Validation of the reporting of local recurrence of rectal cancer in the Swedish ColoRectal Cancer Registry (SCRCR)

Abstract

Background and aims:

The Swedish ColoRectal Cancer Registry (SCRCR) includes data on patients with rectal cancer in Sweden with a coverage rate of 98.5%. Variables on primary diagnosis and treatment have good validity, but the validation of oncological outcomes such as local recurrence is lacking. Since data from the SCRCR are used widely in research and for clinical evaluation, with local recurrence as an important outcome, this study aimed to validate the registration of local recurrence of rectal cancer in the SCRCR.

Methods:

All patients registered with a diagnosis of rectal cancer in 2016 and 2017 who underwent an abdominal resection of the tumor were identified in the SCRCR. Medical records were reviewed and compared to the data registered in the SCRCR.

Results:

A total of 2828 patients were included, of which 166 patients (5.9%) were diagnosed with local recurrence according to medical records within the study period. Of these, 94/166 (57%) were registered with local recurrence in the SCRCR. Patients with non-reported local recurrence more often had concurrent metastases and/or were treated with palliative intent. There were 17 patients reported with local recurrence in the SCRCR without local recurrence identified in the medical records.

Conclusion:

There was a significant underreporting of local recurrence in the SCRCR. Ambiguities in the definition of local recurrence as well as disregarding patients with concurrent metastatic disease probably contributed to the underreporting. Clarifying the definition of local recurrence and stressing the importance of reporting local recurrence regardless of metastatic disease or palliative treatment may improve data accuracy.

Keywords

Rectal cancer local recurrence national quality registry validity

Context and relevance

The Swedish ColoRectal Cancer Registry (SCRCR), as well as many other national quality registries, is widely used for scientific research and clinical quality control, which is why high validity of the registry data is of utmost importance. This is the first paper to validate the data on local recurrence of rectal cancer in the SCRCR specifically, including a large unselected national 2-year cohort of rectal cancer patients. These data are extensively used in research, both as an important outcome measure following rectal cancer treatment and to identify patients for studies on local recurrence. It is thus troublesome that 43% of local recurrences were missing in the registry data, as inadequate validity may influence the results and conclusions drawn based on these data.

Introduction

In recent years, local recurrence has been reported in 5%–10% of patients who have undergone resection of rectal cancer.^1–3 This is an improvement over rates as high as 20%–40% just a few decades ago, which can be attributed to neoadjuvant radiotherapy and advances in surgical technique.^2,4–7 However, as rectal cancer is common with over 700,000 new cases/year worldwide,⁸ many patients are affected by local recurrence. Given that the morbidity and mortality associated with local recurrence is substantial,^9–11 it remains an important outcome measure of rectal cancer treatment.

The Swedish ColoRectal Cancer Registry (SCRCR) is a national registry in which data regarding diagnosis, treatment, and outcome of rectal cancer have been reported prospectively since 1995.¹² Since 2007, it also includes colon cancer. The SCRCR has a coverage of 98.5% of all cases diagnosed in Sweden.¹³ In total, it currently includes over 50,000 patients with rectal cancer. Follow-up is registered at 3 and 5 years; however, tumor recurrence data are expected to be reported at the time of diagnosis according to the manual.¹⁴

The SCRCR has previously been found to have good validity with respect to several variables such as preoperative investigation, neoadjuvant and surgical treatment, and histopathological examination.^15,16 In contrast, variables such as anastomotic leakage and other short-term complications have been found to be underreported.^15,17,18 The validity of the long-term follow-up variables of cancer recurrence, including local recurrence and distant metastases, have been sparsely evaluated previously.^16,19 A recent study including two of the 21 regions in Sweden examined the validity of cancer recurrence in colorectal cancer patients in the registry; however, the analysis did not distinguish local recurrence of rectal cancer from other types of recurrences.²⁰ A substantial difference in the reporting was found between the two included regions, indicating that there might be heterogeneity in the reporting across the country.²⁰ Furthermore, an additional study validating tumor recurrence of colorectal cancer in the SCRCR was recently published,²¹ but it only included a random sample of 700 patients from 12 of the 47 hospitals in Sweden. Validity was reported as the proportion of cases where the data were consistent between the medical records and the SCRCR. The exact agreement was found to be moderate for data on local recurrence, not distinguishing between colon and rectal cancer.²¹ Although the sample size was limited, the study indicated underreporting as well as incorrect reporting of local recurrence in the SCRCR.

