Surgical and Oncologic Textbook Outcomes in Abdominoperineal Resection for Rectal Adenocarcinoma. A Multi-Institutional Retrospective StudyAbstract
Introduction The incidence of low rectal adenocarcinoma has increased. Surgery plays an important role in achieving optimal outcomes. Measuring surgical and oncological quality parameters helps to identify variables that need correction and reduces costs.
Objective To evaluate the results of applying quality parameters known as textbook outcomes (TO) in abdominoperineal resection (APR) due to lower rectal adenocarcinoma.
Materials and Methods The variables comprising the surgical textbook outcomes (STO) and oncological textbook outcomes (OTO) were evaluated in 192 patients undergoing APR for rectal adenocarcinoma. Variables that affected compliance with quality measures were also analyzed.
Results Of the 192 patients, 37% met the STO and 37.5% met the OTO. Complications and R0 resections were the factors that most affected STO compliance. Minimally invasive surgery was associated with higher adherence compared to open surgery. Age over 65 years, transfusions, and incomplete mesorectal resection were variables associated with noncompliance.
Conclusion Noncompliance with TO is associated with a higher rate of recurrence. Implementing quality assessment through STO and OTO helps identify weak points in outcomes, target improvement interventions, and reduce costs.
Keywords
rectal adenocarcinoma; abdominoperineal resection; quality indicators; textbook outcome
Introduction
Rectal cancer incidence has increased globally in recent years. Similarly, a decrease in the age of onset has been noted, to the point that there are proposals to lower the age at which screening should begin.1,2 As part of a multimodal approach to rectal cancer, surgery remains the cornerstone of treatment, and total mesorectal resection is one of the most desirable prognostic variables.
Different surgical procedures and approaches are used to achieve adequate resection. These procedures are influenced by various factors, including rectal lesion location, the experience of the surgical team, adequate pre- and postoperative oncological management, the hospital's complexity etc.
Measuring the quality of rectal cancer surgery outcomes has primarily focused on single parameters such as morbidity, mortality, hospital stay, readmissions, number of resected lymph nodes, circumferential margins etc.1,3,4 These single measurements may be insufficient to reliably verify the quality of surgical treatment for rectal cancer.
In 2013, Kolfschoten et al.5 proposed a composite measurement of a group of known variables for colon cancer, which they called textbook outcomes (TO). These variables currently improve our assessment of surgical quality, to the point that some authors consider them “ideal”,4 using them as measurements in various pathologies.4,6-13 Rectal cancer has not been excluded from this trend, although many of these publications were based on national databases. These studies treat cases in different locations with different procedures, ranging from anterior resections to abdominoperineal resections (APR), ultra-low resections and anastomoses, colostomies etc., making it difficult to reach firm conclusions due to sample heterogeneity.1
In this sense, it is possible to implement two quality measures in the surgical treatment of rectal cancer: on the one hand, the surgical TO (STO), which measures the quality of the procedure itself, and on the other, and closely related to the first, the oncological TO (OTO), which measures the oncological quality of the resection, which will result in a longer survival time.14,15 As previously stated, the measurement of TO in the treatment of rectal cancer in most published studies involves different surgical procedures, making the samples heterogeneous. In our literature review, we did not find any studies assessing these quality measures exclusively in APR for low rectal adenocarcinoma.
The primary objective of this study was to evaluate the results of the composite measure of both surgical and oncological quality in patients with low rectal adenocarcinoma undergoing APR at three centers with experience in the management of this pathology. As a secondary objective, we evaluated other variables beyond the stated parameters that may be associated with TO noncompliance.
Materials and Methods
Patient Selection
All patients with low rectal adenocarcinoma aged 18 years and older who underwent APR between 2016 and 2024, collected from the three institutions, were initially eligible for this study. Pregnant women, patients with APR for anal cancer, or rectal tumors with a histology other than adenocarcinoma, as well as cases with incomplete data collection were excluded. Patients were studied regarding tumor markers, colonoscopy, computed tomography (CT), and magnetic resonance imaging (MRI). All patients were discussed in a tumor committee, where the therapeutic strategy was decided, including the use of neoadjuvant therapy. All patients signed informed consent, and their data are available.
