Zaid Ali Abdulelah1, Ahmed Ali Abdulelah2, Mohammad Alqaisieh3, Asim N Khanfar2, Nouran Husam Hammad4, Eyad Bassam Al Masoud4, Qusai B Odeh5, Mohammad Ali Alshrouf2, Rahaf Maher Abuaisheh5, Haitham Mohammed Abd-Alrahman6 and Amer Khatib7
1Office of Scientific Affairs and Research, King Hussein Cancer Center, Amman, Jordan (Correspondence to ZA Abdulelah:
Abstract
Background: Colorectal cancer is among the leading malignancies globally and in Jordan. It causes significant morbidity and mortality. It can be detected early, but uptake of colorectal cancer screening in Jordan is substantially low.
Aim: To determine the underlying barriers to the uptake of colorectal cancer screening in Jordan.
Methods: A cross-sectional study was conducted in the northern, central and southern regions of Jordan using self-administered questionnaire that evaluated the barriers and attitudes towards colorectal cancer screening among adults aged 45 years and above living in Jordan. The data was analyzed using SPSS version 25.0.
Results: Of the 1477 participants enrolled in the study, 29.1% reported the lack of information about screening as a major barrier to uptake, followed by the fear of any potential complications due to the test (10%), embarrassment associated with colonoscopy (7.8%), and fear of the result (7.4%). Only 9% of the study participants had taken the colonoscopy test for colorectal cancer screening.
Conclusion: Lack of information about colorectal cancer screening, misconceptions and embarrassment drive the low uptake of colorectal cancer screening in Jordan. There is a need for nationwide education and awareness on colorectal cancer screening to address the barriers reported in this study and increase screening uptake.
Keywords: colorectal cancer, screening, uptake, barrier, attitude, colonoscopy, fear, embarrassment, Jordan
Citation: Abdulelah ZA, Abdulelah AA, Alqaisieh M, Khanfar AN, Hammad NH, Al Masoud EB, et al. National survey of barriers to colorectal cancer screening in Jordan. East Mediterr Health J. 2024;30(2):125–135. https://doi.org/10.26719/emhj.24.028. Received: 20/04/22; Accepted: 05/10/23
Copyright © Authors 2024; Licensee: World Health Organization. EMHJ is an open access journal. This paper is available under the Creative Commons Attribution Non-Commercial ShareAlike 3.0 IGO licence (CC BY-NC-SA 3.0 IGO; https://creativecommons.org/licenses/by-nc-sa/3.0/igo).
Background
Colorectal cancer (CRC) is one of the most common cancers: it was the third most common cancer and second leading cause of cancer-related deaths worldwide for both genders in 2020 (1). CRC notably affects males more commonly, with a male:female ratio of 1.25:1. In Jordan, CRC is the second most common cancer, accounting for 10.7% of cancer cases in Jordan and for 9.8% of all cancer-related deaths in Jordan in 2016 (2).
CRC usually develops from a pre-existing non-malignant polyp that generally requires 5–15 years for malignant transformation. Because of this prolonged time interval, CRC is known to be one of the few malignancies that may be prevented in many ways, including modification of lifestyle changes and early detection. Multiple methods exist to screen for CRC, including faecal occult blood test (FOBT), flexible sigmoidoscopy and colonoscopy. For example, annual FOBT screening has been shown to decrease CRC mortality significantly (3). Screening by flexible sigmoidoscopy substantially reduced CRC incidence (4). CRC screening has been shown to reduce overall health care costs (5).
Despite well-established evidence of the benefits of screening, which has made many countries to adopt a national CRC screening programme, many barriers remain. For example, in the United Kingdom, anticipated pain and embarrassment are among the most commonly cited reasons for avoiding screening (6). In Finland, males and individuals younger than 60 years tend to refuse screening more often than older individuals (7).
Even though CRC ranks highly in Jordan in both incidence and mortality, there is no national CRC screening programme, partly due to lack of data on the barriers to screening among the at-risk Jordanian population.
Objective
This study aimed to identify the key barriers to CRC screening and colonoscopy uptake in Jordan. The results may provide insight to policymakers for establishing a national CRC screening programme in Jordan.