Data from the SCRCR are widely used in research. This includes studies with local recurrence as an outcome measure as well as studies using the registry to identify patients with local recurrence for inclusion.^22–35 Furthermore, one of the main purposes of the registry is to enable evaluation of clinical practice to promote an equal and optimal care throughout the country, and local recurrence is one of the most important quality variables in rectal cancer treatment.¹³ Thus, validating this variable is of great importance.

The aim of this study was to validate the registration of local recurrence of rectal cancer in the SCRCR and to determine the proportion of patients with local recurrence registered in the SCRCR and the extent to which the registered local recurrences were correct.

Methods

Study population

A national cohort of all patients registered in the SCRCR who were treated with abdominal resection surgery for primary rectal cancer diagnosed in 2016 and 2017 was included. Patients receiving non-surgical treatment or surgery without abdominal tumor resection, such as formation of a diverting stoma or local excision of the tumor, were excluded.

Definitions

Local recurrence of rectal cancer is defined by the SCRCR as the recurrence of cancer below the level of the promontory originating from the primary rectal tumor, regardless of putative pathogenesis or occurrence of simultaneous distant metastases or if the diagnosis is made by clinical examination, endoscopy, radiology, and/or pathology.¹⁴

Data collection

From the SCRCR, data including preoperative characteristics, neoadjuvant, surgical and adjuvant treatment, and follow-up regarding tumor recurrence were retrieved on 30 June 2022. Medical records for included patients were requested from the 47 Swedish hospitals reporting to the SCRCR. The records included details on neoadjuvant treatment, primary surgery, adjuvant treatment, and all clinical notes and results of all relevant radiological examinations performed following the primary surgery. For any patients with an indication of follow-up in another department or hospital, additional medical records were requested to ensure that the follow-up data were as complete as possible. A retrospective review of the medical records was performed to verify the local recurrence status for each patient using a predefined clinical record form. Only the first local recurrence for each individual patient was included in the validation, thus excluding local re-recurrences. Medical records covering until at least September 2022 (minimum 57 months following diagnosis) or until the death of the patients were scrutinized. However, only local recurrences diagnosed before the data retrieval from the registry on 30 June 2022, were included in the validation. As the stipulated time-points for reporting to the registry are at 3 and 5 years, the validity for local recurrences diagnosed within the first 3 years, as well as for the two annual cohorts, was presented separately to evaluate the importance of a complete 5-year follow-up.

All ambiguous cases were reviewed by three of the authors (S.W., E.H., and E.A.), and discussed to reach a consensus on whether each case was to be considered as local recurrence or not using the SCRCR definition.¹⁴ The data on local recurrence retrieved from the medical records were considered the gold standard and compared to corresponding data from the SCRCR only after the medical record review was completed. A similar consensus procedure was followed to address all cases where the two data sources differed regarding local recurrence reporting.

Statistical analysis

Data were summarized descriptively with measures of central tendency and variance as appropriate. Differences between registered and non-registered local recurrences were analyzed using the chi-square test of independence for categorical variables and the independent-samples Mann–Whitney U-test for continuous variables. A p-value < 0.05 was considered significant. The statistical analysis was performed using SPSS version 29 for Windows.

Ethical considerations

This study was approved by the Swedish Ethical Review Authority (2020-00976, 2022-00855-02, and 2022-02419-02). The study was registered at ClinicalTrials.gov (NCT04404777).