Data Evaluated
Demographic data, tumor characteristics (size and extension, rectal walls involved, neoadjuvant therapy etc.), the approach used (open, laparoscopic, or robotic), data regarding the surgery (operative time, need for blood product transfusion, associated resections, number of lymph nodes resected, margin involvement, total resection of the mesorectum etc.), and data related to the postoperative and follow-up were collected. Complications were stratified according to the Clavien-Dindo classification.16 Overall patient survival was recorded from the day of surgery to the day of death or the last visit to the clinic, measured in months.
Neoadjuvant chemo- and radiotherapy were used in patients with stage T3/N +, while in T4 and/or N2 patients, chemotherapy was preferably administered with a FOLFIRINOX regimen based on their performance status. Surgery was performed between the 8th and 12th weeks after neoadjuvant therapy. Complete resection of the mesorectum was assessed by the surgeon and the pathologist; any doubts about its integrity were interpreted as incomplete.
Resection margins were measured in centimeters by the pathologist, and a circumferential free margin of 1 mm was considered sufficient. To consider a resection R0, all three margins had to be disease-free. Tumor location was also assessed based on its primary location on one of the rectal surfaces or involvement of the entire circumference to evaluate whether this variable confirms that tumors located on the anterior surface could affect the oncological outcome.
Parameter Definition Textbook
Patients were defined as TOQ if they met all of the following parameters: hospital stay of less than 14 days; no readmission within 30 days; no surgical, endoscopic reinterventions; free resection margins; no complications.
The definition of OLT included compliance with the following parameters: hospital stay of less than 14 days; no readmission within 30 days; neoadjuvant treatment; R0 resection; resection of 12 or more lymph nodes.
Statistical Analysis
A retrospective, multicenter study was conducted, prospectively collected from three healthcare institutions, including a total of 192 patients undergoing APR for rectal adenocarcinoma. Sociodemographic and clinical variables were summarized using absolute and relative frequencies for categorical variables. For continuous variables, measures of central tendency and dispersion (mean, median, standard deviation, and interquartile range) were calculated according to the empirical distribution of each variable.
To identify factors associated with data inclusion in oncology (yes/no) and surgical (yes/no) registries, modified Poisson regression models with robust variance estimation were used. This approach allows for direct estimation of prevalence ratios (PRs), providing a more precise and interpretable measure of association than logistic regression when the outcome is binary and relatively common. Exponential coefficients derived from those models were interpreted as prevalence ratios rather than incidence rate ratios.
All analyses were performed using RStudio IDE (Posit PBC), v. 2024.12.1. A p-value < 0.05 was considered statistically significant. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines were used for this study.
Results
Patient Selection
During the study period, 220 APR were performed at the three centers. Of these, 28 (12.8%) patients were excluded, 22 because they were performed for anal squamous cell carcinoma, 1 for rectal melanoma, 2 for tumors of types other than adenocarcinoma, and 3 for lack of necessary data. This resulted in 192 patients, who constitute the study population.
Data Evaluated
Of the 192 patients, 68% were male, with a mean age of 65.2 years. The laparoscopic approach was the most frequently used in 49.7% of patients, followed by the open approach, and finally the robotic approach.
Other demographic and clinicopathological variables analyzed can be seen in Table 1. These included simultaneous resection of lesions, mainly hepatic (29%), the need for blood product transfusion (15%), and a complication rate of 51%, with Clavien-Dindo types 1 and 2 being the most frequent. Complete dissection of the mesorectum was achieved in 84% of patients, the average number of resected lymph nodes was 18, and resection of 12 or more lymph nodes was completed in 78% of patients. Operative mortality at 30-days occurred in 5 patients (2.6%). Margins (proximal + distal + circumferential) were clear in 75.5% of cases.
