Abstract
Introduction
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 prepandemic time period was defined from April 1, 2019 to December 31, 2019. The pandemic time period was defined from April 1, 2020 to 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 prepandemic 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% prepandemic versus 15.2% pandemic, P < 0.001), with less laparoscopic cases (54.0% versus 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 and 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: Colorectal surgery, COVID-19, Discharge destination, Hospital length of stay, Morbidity, Skilled care facilities
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 more than 212 countries and territories, with more than 644 million cases and 6.6 million deaths.1 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.2 Surgical societies including the American College of Surgeons (ACS),3 the Society of Surgical Oncology,4 and the Society of American Gastrointestinal and Endoscopic Surgeons5 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 nondeferrable oncological cases to limit resource utilization, preserve adequate hospital bed capacity, and prevent viral transmission.
The restructuring of healthcare systems, and 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 and/or inpatient admissions. Cancer screening and treatment have been found to be adversely impacted with decline in diagnosis rates and treatment delays.6 Several studies have shown that the pandemic may affect posthospital discharge dispositions due to the limited availability of rehabilitation and skilled nursing facilities.7 , 8 No studies to our knowledge thus far, however, are yet to examine colorectal surgery trends, postoperative outcomes, and postdischarge 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 United States 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 more than 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.9 , 10 This study was reviewed and approved by the Institutional Review Board of the Johns Hopkins University School of Medicine.
Prepandemic and pandemic time periods
The COVID-19 pandemic was declared a national emergency in the United States 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 prepandemic 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 nine-month timeframes were selected for both prepandemic and pandemic periods to account for potential seasonal variation in surgical operative volume and outcomes.
Study population
Patients aged ≥ 18 y who underwent colorectal surgery procedures including partial colectomy, total abdominal colectomy, abdominoperineal resection (APR), low anterior resection, total proctocolectomy, and ostomy creation/revision, as defined by the relevant Current Procedural Terminology codes (Supplemental Table A), were included in the study. Patients were excluded if they met any of the following criteria: (1) American Society of Anesthesiologists (ASA) classification V or missing classification; (2) nonopen, nonlaparoscopic, or nonrobotic cases; (3) discharged against medical advice or with unknown discharge destination; (4) unknown hospital length of stay (LOS); and/or (5) disseminated cancer diagnosis to exclude nonoperable 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 ≥ 30), smoking status, diabetes, hypertension, and preoperative 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, low anterior resection, 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 Tenth Revision codes (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 d postoperatively: wound infection, pneumonia, urinary tract infection, venous thromboembolism, cardiac complication, shock/sepsis, unplanned intubation, bleeding requiring transfusion, renal complication, on ventilator > 48 h, 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 h, organ/space SSI, or reoperation).11
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 prepandemic and during the pandemic. The prepandemic 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.12 Statistical significance was indicated by P < 0.05. All statistical analyses were performed using Stata, version 17.0 (StataCorp, College Station, Texas).
Table 1.
Demographic, clinical, and operative characteristics.
| Characteristic, n (%) | Total 62,393 | Prepandemic |
Pandemic |
P value |
|---|---|---|---|---|
| April-December 2019 |
April-December 2020 |
|||
| 34,810 (55.8) | 27,583 (44.2) | |||
| Age group, years | <0.001 | |||
| <50 | 13,507 (21.7) | 7217 (20.7) | 6290 (22.8) | |
| 50-59 | 12,914 (20.7) | 7240 (20.8) | 5674 (20.6) | |
| 60-69 | 15,955 (25.6) | 8977 (25.8) | 6978 (25.3) | |
| ≥70 | 20,017 (32.1) | 11,376 (32.7) | 8641 (31.3) | |
| Age, median (IQR) | 63 (51-72) | 63 (52-72) | 62 (51-72) | <0.001 |
| Sex | 0.086 | |||
