Introduction

In 2007, a German expert group published a set of quality indicators for the diagnosis and treatment of rectal cancer [1]. The group also proposed benchmarks for each indicator with a clear definition of the numerator and denominator. Thus, a set of 36 quality goals was defined. The feasibility of these quality indicators could be proven by several groups specializing in rectal cancer care [2, 3]. We were also able to give positive proof of the practicability of the quality goals for a consecutive series of patients treated for rectal cancer from 2000 to 2008 [4].

In 2008, the German Ministry of Health together with two German cancer societies and the working group of German tumour centres agreed on a national cancer plan including the strategy that patients with common cancer entities such as colorectal cancer should be treated in certified centres to ensure a high standard of care [5]. Following the instructions of this strategy, our unit was certified in May 2008 by the German Society of General and Visceral Surgery and by the German Cancer Society in 2011. Preconditions for certification were several measures of quality assurance, implementation of structured workflows, and annual external audits [6, 7]. Certification of the German Cancer Society mandated the nomination of at least two specialized colorectal cancer surgeons with a minimum of 10 rectal resections per year [7].

However, the impact of establishing certified centres for colorectal cancer on patient outcomes is difficult to assess and data that prove the benefit is scarce [8]. We hypothesized that implementation of a certified centre improves predefined quality parameters. In order to assess this, we compared the group of rectal cancer patients treated within the structure of a certified colorectal unit with a patient group treated before and documented in an identical manner [4]. The comparison was done using the detailed quality indicators of the German working group [1]. The primary endpoint of the study was the number of achieved quality goals. The secondary endpoint was the comparison of the two groups with respect to every single quality goal.

Patients and methods

Prospective tumour documentation for colorectal cancer patients was established as early as 1981 in our unit by means of a coloproctologic database. It is based on international standards [9, 10] and has been continuously improved over the years taking into account developments in diagnostics, treatment, and refinements in classification. Tumour, node, and metastasis (TNM) classification was done according to the valid edition of the International Union against Cancer (UICC) classification [11,12,13]. Follow-up is organized in a coloproctologic clinic were patients are seen annually for 5 years and biannually thereafter up to 10 years. Written informed consent for follow-up and inquiries is obtained at the outset of treatment. Further details of follow-up have been published previously [14]. According to national regulations, no formal approval of the responsible institutional review board is necessary for this kind of study.

All rectal cancer patients treated from January 2009 until December 2017 were retrieved from the database. Patients with a histologically proven primary adenocarcinoma of the rectum (≤ 16 cm from the anal verge as measured by rigid rectoscopy) were included. Carcinoma in situ was the only exclusion criterion. To provide an overview of potential confounders, we performed a comprehensive comparison of the baseline demographic, clinical, treatment, and pathological parameters. Data was analyzed according to the definitions of the German Working Group and are detailed in the respective tables [1]. Missing data are indicated with the results; the denominator was decreased accordingly. Proportions for the quality indicators are given as percentages with 95% confidence intervals (CI). Local recurrence and overall survival rates were calculated with the Kaplan–Meier method. The starting point for the estimation of local recurrences was the date of operation. However, the starting point for survival analysis was the date of diagnosis to include the time of neoadjuvant therapy. In both calculations, postoperative mortality was excluded. Postoperative mortality was defined as in-hospital death independent of the length of stay, according to the definition of the Working Group [1]. The calculation of cumulative local recurrence rates is not influenced by postoperative mortality [15]. In overall survival, exclusion of postoperative mortality reflects the tumour-related prognosis that can be achieved for the patient according to the chosen treatment [16]. The last follow-up for calculation of recurrence rates and survival analysis was set on 26 March 2019. Patients without known local recurrence or death at 5 years were censored accordingly.

This was in accordance with our previous analysis conducted for patients treated from 2000 until 2008 [4] to ensure a high comparability between the groups. Subsequently, the two groups were compared applying either the χ2 test or the Fisher exact test for categorical variables. To illustrate trends over time, we displayed annual proportions of indicators that showed a statistically significant difference with a linear regression graph fitted for each time period. The log-rank test was applied to local recurrence and survival rates. A p value of < 0.05 was considered significant. For statistical analysis, SPSS V 25 (IBM Corp., Armonk, NY) was used.