The 5 STO criteria were met by 71 patients (36.98%), and the OTO by72 patients (37.5%), as presented in Table 1. Within the STO, 53 patients met at least 4 criteria, while in the OTO, 73 (38%) met the same number.
Table 2 shows the criteria used and their compliance. Within the surgical criteria, complications were the main factor for noncompliance, while within the oncological criteria, it was R0 resection.
When investigating which variables other than those used to measure compliance with the textbook outcome led to noncompliance with quality parameters, we observed the that in STO, patients over 65-years-old, those who received blood product transfusions, and those with incomplete mesorectal resection showed a statistically significant association. Furthermore, noncompliance with the STO was associated with a clear recurrence rate (Table 3).
Regarding OTO, age over 65 years and incomplete mesorectal resection were shown to be the variables most associated with noncompliance (Table 4 and Fig. 1), while the minimally invasive laparoscopic approach was associated with greater compliance with quality criteria. This last variable has a greater difference before the age of 65 years. In patients older than that age, the three pathways tend to be associated with compliance with a smaller difference, as can be seen in Figure 2. Circumferential location of the tumor on the anterior face and operative time were not variables associated with noncompliance with the TO.
Discussion
In recent years, there has been a growing interest in hospital safety and quality of care, especially for cancer patients. Hospital accreditation systems that use composite quality measures and address variables that combine outcome measures (infection, complications, survival etc.) with structural and organizational ones promote environments of safety and quality.17
The use of composite measures such as textbook outcomes favors better outcomes in patients undergoing oncologic surgery, improving hospital stay, the number of complications, and survival.14,17 Obtaining the aforementioned outcomes impacts healthcare system costs, which are a difficult problem to manage.4
The measurement of textbook outcomes in colorectal cancer surgery is increasing, and although most authors recommend their use, there are factors not incorporated into the measurement parameters that may influence their results. These include environmental factors, race, and social vulnerability; it was observed that patients with these variables had poorer adherence to TO.6,18
There are few studies addressing TO measurement in rectal cancer,1,3,19 and only one of them addresses patients with lower rectal cancer, although this multicenter study included different surgical procedures.3
Although there is no universal definition of TO, we used one measurement for surgical outcomes and another for oncological outcomes.1,20 Both measurements are closely related, and adherence to both will result in improved survival and lower costs.
In our evaluation, the STO was met in 37% of patients, and the OTO in 37.5%. Compliance in rectal cancer is generally reported to be around 50%, but the studies incorporate different types of resections. When these results are analyzed in detail, we can observe that the rates for patients who underwent nonsphincter-preserving surgery are similar to those reported in this study.3,19 The APR is complex than sphincter-preserving surgery, so it is expected that in the overall comparison of rectal resections it will have worse outcomes. Low anterior resection syndrome after sphincter-preserving surgery appears to be the problem to be solved.21
Among the parameters measured in STO, complications are the most common factor for noncompliance. This coincides with the majority of studies and is justified, as mentioned above, by the complexity involved in the abdominal and perineal approach. On the other hand, R0 resection was the leading factor for noncompliance within OTO. Undoubtedly, incomplete tumor resection will have a negative impact on patients' oncological prognosis. Complications, the number of resected lymph nodes, and R0 resections are also some of the parameters mentioned in the literature.1,8