Results

Out of a total of 4211 patients diagnosed with rectal cancer during 2016 and 2017 registered in the SCRCR, 2994 unique patients registered as having undergone surgery were identified after the removal of 12 duplicates (Fig. 1). Of these, 159 patients did not meet the inclusion criteria, and medical records were missing for seven patients, leaving 2828 patients included in this study (Fig. 1). Demographic and perioperative data are presented in Table 1.

Fig. 1.

Flowchart.

Table 1.

Demographic and perioperative data.

Demographic and preoperative data	Included patients (n = 2828)
Sex
Female	1108 (39.2%)
Age (years)
Median	70
Range	23-95
ASA^a
1	488 (17.3%)
2	1514 (53.5%)
3	740 (26.2%)
4	36 (1.3%)
Missing	50 (1.8%)
BMI^b
Median	25.5
Range	15.1-52.0
Missing	22 (0.8%)
c-T-stage
T1-2	802 (28.4%)
T3	1447 (51.2%)
T4	515 (18.2%)
Missing	64 (2.3%)
c-N-stage
N0	1145 (40.5%)
N1-2	1641 (58.0%)
Missing	42 (1.5%)
c-M-stage
M0	2583 (91.3%)
M1	243 (8.6%)
Missing	2 (0.1%)
Tumor distance from anal verge (cm)
0-5	779 (27.5%)
6-10	1228 (43.4%)
11-15	810 (28.6%)
Missing	11 (0.4%)
Neoadjuvant therapy
Radiation	1854 (65.6%)
Chemotherapy	674 (23.8%)
Surgical procedure
Anterior resection	1400 (49.5%)
Abdominoperineal excision	1064 (37.6%)
Hartmann’s procedure	350 (12.4%)
Other	14 (0.5%)
Microscopically radical
Radical	2687 (95.0%)
Not radical	107 (3.8%)
Not assessable/missing	34 (1.2%)

ASA denotes American Society of Anesthesiologists physical status.

BMI denotes body mass index.

Out of a total of 173 patients (6.1%) with local recurrence identified through the medical records, 166 (5.9%) were diagnosed prior to data retrieval from the SCRCR on 30 June 2022, and were included in the validation process. Of these, 94/166 (57%) were registered with local recurrence in the SCRCR. Analyzing only local recurrences diagnosed within 3 years of the primary surgery, the registration rate remained consistent, with 56% (74/132) of cases registered. A similar pattern was observed when analyzing patients with a primary diagnosis in 2016 and 2017 separately, with 57% (44/77) and 56% (50/89) of cases registered, respectively.

Comparisons between local recurrences reported and not reported in the registry are presented in Table 2. There was no difference in the proportion of microscopically radical resections (R0) of the primary rectal tumor between reported and non-reported local recurrences. Patients with local recurrences not registered in the SCRCR more often had concurrent distant metastases at the time of local recurrence diagnosis and/or received palliative treatment for the locally recurrent tumor. Of the 72 patients with non-reported local recurrence, 50 (69%) were reported to the registry as having tumor recurrence in the form of metastatic disease. In 7/72 (10%) of the non-reported cases, the reported metastatic disease corresponded to the tumor classified as local recurrence from the medical records. In an additional 16/72 (22%) cases, metastatic disease in the form of peritoneal carcinomatosis or lymph node metastases in the pelvic area or of undefined location that could be interpreted as the identified local recurrence was reported. In the entire cohort (n = 2828), there were 188 patients reported with metastatic disease in these locations that could possibly include a local recurrence (peritoneum, pelvic lymph nodes, lymph nodes of unspecified location, and others with specification in running text).

Table 2.

Comparisons between registered and not registered local recurrences.

