Preferences for Colorectal Cancer Screening Modalities Among the General Population in Saudi Arabia

Background: Colorectal cancer (CRC) could be a leading explanation for cancer-related death. Numerous studies have shown the benefit of early screening for colorectal cancer in reducing mortality. Screening for colorectal cancer is a rational and cost-effective strategy for reducing the incidence of colorectal cancer and related mortality. Despite endorsement by academic and healthcare organizations, patient awareness and compliance with screening are low, partly due to patient-related barriers to screening. Aim: This study aimed to explore the preferred screening method for colorectal cancer in Saudi Arabia in general. Methods: This is a cross-sectional study conducted among the Saudi adult population from September 2021 through February 2022. A self-developed questionnaire was distributed among the population using an online platform. Data were tabulated in Google Forms, and all statistical analyses were performed using SPSS version 26 (IBM Corp., Armonk, NY). Results: During this study, data from 10,781 participants were analyzed. Among them, the most preferred screening modality for colorectal cancer was the stool fecal immunochemical test (41.7%) and the most suitable (33.5%). The most commonly mentioned qualities that influenced choosing a particular screening test were "how the test was performed" (50.4%). Conclusion: Because the stool fecal immunochemical test is the most preferred screening modality for colorectal cancer, this study could serve as a database to aid in the implementation of a colorectal cancer screening program that meets the preferences of the general population of Saudi Arabia.


Introduction
Colorectal cancer (CRC) could be a leading explanation for cancer-related death. Numerous studies have shown the benefit of early screening for colorectal cancer in reducing mortality. However, global screening rates are still low. This study assesses the awareness of CRC risk factors, warning signs, attitudes towards CRC guidelines and screening modalities, and perceived benefits of the screening to identify the most preferable CRC screening test [1]. In addition, this study will investigate screening intentions and previous uptake of CRC screening tests in the general population in Saudi Arabia [2]. Screening for colorectal cancer could be a rational and cost-effective strategy for reducing the incidence of colorectal cancer and related mortality. Despite endorsement by academic and healthcare organizations, patient awareness and compliance with screening are low, partly thanks to patient-related barriers to screening [3]. Early detection of CRC is recommended due to the increased risk of postoperative sepsis after surgery for colon cancer in individuals over 65 who have a BMI ≥ 30 kg/m2, an ASA score of 2 or higher, and additional comorbidities such as diabetes and cardiovascular disease [4,5]. So, it is crucial to understand preferences for screening within the Saudi population, where relatively few people have had CRC screening. A key factor driving the success or failure of any screening program is patients' willingness to undergo the screening test [6]. People in Saudi Arabia should be more aware of colorectal cancer incidence and prognosis, as well as willing to undergo screening with different tests [7]. Only if evidence-based initiatives like the mailed fecal immunochemical test (FIT) outreach are put into practice will they have an impact on health outcomes. However, efforts to put programs in place are frequently constrained by organizational-level issues [8]. There are several colorectal cancer screening procedures available, each with a distinct level of accuracy, suggested frequency, and administration. These tests include annual fecal occult blood testing (FOBT), flexible sigmoidoscopy (FSIG), every five years, and both annual FOBT and FSIG. According to a review from the USA, the five screening methods listed below were all acceptable and fairly equally cost-effective for "average-risk" people starting at age 50: fecal occult blood testing every year, flexible sigmoidoscopy every five years, a combination of fecal occult blood testing every year and flexible sigmoidoscopy every five years, colonoscopy every ten years, and double-contrast barium enema every five to ten years [9]. Based on the research on screening for colorectal cancer in the USA, a comparison was done on a set of personal traits that link with preferences for colorectal cancer screening test qualities, previous colorectal cancer screening behavior, and future colorectal cancer screening intentions [10]. Recommendations for colorectal cancer screening encourage patients to decide on various screening methods that support individual preferences for benefits, risks, screening frequency, and discomfort. A model was devised as an instance of how individuals with varying tolerance for screening complications risk might choose their preferred screening strategy [11][12]. In order to evaluate patients' preferences for mCRC treatment and the relative importance of cost, efficacy improvement, side effect avoidance, and therapeutic convenience, a study was conducted in Singapore to examine patient preferences and the anticipated relative uptake for targeted therapies in mCRC [13]. The adoption of colonoscopy as the primary method for screening for colorectal cancer (CRC) without evidence of patient preferences has been discussed in several studies. An investigation into patients' preferences for the National Cancer Screening Program's (NCSP) CRC primary screening test was carried out in Korea [14]. Furthermore, the majority of the previous studies in Saudi Arabia recruited visitors to shopping malls who were not representative of the general population to assess the knowledge and determinants of CRC screening among the population in Jeddah, Saudi Arabia [15]. A significant influence is generated on the patient-physician interaction by primary care physicians (PCPs), who play a crucial role in providing colorectal cancer (CRC) screening. For instance, colorectal cancer was the second most common cancer in men and the third in women in Thailand. Early screening and surveillance can reduce colorectal cancer morbidity and mortality, and the number of patients with colorectal cancer of all genders has been rapidly increasing. The standard screening guideline for colorectal cancer recommended by national expert groups is to start in asymptomatic, average-risk adults at the age of fifty by the primary care physicians who have a role in arranging and referring patients for colorectal cancer screening. Colonoscopy is the most preferred screening tool [16]. Patients with limited literacy skills are less likely to be knowledgeable about CRC screening compared to patients with adequate literacy skills. A study was conducted in the USA about the effect of health literacy on knowledge of and receipt of colorectal cancer screening. An estimated half of Americans have limited health literacy skills. Low literacy has been associated with less receipt of preventive services. So, primary care providers should ensure patients' understanding of CRC screening when discussing screening options [17][18]. The discussion of patient values and preferences is a critical step in engaging patients to participate in medical decision-making [9]. In conclusion, the public of Saudi Arabia has become more aware of the growing threat of colorectal cancer (CRC) because it is widely thought to be a deadly disease with life-threatening side effects from chemotherapy. It is interesting to note that diagnosis at an early age is noted in both old and new epidemiological reports. The right side of the colon is increasingly recognized as an unusual presentation of CRC. Saudi cancer registry data revealed that males and females in the kingdom experience CRC at a rate of 51% and 62%, respectively, compared to worldwide rates, with 65% and 77% mortality rates reported, respectively, in 1993-2003. All genders are vulnerable to CRC. Despite that, Saudi females have the highest incidence and mortality rates when compared with other populations in less developed areas. Saudi Arabia has public and private tertiary healthcare centers that offer colonoscopies in major cities. But, in the absence of an organized screening program on a national level in Saudi Arabia, colonoscopy is not accessible for screening purposes. Additionally, performing a screening colonoscopy privately would be prohibitively expensive for an average-income individual. There is no actual explanation for the barriers to early detection or organized screening yet. Our study intended to explore the preferable screening tool for CRC. We hypothesize that FIT would be the most preferred CRC screening test among the general population of Saudi Arabia.

