Patterns and predictors of adherence to colorectal cancer screening recommendations in Alberta’s Tomorrow Project participants stratified by risk

In Canada, an estimated 1 in 13 men and 1 in 16 women will develop colorectal cancer (CRC) in their lifetime [1]. As the third most common cancer [1], there is a need to understand how to best identify individuals at risk and provide appropriate screening recommendations, balancing the goals of public health (lowering incidence and mortality of CRC) with economics (efficient use of the health-care system). The premise of screening is to identify early stage cancer development at a time when preventive measures and treatments are most effective and before progression or metastasis occurs [2]. To date, structured CRC screening programs exist or are proposed in ten Canadian provinces and one territory [3].

CRC screening can be done by home stool testing [fecal occult blood test (FOBT) or fecal immunochemical test (FIT)] or endoscopy (flexible sigmoidoscopy or colonoscopy). Consistent adherence to FOBT has been shown to reduce CRC incidence and mortality by 17% [4] and 11% [5], respectively; FIT is a more recent fecal test with improved patient acceptance and diagnostic accuracy [6]. Reductions in CRC incidence and mortality observed for flexible sigmoidoscopy are similar to the FOBT [7]. Colonoscopy is widely considered the gold standard for CRC screening based on its ability to both visualize and remove polyps and neoplastic lesions in all regions of the colon [8]; although there is only indirect evidence of its efficacy as a screening modality [9]. Observational and modeling studies [10, 11] have suggested a reduction in CRC incidence (67 and 81%) and mortality (65 and 83%) with colonoscopy.

Guidelines recommending colorectal cancer screening were first released in Canada in 2001 (Canadian Task Force on Preventive Health Care (CTFPHC) [12]) and in Alberta in 2008 (Alberta Toward Optimized Practice Clinical Practice Guidelines (provincial guidelines) [13]). Both these guidelines and subsequent updates [14, 15] provide risk-dependent screening recommendations for average, moderate and high-risk individuals. Three main criteria determine the level of risk for CRC and, consequently, the recommended screening method, timing and frequency: age, family history of CRC and personal history of certain bowel conditions [13]. In general, FOBT is recommended for average-risk individuals, whereas endoscopy is recommended for high-risk groups, though the 2008 provincial guideline recommended all three options for average risk screening. Over 90% of CRC cases occur in individuals over 50 years [16], and therefore individuals 50 to 74 years without any other risk factors are considered to be at average-risk. Despite its enhanced ability to detect abnormalities, colonoscopy is not recommended as an initial screening modality for average-risk individuals, due to poor compliance, feasibility and cost concerns [12], but rather as a follow-up to a positive FOBT [13]. Family history of CRC is considered a moderate risk - an individual with a first-degree relative (FDR) with CRC has almost a two-fold increased risk for developing CRC, increasing to almost four-fold with two or more affected relatives [17]. Individuals with certain bowel conditions, including inflammatory bowel diseases (IBD, which includes ulcerative colitis and Crohn’s disease [18]) and/or a history of polyps [19] are considered high-risk. Cumulatively, the risk of CRC is the highest for individuals with both a family history of CRC and an inflammatory bowel condition, with relative risks approaching ten-fold [20]. As the level of risk increases based on age, family and personal medical history, the recommended test, age to commence screening, and optimal screening frequency vary (Table 1).

A key component of the guidelines is that the right screening test is used in the right patients; this ensures appropriate patient care along with reduced burden and costs on the health-care system. We have previously reported that when age (50–74 years) was the only indication for testing, the majority of Alberta’s Tomorrow Project (ATP) participants were not up-to-date with CRC screening according to CTFPHC guidelines [21]. However, endoscopy was likely to be more recent than FOBT for participants at moderate and high risk for CRC, suggesting appropriate application and utilization of screening recommendations in higher risk groups. Knowledge of screening status at any one time is important, but consistent screening over time is needed to reduce cancer incidence and mortality. For example, FOBT effectiveness as a screening tool is reduced when patients do not adhere to a regular interval of testing [22]. Predictors of repeated mammography [23] and prostate [24] screenings have been investigated, however, available data regarding predictors of repeated CRC screenings are limited [25, 26]. Here, we expand on previous cross-sectional analyses by our group [21] to determine screening behaviour of ATP participants based on stratified CRC risk, determine screening status and patterns and reasons for screening, as well as to identify predictors for regular screening behaviour.

