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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 4  |  Issue : 3  |  Page : 232-238

Colorectal cancer surveillance after resection: Timing and findings in clinical practice


1 Division of Gastroenterology, King Khalid University Hospital, King Saud University, Riyadh, Saudi Arabia
2 Department of Medicine, Albadaya General Hospital, Alqassim, Saudi Arabia
3 Division of Gastroenterology, Security Forces Hospital, Riyadh, Saudi Arabia
4 Division of Gastroenterology, King Khalid University Hospital, King Saud University, Riyadh; Division of Gastroenterology, King Khalid University Hospital, College of Medicine, King Saud University; Division of Gastroenterology, McGill University Health Centre, McGill University, Montréal, Québec, Canada

Date of Submission15-Oct-2020
Date of Decision08-Mar-2021
Date of Acceptance21-Mar-2021
Date of Web Publication26-Jul-2021

Correspondence Address:
Majid Abdulrahman Almadi
Division of Gastroenterology, King Khalid University Hospital, King Saud University, Riyadh 11461

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jnsm.jnsm_130_20

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  Abstract 


Background: Multiple guidelines have recommended performing surveillance colonoscopies after resection of colorectal cancer. However, there has been debate about the optimal frequency of endoscopic surveillance and its yield. Objective: The objective of this study was to explore the adherence and the yield of surveillance colonoscopy in our population. Design: This was a retrospective cohort study. Setting: This study was carried out in two tertiary care centers in Riyadh of all patients who were found to have colon cancer on colonoscopy. Patients and Methods: All patients who were found to have colon cancer on colonoscopy at one center from January 2016 to July 2019 and the second center from April 2012 to April 2019 were included in the study. The main outcome measures were as follows: rate of adherence to surveillance colonoscopies as well as the rate of synchronous and metachronous tumors identified. The sample size was not calculated. Results: A total of 280 patients were identified with a mean age of 64.5 years (standard deviation: 13.1), 61.4% were male, and the majority (72%) of the original cancers were left sided (rectum – 25.45%, rectosigmoid – 13.45%, sigmoid – 25.82%, and descending colon – 7.27%). Surveillance was performed in 55.7%, 17.9% did not attend their scheduled procedures, 2.1% refused, while there was no clear reason in 8.9%. Surveillance was not applicable to 15.3% of the study population. Over the course of three rounds of surveillance, the timing of the procedures was in line with recommendations in 66.8% in the first round while it was 20% in the second and third rounds. The procedures were normal in 69%, 71.9%, and 90% of the first, second, and third rounds, respectively. Metachronous adenocarcinoma was seen in 2.6% and synchronous adenocarcinoma in 0.6% during the first round. Adenocarcinoma was found in 5 out of 75 patients in the second round and 1 out of 10 in the third round. Conclusion: The attrition rate and deviation from timing suggested by guidelines are high. Furthermore, the yield of surveillance colonoscopies for important findings is clinically relevant. The limitations of this study were as follows: retrospective, probability of unmeasured confounders, as well possibility of attrition bias.

Keywords: Adenoma, colon cancer, colonoscopy, early detection, endoscopy, epidemiology, polyp, prevalence, Saudi Arabia, tumor


How to cite this article:
Aloun AA, Alnafisah KA, Azzam N, Aljebreen A, Alotaibi E, Alkhathami M, Mahrous WK, Alghamdi AA, Alhujairy BA, Al Sir BE, Obeidalah I, Almadi MA. Colorectal cancer surveillance after resection: Timing and findings in clinical practice. J Nat Sci Med 2021;4:232-8

How to cite this URL:
Aloun AA, Alnafisah KA, Azzam N, Aljebreen A, Alotaibi E, Alkhathami M, Mahrous WK, Alghamdi AA, Alhujairy BA, Al Sir BE, Obeidalah I, Almadi MA. Colorectal cancer surveillance after resection: Timing and findings in clinical practice. J Nat Sci Med [serial online] 2021 [cited 2021 Nov 29];4:232-8. Available from: https://www.jnsmonline.org/text.asp?2021/4/3/232/322317




  Introduction Top


The incidence of colon cancer has increased globally, with the 2017 global age-standardized incidence rate being 23.2 (95% uncertainty intervals [UIs]: 22.7–23.7)/100,000 person-years.[1] This is also true in Saudi Arabia where the age-standardized incidence rate in 1990 was 6.7 (95% UI: 5.2–8.7) cases/100,000 person-years to 16.6 (95% UI: 14.2–18.9) cases/100,000 person-years in 2017. Although this represents a 149.2% (95% UI: 76.9–242.9) percentage change, it still is below the global average.[1] This low incidence of colon cancer in Saudi Arabia is concurrent with the findings of lower adenoma prevalence in both screening[2] and symptomatic colonoscopies.[3] Despite the lower incidence, it appears that colon cancer affects the population at a younger age[4] as well as presents at an advanced stage[5],[6] and has a lower 5-year survival.[5],[6] Given these factors, national guidelines have been developed to advocate for colorectal cancer screening[7] as well as studies conducted with the aim of exploring barriers to screening uptake.[8],[9],[10]

An area that has not been explored in our region as of yet, is the adherence to postcolon cancer resection surveillance guidelines. In a meta-analysis of studies looking into endoscopic surveillance after surgery for colorectal cancer, the incidence of recurrent colon cancer was found to be 2.7% (95% confidence interval [CI]: 1.9%–3.9%).[11] It also found that the risk of colorectal cancer at the anastomosis site was lower after 24 months with an odds ratio of 0.56 (95% CI: 0.32–0.98) and 90.8% of all these tumors were detected within 36 months of surgery.[11] It appears that the adherence to international guidelines for postpolypectomy surveillance[12] as well as postcolorectal cancer resection is low.[13],[14],[15]

The purpose of this study was to evaluate the adherence to surveillance colonoscopy based on the recommendations from multiple societies/associations such as the European Society of Gastrointestinal Endoscopy, the European Society of Digestive Oncology, the Association of Coloproctology of Great Britain and Ireland, the British Society of Gastroenterology, the American Cancer Society, and the United States Multi-Society Task Force (USMSTF). We also aimed to explore the incidence of recurrent/secondary colorectal cancer in our population in terms of timing and location of tumor.


