Factors Associated with Colorectal Cancer Screening in Spain: Results of the 2017 National Health Survey

This study aimed to determine the CRC screening coverage of people aged between 50 and 69 years who were living in Spain in 2017 and describe the factors associated with not having had a faecal occult blood test (FOBT). A cross-sectional study was performed using data from the Spanish National Health Survey 2017. We analysed 7568 individuals between the ages of 50 and 69 years. The proportion of respondents between 50 and 69 years old who had had an FOBT was 29.0% (n = 2191). The three autonomous communities with the lowest proportion of respondents who had had an FOBT were Extremadura (8.7%, n = 16), Ceuta–Melilla (10.4%, n = 3), and Andalucia (14.1%, n = 186). The variables associated with not having had an FOBT were being 50–54 years old (PR = 1.09; 95% CI 1.04–1.14), having been born outside of Spain (PR = 1.11; 95% CI 1.06–1.16), not having been vaccinated against the flu (PR = 1.09; 95% CI 1.04–1.15), never having had a colonoscopy (PR = 1.49; 95% CI 1.40–1.59), not having had an ultrasound scan in the last year (PR = 1.09; 95% CI 1.04–1.14), and not having seen a primary care physician in the last month (PR = 1.08; 95% CI 1.04–1.12). The factors associated with not getting an FOBT were young age, having been born outside of Spain, not having been vaccinated against the flu in the last campaign, and not making frequent use of healthcare services.


Introduction
Colorectal cancer (CRC) is the third most common cancer worldwide in males and the second in females, according to the World Health Organization GLOBOCAN database, though the incidence and mortality rates are substantially higher in males than in females [1]. In Spain, CRC is currently the second most common cancer in both sexes, the leading cause of cancer death in women, and the second leading cause of cancer death in men [2].
The risk factors for CRC are being of older age, being overweight or obese, smoking, consuming alcohol, having a sedentary lifestyle, consuming ultra-processed meat, Lynch syndrome, hereditary polyposis syndromes, ulcerative colitis, Crohn's disease, colon polyps (adenomas, serrated polyps), having a personal or family history of CRC, and abdominal radiation exposure [3][4][5][6]. On the other hand, a factor that is associated with a decreased risk of CRC is the combined use of aspirin and metformin, which have different preventive mechanisms and may benefit synergistically [7,8].
The early 1980s saw the introduction of the immunological faecal occult blood test (FOBT), which is based on the reaction of specific antibodies to human haemoglobin and requires no dietary or pharmacological restrictions [21][22][23]. In Spain, cancer screening began in the early 1990s and gradually extended, with levels of access varying between regions [24]. Research shows that patient-level barriers include socioeconomic, cultural, and psychosocial factors [25,26].
In view of the magnitude of the health problem of CRC, in 2003, the European Union urged member states to implement population-based screening programmes using FOBT for the early detection of CRC in men and women aged 50 to 74 years [27]. In 2004, the first clinical practice guidelines for CRC prevention were published in Spain [28], and in 2006, the Spanish Ministry of Health included in its published cancer strategy the objective of performing population-screening pilot studies with FOBT to establish the best method of implementing a population-based programme. One of the latest experiences that has been carried out is the colorectal exam at the Hospitalet de Llobregat's pilot study of cancer screening, promoted by the Department of Health and Social Security of the Generalitat of Catalonia. This experience may provide information in the near future on the acceptability and feasibility of such programmes [29].
The 2009 update of the Spanish cancer strategy approved the launch of populationbased programmes with the aim of achieving 50% coverage of the target population by 2015 [30]. However, a level of participation that is greater than 60% is required to achieve a cost-effective reduction in CRC mortality at the population level [31], and in 2021, the Spanish Ministry of Health raised its target to 65% coverage [32]. The increasing rates of CRC incidence and survival, as well as the high prevalence of known risk factors (inadequate diet, being overweight, having a sedentary lifestyle) and the availability of an effective diagnostic technique, highlight the need to extend population-based early detection programmes to achieve 100% coverage of the target population [33]. Health literacy (HL) has been investigated among the factors that could influence such participation [34].
Population-based screening has been shown to reduce the incidence of and mortality from CRC [2,35,36]. Strategies have been developed to improve the implementation of these prevention programmes, successfully increasing participation in CRC screening in Spain [37]. To ensure the implementation of screening programmes for CRC, The PRECEDE-PROCEED Model provides an excellent framework for health intervention programmes, especially in screening settings, and could improve our understanding of the relationship between variables such as knowledge and screening, highlighting the active role of patients [38].
Previous studies agree that the appropriate age to start screening is 50 years, since 90% of cases occur in people over this age [3,4]. The literature is less conclusive on the age at which screening should end and the best screening tests. In Spain, CRC screening is currently carried out in people aged between 50 and 69 years through a biennial immunological FOBT. People with a positive result have a colonoscopy under sedation. Any person who has already undergone a complete and high-quality colonoscopy with no significant findings is recommended to rejoin the screening programme after 10 years [5].
At present, screening coverage data are available for specific Spanish regions, but not for the whole country [39,40]. For this reason, we aimed to determine the CRC screening coverage of people aged between 50 and 69 years who were living in Spain in 2017 and to describe the factors associated with not having had an FOBT.