Adherence to a regular screening pattern is the optimal surveillance method to detect potential pre-cancerous lesions or polyps at an early stage, which should lead to earlier detection and reduction of cancer incidence. Here, we investigated screening behaviours over time in a subset of Alberta’s Tomorrow Project participants. The majority fell into the average-risk (Age-only) group, where overall screening uptake was low. However, as the personal risk of CRC increased across strata (from average to highest risk), the uptake of screening and the proportion of participants who were regular screeners also increased. The proportion of average and moderate risk participants up-to-date with screening also increased over time. Reasons for screening were also explored, and, overall across all risk strata, the primary reason for undergoing an endoscopic procedure was sign of a possible problem. Future work should investigate barriers to screening uptake in order to maximize participation.

A previous survey in Alberta reported that 3 years after the release of the Canadian Task Force recommendations in 2001 only 11.9% of average-risk individuals were up-to-date for FOBT screening [29]. Here, we observed that only 21.1 and 34.6% of average-risk participants were up-to-date for FOBT at enrollment and follow-up by 2008, respectively (Table 3). Further, findings from the 2003 Canadian Community Health Survey (CCHS) suggested 85% of average-risk respondents were non-adherent to FOBT recommendations [30], compared with 78.9% in the Age-only group in the current study at enrollment. However, no Albertans were included in the study using 2003 CCHS data. These numbers are well below the goal proposed by the Canadian Partnership Against Cancer of 60% adherence to guaiac or immuno-based fecal tests as the initial recommended test for average-risk individuals [31]. Over the 4.2 year follow-up period, the proportion of participants considered up-to-date for overall CRC screening increased from 28.9 to 50.3% in average-risk (Age-only) ATP participants. Over the same period, approximately 39% of average-risk participants who never had a CRC screening test at enrollment had undergone screening by follow-up. In comparison, an Ontario study reported that approximately 21% of average-risk participants (50–59 years) who never had CRC screening at enrollment completed CRC screening during a 6 year follow-up [32], and a study in an older demographic (65–69 years) in Manitoba reported a significant increase in up-to-date status for CRC screening from 20.5 to 56.9% over a longer follow-up period of 17 years [33]. Compared to international studies, the adherence rate to fecal screening completed over three consecutive years amongst average-risk Australians was 55% [34].

Overall uptake of screening tests increased as risk of CRC increased across the strata. In moderate-risk participants (FamilyHx), 53.7% of participants were up-to-date for overall CRC screening at enrollment and this increased to 73.9% at follow-up. These findings are similar to another Alberta-based study in 2009 investigating first-degree relatives of CRC patients, where 60% of respondents were up-to-date [35]. At both enrollment and follow-up, more participants with a family history of CRC were up-to-date for endoscopy than FOBT, which aligns with the recommendation for individuals with a family history of CRC to undergo endoscopy rather than FOBT. Finally, participants with a bowel condition (PersonalHx) were more likely to be up-to-date for an endoscopy (72.6%) rather than FOBT (30.5%) at follow-up. This is in agreement with a hospital-based Canadian study where 90% of eligible ulcerative colitis patients underwent colonoscopy as part of surveillance screening procedures [36] and supports the observation in the present study that the majority of the PersonalHx participants reported undergoing endoscopy due to a physical problem. Overall, the rate of uptake of screening tests in ATP participants is comparable to other provincial and national cohorts, but there is significant room for improvement as the effectiveness of a screening protocol relies on repeated testing at consistent intervals [25]. Therefore, continued efforts to promote regular screening should be a target for public health initiatives.

Despite the release of the Canadian Task Force screening recommendations in 2001, screening rates remained low among adults 50–74 years in the CCHS conducted 2 years after the recommendations were published [37]. To understand what might be impairing screening participation, a random digit dialing survey of 2500 Canadians aged 50–74 years found most respondents believed CRC screening was important; however, only 40% understood that CRC screening should be done even when asymptomatic [38]. Physicians were reported to have pessimistic expectations on patients’ compliance to CRC screening [39], however, Bryant et al. [38] reported high willingness among patients to talk with a health-care provider about screening. This gap between physician perspectives and expectations on one side, and actual patient attitudes on the other, represents a potential target to increase screening participation and appropriateness.

