. Each CPT code was presented along with its verbal description. Respondents were asked to score each code on an integer scale from 1 to 5, with increasing numbers indicating increasing physiologic stress of the surgical procedure. The scoring scale was rooted with exemplars chosen by us (M.C.S., D.E.H.). For each round of scoring, we defined consensus as the modal score when at least 66% of all ratings were identical to the mode, and no score was more than 1-integer unit distant from this mode. Codes that did not reach consensus were presented again in the next round along with the summary of all scores and their mean from the previous round. This consensus process continued for 3 rounds.

    Two of us (M.C.S., D.E.H.) independently assessed codes that did not reach consensus after 3 rounds and assigned scores based on comparison with similar procedures that had reached consensus. If these 2 authors agreed, that score was assigned to the procedure; disagreement between the 2 authors resulted in the procedure being presented to the core authorship group (M.C.S., S.A., P.V., R.S., N.N.M., J.M.J., and D.E.H.), who voted to determine the final score.

    Statistical Analysis

    The RAI scores were categorized into robust (≤20), normal (21-29), frail (30-39), and very frail (≥40) as described elsewhere.23 Point estimates for mortality in each OSS and RAI stratum were calculated for each time point along with their corresponding 95% CIs using exact binomial CIs for proportions. All analyses were performed using Stata Statistical Software, release 14 (StataCorp LLC).

    Results

    The VASQIP data set contained 480 731 records, each with a single principal CPT code. We focused on the 565 most common CPT codes that defined 90.0% of the sample (n = 432 828). Demographic characteristics of this cohort are presented in Table 1; 92.8% were male (n = 401 453) and 69.3% were white (n = 299 809), with a mean (SD) age of 61.0 (12.9) years and a mean (SD) RAI score of 21.25 (7.34). The codes were grouped according to surgical discipline into 11 specialties: general surgery (n = 151), vascular surgery (n = 70), thoracic surgery (n = 20), plastic surgery (n = 25), gynecology (n = 13), urology (n = 61), otolaryngology (n = 34), hand surgery (n = 15), spine surgery (n = 25), neurosurgery (n = 21), and orthopedics (n = 130).

    The Delphi consensus process achieved consensus ratings for 528 of 565 CPT codes (93.4%) after 3 rounds (264 codes [46.7%] in round 1, 209 codes [37.0%] in round 2, and 55 codes [9.7%] in round 3); 32 (5.7%) of the remaining codes were assigned by agreement between 2 of us (M.C.S., D.E.H.), and the final 5 codes (0.9%) were assigned by majority vote of the core authorship group (M.C.S., S.A., P.V., R.S., N.N.M., J.M.J., and D.E.H.). Table 2 shows the 5 most prevalent surgical procedures at each of the 5 levels of the OSS (a full list of CPT codes with associated OSS is available in the eTable in the Supplement). Most of the procedures were classified as low-stress (OSS 2) procedures (240 procedures [42.5%]) or moderate-stress (OSS 3) procedures (179 procedures [31.7%]).

    Table 3 shows 30-, 90-, and 180-day mortality stratified by OSS. The unadjusted mortality rates at all 3 time points were lower for OSS 2 surgical procedures compared with OSS 1 surgical procedures. However, mortality rate increased as OSS increased (eg, 180-day mortality for OSS 1, 2.4%; OSS 2, 1.5%; OSS 3, 5.7%; OSS 4, 8.0%; and OSS 5, 10.2%).

    Figure 1 shows the association between OSS and mortality stratified by different levels of frailty. Among patients without frailty, mortality gradually increased as operative stress increased. Patients who were frail had higher mortality across all procedure types. For example, for OSS 1, 30-day mortality was 1.6% (95% CI, 1.2%-2.0%) for patients who were frail and 10.3% (95% CI, 7.7%-13.5%) for patients who were very frail, whereas it was 0.22% (95% CI, 0.16%-0.30%) for patients without frailty. Similar patterns occurred at 90 and 180 days. By 180 days after OSS 1 to OSS 3 surgical procedures, the mortality rates among patients who were frail was 16.22% (95% CI, 15.65%-16.80%) and among those who were very frail was 43.00% (95% CI, 41.69%-44.32%). A marked decrease in mortality in OSS 5 compared with OSS 4 surgical procedures for patients who were very frail at each time point was found.