Methodology
A population-based cross-sectional study using a self-administered questionnaire was conducted across Jordan by enrolling participants from the northern, central and southern regions of the country. Our exclusion criteria included participants younger than 45 years and those with an active or previous history of colorectal cancer.
The questionnaire was administered by qualified healthcare workers, who underwent comprehensive data collection training for cross-sectional studies. The questionnaire was administered across most of the Jordanian provinces and considered the population distribution across the regions. Potential participants were approached in a variety of settings, including mosques, hypermarkets, parks, schools and government institutions via a simple random convenience sampling method.
Verbal consent was obtained from the participants after explaining the concept and aim of the study and the right of the individual to withdraw from participation at any time. The healthcare workers were readily available to the participants during questionnaire administration to respond to any concerns. The study was conducted ethically in accordance with the World Medical Association Declaration of Helsinki in addition to obtaining an IRB approval from the IRB board of the Abdali Hospital (2021900001).
Questionnaire
The questionnaire was developed through a multiple-step process. A review of similar studies was initially conducted before producing a preliminary questionnaire, which was reviewed by a gastroenterologist and a medical research expert. The questionnaire was pretested among 30 individuals different backgrounds who were not included in the study to ensure that the questions were easy to understand and appropriate for purpose. The final version of the questionnaire in Arabic was approved for the study, along with an English version for non-Arabic-speaking participants.
The questionnaire consisted of 27 questions: 25 multiple-choice and 2 fill-ins (date of birth and name of city/village/camp of residence). The questions were about demographics, presence of comorbidities, smoking status, family history of colon cancer, knowledge of screening methods, and barriers to participation in colorectal cancer screening.
Study population
The age of the target population was set at 45 years or older, as recent guidelines by the American Society of Gastroenterology recommend screening from the age of 45 rather than 50 (8). The population size of this age range was 1 806 880, according to Jordan’s estimated population in 2019. The sample size calculation was done with confidence level set at 95, confidence interval set at 3; the determined sample size was 1066.
Our minimum expected sample size for the study was 1066. Accordingly, we approached 2000 participants, of whom 1607 agreed to participate in the study, with a participation rate of 80.4%. Among the participants, 130 were excluded because their age was below 45 or they refused to answer all the questions. Consequently, 1477 participants were enrolled. At this sample size, the confidence interval was 2.55.
Outcomes
The aim of this study was to obtain data on the barriers to colorectal cancer screening among Jordan’s population. We also aimed to gain insight into the population’s awareness of screening methods. This was done in relation to factors such as marital status, employment, educational level, insurance and gender. The study assessed which factors could have influenced screening among those who underwent colorectal cancer screening and the attitude of participants towards screening methods.
Data analysis
Data from 1477 participants were obtained and a descriptive analysis was performed. All categorical data, such as age group, gender and other factors were presented as counts and percentages. The mean and standard deviation were calculated for continuous data, such as age. Chi-square (χ2) tests were done to investigate the proportional differences. The significant association was set at P≤0.05. SPSS for Windows 25.0 was used for the analysis.
Results
Demographics
In our sample, 942 (62.6%) participants were male, with a mean age of 57.2 ± 8.23 years. More than half of the participants (831, or 56.3%) were from the Central Region of Jordan, whereas 30.8% and 12.9% were from Northern and Southern regions of the country, respectively (see Figure 1).
Notably, 87.3% of the participants were married at the time of enrolment and were more likely to be an employer/employee (43.1%, n=637) or a retiree (23.8%, n=352). The predominant educational level among participants was bachelor’s degree.
Although the most common type of insurance coverage in our sample was provided by the Ministry of Health (41.3%, n=610) followed by Royal Medical Services (19.6%, n=290), 17.1% (n=253) of our participants were not medically insured.
Knowledge of screening
The majority of participants (61.7%, n=911) were unaware of the availability of screening tools for early CRC detection and prevention. Of those who were aware, 39.6% (n= 224) were informed by a physician, 23.7% (n=134) by a friend or relative, and 35.7% (n=202) through awareness campaigns.