The 2008 provincial guidelines for CRC screening and the 2001 CTFPHC guidelines were used in the current study since they coincided with the recruitment period of the ATP cohort. Since then, the provincial and CTFPHC guidelines have been updated in 2013 and 2016, respectively [14, 15]. Current provincial guidelines recommend FIT as the initial screening test for average-risk individuals and moderate-risk individuals with one first-degree relative diagnosed ≥60 years [14]. Since November 2013, FIT is available province-wide and the FOBT is no longer in use in Alberta [14]. FIT holds potential for better patient compliance since, unlike FOBT, it does not require dietary or medical restrictions prior to testing [40].

Little information is available on predictors for non-regular cancer screening patterns, such as episodic or new screeners. A study in Australia on participation to four rounds of FIT testing identified those with an “inconsistent participation” pattern (similar to the definition of “episodic” screeners in the present study) to be younger compared to regular participating individuals [41]. These determinants are similar to what we observed here, with older age increasing the likelihood of screening in average-risk (Age-only) participants. Our previous findings within this cohort provided evidence that other cancer screening tests such as PSA and mammography were significant predictors for FOBT uptake [21]. In this prospective analysis, we again show that average-risk participants who continued to undergo FOBT screening on a regular basis were more likely to have other cancer tests completed (Fig. 3). Sewitch et al. [30] reported that “ever use” for CRC screening was associated with older age, higher levels of income, and presence of chronic disease. Similarly, in the 45 and Up cohort, increased uptake of FOBT was associated with higher education and income [42]. In the present study, age, higher income, and adherence to other cancer screening tests were observed to reduce the odds of being a non-screener for FOBT and overall CRC compared to regular screeners in the average-risk participants. Interestingly, family history of cancer was a significant predictor of being a regular screener in women compared to non-screeners, but not men; while in men, personal history of chronic disease was associated with regular screening, indicating regular interactions with a family physician may influence uptake of CRC screening tests [43]. While Australians in the 45 and Up cohort who reported very good or excellent overall health and quality of life were more likely to report having CRC screening, female ATP participants were more likely to report endoscopy if they instead reported good or fair/poor general health. Other health-conscious behaviours such as higher levels of physical activity or higher intakes of fruits and vegetables, are likely to play a role in screening behaviour and should be explored further.

An individual’s CRC risk should be considered in determining the most appropriate screening test; otherwise, overuse and avoidable harm could occur. In particular, colonoscopy has been scrutinized due to health-care costs and system strains, high expertise required to perform the test, and patient level of comfort or willingness [44]. Colonoscopy is recommended for a subgroup of moderate-risk individuals, as well as for high- and highest risk individuals (Table 1); however, approximately 56.5 and 67.2% of those participants reported receiving a FOBT at enrollment and follow-up, respectively. This emphasizes the importance of selecting the most appropriate test in light of the patient’s risk and clinical recommendations and suggests that efforts to prioritize tests based on risk, given the specific criteria laid out in the guidelines, may improve CRC screening program effectiveness [45]. Limited access to colonoscopy providers in some communities may have prevented optimal utilization, causing some moderate-risk or high-risk participants to initially undergo a FOBT, with the possibility of a colonoscopy referral, depending on FOBT results. Ideally, screening date and outcome would have provided valuable information regarding appropriateness of CRC testing in average-risk (Age-only) and moderate-risk (FamilyHx) participants with a family history of CRC in 1 FDR ≥ 60 years. For example, if an average-risk participant had a positive FOBT and was referred for colonoscopy, this would be entirely appropriate and in line with the provincial guidelines. However, neither enrollment nor follow-up questionnaire captured this information, preventing further investigation of CRC screening tests in those participants.

We observed that ATP participants who are at average-risk for CRC were least adherent to CRC screening recommendations, while those at highest risk were the most adherent. Non-regular screening patterns were most prevalent amongst average- and moderate-risk participants, and represent target groups to promote repeat screening. Low adherence to CRC screening recommendations indicates the need to raise awareness of the most current recommendations – provincial guidelines in 2013 [14] and Canadian Task Force guidelines in 2016 [15] – and promote physician-patient conversations through initiatives at both the health-care system and population level, which has successfully led to higher CRC screening participation rates [50, 51]. Future studies should aim to identify barriers to screening uptake to maximize participation in addition to providing further evidence that regular adherence to screening recommendations reduces the incidence and mortality of CRC.