Knowledge, Attitude, and Practice of Colorectal Cancer Screening Among Primary Healthcare Physicians in Riyadh Second Health Cluster

Background: Colorectal cancer is the third common cancer, and the second common cause of cancer death in the world. According to the 2014 Cancer Incidence Report of the Kingdom of Saudi Arabia, colorectal cancer account for 11.5% from all cancers reported among Saudi nationals. By the year 2030, the incidence of colorectal cancer could increase fourfold among both genders. Aim: The study aimed to conduct to understand the knowledge, attitude, and practice of primary healthcare physicians regarding colorectal cancer screening in Riyadh Second Health Cluster in the city of Riyadh, Saudi Arabia. Materials and methods: A cross-sectional study design, probability proportional to size sampling at the cluster zones level and convenient sampling for the physicians, were used among physicians working in the primary healthcare centers in the city of Riyadh between October 2022 and November 2022. Result: Of the 213 respondents, the mean age of the physician was 35, the majority were males (59%), Saudi Arabian nationality (60%), Resident Physicians (54%) and ≤ five years’ work experience (45%). Sixty-four percent of the study participants believe that the majority of asymptomatic average-risk patients have to start the screening at the age of 45 years old. Ninety-seven percent believe that colorectal cancer screening for asymptomatic average-risk patients aged 45 years and older is effective. Ninety-two percent of the physicians perform colorectal cancer screening for asymptomatic average-risk patients aged 45 years. The mean knowledge score is 4.65 (SD=2.33) with a range of 0 to 10. The mean attitude score is 4.19 (SD=1.28) with a range of 0 to 6. Conclusion: The study found that the physicians had higher attitude and practice towards colorectal cancer screening and adequate knowledge towards colorectal cancer screening. The knowledge and attitude scores are associated with practicing colorectal cancer screening.