    Figure 2 further explores the association between frailty and mortality by adding the number of postoperative complications as a fourth dimension, including failure to rescue (ie, mortality following a complication).8 Regardless of the number of complications, RAI was significantly correlated with mortality at all 3 time points (maximum R2: 21.6% for 30-day mortality; 23.9% for 90-day mortality, and 23.4% for 180-day mortality). At every level of OSS, presence of more complications was associated with higher mortality. Patients who were frail and very frail without any complications had substantial mortality at all OSS levels, and complications among the frail were associated with even higher mortality rates.

    Discussion

    We used a Delphi consensus method to develop the OSS, a new rating system categorizing common surgical CPT codes according to the degree of physiologic stress. In contrast to other surgical risk scoring systems that incorporate specific operative factors,29-32 the OSS provides a consistent, global assessment of operative stress. The development of the OSS allowed us to compare the association of frailty across a diverse array of surgical procedures with differing levels of operative stress. The face validity of this taxonomy was supported by mortality rates that increased with increasing OSS.

    Our findings have important implications for whether operative risk should be conceptualized in terms of high-risk procedures vs high-risk patients. Although OSS 5 surgical procedures are widely recognized as high risk, patients who are frail and very frail who underwent lower-stress procedures (OSS 1-3) had mortality rates exceeding those typically reported for the highest-risk surgical procedures. Although there is no universally accepted definition of high-risk surgery, in-hospital or 30-day mortality rates greater than 1% have been used to identify high-risk procedures.8,24 By this metric, procedures at all levels of OSS are high risk for patients who are frail and very frail. Seib et al17 recently showed that frailty was associated with increased rates of complications after common ambulatory surgical procedures, and Shah et al8 showed that frailty was associated with mortality after high- and low-mortality risk surgical procedures. These results suggest that low-stress procedures are not low risk for patients who are frail. Our data indicate that there are no low-risk procedures among patients who are frail.

    The lower mortality for patients who are frail and very frail after OSS 5 surgical procedures compared with OSS 4 surgical procedures deserves special comment. Similar results were seen by McIsaac et al,6 who have shown that the association of patient frailty with outcomes differs by surgical procedure, with patient frailty having a stronger association with certain minor surgical procedures (eg, appendectomy) than with major surgical procedures (eg, pancreaticoduodenectomy).6,33 Physicians may be more attuned to patient-level risk factors when considering procedures that they perceive as high risk, leading to more careful selection and more vigorous efforts to mitigate postoperative morbidity and mortality. This hypothesis suggests that for these rare OSS 5 procedures, physicians are effectively selecting patients based on factors not captured by the RAI that indicate more favorable outcomes. If correct, this hypothesis indicates an opportunity to improve outcomes through systematic efforts to improve patient selection and optimization among patients who are frail and very frail and who consider undergoing categories OSS 1 to OSS 4 surgical procedures.

    We contend that frailty should be assessed for any patient considering surgery and that frailty-associated risks be discussed with patients in a robust process of shared decision-making. Many patients may still elect to pursue surgical intervention to manage symptoms or preserve independence because data show that older patients value quality of life at least as much as survival.34 Regardless of the indication for a given procedure (ie, palliative or therapeutic), the substantial frailty-associated risk identified here should be considered and factored into the decision-making shared between the care team and the patient.

    Beyond the specific results presented here, this study may have wider implications for surgical outcomes research and practice. This study adds to the growing body of literature showing the usefulness of the RAI as an indicator of postoperative complications and mortality across a number of different time points, patient populations, and stratifications of operative risk.8,22,35-39 Although these data report RAI scores calculated retrospectively from registry data, the RAI can be calculated with a survey instrument administered to patients at the point of care to inform real-time, patient-centered, shared decision-making.37 The information from the RAI, which is easily collected, can help physicians risk stratify their patients, and this information in the future could be incorporated with other risk models (such as the VASQIP risk calculator) to develop even more refined models of stratification. Moreover, the OSS (eTable in the Supplement) could be used in future studies as a means of stratifying the stress of operations.

