Knowledge, attitude and practice towards early screening of colorectal cancer in Riyadh

Address for correspondence: Prof. Sulaiman A. Alshammari, Department of Family and Community Medicine, College of Medicine, King Saud University, PO Box 2925, Riyadh - 11461, Saudi Arabia. E-mail: moc.liamg@ashasma

This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.

Abstract

Background and Aims:

Colorectal cancer (CRC) is a common cause of mortality worldwide. It is preventable, treatable when detected early. The aim of this study is to assess knowledge, attitude and practice (KAP) of the participants toward CRC and its early screening, and identify the sources of information on the subjects.

Methods:

We conducted a cross-sectional study on the people 40y old and above at the primary care clinics at King Saud university medical city (KSUMC) in Riyadh. The estimated sample size was 245 subjects whom we requested to complete a self-administered Arabic questionnaire, which consisted of three parts. These were: 1. Demographic data, 2. KAP toward CRC, its early detection. 3 sources of information of the public about colorectal cancer.

Results:

A total of 231 subjects participated; (54.5%) were male (mean age = 50.7 ± 9.8). About 47% of the participants heard about cancer screening, and 45% knew that colonoscopy is used for such purposes. Another 24.2% were aware that occult blood in the stool test is a method of early detection of colon cancer. About 40% to 50% of the subjects were knowledgeable about hazardous factors and cautioning symptoms for CRC. Only 6.5% of the subjects did an early screening for CRC, but 82.9% would do it if their doctor advised them to do so.

Conclusion:

The participant's knowledge and early checkups of CRC are inadequate. They would undergo early screening if their doctors advised them to do so. It is time to develop a national policy for CRC screening involving primary care doctors and utilizing social media to improve people's information.

Introduction

Colorectal cancer (CRC) is the third most prevalent cancer and the fourth most common cause of death worldwide. It would increase by 60% by the year 2030. Researchers from developed countries observed high rates. Furthermore, the magnitude of the condition increase quickly in third world nations which may be due to the selection of western ways of life by their people[1] In Saudi Arabia, colorectal cancer is the second most common cancer. It ranked as first cancer in men 9.9% and third in women 6.4%.[2]

In 2015, the rate was 9.6 per 100,000 individuals, which was almost double the rate of 2001 as illustrated by the age-standardized rate of CRC in the Saudi population.[3,4] Moreover, the Saudi survival rate (44.6%) is worse than that reported worldwide.[5] This could be attributed to patients presented late with their symptoms[6] In Australia, however, the subjects had significant exposure to media their knowledge about screening was insufficient[7] Researchers from West part of Saudi Arabia reported that the individual's level of education and the endoscopic modality chosen influenced the people's awareness of CRC and readiness for screening. Another Saudi study showed that most of the participants were having the desire to undergo CRC screening. Nevertheless, barriers such as inadequate knowledge, embarrassment, and fear prevent them from doing so.[8] Several modalities of screening are available to identify CRC, which improved the survival rate of CRC patients. These tests can be performed routinely before the age of 50 years, especially in high-risk people such as the past history of CRC and polyps.[8,9] Patients with CRC can experience certain complaints or ambiguous systemic symptoms such as loss of weight or appetite and fatigue. Furthermore, patients may misinterpret these complaints as benign conditions such as Irritable Bowel Syndrome.[10,11,12] Early detection is thus fundamental for decreasing mortality since CRC is a treatable condition. This is only possible by screening or incidentally. Saudi individuals are more likely to attend to their doctors at a late stage of the disease that carries a poor prognosis.[3,13,14] Also, screening is ideal for CRC since it has a long duration between early and advanced stages of the disease.[15,16] The evidence recommended the combination of these health professional efforts with counseling people who may benefit from lifestyle modification to improve survival and quality of life. Furthermore, this is a critical role for healthcare professionals. (Saudi Patients' Knowledge, Behavior, Beliefs, Self-Efficacy, and Barriers Regarding Colorectal Cancer Screening)[17] Recently, Saudi Arabia issued its strategy for health promotion and disease prevention, including colorectal cancer as part of Saud vision 2030. We are aiming to find out the knowledge, attitude, and practice (KAP) of the participants toward colorectal cancer and the early detection screening for it and identify the sources of information on the subjects about colorectal cancer.

