Improving quality of care and clinical outcomes for rectal cancer through clinical audits in a multicentre cancer care organisation

Colorectal cancer is the third most common cancer worldwide and the second in Catalonia; 45% of these tumours are in the rectum [1, 2]. A locally advanced rectal tumour (LART) is defined by the presence of a neoplasm classified as T3/T4, with or without lymph node infiltration (N0/N+), and no metastatic dissemination. Treatment is multidisciplinary and consists of surgery plus radiochemotherapy [3], with careful evaluation of magnetic resonance imaging (MRI) parameters before and after preoperative treatment. The total mesorectal excision is a quality indicator, and the main factor for local control, but in LART the neoadjuvant treatment achieves greater control than surgery alone. Since the results of the Swedish Rectal Cancer Trial were published in 1997 [4], neoadjuvant, multimodal treatment has taken root as the standard treatment strategy. Substantial reductions in local recurrence have been achieved thanks to radiotherapy (RT), both short-course radiotherapy (SCRT) and long-course radiotherapy (LCRT), which is combined with chemotherapy. In historical series, local recurrence was 30 to 45%, compared with less than 10% today [5]. In 2019, multimodality treatment for LART also implies personalised strategies to decrease the surgical burden for patients responding after pre-operative treatment, including ‘wait and watch’ or organ-preservation approaches.

Thus, successful treatment of locally advanced rectal cancer requires a multidisciplinary approach [6, 7]. The complexity of care processes – and the resulting potential for variability in clinical decision-making – make monitoring highly desirable. Clinical audits, for their part, are a widely used instrument to identify variability in clinical practice and areas in need of improvement. Several countries have incorporated audits as a strategy to evaluate health policies [8, 9]. The impact of the results obtained depends to a large extent on the analysis of the outcomes, the quality of the data collected, and the credibility of the audit team. There are few studies that report the effects of corrective measures established based on post-intervention audits [10].

The aim of this study was to assess the effects of the quality improvement action plan on the quality of clinical care processes in patients with rectal cancer, with an emphasis on the diagnostic and neoadjuvant treatment phases.

Table 2 presents the characteristics of the patients included in the ACOR-1 and ACOR-2 cohorts. There were no significant differences in the demographic or clinical profiles, except in histological grade and distance from tumour to mesorectal fascia. Table 3 shows the outcomes for the diagnostic phase after implementing the action plan. Availability of the biopsy report reached 100% in patients in the second period, as did MRI staging in two of the three centres. The MRI reports met the established criteria in 77.5% of the cases, representing a significant rise with respect to the first period. In centre A, there were 10 cases where the report noted the distance from the tumour to the anorectal junction rather than the anal verge (these measures are considered equivalent with respect to the fulfilment of the standard).

The outcomes for the treatment phase are detailed in Table 4. The pattern of neoadjuvant treatment is similar between centres and in both cohorts. In ACOR-2, 62.7% of the patients received a total of 50.4 Gy (LCRT), a significant difference with respect to ACOR-1 that mainly reflects an improvement in centre A.

A protocol for managing treatment interruptions was approved in June 2017. Compliance was 9.7%; we did not observe a significant decrease in patients with prolonged OTT over seven days (in the case of LCRT) or in the percentage of patients who received their last dose on a Monday (radiotherapy units are not active on weekends). A protocol for image-guided radiotherapy was approved in October 2016; the compliance rate was 95.8%.

There was a significant increase in the performance of the MRI restaging procedure in all centres, from 32.5 to 61.3% (Table 5). The proportion of patients in whom surgery was indicated dropped slightly, from 96.7 to 90%, reflecting an increase in patients following a conservative treatment strategy. There was also a significant improvement in the availability of the ypCRM on the anatomical pathology report (ACOR-2: 94.4%).

For the follow-up phase, adverse effects of treatment were reported on 99.8% of the visits, and these were graded for severity according to the CTCAE in 36.2% of the cases.

Clinical audits are a well-known tool for identifying areas to improve in the care process. This study reports the results of an action plan for improving quality in neoadjuvant treatment for locally advanced rectal cancer in three centres, based on the findings of an initial quality audit. The ACOR-1 audit revealed variability in clinical practice between centres and showed suboptimal outcomes for several standard quality indicators. ACOR-2 showed the evolution of these indicators following the implementation of quality improvement measures.

In the diagnostic phase, the MRI is the best tool to identify the patients with locally advanced tumours who would most benefit from neoadjuvant treatment [14]. All the cases audited in ACOR-2 included this test, and there was a significant improvement in the quality of the report. Specifically, there was an increase in adherence to the Mercury Group’s recommendations on reporting rectal cancer MRIs [15], including the distance from the tumour to the mesorectal fascia (CRM), reported in 61.7% of the cases in ACOR-1 and 82.5% in ACOR-2, and the distance to the anal verge or the anorectal union, reported in 68.3 and 96.7% of the cases, respectively (p <  0.001). Overall, the centres did not achieve the optimal level of reporting (85%), but 77.5% of the reports in ACOR-2 did meet the established criteria, compared to just 45% in ACOR-1 – a significant change. We consider that having a proforma, which would include the state of the resection margin (CRM) and the distance from the tumour to the anal verge, would be a decisive factor in achieving optimal reporting, as described by Taylor and colleagues [18, 19].