    Limitations

    This study has limitations. These data derive from veteran patients, and the results may not generalize to other patient populations, especially because women are underrepresented in the sample. Future studies are needed to examine the association among frailty, operative stress, and mortality in nonveteran populations. Moreover, VASQIP data do not distinguish deaths directly related to the surgical procedure from deaths from unrelated causes. However, as a global measure of physiologic reserve, the RAI identifies risk for all-cause mortality, and the likelihood of medium-term mortality likely shifts the risk-benefit ratio because patients who are frail may not live long enough to accrue the benefits of surgery. In addition, the OSS is a physician-rated measure and does not include objective physiologic criteria. However, it is a first attempt to delineate global procedural risk across a broad range of surgical specialties and may pave the way for future research in the magnitude of surgical stress and frailty. The OSS may be particularly useful for disease-agnostic analyses of system-level factors shared across all procedure types. Mortality is not the only or even the most important outcome for patients who are frail, and our data set does not include critically important patient-reported outcome measures, such as quality of life, loss of independence, or human flourishing.40-42

    Conclusions

    These findings suggest that frailty is associated with postoperative mortality across all types of surgical procedures regardless of operative stress, and thus patients who are frail may not have the outcomes that are typical for the general population. Surgeons, anesthesiologists, and referring clinicians may wish to consider frailty to determine whether a surgical procedure is appropriate and what can be done to optimize the outcomes for these patients. There is a substantial opportunity to leverage frailty assessment to inform patient selection and optimization for the medium- and low-stress surgical procedures, which constitute most of the surgical volume at most hospitals. Although the rates of mortality for these lower-stress surgical procedures were lower compared with high-stress surgical procedures, their higher volume translates to more overall mortality. Furthermore, by 180 days, patients who were frail and very frail experienced high rates of mortality after low-stress surgical procedures even when they experienced no complications. Efforts to screen patients for frailty should not only focus on high-stress surgical procedures but should also focus on the low-stress surgical procedures, which are also risky among patients who are frail.

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    Article Information

    Accepted for Publication: August 9, 2019.

    Corresponding Author: Daniel E. Hall, MD, MDiv, MHSc, Department of Surgery, University of Pittsburgh, Ste 1264, 200 Lothrop St, Pittsburgh, PA 15213 (hallde@upmc.edu).

    Published Online: November 13, 2019. doi:10.1001/jamasurg.2019.4620

    Author Contributions: Dr Hall had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Shinall, Arya, Varley, Massarweh, Johanning, Hall.

    Acquisition, analysis, or interpretation of data: Shinall, Arya, Youk, Shah, Massarweh, Shireman, Johanning, Hall.

    Drafting of the manuscript: Shinall, Arya, Youk, Johanning, Hall.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Youk, Hall.

    Obtained funding: Shireman, Hall.

    Administrative, technical, or material support: Arya, Johanning.

    Supervision: Shinall, Arya, Johanning, Hall.

    Conflict of Interest Disclosures: Dr Shinall reported receiving grants from the National Cancer Institute during the conduct of the study. Dr Arya reported receiving grants from the National Institute on Aging, the National Institutes of Health (NIH) during the conduct of the study. Dr Shireman reported receiving grants from the University of Texas Health San Antonio and grants and salary support from South Texas Veterans Health Care System during the conduct of the study. Dr Johanning reported having a patent to Futureassure LLC pending and licensed. Dr Hall reported receiving grants from the Veterans Affairs Office of Research and Development and receiving grants from the NIH during the conduct of the study. No other disclosures were reported.

    Funding/Support: This research was supported by the US Department of Veterans Affairs; the Veterans Health Administration; the Office of Research and Development; grants I21 HX-002345 and XVA 72-909 (Dr Hall) and grant CIN 13-413 (Dr Massarweh) from Health Services Research and Development; grant 5R03AG050930 (Dr Arya) from the National Institute on Aging, NIH; grant K12CA090625 (Dr Shinall) from the National Cancer Institute, NIH; and grant U01 TR002393 (Drs Hall and Shireman).

    Role of the Funder/Sponsor: The funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

    Disclaimer: The opinions expressed here are those of the authors and do not necessarily reflect the position of the Department of Veterans Affairs or the US government.

    Additional Contributions: Thomas A. Longo, MD (Duke University Medical Center, Durham, North Carolina), contributed as a panelist in the modified Delphi consensus panel and was not financially compensated for his work.

    Additional Information: The use of Operative Stress Score for relevant applications involves intellectual property rights reserved by the Board of Regents of the University of Nebraska.