The use of neoadjuvant radiotherapy has been reported as one of the main causes of a decrease in the number of dissected lymph nodes below the recommended limit. Although the incorporation of neoadjuvant radiotherapy as a compliance variable within OTO may be debatable, its use is qualitatively important, since the decrease in tumor size and lymph node reduction demonstrated with its use are factors that favor better outcomes. Multiple variables have been associated with noncompliance according to the TO, among these are patients older than 75 years, multivisceral resections, surgery in tertiary level hospitals, race, stage, conversion to open surgery, ASA, BMI etc.1,14,19
Regarding resections of other viscera in our study, it was not a variable favoring noncompliance; we believe that R0 resection is actually the variable that will favor compliance with the TO. On the other hand, it is interesting that some tertiary level or high volume hospitals have been considered negative factors19 in compliance with the TO, although these authors basically refer to the way of collecting the data, there is the possibility that since they are reference centers for this surgery, the complexity of the cases is greater compared to low volume hospitals and, therefore, the rate of complications, readmissions, and hospital stay is greater, directly affecting compliance with the criteria. In any case, we agree with Bos et al., who mentions that those centers with high volume (> 20 resections per year) have better results than less experienced centers.22
In our study, patients over 65-years-old and those with incomplete mesorectal resection were the variables outside the measured parameters that were associated with TO noncompliance in both groups. Transfusions were a factor associated with STO noncompliance. In another sense, minimally invasive surgery was shown to be a variable associated with compliance with STO, mainly represented by the laparoscopic approach. This is consistent with most of the literature consulted, where minimally invasiveness, decreased blood loss, and decreased hospital stay would be the pillars on which this advantage is based. This can also be applied to robotic surgery, which does not seem to differ from the laparoscopic approach.23-26
One point we have not evaluated but that could favor the minimally invasive approach over the open approach is the case-specific selection of treatment. It is likely that more complex cases are treated openly, while less complex cases are treated with a minimally invasive approach, favoring the presence of bias at the time of comparison. After age 65, the three approaches show compliance curves that are closer to each other. It is difficult to find an explanation for this behavior, which could be due to older patients' lower compliance with the STO than to the approach itself. Another interesting and logical finding of our study was that noncompliance with the STO was associated with a higher recurrence rate, which definitely represents an outcome directly related to the quality of the procedure.
Although the definition of the criteria that should be incorporated into the assessment of TO remains a matter of debate, the use of composite quality measures appears to be the best way to improve the quality of care for patients undergoing cancer surgery, in this case, low rectal adenocarcinoma. The results obtained from measuring the STO and OTO do not differ in terms of APR from those published by other authors, even though these series mostly address rectal tumors at different levels.
Conclusion