for diagnosis and early treatment [4]. The median age at diagnosis was 60 years in males and 57 years in females. The recommended screening for colorectal cancer according to national guidelines of the Ministry of Health and guidelines of the American Cancer Society and the US Preventative Services Task Force (USPSTF) starts at age 45 years [5][6][7]. Recommended screening strategies include annual screening with high-sensitivity FOBT; screening every five years with flexible sigmoidoscopy, or screening with colonoscopy every 10 years [6]. The Saudi expert panel suggests not using colorectal cancer screening for asymptomatic persons at average risk aged 70 years or older [7].
Cancer is the second leading cause of mortality after cardiovascular disease [5]. In the year 2015, its incidence was 17.5 million and mortality was 8.7 million cases worldwide [8]. Colorectal cancer is the third most common cancer after lung and breast cancer worldwide, and the second most common cause of cancer death in the world [4]. Among men, it is the second leading cause of cancer death after lung cancer, and among women the third leading cause of cancer death after breast cancer and lung cancer [5,9]. From 2005 to 2015, colorectal cancer had the fourth highest absolute years of life lost among all types of cancer [5]. In 2015, the incidence of colorectal cancer was 1.7 million, and it caused 832,000 deaths worldwide [8]. It is estimated that in the year 2030, there will be 2.2 million incidences and 1.1 million colorectal cancer-related mortality [10].
Colorectal cancer is the most common cancer among Saudi men and the third most common among Saudi women with a constant rise in the incidence for the past few years [11]. According to the 2014 Cancer Incidence Report of the Kingdom of Saudi Arabia (KSA), colorectal cancer accounted for 11.5% of all cancers reported among Saudi nationals [12]. The Riyadh region has the highest incidence rate among females and second highest among males [12]. The incidence of colorectal cancer in KSA has been on a constant rise over the past few years due to possible Westernization of dietary habits and lack of proper screening [13]. The age at the time of diagnosis is lower compared with developed countries [13].
"Past, Present, and Future of Colorectal Cancer in the Kingdom of Saudi Arabia" study was conducted by Ibrahim et al. in the year 2008. The authors compared the colorectal cancer statistics (from 1994 to 2003) from the National Cancer Registry of KSA with the statistics of the United States of America (USA). They demonstrated that the age-standardized rates of colorectal cancer statics doubled from 1994 to 2003, in contrast to the USA where the rates were progressively declining [14]. The authors mentioned that the rate decline in the USA was associated with screening and early removal of the polyps [15]. On the other hand, in KSA, there was a progressive increase in exposure to risk factors and lack of a nationwide screening program. The authors also estimated that by the year 2030, the incidence of colorectal cancer could increase fourfold among both genders [14].
In 2015, Almadi et al. conducted a cross-sectional survey in Riyadh, KSA, to understand the public knowledge, attitudes, and behavior regarding willingness to undergo colorectal cancer screening using the Health Belief Model (HBM) [16]. Five hundred participants were involved in the survey, among them 35.6% of the study population mentioned that colorectal cancer is common [16]. The mean knowledge score was 10.50 (SD=4.4) with the range of lowest score by 2 to the highest score of 23 [16]. The most commonly recognized tool for screening technique was colonoscopy (50.56%), followed by CT colonography (32.7%), stool-based screening (24.7%), whereas the least appreciated method was flexible sigmoidoscopy (14.7%) [16].
In 2019, the gap between knowledge and colorectal cancer screening using the HBM in 2019: A national survey was conducted by Almadi and Alghamdi [17]. It was a huge nationewide survey throughout the KSA in all 13 jurisdictions. 5720 individuals' responded to the survey via an electronic platform [17]. 15.24% of the study participants had already undergone colorectal cancer screening using various screening techniques, mostly colonoscopy (72.73%). The mean knowledge score was 11.05 (SD=4.4) with a range of 1 to 23. Survey participants had a positive attitude toward colorectal cancer screening as well as to colonoscopy screening technique, and 73% expressed willingness to undergo screening in the future. Even though the majority of participants responded with willingness to undergo screening, no significant correlation was found between knowledge and willingness to undergo screening were predicted. Moreover, the majority of the participants mentioned their interest in screening in the survey, on the other hand, the majority of the participants refused the invitation to undergo screening [17].
Federici et al. conducted a survey on colorectal cancer screening knowledge, attitudes, and practices of general practice physicians in Lazio, Italy in the year 2006 among 699 General Practitioners (GPs). Ninetyfour percent mentioned that colorectal cancer could be prevented. GPs who use guidelines in their practice had statistically significantly higher knowledge in oncological screening. Only 25% of the study participants recommended colorectal cancer screening to their patients. The authors mentioned that the "knowledge about screening and use of guidelines as sources of scientific information are important factors to improve attitudes about screening" [18].
In Saskatchewan, 773 family physicians were included in a survey conducted by Deobald et al. to evaluate the current colorectal cancer screening practices and identify barriers to screening to improve current practice. The authors mentioned that the colorectal cancer screening recommended by a family physician was occurring at a low rate [19]. The waiting time for colonoscopy and access are the main barriers to colorectal cancer screening [19]. The authors mentioned that recently introduced FIT test in the province should improve the overall screening but will require further increases in resources and availability of colonoscopy for follow-up of positive results [19].
In Riyadh, KSA, in the year 2014, Demyati conducted a study to "explore the current knowledge, attitude, and practice of family physicians working in family medicine clinics in National Guard Health Affairs (NGHA), Riyadh, toward colorectal cancer screening and to identify the barriers of the screening" [20]. One hundred seventy family physicians were included, the mean knowledge score was 5.02 (SD=2.73) with a range from 0 to 11. Board-certified physicians had higher knowledge scores than other physicians [20]. 94.6% of the physicians considered that the screening for asymptomatic average-risk patients is effective and 81.5% of the physicians prefer structured screening programs over opportunistic screening programs [20]. The mean attitude score was found to be 6.95 (SD=1) and the range was between 4 and 8. More than half (56.2%) of the physicians are not practicing colorectal cancer screening for asymptomatic average-risk patients [20]. The author concluded that the large proportion of family physicians in the study do not recommend colorectal cancer screening, even though the knowledge level and the positive attitude [20].
A study was conducted in Washington State to understand colorectal cancer screening practices of primary care physicians, by Hannon et al [21]. Seventy-six percent of primary healthcare physicians recommended one or more colorectal cancer screening tests in agreement with American Cancer Society guidelines [21]. And the physicians perceived that colorectal cancer screening is essential. The author mentioned that "educating physicians about the power of their recommendations to affect patient behavior may encourage physicians to recommend colorectal cancer screening to more of their patients strongly" [21]. The author also recommended three interventions to improve colorectal screening [21]. The recommendations are educating primary care physicians about screening guidelines, encouraging physicians to discuss colorectal cancer screening with their patients and improving physicians' capacity to track and follow colorectal cancer screening to completion [21].
Studies show that the main reasons for colorectal cancer deaths are mainly a lack of awareness in the population, financial barriers, and lack of knowledge of colorectal cancer screening guidelines among healthcare physicians and nurses [16,17,22]. Also, a majority of the study authors suggest that early detection of colorectal cancer and educational campaigns plays a huge role in preventing colorectal cancer mortality rate [17,22]. Primary healthcare physicians have an important role in screening practice due to frequent contact with a large population of patients. The involvement of primary healthcare physicians in screening implementation has been recommended by several guidelines [20].
Several studies assessed the knowledge of colorectal cancer and its screening among the general public in KSA [16,17]. And a study conducted by Demyati explored the current knowledge, attitude, and practice of family physicians working in family medicine clinics in National Guard Health Affairs (NGHA), Riyadh [20]. KSA lacks the study knowledge, attitude, and practice of colorectal cancer screening among primary healthcare physicians.
Based on the gap in the literature, the study aimed to understand the knowledge, attitude, and practice of primary healthcare physicians regarding colorectal cancer screening in Riyadh, Saudi Arabia.
The specific research objectives are as follows: 1. To assess the current knowledge and attitude of physicians working in primary healthcare centers of Riyadh Second Health Cluster in the city of Riyadh toward screening for colorectal cancer.
2. To determine the practice and adherence to national or international screening guidelines among physicians working in primary healthcare centers of Riyadh Second Health Cluster in the city of Riyadh toward screening for colorectal cancer.
3. To identify the current barriers to implementing colorectal cancer screening recommendations in primary healthcare centers of Riyadh Second Health Cluster in the city of Riyadh to improve current practice.