Materials and Methods
We performed a cross-sectional study using the Spanish National Health Survey 2017 (ENSE17) [41], carried out by the Spanish National Statistics Institute [42]. The ENSE17 data were collected through 23,089 computer-assisted, interviewer-administered, personal interviews that were carried out between October 2016 and October 2017 in 10,595 men and 12,494 women aged 15 years or older.
Our study included men and women aged between 50 and 69 years, who are considered the medium-risk population for CRC and are therefore eligible for stool occult blood testing, according to the 2016 Programme of Prevention and Health Promotion (PAPPS) [43]. Respondents with missing data were excluded.
The dependent variable of our study was whether or not respondents had had an FOBT. This information was collected through question 95 of module Q of the ENSE17, regarding preventive practices: "Have you ever had a faecal occult blood test?", to which respondents could answer "Yes", "No", or "Don't know/no answer" (DN/NA).
The explanatory variables were divided into four modules. Sociodemographic variables were age, sex, body mass index (underweight/normal, overweight, obese, DK/NA), country of birth (Spain, outside Spain), Spanish autonomous community of residence, marital status (single, married, widowed, separated, divorced), socio-occupational class (manager with 10 or more employees, manager with fewer than 10 employees, intermediate occupation or own-account worker, skilled technical occupation, skilled primary sector worker, nonskilled worker, DK/NA), and educational attainment (illiterate, incomplete primary education, primary education, compulsory secondary education, upper secondary education, intermediate vocational training, higher vocational training, university education). Health determinants were main daily activity (mostly sitting, mostly standing, walking with some weight, manual labour, not applicable), physical activity in free time (none, occasional, several times a month, several times a week), consumption of fruit and vegetables (neither fruit nor vegetables every day, fruit or vegetables every day, fruit and vegetables every day), smoking (daily smoker, nondaily smoker, ex-smoker, non-smoker), and alcohol consumption (5-6 days/week, 3-4 days/week, 1-2 days/week, 2-3 days/month, once a month, less than once a month, never in the last 12 months, never). Healthcare variables included use of healthcare services (hospital admissions and emergency department visits in the last year, primary care visits in the last month) and specific preventive or diagnostic procedures (flu vaccination in the last campaign; colonoscopy ever; blood/urine tests, X-ray, computed tomography scan, ultrasound, magnetic resonance imaging in the last year). Finally, the health status module included variables related to self-perceived health (very good, good, fair, poor, very poor) and comorbidities (diabetes mellitus, high blood pressure).

Statistical Analysis
We performed a descriptive analysis of all variables by calculating absolute frequencies and percentages. To identify the factors associated with having had an FOBT, we prepared contingency tables and applied the Chi-squared test. To estimate the magnitudes of the associations of different variables with not having had an FOBT, we fitted Poisson multivariable models with robust variance (Petersen 2008) [44]. Prevalence ratios (PRs) were calculated with their 95% confidence intervals (95% CIs). We used a stepwise variable selection procedure based on the Akaike Information Criterion, taking into account the possible multicollinearity of the variables. Goodness-of-fit and classification indicators such as the area under the receiver operating characteristics curve (AUC) were calculated. For the statistical analysis, we used the software environment R version 3.0.2 ( R Foundation for Statistical Computing, Viena, Austria).

