Abstract
Background
In Saudi Arabia, colorectal cancer (CRC) is the most common cancer in males and the third most common cancer in females. The current gold standard for colorectal cancer diagnosis is colonoscopy. Several concerns regarding the balance of ordering colonoscopy procedures for patients presenting with signs and symptoms. There are also several concerns regarding over-ordering the procedure when unnecessary. The current study aimed to evaluate the association between colorectal cancer and colonoscopic conditions in Saudi patients.
Methods
A 10-year cross-sectional study was conducted at Alnoor Specialty Hospital, Makkah, over the last ten years. Colonoscopy reports of patients were evaluated to identify the colonoscopy manifestations associated with mass, polyps, and bleeding.
Results
The current study evaluated 2158 cases admitted to the hospital for colonoscopic diagnosis. Results indicated that most of the patients were males (55.4%). Additionally, results showed a significant statistical association between tumor and bleeding, polyp, and hemorrhage. Moreover, it highlighted the association between polyps and bleeding, inflammation, and diverticulosis.
Conclusion
CRC screening in Saudi Arabia is comprehensive; however, there are a few areas for improvement, including standardization of colorectal cancer pathology reporting to improve the health system's quality. Also, the current study identified conditions that are significantly associated with reported colon polyps and tumors, which could aid in stratifying patients selected for screening via colonoscopy.
Keywords: Colorectal Cancer; Saudi Arabia; Colonoscopy Screening; Polyp, Bleeding; Inflammation; Diverticulosis
Introduction
Colorectal cancer (CRC) is the third most common cancer worldwide, with an increasing incidence and mortality rate (1). The incidence has increased significantly in both genders over the past few decades (2, 3). In Saudi Arabia, CRC is the most common type of cancer in males and the third most common in females (less than 14 years old) (4, 5). According to the latest statistics published in 2018 by the Saudi Ministry of Health, the male-to-female ratio of CRC incidence is 115:100 (MOH, 2018). About 30% of CRC cases have distant metastases at diagnosis in Saudi Arabia, compared to only 10% in the United States (4, 6, 7). This raises the question of whether this is due to inadequate CRC screening programs or a lack of public knowledge or awareness of early signs of cancer.
Screening protocols for CRC vary internationally, including the newly approved blood test for methylated Septin9, stool testing, radiology, and colonoscopy procedures with a wide range of specificity and sensitivity (8–10). This is one of the obstacles to planning and implementing a successful screening of CRC globally (8, 11). Additionally, colonoscopy and other screening methods for CRC reduced mortality but did not reduce the incidence (12, 13). This urges the identification of CRC risk factors to help solidify the screening program strategies and improve patient selection criteria.
The management of colorectal cancer varies according to the disease stage and may include laparoscopic surgery, chemoradiotherapy, and sphincter-preserving surgery. Consequently, patients may suffer from malnutrition, bowel dysfunction, and urinary and sexual dysfunction. Follow-up care extended for three years and involved some serological tests and computed tomography (CT) scans to detect the recurrence of the disease (14).
Non-modifiable risk factors for CRC include age and genetic mutations of some genes, such as APC, MLH1, and MSH2. Westernized nutritional patterns, physical inactivity, obesity, and smoking were also considered risk factors for CRC (15, 16). The most identified CRC risk factors are inflammatory bowel diseases, including Crohn's disease and ulcerative colitis (17). Furthermore, active bleeding, diverticulosis, hemorrhoids, and a history of polyps are all considered CRC risk factors (18, 19).
Colorectal polyps were one of the most frequently reported conditions affecting the colon, but not all were considered to have malignant potential (20). Neoplastic polyps of the colon, however, are of clinical importance because they are considered premalignant conditions (21) and can be considered the earliest form of colorectal cancer CRC (10). Most polyps are usually detected in asymptomatic patients, requiring about ten years to acquire neoplastic and malignant properties. Removing polyps from the colon is imperative before gaining malignant properties (20). Winawer et al. concluded in their study that none of the asymptomatic patients that underwent polypectomy by colonoscopy died from CRC (22). This conclusion indicates the importance of early detection and removal of polyps, and colonoscopy remains the main procedure for identifying polyps. Other conditions are also considered risk factors for developing CRC, including inflammatory bowel disease (IBD), bleeding, and hemorrhoids.