| Male | 30,066 (48.2) | 16,668 (47.9) | 13,398 (48.6) | |
| Female | 32,323 (51.8) | 18,140 (52.1) | 14,183 (51.4) | |
| Race | <0.001 | |||
| White | 43,569 (69.6) | 24,872 (71.5) | 18,697 (67.9) | |
| Black | 5560 (8.9) | 3085 (8.9) | 2475 (9.0) | |
| Other | 2529 (4.1) | 1308 (3.8) | 1221 (4.4) | |
| Unknown | 10,675 (17.1) | 5545 (15.9) | 5130 (18.6) | |
| ASA classification | <0.001 | |||
| I-II | 23,975 (38.4) | 13,689 (39.3) | 10,286 (37.3) | |
| III | 32,776 (52.5) | 18,065 (51.9) | 14,711 (53.3) | |
| IV | 5642 (9.0) | 3056 (8.8) | 2586 (9.4) | |
| Dependent functional status | 1789 (2.9) | 953 (2.7) | 836 (3.0) | 0.030 |
| Obesity | 21,731 (35.4) | 12,352 (36.1) | 9379 (34.9) | 0.001 |
| Current smoker | 9812 (15.7) | 5508 (15.8) | 4304 (15.6) | 0.455 |
| Diabetes | 9493 (15.2) | 5369 (15.4) | 4124 (15.0) | 0.103 |
| Hypertension | 28,780 (46.1) | 16,355 (47.0) | 12,425 (45.1) | <0.001 |
| Steroid use | 6548 (10.5) | 3480 (10.0) | 3068 (11.1) | <0.001 |
| Transfer status | 0.004 | |||
| Home | 58,039 (93.0) | 32,475 (93.3) | 25,564 (84.8) | |
| Nursing home/chronic care facility | 602 (1.0) | 346 (1.0) | 256 (0.9) | |
| Outside hospital | 3348 (5.4) | 1773 (5.1) | 1575 (5.7) | |
| Other/unknown | 404 (0.7) | 216 (0.6) | 188 (0.7) | |
| Emergent case | 8624 (13.8) | 4437 (12.7) | 4187 (15.2) | <0.001 |
| Procedure type | 0.001 | |||
| Partial colectomy | 54,453 (87.3) | 30,481 (87.6) | 23,972 (86.9) | |
| Total colectomy | 2959 (4.7) | 1588 (4.6) | 1371 (5.0) | |
| APR | 2693 (4.3) | 1436 (4.1) | 1257 (4.6) | |
| LAR | 1136 (1.8) | 671 (1.9) | 465 (1.7) | |
| Total proctocolectomy | 1152 (1.9) | 634 (1.8) | 518 (1.9) | |
| Ostomy creation/revision | 2325 (3.7) | 1303 (3.7) | 1022 (3.7) | 0.803 |
| Operative approach | <0.001 | |||
| Robotic | 9941 (15.9) | 5469 (15.7) | 4472 (16.2) | |
| Laparoscopic | 32,878 (52.7) | 18,804 (54.0) | 14,074 (51.0) | |
| Open planned | 19,574 (31.4) | 10,537 (30.3) | 9037 (32.8) | |
| Indication | <0.001 | |||
| Benign neoplasm | 4117 (6.6) | 2549 (7.3) | 1568 (5.7) | |
| Colorectal malignancy | 25,638 (41.1) | 14,281 (41.0) | 11,357 (41.2) | |
| Diverticular disease | 14,807 (23.7) | 8417 (24.2) | 6390 (23.2) | |
| IBD | 6907 (11.1) | 3684 (10.6) | 3223 (11.7) | |
| Volvulus | 1885 (3.0) | 1011 (2.9) | 874 (3.2) | |
| Other | 9039 (14.5) | 4868 (14.0) | 4171 (15.1) |
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 prepandemic 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. Twelve point seven percent of cases (n = 4437) prepandemic were emergent compared to 15.2% (n = 4187) during the pandemic (P < 0.001). Comparisons between prepandemic 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 prepandemic period (prepandemic 87.4% versus pandemic 82.9%, P < 0.001) and the largest increase in proportion of cases performed emergently (prepandemic 12.6% versus pandemic 17.1%, P < 0.001). Although subsequent quarters continued to show statistically significant decreased proportion of elective cases (Q3: 87.0% versus 85.7%, P = 0.005; Q4: 87.4% versus 85.5%, P < 0.001) and increased proportion of emergent cases (Q3: 13.0% versus 14.3%, P < 0.001; Q4: 12.6% versus 14.5%, P < 0.001), these trends were less pronounced (Fig. 1 ).
Fig. 1.
Proportion of elective and emergency colorectal surgery cases before and during the COVID-19 pandemic.
Compared to patients who underwent colorectal surgery prepandemic, patients who underwent surgery during the pandemic tended to be slightly younger (median age prepandemic 63 y versus pandemic 62 y, P < 0.001), have higher ASA class (III/IV), were more frequently diagnosed with dependent functional status (2.7% versus 3.0%, P = 0.030), and less frequently diagnosed with obesity (36.1% versus 34.9%, P = 0.001) or hypertension (47.0% versus 45.1%, P < 0.001) (Table 1). Patients during the pandemic presented from home less frequently (93.3% versus 84.8%, P = 0.003) and were transferred from outside hospitals more frequently (5.1% versus 5.7%, P = 0.001).
Regarding operative characteristics, the proportion of laparoscopic surgeries during the pandemic decreased (54.0% versus 51.0%, P < 0.001) and the proportion of planned open surgeries slightly increased (30.3% versus 32.8%, P < 0.001). Although the proportion of colorectal malignancy as a surgical indication did not change from prepandemic to pandemic (41.0% versus 41.2%, P = 0.762), surgical indications for volvulus (2.9% versus 3.2%, P < 0.001), and IBD (10.6% versus 11.7%, P < 0.001) increased. Conversely, surgical indications for benign neoplasms (7.3% versus 5.7%, P < 0.001) and diverticular disease (24.2% versus 23.2%, P = 0.003) decreased. The frequency of various colorectal procedure types were comparable prepandemic and during the pandemic, including for ostomy creation/revision (3.7% versus 3.7%, P = 0.803).