Method

We conducted this descriptive cross-sectional study from September 2017 to February 2018 at the primary care clinics at KSUMC. The inclusion criteria for the subjects were 40 year old and above Arabic speaker resident in Riyadh of both sex. We estimated the sample size according to the following formula:

N = Z2 × p × (1 – p)/C2,

where N = sample size, Z = 1.96 at 95% level of significance, P = prevalence of low awareness (20%), and C = degree of precision (0.05). The estimated sample size was 245. We excluded people with a history of cancer. We randomly selected attendants of KSUMC outpatient clinics who fulfilled the inclusion criteria to complete the questionnaire.

The investigators developed a validated, self-administered questionnaire in the Arabic language according to the findings from three published literature.[18,19,20] The questionnaire consisted of three main parts: 1. Socio-demographic variables” age, gender, marital status, level of education, and occupation. 2. KAP of the participants toward CRC and its early detection screening. 3. Sources of information of the public about colorectal cancer such as awareness campaigns, health educational booklets, television, radio, newspaper, doctors, friends, websites, and social media.

A total of 24 knowledge questions aimed at assessing participants' knowledge, plus three attitude and 2practice questionnaires towards colorectal cancer and its early screening (see appendix). The possible answers to these questions were “yes,” “no,” and “I do not know.” Correct responses were assigned a score of 1, while incorrect responses or “I do not know” were assigned.

We assessed the three attitude questions using a Likert scale (strongly agree, agree, neutral, disagree, and strongly disagree). The authors ask the participants about their sources of information (such as doctors, friends, television, or the internet).

Academic experts (five family physicians, two surgeons, and one preventive medicine professor) reviewed the questionnaire. Before the conduction of the main study, the authors did a pilot study with 20 individuals to test the clarity, difficulties, applicability of the questionnaire, and to identify any difficulties. Also, during the pilot investigation, the instruments were found to conform to the scientific and cultural values for the Saudi community, and the authors estimated the time needed to complete it. We modified the questionnaire according to the results of the pilot study. People who participated in the pilot study spent 10 and 15 minutes to complete it. We excluded them from the main study. Cronbach's alpha for the knowledge items of the modified instrument was 0.88.

Before the conduct of the study, we got approval from the Institutional Review Board, college of medicine, King Saud University on 1-2-2015. Research Project No. E-15-1406. We strictly adhere to ethical codes of conduct at all stages of the project. All of the participants' information remained strictly anonymous and confidential.

We categorized the total score of the 24 knowledge questions into two as good (median score and above) and bad (below median score) knowledge.

We analyzed the data using the Statistical Package for Social Studies (SPSS 22; IBM Corp., New York, NY, USA). The investigators expressed categorical variables as percentages and using Chi-square. A P value < 0.05 was considered statistically significant.

Results

A total of 231 participants completed the study questionnaire, 126 (54.5%) were male. The response rate was 94.3%. Table 1 shows the level of participants' knowledge of colorectal cancer by their characteristics. The total sample means age was 50.7 (±9.8) years. Approximately 68.0% of the participants were married. The educational level for 90.9% of the participants was university and above. Ninety percent of the participants were working. Forty percent (17.3%) of the participants were having a family history of colorectal cancer.

Table 1

The level of participants’ knowledge of colorectal cancer by their characteristics. (n=231)

* Significant P value

The knowledge of those 50 years old and above and positive family history of cancer was better than their counterparts. These differences were statistically significant (P-value < 0.005).

Table 2 shows the knowledge and practice towards colorectal cancer and its early screening. About 47% of the participants heard about cancer screening tests, and 45% knew that colonoscopy is one of the procedures for such purposes. Another 24.2% were aware that blood in stool is one of the methods of early detection of colon cancer.