Inflammatory bowel diseases (IBD) were epidemiologically highlighted as factors that increase the risk of CRC (17, 23). Other studies found that CRC is a major cause of death for cases diagnosed with IBD (8). This has been attributed to the repeated insults to the mucosa of the colon during the inflammatory episodes of the disease (8). The risk of developing CRC in IBD patients increases with age (17, 24). The relationship between IBD and CRC development has led many healthcare organizations in the United States and the United Kingdom to increase surveillance of the affected population (17). In fact, repeated colonoscopy in IBD patients resulted in early detection of CRC in IBD patients and reduced mortality consequently (17, 24, 25).
Previous studies recommend early colonoscopy for patients with gastrointestinal bleeding (26). It was found that around 93% of patients diagnosed with CRC presented with bleeding (21). Another study found that 77% of patients diagnosed with CRC had a positive fecal occult blood test (27). In 2013, a study found that CRC patients with symptomatic bleeding were less likely to have metastasis at diagnosis (28). This study signifies the importance of screening patients with colorectal bleeding as a symptom to reduce mortality if a malignancy causes it; therefore, early detection and intervention (26, 28).
Another factor that is related to the development of CRC is hemorrhoid. However, there are several debates regarding the association of this condition with CRC. A study conducted in Taiwan for ten years about the association between CRC and hemorrhoids concluded that patients with hemorrhoids had an increased risk of developing CRC (29). Other studies suggested that hemorrhoids give false-positive fecal occult blood tests, and therefore, they suggested excluding patients with hemorrhoids from CRC screening (30). This was contradicted by other studies that concluded that hemorrhoids delayed CRC diagnosis due to diagnostic processes other than colonoscopy (31, 32). Thus, emphasizing the importance of colonoscopy as a screening test for patients with hemorrhoids to avoid the missed opportunity of diagnosis.
Identifying the risk factors and/or early clinical signs associated with CRC facilitates the design of more effective and sensitive CRC screening programs. For that reason, identifying the relationship between different symptoms and clinical conditions in colonoscopy reports with the probability of having a mass and/or polyps was essential. This study aims to evaluate the association of these colonoscopy manifestations with identifying masses (tumors) and polyps.
Methods
Study design and population: The current study is a 10-year cross-sectional retrospective analysis of patients who underwent colonoscopy procedures in Al Noor Specialist Hospital, Makkah, Saudi Arabia. It included an analysis of all colonoscopy reports between March 01, 2010, and December 30, 2020.
Data collection: The following data were collected from the Al Noor Specialist Hospital medical record archive: demographic data and complete colonoscopy reports. The colonoscopy reports were further evaluated to extract the selected conditions for analysis. These conditions included tumor and polyps, symptoms including bleeding, ulcers, inflammation, associated conditions (diverticulosis, hemorrhoids), and known risk factors (ulcerative colitis, Crohn's disease).
Ethical approval: The current study was approved by the Committee for Research Ethics for the Health of Makkah Region, Ministry of Health (H-02-K-076-0103-268).
Statistical analysis: The data analysis was conducted using the Statistical Packages for Social Sciences (SPSS) version 28 (IBM Corp, Armonk, NY, USA). Descriptive statistics of frequency and percentage and mean±standard deviation were performed for categorical and continuous variables, respectively. The chi-square test was used to examine differences in the prevalence of different categorical variables. A p-value ≤ 0.05 was considered statistically significant.
Results
Frequency of reported conditions in colonoscopy reports: The current study included 2158 Saudi patients that underwent colonoscopy at Al Noor Specialist Hospital during the 2010–2020 period. These reports were evaluated, and several conditions were identified according to this study's methodology. Male patients were higher (55.4%) than female patients (44.6%). Out of the total number of patients, 8% and 14% of patients were reported to have tumors and polyps, respectively. Results showed that hemorrhoid and inflammation were the most reported conditions (41.4% and 17.3%, respectively). Additionally, bleeding, ulcers, and diverticulosis were reported. Ulcerative colitis and Crohn's disease were the least reported diseases, with only 2% for the former and 0.6% for the latter (Table 1).
Table 1.
