Impact of comorbid conditions on participation in an organised colorectal cancer screening programme: a cross-sectional study

Cross-sectional study carried out at 10 Barcelona primary care centres involved in the BCCSP from July 2011 to May 2012. The inclusion criterion for this ad hoc analysis was individuals eligible to participate in the first round of the BCCSP (i.e. men and women aged 50 to 69 at average risk of colorectal cancer) included in the Colo-alert trial (n = 41,042) [18]. The exclusion criterion for this ad hoc analysis was the presence of BCCSP exclusion criteria (n = 3100). Individuals with missing data on comorbidities were excluded (n = 1734; 4.6%). In the end, a total of 36,208 individuals were included in the study (Fig. 1).

The Colo-alert trial was a cluster randomised clinical trial (RCT) in primary care, that evaluated the effectiveness of an alert in the electronic medical record (intervention group) to encourage colorectal cancer screening participation compared to usual care (control group) in which primary care professionals were involved in order to improve colorectal cancer screening participation [19]. The BCCSP was launched in December 2009 and the first round lasted until May 2012. The target population comprised 197,795 individuals invited based on the primary care centre they had been assigned to. More specifically, the specific cohort of individuals enrolled in the cluster-RCT included those individuals assigned to the last 10 primary care centres that were invited from July 2011 to May 2012. These centres, run by the Catalan Institute of Health, were waiting to start the first round of the BCCSP at the time the intervention was started. Of the 11 primary care centres invited to take part in the RCT (n = 148 general practitioners -GP- and 57,020 patients), one refused to participate (n = 18 GP and 5953 patients). Subsequently, 10,025 patients who did not have a GP assigned to a participating centre at the start of the study were excluded. Therefore, they were not eligible to receive the RCT intervention. Following the above exclusions, we considered the appropriateness of including the entire population - 130 GP with 41,042 individuals.

The main dependent variable was participation in the BCCSP within 1 year of the date of invitation.

The main explanatory variable was comorbidity according to clinical risk group (CRG) status [20]. The Catalan Institute of Health incorporated the CRG tool as a model for grouping morbidities. Its use involves a computerised calculation based on a patient’s basic information as collected in their electronical medical record (age, sex, International Classification of Diseases 10) and the assignment and visualisation of the CRG stratification results for each user in the computerised medical record used by GP. The CRG status includes the following nine categories:

This study assessed the impact of comorbidity on FIT-based colorectal cancer screening programme uptake in men and women aged 50 to 69. Individuals with multiple minor chronic diseases were more likely to participate in the screening programme compared to healthy subjects. In contrast, subjects who had three or more dominant chronic diseases were less likely to participate in the programme.

The total crude participation rate in the BCCSP (48%) observed in this study reached the standard of more than 45% referred to in the European guidelines [4]. It was higher than the average colorectal cancer screening rates in Spain (43.8%) [6], but lower than the results for the programme in the Basque Country (64.3%) [22] in Spain and other European colorectal cancer screening programmes (UK: 57.4%) [23]. Like other Spanish programmes, participation was higher among women than men [6]. Healthy individuals made up 22.1% of the sample. In Spain, two surveys, nationally representative, carried out in an adult population and with data self-reported by the participants showed that 40% [24] and 16% [25] of the population did not have any of the chronic diseases on a preselected list of prevalent chronic diseases. The rate for individuals in the groups with the highest level of comorbidities (i.e., three or more dominant chronic diseases, malignancies or catastrophic conditions) was 2.9%, a figure similar to the 2.3% of bowel screening non-participants who had a medical reason for not participating in the Scottish programme [31].

To date, few studies have investigated the presence of comorbidities in people who have been invited to take part in a colorectal cancer screening programme. Furthermore, few studies have explored the effect of comorbidity on colorectal cancer screening participation and results have been controversial. Some of them highlight a positive association between screening uptake and better health status [26, 27] as it is correlated with perceived benefits that increase the likelihood of cancer screening [27]. Others show this association in the event of coexisting health problems or chronic diseases, given that these subjects contact health services more often than healthy people, and therefore can receive recommendations for screening [26, 27]. A recent systematic review focusing on facilitators and barriers to colorectal cancer screening adherence reported that individuals with a chronic disease, such as hypertension, cardiovascular disease, diabetes, arthritis, ulcers, asthma or emphysema, were more likely to participate in colorectal cancer screening, both for faecal occult blood tests and endoscopies [27]. This systematic review included seven studies specifically assessing the effect of having a chronic monitorable disease on colorectal cancer screening adherence, of which five reported the chronic disease as a significant facilitator [27]. In fact, two nationwide surveys performed in Spain based on self-reported data found significant higher compliance with colorectal cancer screening as the number of chronic conditions increased [24] or in the event of an existing comorbidity [25].