If the result for each quality goal was within the range of the predefined benchmark, the goal was counted as achieved. For indicator 5b (tumour removal clinical stages I–II), the benchmark was interpreted as ≥ 90% without upper limit, because the rationale for an upper limit was not clear. Indicator 7b (neoadjuvant treatment depending on MR-assessed infiltration of potential CRM) describes a peculiar situation and applied in our series only to patients treated within the OCUM trial [17, 18]. It was summarized in indicator 7a. If only the 95% CI comprised the benchmark, the goal was counted as nearly achieved [2]. Indicators with six or fewer patients in the denominator were not assessed for the achievement of the benchmark.

The study, although retrospective in nature, is based on prospective data and has a longitudinal character regarding the implementation of a certified centre.

Results

For the time period from 2009 until 2017, we identified 481 patients with histologically proven adenocarcinoma of the rectum (334 males, 147 females) from the database. The median age of the study population was 68 (range 36–93) years. Median follow-up was 53.0 (range 1–128) months with 23 (4.8%) patients lost to follow-up. In comparison with the 2000–2008 group, there were significantly more patients with an elevated CEA level (39.1% vs. 28.4%, p < 0.001) and with clinical stages III (53.3% vs. 34.7%, p < 0.001) and IV (26.9% vs. 16.8%, p < 0.001). The proportion of patients who did not undergo tumour resection remained stable (13.5% vs. 13.8%, p = 0.877) as did the proportion of sphincter preserving radical operations (62.1% vs. 57.3%, p = 0.169). The proportion of intersphincteric resections, however, increased significantly (6.0% vs. 2.1%, p = 0.001), while the proportion of abdominoperineal excisions (APE) decreased (13.7% vs. 17.3%, p = 0.070). Neoadjuvant therapy was administered in 57.8% vs. 43.3% (p < 0.001). Adjuvant radio(chemo)therapy almost disappeared (1.7% vs. 12.0%, p < 0.001) owing to the shift towards neoadjuvant therapy in the 2004 guidelines [19]. Pathologic parameters, especially TNM classification, were difficult to compare because of the different proportions of neoadjuvant therapy in the two time intervals. However, we observed a significant decrease of the pUICC stage I (16.1% vs. 25.5%, p = 0.001). The proportion of poorly differentiated carcinomas was significantly lower in the 2009–2017 group (15.5% vs. 23.4%, p = 0.003). In neoadjuvantly treated patients, the proportion of complete tumour regression according to Dworak [20] did not change significantly (14.2% vs. 17.2%, p = 0.389). Further patient and tumour characteristics are given in Tables 1, 2 and 3.

Table 1 Pretreatment characteristics
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Table 2 Treatment characteristics
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Table 3 Pathologic characteristics*
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Overall, 25 of the 36 quality goals could be achieved in the 2009–2017 period. The set of achieved goals comprised as important goals as postoperative mortality in elective (0.8%) and emergency (14.3%) operations, pathologic CRM (only 2.5% positive), cumulative local recurrence rate at 5 years for stages (y)p0–III (4.6%) and almost all survival parameters (Tables 4, 5, 6 and 7). The 5-year overall survival for stages (y)p0–III was 80.2%.

Table 4 Quality indicators for diagnostics of rectal carcinoma
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Table 5 Indicators of process quality of therapy
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Table 6 Indicators for the outcome quality of therapy: surrogate indicators
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Table 7 Indicators for the outcome quality of therapy: definitive indicators
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In the 2009–2017 group, 6 more quality goals could be achieved than in the 2000–2008 group. Amongst the improved quality indicators are the proportion of anastomotic leaks in anastomoses up to 7 cm from the anal verge (13.5% vs. 22.1%, p = 0.018) and the local recurrence rate of stage (y)pIII rectal cancers (7.7% vs. 17.8%, p = 0.085; Fig. 1). Furthermore, the quality of mesorectal excision improved significantly (0.3% incomplete resections vs. 5.5%, p = 0.002). For the proportion of APE in rectal cancers of the lower third, no benchmark was defined, but we could show a significant decrease from 60.0% to 47.1%, p = 0.037. Trends over time are displayed for proportions of both anastomotic leaks and APE in Figs. 2 and 3.