Study design
A cross-sectional descriptive study design was used to assess the knowledge, attitude, and practice among primary healthcare physicians working in Riyadh Second Health Cluster in the city of Riyadh, Saudi Arabia between October 2022 and November 2022 regarding colorectal cancer screening.

Study setting and population
The study participants are primary healthcare physicians working under the primary healthcare centers of Riyadh Second Health Cluster in the city of Riyadh in the five zones (zone one, two, three, four, and five) of Riyadh city.

Inclusion criteria
Physicians working in Primary Healthcare Centers (PHC) of Riyadh Second Health Cluster in the city of Riyadh who are practicing as residents, registrars, or consultants.

Exclusion criteria
Physicians not available on the date of data collection, physicians on vacation, or physicians who refused consent.

Sample size estimation
A total number of 356 primary healthcare physicians were registered with Riyadh Second Health Cluster in the city of Riyadh at the time we conducted our survey. The sample size was calculated assuming the prevalence of 44% (according to a study conducted by Demyati that reported that 56.2% of the physicians are not practicing colorectal cancer screening for asymptomatic average-risk patients), a precision of 7%, an alpha level of 5%, assuming non-responding physicians 10%, the calculated minimum sample size is 170 physicians [20].

Sampling technique
The sampling technique is probability proportional to size sampling at the cluster zones (five zones in the city of Riyadh) level. A list of total number of physicians in each zone was obtained from the Riyadh Second Health Cluster and PPS was applied to get the number of physicians to be selected from each sector. This was 43 for the Zone One, 36 for the Zone Two, 30 for the Zone Three, 27 for the Zone Four, and 34 for the Zone Five. Then, four to six of the largest PHCs were selected in each zone. Then, depending on the sample required, the number of physicians who met the inclusion criteria from each PHC was selected conveniently.