Comparisons between registered and not registered local recurrences	Local recurrences registered (n = 94)	Local recurrences not registered (n = 72)	P-value
Diagnosed at follow-up			p = 0.352
Yes	52 (55%)	45 (63%)
No	42 (45%)	27 (38%)
Microscopically radical (R0) resection of the primary rectal tumor			p = 0.551
Yes	79 (84%)	61 (85%)
No	14 (15%)	10 (14%)
Uncertain	1 (1%)	1 (1%)
Concurrent metastatic disease^a			p < 0.001
Yes	34 (36%)	56 (78%)
No	60 (64%)	16 (22%)
Treatment intent^b			p < 0.001
Curative	46 (49%)	13 (18%)
Palliative	47 (50%)	59 (82%)
Unknown	1 (1%)	0
Time from surgery to diagnosis of local recurrence (days)			p = 0.807
Median	612	553
Range	40-1862	44-2064
Time from diagnosis of local recurrence to date of data retrieval from the registry (days)			p = 0.812
Median	1219	1304
Range	197-2098	84-2212

At the time of diagnosis of local recurrence, diagnosed within 1 month after diagnosis of local recurrence.

For the local recurrence, at the time of diagnosis of local recurrence.

There was no difference between reported and non-reported local recurrences with regard to the time from the primary surgery to the diagnosis of local recurrence nor in the time between the diagnosis of local recurrence and the retrieval of data from the registry. There were regional differences, with the proportion of reported local recurrences varying from 45% to 70% across regions (Table 3). Furthermore, there were differences in reporting depending on the type of hospital with regional hospitals having the highest reported proportion, followed by county hospitals, and local hospitals having the lowest.

Table 3.

Registered proportions across health-care regions and hospital levels.

Comparisons between regions and hospital levels	Local recurrences registered (n = 94)	Local recurrences not registered (n = 72)
Health-care region^a,b
1	25 (57%)	19 (43%)
2	22 (54%)	19 (46%)
3	14 (70%)	6 (30%)
4	15 (63%)	9 (38%)
5	9 (53%)	8 (47%)
6	9 (45%)	11 (55%)
Type of enrolling hospital^b
Regional (university)	41 (65%)	22 (35%)
County	41 (53%)	36 (47%)
Local	12 (46%)	14 (54%)

Swedens 21 regions are divided into six health-care regions.

Percentage distribution displayed per row for comparison between regions/types of hospital.

There were 17 local recurrences registered in the SCRCR that were not identified or recognized as local recurrences by reviewing the medical records, corresponding to 15% of the registered local recurrences. Most of these patients had metastatic disease (10/17) or a new primary rectal tumor (5/17) but no apparent local recurrence according to the medical records. Of the patients with metastatic disease, six had lymph node metastases outside of the pelvic area, three had liver and/or lung metastases, and one had peritoneal carcinomatosis.

Discussion

This validation of local recurrence of rectal cancer in the SCRCR revealed considerable underreporting, with 43% of local recurrences missing in the registry data. In addition, there was some overreporting with 15% of the patients reported as having local recurrence in the registry not having local recurrence documented in their medical records.

When collecting data for a registry, one of the most important steps is to clearly define what the data entail. There is still no uniform, generally accepted definition of local recurrence of rectal cancer, although it is usually described in terms of recurrent cancer growth within the lesser pelvis.^36,37 While this definition is in line with the definition used in the SCRCR reporting manual,¹⁴ it is only described as recurrence in the same area as the primary tumor in the reporting form. The SCRCR reporting manual further states that the diagnosis of local recurrence should be made regardless of assumed pathogenesis and concurrent metastatic disease.¹⁴ Thus, applying this definition strictly, all cases of tumor growth in the lesser pelvis originating from the primary rectal cancer should be classified as local recurrence. This could include peritoneal carcinomatosis situated in this region. However, this may not be in line with the general opinion of the medical profession on what constitutes local recurrence of rectal cancer, which is why we chose to differentiate within this group. In patients with generalized carcinomatosis, a distinctive, focal tumor in the lesser pelvis was considered as local recurrence, while small nodules in this context were not.

