Barriers and facilitators of colorectal cancer screening in Asia

Purpose One of the most common cancers in Asia is colorectal cancer (CRC). Early diagnosis and timely treatment are necessary for preventing complications and advanced stages of the disease. It is important to evaluate barriers and facilitators of screening in different countries. This systematic review aimed to identify the barriers and facilitators of CRC screening in Asia. Methods In this systematic review, for identifying barriers and facilitators of CRC screening, a comprehensive search was conducted in PubMed, Web of Science and Scopus in 12 December 2020. Combination keywords such as colorectal cancer, screening, sigmoidoscopy, colonoscopy, faecal occult blood test, barriers, facilitators and the names of each Asian country were used for searching. Full text original studies in English language were accepted in the review. Results In total, 36 articles were included in the review. Barriers and facilitators were evaluated. The most common reported barriers were lack of knowledge, fear of result, fear of procedure, fear of pain, lack of awareness, high cost and lack of gastrointestinal symptoms. The most frequent facilitators were having knowledge and awareness of CRC screening, perceived risk and severity, family history of cancer and physician recommendation. Conclusion For promoting success in CRC screening programmes, knowing what the barriers and facilitators are is necessary. Awareness and various personal, professional and social factors have been shown to be the major barriers toward CRC screening in most Asian countries.


Study quality assessment
Scores for cross-sectional studies ranged 5-7 by Ottawa scale. Samples of studies were representative of target population in 30 studies. Data collection procedures were described well by all of studies. Reported studies using self-administered questionnaire and some of them using health belief model (HBM) questionnaire. A total of 36 studies were used sufficient analysis methods and analysis linkage. A total of 26 studies had good quality score, and 10 studies had fair quality score by Ottawa quality scale ( Table 2).
Barriers and facilitators are shown in Table 3. Table 1. Characteristics of included studies in the review.

Knowledge of screening
In any screening programme, especially CRC screening, knowledge and awareness are considered as a crucial element. Knowledge of risk factors and screening methods leads to increased use of screening [12,28,30]. General lack of knowledge of CRC screening methods and risk factors were known as barriers in five studies of different countries [20,22,28,34,47]. Althobaiti and Jradi [28] showed that low participation in screening is related to lack of knowledge of screening and symptoms of CRC. Low level of knowledge stems from low level of education in relation to low level of awareness and attitudes. Another study among older Saudis showed that prior information about signs and risk factors had positive influence on awareness and intention to screening [29]. In a study in United Arab Emirates, overall evaluation of knowledge revealed a poor level of knowledge on risk factors, and only 40% of adults identified FOBT as a main screening test for CRC prevention [12].
In a study in China, individuals who have knowledge of screening tests were six times more likely to perform CRC screening rather than those who do not have any knowledge (high: AOR: 6.68, 95% CI = (4.36, 10.24), p < 0.001) [15]. Positive attitude that screening can be effective in early detection and reducing treatment time leads to decision to participate in CRC screening. Results of three studies demonstrate that when persons are aware of signs and risk factors of CRC, their participation in CRC screening increases [12,29,51]. According to Tfaily et al [38] study in Lebanon, people with higher awareness of risk factors were 2.2 times more likely to participate in CRC screening (OR = 2.221, 95% CI = (1.023, 4.820), p-value = 0.04). Believing that CRC is preventable is about (73.3%) and curable (70.5%) effected on CRC screening two times more strongly for choosing FOBT method as test (OR = 2, 95% CI: 1.04-2.29) [21].

