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Original Contributions: Colorectal Cancer

Compliance With Preoperative Elements of the American Society of Colon and Rectal Surgeons Rectal Cancer Surgery Checklist Improves Pathologic and Postoperative Outcomes

Garfinkle, Richard M.D.; Vasilevsky, Carol-Ann M.D.; Ghitulescu, Gabriela M.D.; Morin, Nancy M.D.; Faria, Julio M.D.; Boutros, Marylise M.D.

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Diseases of the Colon & Rectum: January 2020 - Volume 63 - Issue 1 - p 30-38
doi: 10.1097/DCR.0000000000001511
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Abstract

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The management of patients with rectal cancer has become increasingly complex. In addition to high-quality total mesorectal excision surgery, there are a number of preoperative, intraoperative, and postoperative tasks that should be completed to optimize patient outcomes. These tasks require a multidisciplinary approach and the coordination of care between multiple specialists, such as surgeons, medical and radiation oncologists, radiologists, and pathologists.1,2 Moreover, with the increased demand for rectal cancer surgery to be delivered by experienced surgeons at high-volume centers, more patients can be expected to travel far distances for their treatment,3 which increases the requirement for well-coordinated care to complete all of the appropriate tasks.

Recognizing these rising complexities in care, the Quality and Safety Assessment Committee of the American Society of Colon and Rectal Surgeons (ASCRS) developed a comprehensive rectal cancer surgery checklist in 2012 composed of the essential elements of preoperative, intraoperative, and postoperative care for patients undergoing rectal cancer surgery.4 The goal of this checklist was to improve and standardize clinical care, with an emphasis on reminding clinicians of tasks that, if omitted, may lead to serious consequences. The use of checklists not only improves adherence to critical processes of care,5 but also encourages a nonhierarchical team-based approach and improves communication among treating team members.6 In surgery, checklists have already proven to be effective, with the World Health Organization Surgical Safety Checklist providing the most prominent example of a checklist’s abilities to reduce perioperative morbidity and mortality.7,8 The use of a cancer-specific surgical checklist has also been correlated with improved oncologic outcomes in other malignancies.9

The preoperative elements of the ASCRS rectal cancer surgery checklist represent a particularly important aspect of the checklist; in addition to being the largest portion of the checklist, compliance with these elements has the most direct influence on treatment decision-making. The purpose of this study was to evaluate the association between compliance with preoperative elements of the ASCRS rectal cancer surgery checklist and pathologic outcomes, surgical morbidity, and length of stay (LOS) after rectal cancer resection.

MATERIALS AND METHODS

This was a retrospective cohort study making use of the American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP), which is a nationwide initiative that generates prospectively collected Health Insurance Portability and Accountability Act–compliant surgical outcomes data. Trained clinical reviewers collect a large group of variables in several categories, including demographics, surgical profiles, preoperative data, and 30-day postoperative outcomes. Furthermore, a quality assessment audit was performed and reported that ACS-NSQIP has implemented audit and training procedures that are highly effective in collecting robust data with reliability and accuracy that is constantly improving.10

Patient Identification

After institutional review board approval, we identified all patients from the 2016–2017 ACS-NSQIP proctectomy-targeted database who underwent elective proctectomy for rectal cancer, according to Current Procedural Terminology codes (low anterior resection: 45111, 45112, 45119, 44145, 44146, 44207, 44208, 45397; abdominoperineal resection (APR): 45110, 45395) and International Classification of Disease (ICD) codes (malignant neoplasm of rectum: ICD-9-CM 154.1 or ICD-10-CM C20). Patient data from the proctectomy-targeted database were then linked to the general database for demographic and general operative and postoperative data, and only patients with values in both data sets were additionally included. Patients who underwent emergency resections, had preoperative sepsis, had an ASA score >4, or were coded as having a “clean” surgical wound (versus clean-contaminated or contaminated) were excluded.

Defining Compliance for Checklist Elements

The ASCRS rectal cancer surgery checklist is composed of 10 preoperative elements, of which 6 are captured in the ACS-NSQIP database and were included in this analysis (Table 1): complete preoperative evaluation of the colon, pretreatment tumor location within the rectum, pretreatment clinical staging of the tumor and regional nodes, pretreatment clinical staging of distant metastasis, appropriate use of neoadjuvant radiotherapy, and preoperative stoma marking.

