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Colorectal Surgery Outcomes in the United States during the COVID-19 Pandemic

Published:January 22, 2023DOI:https://doi.org/10.1016/j.jss.2022.12.041

      Highlights

      • During the COVID-19 pandemic, the proportion of emergent cases increased in the United States.
      • Patients presented to the hospital with higher ASA classification and had higher rates of overall and serious morbidity, increased proportion of discharge to home, and decreased proportion of discharge to skilled nursing facilities.
      • Multivariable analysis demonstrated increased odds of overall and serious morbidity, as well as in-hospital mortality, during Q3 July-September and/or Q4 October-December of the 2020 pandemic.

      Abstract

      Background

      The purpose of this study was to assess colorectal surgery outcomes, discharge destination, and readmission in the United States during the COVID-19 pandemic.

      Methods

      Adult colorectal surgery patients in the American College of Surgeons National Surgical Quality Improvement Program database (2019-2020) and its colectomy and proctectomy procedure-targeted files were included. The pre-pandemic time period was defined from April 1, 2019-December 31, 2019. The pandemic time period was defined from April 1, 2020-December 31, 2020 in quarterly intervals (Q2 April-June; Q3 July-September; Q4 October-December). Factors associated with morbidity and in-hospital mortality were assessed using multivariable logistic regression.

      Results

      Among 62,393 patients, 34,810 patients (55.8%) underwent colorectal surgery pre-pandemic, and 27,583 (44.2%) during the pandemic. Patients who had surgery during the pandemic had higher American Society of Anesthesiologists class and presented more frequently with dependent functional status. The proportion of emergent surgeries increased (12.7% pre-pandemic vs. 15.2% pandemic, p<0.001), with fewer laparoscopic cases (54.0% vs. 51.0%, p<0.001). Higher rates of morbidity with a greater proportion of discharges to home and lesser proportion of discharges to skilled care facilities were observed with no considerable differences in length of stay or worsening readmission rates. Multivariable analysis demonstrated increased odds of overall and serious morbidity, as well as in-hospital mortality, during Q3 and/or Q4 of the 2020 pandemic.

      Conclusions

      Differences in hospital presentation, inpatient care, and discharge disposition of colorectal surgery patients were observed during the COVID-19 pandemic. Pandemic responses should emphasize balancing resource allocation, educating patients and providers on timely medical workup and management, and optimizing discharge coordination pathways.

      Keywords

      Introduction

      The COVID-19 pandemic has brought unprecedented challenges to every aspect of society. Since the World Health Organization declared the SARS-CoV-2 coronavirus outbreak a pandemic on March 11, 2020, COVID-19 has had disease transmission to over 212 countries and territories, with over 644 million cases and 6.6 million deaths.

      The Johns Hopkins University. Johns Hopkins Coronavirus Resource Center. Accessed December 2, 2022. https://coronavirus.jhu.edu/

      Like many countries, the United States has faced dramatic rates of hospitalizations for patients with COVID-19 that have strained healthcare delivery and resulted in large-scale changes in institutional practices. These changes presented unique challenges to surgical departments. As the pandemic was declared a U.S. national emergency in March 2020, the Centers for Disease Control and Prevention recommended rescheduling elective surgeries and shifting elective inpatient surgeries to outpatient settings when feasible.
      • Moletta L.
      • Pierobon E.S.
      • Capovilla G.
      • Costantini M.
      • Salvador R.
      • Merigliano S.
      • Valmasoni M.
      International guidelines and recommendations for surgery during Covid-19 pandemic: a systematic review.
      Surgical societies including the American College of Surgeons (ACS),

      American College of Surgeons. Guidelines for triage and management of elective cancer surgery cases during the acute and recovery phases of coronavirus disease 2019 (COVID-19) pandemic. Accessed March 1, 2022. https://www.facs.org/-/media/files/covid19/acs_triage_and_management_elective_cancer_surgery_during_acute_and_recovery_phases.ashx

      the Society of Surgical Oncology (SSO),

      Society of Surgical Oncology (SSO). Cancer surgeries in the time of COVID-19: a message from the SSO president and president-elect. Accessed March 1, 2022. https://www.surgonc.org/wp-content/uploads/2020/03/COVID-19-Letter-to-Members.pdf

      and the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES)

      Society of American Gastrointestinal and Endoscopic Surgeons. SAGES and EAES recommendations regarding surgical response to COVID-19 crisis. Accessed March 1, 2022. https://www.sages.org/recommendations-surgical-response-covid-19

      issued recommendations for surgeries that should be prioritized or could be safely postponed. As a result, many surgical departments limited elective surgeries and prioritized only urgent/emergent, and non-deferrable oncological cases to limit resource utilization, preserve adequate hospital bed capacity, and prevent viral transmission.
      The restructuring of healthcare systems, as well as the general public’s behavior and perceptions to the pandemic, has led to various observed patterns in healthcare delivery and outcomes. Hospitals globally have reported decreased emergency department (ED) and/or inpatient admissions. Cancer screening and treatment have been found to be adversely impacted with decline in diagnosis rates and treatment delays.
      • Donlon N.E.
      • Hayes C.
      • Davern M.
      • Bolger J.C.
      • Irwin S.C.
      • Butt W.T.
      • McNamara D.A.
      • Mealy K.
      Impact of COVID-19 on the diagnosis and surgical treatment of colorectal cancer: a national perspective.
      Several studies have shown that the pandemic may affect post-hospital discharge dispositions due to the limited availability of rehabilitation and skilled nursing facilities.
      • Thau L.
      • Siegal T.
      • Heslin M.E.
      • Rana A.
      • Yu S.
      • Kamen S.
      • Chen A.
      • Vigilante N.
      • Gallagher S.
      • Wegner K.
      • Thon J.M.
      • Then R.
      • Patel P.
      • Yeager T.
      • Jovin T.G.
      • Kumar R.J.
      • Owens D.E.
      • Siegler J.E.
      Decline in rehab transfers among rehab-eligible stroke patients during the COVID-19 pandemic.
      ,
      • Wexner S.D.
      • Cortés-Guiral D.
      • Gilshtein H.
      • Kent I.
      • Reymond M.A.
      COVID-19: impact on colorectal surgery.
      No studies to our knowledge thus far, however, have yet to examine colorectal surgery trends, postoperative outcomes, and post-discharge destinations at the U.S. national-level during the COVID-19 pandemic.
      Using the 2019-2020 American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP) database and its procedure-targeted colectomy and proctectomy files, we sought to elucidate the state of colorectal surgery in the U.S. during the COVID-19 pandemic, specifically in terms of surgical outcomes, discharge destination, and readmission. Understanding these outcomes will offer greater insights into areas in need of healthcare quality improvement and will equip the healthcare system with tools for future pandemic preparedness responses.