Discussion
The results of this study show that the CRC screening coverage of the Spanish population aged 50 to 69 years was 29% in 2017. The factors independently associated with not having had an FOBT were the respondents' autonomous community of residence, age, and country of birth, as well as whether the respondent had been vaccinated against the flu in the last campaign, had ever undergone a colonoscopy, had had an ultrasound scan in the last year, or had seen their primary care physician in the last month.
According to our findings, the prevalence of participation in CRC screening in Spain in 2017 was far from the objective of 65% proposed in the last update of the Spanish Health Ministry's cancer strategy [32]. For programmes to be considered effective, the European guidelines for the quality assurance of CRC screening and diagnosis recommend participation rates above 65% and specify a minimum acceptable level of 45% [45]. The participation rates for CRC screening programmes in European Union member states range from 7.2% to 90.1%, with considerable variability between countries [46].
While previous studies in the Spanish population found that women were more likely to participate in CRC cancer screening programmes [24,[47][48][49][50], sex was not associated with having had an FOBT in our study. Regarding country of birth, we found that nonparticipation in the screening programme was associated with being born outside of Spain, which is in line with the findings reported by Rosano et al. in 2017 [51]. With respect to age, lower participation in screening was associated with being aged 50-59 years versus 60-69 years, as in previous studies that found a positive association between participation and age [48,49,51]. In contrast, the reported CRC screening coverage in Belgium in 2017 was 30% in people aged 55 to 59 years, 26.6% between 60 and 64 years, 25.1% between 65 and 69 years, and 52.6% between 70 and 74 years [52], with the highest values found in the youngest and oldest people. In younger people, feeling healthy and less vulnerable to disease could be a barrier to participation [49].
We found a lower coverage in smokers, like other authors [53,54], and in people who did not eat fruit or vegetables every day. This could be because these groups are generally less concerned about their health and therefore tend to participate less in preventive health programmes.
Concerning the use of healthcare services, lower screening coverage was associated with not having been vaccinated against flu in the last campaign, never having had a colonoscopy, not having had an ultrasound scan in the last year, and not having visited a primary care physician in the last month. These data could indicate that people who have less contact with healthcare professionals participate less in screening programmes, and that receiving information on screening from a primary care physician encourages participation. This highlights the important influence of primary care on adherence to screening programmes, as shown in other studies [53,[55][56][57]. The factor of not accessing preventive services within the stipulated period of time is associated with low participation in screening programmes, since it is correlated with the individual perception of health.
HL has been proposed as a predictor of an individual's health status [58]. It can be defined as "people's ability to make judgements and take decisions in everyday life concerning healthcare, disease prevention, and health promotion to maintain or improve their quality of life" [59]. For this reason, low levels of HL have been associated with several adverse health outcomes, such as increased hospitalization, higher rates of medication nonadherence, and lower uptake of preventive interventions, including cancer screening programmes [34].
We found no association between not having had an FOBT and having chronic diseases such as diabetes, high blood pressure, or obesity, whereas previous studies have found that people with chronic diseases are more adherent to CRC screening programmes [60,61].
Regarding socio-occupational class, the multivariable analysis in our study found no independent association with failure to have an FOBT. In contrast, a previous study carried out in Barcelona (Spain) concluded that the most and the least disadvantaged groups were less likely to participate in CRC screening programmes, possibly due to a lack of knowledge and understanding in the case of the first group and, in the case of the last group, because they have access to private healthcare [62].
In our study, we found varying coverage among the different autonomous communities. The uneven implementation of screening across the country is due to the fact that each autonomous community has a regional government that independently manages its own healthcare system, including preventive activities [63]. The strategies implemented in the autonomous communities with higher coverage include those aimed at improving healthcare access among vulnerable people, identifying the barriers to and facilitators of participation in screening, and reducing inequalities in participation. The associated activities include holding meetings with political leaders of the autonomous communities; sending information to be distributed throughout the municipalities in collaboration with city councils; sending tests to homes and enabling participants to submit samples in all primary care centres; sending tests to care homes; conducting cross-sectional analyses of participants and non-participants to identify their profiles and thus develop specific strategies to increase uptake; increasing participation through informative talks in the press and on the radio; implementing the practice of reminder calls from medical and/or nursing staff; holding talks in collaboration with the Spanish Association Against Cancer (AECC); and ensuring that in all primary care centres, people eligible for screening are educated about its importance before being invited for the test [24,47,49,55,64]. In the autonomous communities with lower participation, these activities are only partially implemented, if at all.
The present study can be included in the above-mentioned strategies, as we aimed to identify the factors associated with failure to have an FOBT and thus understand how to increase coverage in the Spanish population. The autonomous communities with lower participation in the screening programme could try to increase uptake by adopting the most effective strategies applied in the autonomous communities with higher participation. As the characteristics linked to not having had an FOBT in our study were being young and not making frequent use of healthcare services, the use of alternative channels to disseminate information about CRC screening programmes could help to raise awareness of their importance. We were unable to assess the reasons for non-participation or the medical histories of people who chose not to participate; this information could be useful for future surveys.
Our study has some limitations. Firstly, because this is a cross-sectional study, we were unable to establish a causal relationship between screening and the variables studied. Secondly, the fact that our results are based on self-reported data collected through a survey means they may be subject to recall bias. However, self-reported chronic diseases have been considered a useful source of information for prevalence studies and have been validated by different studies [65]. One strength of our study is that our source of data-the ENSE17-is administered in all autonomous communities and is one of the largest data-collection programmes of the Spanish Ministry of Health. The results of this national survey have been validated and are considered an essential element of territorial cohesion for population monitoring.

Conclusions
According to the data of the 2017 ENSE, the coverage of CRC screening in the Spanish population aged 50 to 69 years was low and varied among the different autonomous communities. The factors associated with failure to have an FOBT were young age, having been born outside of Spain, not having been vaccinated against the flu in the last campaign, and not making frequent use of healthcare services.
Supplementary Materials: The following supporting information can be downloaded at: https://www. mdpi.com/article/10.3390/ijerph19095460/s1, Table S1: Absolute and relative frequencies of respondents who had/had not had a faecal occult blood test (FOBT) according to all explanatory variables.  Institutional Review Board Statement: The study was conducted according to the guidelines of the Declaration of Helsinki. This study was exempt from ethics review because there were no human participants and only sources of data were used.