Data collection tools
The questionnaire contains questions regarding the demographic characteristics of the physician and cancer screening knowledge, attitude, current practice, and barriers to practicing screening of colorectal cancer of the physician. The items of the questionnaire were adapted from a validated questionnaire of a survey conducted by Demyati in 2014 and entitled "Knowledge, Attitude, Practice, and Perceived Barriers of Colorectal Cancer Screening among Family Physicians in National Guard Health Affairs, Riyadh" [20]. These items were adapted with permission from the author and were customized by adding and eliminating questions to be in line with the characteristics of PHCs of Riyadh Second Health Cluster. A pilot study was conducted on 10 physicians to check understanding of the questionnaire. The questionnaire contains the following domains: Domain 1: demographic characteristics: Age, Gender, Nationality (Saudi, Non-Saudi), Medical degree, Zone and Years in practice.

Data Management
All data from the questionnaire were entered into an Excel spreadsheet (Microsoft, Redmond, WA, USA) and to check for the accuracy of the entered data, randomly 10% of the questionnaire was selected and rechecked. For statistical analysis we used SPSS v.20 (IBM Corp., Armonk, NY, USA).
The primary outcome was the practice of colorectal cancer screening among PHC physicians. Secondary outcome variables included the knowledge and attitude scores of the physicians. The variables like age, gender, nationality, medical degree, zone, and years in practice are considered control variables according to the literature.

Statistical Analysis
The descriptive analysis was performed and presented demographic data of the physicians. Continuous variables were presented by means and standard deviations, and knowledge and attitude scores are compared with control variables using independent t-tests and ANOVA. Categorical and ordinal variables were presented by percentages, and the primary outcome variable practice was compared with control variables using Chi-square (χ2) tests.
The knowledge score was computed by giving one point to the correct answers and zero points to the wrong answers and for the option "not sure." The items included for knowledge score calculation are as follows, 45 years of age as starting age for asymptomatic average-risk patients screening, aware about stopping age for screening, aware about FOBT types Guaiac FOBT and FIT, aware about FOBT office card and FOBT home kit, ordering two samples for each FOBT, FBOT screening annually, flexible sigmoidoscopy screening every five years, and colonoscopy screening every 10 years. There were 10 items, with a minimum score of zero and a maximum score of 10. The items included in the knowledge score are based on the prior study [20].
The attitude score was computed by giving one point for the correct answer and zero points for the wrong answers and the option "not sure." The items included for attitude score calculation are as follows: CRC screening is effective for the asymptomatic average-risk patient, FOBT is effective, flexible sigmoidoscopy is effective, colonoscopy is effective, double-contrast barium enema is effective, and CT-colonography is effective. There were six items, with a minimum score of 0 and a maximum score of 6. The items included in the attitude score are based on the prior study [20].

Ethical considerations
This study was conducted with the ethical standards mentioned by the Ministry of Health (MOH) and the local Institutional Review Board (IRB) Ethical approval for this study was obtained from King Fahad Medical City IRB, Saudi Arabia (approval 22-498E). Consent was obtained from all participants before participating in the study. Participants were informed of their right to refuse participation or withdrawal from the study at any time without any penalties or consequences. The participants were made aware of the anonymity of their participation and informed that under no circumstances will any of their personal identifying information be collected or revealed or published. No incentive was given to the participants for participation. All the data collection forms were kept under strict confidentiality, accessible only to the researcher. The study did not anticipate any harm to the participants as a result of participating in the study.

Demographic statistics
Overall, 213 participants were included in the study, among them, 37% from Zone One, 23% from Zone Two, 13% from Zone Three, 11% from Zone Four, and 16% from Zone Five. The mean age of the study participants was 35.34 (SD=8.56) with the minimum and maximum age range of the physicians being 25 and 62, respectively. Among them, 59% were male, and 41% were female. The majority of the physicians were considered to be Saudi Arabian nationality with a percentage of 60%. Fifty-four percent of the physicians were reported as residents, 38% as registrars and the rest (8%) as consultants. Experience of the physicians with less than or equal to five years, six to 10 years, 11 to 15 years and more than 15 years of experience are 45%, 27%, 11%, and 16% respectively ( Table 1).