      Methods

      Data Source

      This was a retrospective analysis using the 2019–2020 ACS-NSQIP database and its colectomy and proctectomy procedure-targeted files. ACS-NSQIP is a nationally-validated, risk-adjusted, outcomes-based database developed by surgeons that collects data on patients undergoing surgery from over 700 participating member hospitals of varying size and academic affiliation. Certified surgical clinical reviewers prospectively collect data on more than 150 perioperative variables with the purpose of evaluating and improving surgical quality of care.

      American College of Surgeons. About ACS-NSQIP. Accessed March 1, 2022. https://www.facs.org/quality-programs/acs-nsqip/about

      ,

      American College of Surgeons. ACS NSQIP Participant Use Data File. Accessed March 1, 2022. https://www.facs.org/quality-programs/acs-nsqip/participant-use

      This study was reviewed and approved by the Institutional Review Board of the Johns Hopkins University School of Medicine.

      Pre-Pandemic and Pandemic Time Periods

      The COVID-19 pandemic was declared a national emergency in the U.S. on March 13, 2020. Because ACS-NSQIP records calendar year quarters instead of full dates, the quarter starting closest to March 13, 2020 was defined as the beginning of the pandemic time period in this study. As such, the pre-pandemic time period was defined from April 1, 2019 to December 31, 2019, and the pandemic time period was defined from April 1, 2020 to December 31, 2020 (quarter 2 [Q2]: April 1-June 30; Q3: July 1-September 30; Q4: October 1-December 31). Similar 9-month timeframes were selected for both pre-pandemic and pandemic periods to account for potential seasonal variation in surgical operative volume and outcomes.

      Study Population

      Patients ≥ 18 years of age who underwent colorectal surgery procedures including partial colectomy, total abdominal colectomy, abdominoperineal resection (APR), low anterior resection (LAR), total proctocolectomy, and ostomy creation/revision, as defined by the relevant Current Procedural Terminology (CPT) codes (Supplemental Table A), were included in the study. Patients were excluded if they met any of the following criteria: a) American Society of Anesthesiologists (ASA) classification V or missing classification, b) non-open, non-laparoscopic, or non-robotic cases, c) discharged against medical advice or with unknown discharge destination, d) unknown hospital LOS, and/or e) disseminated cancer diagnosis to exclude non-operable colorectal cancer cases.

      Baseline characteristics of patients

      Demographic characteristics included age (<50, 50-59, 60-69, ≥ 70), sex, and race (white, black, other, unknown). Baseline clinical characteristics included ASA classification (I-II, III, IV), dependent functional status, obesity (Body Mass Index [BMI] ≥ 30), smoking status, diabetes, hypertension, and pre-operative chronic steroid use. Additional characteristics included transfer origin (from home, nursing home or chronic care facility, outside hospital, other/unknown), emergent operation status, procedure type (partial colectomy, total abdominal colectomy, APR, LAR, total proctocolectomy), ostomy creation/revision, operative approach (robotic, laparoscopic, open planned), and surgical indication (benign neoplasm, colorectal malignancy, diverticular disease, inflammatory bowel disease [IBD], volvulus, other). Operative approach was categorized based on an intention-to-treat approach. Surgical indication was defined using the “indication for surgery” variable from the ACS-NSQIP colectomy-targeted file and the International Classification of Diseases 10th Revision codes (ICD-10) (Supplemental Table B).

      Outcomes

      The primary outcome was postoperative morbidity. Overall morbidity was defined as the occurrence of one or more of the following adverse events within 30 days postoperatively: wound infection, pneumonia, urinary tract infection (UTI), venous thromboembolism (VTE), cardiac complication, shock/sepsis, unplanned intubation, bleeding requiring transfusion, renal complication, on ventilator >48 hours, organ/space surgical site infection (SSI), and anastomotic leak. Serious morbidity was defined based on Clavien-Dindo class III-IV (cardiac or renal complications, shock/sepsis, unplanned intubation, on ventilator >48 hours, organ/space SSI, or re-operation).
      • Dindo D.
      • Demartines N.
      • Clavien P.-A.
      Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.
      Secondary outcomes included in-hospital mortality, hospital LOS, discharge destination, and 30-day postoperative readmission. LOS was defined as number of days from operation to discharge. Discharge destination was categorized into home, skilled care (skilled care facility, separate acute care, rehabilitation facility), unskilled care (unskilled facility, facility which is not home, multilevel senior community), and hospice.

      Statistical analysis

      Baseline characteristics and outcomes were compared between patients who underwent colorectal procedures pre-pandemic and during the pandemic. The pre-pandemic period was also compared to each of the three quarters during the pandemic. Pearson’s chi-squared test was used for categorical variables, and Kruskal-Wallis (or Wilcoxon rank-sum (Mann-Whitney), when appropriate) test was used for continuous variables. Multivariable logistic regression analysis was used to identify factors associated with overall morbidity, serious morbidity, and in-hospital mortality while adjusting for all baseline characteristics listed in Table 1. Hosmer-Lemeshow goodness-of-fit test was used to evaluate the models.

      Hosmer DW LS, Sturdivant RX. Applied Logistic Regression, 2nd ed. New York: Wiley, 2000.