Table 2

Knowledge and practice towards colorectal cancer and its early Screening (n=231)

Out of all men and women, 51.4% thought they are susceptible to colon cancer. About 55% of the study subjects think consumption of food with high-Fat content, and Low Fiber is a risk factor for CRC. Also, 41.6% of them knew that the presence of polyps in the lining of the colon and rectum predispose them to colon cancer. A third 33.8% of respondents thought that physical inactivity is a risk factor for colon cancer. With regards to symptoms, 38.1% of participants thought that the presence of blood in the stool is a warning symptom; others between 38.1-45.5% thought that sudden weight loss and change in the number of bowel motions as symptoms of colon cancer respectively. About a third thought that the feeling of an emptied rectum with defecation and pain and cramps in the stomach was colorectal cancer symptoms. Even though 30.7% of the participants thought about doing a screening for early detection of colon cancer. Only 6.5% of the subjects did early checkups for colon cancer.

Table 3 shows the attitude towards the early screening of colorectal cancer. The participants who thought they were susceptible to colon cancer account for 25.5%. About 21.1% of the participants thought that their information about colon cancer was adequate. Nevertheless, 75.3% of them would undergo early screening for colon cancer if their doctor advised them to do so.

Table 3

Attitude towards early screening of colorectal cancer

Table 4 shows the participants' reasons for not doing CRC screening. About a quarter of the subjects attributed the reasons for the absence of symptoms. Furthermore, the lack of awareness of the need for such screening was another reason.

Table 4

Reasons for not doing CRC screening

Figure 1 shows the sources of information of the participants about the early screening of colorectal cancer. Awareness campaigns and health educational booklets represent the highest source for information (22.9%, 22.1%), respectively. Doctors and friends account for about 16% of the sources of information. Social media and websites of MOH represent about 10% or less of the sources of information.

Sources of information of the participants about early screening of colorectal cancer

Discussion

Colorectal cancer is common in Saudi Arabia.[21,22,23] Early diagnosis is essential for reducing mortality since CRC has an excellent prognosis if detected in early stages.[24,25] This only possible by screening or incidentally.[15,16,25] Cancer diagnosis delay can occur due to (diseased individual, health professionals, and the healthcare system itself)[26,27]

However, screening is ideal for CRC since it has a long duration between early and advanced stages. Also, prognosis mainly depends on the stage at diagnosis, even though, so far, there has been no national arrangement for CRC screening despite expanding disease rate.

Our study reported inadequate knowledge among the surveyed participants. A more than three-quarters think that their information about colon cancer was inadequate. About 47% of the participants heard about cancer screening tests, and 45% knew that colonoscopy is one of the procedures for such purposes. Another 24.2% were aware that blood in stool is a test of early detection of colon cancer. Many studies have reported similar results in different countries, including Saudi Arabia.[28,29,30,31,32] Greece,[33], Australia,[7] and Spain.[34]

In contrast to other studies, the female is associated with poor knowledge and longer diagnostic interval and reported more barriers, for example, fear about what the diagnosis might be, and also transportation difficulties.[29,36] Studies revealed that the higher the educational achievement of the person, probably they will recognize the seriousness of the symptom more and seek help early.[29,37] which was not the case among our participants.

The participants who thought they were susceptible to colon cancer account for 25.5%. Out of all subjects, 3.9% thought colon cancer is preventable, and 4.8% of them believed that early detection of CRC leads to an excellent prognosis. Further, 51.9% thought colon cancer to be fatal if not treated.

The majority of the subjects 55.4% incriminated imbalanced dietary consumption as a risk factor for CRC. Also, about half 41.6% of them knew that the presence of polyps in the lining of the colon and rectum predispose patients to colon cancer. Only a third of respondents thought that poor lifestyle, such as physical inactivity and tobacco smoking is a risk factor to colon cancer. These findings of risk factors were similar to those reported by other authors.[4,32,38] The findings emphasize the potential of risk factors modification on prevention and reduction of the burden of CRC in Saudi Arabia. Even though 17.3% of the participants were having a family history of CRC. This risk was not adequately appreciated by our participants to go for screening, which is different from other studies.[28,31,39] The current study showed that only about 17% of the participants received their information from doctors. This shortcoming draws the attention of health professionals to encourage eligible people, particularly those at high risk, and with a positive family history to undergo CRC screening. Also, they warned the rest of the family about their higher risk of CRC. This perceived increased risk of the disease or better knowledge about the disease-improved uptake of screening.[40,41]

Reducing the exposure to these risk factors and following the screening guidelines would make an effect on the prevalence of colorectal cancer.[4,42] The modern-day refocus of the healthcare system on public health interventions to prevent diseases was awaited for a long time to shift the growing incidence of lifestyle threat factors, which include a sedentary lifestyle, increased body mass index, and tobacco consumption.