Knowledge of the physicians regarding colorectal cancer screening
Sixty-four percent of the study participants believe that the majority of asymptomatic average-risk patients have to start the screening at the age of 45 years old. The majority of the physicians (60%) also believe that screening for a healthy population is no longer recommended after a particular age, the mean age is 72.97 with the range of 50 to 90 years old.
As per the physician's knowledge, the frequency of screening with FOBT is one year (45%), two years (19%), three years (19%) and not sure (17%). Forty-seven percent of the physicians are aware of the Guaiac FOBT type, and 46% are aware of the fecal immunochemical testing FOBT type. In the ways of conducting FOBT tests, 35% of the physicians were aware the FOBT card can be done in the office during the digital rectal examination, and 48% of the physician agree that the FOBT kits can be given to the patients to do the test at home. For colorectal cancer screening using FOBT, 8% of the physician said that one sample should be ordered, 42% for two samples, 23% for three samples and 28% are not sure about several samples to be collected.
For the assessment of knowledge about the frequency of screening with sigmoidoscopy 2% of the physician answered it should be done every one year, 28% are for every three years, the majority (51%) are for every five years, 7% for every 10 years and 125 are not sure. For colonoscopy, the majority (46%) answered it should be done every 10 years (

Attitude of the physicians regarding colorectal cancer screening
The vast majority of the physicians, around 97%, believe that colorectal cancer screening for asymptomatic average-risk patients aged 45 years and older is effective. For the following screening procedures fecal occult blood testing, flexible sigmoidoscopy, colonoscopy, double-contrast barium enema, and CT-colonography, 80%, 82%, 91%, 25% and 35% of the physicians respectively believe that it reduces colorectal cancer mortality in average-risk patients aged 45 years and older (

Practice of the physicians in colorectal cancer screening
Almost 92% of the physicians perform colorectal cancer screening for asymptomatic average-risk patients aged 45 years and older. Among them, 90% of physicians prefer a structured screening program to conduct colorectal cancer screening, and overall, 77% of physicians prefer a structured screening program. During a typical month, the majority of the physicians (55%) order or perform FOBT screening tests one to five times. In contrast to FOBT, during a typical month, 10% of the physicians refer asymptomatic, average-risk patients for screening sigmoidoscopy, or colonoscopy one to five times. Ninety percent of the physicians do not order or perform sigmoidoscopy or colonoscopy for asymptomatic or average-risk patients ( Table 4).   Barriers to recommending colorectal cancer screening

Attitude score and its comparison with control variables
The mean attitude score is 4.19 (SD=1.28), with a range from 0 to 6. The participants aged >40 years old had significantly higher mean attitude score 4.63 (SD=1.25) compared to those aged ≤40 years (p-value=0.008). In the variable years in practice, ≤ five years had significantly lesser mean attitude score 3.99 (SD=1.15) compared with the >15 years in practice mean score 4.71 (SD=1.18). The other control variable gender (p-value=0.095), nationality (p-value=0.510), medical degree (p-value=0.117), and zone (p-value=0.431), did not show statistically significant mean difference in the attitude score (

Practice in comparison with control variables
Almost 92% of the physicians perform colorectal cancer screening for asymptomatic average-risk patients aged 45 years and older. In comparing practice with other control variables, none of the control variables showed a statistically significant difference. The variables are age (p-value=0.595), gender (p-value=0.745), nationality (p-value=0.681), medical degree (p-value=0.529), zone (p-value=0.643) and years in practice (p-value=0.875). Table 9 summarizes the Chi-Square analysis for practice and its comparison with control variables.

Univariate logistic regression analysis
To predict the association of independent variable (knowledge score and attitude score) with the dependent variable (practicing colorectal cancer screening), we ran a univariate logistic regression analysis. In the analysis, the knowledge score is associated with practicing the colorectal cancer screening (odds=1.310 and the p-value=0.019), which possibly explains that the physicians with higher knowledge scores are more likely to practice colorectal cancer screening. The attitude score is associated with practicing colorectal cancer screening (odds=1.404 and the p-value=0.049), which possibly explain that the physicians with higher attitude scores are more likely to practice colorectal cancer screening (