TABLE 1.
TABLE 1.:
ASCRS rectal cancer surgery checklist preoperative elements and corresponding ACS-NSQIP variables

When assessing for complete preoperative evaluation of the colon, if a patient’s colonoscopy was incomplete because of an obstructing lesion, this element was considered complete. Pretreatment tumor location was based on preoperative clinic notes, preoperative endoscopy, or the operative report. Locoregional and distant pretreatment clinical staging were performed with MRI with or without transrectal ultrasound and CT scans of the chest and abdomen, respectively. The use of neoadjuvant radiotherapy was considered appropriate in locally advanced tumors (American Joint Committee on Cancer stage II or III; cT-stage >2 and/or cN-stage +). Finally, recognizing that not all rectal cancer resections require proximal diversion, in this study, preoperative stoma marking was considered a requirement for checklist compliance only in irradiated and/or mid low rectal cancers.11

For the purpose of this analysis, modified preoperative checklist compliance (mPCC(+)) was defined as having all 6 preoperative elements complete. Patients with 0 to 5 of 6 elements complete were considered mPCC(–).

Outcomes

The outcomes of interest included pathologic and 30-day postoperative outcomes. Pathologic outcomes included circumferential resection margin (CRM) status, distal resection margin (DRM) status, and an adequate lymph node harvest (≥12 nodes evaluated). Thirty-day postoperative outcomes included surgical morbidity (defined as the presence of any one of the following: surgical site infection [superficial, deep, or organ space], wound dehiscence, postoperative bleeding, anastomotic leak, postoperative ileus, or reoperation) and postoperative LOS.

Statistical Analysis

Patient demographics, medical comorbidities, and tumor, treatment, and operative characteristics were presented as means with SDs, medians with interquartile ranges (Q1 to Q3), or frequencies with proportions, where appropriate. Multiple logistic regression was used to assess for the association between mPCC(+) and a positive CRM, positive DRM, adequate lymph node harvest, and surgical morbidity. ORs were reported with 95% CIs. Multiple linear regression was used to assess for the association between mPCC(+) and LOS. Covariates for each multivariate regression model were selected based on subject knowledge. To account for the significant impact of appropriate neoadjuvant radiotherapy use (relative to other preoperative checklist elements) on CRM status, a sensitivity analysis was performed, whereby radiotherapy was removed as part of the exposure and used as a covariate in the regression model for CRM positivity. An α = 0.05 was set for statistical significance. All of the statistical analyses were performed with R version 3.5.1.12

Institutional Data Review

In recognizing that only 6 preoperative elements were available in the ACS-NSQIP database, we performed an additional chart review on the patients from our institution who were included in the ACS-NSQIP proctectomy-specific database from 2016 to 2017. We defined these patients as being mPCC(+) or mPCC(–) using the data already collected by our ACS-NSQIP reviewers (ie, not supplemented by additional chart review or discussions with attending physicians) and performed a limited chart review (electronic medical charts only) to collect data on the presence or absence of the 4 remaining preoperative elements, including formal pathology review for invasive carcinoma; assessment of family history, stool continence, and sexual function; documentation of a multidisciplinary tumor board meeting; and preoperative CEA level. The proportion of mPCC(+) patients who truly had all 10 preoperative elements complete was reported.

RESULTS

A total of 2217 patients underwent an elective rectal cancer resection and met inclusion criteria. The median age was 62.0 years (range, 53.0–71.0 y), and 61.6% of patients were men. The majority of patients had an ASA score of III or IV (64.3%), and the median BMI was 26.9 kg/m2 (range, 23.4–31.0 kg/m2). Most patients received neoadjuvant radiotherapy (59.5%), underwent an APR (60.2%), and had a minimally invasive resection (57.0%).