Perceived severity, seriousness, barriers, risk, susceptibility, benefit
Other motivators of participation in CRC screening are perceived risk, severity and seriousness barriers. In many studies, results showed that perceived severity, seriousness and susceptibility leads to screening, and results of perceived barriers had a negative effect on screening [18,42,46,48,[50][51][52]. In a study, perception towards sub scales and health motivators was seen. Results showed that there was a significant positive correlation between knowledge of CRC screening and perceived susceptibility, seriousness and perceived barriers. Knowledge of CRC screening has a greater effect on perceived susceptibility to CRC, the seriousness of CRC, barriers for CRC and health motivation than those without knowledge about it [46,52]. Participants who perceived fewer barriers (OR = 0.37; 95% CI: 0.21-0.89), perceived more susceptibility (OR = 2.99; 95% CI: 1.23-5.45) were more likely to utilise screening tests [50]. Studies showed that some facilitators such as knowledge, awareness, sociodemographic factors, self-efficacy, perceived barriers, susceptibility, severity and benefits had positive influence on CRC screening [12,20,27,28].
Results of five studies showed fear of the painful medical procedures [11,20,38,39,41]. Fear of tumour detection and test result subsequent fear of developing CRC and fear of complications cause ignorance of screening [11,22,29,33,41,43,46,49]. Of the included studies, 51.6% reported fear of painful medical procedures as perceived barriers [11]. Procedure of screening may be embarrassment for participants. Al-naggar et al [22] showed that participants did not want to do screening, because of shyness (55.1%), painful procedure in FOBT (53.5%), embarrassment (55.1%) in sigmoidoscopy and then 32.1% fear of cancer detection.
According to Althobaiti and Jradi's [28] study, it was described that among medical students, knowledge of CRC factors and screening modalities was poor (52.47% and 57.83%, respectively). On the other hand, increase in medical education increased knowledge of screening three-fold (OR = 3.23; 95% CI: 2.01-5.18) and attitudes toward low level of medical science education were increased two (OR = 2.74; 95% CI: 1.86-4.03) times higher [28].
Results of Chen's study [31] showed that majority of physicians' barriers toward CRC were identified as lack of knowledge of colorectal guidelines (46.7%) and lack of sufficient information about CRC patients for early screening (43.8%). A study in Singapore on motivators such as presence of symptoms (92%), physician's recommendation (81.4%) and family history (70.7%) reported increased screening. Physicians recommendation had 7.15 times higher influence (OR = 7.10 (95% CI: 3.08-16.4), p < 0.001) on screening among survivors [17]. Recommendation by a doctor has a positive effect on screening, while believing that the screening process is painful has a negative effect on screening. The results of a study show that 95% of people report lack of doctor's advice as a barrier to screening [12,49]. Physician recommendations and advice [12,37,40], promoting knowledge and awareness of medical staff and students, reconciling guidelines of CRC screening are the strong motivating factors of CRC screening in different studies [24,31,34,37,48]. In a study among Saudi patients, 43% of the participants got knowledge of screening by regular awareness programmes from health care system [11].

Costs of screening
Medical costs associated with screening were a barrier in six studies. Huang et al [17] reported that cost of screening is too expensive and caused 50% of barrier of screening.
Long waiting times in public hospitals is one of the barriers in Saudi Arabia, Korea and Malaysia [12,36,41,43].

Accessibility
One of the important barriers for screening was about accessibility, lack of transportation and screening availability which differ from area residency in a country. More barriers have been reported from participants who live in rural areas [20]. In a study in Saudi Arabia, general lack of unavailability of FOBT was the only important barrier of CRC screening [20].
In a study in Singapore, younger participants (OR = 3.21, 95% CI: 1.01-5.41, p < 0.01) and more educated (OR = 1.54, 95% CI: 0.48-2.61), p < 0.01) had the highest rate of screening [51]. In a study of Al-Hajeili et al [14], level of education (p = 0.001) and region of residence (p = 0.02) significantly associated with knowledge of screening, knowledge about colonoscopy was associated with gender (p = 0.03), educational level (p < 0.01) and family history of CRC (p = 0.04). According to the study by Alhuzaim et al [11], the level of education has a positive role in the knowledge, behavior and self-efficacy of the participants. In this study, 65% of educated people are more inclined to be screened.
According to this study, increased age > 50 and level of education below secondary school were associated with decreased odds of CRC screening, odds ratio of age 0.9 (OR = 0.9, 95% CI: 0.50-0.99, p = 0.002) indicated low CRC screening than younger participants and about educational level 0.7 (OR = 0.7, 95% CI: 0.53-0.95, p = 0.02) below secondary school had lower CRC screening compared with high level of education [37]. On the other hand, study of Tfaily et al [38] demonstrated that older participants (above 50 years of age) had two times more knowledge and 55% awareness about CRC screening and 43% willingness to do screening. The study of Galal et al [29] showed that gender, unmarried and having less than college education were considered reducing predictors of CRC screening. Unmarried participants had 0.11 times lower CRC screening-rate (OR = 0.11; 95% CI: 0.10-0.23; p = 0.001) than married participants for screening. In a study among adults in United Arabs Emirates, knowledge of participations between UAE nationals and non-UAE nationals had significantly differences (p < 0.001), non-UAE nationals had better knowledge [12].
People over the age of 50 were more aware of the signs and symptoms than other participants in the study [38]. One of the important motivators that influences CRC screening is self-efficacy [11,45]. In a study in Iran, self-efficacy (OR = 1.17, 95% CI: 1.08-1.27) plays a role as a motivator variable about CRC screening among other participants [45].