Unadjusted outcomes
On unadjusted analysis, patients who underwent surgery during the pandemic had higher rates of overall morbidity (prepandemic = 24.0% versus pandemic 27.0%, 26.2%, 25.7% for Q2/Q3/Q4 2020, respectively, P < 0.001) and serious morbidity (prepandemic = 14.6% versus pandemic 16.5%, 15.5%, 15.9%, P < 0.001) (Table 2 ). In particular, significantly higher rates of shock/sepsis (prepandemic = 7.6% versus pandemic 9.0%, 8.5%, 8.3%, P < 0.001) and bleeding requiring transfusion (prepandemic = 8.6% versus 10.2%, 9.5%, 9.5%, P < 0.001) were observed across all pandemic quarters compared to prepandemic. Significantly higher rates of pneumonia (prepandemic = 2.0% versus Q2 2020 = 2.6%, P = 0.002; prepandemic = 2.0% versus Q4 2020 = 3.0%, P < 0.001) and organ SSI (prepandemic = 5.6% versus Q2 2020 = 6.9%, P < 0.001; prepandemic = 5.6% versus Q4 2020 = 6.6%, P < 0.001) were observed in Q2 and Q4 2020. Anastomotic leak rates also increased significantly in Q2 2020 (prepandemic = 2.4% versus 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: prepandemic = 1.7% versus Q2 2020 = 2.1%, P = 0.004; prepandemic = 1.7% versus Q4 2020 = 2.1%, P = 0.005; 30-day mortality: prepandemic = 2.3% versus Q2 2020 = 2.7%, P = 0.012; prepandemic = 2.3% versus Q4 2020 = 2.6%, P = 0.041). Hospital LOS, however, was not clinically significantly different during the pandemic compared to prepandemic.
Table 2.
Thirty-day outcomes stratified by pandemic and prepandemic quarters.
| Outcome (%) | Prepandemic April-December 2019 |
Pandemic Q2 April-June 2020 |
Pandemic Q3 July-September 2020 |
Pandemic Q4 October-December 2020 |
P value |
|---|---|---|---|---|---|
| 34,810 (55.8) | 7992 (12.8) | 10,096 (16.2) | 9495 (15.2) | ||
| Discharge destination† | <0.001 | ||||
| Home | 31,108 (90.9) | 7245 (92.6)∗ | 9180 (92.6)∗ | 8658 (93.1)∗ | |
| Skilled care | 2980 (8.7) | 531 (6.8)∗ | 687 (6.9)∗ | 588 (6.3)∗ | |
| Unskilled care | 39 (0.1) | 12 (0.2) | 7 (0.1) | 13 (0.1) | |
| Hospice | 105 (0.3) | 34 (0.4) | 38 (0.4) | 38 (0.4) | |
| Overall morbidity‡ | 8338 (24.0) | 2160 (27.0)∗ | 2646 (26.2)∗ | 2441 (25.7)∗ | <0.001 |
| Serious morbidity§ | 5076 (14.6) | 1316 (16.5)∗ | 1569 (15.5)∗ | 1510 (15.9)∗ | <0.001 |
| Wound infection | 1731 (5.0) | 384 (4.8) | 504 (5.0) | 439 (4.6) | 0.514 |
| Pneumonia | 700 (2.0) | 204 (2.6)∗ | 233 (2.3) | 282 (3.0)∗ | <0.001 |
| UTI | 667 (1.9) | 147 (1.8) | 200 (2.0) | 184 (1.9) | 0.920 |
| VTE | 599 (1.7) | 146 (1.8) | 210 (2.1)∗ | 156 (1.6) | 0.071 |
| Cardiac | 431 (1.2) | 111 (1.4) | 153 (1.5)∗ | 122 (1.3) | 0.163 |
| Shock/sepsis | 2641 (7.6) | 718 (9.0)∗ | 862 (8.5)∗ | 783 (8.3)∗ | <0.001 |
| Intubation | 455 (1.3) | 109 (1.4) | 132 (1.3) | 136 (1.4) | 0.802 |
| Bleeding requiring transfusion | 2986 (8.6) | 812 (10.2)∗ | 956 (9.5)∗ | 898 (9.5)∗ | <0.001 |
| Renal complication | 465 (1.3) | 118 (1.5) | 120 (1.2) | 141 (1.5) | 0.233 |
| On ventilator > 48 h | 761 (2.2) | 200 (2.5) | 222 (2.2) | 230 (2.4) | 0.233 |
| Organ/space SSI | 1944 (5.6) | 550 (6.9)∗ | 595 (5.9) | 627 (6.6)∗ | <0.001 |
| Anastomotic leak | 846 (2.4) | 236 (3.0)∗ | 258 (2.6) | 248 (2.6) | 0.061 |
| In-hospital mortality | 578 (1.7) | 170 (2.1)∗ | 184 (1.8) | 198 (2.1)∗ | 0.005 |
| 30-day mortality | 785 (2.3) | 218 (2.7)∗ | 238 (2.4) | 248 (2.6)∗ | 0.034 |
| LOS (days), median (IQR) | 4 (3-7) | 5 (3-7) | 4 (3-7) | 4 (3-7) | <0.001 |
| Readmission | 3636 (10.5) | 823 (10.3) | 1081 (10.7) | 897 (9.5)∗ | 0.018 |
UTI = urinary tract infection; VTE = venous thromboembolism; SSI = surgical site infection; LOS = length of hospital stay; IQR = interquartile range.