Of the preoperative checklist elements available, documentation of pretreatment tumor location (91.3%), complete preoperative evaluation of the colon (86.6%), and preoperative stoma marking (84.0%) had the highest rates of completion. Pretreatment staging of distant metastasis had the lowest overall completion (70.8%; Fig. 1). Only 836 patients (37.7%) had all of the checklist elements complete (mPCC(+)), whereas 1381 (62.3%) did not (mPCC(–)). The median number of checklist elements completed was 5.0 (range, 4.0–6.0). A total of 655 patients (29.5%) had 5 of 6 elements complete–making up nearly half (655/1381 = 47.4%) of the mPCC(–) group–whereas very few patients had ≤2 (3.2%) of 6 complete (Fig. 2). Table 2 presents patient, tumor, and operative characteristics. mPCC(+) patients were younger than mPCC(–) patients (60.0 vs 63.0 y; p < 0.001) but were otherwise similar in terms of demographics and comorbidities. The groups were also similar with regard to procedure performed, operative approach, and operative time. Statistical tests were not performed to evaluate the distribution of tumor characteristics, because the mPCC(–) group had inherently higher rates of missing information for these variables secondary to incomplete preoperative testing.

TABLE 2.
TABLE 2.:
Patient, tumor, and operative characteristics
FIGURE 1.
FIGURE 1.:
Compliance with individual preoperative checklist elements.
FIGURE 2.
FIGURE 2.:
Number of completed checklist elements. mPCC(+) = modified preoperative checklist compliance with all 6 preoperative elements complete.

mPCC(+) patients were less likely to have a positive CRM (4.1% vs 9.2%; p < 0.001) and positive DRM (1.2% vs 2.3%; p < 0.001) and were more likely to have an adequate lymph node harvest ≥12 (82.7% vs 75.3%; p < 0.001). mPCC(+) patients also had less surgical morbidity (30.0% vs 35.2%; p = 0.01) and a shorter median LOS (5.0 vs 6.0 d; p < 0.001; Table 3). Individual morbidities, such as anastomotic leak, surgical site infection, and postoperative ileus, were similar between groups, as were rates of 30-day readmission and mortality. After adjusting for age, sex, race, BMI, ASA score, procedure performed, operative approach, operative time, and final pathological stage, mPCC(+) was associated with lower odds of CRM positivity (OR = 0.47 (95% CI, 0.31–0.71); p < 0.001) and higher odds of an adequate lymph node harvest ≥12 (OR = 1.60 (95% CI, 1.29–2.00); p < 0.001). mPCC(+) was not associated with lower odds of DRM positivity (OR = 0.51 (95% CI, 0.22–1.05); p = 0.08). After adjusting for the same 9 covariates, as well as the presence of chronic obstructive pulmonary disorder, congestive heart failure, hypertension, renal failure, bleeding disorder, steroids, preoperative ascites, smoking, preoperative weight loss, and preoperative functional status, mPCC(+) was associated with reduced surgical morbidity (OR = 0.78 (95% CI, 0.65–0.95); p = 0.01) and shorter LOS (β = –0.87 (95% CI, –1.51 to –0.24); p = 0.007).

TABLE 3.
TABLE 3.:
Pathologic and 30-day postoperative outcomes

The number of checklist elements complete (rather than mPCC(+) as a binary outcome) was also assessed in the same 5 regression models. Number of elements complete was significantly associated with reduced CRM positivity (OR = 0.71 (95% CI, 0.62–0.82); p < 0.001) and DRM positivity (OR = 0.69 (95% CI, 0.49–0.99); p = 0.04), higher odds of an adequate lymph node harvest ≥12 (OR = 1.19 (95% CI 1.09–1.30); p < 0.001), reduced surgical morbidity (OR = 0.92 (95% CI, 0.84–0.99); p = 0.04), and shorter LOS (β = –0.33 (95% CI, –0.60 to –0.05); p = 0.02).

To account for the significant impact of appropriate neoadjuvant radiotherapy use (relative to other preoperative checklist elements) on CRM status, we performed a second regression analysis for CRM positivity, whereby we varied the definition of mPCC(+) to require 5 of 5 checklist elements and adjusted for radiotherapy as a covariate. When defined as 5 of 5 checklist elements, mPCC(+) remained significantly associated with reduced CRM positivity (OR = 0.61 (95% CI, 0.42–0.88); p = 0.009) compared with mPCC(–) (0–4/5 elements), after adjusting for neoadjuvant radiotherapy use (OR = 0.49 (95% CI, 0.31–0.64); p < 0.001) and the same 9 covariates.