Materials And Methods
The population of Saudi Arabia was studied in this descriptive cross-sectional study. The study was carried out in Saudi Arabia between September 2021 and February 2022. A self-administered software questionnaire was distributed to the general public at random via social media. The mid-year population in Saudi Arabia in 2020 was used for sample size calculation, and the values were placed in the level of precision formula with a margin error determined as 5% and a confidence level of 95% that yielded a sample size of 385 [19]. The total number of participants in this study was 10,781. Before the online survey began, all participants were given a webpage describing the study's goals and asked for informed consent. Every survey response was connected to an internet protocol in order to prevent responses from being repeated. The Medical College Institutional Review Board at Al-Imam Mohammad Ibn Saud Islamic University, Riyadh, Saudi Arabia, approved this study protocol (project number: 99-2021).
The general population in Saudi Arabia of either gender, aged 18 years and above, who were able to read and write Arabic (the official language of Saudi Arabia) were included in the study. Adults outside of Saudi Arabia and those less than 18 years old or diagnosed with colorectal cancer were excluded from this study.
A self-developed questionnaire included 22 questions: 13 asked about socio-demographic characteristics, and the other 9 were about the preferences of the general population of Saudi Arabia regarding colorectal screening methods. Two consultants validated this questionnaire, and a pilot study was performed on 20 people prior to distribution.
The data were analyzed using Statistical Packages for Social Sciences (SPSS) version 26 (IBM Corp., Armonk, NY, USA). Both descriptive and inferential statistics were conducted. In descriptive statistics, all categorical variables were presented as numbers and percentages. The relationship between the colorectal cancer screening preference and the socio-demographic characteristics of participants has been examined using the Chi-square test. A p-value cutoff point of 0.05 at 95% CI was used to determine statistical significance.