Symptoms of CRC can vary from specific to systemic such as loss of weight or appetite and fatigue, which explained why patients may misinterpret them as benign or self-limiting diseases such as IBS. Our participants thought that sudden change in the number of bowel motions, the presence of blood in the stool, sudden weight loss was warning symptoms of colon cancer immediate help-seeking in our study. A third thought that the feeling of the not fully emptied rectum with defecation and pain and cramps in the stomach is colorectal cancer symptoms. These findings are similar to previous studies.[10,11,12,43,44,45] A previous study that what affects the help-seeking is the symptom profile of the late-stage disease.[31,35,46]

Only 30.7% thought about undergoing screening for early detection of colon cancer, and only 6.5% of the subjects did early checkups for colon cancer. This poor uptake is similar to a previous local study that reported a low rate of 5.64% colorectal cancer screening practice among the elderly Saudi population.[47] Several reasons may explain this low uptake of CRC screening, including low awareness of screening existence and personal fears,[31,32] low physician adherence to recommend CRC screening or low expectation of help.[48,49] Moreover, there is a lack of national policy.[23] Nevertheless, 75.3% of them would undergo early screening for colon cancer if their doctor advised them to do so. One-fourth of the participants attributed the reasons for not undergoing CRC screening to the absence of symptoms or lack of awareness of the need for such screening. While about 7% thought fear or embarrassment of the procedure would be their barrier. Furthermore, lack of time, the difficulty of getting an appointment played a role in a minority of subjects. The previous study stated that misinterpretation of the symptoms, embarrassment, and fear is associated with more endorsed barriers to help-seeking.[12,46,50,51,52,53,54]

The current evidence recommends screening for colorectal cancer in Saudi people who are at average risk and do not suffer from symptoms. The American Cancer Society recommends colonoscopy in the normal population from age 45 and for at-risk patients, ten years earlier than the age of the affected patient.[55]

The already conducted health awareness campaign participated in raising the knowledge and awareness of only a quarter of the subjects (22.9%). Doctors were not actively promoting CRC screening, as reflected by the subjects' responses.

The participants attributed only 17% of their knowledge to doctors. Social media were not adequately utilized in such a vital area, as it only represents 2.2 to 7.4% of the sources of information.

Fortunately, the current strategy of the healthcare system aimed at modifying the risk factors following the Vision 2030 and the National Transformation Program 2020 (NTP).[4] We expect this step to detect cases at early stages and hence lead to better prognosis than previously reported studies.[3,13]

The family physician and his team, supported by health decision-makers are the optimal environment for health promotion and disease prevention. Hence, the primary care team should not miss the opportunity to check the colorectal screening records and emphasize the importance of such a procedure for those attending their clinics for whatsoever reasons. They can send a reminder to eligible people and follow-up defaulters, solve barriers, and reduce disparity in health services coverage, towards CRC screening. A previous study showed that high levels of Primary Care Physician interaction result in improvements in CRC screening adherence.[56]

Fully integrated health education campaigns and awareness programs into the health system can ensure individual use services that are available to prevent CRC cancers. Utilizing paid television advertising and commonly used social media for CRC screening campaigns increase public motivation to participate and in the end prevent a huge number of bowel most cancers deaths.[57]

Conclusion

The awareness and knowledge of our sample about colorectal cancer were inadequate. Raising the level of knowledge is anticipated to increase the readiness to do the screening. The present data may be useful as fundamental data in making health policy in this area toward the management and prevention of CRC. Such an effort enhanced the recently issued strategy for health promotion and disease prevention, including colorectal cancer as part of Saudi vision 2030. Health professionals should encourage eligible people to go for screening and utilizing social media to improve people's information.

Limitation of the Study

Our study was limited to the primary care clinics of King Saud University Medical City (KSUMC) in Riyadh. We cannot ascertain the generalizability of our findings, as all of the participants come from a single center. So it is advisable to recruit more centers and from all regions of Saudi Arabia. Despite these limitations, we believe that this study can improve awareness, attitude, and practice toward colorectal screening in Saudi Arabia. The data gathered was self-reported by respondents, not subjected to independent verification, and potentially influenced by recall bias.