Among participants who were aware of CRC screening, their level of education was significantly associated: individuals with a postgraduate degree and those with a bachelor’s degree were most likely to be aware of screening tools for CRC (P
Participants who underwent colonoscopy screening
Among the participants, 9% (n=133) underwent colonoscopy screening. Most of those who underwent screening had done it within 2 years prior to enrolment in our study (45.1%), whereas 20.3% had done it within the same year of enrolment, and 34.6% did it 3 or more years prior to enrolment (Figure 2).
Our findings revealed that individuals who had a postgraduate degree were most likely to undergo a colonoscopy screening compared to participants with lower educational levels (P<0.001). individuals="" with="" a="" family="" history="" of="" crc="" were="" significantly="" associated="" previously="" undergoing="" screening="" colonoscopy="" p="0.014).
Moreover, individuals who have had a screening colonoscopy were significantly more knowledgeable about the availability of CRC screening tools (PTable 1 summarizes the characteristics of patients who underwent screening colonoscopy in comparison to those who did not. Table 2 summarizes the relationship between the level of education and the presence of prior knowledge of screening and its modalities in association with the key reported barriers.
Attitudes towards screening colonoscopy
Among participants who answered, “I do not have enough information” (29.1) when asked if they would undergo a screening colonoscopy, employment status was statistically significant: unemployed individuals and housewives were more likely to choose this answer.
Prior CRC screening knowledge was also significant: participants who were unaware of the availability of CRC screening tools were more likely to choose this answer (PTable 3).
There was a statistically significant association between refusal to undergo screening colonoscopy due to “fear of the results” and gender: females were more likely to fear the results of the screening test (PTable 4).
Among participants who refused screening colonoscopy because of embarrassment, there was a significant lack of prior knowledge of screening (P=0.003). There were no significant associations between embarrassment of colonoscopy and gender, marital and educational status (see Table 5).
Among participants who answered, “I fear complications of the procedure” when asked if they would undergo a screening colonoscopy (10%), educational status was significant: participants who only finished primary/elementary school were more likely to refuse screening colonoscopy due to fear of complications compared to college graduates (P
Participants with no previous knowledge of CRC screening were also more likely to fear complications (PTable 6).
Figure 3 shows all of the reported barriers to CRC screening and their prevalence among the participants.
Faecal occult blood test as a screening tool
Of the study participants, 6.5% (n=94) had previously undergone FOBT for CRC screening purposes. These participants were found to be more knowledgeable and aware of the role of screening in the prevention of CRC (P
Discussion
Jordan lacks an established CRC screening programme or well-structured and comprehensive awareness campaigns targeted towards CRC screening. There are many reasons for the absence of these vital healthcare initiatives and programmes. Only few studies have been conducted in Jordan on the barriers to CRC and those studies targeted age groups that were partially or fully out of the scope of CRC screening at the time of the study and, in some instances, only included a small sample size (9–11). Coupled with the fact that Jordan is a lower-middle-income country with limited resources, these factors may help explain the lack of comprehensive national screening and awareness programmes.
Our study included 1477 participants from all Jordanian regions, exceeding previous studies in Jordan, and provides a more general indication of the barriers to CRC screening in the country (9,10).
In Jordan, knowledge of the availability of CRC screening methods is low (around 20%) (9–11). Approximately 38.3% of our study participants said they were aware of CRC screening, with 42.4% aware of both colonoscopy and FOBT as screening tools. Our sample’s CRC screening knowledge, despite being higher than previous studies in Jordan, is lower than in developed countries, such as Spain and the United States (12,13).
Our study revealed a positive association between the level of education and an individual’s awareness of CRC screening. Those with a higher educational status were more knowledgeable about CRC screening, thus conflicting with Taha et al. results (9), which found no such association.
Despite the fact that 30.9% of our sample was knowledgeable about the availability and use of colonoscopy as a screening tool, only 9% of the participants underwent colonoscopy screening. This suggests that many factors in a complex process – other than lack of knowledge – prevent individuals from undergoing screening. A study in neighbouring West Bank also yielded very low participation rates for CRC screening; only 7% of their sample had previously undergone colonoscopy screening. Similar participation rates elsewhere in the Eastern Mediterranean Region are expected due to significant overlap and similar sociocultural practices.