Characteristic of patients undergoing colonoscopy (n = 2158)
| Characteristic | n | % | |
| Total | 2158 | ||
| Female | 963 | 44.6 | |
| Gender | Male | 1195 | 55.4 |
| Tumors | Yes | 173 | 8.0 |
| No | 1985 | 92.0 | |
| Polyp | Yes | 313 | 14.5 |
| No | 1845 | 85.5 | |
| Bleeding | Yes | 249 | 11.5 |
| No | 1909 | 88.5 | |
| Ulcer | Yes | 223 | 10.3 |
| No | 1935 | 89.7 | |
| Inflammation | Yes | 373 | 17.3 |
| No | 1784 | 82.7 | |
| Haemorrhoid | Yes | 893 | 41.4 |
| No | 1265 | 58.6 | |
| Diverticulosis | Yes | 199 | 9.2 |
| No | 1959 | 90.8 | |
| Ulcerative Colitis | Yes | 44 | 2.0 |
| No | 2114 | 98.0 | |
| Crohn's disease | Yes | 12 | 0.6 |
| No | 2146 | 99.4 | |
Bleeding, polyp and hemorrhoid showed association with tumors in colonoscopy reports. Table 2 shows the association between tumors and gender, bleeding, polyp, ulcer, inflammation, diverticulosis, hemorrhoid, ulcerative colitis, and Crohn's disease. Results indicated that only 173 (8%) cases reported tumors. The association analysis indicated that the tumor was associated with a bleeding, polyp, and hemorrhoid (53, 43, and 36, respectively; p-value= 0.001). Results also indicated no statistical association between tumors and diverticulosis, ulcerative colitis, and Crohn's disease (11, 1, and 1, respectively; p-value > 0.005). Additionally, among the 173 cases, only 19 had an ulcer, and 21 had colorectal inflammation.
Table 2.
The association of tumors with gender and other colonoscopic conditions
| Characteristics | Tumour | Chi-Square | p-value | ||||
| YES | NO | ||||||
|
| |||||||
| n | % | n | % | ||||
| Gender | Female | 82 | 3.8 | 881 | 40.8 | 0.586 | 0.444 |
| Male | 91 | 4.2 | 1104 | 51.2 | |||
| Bleeding | Yes | 53 | 2.5 | 196 | 9.1 | 67.202 | 0.001 |
| No | 120 | 5.6 | 1789 | 82.9 | |||
| Polyp | Yes | 43 | 2.0 | 270 | 12.5 | 16.251 | 0.001 |
| No | 130 | 6.0 | 1715 | 79.5 | |||
| Ulcer | Yes | 19 | 0.9 | 204 | 9.5 | 0.085 | 0.770 |
| No | 154 | 7.1 | 1781 | 82.5 | |||
| Inflammation | Yes | 21 | 1.0 | 352 | 16.3 | 3.493 | 0.062 |
| No | 152 | 7.0 | 1632 | 75.6 | |||
| Diverticulosis | Yes | 11 | 0.5 | 188 | 8.7 | 1.842 | 0.175 |
| No | 162 | 7.5 | 1797 | 83.3 | |||
| Haemorrhoid | Yes | 36 | 1.7 | 857 | 39.7 | 32.812 | 0.001 |
| No | 137 | 6.3 | 1128 | 52.3 | |||
| Ulcerative Colitis | Yes | 1 | 0.0 | 43 | 2.0 | 2.010 | 0.156 |
| No | 172 | 8.0 | 1942 | 90.0 | |||
| Crohn's disease | Yes | 1 | 0.0 | 11 | 0.5 | 0.002 | 0.968 |
| No | 172 | 8.0 | 1974 | 91.5 | |||
The impact of the clinical manifestation of CRC on cancer diagnosis: The association of polyp with gender, bleeding, ulcer, inflammation, diverticulosis, hemorrhoid, ulcerative colitis, and Crohn's disease are presented in table 3. Results indicated that 313 patients (14.5%) reported having polyp in their colonoscopy report. Furthermore, polyps' formation was higher in male than female patients (203 and 110, respectively) with a highly significant difference (p-value= 0.001). Inflammation, bleeding, and diverticulosis were polyps' most common associated conditions (71, 49, and 40 cases, respectively). The association between polyp and inflammation was highly statistically significant (p-value= 0.006). The association between reporting polyps with bleeding and diverticulosis was also significant (p-value= 0.014 and 0.019, respectively).
Table 3.