    References
    1.
    Makary  MA, Segev  DL, Pronovost  PJ,  et al.  Frailty as a predictor of surgical outcomes in older patients.  J Am Coll Surg. 2010;210(6):901-908. doi:10.1016/j.jamcollsurg.2010.01.028PubMedGoogle ScholarCrossref
    2.
    Robinson  TN, Wu  DS, Pointer  L, Dunn  CL, Cleveland  JC  Jr, Moss  M.  Simple frailty score predicts postoperative complications across surgical specialties.  Am J Surg. 2013;206(4):544-550. doi:10.1016/j.amjsurg.2013.03.012PubMedGoogle ScholarCrossref
    3.
    Lin  HS, Watts  JN, Peel  NM, Hubbard  RE.  Frailty and post-operative outcomes in older surgical patients: a systematic review.  BMC Geriatr. 2016;16(1):157. doi:10.1186/s12877-016-0329-8PubMedGoogle ScholarCrossref
    4.
    Robinson  TN, Wallace  JI, Wu  DS,  et al.  Accumulated frailty characteristics predict postoperative discharge institutionalization in the geriatric patient.  J Am Coll Surg. 2011;213(1):37-42. doi:10.1016/j.jamcollsurg.2011.01.056PubMedGoogle ScholarCrossref
    5.
    Kim  SW, Han  HS, Jung  HW,  et al.  Multidimensional frailty score for the prediction of postoperative mortality risk.  JAMA Surg. 2014;149(7):633-640. doi:10.1001/jamasurg.2014.241PubMedGoogle ScholarCrossref
    6.
    McIsaac  DI, Bryson  GL, van Walraven  C.  Association of frailty and 1-year postoperative mortality following major elective noncardiac surgery: a population-based cohort study.  JAMA Surg. 2016;151(6):538-545. doi:10.1001/jamasurg.2015.5085PubMedGoogle ScholarCrossref
    7.
    McIsaac  DI, Taljaard  M, Bryson  GL,  et al.  Frailty as a predictor of death or new disability after surgery: a prospective cohort study  [published ahead of print July 24, 2018].  Ann Surg. 2018. doi:10.1097/SLA.0000000000002967PubMedGoogle Scholar
    8.
    Shah  R, Attwood  K, Arya  S,  et al.  Association of frailty with failure to rescue after low-risk and high-risk inpatient surgery.  JAMA Surg. 2018;153(5):e180214. doi:10.1001/jamasurg.2018.0214PubMedGoogle Scholar
    9.
    Joseph  B, Phelan  H, Hassan  A,  et al.  The impact of frailty on failure-to-rescue in geriatric trauma patients: a prospective study.  J Trauma Acute Care Surg. 2016;81(6):1150-1155. doi:10.1097/TA.0000000000001250PubMedGoogle ScholarCrossref
    10.
    Arya  S, Kim  SI, Duwayri  Y,  et al.  Frailty increases the risk of 30-day mortality, morbidity, and failure to rescue after elective abdominal aortic aneurysm repair independent of age and comorbidities.  J Vasc Surg. 2015;61(2):324-331. doi:10.1016/j.jvs.2014.08.115PubMedGoogle ScholarCrossref
    11.
    Saxton  A, Velanovich  V.  Preoperative frailty and quality of life as predictors of postoperative complications.  Ann Surg. 2011;253(6):1223-1229. doi:10.1097/SLA.0b013e318214bce7PubMedGoogle ScholarCrossref
    12.
    Augustin  T, Burstein  MD, Schneider  EB,  et al.  Frailty predicts risk of life-threatening complications and mortality after pancreatic resections.  Surgery. 2016;160(4):987-996. doi:10.1016/j.surg.2016.07.010PubMedGoogle ScholarCrossref
    13.
    Farhat  JS, Velanovich  V, Falvo  AJ,  et al.  Are the frail destined to fail? frailty index as predictor of surgical morbidity and mortality in the elderly.  J Trauma Acute Care Surg. 2012;72(6):1526-1530. doi:10.1097/TA.0b013e3182542fabPubMedGoogle ScholarCrossref
    14.
    Suskind  AM, Walter  LC, Jin  C,  et al.  Impact of frailty on complications in patients undergoing common urological procedures: a study from the American College of Surgeons National Surgical Quality Improvement database.  BJU Int. 2016;117(5):836-842. doi:10.1111/bju.13399PubMedGoogle ScholarCrossref