Results
In total, 10,781 participants were involved. Table 1 presented the socio-demographic characteristics of the participants. The most common age group was 18-25 years old (55.9%), with females dominating the males (67% vs. 33%). Respondents living in the western region constitute 24.5%, while those living in the northern region constitute 22.8%. Most respondents were of Saudi nationality (96%) and nearly two-thirds had bachelor's degrees (64.1%). The proportion of participants who were working in the medical field was 3.8%. Furthermore, the majority of the respondents were unemployed (62.5%), and 63.7% had a monthly income of less than 6,000 SAR per month. The prevalence of participants who had an associated chronic disease was 17.4%. Additionally, a family history of colorectal cancer was found among 4.7%.

Study variables N (%)
Age group

FIGURE 1: Specific type of chronic disease
In Figure 2, respondents believed that the most common risk factors for colorectal cancer were physical inactivity (23.6%) and smoking (10.4%).

FIGURE 2: Knowledge about the risk factor of colorectal cancer
In Figure 3, respondents preferred the stool fecal immunochemical test because it was more accurate (47.9%) and because they had problems with other screening methods (40%). Other participants preferred fecal stool occult blood in terms of screening interval (41.7%), preparation required prior to screening (41.2%), complications from other screening modalities (40.6%), and screening method (39.2%).

FIGURE 3: Preferred screening test modality according to a pattern of examination
Participants' behavior regarding colorectal screening was given in Table 2. It can be observed that most of the respondents did not discuss the early colorectal cancer screening methods with their doctors (92.8%), and most of them had not tried the screening test (93.4%), with only 2.3% of the respondents having tried the fecal stool occult blood test. The most commonly mentioned qualities that influenced choosing a particular screening test were "how the test was performed" (50.4%) and the accuracy of the test (46.9%). Stool fecal immunochemical testing was the most common (33.5%) and preferable (41.7%) screening modality in the study population.

Variables N (%)
Have you ever discussed with your doctor about early screening for colorectal cancer?  When measuring the relationship between the most preferred screening modality and the demographic characteristics of the participants, we found that the prevalence of respondents who preferred the stool fecal immunochemical test was more common among those who were 18-25 years old (p < 0.001), females (p < 0.001), those living in the Western region (p < 0.001), unemployed participants (p < 0.001), those who earned less than 6,000 SAR per month (p < 0.001), and those with a family history of cancer (p = 0.001), while the prevalence of respondents who preferred colonoscopy was more common among those who have associated chronic diseases (p = 0.003) ( Table 3).
Most preferred colorectal cancer screening modality P-