The association of the polyp with gender and other colonoscopic conditions
| Characteristics | Polyp | Chi-Square | p-value | ||||
|
| |||||||
| YES | NO | ||||||
| n | % | n | % | ||||
| Gender | Female | 110 | 5.1 | 853 | 39.5 | 13.317 | 0.001 |
| Male | 203 | 9.4 | 992 | 46.0 | |||
| Bleeding | Yes | 49 | 2.3 | 200 | 9.3 | 6.078 | 0.014 |
| No | 264 | 12.2 | 1645 | 76.2 | |||
| Ulcer | Yes | 38 | 1.8 | 185 | 8.6 | 1.290 | 0.256 |
| No | 275 | 12.7 | 1660 | 76.9 | |||
| Inflammation | Yes | 71 | 3.3 | 302 | 14.0 | 7.440 | 0.006 |
| No | 242 | 11.2 | 1542 | 71.5 | |||
| Diverticulosis | Yes | 40 | 1.9 | 159 | 7.4 | 5.537 | 0.019 |
| No | 273 | 12.7 | 1686 | 78.1 | |||
| Haemorrhoid | Yes | 130 | 6.0 | 763 | 35.4 | 0.004 | 0.953 |
| No | 183 | 8.5 | 1082 | 50.1 | |||
| Ulcerative Colitis |
Yes | 7 | 0.3 | 37 | 1.7 | 0.071 | 0.789 |
| No | 306 | 14.2 | 1808 | 83.8 | |||
| Crohn's disease | Yes | 1 | 0.0 | 11 | 0.5 | 0.371 | 0.543 |
| No | 312 | 14.5 | 1834 | 85.0 | |||
Discussion
The present study investigated the colonoscopic reports of patients admitted to Alnoor Specialty Hospital over the last ten years. Results revealed that most patients who underwent colonoscopy were male, and the main reported conditions were hemorrhoids, polyps, and inflammation. Although colon cancer is more common in males, other colonic disorders such as colonic polyps, Crohn's disease, and hemorrhoids are more frequent in females (33–35). Thus, gender-specific differences in colonic disorders should be acknowledged in colonoscopy testing/screening reports to avoid late diagnosis and improve the management and prevent deterioration of the case.
The findings of the current study showed that colonic tumor was significantly associated with bleeding, polyps, and hemorrhoids. At the same time, colonic polyps were significantly associated with inflammation, diverticulosis, and bleeding. Although only 2.3% of patients with polyps and 2.5% with tumors presented with bleeding, it was considered a significant factor related to colonic conditions, tumors, and polyps. Bleeding is one of the most common symptoms of colorectal polyps and indicates colonoscopy (36). Moreover, it was considered an acute complication in patients with colon cancer (37). Bleeding was also associated with various colon ulcerative, benign, and malignant conditions (38). Another study demonstrated that bleeding was the main symptom in most CRC patients (28). Collectively, these findings highlight the necessity of colonoscopy for patients with colonic bleeding.
Similar to previously published findings, our data identified a significant association between colonic tumors and hemorrhoids. A study has suggested that patients with hemorrhoids had a roughly two-fold greater chance of developing CRC and highlighted the urge to screen colonoscopy for patients with hemorrhoids (29). Furthermore, colonoscopy was recommended for patients with hemorrhoids because CRC and hemorrhoids share similar lifestyle-associated risk factors, including low fiber consumption, obesity, and insufficient exercise (39).
Although polyps were considered benign growth, polypectomy was essential to CRC prevention (40). Therefore, patients with a history of polyps are subject to annual surveillance colonoscopy (41). Another benign colonic condition that was found to be associated with polyps was diverticulosis. Several studies investigated diverticulosis as a risk factor for polyps and/or CRC and showed conflicting findings. Some studies argue that diverticulitis was not a risk factor for polyps or CRC (42, 43). Several studies showed a significant association between diverticulosis and pre-cancerous polyps, but patients with diverticulosis were highly likely to develop polyps (25, 44, 45). Other studies have also linked diverticulosis to CRC (46, 47). Extensive prospective cohort studies were needed to validate the conflicting data on diverticular disease as a risk factor to determine the significance of colonoscopy following the diagnosis of diverticular disease by ultrasound abdominal ultrasound and elevated C-reactive protein (CRP) value.
The current data showed that inflammation was significantly associated with polyps but not tumors. However, the association between inflammation and CRC was well established (48). Colonic inflammation includes colitis, salmonellosis, shigellosis, travelers' diarrhea, diverticular disease, inflammatory bowel syndrome, and inflammatory bowel disease. Colonoscopy reports evaluated in the current cohort study lacked histopathological findings, including the classification of the inflammatory conditions. This limitation complicates the analysis of the association between polyps and different types of colonic inflammation in the current data set. However, previous reports showed multiple associations between colonic inflammatory conditions (49). Inflammatory colon conditions, such as microscopic colitis, inflammatory bowel disease (IBD), and active colitis, are associated with decreased prevalence of all types of colon polyps, including hyperplastic polyps, serrated adenomas, and adenomas (50, 51). In contrast, IBD, including Ulcerative Colitis and Crohn's disease, were significantly associated with tumor development (17, 49).
Still, several challenges were under review to follow up cases of history of polyps, and several researchers were working on improving the recommendations for post-polypectomy surveillance by colonoscopy (24). The problem with post-polypectomy screening is that patients are usually asymptomatic, which leads to a drain on the healthcare system. Also, increased intervals between screenings could result in missed diagnoses in some cases (24). Altogether, this signifies the importance of conducting more analyses of retrospective studies to improve the guidelines and recommendations for post-polypectomy surveillance based on evidence.