Fig. 1
figure 1

Cumulative local recurrence rates for UICC stages (y)pIII. Five-year local recurrence rate for time period 2000–2008 (n = 106) = 17.8% and for time period 2009–2017 (n = 96) = 7.7% (p = 0.085). R0-resected patients only, postoperative mortality excluded

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Fig. 2
figure 2

Annual proportions of anastomotic leaks (AL). The dotted line marks the implementation of the certified centre. The red lines represent linear regression curves for each time period. Note: In 2006, 2017 and 2018, the proportion of AL was zero

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Fig. 3
figure 3

Annual proportions of abdomino-perineal excisions (APE) for rectal cancers of the lower third. The dotted line marks the implementation of the certified centre. The red lines represent linear regression curves for each time period. Note: In 2013, the proportion of APE was zero

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Another 5 quality goals were nearly achieved and only 4 quality goals were missed in 2009–2017. Missed goals included the proportion of specimens with ≥ 12 retrieved lymph nodes. Whereas the proportion remained stable for patients without neoadjuvant radio(chemo)therapy (76.6% vs. 76.4% in 2000–2008), it improved for patients after neoadjuvant therapy (58.2% vs. 45.7%, p = 0.120). We could not detect differences in overall survival, neither in the 2009–2017 group (73.3% for < 12 lymph nodes vs. 78.2% for ≥ 12 lymph nodes, p = 0.306), nor in the 2000–2008 group (69.6% for < 12 lymph nodes vs. 73.8% for ≥ 12 lymph nodes, p = 0.581).

Overall, the quality of documentation increased with the quality of mesorectal excision and pathologic CRM completely documented and urinary catheter newly documented in the 2009–2017 period. In the 2000–2008 group, three goals could not be evaluated; in the current group, this applied to two goals.

Discussion

Our study shows that despite starting from a high level, further improvements in the quality of rectal cancer treatment are possible with the implementation of a certified centre. Improved key indicators were the local recurrence rate for stage (y)pIII tumours and the anastomotic leak rate in low anastomoses. Furthermore, we could decrease the proportion of abdominoperineal excisions.

The reasons for improvement are complex and multifactorial, with causal factors for singular developments difficult to specify. However, certification as a centre necessitates the implementation of a whole bundle of measures aimed at improving the structure, process and outcome quality. These measures include the regular discussion of all rectal cancer patients in the multidisciplinary team (MDT), quality meetings at a regular base and annual audits [7, 23,24,25]. Furthermore, every elective operation must be done or supervised by a specialized surgeon, and a certain percentage of patients must be included in registered clinical studies.

Local recurrence

Local recurrence is the key quality indicator of rectal cancer treatment with major improvements within the last decades. The most important step towards an overall local recurrence rate of below 10% was the embryology-based surgical technique with the introduction of total mesorectal excision [26, 27]. This approach was supplemented by extralevator abdominoperineal excision (ELAPE) for very low-lying tumours [28,29,30]. Both steps were flanked by a critical pathological work-up of the specimens resulting in measurements of the CRM and specimen grading [31,32,33]. Additionally, the assessment of the tumour in relation to the potential CRM became available with improved MRI techniques [34,35,36]. These diagnostic measures gave a stimulating feedback to the surgeon. The nomination of specialized surgeons very likely accelerated the improvement of surgical quality [37,38,39]. Furthermore, multidisciplinary management with (neoadjuvant) radio(chemo)therapy was able to further halve local recurrence rates [40, 41].

The low local recurrence rate for all tumours in our series reflects the implementation of these developments. In particular, the improvement of local recurrences in stage (y)pIII tumours might be a result of regular discussion at our MDT with a tailored approach to these advanced tumours [42]. In the high-risk group, however, this positive trend was offset by a rather high local recurrence rate in stage (y)pII. Local recurrence in the latter stage depends heavily on the proportion of (y)pT4N0 to (y)pT3N0 tumours. In our series, the percentage of (y)pT4N0 tumours was double as high (7.9%) in 2009–2017 than in 2000–2008 (3.8%).

Overall, our recurrence rates compare favourably with the literature (cumulative 5-year local recurrence rate for stages (y)p0–III 4.6% (2009–2017 period) in our series compared with 3.5–10.6% [2, 3, 43]).

Anastomotic leak

The rather high anastomotic leak rate in our previous study induced a permanent discussion at the quality meetings with the successive implementation of measures that lead to stepwise improvement of the leak rate. Amongst these measures were the training of junior surgeons in the handling of stapling devices and the introduction of oral antibiotics in preoperative bowel preparation. Again, the increased case load of the specialized surgeons may also have contributed to the success. Reduction of anastomotic leak rates has been reported by various groups that analyzed the benefit of surgical specialization [44, 45].