Financial support and sponsorship

Conflicts of interest

There are no conflicts of interest.

Acknowledgments

The authors are thankful to Health Promotion and Health Education Research Chair. Department of Family and Community Medicine, College of Medicine, King Saud University, Riyadh, Saudi Arabia. Special thanks also to the patients who participated in the study.

Appendix: Knowledge, attitude, and practice towards colorectal cancer and its early screening questionnaire items:

General knowledge questions

Have you ever heard of early cancer screening tests?

Colon cancer is a preventable condition

I think colon cancer is fatal

Colon cancer recovery rates increase when detected in the early stages

Risk factors for colon cancer

Men and women are prone to colon cancer

High Fat Low Fiber Diet

The presence of polyps in the lining of the colon and rectum

Symptoms of colon cancer

The presence of blood in the stool

Sudden weight loss

Increase mucus secretions in the stool

Feeling that the rectum was not fully emptied with defecation

Pain and cramps in the stomach

Sudden change in the number of bowel motions and Diarrhea

Methods of early detection of colon cancer

Blood detection in the stool sample

Barium dye for the large intestine

Abdominal CT scan

Clinical examination of the rectum

Attitude towards early screening of colorectal cancer

I think I am susceptible to colon cancer

Older adults are more susceptible to colon cancer

I will undergo early screening for colon cancer if my doctor advises me to do so.

Practice

Have you done early checkups for colon cancer?

Have you ever thought about undergoing screening for early detection of colon cancer?

Sources of information of the participants about the early screening of colorectal cancer

References

1. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017; 66 :683–91. [PubMed] [Google Scholar]

2. Saudi Health Council NHIC, Saudi Cancer Registry. Cancer Incidence Report Saudi Arabia. 2015 [Google Scholar]

3. Alsanea N, Abduljabbar AS, Alhomoud S, Ashari LH, Hibbert D, Bazarbashi S. Colorectal cancer in Saudi Arabia: Incidence, survival, demographics and implications for national policies. Ann Saudi Med. 2015; 35 :196–202. [PMC free article] [PubMed] [Google Scholar]

4. Al-Zalabani A. Preventability of colorectal cancer in Saudi Arabia: Fraction of cases attributable to modifiable risk factors in 2015-2040. Int J Environ Res Public Health. 2020; 17 :320. [PMC free article] [PubMed] [Google Scholar]

5. Al-Ahwal MS, Shafik YH, Al-Ahwal HM. First national survival data for colorectal cancer among Saudis between 1994 and 2004: What's next? BMC Public Health. 2013; 13 :73. [PMC free article] [PubMed] [Google Scholar]

6. Forbes L, Simon A, Warburton F, Boniface D, Brain KE, Dessaix A, et al. Differences in cancer awareness and beliefs between Australia, Canada, Denmark, Norway, Sweden and the UK (the International Cancer Benchmarking Partnership): Do they contribute to differences in cancer survival? Br J Cancer. 2013; 108 :292. [PMC free article] [PubMed] [Google Scholar]

7. Christou A, Thompson SC. Colorectal cancer screening knowledge, attitudes and behavioural intention among Indigenous Western Australians. BMC Public Health. 2012; 12 :528. [PMC free article] [PubMed] [Google Scholar]

8. Alhuzaim W, Alosaimi M, Almesfer AM, Al Shahrani NM, Alali AH, Alibrahim KIF, et al. Saudi Patients' knowledge, behavior, beliefs, self-efficacy and barriers regarding colorectal cancer screening. IJPRAS. 2020; 9 :4–20. [Google Scholar]

9. Bhatt DB, Emuakhagbon V-S. Current trends in colorectal cancer screening. Curr Colorectal Cancer Rep. 2019; 15 :45–52. [Google Scholar]

10. Hansen PL, Hjertholm P, Vedsted P. Increased diagnostic activity in general practice during the year preceding colorectal cancer diagnosis. Int J Cancer. 2015; 137 :615–24. [PubMed] [Google Scholar]

11. Rasmussen S, Larsen PV, Søndergaard J, Elnegaard S, Svendsen RP, Jarbøl DE. Specific and non-specific symptoms of colorectal cancer and contact to general practice. Fam Pract. 2015; 32 :387–94. [PubMed] [Google Scholar]