Turkey’s engagement rate (20–30%) in CRC screening practices is substantially higher than Jordanian and Palestinian participation rates, but lower than some European countries (14); for instance, 43% has been reported in the United Kingdom (15). In Germany only 2–3% of individuals eligible for colonoscopy screening undergo the procedure (16). These rates reinforce the notion that participation in CRC screening, particularly colonoscopy, is limited due to various barriers.
One of the widely noted barriers to CRC screening is limited knowledge of the availability of screening methods (17–20). Approximately 29% of our sample had limited knowledge and information about CRC screening. One way to overcome this is improve awareness and knowledge through educational programmes, including the use of videos (21).
Another barrier, particularly among females, was fear of the potential results of the procedure. This is because any positive results from testing could trigger anxiety (17,21). This finding is consistent with other studies indicating that an individual’s fear of positive results is a major barrier to CRC screening (14,22,23). We did not find any studies indicating a compelling association between gender and fear of results.
Embarrassment is another barrier to colonoscopy, as the procedure involves exposure of intimate body parts; this embarrassment was particularly significant among individuals who were aware only of colonoscopy as a screening tool for CRC. This finding can be further explained by the fact that Jordan is a conservative country where people regard the exposure of intimate body parts, even for medical purposes, as repulsive. Embarrassment associated with colonoscopy is a universal barrier to CRC screening due to the nature of the procedure and, in some instances, procedures for preparing the bowel (24).
Unlike FOBT, colonoscopy is an invasive procedure that can result in serious complications in very rare instances, primarily perforation and post-colonoscopy bleeding (25). Despite the rarity of such events, one of the anxiety-triggering factors among individuals undergoing colonoscopy is the fear of complications. A systematic review revealed that around 53% among individuals undergoing colonoscopy reported a fear of complications. Among those who refused colonoscopy, 21–32% reported that fear and anxiety about developing complications after the procedure was the deciding factor in avoiding colonoscopy (25,26). This was also observed to a lesser extent in our study, where 148 (10%) participants said they would refuse to undergo colonoscopy screening due to fear of complications following the procedure.
Individuals who are only knowledgeable about colonoscopy as a screening method are also likely to refuse screening due to fear of complications. This indicates limited understanding of the procedure and its setting; the incidence of complications following colonoscopy is approximately 0.05% with an even lower prevalence in colonoscopies conducted for screening purposes (25). Individuals who would still refuse colonoscopy, despite having accurate information about the procedure, may benefit from learning about FOBT, as it is non-invasive.
Our study revealed that participants who underwent colonoscopy for screening purposes (9%) were significantly more knowledgeable about CRC screening and had a higher educational level than those who did not undergo colonoscopy, further highlighting the importance of knowledge and education. A previous study in Jordan conducted by Taha et al. (9) reported similar results, where pre-existing knowledge of CRC and available screening tools were significantly associated with undergoing CRC screening.
We found a significant relationship between participants who underwent colonoscopy screening and those who were informed about CRC methods by a physician. This aligns with the findings of Honein-AbouHaidar et al. (24), which indicate that primary care physicians’ advice and recommendations positively influence CRC screening uptake.
We identified a strong association between participation in colonoscopy screening and a positive family history, which is consistent with findings from several studies indicating higher participation rates in CRC screening among first-degree relatives of CRC patients; Mack et al. (27) reported a participation rate of approximately 70% among first-degree relatives (27–31).
Limitations
The study may be limited by the use of a self-administered questionnaire and its quantitative nature rather than a qualitative or mixed methods design. Our sample was predominantly male. However, our study design was principally driven by a cultural aspect of Jordan, where asking an individual direct questions on something that is private or embarrassing is unacceptable. Accordingly, a quantitative study design with a self-administered questionnaire was determined to be the most culturally appropriate. The male-to-female ratio of our sample was also influenced by this. The focus of this study was predominantly on colonoscopy as a screening method and not other available screening tests, mostly due to its higher sensitivity.
Conclusion
Our findings show that, in addition to the lack of knowledge of CRC screening, there is a perceived fear of the results of the screening and complications that could arise following colonoscopy, and a feeling of embarrassment from the procedure. Therefore, nationwide awareness campaigns and screening programmes are needed to tackle these barriers. Findings from this study could be useful in designing such programmes.
Funding: None.
Competing interests: None declared.