Proportion APE

A further observation of our study is that the proportion of APE for tumours of the lower third of the rectum could significantly be reduced from 60.0 to 47.1%. Many factors have contributed to this development as the better MRI assessment of tumours of the lower third with high-resolution MRI and criteria according to the Low Rectal Cancer (MERCURYII) study [36] and surgical specialization [38, 46, 47]. Apart from surgical improvements and the oncologic feasibility, there are nowadays functional scores at hand that allow a proper counselling of patients in the decision-making process if an ultralow anterior/intersphincteric resection is discussed against an APE [48]. In our patient cohort, only very few patients declared that a permanent stoma would have been the better choice indicating an appropriate patient selection [49].

Pathologic CRM

The most important surrogate prognostic parameter is the free pathologic CRM [32]. It reflects various parameters of process quality such as exact MRI assessment of the primary tumour (and its lymph nodes) in relation to the mesorectal fascia, the correct decision-making of the MDT with respect to neoadjuvant therapy, the quality of re-assessment after neoadjuvant therapy and the quality of surgery including strategies to extend the operation in areas where the mesorectal fascia is infiltrated [50,51,52,53]. It strongly correlates to local recurrence and was chosen as the study endpoint in many important studies [36, 54,55,56]. Recent studies have reported a pathologic CRM involvement in 5.4 to 10% [51, 57, 58]. In our series, it improved from 5.2 to 2.5% and was in both time periods well below the target value of < 10%.

Survival

Survival data also improved favourably. Especially in stages (y)pIII, overall survival at 5 years improved from 60.7 to 69.4% and was well beyond the benchmark of 55%. The reasons for this development are similar to those given for the improvement of local recurrence rates [59, 60]. Furthermore, trends as advanced liver surgery, peritoneal surface surgery with hyperthermic intraperitoneal chemotherapy (HIPEC), the availability of targeted therapy, radiofrequency ablation (RFA) and selective intracorporal radiotherapy (SIRT) have contributed to improved survival in those patients who develop metachronous metastases. The benchmark was only nearly achieved for stages (y)p0–I. The cause for the latter is not quite clear; only 3 of the 13 events in the 2009–2017 group (n = 133) were tumour-related.

Urinary function

The newly documented quality indicator was urinary function. Data that would allow a reasonable benchmark are rare in the literature. We noticed that 6.8% of patients were discharged with a permanent urinary catheter (suprapubic and urethral combined), which is well below 10%. Merkel et al. reported a proportion of 5.8% in the most recent patient group of their study [2]. Therefore, the proposed target value seems to be reasonable; however, it does not take T4 tumours with the possible need to remove the pelvic side wall compartment and the ensuing inevitable damage to autonomic nerves into account.

Retrieved lymph nodes

The number of retrieved lymph nodes was amongst the quality goals that were not achieved. While the proportion of patients with ≥ 12 investigated lymph nodes improved considerably in patients after neoadjuvant radio(chemo)therapy, it remained stable for patients without neoadjuvant treatment. Lymph node detection is an indicator of both surgical and pathological quality. As a direct effect of external auditing and measures taken to enhance the number of retrieved lymph nodes, we could indeed detect a continuous improvement in the last few years; however, for the entire 2009–2017 period, it was not sufficient for an achievement or near achievement of the goal.

A number of studies indicate that lymph node retrieval is a prognostic factor with respect to survival [61,62,63,64]. There is, however, some controversy in the literature as to the threshold of examined lymph nodes, which was given at a range of 8–9 in some studies [65,66,67]. The impact of lymph node yield after neoadjuvant CRT is also not yet clear, because preoperative treatment may well result in complete disappearance of lymph nodes [68,69,70]. For ypN0 cancers, no correlation of survival with number of retrieved lymph nodes was found [67, 71, 72]. We could not detect a significant difference in survival for patients with less than 12 examined lymph nodes compared to the group with ≥ 12 nodes in our series. It may well be that a stable surgical quality can compensate the drawbacks that might result from a limited lymph node retrieval [73,74,75].

The strength of our study is the completeness and quality of our database, which enabled us to analyze our quality parameters shortly after the set of quality indicators was published in 2007. The availability of a level 3 guideline and its full implementation in daily clinical practice [19] coincided with the certification of our unit as a coloproctologic/bowel cancer centre. Thus, phase 2 of the study reflects the adherence to guidelines and the results achievable with this strategy. The implementation of a certified centre in 2008 can be seen as an “intervention,” and the following time period mirrors the effect of it. There are only minor changes in the two patient groups as reflected by the demographic data and a number of quality indicators that characterize the composition of the groups. A direct comparison of the two groups which comprise more than 1000 patients with rectal cancer is therefore warranted and shows an improvement in four quality goals (11.1%) that could now be achieved. Another two quality goals that were not documented before or not applicable were now additionally achieved. This observation adds to the growing body of evidence that treatment of patients within centres improves quality of care [76,77,78].