12. Oberoi DV, Jiwa M, McManus A, Hodder R. Men's help-seeking behavior with regards to lower bowel symptoms. Am J Health Behav. 2015; 39 :212–21. [PubMed] [Google Scholar]

13. Haggstrom D, Cheung W. In: Approach to the long-term survivor of colorectal cancer. Nekhlyudov L, editor. Waltham, MA, USA: UpToDate; 2015. [Google Scholar]

14. Aljebreen AM. Clinico-pathological patterns of colorectal cancer in Saudi Arabia: Younger with an advanced stage presentation. Saudi J Gastroenterol. 2007; 13 :84. [PubMed] [Google Scholar]

15. Smith RA, Manassaram-Baptiste D, Brooks D, Doroshenk M, Fedewa S, Saslow D, et al. Cancer screening in the United States, 2015: A review of current American cancer society guidelines and current issues in cancer screening. CA Cancer J Clin. 2015; 65 :30–54. [PubMed] [Google Scholar]

16. Mack LA, Stuart H, Temple WJ. Survey of colorectal cancer screening practices in a large Canadian urban centre. Can J Surg. 2004; 47 :189–94. [PMC free article] [PubMed] [Google Scholar]

17. Clinton SK, Giovannucci EL, Hursting SD. The World Cancer Research Fund/American Institute for Cancer Research Third Expert Report on Diet, Nutrition, Physical Activity, and Cancer: Impact and future directions. J Nutr. 2019 doi: 101093/jn/nxz268. [PMC free article] [PubMed] [Google Scholar]

18. Yakout SM, Moawed S, Gemeay EM. Cervical cancer and screening test (PAP Test): Knowledge and beliefs of Egyptian women. Am J Nurs. 2016; 5 :175–84. [Google Scholar]

19. Salem MR, Amin TT, Alhulaybi AA, Althafar AS, Abdelhai RA. Perceived risk of cervical cancer and barriers to screening among secondary school female teachers in Al Hassa, Saudi Arabia. Asian Pac J Cancer Prev. 2017; 18 :969. [PMC free article] [PubMed] [Google Scholar]

20. Guvenc G, Akyuz A, Açikel CH. Health belief model scale for cervical cancer and Pap smear test: Psychometric testing. J Adv Nurs. 2011; 67 :428–37. [PubMed] [Google Scholar]

21. Althubiti MA, Nour Eldein MM. Trends in the incidence and mortality of cancer in Saudi Arabia. Saudi Med J. 2018; 39 :1259–62. [PMC free article] [PubMed] [Google Scholar]

22. Herzallah HK, Antonisamy BR, Shafee MH, Al-Otaibi ST. Temporal trends in the incidence and demographics of cancers, communicable diseases, and non-communicable diseases in Saudi Arabia over the last decade. Saudi Med J. 2019; 40 :277. [PMC free article] [PubMed] [Google Scholar]

23. Aljumah AA, Aljebreen AM. Policy of screening for colorectal cancer in Saudi Arabia: A prospective analysis. Saudi J Gastroenterol. 2017; 23 :161. [PMC free article] [PubMed] [Google Scholar]

24. Richards M. The size of the prize for earlier diagnosis of cancer in England. Br J Cancer. 2009; 101 (S2):S125. [PMC free article] [PubMed] [Google Scholar]

25. Lindholm E, Brevinge H, Haglind E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg. 2008; 95 :1029–36. [PubMed] [Google Scholar]

26. Al-Azri MH. Delay in cancer diagnosis: Causes and possible solutions. Oman Med J. 2016; 31 :325–6. [PMC free article] [PubMed] [Google Scholar]

27. Lyratzopoulos G, Abel G, McPhail S, Neal R, Rubin G. Measures of promptness of cancer diagnosis in primary care: Secondary analysis of national audit data on patients with 18 common and rarer cancers. Br J Cancer. 2013; 108 :686–90. [PMC free article] [PubMed] [Google Scholar]