    15.
    Adams  P, Ghanem  T, Stachler  R, Hall  F, Velanovich  V, Rubinfeld  I.  Frailty as a predictor of morbidity and mortality in inpatient head and neck surgery.  JAMA Otolaryngol Head Neck Surg. 2013;139(8):783-789. doi:10.1001/jamaoto.2013.3969PubMedGoogle ScholarCrossref
    16.
    George  EM, Burke  WM, Hou  JY,  et al.  Measurement and validation of frailty as a predictor of outcomes in women undergoing major gynaecological surgery.  BJOG. 2016;123(3):455-461. doi:10.1111/1471-0528.13598PubMedGoogle ScholarCrossref
    17.
    Seib  CD, Rochefort  H, Chomsky-Higgins  K,  et al.  Association of patient frailty with increased morbidity after common ambulatory general surgery operations.  JAMA Surg. 2018;153(2):160-168. doi:10.1001/jamasurg.2017.4007PubMedGoogle ScholarCrossref
    18.
    Rumer  KK, Saraswathula  A, Melcher  ML.  Prehabilitation in our most frail surgical patients: are wearable fitness devices the next frontier?  Curr Opin Organ Transplant. 2016;21(2):188-193. doi:10.1097/MOT.0000000000000295PubMedGoogle ScholarCrossref
    19.
    Halloway  S, Buchholz  SW, Wilbur  J, Schoeny  ME.  Prehabilitation interventions for older adults: an integrative review.  West J Nurs Res. 2015;37(1):103-123. doi:10.1177/0193945914551006PubMedGoogle ScholarCrossref
    20.
    Gillis  C, Li  C, Lee  L,  et al.  Prehabilitation versus rehabilitation: a randomized control trial in patients undergoing colorectal resection for cancer.  Anesthesiology. 2014;121(5):937-947. doi:10.1097/ALN.0000000000000393PubMedGoogle ScholarCrossref
    21.
    Carli  F, Awasthi  R, Gillis  C, Kassouf  W.  Optimizing a frail elderly patient for radical cystectomy with a prehabilitation program.  Can Urol Assoc J. 2014;8(11-12):E884-E887. doi:10.5489/cuaj.2025PubMedGoogle ScholarCrossref
    22.
    Hall  DE, Arya  S, Schmid  KK,  et al.  Development and initial validation of the Risk Analysis Index for measuring frailty in surgical populations.  JAMA Surg. 2017;152(2):175-182. doi:10.1001/jamasurg.2016.4202PubMedGoogle ScholarCrossref
    23.
    Arya  S, Varley  P, Youk  A,  et al.  Recalibration and external validation of the Risk Analysis Index: a surgical frailty assessment tool  [published online March 19, 2019].  Ann Surg. 2019. doi:10.1097/SLA.0000000000003276PubMedGoogle Scholar
    24.
    Schwarze  ML, Barnato  AE, Rathouz  PJ,  et al.  Development of a list of high-risk operations for patients 65 years and older.  JAMA Surg. 2015;150(4):325-331. doi:10.1001/jamasurg.2014.1819PubMedGoogle ScholarCrossref
    25.
    Massarweh  NN, Kaji  AH, Itani  KMF.  Practical guide to surgical data sets: Veterans Affairs Surgical Quality Improvement Program (VASQIP).  JAMA Surg. 2018;153(8):768-769. doi:10.1001/jamasurg.2018.0504PubMedGoogle ScholarCrossref
    26.
    Powell  C.  The Delphi technique: myths and realities.  J Adv Nurs. 2003;41(4):376-382. doi:10.1046/j.1365-2648.2003.02537.xPubMedGoogle ScholarCrossref
    27.
    Jones  J, Hunter  D.  Consensus methods for medical and health services research.  BMJ. 1995;311(7001):376-380. doi:10.1136/bmj.311.7001.376PubMedGoogle ScholarCrossref
    28.
    Harris  PA, Taylor  R, Thielke  R, Payne  J, Gonzalez  N, Conde  JG.  Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.  J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010PubMedGoogle ScholarCrossref