      Statistical significance was indicated by p < 0.05. All statistical analyses were performed using Stata, version 17.0 (StataCorp, College Station, Texas, USA).
      Table 1Demographic, Clinical, and Operative Characteristics
      Characteristic, n (%)Total 62393Pre-pandemicPandemicp
      April-Dec 2019April-Dec 2020
      34810 (55.8)27583 (44.2)
      Age group, years<0.001
       <5013507 (21.7)7217 (20.7)6290 (22.8)
       50-5912914 (20.7)7240 (20.8)5674 (20.6)
       60-6915955 (25.6)8977 (25.8)6978 (25.3)
       >7020017 (32.1)11376 (32.7)8641 (31.3)
      Age, median (IQR)63 (51-72)63 (52-72)62 (51-72)<0.001
      Sex0.086
       Male30066 (48.2)16668 (47.9)13398 (48.6)
       Female32323 (51.8)18140 (52.1)14183 (51.4)
      Race<0.001
       White43569 (69.6)24872 (71.5)18697 (67.9)
       Black5560 (8.9)3085 (8.9)2475 (9.0)
       Other2529 (4.1)1308 (3.8)1221 (4.4)
       Unknown10675 (17.1)5545 (15.9)5130 (18.6)
      ASA classification<0.001
       I-II23975 (38.4)13689 (39.3)10286 (37.3)
       III32776 (52.5)18065 (51.9)14711 (53.3)
       IV5642 (9.0)3056 (8.8)2586 (9.4)
      Dependent functional status1789 (2.9)953 (2.7)836 (3.0)0.030
      Obesity21731 (35.4)12352 (36.1)9379 (34.9)0.001
      Current smoker9812 (15.7)5508 (15.8)4304 (15.6)0.455
      Diabetes9493 (15.2)5369 (15.4)4124 (15.0)0.103
      Hypertension28780 (46.1)16355 (47.0)12425 (45.1)<0.001
      Steroid use6548 (10.5)3480 (10.0)3068 (11.1)<0.001
      Transfer status0.004
       Home58039 (93.0)32475 (93.3)25564 (84.8)
       Nursing home/chronic care facility602 (1.0)346 (1.0)256 (0.9)
       Outside hospital3348 (5.4)1773 (5.1)1575 (5.7)
       Other/unknown404 (0.7)216 (0.6)188 (0.7)
      Emergent case8624 (13.8)4437 (12.7)4187 (15.2)<0.001
      Procedure type0.001
       Partial colectomy54453 (87.3)30481 (87.6)23972 (86.9)
       Total colectomy2959 (4.7)1588 (4.6)1371 (5.0)
       APR2693 (4.3)1436 (4.1)1257 (4.6)
       LAR1136 (1.8)671 (1.9)465 (1.7)
       Total proctocolectomy1152 (1.9)634 (1.8)518 (1.9)
      Ostomy creation/revision2325 (3.7)1303 (3.7)1022 (3.7)0.803
      Operative approach<0.001
       Robotic9941 (15.9)5469 (15.7)4472 (16.2)
       Laparoscopic32878 (52.7)18804 (54.0)14074 (51.0)
       Open planned19574 (31.4)10537 (30.3)9037 (32.8)
      Indication<0.001
       Benign neoplasm4117(6.6)2549 (7.3)1568 (5.7)
       Colorectal malignancy25638 (41.1)14281 (41.0)11357 (41.2)
       Diverticular disease14807 (23.7)8417 (24.2)6390 (23.2)
       IBD6907 (11.1)3684 (10.6)3223 (11.7)
       Volvulus1885 (3.0)1011 (2.9)874 (3.2)
       Other9039 (14.5)4868 (14.0)4171 (15.1)
      Abbreviations: IQR, Interquartile range; ASA, American Society of Anesthesiologists; APR, Abdominoperineal resection; LAR, Low anterior resection; IBD, Inflammatory bowel disease

      Results

      Study population

      A total of 96,658 patients who underwent colorectal surgery during the study period were identified in ACS-NSQIP. After applying our exclusion criteria, 62,393 patients were included in our study, with 34,810 colorectal surgery patients (55.8%) in the pre-pandemic time period, and 27,583 patients (44.2%) in the pandemic time period. Among patients who had surgery during the pandemic, 7992 patients (29.0%) were operated on in Q2 2020, 10,096 patients (36.6%) in Q3 2020, and 9495 patients (34.4%) in Q4 2020. 12.7% of cases (n=4437) pre-pandemic were emergent compared to 15.2% (n=4187) during the pandemic (p<0.001). Comparisons between pre-pandemic and pandemic time periods for each corresponding quarter demonstrated an increased proportion of emergent cases during the pandemic. This trend was most pronounced when comparing cases performed from Q2 April to June, with the largest decrease in proportion of cases performed electively during the pandemic compared to the pre-pandemic period (pre-pandemic 87.4% vs. pandemic 82.9%, p<0.001) and the largest increase in proportion of cases performed emergently (pre-pandemic 12.6% vs. pandemic 17.1%, p<0.001). Although subsequent quarters continued to show statistically significant decreased proportion of elective cases (Q3: 87.0% vs. 85.7%, p=0.005; Q4: 87.4% vs. 85.5%, p<0.001) and increased proportion of emergent cases (Q3: 13.0% vs. 14.3%, p<0.001; Q4: 12.6% vs. 14.5%, p<0.001), these trends were less pronounced (Figure 1).
      Figure thumbnail gr1
      Figure 1Proportion of elective and emergency colorectal surgery cases before and during the COVID-19 pandemic.
      Compared to patients who underwent colorectal surgery pre-pandemic, patients who underwent surgery during the pandemic tended to be slightly younger (median age pre-pandemic 63 years vs. pandemic 62 years, p<0.001), have higher ASA class (III/IV), were more frequently diagnosed with dependent functional status (2.7% vs. 3.0%, p=0.030), and less frequently diagnosed with obesity (36.1% vs. 34.9%, p=0.001) or hypertension (47.0% vs. 45.1%, p<0.001) (Table 1). Patients during the pandemic presented from home less frequently (93.3% vs. 84.8%, p=0.003) and were transferred from outside hospitals more frequently (5.1% vs. 5.7%, p=0.001).
      Regarding operative characteristics, the proportion of laparoscopic surgeries during the pandemic decreased (54.0% vs. 51.0%, p<0.001) and the proportion of planned open surgeries slightly increased (30.3% vs. 32.8%, p<0.001). Although the proportion of colorectal malignancy as a surgical indication did not change from pre-pandemic to pandemic (41.0% vs. 41.2%, p=0.762), surgical indications for volvulus (2.9% vs. 3.2%, p<0.001) and IBD (10.6% vs. 11.7%, p<0.001) increased. Conversely, surgical indications for benign neoplasms (7.3% vs. 5.7%, p<0.001) and diverticular disease (24.2% vs. 23.2%, p=0.003) decreased. The frequency of various colorectal procedure types were comparable pre-pandemic and during the pandemic, including for ostomy creation/revision (3.7% vs. 3.7%, p=0.803).