After applying the same cohort inclusion and exclusion criteria to our own institution’s ACS-NSQIP patients, we identified 42 patients who underwent rectal cancer resection in 2016–2017. Among the 31 patients (31/42 = 73.8%) who were mPCC(+), 29 (93.5%) had the additional 4 preoperative elements complete (excluding preoperative sexual function assessment) and would have been considered 10 of 10 had these variables been available in the database.

DISCUSSION

The aim of this study was to determine whether compliance with preoperative elements of the ASCRS rectal cancer surgery checklist was associated with improved pathologic and 30-day postoperative outcomes. The ASCRS rectal cancer surgery checklist was first published electronically in 2012 on the society’s webpage and was later published in 2016 in Diseases of the Colon & Rectum.4 To our knowledge, this is the first study to correlate the checklist with outcomes after rectal cancer surgery. Our study demonstrated that compliance with preoperative elements of the checklist was associated with reduced CRM positivity, improved lymph node harvest, reduced postoperative surgical morbidity, and a shorter LOS after rectal resection.

The elements included in the ASCRS rectal cancer surgery checklist were developed based on a review of the available literature at the time and were modified and finalized based on a majority consensus. The committee followed the essential steps in checklist development introduced by the creators of the World Health Organization Surgical Safety Checklist13 and involved many society members and experts to maximize buy-in from potential users. The checklist incorporates 3 phases of rectal cancer care, including preoperative, intraoperative, and postoperative care. For several reasons, we focused on preoperative checklist elements in this analysis. First, it represents the largest portion of the checklist with the greatest number of elements. Second, the completion and subsequent results of the preoperative elements have the greatest impact on successfully setting the stage for future treatment. For example, the identification of a synchronous colon cancer on preoperative colonoscopy would alter the surgical plan, whereas proper locoregional staging would dictate the delivery of neoadjuvant radiotherapy. Lastly, most of the intraoperative and postoperative variables are not available in the ACS-NSQIP database. As the authors of the checklist highlight, the intraoperative elements focus on the documentation of surgery-specific items (eg, assessing the integrity of pelvic nerves, documenting the rationale for sphincter preservation versus permanent stoma),4 which would be hard to gather from a large multicenter database.

The ASCRS rectal cancer surgery checklist elements are aligned with the standards put forth by the National Accreditation Program for Rectal Cancer (NAPRC).14 The NAPRC was developed through a collaboration between the Optimizing the Surgical Treatment of Rectal Cancer Consortium and the American College of Surgeon Commission on Cancer, with the goal of reducing variability in care and outcomes by centralizing rectal cancer care to accredited sites. Brady et al15 recently queried the National Cancer Database to assess the current status of rectal cancer care in the United States and found that completion of all included NAPRC process measures (limited to those available in the database) only occurred in 28.1% of patients, which is similarly low to the rate of mPCC(+) in the present study (37.7%). On multivariable analysis, they identified age, race, geographic location, year of diagnosis, and disease stage as important predictors of completing all of the process measures, whereas year of treatment, annual resection volume, and size of rectal cancer program were predictors of completing all of the performance measures. However, they did not correlate the completion of all measures with postoperative outcomes, and whereas the inclusion of each individual NAPRC process measure was heavily supported by evidence (much like the ASCRS checklist items), reporting on the collective benefit of all measures could aid in the dissemination and adoption of such standards.

In the present study, we demonstrated that compliance with preoperative elements of the ASCRS checklist was significantly associated with improved pathologic and 30-day postoperative outcomes. The protective association with CRM status remained on our sensitivity analysis, even after removing radiotherapy from the exposure and adjusting for it as a covariate in the regression model. The clear benefit observed in mPCC(+) patients across a wide range of postoperative outcomes suggests a potential systems effect in play, particularly given the lack of any biologically plausible association between many of the checklist elements and certain outcomes (eg, complete preoperative colonoscopy or preoperative stoma marking and margin status or lymph node harvest). One possibility is that mPCC(+) patients had their resections performed by more qualified rectal cancer surgeons at institutions with a more refined infrastructure for rectal cancer care. Multiple studies have demonstrated that both surgeon and hospital annual rectal cancer volume, in addition to subspecialty training, can impact rates of postoperative morbidity and locoregional recurrence.16–18 Unfortunately, ACS-NSQIP does not include surgeon and hospital characteristics, which limits our ability to truly elucidate how these provider-level checklist interventions impact patient-level outcomes. It is also possible that the more qualified rectal cancer surgeons are more meticulous at adhering to and documenting preoperative processes of care. Only 1 study has previously attempted to evaluate predictors of compliance with the ASCRS checklist. Using their own institution’s data, Chapman et al19 found that surgeon experience was inversely associated with checklist compliance, hypothesizing that senior surgeons (>10 y in practice) may have more confidence in their own treatment decisions and more readily rely on their own practice patterns. Their findings were consistent with previous work that demonstrated resistance from senior physicians as a major barrier to surgical checklist implementation.20