Indicates statistical significance (reference = prepandemic group).
Discharge Destination: n = 61,263 patients; Prepandemic: n = 34,232; Pandemic: n = 27,031.
Overall morbidity: Wound infection, pneumonia, UTI, VTE, cardiac complication, shock/sepsis, unplanned intubation, bleeding transfusion, renal complication, on ventilator > 48 h, organ/space SSI, and anastomotic leak.
Serious morbidity: Clavien-Dindo III-IV (cardiac complication, shock/sepsis, unplanned intubation, renal complication, on ventilator > 48 h, organ/space SSI, and reoperation).
Patients who underwent colorectal surgery during the pandemic had a higher proportion of discharge to home (prepandemic = 90.9% versus pandemic = 92.6%, 92.6%, 93.1%, P < 0.001) and lower proportion of discharge to skilled care facilities (prepandemic = 8.7% versus 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 y (interquartile range 50-71 y). Although 30-day postoperative readmission rates were similar to prepandemic readmission rates for the first two quarters of the pandemic, there was a significantly decreased readmission rate for Q4 2020 (prepandemic = 10.4% versus 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 (odds ratio [OR]: 1.11, 95% confidence interval [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 3.
Multivariable logistic regression analysis: factors associated with overall morbidity, serious morbidity, and in-hospital mortality.
| Overall morbidity |
Serious morbidity |
In-hospital mortality |
||||
|---|---|---|---|---|---|---|
| OR (95% CI) | P value | OR (95% CI) | P value | OR (95% CI) | P value | |
| Pandemic timeline | ||||||
| Prepandemic (April-December 2019) | Reference | Reference | Reference | |||
| Pandemic (Q2 April-June 2020) | 1.06 (0.99-1.12) | 0.079 | 1.03 (0.95-1.11) | 0.494 | 1.09 (0.89-1.33) | 0.385 |
| Pandemic (Q3 July-September 2020) | 1.11 (1.05-1.17) | <0.001 | 1.04 (0.97-1.12) | 0.240 | 0.98 (0.81-1.19) | 0.843 |
| Pandemic (Q4 October-December 2020) | 1.08 (1.02-1.14) | 0.009 | 1.10 (1.03-1.18) | 0.006 | 1.28 (1.06-1.54) | 0.010 |
| Age group, years | ||||||
| <50 | Reference | Reference | Reference | |||
| 50-59 | 0.97 (0.91-1.04) | 0.424 | 0.91 (0.84-0.98) | 0.018 | 1.62 (1.13-2.32) | 0.009 |
| 60-69 | 1.09 (1.02-1.16) | 0.009 | 1.04 (0.96-1.13) | 0.302 | 2.56 (1.85-3.55) | <0.001 |
| ≥70 | 1.24 (1.16-1.33) | <0.001 | 1.10 (1.01-1.19) | 0.021 | 4.54 (3.29-6.25) | <0.001 |
| Sex | ||||||
| Male | Reference | Reference | Reference | |||
| Female | 0.99 (0.95-1.03) | 0.498 | 0.81 (0.77-0.85) | <0.001 | 0.79 (0.69-0.91) | 0.001 |
| Race | ||||||
| White | Reference | Reference | Reference | |||
| Black | 1.20 (1.12-1.29) | <0.001 | 1.21 (1.12-1.32) | <0.001 | 1.05 (0.84-1.32) | 0.643 |
| Other | 1.09 (0.98-1.22) | 0.100 | 0.82 (0.71-0.94) | 0.006 | 0.84 (0.54-1.31) | 0.444 |
| Unknown | 1.00 (0.94-1.06) | 0.967 | 0.78 (0.73-0.84) | <0.001 | 0.77 (0.63-0.95) | 0.016 |
| ASA classification | ||||||
| I-II | Reference | Reference | Reference | |||
| III | 1.49 (1.42-1.56) | <0.001 | 1.47 (1.39-1.56) | <0.001 | 4.47 (3.06-6.54) | <0.001 |
| IV | 3.03 (2.80-3.27) | <0.001 | 2.99 (2.74-3.27) | <0.001 | 16.00 (10.86-23.56) | <0.001 |
| Dependent functional status | 1.61 (1.43-1.81) | <0.001 | 1.35 (1.19-1.53) | <0.001 | 1.51 (1.22-1.88) | <0.001 |