      Unadjusted outcomes

      On unadjusted analysis, patients who underwent surgery during the pandemic had higher rates of overall morbidity (pre-pandemic=24.0% vs. pandemic 27.0%, 26.2%, 25.7% for Q2/Q3/Q4 2020, respectively, p<0.001) and serious morbidity (pre-pandemic=14.6% vs. pandemic 16.5%, 15.5%, 15.9%, p<0.001) (Table 2). In particular, significantly higher rates of shock/sepsis (pre-pandemic=7.6% vs. pandemic 9.0%, 8.5%, 8.3%, p<0.001) and bleeding requiring transfusion (pre-pandemic=8.6% vs. 10.2%, 9.5%, 9.5%, p<0.001) were observed across all pandemic quarters compared to pre-pandemic. Significantly higher rates of pneumonia (pre-pandemic=2.0% vs. Q2 2020=2.6%, p=0.002; pre-pandemic=2.0% vs. Q4 2020=3.0%, p<0.001) and organ SSI (pre-pandemic=5.6% vs. Q2 2020=6.9%, p<0.001; pre-pandemic=5.6% vs. Q4 2020=6.6%, p<0.001) were observed in Q2 and Q4 2020. Anastomotic leak rates also increased significantly in Q2 2020 (pre-pandemic=2.4% vs. Q2 2020=3.0%, p=0.007) but had similar rates during the remainder of the observed pandemic timeframe. In-hospital mortality and 30-day mortality rates increased during the pandemic and were also statistically significant in Q2 and Q4 of the 2020 pandemic (in-hospital mortality: pre-pandemic=1.7% vs. Q2 2020=2.1%, p=0.004; pre-pandemic=1.7% vs. Q4 2020=2.1%, p=0.005; 30-day mortality: pre-pandemic=2.3% vs. Q2 2020=2.7%, p=0.012; pre-pandemic=2.3% vs. Q4 2020=2.6%, p=0.041). Hospital LOS, however, was not clinically significantly different during the pandemic compared to pre-pandemic.
      Table 230-Day Outcomes Stratified by Pandemic and Pre-Pandemic Quarters
      Outcome (%)Pre-pandemic April-Dec 2019Pandemic Q2 April-June 2020Pandemic Q3 July-Sep 2020Pandemic Q4 Oct-Dec 2020p
      34810 (55.8)7992 (12.8)10096 (16.2)9495 (15.2)
      Discharge destination
      Discharge Destination: n=61263 patients; Pre-pandemic: n=34232, Pandemic: n=27031
      <0.001
       Home31108 (90.9)7245 (92.6)
      Indicates statistical significance (reference = pre-pandemic group)
      9180 (92.6)
      Indicates statistical significance (reference = pre-pandemic group)
      8658 (93.1)
      Indicates statistical significance (reference = pre-pandemic group)
       Skilled Care2980 (8.7)531 (6.8)
      Indicates statistical significance (reference = pre-pandemic group)
      687 (6.9)
      Indicates statistical significance (reference = pre-pandemic group)
      588 (6.3)
      Indicates statistical significance (reference = pre-pandemic group)
       Unskilled Care39 (0.1)12 (0.2)7 (0.1)13 (0.1)
       Hospice105 (0.3)34 (0.4)38 (0.4)38 (0.4)
      Overall morbidity
      Overall morbidity: Wound infection, pneumonia, UTI, VTE, cardiac complication, shock/sepsis, unplanned intubation, bleeding transfusion, renal complication, on ventilator >48 hours, organ/space SSI, and anastomotic leak.
      8338 (24.0)2160 (27.0)
      Indicates statistical significance (reference = pre-pandemic group)
      2646 (26.2)
      Indicates statistical significance (reference = pre-pandemic group)
      2441 (25.7)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
      Serious morbidity
      Serious morbidity: Clavien-Dindo III-IV (cardiac complication, shock/sepsis, unplanned intubation, renal complication, on ventilator >48 hours, organ/space SSI, and reoperation)
      5076 (14.6)1316 (16.5)
      Indicates statistical significance (reference = pre-pandemic group)
      1569 (15.5)
      Indicates statistical significance (reference = pre-pandemic group)
      1510 (15.9)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
       Wound infection1731 (5.0)384 (4.8)504 (5.0)439 (4.6)0.514
       Pneumonia700 (2.0)204 (2.6)
      Indicates statistical significance (reference = pre-pandemic group)
      233 (2.3)282 (3.0)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
       UTI667 (1.9)147 (1.8)200 (2.0)184 (1.9)0.920
       VTE599 (1.7)146 (1.8)210 (2.1)
      Indicates statistical significance (reference = pre-pandemic group)
      156 (1.6)0.071
       Cardiac431 (1.2)111 (1.4)153 (1.5)
      Indicates statistical significance (reference = pre-pandemic group)
      122 (1.3)0.163
       Shock/sepsis2641 (7.6)718 (9.0)
      Indicates statistical significance (reference = pre-pandemic group)
      862 (8.5)
      Indicates statistical significance (reference = pre-pandemic group)
      783 (8.3)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
       Intubation455 (1.3)109 (1.4)132 (1.3)136 (1.4)0.802
       Bleeding requiring transfusion2986 (8.6)812 (10.2)
      Indicates statistical significance (reference = pre-pandemic group)
      956 (9.5)
      Indicates statistical significance (reference = pre-pandemic group)
      898 (9.5)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
       Renal complication465 (1.3)118 (1.5)120 (1.2)141 (1.5)0.233
       On ventilator >48 hrs761 (2.2)200 (2.5)222 (2.2)230 (2.4)0.233
      Organ/space SSI1944 (5.6)550 (6.9)
      Indicates statistical significance (reference = pre-pandemic group)
      595 (5.9)627 (6.6)
      Indicates statistical significance (reference = pre-pandemic group)
      <0.001
       Anastomotic leak846 (2.4)236 (3.0)
      Indicates statistical significance (reference = pre-pandemic group)
      258 (2.6)248 (2.6)0.061
      In-hospital mortality578 (1.7)170 (2.1)
      Indicates statistical significance (reference = pre-pandemic group)
      184 (1.8)198 (2.1)
      Indicates statistical significance (reference = pre-pandemic group)
      0.005
      30-day Mortality785 (2.3)218 (2.7)
      Indicates statistical significance (reference = pre-pandemic group)
      238 (2.4)248 (2.6)
      Indicates statistical significance (reference = pre-pandemic group)
      0.034
      LOS (days), median (IQR)4 (3-7)5 (3-7)4 (3-7)4 (3-7)<0.001
      Readmission3636 (10.5)823 (10.3)1081 (10.7)897 (9.5)
      Indicates statistical significance (reference = pre-pandemic group)
      0.018
      Abbreviations: UTI, urinary tract infection; VTE, venous thromboembolism; SSI, surgical site infection; LOS, Length of hospital stay; IQR, Interquartile range
      Indicates statistical significance (reference = pre-pandemic group)
      a Discharge Destination: n=61263 patients; Pre-pandemic: n=34232, Pandemic: n=27031
      b Overall morbidity: Wound infection, pneumonia, UTI, VTE, cardiac complication, shock/sepsis, unplanned intubation, bleeding transfusion, renal complication, on ventilator >48 hours, organ/space SSI, and anastomotic leak.
      c Serious morbidity: Clavien-Dindo III-IV (cardiac complication, shock/sepsis, unplanned intubation, renal complication, on ventilator >48 hours, organ/space SSI, and reoperation)
      Patients who underwent colorectal surgery during the pandemic had a higher proportion of discharge to home (pre-pandemic=90.9% vs. pandemic=92.6%, 92.6%, 93.1%, p<0.001) and lower proportion of discharge to skilled care facilities (pre-pandemic=8.7% vs. pandemic=6.8%, 6.9%, 6.3%, p<0.001). The median age of patients discharged to home before and during the pandemic was the same at 61 years (IQR 50-71 years). Although 30-day postoperative readmission rates were similar to pre-pandemic readmission rates for the first two quarters of the pandemic, there was a significantly decreased readmission rate for Q4 2020 (pre-pandemic=10.4% vs 9.4%, p=0.018).