Ideal guidelines for colonoscopy ought to lead to early detection of CRC, improve prognosis, and effectively use medical resources and personnel. Early detection of CRC was associated with a better prognosis and reduced mortality from CRC (52, 53). Current screening guidelines involve tests to detect the presence of blood in the stool, such as fecal occult blood tests and fecal immunochemical tests. CRC screening guidelines also involve colonoscopy or sigmoidoscopy but less frequently and at an older age (beginning at age 50) (54). With the increased incidence and morbidity from CRC, screening guidelines should be revisited, especially because studies showed that screening tests for fecal blood were ineffective (55), and colonoscopy might miss some CRC lesions. Therefore, symptoms and clinical conditions should be identified, and their association with CRC investigated to develop well-detailed guidelines for screening and surveillance colonoscopy.
A large-scale study is not available in Saudi Arabia and is necessary to evaluate the colonoscopic conditions diagnosed during the procedure. The current study compromises a sample collected from a single hospital in Makkah. The sample size included more than 2000 patients admitted to Alnoor Specialty Hospital for ten years. Though a higher number of male patients underwent colonoscopy, there was a significant association of polyps in female patients. In the same sample, there was a relationship between identifying tumors and other conditions, including bleeding, polyps, and hemorrhoids.
On the other hand, polyp identification in patients was associated with bleeding, inflammation, and diverticulosis. The research has previously identified such an association, and the current study found that the conditions correlated with tumors are somewhat different from those correlated with polyp identification. This kind of study aids in identifying patients with high risk and aids in stratifying them for early screening of colorectal cancer. Until this study was conducted, few publications reviewed the retrospective data on colonoscopy in Saudi Arabia. Additional research on a larger dataset collected from different centers is recommended to verify this study's conclusion and draw a nationwide conclusion.
In conclusion, this study shows that CRC screening in Saudi Arabia is comprehensive; however, there are few rooms for improvement, such as standardization of colorectal cancer pathology reporting. Quality pathology reporting could improve cancer management as well as facilitate international comparisons. Also, more efforts should be made to improve public awareness about the risk factors of CRC and the importance of colonoscopy screening.
Acknowledgement
The author would like to thank the Alnoor Specialty Hospital, Makkah, Saudi Arabia, for supporting this work.
References
- 1.Almatroudi A. The incidence rate of colorectal cancer in Saudi Arabia: an observational descriptive epidemiological analysis. International Journal of General Medicine. 2020;13:977. doi: 10.2147/IJGM.S277272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Karsa L, Lignini T, Patnick J, Lambert R, Sauvaget C. The dimensions of the CRC problem. Best practice & research Clinical gastroenterology. 2010;24(4):381–396. doi: 10.1016/j.bpg.2010.06.004. [DOI] [PubMed] [Google Scholar]
- 3.Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: incidence, mortality, survival, and risk factors. Przeglad gastroenterologiczny. 2019;14(2):89. doi: 10.5114/pg.2018.81072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.MOH, author. Health Days 2018: Colorectal Cancer Awareness Month. Ministry of Health-Kingdom of Saudi Arabia; 2018. [Google Scholar]
- 5.Gosadi IM. National screening programs in Saudi Arabia: overview, outcomes, and effectiveness. Journal of infection and public health. 2019;12(5):608–614. doi: 10.1016/j.jiph.2019.06.001. [DOI] [PubMed] [Google Scholar]
- 6.Alyabsi M, Alhumaid A, Allah-Bakhsh H, Alkelya M, Aziz MA. Colorectal cancer in Saudi Arabia as the proof-of-principle model for implementing strategies of predictive, preventive, and personalized medicine in healthcare. EPMA Journal. 2020;11(1):119–131. doi: 10.1007/s13167-019-00186-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Labianca R, Merelli B. Screening and diagnosis for colorectal cancer. present and future. Tumori Journal. 2010;96(6):889–901. [PubMed] [Google Scholar]