| Obesity | 1.07 (1.03-1.12) | 0.002 | 1.08 (1.02-1.14) | 0.005 | 1.22 (1.05-1.41) | 0.008 |
| Current smoker | 1.22 (1.16-1.29) | <0.001 | 1.35 (1.26-1.43) | <0.001 | 1.27 (1.06-1.52) | 0.008 |
| Diabetes | 1.12 (1.06-1.19) | <0.001 | 1.06 (0.99-1.14) | 0.090 | 1.06 (0.90-1.25) | 0.484 |
| Hypertension | 1.10 (1.05-1.16) | <0.001 | 1.05 (0.99-1.11) | 0.116 | 1.06 (0.91-1.24) | 0.457 |
| Steroid use | 1.26 (1.17-1.35) | <0.001 | 1.14 (1.05-1.24) | 0.002 | 1.36 (1.10-1.68) | 0.004 |
| Transfer status | ||||||
| Home | Reference | Reference | Reference | |||
| Nursing home/chronic care facility | 1.40 (1.15-1.72) | 0.001 | 1.29 (1.04-1.60) | 0.021 | 1.81 (1.30-2.51) | <0.001 |
| Outside hospital | 1.45 (1.33-1.57) | <0.001 | 1.35 (1.24-1.48) | <0.001 | 1.48 (1.25-1.77) | <0.001 |
| Other/unknown | 1.13 (0.90-1.42) | 0.295 | 1.05 (0.81-1.35) | 0.726 | 1.78 (1.15-2.77) | 0.010 |
| Emergent case | 2.18 (2.05-2.32) | <0.001 | 2.85 (2.67-3.05) | <0.001 | 3.28 (2.77-3.89) | <0.001 |
| Procedure type | ||||||
| Partial colectomy | Reference | Reference | Reference | |||
| Total colectomy | 1.80 (1.64-1.97) | <0.001 | 1.63 (1.47-1.81) | <0.001 | 1.87 (1.50-2.34) | <0.001 |
| APR | 1.74 (1.59-1.91) | <0.001 | 1.48 (1.32-1.67) | <0.001 | 0.53 (0.78-1.00) | 0.049 |
| LAR | 1.11 (0.96-1.28) | 0.172 | 0.94 (0.77-1.14) | 0.511 | 0.25 (0.06-1.01) | 0.052 |
| Total proctocolectomy | 2.13 (1.85-2.44) | <0.001 | 1.72 (1.45-2.04) | <0.001 | 0.92 (0.44-1.89) | 0.817 |
| Ostomy creation/revision | 1.39 (1.26-1.53) | <0.001 | 1.36 (1.21-1.51) | <0.001 | 1.09 (0.81-1.48) | 0.585 |
| Operative approach | ||||||
| Laparoscopic | Reference | Reference | Reference | |||
| Robotic | 0.91 (0.86-0.98) | 0.007 | 1.12 (1.03-1.21) | 0.005 | 1.04 (0.70-1.53) | 0.859 |
| Open planned | 2.13 (2.04-2.24) | <0.001 | 1.97 (1.86-2.09) | <0.001 | 3.01 (2.46-3.68) | <0.001 |
| Indication | ||||||
| Benign neoplasm | Reference | Reference | Reference | |||
| Malignancy | 1.47 (1.32-1.63) | <0.001 | 1.34 (1.16-1.54) | <0.001 | 1.23 (0.72-2.10) | 0.441 |
| Diverticular disease | 2.01 (1.80-2.24) | <0.001 | 2.48 (2.15-2.87) | <0.001 | 0.94 (0.54-1.64) | 0.836 |
| IBD | 1.79 (1.58-2.03) | <0.001 | 1.90 (1.61-2.24) | <0.001 | 1.15 (0.61-2.15) | 0.668 |
| Volvulus | 1.02 (0.87-1.19) | 0.815 | 1.20 (0.99-1.45) | 0.066 | 1.17 (0.64-2.11) | 0.614 |
| Other | 2.24 (2.00-2.51) | <0.001 | 2.62 (2.26-3.04) | <0.001 | 2.43 (1.42-4.17) | 0.001 |
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 prepandemic 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 prepandemic 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 y (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 y (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 multifaceted 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,13 Ireland,6 and Singapore14 and for noncolorectal procedures such as spine surgeries in the United States.15 This decrease in surgical volume may be attributed to early recommendations from professional societies to limit nonurgent surgeries; diagnostic testing like colonoscopy was also limited, resulting in less surgical referrals.3, 4, 5 , 13 In addition, patients may have avoided seeking healthcare or were managed medically rather than surgically, for fear of contracting COVID-19 or contributing to an overwhelmed healthcare system.