      Factors associated with 30-day overall morbidity, serious morbidity, and in-hospital mortality

      Multivariable logistic regression analysis demonstrated that Q3 and Q4 of the 2020 pandemic were associated with increased odds of overall morbidity (OR: 1.11, 95% CI: [1.05-1.17], p<0.001, OR:1.08, 95% CI: [1.02-1.14], p=0.009), whereas Q2 of the 2020 pandemic did not have increased odds of overall morbidity (OR: 1.06, 95% CI: [0.99-1.12], p=0.079) (Table 3). Factors associated with at least a two-fold increased odds of overall morbidity were: ASA class IV, having an emergent case, having an open surgery, and having diverticular disease as the surgical indication. Other factors that significantly impacted overall morbidity (but less than two-fold) included: older age, black race, ASA class III, dependent functional status, obesity, current smoking history, diabetes, hypertension, steroid use, transfer from a nursing home or outside hospital, patients who underwent total colectomy, APR, total proctocolectomy, or ostomy creation/revision, and who had colorectal malignancy or IBD (Table 3). Patients who underwent robotic procedures had decreased odds of overall morbidity (OR: 0.91, 95% CI: [0.86-0.98], p=0.007) when compared to patients who underwent laparoscopic procedures.
      Table 3Multivariable Logistic Regression Analysis: Factors Associated with Overall Morbidity, Serious Morbidity, and In-Hospital Mortality
      Overall MorbiditySerious MorbidityIn-Hospital Mortality
      OR (95% CI)pOR (95% CI)pOR (95% CI)p
      Pandemic Timeline
       Pre-Pandemic (April-Dec 2019)ReferenceReferenceReference
       Pandemic (Q2 April-June 2020)1.06 (0.99-1.12)0.0791.03 (0.95-1.11)0.4941.09 (0.89-1.33)0.385
       Pandemic (Q3 July-Sept 2020)1.11 (1.05-1.17)<0.0011.04 (0.97-1.12)0.2400.98 (0.81-1.19)0.843
       Pandemic (Q4 Oct-Dec 2020)1.08 (1.02-1.14)0.0091.10 (1.03-1.18)0.0061.28 (1.06-1.54)0.010
      Age group, years
       <50ReferenceReferenceReference
       50-590.97 (0.91-1.04)0.4240.91 (0.84-0.98)0.0181.62 (1.13-2.32)0.009
       60-691.09 (1.02-1.16)0.0091.04 (0.96-1.13)0.3022.56 (1.85-3.55)<0.001
       >701.24 (1.16-1.33)<0.0011.10 (1.01-1.19)0.0214.54 (3.29-6.25)<0.001
      Sex
       MaleReferenceReferenceReference
       Female0.99 (0.95-1.03)0.4980.81 (0.77-0.85)<0.0010.79 (0.69-0.91)0.001
      Race
       WhiteReferenceReferenceReference
       Black1.20 (1.12-1.29)<0.0011.21 (1.12-1.32)<0.0011.05 (0.84-1.32)0.643
       Other1.09 (0.98-1.22)0.1000.82 (0.71-0.94)0.0060.84 (0.54-1.31)0.444
       Unknown1.00 (0.94-1.06)0.9670.78 (0.73-0.84)<0.0010.77 (0.63-0.95)0.016
      ASA classification
       I-IIReferenceReferenceReference
       III1.49 (1.42-1.56)<0.0011.47 (1.39-1.56)<0.0014.47 (3.06-6.54)<0.001
       IV3.03 (2.80-3.27)<0.0012.99 (2.74-3.27)<0.00116.00 (10.86-23.56)<0.001
      Dependent functional status1.61 (1.43-1.81)<0.0011.35 (1.19-1.53)<0.0011.51 (1.22-1.88)<0.001
      Obesity1.07 (1.03-1.12)0.0021.08 (1.02-1.14)0.0051.22 (1.05-1.41)0.008
      Current smoker1.22 (1.16-1.29)<0.0011.35 (1.26-1.43)<0.0011.27 (1.06-1.52)0.008
      Diabetes1.12 (1.06-1.19)<0.0011.06 (0.99-1.14)0.0901.06 (0.90-1.25)0.484
      Hypertension1.10 (1.05-1.16)<0.0011.05 (0.99-1.11)0.1161.06 (0.91-1.24)0.457