28. Al Wutayd O, Alamri F, Ali AM, Kassim KA, Ibrahim AK. Colorectal cancer risk factors: A study of knowledge, attitude and practice among adults in Riyadh, Saudi Arabia. Cancer Res J. 2015; 3 :94–9. [Google Scholar]

29. Al-Azri M, Al-Kindi J, Al-Harthi T, Al-Dahri M, Panchatcharam SM, Al-Maniri A. Awareness of stomach and colorectal cancer risk factors, symptoms and time taken to seek medical help among public attending primary care setting in Muscat Governorate, Oman. J Cancer Educ. 2019; 34 :423–34. [PubMed] [Google Scholar]

30. Almadi MA, Alghamdi F. The gap between knowledge and undergoing colorectal cancer screening using the Health Belief Model: A national survey. Saudi J Gastroenterol. 2019; 25 :27–39. [PMC free article] [PubMed] [Google Scholar]

31. Galal YS, Amin TT, Alarfaj AK, Almulhim AA, Aljughaiman AA, Almulla AK, et al. Colon cancer among older Saudis: Awareness of risk factors and early signs and perceived barriers to screening. Asian Pac J Cancer Prev. 2016; 17 :1837–46. [PubMed] [Google Scholar]

32. Zubaidi AM, AlSubaie NM, AlHumaid AA, Shaik SA, AlKhayal KA, AlObeed OA. Public awareness of colorectal cancer in Saudi Arabia: A survey of 1070 participants in Riyadh. Saudi J Gastroenterol. 2015; 21 :78–83. [PMC free article] [PubMed] [Google Scholar]

33. Papanikolaou IS, Sioulas AD, Kalimeris S, Papatheodosiou P, Karabinis I, Agelopoulou O, et al. Awareness and attitudes of Greek medical students on colorectal cancer screening. World J Gastrointest Endosc. 2012; 4 :513–7. [PMC free article] [PubMed] [Google Scholar]

34. Gimeno-García A, Quintero E, Nicolás-Pérez D, Jiménez-Sosa A. Public awareness of colorectal cancer and screening in a Spanish population. Public Health. 2011; 125 :609–15. [PubMed] [Google Scholar]

35. Mounce LT, Price S, Valderas JM, Hamilton W. Comorbid conditions delay diagnosis of colorectal cancer: A cohort study using electronic primary care records. Br J Cancer. 2017; 116 :1536. [PMC free article] [PubMed] [Google Scholar]

36. Mulka O. NICE suspected cancer guidelines. Br J Gen Pract. 2005; 55 :580–1. [PMC free article] [PubMed] [Google Scholar]

37. Oberoi DV, Jiwa M, McManus A, Parsons R. Do men know which lower bowel symptoms warrant medical attention? A web-based video vignette survey of men in Western Australia. Am J Men's Health. 2016; 10 :474–86. [PubMed] [Google Scholar]

38. Naing C, Lai PK, Mak JW. Immediately modifiable risk factors attributable to colorectal cancer in Malaysia. BMC Public Health. 2017; 17 :637. [PMC free article] [PubMed] [Google Scholar]

39. Puteh SEW, Khairudin SNA, Kabinchong C, Musa N, Joo CK, Saad NM, et al. Relationship of knowledge, attitude, practice (KAP) and demographic factors with quality of life among urban colorectal cancer patients in Malaysia. Middle East J Cancer. 2014; 5 :31–40. [Google Scholar]

40. Hall N, Birt L, Banks J, Emery J, Mills K, Johnson M, et al. Symptom appraisal and healthcare-seeking for symptoms suggestive of colorectal cancer: A qualitative study. BMJ Open. 2015; 5 :e008448. [PMC free article] [PubMed] [Google Scholar]

41. Almadi MA, Mosli MH, Bohlega MS, Al Essa MA, AlDohan MS, Alabdallatif TA, et al. Effect of public knowledge, attitudes, and behavior on willingness to undergo colorectal cancer screening using the health belief model. Saudi J Gastroenterol. 2015; 21 :71–7. [PMC free article] [PubMed] [Google Scholar]

42. Levin TR, Corley DA, Jensen CD, Schottinger JE, Quinn VP, Zauber AG, et al. Effects of organized colorectal cancer screening on cancer incidence and mortality in a large community-based population. Gastroenterology. 2018; 155 :1383–91 e5. [PMC free article] [PubMed] [Google Scholar]