Importantly, a higher proportion of operations were performed emergently rather than electively. Moreover, patients operated on during the pandemic were admitted less frequently from home and more often transferred from other hospitals. This shift to more emergent surgeries may be attributed partially to hospitals limiting elective operations while continuing emergent operations, as has been observed internationally.16 However, a potentially concerning factor is that patients may have had delayed presentations to the healthcare system to avoid being exposed to COVID-19 or healthcare providers may have delayed referrals. Such delays may have resulted in disease progression necessitating emergent management. Our study showed that the rates of colorectal surgery patients with higher ASA classification and dependent functional status increased during the pandemic—an observation also noted in surgical specialties such as acute care/emergency surgery.17 , 18 A study in the United Kingdom showed that general surgery patients admitted during the pandemic were frailer and presented more frequently with acute surgical pathologies such as bowel obstruction and perforation.18 Another study showed a significant decrease in urgent, suspected colorectal cancer referrals and diagnoses, resulting in more emergency presentations of bowel obstruction.19 In one Spanish hospital, the COVID-19 pandemic resulted in a 48% reduction in the new diagnosis of colorectal cancer, with 12.1% of patients being diagnosed emergently compared to 3.6% prepandemic.20 Given that emergent presentations of gastrointestinal pathologies have been associated with poorer outcomes, these observations highlight the need to prioritize health system resources to maintain adequate and timely diagnosis and management.21 , 22
Interestingly, despite patients presenting with higher ASA classification, dependent functional status, and a greater proportion of emergent cases, our study showed that the rates of ostomy creation/revision were similar to those prepandemic, which may partially reflect the relatively comparable rates of surgical indications before and during the pandemic for which ostomies would most likely be performed or indicated. Notably, the proportion of colorectal surgeries performed for cancer remained stable during the pandemic. On one hand, cancer surgery was prioritized to continue during the pandemic23; however, there has also been a recognized decline in cancer diagnoses due to less screening colonoscopies and referrals.13 Fortunately, our study shows that despite these two seemingly opposing factors, cancer patients were able to undergo surgical management with no significant differences to prepandemic levels. With regards to other indications, the proportions of surgeries for volvulus and IBD increased, while the proportions of surgeries for benign neoplasm and diverticular disease decreased. Volvulus often presents emergently, so operations were maintained during the pandemic. Although patients with diverticular disease may present acutely, some of these patients may have been managed medically rather than with definitive surgery. Elective resections for patients with recurrent diverticulitis who did not present acutely may have been postponed or canceled during the pandemic. Patients with benign neoplasm may have delayed surgical management and elected to undergo surveillance instead.
Our study also found that the frequency of laparoscopic surgery decreased and the frequency of open surgery increased during the pandemic. This observation has been demonstrated in colorectal cohorts in other countries.6 Early in the pandemic, there was concern that COVID-19 could potentially be transmitted during laparoscopy after establishing pneumoperitoneum, so laparoscopy was considered an aerosol-generating procedure.8 , 24 Institutions and/or surgeons may have elected to perform more open rather than laparoscopic surgeries to mitigate viral exposure. Early recommendations from Society of American Gastrointestinal and Endoscopic Surgeons advised that “consideration be given to the possibility of viral contamination to staff during surgery either open, laparoscopic, or robotic” and offered practical measures for surgery, intubation and extubation, and personal protective equipment.5 A more recent systematic review, however, has since concluded that there is no evidence to date to support the transmission of COVID-19 by laparoscopic surgery and that laparoscopy can be performed with adequate precautions.25 Another reason for the decrease in laparoscopic surgeries may be the increase in emergency operations during the pandemic and the increase in numbers of sicker patients unable to tolerate pneumoperitoneum.
Regarding surgical outcomes, patients who underwent colorectal surgery during the pandemic had significantly worse overall and serious morbidity than patients who had surgery prepandemic. The odds of in-hospital mortality were also significantly greater during October-December 2020. Although studies have shown that COVID-19 patients have worse postoperative outcomes than COVID-negative patients,26 , 27 patients without COVID-19 may also have poorer outcomes. One U.K. study reported significantly higher rates of Clavien-Dindo Grade ≥ 3 complications and all-cause 30-day mortality in COVID-negative adult emergency general surgery patients compared to prepandemic patients.18 Another study of 25 hospitals in Spain reported that although COVID-negative emergency general and gastrointestinal surgery patients had similar rates of 30-day morbidity, hospital LOS, and readmission, there was a trend toward higher 30-day mortality rates and significantly greater failure-to-rescue rates; the authors identified root causes to include barriers in communication/technology and nurse understaffing.27 In an international longitudinal cohort study of adult emergency surgical patients during the first wave of the pandemic from March to August 2020, the peak months of the first wave were associated with significantly higher in-hospital mortality compared to nonpeak months.16 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 United States, these specific 3 mo coincided with the largest rise in COVID-19 cases, deaths, and hospitalizations for the observed 2020 pandemic year (Fig. 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.
Fig. 2.