      Steroid use1.26 (1.17-1.35)<0.0011.14 (1.05-1.24)0.0021.36 (1.10-1.68)0.004
      Transfer status
       HomeReferenceReferenceReference
       Nursing home/chronic care facility1.40 (1.15-1.72)0.0011.29 (1.04-1.60)0.0211.81 (1.30-2.51)<0.001
       Outside hospital1.45 (1.33-1.57)<0.0011.35 (1.24-1.48)<0.0011.48 (1.25-1.77)<0.001
       Other/unknown1.13 (0.90-1.42)0.2951.05 (0.81-1.35)0.7261.78 (1.15-2.77)0.010
       Emergent case2.18 (2.05-2.32)<0.0012.85 (2.67-3.05)<0.0013.28 (2.77-3.89)<0.001
      Procedure type
       Partial colectomyReferenceReferenceReference
       Total colectomy1.80 (1.64-1.97)<0.0011.63 (1.47-1.81)<0.0011.87 (1.50-2.34)<0.001
       APR1.74 (1.59-1.91)<0.0011.48 (1.32-1.67)<0.0010.53 (0.78-1.00)0.049
       LAR1.11 (0.96-1.28)0.1720.94 (0.77-1.14)0.5110.25 (0.06-1.01)0.052
       Total proctocolectomy2.13 (1.85-2.44)<0.0011.72 (1.45-2.04)<0.0010.92 (0.44-1.89)0.817
      Ostomy creation/revision1.39 (1.26-1.53)<0.0011.36 (1.21-1.51)<0.0011.09 (0.81-1.48)0.585
      Operative approach
       LaparoscopicReferenceReferenceReference
       Robotic0.91 (0.86-0.98)0.0071.12 (1.03-1.21)0.0051.04 (0.70-1.53)0.859
       Open planned2.13 (2.04-2.24)<0.0011.97 (1.86-2.09)<0.0013.01 (2.46-3.68)<0.001
      Indication
       Benign neoplasmReferenceReferenceReference
       Malignancy1.47 (1.32-1.63)<0.0011.34 (1.16-1.54)<0.0011.23 (0.72-2.10)0.441
       Diverticular disease2.01 (1.80-2.24)<0.0012.48 (2.15-2.87)<0.0010.94 (0.54-1.64)0.836
       IBD1.79 (1.58-2.03)<0.0011.90 (1.61-2.24)<0.0011.15 (0.61-2.15)0.668
       Volvulus1.02 (0.87-1.19)0.8151.20 (0.99-1.45)0.0661.17 (0.64-2.11)0.614
       Other2.24 (2.00-2.51)<0.0012.62 (2.26-3.04)<0.0012.43 (1.42-4.17)0.001
      Abbreviations: IQR, Interquartile range; ASA, American Society of Anesthesiologists; APR, Abdominoperineal resection; LAR, Low anterior resection; IBD, Inflammatory bowel disease
      With regards to serious morbidity, there were no significant differences between the pre-pandemic period and the first two quarters of the 2020 pandemic. However, the latter time period from Q4 2020 was associated with increased odds of serious morbidity (OR: 1.10, 95% CI: [1.03-1.18), p=0.006) (Table 3). Factors associated with increased odds of serious morbidity were similar to those for overall morbidity. Younger and female patients were associated with decreased odds of serious morbidity.
      In terms of in-hospital mortality, no significant differences were observed between the pre-pandemic period and the first two quarters of the pandemic. As with overall and serious morbidity, however, Q4 2020 was associated with increased odds of in-hospital mortality (OR: 1.28, 95% CI: [1.06-1.54], p=0.010) (Table 3). Factors associated with at least a two-fold increased odds of in-hospital mortality were: ASA class IV (OR: 16.00, 95% CI: [10.86-23.56], p<0.001), ASA class III (OR: 4.47, 95% CI: [3.06-6.54], p<0.001), age > 70 (OR: 4.54, 95% CI: [3.29-6.25], p<0.001), having an emergent case (OR: 3.28, 95% CI: [2.77-3.89], p<0.001), having an open surgery (OR: 3.01, 95% CI: [2.46-3.68], p<0.001), and age 60-69 (OR: 2.56, 95% CI: [1.85-3.55), p<0.001). Female patients had decreased odds of in-hospital mortality (OR: 0.79, 95% CI: [0.69-0.91], p=0.001).