The number of patients coming to the ICO-ICS unit with a diagnosis in hand increased significantly, probably due to the centralisation policies implemented for this pathology in the region [20]. All the cases diagnosed in the ICO unit were reviewed by a tumour board to approve the therapeutic strategy.

In ACOR-2, the treatment plan adopted most frequently was radiochemotherapy, with LCRT and a dose of 50.4 Gy. Compared with the outcomes observed in ACOR-1, ACOR-2 showed greater standardisation between centres and better adherence to the approved guidelines, although some variability persists, which is consistent with other studies [21]. For example, two of the centres used SCRT in 20% of the patients, while the other did so in just 5%. This difference is probably due to the divergent approaches in patients of advanced age. One centre adheres to the strategy for avoiding surgery in frail patients, so its adoption of LCRT is more assiduous. In contrast, the other two centres favour the avoidance of chemotherapy [22, 23].

We also noted an increase in the use of volumetric modulated arc therapy (VMAT), from 2.5 to 20.8% (p <  0.001), and its dissemination in all three centres. Although the radiated intestinal volume may be susceptible to late toxicity, VMAT reduces acute toxicity and consequently, treatment interruptions [16]. Thus, consensus-based indications were developed for patients with tumours that infiltrated into adjacent organs, and in general when treatment of the external iliac lymph nodes and/or the groin nodes is unavoidable.

One of the action plan’s target areas was OTT. Even though special efforts were made to improve this indicator, both audits showed that the overall RT treatment time was still more than seven days longer than planned for LCRT, usually because of weekday public holidays and technical inspections of the accelerators. There were no significant changes between study periods. We also observed a non-significant improvement in the percentage of patients whose last RT session was on a Monday. To improve this aspect, a protocol for managing treatment interruptions was designed and finally approved in June 2017. The delay in approval is probably the reason that we identified only seven patients in whom it was appropriately applied (four of them in centre B). Indeed, the included patients initiated treatment only from June to December 2017. Thus, the centres still have work to do in improving adherence to the treatment. As with any measure that affects the daily work routine and entails organisational changes, achieving success in this endeavour will be challenging [24].

Another target area was the standardisation of IGRT during treatment. This measure, too, was subject to a new protocol (approved in October 2016), and adherence was 95.8%.

Once the neoadjuvant treatment is finalised, restaging (primarily based on MRI) is necessary to define the surgical technique. We observed a significant rise in the adoption of this approach in all three centres, with 32.5% of all cases undergoing MRI restaging in ACOR-1 and 61.3% in ACOR-2 (p <  0.001). Moreover, there is already a consolidated scientific basis permitting selected patients to follow a conservative strategy and avoid surgery, that is, ‘watch and wait’ [25, 26]. In our case, in ACOR-2, surgery was indicated in 90% of the patients, compared to 96.7% in ACOR-1 (p = 0.035). In 3/12 patients (25%) in whom surgery was not indicated, the reason was having cT₀N₀ after completing chemoradiotherapy_.

Without a doubt, the most important quality indicator in neoadjuvant treatment of rectal cancer for local control and survival is the state of the circumferential resection margin (ypCRM). This detail was not described in the anatomical pathology report for 34.5% of the surgical specimens in ACOR-1, compared to 5.6% in ACOR-2 (p <  0.001). Overall, 14.8% of the surgical specimens showed CRM involvement (ypCRM+), which is consistent with the literature [27, 28]. Considering the RT strategy, 13% of the LCRT treatments had ypCRM+, compared to 25% of those with SCRT treatment. We considered the proportion of 10% to be optimal.

With regard to the low-quality reporting of adverse events over the clinical course (absence of grading and aspects related to sexual function or bowel control), the specific list of CTCAE (v 4.0) criteria [15] helped to moderately improve reporting. Nevertheless, the results obtained in ACOR-2 highlight the need to double down on efforts to improve this aspect.

The ultimate aim of treatment is not only to cure disease, but also to restore the person’s dignity and achieve their social reinsertion. To this end, it is essential to understand the impact of dysfunctions and symptoms derived from treatment on patients’ quality of life [29]. Future studies are necessary to explore this aspect in the long term, applying specific validated instruments like the EORTC questionnaires for quality of life in cancer patients and for colorectal quality of life in patients with rectal cancer receiving neoadjuvant treatment.

This study has several limitations. Some are related to the design of the audit, which included only 40 clinical histories per centre, limiting the power of the assessment, especially for clinical outcomes. In addition, the period selected (especially for the ACOR-2) allowed little time for the consolidation of changes derived from the action plan. Moreover, the data collected were from clinical histories; any measure taken but not recorded on the patient’s electronic medical record would, for the purposes of the clinical audit, be non-existent.

In conclusion, this study analyses the influence of feedback from clinical audit data in improving neoadjuvant treatment procedures in rectal cancer. Our results show progress as well as areas in which additional efforts should be made, including: decreasing the percentage of positive ypCRMs; limiting treatment interruptions in order to reduce overall treatment time; and better selection of therapeutic options in elderly patients, according to frailty and mobility. In short, the audit undertaken shows total or partial correction in most areas targeted for quality improvements following the first audit, a decrease in variability between centres, and an improvement in adherence to clinical practice guidelines for rectal cancer.