- 8.Soetikno R, Chiu HM, Asokkumar R, Sanduleanu S, Tanaka S, Rastogi A, Uedo N, Hammad H, Triadafilopoulos G. Letter to the Editor in Response to “Endoscopic Recognition and Management Strategies for Malignant Colorectal Polyps: Recommendations of the US Multi-Society Task Force on Colorectal Cancer”. Gastroenterology. 2021;160(6):2216–2220. doi: 10.1053/j.gastro.2020.12.051. [DOI] [PubMed] [Google Scholar]
- 9.Issa IA, Noureddine M. Colorectal cancer screening: An updated review of the available options. World journal of gastroenterology. 2017;23(28):5086. doi: 10.3748/wjg.v23.i28.5086. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Shaukat A, Kaltenbach T, Dominitz JA, Robertson DJ, Anderson JC, Cruise M, Burke CA, Gupta S, Lieberman D, Syngal S. Endoscopic recognition and management strategies for malignant colorectal polyps: recommendations of the US Multi-Society Task Force on Colorectal Cancer. Gastrointestinal endoscopy. 2020;92(5):997–1015. doi: 10.1016/j.gie.2020.09.039. e1011. [DOI] [PubMed] [Google Scholar]
- 11.Citarda F, Tomaselli G, Capocaccia R, Barcherini S, Crespi M, Group IMS Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence. Gut. 2001;48(6):812–815. doi: 10.1136/gut.48.6.812. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Byers T, Levin B, Rothenberger D, Dodd GD, Smith RA. American Cancer Society guidelines for screening and surveillance for early detection of colorectal polyps and cancer: update 1997. CA: a cancer journal for clinicians. 1997;47(3):154–160. doi: 10.3322/canjclin.47.3.154. [DOI] [PubMed] [Google Scholar]
- 13.Muller AD, Sonnenberg A. Prevention of colorectal cancer by flexible endoscopy and polypectomy: a case-control study of 32 702 veterans. Annals of internal medicine. 1995;123(12):904–910. doi: 10.7326/0003-4819-123-12-199512150-00002. [DOI] [PubMed] [Google Scholar]
- 14.Brown KG, Solomon MJ, Mahon K, O'Shannassy S. Management of colorectal cancer. Bmj. 2019;366 doi: 10.1136/bmj.l4561. [DOI] [PubMed] [Google Scholar]
- 15.Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nature reviews Gastroenterology & hepatology. 2019;16(12):713–732. doi: 10.1038/s41575-019-0189-8. [DOI] [PubMed] [Google Scholar]
- 16.O'Sullivan DE, Sutherland RL, Town S, Chow K, Fan J, Forbes N, Heitman SJ, Hilsden RJ, Brenner DR. Risk factors for early-onset colorectal cancer: A systematic review and meta-analysis. Clinical Gastroenterology and Hepatology. 2021 doi: 10.1016/j.cgh.2021.01.037. [DOI] [PubMed] [Google Scholar]
- 17.Stidham RW, Higgins PD. Colorectal cancer in inflammatory bowel disease. Clinics in colon and rectal surgery. 2018;31(03):168–178. doi: 10.1055/s-0037-1602237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Holtedahl K, Borgquist L, Donker GA, Buntinx F, Weller D, Campbell C, Månsson J, Hammersley V, Braaten T, Parajuli R. Symptoms and signs of colorectal cancer, with differences between proximal and distal colon cancer: a prospective cohort study of diagnostic accuracy in primary care. BMC Family Practice. 2021;22(1):1–13. doi: 10.1186/s12875-021-01452-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Cooper GS, Xu F, Schluchter MD, Koroukian SM, Sloan JSB. Diverticulosis and the risk of interval colorectal cancer. Digestive diseases and sciences. 2014;59(11):2765–2772. doi: 10.1007/s10620-014-3246-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Secretariat MA, author. Screening methods for early detection of colorectal cancers and polyps: summary of evidence-based analyses. Ontario Health Technology Assessment Series. 2009;9(6):1. [PMC free article] [PubMed] [Google Scholar]
- 21.Shussman N, Wexner SD. Colorectal polyps and polyposis syndromes. Gastroenterology report. 2014;2(1):1–15. doi: 10.1093/gastro/got041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Winawer SJ, Zauber AG, Ho MN, O'brien MJ, Gottlieb LS, Sternberg SS, Waye JD, Schapiro M, Bond JH, Panish JF. Prevention of colorectal cancer by colonoscopic polypectomy. New England Journal of Medicine. 1993;329(27):1977–1981. doi: 10.1056/NEJM199312303292701. [DOI] [PubMed] [Google Scholar]