      Discussion

      The COVID-19 pandemic has had a profound impact on healthcare delivery worldwide. This study is the first to our knowledge to use ACS-NSQIP to examine U.S. colorectal surgery outcomes, discharge destination, and readmission during the COVID-19 pandemic. The ACS-NSQIP offers a unique opportunity to assess not only postoperative complications but also discharge disposition and other healthcare quality measures at a national level. From our retrospective analysis, we found that patients presented to the hospital with higher ASA classification during the pandemic and that the proportion of emergent cases increased. We identified that patients undergoing colorectal surgery had higher rates of overall and serious morbidity. Moreover, the proportion of patients discharged home increased, whereas the proportion of patients discharged particularly to skilled nursing facilities decreased. Latter months of the observed pandemic timeframe also showed increased odds of in-hospital mortality. These findings highlight the multi-faceted differences that were observed across the healthcare delivery process—from initial hospital presentation to inpatient care and final discharge disposition—during the COVID-19 pandemic.
      Our findings demonstrate a decrease in the total number of colorectal procedures performed during the pandemic, with the greatest decrease occurring from April-June 2020, coinciding with the start of the pandemic. Similar trends showing the greatest decrease in surgical volume in the early months of the pandemic with gradual resumption of surgical operations over the following months have been observed for colorectal procedures performed in England,
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      Impact of the COVID-19 pandemic on emergency adult surgical patients and surgical services: an international multi-center cohort study and department survey.
      Given these findings, it is likely that the poorer morbidity and mortality outcomes observed in our study are due to a combination of patient and hospital-related factors. Factors associated with increased odds of overall and serious morbidity and in-hospital mortality include higher ASA classification, emergent cases, and having comorbidities. That patients who underwent colorectal surgery during the pandemic tended to have these baseline characteristics could potentially contribute to poorer postoperative outcomes. However, the resource strain on hospitals during the pandemic is another notable factor, as evidenced by the significant odds of morbidity and in-hospital mortality in October to December 2020. In the U.S., these specific three months coincided with the largest rise in COVID-19 cases, deaths, and hospitalizations for the observed 2020 pandemic year (Figure 2). Hospitals may have felt a greater demand on their resources including issues with bed capacity and staffing to treat COVID-19 patients during this time, leading to the diversion of resources from non-COVID specialties and healthcare services. The issue of nursing staffing shortages has become a national crisis during the pandemic, with hospitals needing to hire travel nurses to replace the long-term floor and/or operating room nurses leaving their jobs. Such staff turnover may have increased postoperative morbidity due to suboptimal nurse-to-patient ratios and unfamiliarity with institution-specific colorectal surgery inpatient protocols.
      Figure thumbnail gr2
      Figure 2Rates of COVID-19 cases, deaths, and hospitalizations in the United States. Data Sources: Cases and deaths data from the Johns Hopkins University Center for Systems Science and Engineering (JHU CCSE), hospitalization data from the U.S. Department of Health and Human Services; https://coronavirus.jhu.edu/region/united-states. Gray, dashed lines delineate the date when the U.S. declared COVID-19 a pandemic (March 13, 2020), as well as the date cutoffs for each quarterly time period as defined by ACS-NSQIP (Q2 April 1-June 30; Q3 July 1-September 30; Q4 October 1-December 31).
      Despite colorectal surgery patients having higher morbidity rates during the pandemic, hospital LOS was clinically comparable to LOS pre-pandemic. This was similarly observed at an Italian hospital for patients undergoing colorectal cancer resection during the first pandemic wave.
      • Allaix M.E.
      • Lo Secco G.
      • Velluti F.
      • De Paolis P.
      • Arolfo S.
      • Morino M.
      Colorectal surgery during the COVID-19 outbreak: do we need to change?.
      Other studies, however, have reported decreased LOS during the pandemic for blunt trauma patients,
      • Yeates E.O.
      • Grigorian A.
      • Schellenberg M.
      • Owattanapanich N.
      • Barmparas G.
      • Margulies D.
      • Juillard C.
      • Garber K.
      • Cryer H.
      • Tilou A.
      • Burruss S.
      • Penaloza-Villalobos L.
      • Lin A.
      • Figueras R.A.
      • Coimbra R.
      • Brenner M.
      • Costantini T.
      • Santorelli J.
      • Curry T.
      • Wintz D.
      • Biffl W.
      • Schaffer K.B.
      • Duncan T.K.
      • Barbaro C.
      • Diaz G.
      • Johnson A.
      • Chinn J.
      • Naaseh A.
      • Leung A.
      • Grabar C.
      • Nahmias J.
      Decreased hospital length of stay and intensive care unit admissions for non-COVID blunt trauma patients during the COVID-19 pandemic.
      thoracolumbar adult spinal deformity surgical patients,
      • Wang K.Y.
      • McNeely E.L.
      • Dhanjani S.A.
      • Raad M.
      • Puvanesarajah V.
      • Neuman B.J.
      • Cohen D.
      • Khanna A.J.
      • Kebaish F.
      • Hassanzadeh H.
      • Kebaish K.M.
      COVID-19 significantly impacted hospital length of stay and discharge patterns for adult spinal deformity patients.
      and hip fracture surgical patients.
      • Shemesh S.
      • Bebin A.
      • Niego N.
      • Frenkel Rutenberg T.
      The impact of the COVID-19 2020 pandemic on hospital length of stay following fragility hip fracture surgery.
      Such variations in LOS may be due to the competing demands of hospitals to discharge patients as soon as possible to reduce viral transmission and maintain bed capacity while ensuring that patients meet benchmarks for safe hospital discharge, as well as patients’ preferences to be discharged sooner at a time when many hospitals had implemented visitor restrictions. In the case of colorectal surgery patients, these benchmarks for discharge may include achieving adequate pain control, return of bowel function, ability to tolerate oral intake, and appropriate ambulation. Because these are patient-dependent factors, the pandemic may have had less of an effect on LOS for colorectal patients. 30-day postoperative readmission was also largely unchanged for colorectal patients during the pandemic, except when readmission rates decreased during the last three months of 2020 when COVID-19 cases and hospitalizations were highest and may have deterred patients from coming into hospitals. Other studies have also demonstrated no significant increase in hospital readmission rates during the pandemic, suggesting that hospitals were able to maintain safe discharge criteria.
      • Wang K.Y.
      • McNeely E.L.
      • Dhanjani S.A.
      • Raad M.
      • Puvanesarajah V.
      • Neuman B.J.
      • Cohen D.
      • Khanna A.J.
      • Kebaish F.
      • Hassanzadeh H.
      • Kebaish K.M.
      COVID-19 significantly impacted hospital length of stay and discharge patterns for adult spinal deformity patients.
      ,
      • Shao C.C.
      • McLeod M.C.
      • Gleason L.
      • Marques I.
      • Chu D.I.
      • Gunnells D.
      Effect of COVID-19 pandemic restructuring on surgical volume and outcomes of non-COVID patients undergoing surgery.
      Moreover, it is possible that patients who were discharged to home received more support from family members and/or caregivers who may have been present at home during the early lockdown periods of pandemic.
      Although various inpatient outcomes during the pandemic have been assessed in several studies, fewer studies have investigated its effect on discharge disposition and coordination. Our study shows that patients who underwent colorectal surgery during the pandemic had higher proportion of discharge to home and lower proportion of discharge to skilled care facilities including separate acute care and rehabilitation facilities. Similar trends have also been observed in other patient populations such as orthopedic surgery spine patients and stroke patients.