Discussion
This study evaluated the general population's preference for CRC screening methods. It is a representative study of Saudi Arabia due to the high number of responses and their equal distribution throughout the country. Studies suggest that patient choices for CRC screening modalities vary by country [20][21]. In our study, stool FIT was the most preferred screening modality by the general population (41.7%), while stool fecal occult blood testing (31%) and colonoscopy were the second and third options. Several papers indicated colonoscopy as the most preferred choice of screening modality for CRC [14][15][22][23][24]. Wong et al. [25] further indicated that the screening method using colonoscopy could be a better choice due to its ability to eliminate the adenomatous polyp. However, some papers suggested that FIT is the more effective CRC screening method [21,26], which was consistent with our findings.
The FIT screening method was more prevalent in the younger age group, females, unemployed respondents, and those who had a low-income level, while colonoscopy was more preferred by those who had associated chronic diseases. The preference of low-income residents for the FIT supports its usefulness for easing the economic burden. This is in contrast with the paper of Cho et al. [14]. They reported that FIT was more preferred by elderly patients, while colonoscopy was preferred by patients with higher education levels, a higher income level, or individuals with a family member or acquaintance with a history of CRC. On the other hand, we noted that the preference for the CRC screening method based on nationality and educational level did not vary significantly among the groups, which was in accordance with the paper of Al-Masoudi et al [15]. Although our study established FIT as the most suitable (33.5%) and preferable (41.7%) CRC screening method, the overall concern of respondents when choosing a screening modality is about how the test will be performed (50.4%) and the accuracy of the screening method (46.9%). As Tfaily et al. [1] emphasized, awareness about CRC screening is important to ease down the stigma of shame and embarrassment that attests to being the major stumbling block toward the willingness to undergo a CRC screening test.
The surgical field has witnessed fast and ongoing technological advancements in recent years. Adopting the IoT concept in surgical practice was one of the most revolutionary developments. Less time is spent doing surgery, more people have access to high-quality care, and surgical education is safer and more efficient. These are the key tangible benefits of IoT integration [27]. Thus, to add to this field through our study, we modified the application of FIT in the country and provided a home take-up, delivery of the sample test to the hospital, and the reach of its results through a phone application. With this addition, we eased access to the screening test at a low cost, which benefits all socioeconomic levels in the country. In low-income, uninsured populations, Van der Steen compared the advantages and effectiveness of the fecal immunochemical test to the colonoscopy. It turned out that the FIT prevented more CRC deaths than the colonoscopy, which only screened those who could afford it and thus only resembled a small portion of the targeted population [28]. The highest responses we got in our study were from the young age group, and that can be explained as they represent the largest number in the population of Saudi Arabia [19]. Most of them preferred FIT as a screening method for CRC, which supports the initiation of a national colorectal cancer screening program that suits the preferences of the population and meets the requirements of public and private healthcare centers in Saudi Arabia.
Respondents preferred FIT due to its accuracy (47.9%) or being upset with other screening modalities (40%). Others preferred fecal occult blood tests due to the duration of the screening (41.7%) and preparation requirements before the screening (41.2%). These findings are almost consistent with the paper of Calderwood et al. [22]. Based on their accounts, patients who preferred colonoscopy chose accuracy (76%) and frequency of testing (10%), whereas patients who preferred a stool-based test chose discomfort (52%) and complications (23%) as the most important features. In another published study done in the United States [11], they documented that the majority are more than willing to undergo a colorectal cancer screening test if the test does not involve radiation (73%), does not involve the insertion of a tube or device into the rectum (78%), does not involve a pre-procedural bowel cleansing regimen (73%), and does not involve sedation (60%). However, in Korea [14], researchers indicated that 12.9% of patients who underwent screening tests had bad experiences with both FIT and colonoscopy. Despite some barriers to undergoing CRC screening, the importance of taking the test is vital. As Hyams et al. [24] suggested, the effectiveness of the screening method is the most important criterion for making a decision.
Moreover, most of the respondents (92.8%) did not discuss the early colorectal cancer screening methods with their doctors for CRC, and only 2.8% were able to do so. Likewise, 93.4% of the respondents have not tried the CRC screening. Perhaps this is because the majority of our participants were in the younger age group (18-25 years) and have not reached the required age bracket for CRC screening practices. According to publications, patients are more than willing to undergo CRC screening [2,11], but the actual screening test did not reach the required target [1,2].
The risk factor for CRC is important to tackle since it could be associated with the willingness to undergo CRC screening. In our study, physical inactivity (23.6%), smoking (10.4%), and eating red meat (8.1%) were the most commonly mentioned risk factors for CRC. Eating red meat, a low-fiber diet, and a low intake of vegetables and fruits were determined as the most common risk factors for CRC, which were reported in Korea [14], Spain [2], and Lebanon [1].

Limitations
First, an unavoidable selection bias existed in our web-based survey because the study only involved participants who had access to the internet. Second, the results are based on a single survey of the population of Saudi Arabia. Therefore, the generalization of the results of this study to other countries is limited. Finally, the researchers developed the survey because there is no previous well-established, standardized questionnaire covering this topic to the best of our knowledge.

Conclusions
Stool fecal immunochemical testing was preferred by the general population more than fecal occult blood tests or colonoscopies. This preference is likely demonstrated by females who are younger, unemployed, have a low monthly income, and have a family history of cancer. This research could represent a database that helps with the initiation of a colorectal cancer screening program that suits the preferences of the general population of Saudi Arabia. Moreover, awareness campaigns are necessary to increase the willingness of the general population to undergo colorectal cancer screening, specifically after the age of 45. Finally, early screening and detection are necessary to reduce the burden and costly treatment of any disease, including CRC.

Informed consent
We are a research group from Imam Mohammed Ibn Saud Islamic University -College of Medicine. We like to invite you to participate in our survey which is targeting above 18 years old Saudi citizens and residents who are free of active colorectal cancer.
We would like you to answer questions regarding your demographic data, medical history, and your preference of the colorectal cancer screening method.
If you agree to participate please know that the survey will not take more than 5 minutes and all answers will be handled with privacy and discreteness and will be only accessible by the research team only. Also, your participation is not mandatory and you have the right to not participate or quit anytime you want.
Thank you for your time and your cooperation.     Based on the following information, which would suit you more?

Fecal stool occult blood None
Stool fecal immunochemical test None Sigmoidoscopy You need to empty your colon, which can be done by following a clear liquid diet the day before, take a laxative the night before the exam, and use an enema kit.

Colonoscopy
You need to empty your colon, which can be done by following a clear liquid diet the day before, take a laxative the night before the exam, and use an enema kit. Must come with an escort because sedation is given.