Lack of signs and symptoms
One of the barriers of screening CRC reported by participants included lack of symptoms. Six studies reported that participants with no symptoms lead to lower screening history of symptoms and believed sickness caused more participation in screening [3,4,20,[22][23][29][30][31]. In a study in Saudi Arabia, 73.4% participants reported absence of signs and symptoms as the most important barrier [20].

Social factors and communications
Family and friends and relatives' recommendations have a role in raising sufficient awareness.

Comparisons of countries
Studies from Saudi Arabia and Palestine demonstrated that one of most common barriers was lack of physician recommendation, absence of signs and symptoms and lack of knowledge of CRC [11,20,21,30,37]. In the eastern region of Saudi Arabia, lack of provider's knowledge of recommended screening and lack of public awareness of CRC screening were most common barriers [29]. Financial problems had no effect on participating in CRC screening, because a large population had access to free screening tests that covered by the ministry of health [11,20,21,29,30,40,53]. In south East of Asia, Malaysia and Singapore, fear of cancer, avoiding doing screening after lack of knowledge, lack of recommendation by physician were the most common barriers of CRC screening [22,34,35,43,46,48,49]. In a study from Iran, more than 90% population did not have any knowledge of CRC risk factors, symptoms and screening tests [23]. The rate of FOBT screening was 29.9% [24]. Lack of awareness and limited literacy, lack of physician recommendation were as the most common barriers [23,24]. In South Korea, only 31.7% of target population participated in screening programmes and one of the barriers was cost of screening that most of the cost paid by participants [41]. Using information sources such as media, videos, books and physician recommendation was found to have an impact on CRC screening. On the other hand, the main factors for ignoring the screening are the lack of knowledge, cost, fear of diagnosis, fear of screening procedures, lack of time, embarrassment. Remarkably, the difference in facilitators and barriers results in different groups with different sociodemographic factors and different guidelines which use the maximum reported score of doing screening modalities is 73% and the lowest is 0.7%. Information on factors on CRC screening such as knowledge, attitude and barriers are poor and need to be further considered, raising knowledge and awareness are equal for reducing barriers. However, appropriate guidelines and protocols must be developed.

Discussion
Lack of integrated guidelines in countries and low level of knowledge among medical students are also common barriers. Asian population had a poor knowledge-rate and low rate of screening in comparison to western and American societies [54,55]. On the other hand, media and social communications and family history of cancer, physician recommendation played an effective role on screening-participation. The most common barriers in Asian countries were lack of knowledge, lack of physician recommendation and fear of screening. In comparison to western countries' fear of screening results and fear of screening procedure, in American countries cost of screening was the most common barrier of screening. Physician recommendation in Asian countries was low in contrast to the American physician recommendation was 72.6% [47,55].

Strength and limitations of the review
Our search strategy was inclusive and we searched a wide range of databases and then to enhance sensitivity we retrieved full text of all selected articles. We included studies with a large number of participants, who intended to evaluate screening barriers and facilitators. We compared barriers and facilitators from different regions of Asia.
In this review, we compared countries and demonstrated barriers and facilitators of each studies. A limitation was that we used quantitative studies and we recommended to use both qualitative and quantitative studies.

Conclusion
We found that lack of knowledge and awareness about CRC and CRC screening was preventing participation in CRC screening in Asia. While interventional education and guidelines are concurrent with logistics, cultural and motivational barriers must be overcome for reducing inequities in participation in CRC screening. Awareness programmes by health care officials, governments and health care organisations can lead to increased knowledge and ultimately to regular participation in screening. Our study showed that Asian countries have similar barriers and facilitators.

Funding
Not applicable.

Conflicts of interest
None.

Availability of data
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Ethics approval
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Consent to participate
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