- 23.Wang Z-H, Fang J-Y. Colorectal cancer in inflammatory bowel disease. epidemiology, pathogenesis and surveillance. Gastrointestinal tumors. 2014;1(3):146–154. doi: 10.1159/000365309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Winawer SJ, Zauber AG, Fletcher RH, Stillman JS, O'brien MJ, Levin B, Smith RA, Lieberman DA, Burt RW, Levin TR. Guidelines for colonoscopy surveillance after polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society. Gastroenterology. 2006;130(6):1872–1885. doi: 10.1053/j.gastro.2006.03.012. [DOI] [PubMed] [Google Scholar]
- 25.Wang F-W, Chuang H-Y, Tu M-S, King T-M, Wang J-H, Hsu C-W, Hsu P-I, Chen W-C. Prevalence and risk factors of asymptomatic colorectal diverticulosis in Taiwan. BMC gastroenterology. 2015;15(1):1–6. doi: 10.1186/s12876-015-0267-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Qureshi W, Adler D, Davila R, Egan J, Hirota W, Leighton J, Rajan E, Zuckerman M, Fanelli R, Wheeler-Harbaugh J. Standards of Practice Committee: ASGE Guideline: the role of endoscopy in the management of variceal hemorrhage, updated July 2005. Gastrointest Endosc. 2005;62(5):651–655. doi: 10.1016/j.gie.2005.07.031. [DOI] [PubMed] [Google Scholar]
- 27.Majumdar SR, Fletcher RH, Evans AT. How does colorectal cancer present? Symptoms, duration, and clues to location. The American journal of gastroenterology. 1999;94(10):3039–3045. doi: 10.1111/j.1572-0241.1999.01454.x. [DOI] [PubMed] [Google Scholar]
- 28.Hreinsson J, Jonasson J, Bjornsson E. Bleeding-related symptoms in colorectal cancer: a 4-year nationwide population-based study. Alimentary pharmacology & therapeutics. 2014;39(1):77–84. doi: 10.1111/apt.12519. [DOI] [PubMed] [Google Scholar]
- 29.Wu E-B, Sung F-C, Lin C-L, Wu K-L, Chen K-B. Colorectal Cancer Risk in Patients with Hemorrhoids: A 10-Year Population-Based Retrospective Cohort Study. International journal of environmental research and public health. 2021;18(16):8655. doi: 10.3390/ijerph18168655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Ting P-H, Lin X-H, Jiang J-K, Luo J-C, Chen P-H, Wang Y-P, Hsin I-F, Perng CL, Hou M-C, Lee FY. The factors associated with negative colonoscopy in screening subjects with positive immunochemical stool occult blood test outcomes. Journal of the Chinese Medical Association. 2018;81(9):759–765. doi: 10.1016/j.jcma.2017.11.015. [DOI] [PubMed] [Google Scholar]
- 31.Siminoff LA, Rogers HL, Harris-Haywood S. Missed opportunities for the diagnosis of colorectal cancer. BioMed research international. 2015;2015 doi: 10.1155/2015/285096. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Singh H, Daci K, Petersen LA, Collins C, Petersen NJ, Shethia A, El-Serag HB. Missed opportunities to initiate endoscopic evaluation for colorectal cancer diagnosis. The American journal of gastroenterology. 2009;104(10):2543. doi: 10.1038/ajg.2009.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Greuter T, Manser C, Pittet V, Vavricka SR, Biedermann L. Gender differences in inflammatory bowel disease. Digestion. 2020;101(1):102–108. doi: 10.1159/000504701. [DOI] [PubMed] [Google Scholar]
- 34.Alomari M, Al Momani L, Sarmini MT, Khazaaleh S, Nehme F, Wadhwa V, Thota PN, Sanaka MR. 264 The Differences in Prevalence, Distribution, and Detection Rates of Colonic Polyps Between Genders. Official journal of the American College of Gastroenterology ACG. 2019;114:S152–S154. [Google Scholar]
- 35.Avsar A, Keskin H. Haemorrhoids during pregnancy. Journal of Obstetrics and Gynaecology. 2010;30(3):231–237. doi: 10.3109/01443610903439242. [DOI] [PubMed] [Google Scholar]
- 36.Soleimaninejad M, Sharifian M. Evaluation of colonoscopy data for colorectal polyps and associated histopathological findings. Annals of Medicine and Surgery. 2020;57:7–10. doi: 10.1016/j.amsu.2020.07.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Yang X-F, Pan K. Diagnosis and management of acute complications in patients with colon cancer: bleeding, obstruction, and perforation. Chinese Journal of Cancer Research. 2014;26(3):331. doi: 10.3978/j.issn.1000-9604.2014.06.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Lee EW, Laberge JM. Differential diagnosis of gastrointestinal bleeding. Techniques in vascular and interventional radiology. 2004;7(3):112–122. doi: 10.1053/j.tvir.2004.12.001. [DOI] [PubMed] [Google Scholar]