      • Thau L.
      • Siegal T.
      • Heslin M.E.
      • Rana A.
      • Yu S.
      • Kamen S.
      • Chen A.
      • Vigilante N.
      • Gallagher S.
      • Wegner K.
      • Thon J.M.
      • Then R.
      • Patel P.
      • Yeager T.
      • Jovin T.G.
      • Kumar R.J.
      • Owens D.E.
      • Siegler J.E.
      Decline in rehab transfers among rehab-eligible stroke patients during the COVID-19 pandemic.
      ,
      • Wang K.Y.
      • McNeely E.L.
      • Dhanjani S.A.
      • Raad M.
      • Puvanesarajah V.
      • Neuman B.J.
      • Cohen D.
      • Khanna A.J.
      • Kebaish F.
      • Hassanzadeh H.
      • Kebaish K.M.
      COVID-19 significantly impacted hospital length of stay and discharge patterns for adult spinal deformity patients.
      One study found that among rehabilitation-eligible stroke survivors, there was decreased odds of discharge to rehabilitation facilities during the pandemic.
      • Thau L.
      • Siegal T.
      • Heslin M.E.
      • Rana A.
      • Yu S.
      • Kamen S.
      • Chen A.
      • Vigilante N.
      • Gallagher S.
      • Wegner K.
      • Thon J.M.
      • Then R.
      • Patel P.
      • Yeager T.
      • Jovin T.G.
      • Kumar R.J.
      • Owens D.E.
      • Siegler J.E.
      Decline in rehab transfers among rehab-eligible stroke patients during the COVID-19 pandemic.
      As the pandemic surged, skilled care and rehabilitation centers across the country were met with increased capacity demands to accommodate the rapid influx of COVID-19 patients with skilled care needs.
      • Khan F.
      • Amatya B.
      Medical rehabilitation in pandemics: towards a new perspective.
      ,
      • Levin S.R.
      • Gitkind A.I.
      • Bartels M.N.
      Effect of the COVID-19 pandemic on postacute care decision making.
      From a study using U.S. national insurance claims data of patients ≥ 65 years, discharges to skilled nursing facilities declined from 19% in 2019 to 14% by October 2020, and spending towards skilled nursing facilities declined by half.
      • Werner R.M.
      • Bressman E.
      Trends in post-acute care utilization during the COVID-19 pandemic.
      Possible explanations include patient, family, caregiver, and provider preferences for home post-discharge care, as well as bed scarcity and staffing shortages in skilled care facilities. Despite an increased proportion of discharges to home rather than to other facilities, the readmission rates of colorectal patients did not increase significantly during the pandemic, an observation that may be multifactorial due to patient motivation and having adequate caregiver support, home care nursing, or follow-up. More granular studies are warranted to investigate these trends in discharge coordination and may generate dialogue on re-examining patient selection criteria to discharge facilities, especially during times of limited resources. Nevertheless, the shift in discharge disposition and post-acute care utilization highlights the widespread impact of the pandemic on all levels of patient care, including ancillary healthcare services.
      Although the ACS-NSQIP is a national, standardized, multi-institutional database with a primary focus of measuring surgical quality of care, limitations inherent to the database exist. Firstly, the ACS-NSQIP database includes data collected from largely academic centers. Therefore, this database may not capture as much data from community hospitals that could potentially encounter more significant healthcare strains during the pandemic. The results from our study, therefore, may serve as a conservative assessment of the impact the pandemic has had in typically more well-resourced hospitals. Because ACS-NSQIP does not identify the geographic location and distribution of hospitals, an assessment of geographic variations as waves of the pandemic spread across the U.S. at different timepoints cannot be determined. Moreover, ACS-NSQIP does not record the exact date of surgery but only the quarter of the year in which the surgery was performed; as such, creating precise cutoffs based on pandemic peaks and/or COVID-19 variants cannot be performed. However, it is worth noting that in our study, each wave of the pandemic in 2020 was captured by a different NSQIP quarter, thereby allowing for some indirect comparisons (Figure 2). Because the latest ACS-NSQIP data is only available through December 2020, the latter impact of the pandemic in 2021 and its associated variants cannot be assessed until more data is publicly available.
      Finally, COVID-19 status in patients undergoing surgery during the pandemic were unable to be identified due to ICD-coding inconsistencies. It is possible that some of the increased morbidity observed in colorectal patients during the pandemic may be attributed to patients having a concomitant diagnosis of COVID-19. Given the implementation of pre-operative COVID-19 testing for elective cases in many U.S. hospitals, however, it is likely that these patients comprise a smaller subpopulation than COVID-negative colorectal surgery patients. Indeed, numerous studies have supported the impact of the pandemic and the burdens placed on the entire healthcare system for all patients. Future studies accounting for U.S. geographic variations in the timing of pandemic waves and responses should be explored. Nevertheless, the strengths of our study include using a national, standardized database to investigate specific surgical outcomes measures, allowing for a robust sample size. As prior studies have been predominantly single-institution or international studies, this is the first study to assess colorectal surgery outcomes nationally in the U.S. during the pandemic.
      The COVID-19 pandemic is a global crisis that has disrupted every aspect of society. Our study demonstrates that during the COVID-19 pandemic in the U.S, overall colorectal surgery case volume decreased; additionally, a larger proportion of emergent cases, higher rates of postoperative overall and serious morbidity, and increased proportion of discharges to home were observed. As healthcare systems continue to face the challenges of this pandemic, emphasis must be placed on balancing resource allocation, educating patients and providers to continue timely medical workup and management when presented with concerning health symptoms, and optimizing discharge coordination and post-acute care planning pathways. Through lessons learned from this pandemic, healthcare systems can become better equipped at effectively anticipating, mobilizing, and utilizing resources for future pandemic preparedness responses without compromising quality of care.

      Conflicts of Interest

      None

      Grant Support and Other Assistance

      Sophia Y. Chen and Shannon R. Radomski received financial support from National Cancer Institute (NCI) Grant 5T32CA126607-12. Mr. Edwin Lewis provided generous support of Dr. Efron's Department of Surgery Research Fund. Mr. Peter T. Nicholl provided generous support of Dr. Safar’s Department of Surgery Research Fund.

      Co-author Contributions

      Study design: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., B.S. Data acquisition and analysis: S.Y.C., S.N.R., M.S., A.P. Interpretation of data: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., B.S. Drafting work: S.Y.C., S.N.R., M.S., A.P. Critical revision: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., B.S. Final approval/accountability: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., B.S.

      Acknowledgements

      Sophia Y. Chen and Shannon R. Radomski received financial support from National Cancer Institute (NCI) Grant 5T32CA126607-12.
      Mr. Edwin Lewis provided generous support of Dr. Efron's Department of Surgery Research Fund. Mr. Peter T. Nicholl provided generous support of Dr. Safar’s Department of Surgery Research Fund.
      The authors would like to acknowledge the role of the Johns Hopkins Surgery Center for Outcomes Research (JSCOR) for supporting this study.

      Supplementary data

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