43. John S, George S, Primrose J, Fozard J. Symptoms and signs in patients with colorectal cancer. Colorectal Dis. 2011; 13 :17–25. [PubMed] [Google Scholar]

44. Whitaker K, Smith CF, Winstanley K, Wardle J. What prompts help-seeking for cancer 'alarm'symptoms? A primary care based survey. Br J Cancer. 2016; 114 :334. [PMC free article] [PubMed] [Google Scholar]

45. Young CJ, Sweeney JL, Hunter A. Implications of delayed diagnosis in colorectal cancer. Aust N Z J Surg. 2000; 70 :635–8. [PubMed] [Google Scholar]

46. Walter FM, Emery JD, Mendonca S, Hall N, Morris HC, Mills K, et al. Symptoms and patient factors associated with longer time to diagnosis for colorectal cancer: Results from a prospective cohort study. Br J Cancer. 2016; 115 :533. [PMC free article] [PubMed] [Google Scholar]

47. Khoja A, Aljawadi M, Al-Shammari SA, Bokhari NN, Aldarwish AA, Mardini WK, et al. Utilization of colorectal cancer screening among Saudi elderly population: A study from the Saudi National Survey for elderly health. Asian Pac J Cancer Prev. 2018; 19 :3401. [PMC free article] [PubMed] [Google Scholar]

48. Mosli M, Alnahdi Y, Alghamdi A, Baabdullah M, Hadadi A, Khateery K, et al. Knowledge, attitude, and practices of primary health care physicians toward colorectal cancer screening. Saudi J Gastroenterol. 2017; 23 :330–6. [PMC free article] [PubMed] [Google Scholar]

49. Oberoi DV, Jiwa M, McManus A, Hodder R. Barriers to help-seeking in men diagnosed with benign colorectal diseases. Am J Health Behav. 2015; 39 :22–33. [PubMed] [Google Scholar]

50. Fish JA, Prichard I, Ettridge K, Grunfeld EA, Wilson C. Psychosocial factors that influence men's help-seeking for cancer symptoms: A systematic synthesis of mixed methods research. Psycho-Oncol. 2015; 24 :1222–32. [PubMed] [Google Scholar]

51. McLachlan S, Mansell G, Sanders T, Yardley S, Van der Windt D, Brindle L, et al. Symptom perceptions and help-seeking behaviour prior to lung and colorectal cancer diagnoses: A qualitative study. Fam Pract. 2015; 32 :568–77. [PMC free article] [PubMed] [Google Scholar]

52. Yousaf O, Grunfeld EA, Hunter MS. A systematic review of the factors associated with delays in medical and psychological help-seeking among men. Health Psychol Rev. 2015; 9 :264–76. [PubMed] [Google Scholar]

53. Oberoi D, Jiwa M, McManus A, Hodder R, De Nooijer J. Help-seeking experiences of men diagnosed with colorectal cancer: A qualitative study. Eur J Cancer Care. 2016; 25 :27–37. [PubMed] [Google Scholar]

54. Emery JD, Walter FM, Gray V, Sinclair C, Howting D, Bulsara M, et al. Diagnosing cancer in the bush: A mixed-methods study of symptom appraisal and help-seeking behaviour in people with cancer from rural Western Australia. Fam Pract. 2013; 30 :294–301. [PubMed] [Google Scholar]

55. Wolf AM, Fontham ET, Church TR, Flowers CR, Guerra CE, LaMonte SJ, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA A Cancer J Clin. 2018; 68 :250–81. [PubMed] [Google Scholar]

56. Lotfi-Jam K, O'Reilly C, Feng C, Wakefield M, Durkin S, Broun K. Increasing bowel cancer screening participation: Integrating population-wide, primary care and more targeted approaches. Public Health Res Pract. 2019:29. doi: 1017061/phrp2921916. [PubMed] [Google Scholar]

57. Durkin SJ, Broun K, Spittal MJ, Wakefield MA. Impact of a mass media campaign on participation rates in a National Bowel Cancer Screening Program: A field experiment. BMJ Open. 2019; 9 :e024267. [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Family Medicine and Primary Care are provided here courtesy of Wolters Kluwer -- Medknow Publications