Enquête nationale sur les obstacles au dépistage du cancer colorectal en Jordanie
Résumé
Contexte : Le cancer colorectal figure parmi les principales affections malignes en Jordanie et dans le monde. Il est à l'origine d'une morbidité et d'une mortalité importantes et peut être détecté à un stade précoce, mais son taux de dépistage en Jordanie demeure très faible.
Objectif : Déterminer les obstacles sous-jacents au dépistage du cancer colorectal en Jordanie.
Méthodes : Une étude transversale a été menée dans les régions du nord, du sud et du centre de la Jordanie au moyen d'un questionnaire auto-administré qui a permis d'examiner les obstacles et les attitudes vis-à-vis du dépistage du cancer colorectal chez les adultes âgés de 45 ans et plus, vivant dans le pays. Les données ont été analysées à l'aide du logiciel SPSS version 25.0.
Résultats : Sur les 1477 participants inclus dans l'étude, 29,1 % ont indiqué que le manque d'informations sur le dépistage représentait un obstacle majeur à sa réalisation, suivi de la crainte de complications potentielles dues au test (10 %), de la gêne associée à la coloscopie (7,8 %) et de la crainte du résultat (7,4 %). Seulement 9 % des participants à l'étude avaient réalisé une coloscopie pour le dépistage de ce cancer.
Conclusion : Le manque d'informations, les préjugés et la gêne sont les principales causes du faible taux de recours au dépistage du cancer colorectal en Jordanie. Il est nécessaire de mettre en place un programme national d'éducation et de sensibilisation à ce sujet afin d'éliminer les obstacles mentionnés dans cette étude et d'augmenter le taux de recours au dépistage.
المسح الوطني للعوائق التي تحول دون فحص سرطان القولون والمستقيم في الأردن
زيد علي عبد الله، أحمد علي عبد الله، محمد القيسي، عاصم ن. خنفر، نوران حسام حماد، إياد بسام المسعود، قصي ب. عودة، محمد علي الشروف، رهف ماهر أبوعيشة، هيثم محمد عبد الرحمن، عامر الخطيب
الخلاصة
الخلفية: يُعَد سرطان القولون والمستقيم من الأورام الخبيثة المنتشرة على مستوى العالم وفي الأردن. ويتسبب في معدلات كبيرة من المراضة والوفيات. ويمكن الكشف عن سرطان القولون والمستقيم في وقت مبكر، ولكن الإقبال على فحص سرطان القولون والمستقيم في الأردن منخفض إلى حدٍّ كبير.
الأهداف: هدفت هذه الدراسة الى تحديد العقبات الأساسية التي تحول دون الإقبال على فحص سرطان القولون والمستقيم في الأردن.
طرق البحث: أُجريت دراسة مقطعية في المناطق الشمالية والوسطى والجنوبية من الأردن باستخدام استبيان يُستكمل ذاتيًّا، لتقييم العوائق والمواقف تجاه فحص سرطان القولون والمستقيم لدى البالغين البالغة أعمارهم 45 عامًا فأكثر، الذين يعيشون في الأردن. وحُلِّلت البيانات بالإصدار 25,0 من برنامج SPSS.
النتائج: من بين المشاركين في الدراسة البالغ عددهم 1477 مشاركًا، أفاد 1,92% منهم أن نقص المعلومات عن الفحص يمثل عائقًا رئيسيًّا أمام الإقبال عليه، يليه الخوف من أي مضاعفات محتملة قد تنجم عن الاختبار (01%)، والحرج المرتبط بإجراء تنظير القولون (8,7%)، والخوف من نتائج الفحص (%7,4). ولم يخضع لإجراء تنظير القولون للكشف عن سرطان القولون والمستقيم سوى 9% من السكان الذين شملتهم الدراسة.
الاستنتاجات: يؤدي نقص المعلومات عن فحص سرطان القولون والمستقيم والمفاهيم الخاطئة والحرج إلى انخفاض الإقبال على الخضوع لهذا الفحص في الأردن. وهناك حاجة إلى التثقيف والتوعية على الصعيد الوطني بشأن فحص سرطان القولون والمستقيم من أجل التغلب على العوائق المُبلَغ عنها في هذه الدراسة، وزيادة الإقبال على الخضوع للفحص.