Rates 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 United States declared COVID-19 a pandemic (March 13, 2020) and 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 prepandemic. This was similarly observed at an Italian hospital for patients undergoing colorectal cancer resection during the first pandemic wave.28 Other studies, however, have reported decreased LOS during the pandemic for blunt trauma patients,29 thoracolumbar adult spinal deformity surgical patients,15 and hip fracture surgical patients.30 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 and 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. Thirty-day postoperative readmission was also largely unchanged for colorectal patients during the pandemic, except when readmission rates decreased during the last 3 mo 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.15 , 31 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, less 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.7 , 15 One study found that among rehabilitation-eligible stroke survivors, there was decreased odds of discharge to rehabilitation facilities during the pandemic.7 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.32 , 33 From a study using U.S. national insurance claims data of patients aged ≥ 65 y, discharges to skilled nursing facilities declined from 19% in 2019 to 14% in October 2020 and spending toward skilled nursing facilities declined by half.34 Possible explanations include patient, family, caregiver, and provider preferences for home postdischarge care and 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 postacute 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. First, 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 United States at different time points 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 (Fig. 2). Because the latest ACS-NSQIP data are only available through December 2020, the latter impact of the pandemic in 2021 and its associated variants cannot be assessed until more data are publicly available.
Finally, COVID-19 status in patients undergoing surgery during the pandemic were unable to be identified due to International Classification of Diseases–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 preoperative 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 United States 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 United States, overall colorectal surgery case volume decreased; in addition, 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 postacute care planning pathways. Through lessons learned from this pandemic, healthcare systems can become better equipped at effectively anticipating, mobilizing, and using resources for future pandemic preparedness responses without compromising quality of care.
Author Contributions
Study design: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., and B.S. Data acquisition and analysis: S.Y.C., S.N.R., M.S., and A.P. Interpretation of data: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., and B.S. Drafting work: S.Y.C., S.N.R., M.S., and A.P. Critical revision: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., and B.S. Final approval/accountability: S.Y.C., S.N.R., M.S., A.P., A.G., C.A., J.E.E., and B.S.
Acknowledgments
The authors would like to acknowledge the role of the Johns Hopkins Surgery Center for Outcomes Research (JSCOR) for supporting this study.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.jss.2022.12.041.
Disclosure
None declared.
Funding
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.
Supplementary Materials
References
- 1.The Johns Hopkins University Johns Hopkins coronavirus resource center. https://coronavirus.jhu.edu/ Available at:
- 2.Moletta L., Pierobon E.S., Capovilla G., et al. International guidelines and recommendations for surgery during Covid-19 pandemic: a systematic review. Int J Surg. 2020;79:180–188. doi: 10.1016/j.ijsu.2020.05.061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.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. https://www.facs.org/-/media/files/covid19/acs_triage_and_management_elective_cancer_surgery_during_acute_and_recovery_phases.ashx Available at:
- 4.Society of Surgical Oncology (SSO) Cancer surgeries in the time of COVID-19: a message from the SSO president and president-elect. https://www.surgonc.org/wp-content/uploads/2020/03/COVID-19-Letter-to-Members.pdf Available at:
- 5.Society of American Gastrointestinal and Endoscopic Surgeons SAGES and EAES recommendations regarding surgical response to COVID-19 crisis. https://www.sages.org/recommendations-surgical-response-covid-19 Available at:
- 6.Donlon N.E., Hayes C., Davern M., et al. Impact of COVID-19 on the diagnosis and surgical treatment of colorectal cancer: a national perspective. Dis Colon Rectum. 2021;64:1305–1309. doi: 10.1097/DCR.0000000000002230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Thau L., Siegal T., Heslin M.E., et al. Decline in rehab transfers among rehab-eligible stroke patients during the COVID-19 pandemic. J Stroke Cerebrovasc Dis. 2021;30:1–7. doi: 10.1016/j.jstrokecerebrovasdis.2021.105857. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Wexner S.D., Cortés-Guiral D., Gilshtein H., Kent I., Reymond M.A. COVID-19: impact on colorectal surgery. Colorectal Dis Jun. 2020;22:635–640. doi: 10.1111/codi.15112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.American College of Surgeons About ACS-NSQIP. https://www.facs.org/quality-programs/acs-nsqip/about Available at:
- 10.American College of Surgeons ACS NSQIP participant use data file. https://www.facs.org/quality-programs/acs-nsqip/participant-use Available at:
- 11.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. Ann Surg. 2004;240:205–213. doi: 10.1097/01.sla.0000133083.54934.ae. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Hosmer D.W.L.S., Sturdivant R.X. Applied Logistic Regression. 2nd ed. Wiley; New York: 2000. [Google Scholar]
- 13.Morris E.J.A., Goldacre R., Spata E., et al. Impact of the COVID-19 pandemic on the detection and management of colorectal cancer in England: a population-based study. Lancet Gastroenterol Hepatol. 2021;6:199–208. doi: 10.1016/S2468-1253(21)00005-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Lee T., Cheng D.Z., Foo F.-J., et al. Did the COVID-19 lockdown result in a delay of colorectal cancer presentation and outcomes? A single centre review. Langenbecks Arch Surg. 2022;407:739–745. doi: 10.1007/s00423-022-02448-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Wang K.Y., McNeely E.L., Dhanjani S.A., et al. COVID-19 significantly impacted hospital length of stay and discharge patterns for adult spinal deformity patients. Spine. 2021;46:1551–1556. doi: 10.1097/BRS.0000000000004204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Winter Beatty J., Clarke J.M., Sounderajah V., et al. Impact of the COVID-19 pandemic on emergency adult surgical patients and surgical services: an international multi-center cohort study and department survey. Ann Surg. 2021;274:904–912. doi: 10.1097/SLA.0000000000005152. [DOI] [PubMed] [Google Scholar]
- 17.Aviran E., Laks S., Benvenisti H., et al. The impact of the COVID-19 pandemic on general surgery acute admissions and urgent operations: a comparative prospective study. Isr Med Assoc J. 2020;11:673–679. [PubMed] [Google Scholar]
- 18.McLean R.C., Young J., Musbahi A., et al. A single-centre observational cohort study to evaluate volume and severity of emergency general surgery admissions during the COVID-19 pandemic: is there a "lockdown" effect? Int J Surg. 2020;83:259–266. doi: 10.1016/j.ijsu.2020.09.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Shinkwin M., Silva L., Vogel I., et al. COVID-19 and the emergency presentation of colorectal cancer. Colorectal Dis. 2021;23:2014–2019. doi: 10.1111/codi.15662. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Suárez J., Mata E., Guerra A., et al. Impact of the COVID-19 pandemic during Spain's state of emergency on the diagnosis of colorectal cancer. J Surg Oncol. 2021;123:32–36. doi: 10.1002/jso.26263. [DOI] [PubMed] [Google Scholar]
- 21.McPhail S., Elliss-Brookes L., Shelton J., et al. Emergency presentation of cancer and short-term mortality. Br J Cancer. 2013;109:2027–2034. doi: 10.1038/bjc.2013.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Fligor S.C., Wang S., Allar B.G., et al. Gastrointestinal malignancies and the COVID-19 pandemic: evidence-based triage to surgery. J Gastrointest Surg. 2020;24:2357–2373. doi: 10.1007/s11605-020-04712-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.COVIDSurg Collaborative Effect of COVID-19 pandemic lockdowns on planned cancer surgery for 15 tumour types in 61 countries: an international, prospective, cohort study. Lancet Oncol. 2021;22:1507–1517. doi: 10.1016/S1470-2045(21)00493-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Ren X., Chen B., Hong Y., et al. The challenges in colorectal cancer management during COVID-19 epidemic. Ann Transl Med. 2020;8:498. doi: 10.21037/atm.2020.03.158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.El Boghdady M., Ewalds-Kvist B.M. Laparoscopic surgery and the debate on its safety during COVID-19 pandemic: a systematic review of recommendations. Surgeon. 2021;19:e29–e39. doi: 10.1016/j.surge.2020.07.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Doglietto F., Vezzoli M., Gheza F., et al. Factors associated with surgical mortality and complications among patients with and without Coronavirus Disease 2019 (COVID-19) in Italy. JAMA Surg. 2020;155:691–702. doi: 10.1001/jamasurg.2020.2713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Osorio J., Madrazo Z., Videla S., et al. Analysis of outcomes of emergency general and gastrointestinal surgery during the COVID-19 pandemic. Br J Surg. 2021;108:1438–1447. doi: 10.1093/bjs/znab299. [DOI] [PubMed] [Google Scholar]
- 28.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? Updates Surg. 2021;73:173–177. doi: 10.1007/s13304-020-00947-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Yeates E.O., Grigorian A., Schellenberg M., et al. Decreased hospital length of stay and intensive care unit admissions for non-COVID blunt trauma patients during the COVID-19 pandemic. Am J Surg. 2022;224:90–95. doi: 10.1016/j.amjsurg.2022.02.055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.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. Isr Med Assoc J. 2021;23:469–474. [PubMed] [Google Scholar]
- 31.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. Am Surg. 2021;88:489–497. doi: 10.1177/00031348211054528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Khan F., Amatya B. Medical rehabilitation in pandemics: towards a new perspective. J Rehabil Med. 2020;52:jrm00043. doi: 10.2340/16501977-2676. [DOI] [PubMed] [Google Scholar]
- 33.Levin S.R., Gitkind A.I., Bartels M.N. Effect of the COVID-19 pandemic on postacute care decision making. Arch Phys Med Rehabil. 2021;102:323–330. doi: 10.1016/j.apmr.2020.10.104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Werner R.M., Bressman E. Trends in post-acute care utilization during the COVID-19 pandemic. J Am Med Dir Assoc. 2021;22:2496–2499. doi: 10.1016/j.jamda.2021.09.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.