This study has weaknesses, including, first, that it is a retrospective study; second, that the patients were treated by different surgical teams in different centers with varying complexities; and third, that some variables could not be measured due to lack of data and therefore could not be compared. As a strength, this study is, to our knowledge, the first to assess STO and OTO in the literature search conducted on APR solely for low rectal adenocarcinoma, avoiding the data heterogeneity from other studies. It also provides valuable data regarding compliance with composite quality measures and, primarily, the factors that could cause these measures to fail (complications, R0 etc.), which would initially allow for the development of targeted improvement interventions.
Data Availability
Data will be available upon request to the corresponding author.
References
-
1 Naffouje SA, Ali MA, Kamarajah SK, White B, Salti GI, Dahdaleh F. Assessment of textbook oncologic outcomes following proctectomy for rectal cancer. J Gastrointest Surg 2022;26(06): 1286–1297. Doi: 10.1007/s11605-021-05213-9
» https://doi.org/10.1007/s11605-021-05213-9 -
2 Sofia S, Degiuli M, Anania G, et al. Textbook outcome in colorectal surgery for cancer: An Italian version. J Clin Med 2024;13(16): 4687. Doi: 10.3390/jcm13164687
» https://doi.org/10.3390/jcm13164687 -
3 Sun Y, Jiang W, Tang Z, Wang X, Huang Y, Chi P. Textbook outcome in low rectal cancer after neoadjuvant chemoradiotherapy: Post hoc analysis of the LASRE randomized clinical trial. Eur J Surg Oncol 2024;50(09):108519. Doi: 10.1016/j.esjo.2024.108519
» https://doi.org/10.1016/j.esjo.2024.108519 -
4 Aquina CT, Hamad A, Becerra AZ, et al. Is textbook oncologic outcome a valid hospital-quality metric after high-risk surgical oncology procedures? Ann Surg Oncol 2021;28(13):8028–8045. Doi: 10.1245/s10434-021-10478-0
» https://doi.org/10.1245/s10434-021-10478-0 -
5 Kolfschoten NE, Kievit J, Gooiker GA, et al. Focusing on desired outcomes of care after colon cancer resections; hospital variations in ‘textbook outcome’. Eur J Surg Oncol 2013;39(02):156–163. Doi: 10.1016/j.ejso.2012.10.007
» https://doi.org/10.1016/j.ejso.2012.10.007 -
6 Hyer JM, Tsilimigras DI, Diaz A, et al. High social vulnerability and "textbook outcomes" after cancer operation. J Am Coll Surg 2021;232(04):351–359. Doi: 10.1016/j.jamcollsurg.2020.11.024
» https://doi.org/10.1016/j.jamcollsurg.2020.11.024 -
7 Kulshrestha S, Bunn C, Patel PM, et al. Textbook oncologic outcome is associated with increased overall survival after esophagectomy. Surgery 2020;168(05):953–961. Doi: 10.1016/j.jsurg.2020.05.038
» https://doi.org/10.1016/j.jsurg.2020.05.038 -
8 Mac Curtain B, Qian WO, Mahoney A, et al. "Textbook Outcome (s)" in colorectal surgery: a systematic review and meta/analysis. Ir J Med Sci 2024;193(05):2187–2194. Doi: 10.1007/s11845-024-03747-w
» https://doi.org/10.1007/s11845-024-03747-w -
9 Sweigert PJ, Eguia E, Baker MS, et al. Assessment of textbook oncologic outcomes following pancreaticoduodenectomy for pancreatic adenocarcinoma. J Surg Oncol 2020;121(06): 936–944. Doi: 10.1002/jso.25861
» https://doi.org/10.1002/jso.25861 -
10 Merath K, Chen Q, Bagante F, et al. A multi-institutional international analysis of textbook outcomes among patients undergoing curative-intent resection of intrahepatic cholangiocarcinoma. JAMA Surg 2019;154(06):e190571. Doi: 10.1001/jamasurg.2019.0571
» https://doi.org/10.1001/jamasurg.2019.0571 -
11 Van Roessel S, Mackay TM, Van Dieren S, et al; Dutch Pancreatic Cancer Group. Textbook outcome: nationwide analysis of a novel quality measure in pancreatic surgery. Ann Surg 2020;271(01): 155–162. Doi: 10.1097/SLA0000000000003451
» https://doi.org/10.1097/SLA0000000000003451 -
12 Wiseman JT, Ethun CG, Cloyd JM, et al. Analysis of textbook outcomes among patients undergoing resection of retroperitoneal sarcoma: A multi-institutional analysis of the US Sarcoma Collaborative. J Surg Oncol 2020;122(06):1189–1198. Doi: 10.1002/jso.26136
» https://doi.org/10.1002/jso.26136 -