Biopsy confirmation of local recurrence is not required for diagnosis, as this can be difficult to achieve and frequently yields false negative results.^36,38 The diagnosis is in most cases based on radiology findings. Radiological interpretation can be difficult, as scarring or tissue lesions related to previous radiotherapy, surgery, or postoperative infection can be difficult to distinguish from tumor growth. As deciding what should be classified as local recurrence can be difficult, we applied a thorough consensus process, ensuring that the definition was used consistently in the assessment of each case. However, this process required the participation of three surgeons. Thus, as reporting often is performed by research nurses or administrative hospital personnel, it is possible that there is a need for increased support to improve reporting. Even so, in many cases, the non-registered local recurrences were documented as local recurrences in the medical records and should thus have been reported to the registry as such. Cases misclassified and reported as metastatic disease could, through review of the medical records on a case-by-case basis for a large number of patients, be identified from the registry. However, the vast majority of unreported local recurrences would remain unidentified.

Furthermore, we identified a risk of bias in the registry, as the presence of concurrent metastatic disease and palliative treatment was more common in non-reported cases. In addition to the difficulty in tumor classification, this could be due to only reporting distant metastases in patients with synchronously diagnosed local recurrence or refraining from reporting local recurrence in patients with previously reported metastatic disease. We also found a difference in the reporting of local recurrence between regions and types of hospitals. This may probably be attributed to different procedures for reporting to the registry and parties responsible for the registration. Considering that the SCRCR, as well as many other national quality registries, is used extensively for both scientific research and clinical quality control, the inadequate validity of local recurrence data is troubling, as it may influence the results and conclusions drawn regarding this outcome. Thus, this is important to consider when conducting as well as interpreting the results of studies based on these data.

The years selected for the validation were chosen to provide the most recent cohort possible while ensuring that a sufficiently long follow-up period had elapsed. One may consider whether the results of a new validation based on a more recent cohort would differ; however, as no substantial changes to the registry or the reporting processes have been implemented, a significant difference appears unlikely.

The main strength of this study is the national cohort design including all eligible patients over 2 years, yielding a large and unselected cohort instead of a sample, as often suggested by validation manuals^39,40 This unselected approach ascertains that the study cohort reflects the clinical reality. A limitation could be that the request for medical records was addressed only to the department of surgery reporting to the registry. This was mitigated through retrieving records from additional departments if the medical record review indicated follow-up elsewhere. In addition, it could be argued that including all patients who had undergone abdominal resection of the rectal tumor, regardless of whether the treatment was considered curative or not, could result in a higher proportion of non-reported cases. However, sensitivity analysis in this regard showed no more than a marginal impact on the reported proportion of local recurrences. Finally, not all patients had a complete 5-year follow-up, which is when the final planned reporting to the registry occurs. However, separate analyses of local recurrences diagnosed within 3 years, when the first planned follow-up occurs, as well as of those diagnosed in 2016, where all had follow-up exceeding 5 years, showed corresponding reporting rates.

In conclusion, there was a significant underreporting of local recurrence of rectal cancer in the SCRCR. To address this, a clarification of the definition of local recurrence and how it should be applied, as well as emphasis on the importance of reporting regardless of metastatic disease or treatment intent, could improve data accuracy.

Footnotes

Data availability statement

Research data are not shared, as this is not included in the ethic approval.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was financed by grants from the Swedish state under the agreement between the Swedish government and the county councils concerning research and education of doctors, the ALF-agreement (ALFGBG-965084 and ALFGBG-984105), the Swedish Cancer Society 19 0333 Pj, 22 2265 Pj, and 24 3733 Pj 01H, and the Swedish Research Council 2021-01025.

Ethical considerations

This study was approved by the Swedish Ethical Review Authority (2020-00976, 2022-00855-02, and 2022-02419-02). The study was registered at ClinicalTrials.gov (NCT04404777).

ORCID iDs

Sophia Waldenstedt

Eva Haglind

Eva Angenete

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