The rate of sphincter preservation is another significant and highly variable quality metric of rectal cancer surgery that depends on many of the same systems factors listed above.21,22 We did not find significant differences in APR rates between mPCC(+) and mPCC(–) groups. However, the incidence of APR overall (60%) in this database was high, which should serve as a reminder that contribution to ACS-NSQIP is voluntary and is not necessarily a representative random sample of the nation.

To account for the heterogeneous degree of checklist compliance in the mPCC(–) group (anywhere from 0 to 5 of 6 elements), we performed a secondary analysis to evaluate the incremental benefit of completing 1 checklist element. The association between the number of checklist elements complete and each outcome remained significantly protective. For example, the completion of 1 additional checklist element further decreased the odds a positive CRM by ≈30% and reduced surgical morbidity by ≈10%. Such an analysis is flawed by the assumption that each checklist element is equally associated with the outcome (which is unlikely to be true); however, this dose–response relationship provides added strength for the observed statistical association between checklist compliance and the outcomes of interest. Although complete checklist compliance should always be promoted as the standard, physicians should still strive to complete and document as many elements as possible.

The strengths of this study are the use of a reliable and validated prospectively collected database, the large number of patients included, and the robust statistical analysis. However, our results should also be considered in light of several limitations. Similar to the study assessing completion of NAPRC standards using the National Cancer Database,15 we were limited to checklist elements available in ACS-NSQIP; therefore, we could not validate the entire preoperative checklist. However, in a small sample of our own institution’s ACS-NSQIP patients with rectal cancer, 93.5% of patients who had 6 of 6 elements complete also had the remaining 4 elements complete, suggesting that the completion of individual preoperative elements is likely correlated. We also cannot be certain whether incomplete tasks were not performed or simply not recorded in a reliably retrievable manner, which could be a reflection of poor documentation and record keeping rather than omission of a task. Maniar et al23 previously demonstrated an association between compliance with ASCRS checklist elements and the use of synoptic operative reporting, suggesting that improved means of documentation may enhance checklist compliance. The checklist also qualifies the radiotherapy variable as the “consideration” of neoadjuvant treatment for locally advanced disease, which we could not decipher from the database and thus could only include appropriate use of neoadjuvant treatment. Furthermore, despite our best efforts on sensitivity analysis to adjust for the use of neoadjuvant radiation, this important difference between the 2 groups cannot be overlooked and may be reflective of other unmeasured confounders. Another limitation of this study is that the database is missing important surgeon and hospital variables that could be associated with both mPCC(+) and the outcomes of interest. Thus, we are assessing surgeon- and hospital-driven interventions with patient-level, rather than provider-level, outcomes. ICD-9/10 codes also do not characterize the lesions histologically, and thus it is possible to have included a few rare cases of malignant rectal neuroendocrine tumors or melanoma, which may not share the same relevance with regard to the checklist elements. Lastly, data on long-term oncologic outcomes are unavailable in this database; however, CRM status has repeatedly demonstrated to be a strong indicator of recurrence-free survival and is often used as a surrogate.24,25

CONCLUSION

Compliance with 6 preoperative elements of the ASCRS rectal cancer surgery checklist is associated with significantly improved pathologic outcomes and reduced postoperative morbidity. The checklist should serve as an important resource for all surgeons who perform rectal cancer surgery to prevent the omission of important processes of care. Additional research should aim at validating the remaining elements of the checklist and correlating the checklist with long-term oncologic outcomes to further encourage its use and dissemination.

ACKNOWLEDGMENTS

The authors thank Georgia Rigas, Sarah Sabboobeh, Marie Demian, and Elektra McDermott for their editorial assistance.

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Keywords:

American Society of Colon and Rectal Surgeons; Checklist; Postoperative outcomes; Rectal cancer

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