- 39.Matkovic Z, Zildzic M. Colonoscopic Evaluation of Lower Gastrointestinal Bleeding (LGIB): Practical Approach. Medical Archives. 2021;75(4):274. doi: 10.5455/medarh.2021.75.274-279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Duloy AM, Keswani RN. Assessing the quality of polypectomy and teaching polypectomy. Gastrointestinal Endoscopy Clinics. 2019;29(4):587–601. doi: 10.1016/j.giec.2019.06.001. [DOI] [PubMed] [Google Scholar]
- 41.Bonnington SN, Rutter MD. Surveillance of colonic polyps: are we getting it right? World journal of gastroenterology. 2016;22(6):1925. doi: 10.3748/wjg.v22.i6.1925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Meurs-Szojda M, sive Droste JT, Kuik D, Mulder C, Felt-Bersma R. Diverticulosis and diverticulitis form no risk for polyps and colorectal neoplasia in 4,241 colonoscopies. International journal of colorectal disease. 2008;23(10):979–984. doi: 10.1007/s00384-008-0510-4. [DOI] [PubMed] [Google Scholar]
- 43.Lee HJ, Park SJ, Cheon JH, Kim TI, Kim WH, Kim HJ. The relationship between diverticulosis and colorectal neoplasia: A meta-analysis. PloS one. 2019;14(5):e0216380. doi: 10.1371/journal.pone.0216380. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Muhammad A, Lamendola O, Daas A, Kumar A, Vidyarthi G. Association between colonic diverticulosis and prevalence of colorectal polyps. International Journal of Colorectal Disease. 2014;29(8):947–951. doi: 10.1007/s00384-014-1908-9. [DOI] [PubMed] [Google Scholar]
- 45.Hirata T, Kawakami Y, Kinjo N, Arakaki S, Arakaki T, Hokama A, Kinjo F, Fujita J. Association between colonic polyps and diverticular disease. World Journal of Gastroenterology: WJG. 2008;14(15):2411. doi: 10.3748/wjg.14.2411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Kieff BJ, Eckert GJ, Imperiale TF. Is diverticulosis associated with colorectal neoplasia? A cross-sectional colonoscopic study. Official journal of the American College of Gastroenterology| ACG. 2004;99(10):2007–2011. doi: 10.1111/j.1572-0241.2004.30332.x. [DOI] [PubMed] [Google Scholar]
- 47.Morini S, Zullo A, Hassan C, Tomao S, Campo SM. Diverticulosis and colorectal cancer: between lights and shadows. Journal of clinical gastroenterology. 2008;42(7):763–770. doi: 10.1097/MCG.0b013e31816200fb. [DOI] [PubMed] [Google Scholar]
- 48.Nasef NA, Mehta S. Role of inflammation in pathophysiology of colonic disease: An update. International journal of molecular sciences. 2020;21(13):4748. doi: 10.3390/ijms21134748. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Franks AL, Slansky JE. Multiple associations between a broad spectrum of autoimmune diseases, chronic inflammatory diseases and cancer. Anticancer research. 2012;32(4):1119–1136. [PMC free article] [PubMed] [Google Scholar]
- 50.Sonnenberg A, Genta RM. Low prevalence of colon polyps in chronic inflammatory conditions of the colon. Official journal of the American College of Gastroenterology| ACG. 2015;110(7):1056–1061. doi: 10.1038/ajg.2015.130. [DOI] [PubMed] [Google Scholar]
- 51.Yen EF, Pokhrel B, Bianchi LK, Roy HK, Du H, Patel A, Hall CR, Witt BL. Decreased colorectal cancer and adenoma risk in patients with microscopic colitis. Digestive diseases and sciences. 2012;57(1):161–169. doi: 10.1007/s10620-011-1852-2. [DOI] [PubMed] [Google Scholar]
- 52.Gupta AK, Brenner DE, Turgeon DK. Early detection of colon cancer. Molecular diagnosis & therapy. 2008;12(2):77–85. doi: 10.1007/BF03256273. [DOI] [PubMed] [Google Scholar]
- 53.Buie WD, Attard J-AP. Follow-up recommendations for colon cancer. Clinics in colon and rectal surgery. 2005;18(03):232–243. doi: 10.1055/s-2005-916284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Hultcrantz R. Aspects of Colorectal cancer screening, methods, age and gender. Journal of Internal Medicine. 2021;289(4):493–507. doi: 10.1111/joim.13171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Ferlizza E, Solmi R, Sgarzi M, Ricciardiello L, Lauriola M. The Roadmap of Colorectal Cancer Screening. Cancers. 2021;13(5):1101. doi: 10.3390/cancers13051101. [DOI] [PMC free article] [PubMed] [Google Scholar]