References
1. Wolf AMD, Fontham ETH, 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 Cancer J Clin. 2018;68(4):250–281. DOI:10.3322/caac.21457.
2. Nimri O, Arqoup K. Statistical Digest Jordan Cancer Registry (JCR) Cancer Incidence in Jordan -2016 Non-Communicable Diseases Directorate-MOH. 2020;21. DOI:10.13140/RG.2.2.31627.92961.
3. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med. 1993;328(19):1365–1371. DOI: 10.1056/NEJM199305133281901.
4. Schoen RE, Pinsky PF, Weissfeld JL, Yokochi LA, Church T, Laiyemo AO et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med. 2012;366(25):2345–2357. 10.1056/NEJMoa1114635.
5. Lansdorp-Vogelaar I, Knudsen AB, Brenner H. Cost-effectiveness of colorectal cancer screening. Epidemiol Rev. 2011;33(1):88–100. DOI:10.1093/epirev/mxr004.
6. Von Wagner C, Bonello B, Stoffel S, Skrobanski H, Freeman M, Kerrison RS et al. Barriers to bowel scope (flexible sigmoidoscopy) screening: A comparison of non-responders, active decliners and non-attenders. BMC Public Health. 2018;18(1):1–14. DOI:10.1186/s12889-018-6071-8.
7. Artama M, Heinävaara S, Sarkeala T, Prättälä R, Pukkala E, Malila N. Determinants of non-participation in a mass screening program for colorectal cancer in Finland. Acta Oncol. 2016;55(7):870–874. DOI:10.1080/0284186X.2016.1175658.
8. Shaukat A, Kahi CJ, Burke CA, Rabeneck L, Sauer BG, Rex DK. ACG Clinical Guidelines: Colorectal Cancer Screening 2021. Am J Gastroenterol. 2021;116(3):458–479. DOI:10.14309/ajg.0000000000001122.
9. Taha H, Al Jaghbeer M, Al-Sabbagh MQ, Al Omari L, Berggren V. Knowledge and Practices of Colorectal Cancer Early Detection Examinations in Jordan: A Cross Sectional Study. Asian Pac J Cancer Prev. 2019;20(3):831–838. DOI:10.31557/APJCP.2019.20.3.831.
10. Omran S, Ismail AA. Knowledge and beliefs of Jordanians toward colorectal cancer screening. Cancer Nurs. 2010;33(2):141–148. DOI:10.1097/NCC.0b013e3181b823f3.
11. Ahmad MM, Dardas L, Dardas L, Ahmad H. Colorectal cancer in Jordan: prevention and care. Glob Health Promot. 2015;22(4):39–47. DOI:10.1177/1757975914547712.
12. Ricardo-Rodrigues I, Hernandez-Barrera V, Jiménez-García R. Awareness of colonoscopy as a screening method for colorectal cancer and its uptake in Spain. Eur J Cancer Prev. 2014;23(5):398–404. DOI:10.1097/CEJ.0000000000000026.
13. Janz NK, Wren PA, Schottenfeld D, Guire KE. Colorectal cancer screening attitudes and behavior: a population-based study. Prev Med. 2003;37(6):627–634. DOI: 10.1016/j.ypmed.2003.09.016
14. Sahin MK, Aker S, Arslan HN. Barriers to Colorectal Cancer Screening in a Primary Care Setting in Turkey. J Community Health. 2017;42(1):101–108. DOI:10.1007/s10900-016-0235-1.
15. McGregor LM, Bonello B, Kerrison RS, Nickerson C, Baio G, Berkman L et al. Uptake of Bowel Scope (Flexible Sigmoidoscopy) Screening in the English National Programme: the first 14 months. J Med Screen. 2016;23(2):77–82. DOI:10.1177/0969141315604659.
16. Hoffmeister M, Holleczek B, Zwink N, Stock C, Stegmaier C, Brenner H. Screening for Bowel Cancer: Increasing Participation via Personal Invitation. Dtsch Arztebl Int. 2017;114(6):87–93. DOI:10.3238/arztebl.2017.0087.
17. Greiner KA, Born W, Nollen N, Ahluwalia JS. Knowledge and perceptions of colorectal cancer screening among urban African Americans. J Gen Intern Med. 2005;20(11):977–983. DOI:10.1111/j.1525-1497.2005.0165.x.