13 Denbo J, Anaya DA. Textbook outcomes following liver resection for cancer: a new standard for quality benchmarking and patient decision making. Ann Surg Oncol 2020;27(09):3118–3120. Doi: 10.1245/s10434-020-08550-2
» https://doi.org/10.1245/s10434-020-08550-2 -
14 Kryzauskas M, Bausys A, Abeciunas V, et al. Achieving textbook outcomes in colorectal cancer surgery is associated with improved long-termsurvival: results of the multicenter prospective cohort study. J Clin Med 2024;13(05):1304. Doi: 10.3390/jcm13051304
» https://doi.org/10.3390/jcm13051304 -
15 Russolillo N, Gentile V, Ratti F, et al. Incidence and predictors of textbook outcome after simultaneous liver and rectal surgeries for Stage IV rectal cancer. Colorectal Dis 2022;24(01):50–58. Doi: 10.1111/codi.15912
» https://doi.org/10.1111/codi.15912 -
16 Dindo D, Demartines N, Clavien PA. Classification of surgical complications. A new proposal with evaluation in a cohort of patients and results of a survey. Ann Surg 2004;240(02): 205–213. Doi: 10.1097/01.sla.0000133083.54934.ae
» https://doi.org/10.1097/01.sla.0000133083.54934.ae -
17 Mehta R, Tsilimigras DI, Paredes A, et al. Assessment of hospital quality and safety standards among Medicare beneficiaries undergoing surgery for cancer. Surgery 2021;169(03):573–579. Doi: 10.1016/j.surg.2020.10.003
» https://doi.org/10.1016/j.surg.2020.10.003 -
18 Shaikh CF, Woldesenbet S, Munir MM, et al. Association between the environmental quality index and textbook outcomes among Medicare beneficiaries undergoing surgery for colorectal cancer (CRC). J Surg Oncol 2023;127(07):1143–1151. Doi: 10.1002/jso.27229
» https://doi.org/10.1002/jso.27229 -
19 Warps A, Detering R, Tollenaar R, Tanis P, Dekker JDutch ColoRectal Audit Group. Textbook outcome after rectal surgery as composite measure for quality of care: a population-based study. Eur J Surg Oncol 2021;47(11):2821–2829. Doi: 10.1016/j.ejso.2021.05.045
» https://doi.org/10.1016/j.ejso.2021.05.045 -
20 Aiken T, Abbott DE. Textbook oncologic outcome: A promising summary metric of high-quality care, but are we on the same page? J Surg Oncol 2020;121(06):923–924. Doi: 10.1002/jso.25872
» https://doi.org/10.1002/jso.25872 -
21 Tudela ACd, Marinello F, Basany EE. And after surgery, what's new for the rectal cancer survivor? Cir Esp 2025;103(04):237–243. Doi: 10.1016/j.ciresp.2024.01.001
» https://doi.org/10.1016/j.ciresp.2024.01.001 -
22 Bos ACRK, Van Erning FN, Elferink MAG, et al. No difference in overall survival between hospital volumes for patients with colorectal cancer in the Netherlands. Dis Colon Rectum 2016;59(10):943–952. Doi: 10.1097/DCR0000000000000660
» https://doi.org/10.1097/DCR0000000000000660 -
23 Jiang WZ, Xu JM, Xing JD, et al; LASRE trial investigators. Shortterm outcomes of laparoscopy-assisted vs open surgery for patients with low rectal cancer: The LASRE randomized clinical trial. JAMA Oncol 2022;8(11):1607–1615. Doi: 10.1001/jamaoncol.2022.4079
» https://doi.org/10.1001/jamaoncol.2022.4079 -
24 Fleshman J, Branda M, Sargent DJ, et al. Effect of laparoscopicassisted resection vs open resection of stage II or III rectal cancer on pathologic outcomes: the ACOSOG Z6051 randomized clinical trial. JAMA 2015;314(13):1346–1355. Doi: 10.1001/jama.2015.10529
» https://doi.org/10.1001/jama.2015.10529 -
25 Van der Pas MH, Haglind E, Cuesta MA, et al; COlorectal cancer Laparoscopic or Open Resection II (COLOR II) Study Group. Laparoscopic versus open surgery for rectal cancer (COLOR II): shortterm outcomes of a randomised, phase 3 trial. Lancet Oncol 2013;14(03):210–218. Doi: 10.1016/S1470-2045(13)70016-0
» https://doi.org/10.1016/S1470-2045(13)70016-0 -
26 Tang B, Lei X, Ai J, Huang Z, Shi J, Li T. Comparison of robotic and laparoscopic rectal cancer surgery: a meta-analysis of randomized controlled trials. World J Surg Oncol 2021;19(01):38. Doi: 10.1186/s12957-021-02128-2
» https://doi.org/10.1186/s12957-021-02128-2
Edited by
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Editor-in-Chief:
Henrique Sarubbi Fillmann.