The German Cancer Society implemented its own set of quality indicators and benchmarks for annual reporting at the external audits. Likewise, quality indicators were defined within the German Guidelines Colorectal Cancer [79]. Both sets of quality indicators underwent a process of refining over the years with changing items and target values. The 31 quality indicators defined by the German Cancer Society in 2018 reflected only five indicators as defined by the Working Group and used herein. The local recurrence rate at 5 years is not reported. The most recent version of the German Guidelines (released in 2019) defines only 12 quality indicators without target values. There are several reasons for these differences including the coverage of quality indicators that only apply to colon cancer, the definition of more general goals and the function of quality indicators as control instruments. To provide a comprehensive report on rectal carcinoma treatment outcome, we esteem the quality indicators as published by the working group as the most detailed set of parameters available so far. Nevertheless, some quality indicators may need to be reconsidered, such as the R1,2 rate of < 20% or the inclusion of the distance of the tumour to the mesorectal fascia in pretherapeutic MRI. It is, however, beyond the scope of this study to provide suggestions for change, because for that a formal consensus process based on a meta-analysis for each item would be needed.

While the German approach to higher specialization is via voluntary certification, there are some European countries that implemented centralization by administration and auditing on a national/regional level. Reports from these countries, namely Sweden, Norway, Netherlands and Spain (Catalonia), show a permanent improvement in a number of quality indicators, especially regarding survival, local recurrence, negative CRM, use of neoadjuvant treatment, discussion at MDTs and mortality [78, 80,81,82,83]. For local recurrence, a decrease at 5 years on a national level from 8.7 to 5.0% was recently reported from Sweden [80] and from 14.5 to 5.0% from Norway [83]. A voluntary training program in Spain also resulted in a 5-year local recurrence rate of 4.7% [84].

While these data underline the benefit of centralization, it has recently been questioned with respect to German cancer centres. Vogel did not find factors associated with anastomotic leak reflected in the subset of structure and process parameters of the data entry form [85]. Likewise, Ghadban et al. could not detect improvements in several aspects of morbidity on a national level despite the annual numeric increase of certified bowel cancer centres [86]. However, they used administrative data which were not based on a dedicated cancer registry or structured audit. The quality of these data is therefore questionable [87].

Our study reveals some limitations that need to be discussed. First, although based on prospectively collected data, the study is retrospective in nature. However, the inclusion of all consecutive patients, the high follow-up rate and the assessment by means of predefined quality indicators render the results valid for general conclusions. Second, during the study period, four editions of the TNM classification were in operation. Apart from a number of subclassifications which were of no relevance for our study, there were changes regarding the classification of small perirectal tumour deposits. Whereas these deposits were classified as T3 if smaller than 3 mm (5th ed.) or if irregular in shape (6th ed.), they were classified as lymph nodes (N1c) in the 7th and 8th editions [11,12,13, 21]. Therefore, some patients were classified N positive in the recent group with the resulting stage migration. The magnitude of affected patients, however, is only in the range of 1% (2 patients out of 317 resected patients without distant metastases). Third, the complexity of the analyses and the long time period make the study liable for confounding. Whereas we displayed patient, treatment and pathological characteristics of the two cohorts and used the predefined numerators and denominators to maximize comparability, additional potential confounders may bias the results. These includes more detailed characteristics that were not included in the database like performance status or co-morbidities, as well as diagnostic and treatment measures that evolved over time independently of the centralization of patient care. The latter include a more comprehensive staging by high-resolution MRI, refined surgical techniques as ELAPE, the introduction of new strategies in the management of metachronous metastases and the start of a screening colonoscopy program in 2002. However, the implementation of these new developments is likely to be accelerated by the multidisciplinary teamwork of a certified centre.

Conclusion

Implementation of clinical pathways within a certified centre is associated with an improvement in the quality of care for rectal cancer patients. Using a set of 36 predefined quality goals, six more quality goals could be achieved as compared with a previous study period. Improvement was detected in complex indicators such as the local recurrence rate in stage (y)pIII patients, anastomotic leak rate in low anastomoses and the APE rate for low rectal cancers. Certification as a specialized centre therefore signals high standard of care.