18. Javanparast S, Ward PR, Carter SM, Wilson CJ. Barriers to and facilitators of colorectal cancer screening in different population subgroups in Adelaide, South Australia. Med J Aust. 2012;196(8):521–523. DOI:10.5694/mja11.10701.
19. Brouse CH, Basch CE, Wolf RL, Shmukler C. Barriers to colorectal cancer screening: an educational diagnosis. J Cancer Educ. 2004;19(3):170–173. DOI:10.1207/s15430154jce1903_12.
20. Shokar NK, Vernon SW, Weller SC. Cancer and colorectal cancer: knowledge, beliefs, and screening preferences of a diverse patient population. Fam Med. 2005;37(5):341–347. PMID: 15883900.
21. Ma GX, Wang MQ, Toubbeh J, Tan Y, Shive S, Wu D. Factors Associated with Colorectal Cancer Screening Among Cambodians, Vietnamese, Koreans and Chinese Living in the United States. N Am J Med Sci. 2012;5(1):1–8. DOI:10.7156/v5i1p001.
22. Rawl SM, Menon U, Champion VL, Foster JL, Skinner CS. Colorectal cancer screening beliefs. Focus groups with first-degree relatives. Cancer Pract. 2000;8(1):32–37. DOI:10.1046/j.1523-5394.2000.81006.x.
23. Reynolds LM, Bissett IP, Consedine NS. Emotional predictors of bowel screening: the avoidance-promoting role of fear, embarrassment, and disgust. BMC Cancer. 2018;18(1):1–9. DOI:10.1186/s12885-018-4423-5.
24. Honein-AbouHaidar GN, Kastner M, Vuong V, Perrier L, Daly C, Rabeneck L et al. Systematic Review and Meta-study Synthesis of Qualitative Studies Evaluating Facilitators and Barriers to Participation in Colorectal Cancer Screening. Cancer Epidemiol Biomarkers Prev. 2016;25(6):907–917. DOI:10.1158/1055-9965.EPI-15-0990.
25. Yang C, Sriranjan V, Abou-Setta AM, Poluha W, Walker JR, Singh H. Anxiety Associated with Colonoscopy and Flexible Sigmoidoscopy: A Systematic Review. Am J Gastroenterol. 2018;113(12):1810–1818. DOI:10.1038/s41395-018-0398-8.
26. Reumkens A, Rondagh EJA, Bakker CM, Winkens B, Masclee AAM, Sanduleanu S. Post-Colonoscopy Complications: A Systematic Review, Time Trends, and Meta-Analysis of Population-Based Studies. Am J Gastroenterol. 2016;111(8):1092–1101. DOI:10.1038/ajg.2016.234.
27. Bhise V, Modi V, Kalavar A, Espadas D, Hanser L, Gould M et al. Patient-Reported Attributions for Missed Colonoscopy Appointments in Two Large Healthcare Systems. Dig Dis Sci. 2016;61(7):1853–1861. DOI:10.1007/s10620-016-4096-3.
28. Mack LA, Cook LS, Temple WJ, Carlson LE, Hilsden RJ, Paolucci EO. Colorectal cancer screening among first-degree relatives of colorectal cancer patients: benefits and barriers. Ann Surg Oncol. 2009;16(8):2092–2100. DOI:10.1245/s10434-009-0528-z.
29. Madlensky L, Esplen MJ, Gallinger S, McLaughlin JR, Goel V. Relatives of colorectal cancer patients: Factors associated with screening behavior. Am J Prev Med. 2003;25(3):187–194. DOI:10.1016/S0749-3797(03)00202-2.
30. Codori AM, Petersen GM, Miglioretti DL, Boyd P. Health beliefs and endoscopic screening for colorectal cancer: potential for cancer prevention. Prev Med. 2001;33(2 pt1):128–136. DOI: 10.1006/pmed.2001.0862.
31. Manne S, Markowitz A, Winawer S, Meropol NJ, Haller D, Rakowski W et al. Correlates of colorectal cancer screening compliance and stage of adoption among siblings of individuals with early onset colorectal cancer. Heal Psychol. 2002;21(1):3–15. DOI:10.1037/0278-6133.21.1.3.