    29.
    Copeland  GP, Jones  D, Walters  M.  POSSUM: a scoring system for surgical audit.  Br J Surg. 1991;78(3):355-360. doi:10.1002/bjs.1800780327PubMedGoogle ScholarCrossref
    30.
    Scott  S, Lund  JN, Gold  S,  et al.  An evaluation of POSSUM and P-POSSUM scoring in predicting post-operative mortality in a level 1 critical care setting.  BMC Anesthesiol. 2014;14:104. doi:10.1186/1471-2253-14-104PubMedGoogle ScholarCrossref
    31.
    Haga  Y, Ikei  S, Ogawa  M.  Estimation of Physiologic Ability and Surgical Stress (E-PASS) as a new prediction scoring system for postoperative morbidity and mortality following elective gastrointestinal surgery.  Surg Today. 1999;29(3):219-225. doi:10.1007/BF02483010PubMedGoogle ScholarCrossref
    32.
    Haga  Y, Ikejiri  K, Wada  Y,  et al.  A multicenter prospective study of surgical audit systems.  Ann Surg. 2011;253(1):194-201. doi:10.1097/SLA.0b013e3181f66199PubMedGoogle ScholarCrossref
    33.
    McIsaac  DI, Moloo  H, Bryson  GL, van Walraven  C.  The association of frailty with outcomes and resource use after emergency general surgery: a population-based cohort study.  Anesth Analg. 2017;124(5):1653-1661. doi:10.1213/ANE.0000000000001960PubMedGoogle ScholarCrossref
    34.
    Fried  TR, Bradley  EH, Towle  VR, Allore  H.  Understanding the treatment preferences of seriously ill patients.  N Engl J Med. 2002;346(14):1061-1066. doi:10.1056/NEJMsa012528PubMedGoogle ScholarCrossref
    35.
    van der Windt  DJ, Bou-Samra  P, Dadashzadeh  ER, Chen  X, Varley  PR, Tsung  A.  Preoperative Risk Analysis Index for frailty predicts short-term outcomes after hepatopancreatobiliary surgery.  HPB (Oxford). 2018;20(12):1181-1188. doi:10.1016/j.hpb.2018.05.016PubMedGoogle ScholarCrossref
    36.
    Esses  G, Andreopoulos  E, Lin  HM, Arya  S, Deiner  S.  A comparison of three frailty indices in predicting morbidity and mortality after on-pump aortic valve replacement.  Anesth Analg. 2018;126(1):39-45. doi:10.1213/ANE.0000000000002411PubMedGoogle ScholarCrossref
    37.
    Hall  DE, Arya  S, Schmid  KK,  et al.  Association of a frailty screening initiative with postoperative survival at 30, 180, and 365 days.  JAMA Surg. 2017;152(3):233-240. doi:10.1001/jamasurg.2016.4219PubMedGoogle ScholarCrossref
    38.
    Isharwal  S, Johanning  JM, Dwyer  JG, Schimid  KK, LaGrange  CA.  Preoperative frailty predicts postoperative complications and mortality in urology patients.  World J Urol. 2017;35(1):21-26. doi:10.1007/s00345-016-1845-zPubMedGoogle ScholarCrossref
    39.
    Ernst  KF, Hall  DE, Schmid  KK,  et al.  Surgical palliative care consultations over time in relationship to systemwide frailty screening.  JAMA Surg. 2014;149(11):1121-1126. doi:10.1001/jamasurg.2014.1393PubMedGoogle ScholarCrossref
    40.
    Berian  JR, Mohanty  S, Ko  CY, Rosenthal  RA, Robinson  TN.  Association of loss of independence with readmission and death after discharge in older patients after surgical procedures.  JAMA Surg. 2016;151(9):e161689. doi:10.1001/jamasurg.2016.1689PubMedGoogle Scholar
    41.
    VanderWeele  TJ.  On the promotion of human flourishing.  Proc Natl Acad Sci U S A. 2017;114(31):8148-8156. doi:10.1073/pnas.1702996114PubMedGoogle ScholarCrossref
    42.
    VanderWeele  TJ, McNeely  E, Koh  HK.  Reimagining health-flourishing.  JAMA. 2019;321(17):1667-1668. doi:10.1001/jama.2019.3035PubMedGoogle ScholarCrossref
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