Discussion
The study assessed the knowledge, attitude, and practice of primary healthcare physicians regarding colorectal cancer screening in Riyadh Second Health Cluster in the city of Riyadh, Saudi Arabia. Using a cross-sectional survey. We surveyed 213 physicians working in PHC in five zones of the city of Riyadh.
The mean age of the physician was 35, the majority were males (59%), Saudi Arabian nationality (60%), resident physicians (54%) and ≤ five years' work experience (45%). There were some differences in the characteristics of the study participants in comparison with other similar studies. In the survey conducted among family physicians in NGHA the majority were females (52%) and the mean age was 38 years old [20]. The study conducted in Saskatchewan among family physicians had 50% of the physicians practicing for around six to 10 years [19].
In the study conducted in Saskatchewan [19], 79.9% of respondents recommending screening beginning at age 50 and 78.9% for the previous study conducted in KSA [20], Riyadh comparatively in our study only 64% of the study participants believe that the majority of asymptomatic average-risk patients, have to start the screening at the age of 45 years old. Around 47% were aware of FOBT types, Guaiac FOBT and 46% FIT, 35% were aware of FOBT office card and 48% of FOBT home kit, 42% were aware of ordering two samples for each FOBT, 45% of the responded for FBOT screening annually, 51% were aware of flexible sigmoidoscopy screening every five years, and 46% aware of colonoscopy screening every 10 years. The study is more or less consistent with the study finding conducted in NGHA [20] The majority of the participants in our study had a positive attitude towards colorectal cancer screening, which is consistent with the other studies, except for the screening method of double-contrast barium enema and CT-colonography; only 25% and 35% of the physicians respectively believe that they reduce colorectal cancer mortality in average-risk patients aged 50 years and older.
Ninety-two percent of the physicians perform colorectal cancer screening for asymptomatic average-risk patients aged 50 years and older contrasting with the previous study in Riyadh where 50% perform colorectal cancer screening [20]. None of the control variables had a significant association with the practice whereas the previous study conducted in Riyadh male participants and physicians aged >40 significantly higher colorectal cancer screening practice. In our study, 45% mentioned that they usually discuss FOBT screening tests with their patients in contrast with the study conducted in Saskatchewan where 71.8% recommend FOBT and 80.8% for the previous study conducted in Riyadh [19,20]. The most preferred screening method in our study is FOBT whereas in the study conducted in Saskatchewan colonoscopy was the most preferred method [19].
The barriers like patient unawareness of colorectal cancer screening (48%), patients do not follow through to complete colorectal cancer screening tests (60%), no policy and procedure in the workplace for screening (45%) and no reminder system in the workplace (45%) are reported that it usually occurs among the majority of the physicians.
The mean knowledge score is 4.65 (SD=2.33) with a range of 0 to 10. None of the control variables showed a statistically significant mean difference in the knowledge score except the variable medical degree; Consultant mean 6.35 (SD=2.23) and Registrar mean 5.38 (SD=2.15) had significantly higher knowledge scores. The mean attitude score is 4.19 (SD=1.28), the participants aged >40 years old and >15 years in practice had significantly higher mean attitude score 4.63 (SD=1.25) and 4.71 (SD=1.18) respectively.

Strengths and limitations
The study utilized a questionnaire from a previously conducted study, which increases the validity of the questionnaire. The study included physicians from all zones of the Riyadh Second Health Cluster in the city of Riyadh, increasing the generalizability of the study findings to the Riyadh city. However, the study cannot be generalized to the whole Kingdom because it is conducted only in Riyadh city.

Conclusions
The majority of the study participants believe that the mainstream of asymptomatic average-risk patients have to start screening at the age of 45 years old. Majority of the physicians believe that colorectal cancer screening for asymptomatic average-risk patients aged 45 years and older is effective, and the physicians perform colorectal cancer screening for asymptomatic average-risk patients aged 45 years. The study found that the physicians had higher attitudes and practice towards colorectal cancer screening and satisfactory knowledge about the screening guidelines. The knowledge and attitude scores are associated with practicing colorectal cancer screening; in other words, the physicians with higher knowledge and attitude scores are more likely to practice colorectal cancer screening.
Based on the study findings, physicians need frequent seminars and continuing medical education programs on colorectal cancer screening. We recommend implementing policies and a reminder system to practice colorectal cancer screening. Furthermore, the patient's knowledge and willingness to be screened for colorectal cancer are important factors in practicing colorectal cancer screening. Therefore, an educational program should be initiated for the general population.

Additional Information Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. King Fahad Medical City issued approval 22-498E. Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.