Contrary to these results, we found an inverse association between having a dominant chronic disease and completion of FIT, although we could not assess the interaction with the specific type of disease. Our results were in line with those reported by Liu et al., who found a significant negative association between three or more chronic conditions and colorectal screening (i.e., faecal occult blood test or colonoscopy) after adjusting for the number of visits to primary care [13]. Therefore, the number of medical visits should be included when the effect of comorbidity on screening participation is analysed. Some authors have hypothesized that specific differential impact of different comorbidities could explain these differences, regardless of whether there are comorbidities or not, the number of diseases, and other composite measures [12, 13, 28]. In that sense, hypertension has been associated with higher participation in colorectal cancer screening [14], whereas other studies found other chronic diseases that demand significant time with GP in the clinic for management, such as diabetes or heart disease reduced the likelihood of being up to date with screening [13]. In this regard, in our study we observed how participation is higher in individuals with multiple minor chronic diseases, possibly as they are in more frequent contact with health services compared to the healthy population and as they had a lower level of comorbidity compared to subjects who had multiple dominant chronic diseases, who participated less in the colorectal cancer screening programme.

Since recommending screening among patients with limited life expectancy for whom screening tests have little benefit and may even be harmful, older people have been a focus of research [11, 15, 29, 30]. Controversial results have been found in people aged 65 years or older with regard to the association between comorbidity and colorectal cancer screening uptake, with the results ranging from non-significant [28] to a weak association [11].

Feedback from GP suggested that some participants invited had a specific medical reason (the highest number of comorbidities) for not being screened [31]. A more holistic view will help us to determine which individuals are at an increased risk of developing colorectal cancer or its precursor lesions, how these factors influence participating in population programmes, and which individuals may benefit most from colorectal cancer screening [31]. The role of GP has been changing with the introduction of organised programmes in which they do not directly order screening tests, but rather have an essential role in increasing participation and informing the target population [32]. The primary care setting offers a chance to address colorectal cancer screening issues with patients who attend for other reasons. Taking into account background comorbidities, previous screening history, colorectal cancer risk, and individual preferences for screening could lead to a desirable informed-decision, optimizing the benefits and cost effectiveness of colorectal cancer screening. We should pay special attention to individuals with chronic dominant diseases, individualising the risk/benefit balance of screening.

The strengths of this study include a large sample population at average risk of developing colorectal cancer, in terms of age, sex, comorbidities and socioeconomic status. The population of the 10 centres included in the RCT is representative of the population invited to the first round of screening in Barcelona based on the sociodemographic data published. Comorbidities are associated with a major use of health resources and may increase the opportunity of receiving a cancer screening recommendation from a doctor. In this study, the number of visits to primary care was also reported and appropriately analysed as a determining confounding factor. To our knowledge, this is the first study using CRG categories to assess the impact of comorbidity on a colorectal cancer screening programme. In this regard, in addition to the presence and the number of comorbidities, additional information, such as the severity of the chronic disease (i.e., minor or dominant) or its duration (i.e., acute, chronic) was given. The scientific literature is heterogeneous, since no gold standard approach exists for measuring comorbidity in the context of cancer [33]. The suitability of alternative measures may depend on the research question and also availability of data [33]. As a result, it is difficult to compare results between studies with appropriate accuracy, because the results are heavily dependent on the list of comorbidities used in each study. When reporting the effect of comorbidity on cancer screening participation, comorbidities have been measured in the literature as present or not, as a number [12, 13, 24] and/or type [13, 14] of chronic diseases, as well as using specific composite indicators (i.e., Charlson score [11]). As a limitation of the present study, we had no information about the specific type of chronic conditions or the International Classification of Diseases code, which meant we were unable to examine their interaction with the CRG categories assessed in the study. It should be pointed out that the patients excluded due to a lack of information on the comorbidity variable had a clinical profile less favourable for colorectal cancer screening participation. Nevertheless, the percentage of exclusions for this reason was small (4.6%). As expected, there was a not negligible percentage of missing lifestyle data (i.e., smoking, alcohol), especially for body mass index. This may be because weight, and hence body mass index, is widely unmeasured in primary care databases [34]. It is important to mention that this study had an urban population as the BCCSP was carried out in the city of Barcelona and more studies would be required to extrapolate these data to the entire population at average risk of developing colorectal cancer in Catalonia. This study took place in the context of a FIT population-based colorectal cancer screening programme, so the results cannot be generalised to other colorectal cancer screening tests (i.e., colonoscopy), although faecal testing is the most frequently used type of testing in Europe.