  Patients and Methods Top


Study design and setting

This is a retrospective cohort study that was performed at two tertiary care hospitals in Riyadh, Saudi Arabia, one of which was an academic teaching hospital.

Patients' selection

Using an electronic endoscopic reporting database, all patients who underwent a colonoscopy at one center from January 2016 to July 2019 and the second center from April 2012 to April 2019 and were found to have colon cancer were included in the study. Endoscopy reports were reviewed, and data collected included age, sex, location of the original tumor, whether surveillance colonoscopies were performed, the timing and findings on those subsequent colonoscopies as well as the histological findings of the lesions identified at each endoscopy. We included all patients who had a complete colonoscopy before surgery as well as a histopathological confirmation of adenocarcinoma on biopsy. We excluded patients who had inflammatory bowel disease or those who had an incomplete colonoscopy or suboptimal preparation as documented in the endoscopy report. Currently, there are no guidelines within the Kingdom of Saudi Arabia for the timing of surveillance of colon cancer from the point of view of performing colonoscopies and, as such, what is currently practiced is that international guidelines were adopted [Table 1]. We mapped the procedures as a continuum and segment those practices against these guidelines.
Table 1: Recommendation of various organizations on the frequency of colonoscopy after surgical resection of colon cancer

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Synchronous tumors were defined as those found in the same patient up to 6 months after the initial diagnosis, while metachronous tumors were defined as those seen after 6 months and were located away from the anastomosis.[16],[17],[18]

No personal identification information or other personal identifiers were recorded to ensure patient confidentiality.

Statistical analysis

Descriptive statistics were computed for continuous variables, including minimum and maximum values, means, standard deviations (SDs), as well as 95% CIs and frequencies for categorical variables when appropriate. If hypothesis testing was used, the Pearson's Chi-squared t-test and, where appropriate, the Fisher's exact tests were used.[19] A one-way analysis of variance to test for differences among groups when comparing more than one group was performed when appropriate.

R Studio[20] was used for analysis using the R statistical language.[21] A statistical significance threshold of P = 0.05 was adopted. No attempt at imputation was made for missing data.


  Results Top


Demographics and historical data

A total of 280 patients were identified with a mean age of 64.5 (SD: 13.1; range: 25–101). Males composed 61.4% (95% CI: 55.7%–67.4%) while 38.6% were female (95% CI: 32.9%–44.5%). The locations of the lesions identified were rectum (25.5%), rectosigmoid (13.5%), sigmoid (25.8%), descending colon (7.3%), splenic flexure (4.0%), transverse colon (4.4%), hepatic flexure (5.1%), ascending colon (6.5%), and the cecum (8.0%) [Figure 1].
Figure 1: Location of tumors for the patient population that was included in the study

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Surveillance colonoscopies were only performed in 156 (55.7%) while 50 patients (17.9%) did not abide to the recommendation, and 6 patients (2.1%) refused. At the time of gathering data, 16 (5.7%) were still awaiting surgery and 7 (2.5%) had died. It was not indicated in 20 (7.1%) as they were either inoperable or had metastasis or they had a total colectomy due to familial adenomatous polyposis syndrome. There was no clear reason that was documented for the remainder 25 patients (8.9%).

There was no association between the sex (females 66.3% vs. 64.6% males, P = 0.79), nor the location of the primary resected tumor (P = 0.23) and undergoing the first surveillance colonoscopy. There was also no difference in the age of those who had the first surveillance colonoscopy as compared to those who did not (64.2 years vs. 66.3 years, respectively, P = 0.24) [Figure 2].
Figure 2: Distribution of the location of colon cancer in the cohort included in the study by age and gender

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Timing and results of the first surveillance colonoscopy

For those who had a colonoscopy performed (n = 156), 105 (66.9%) were around the 1-year recommendation for surveillance while it was performed more than 1 year after surgical resection in 27.4% and much earlier in 5.8% [Figure 3].
Figure 3: The timing of the performance of surveillance colonoscopy based on the guidelines

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Of those who had a surveillance colonoscopy, 68.2% were normal while 31.8% were not. Of the abnormal findings on the first surveillance colonoscopies, an adenoma without dysplasia was found in 8.9%, hyperplastic polyps in 3.2%, a metachronous adenocarcinoma in 2.6%, anastomotic stenosis in 2.6%, an adenoma with dysplasia in 1.9%, a synchronous adenocarcinoma in 0.6%, while 10.8% had nonspecific findings [Figure 4].
Figure 4: Findings on each round of surveillance colonoscopy

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Timing and results of the second surveillance colonoscopy

A total of 75 patients had a second surveillance colonoscopy and 29 (38.7%) of those were after 1 year of the prior colonoscopy, 15 (20%) were after 2 years, 15 (20%) after 3 years, 9 (12%) after 4 years, 4 (5.3%) after 5 years, and a patient had his second surveillance colonoscopy after 6 years. Two patients had their second colonoscopy only after 6 months from the first surveillance colonoscopy [Figure 3].

The findings on the second surveillance colonoscopy were normal in 71.8%. Of the abnormalities that were detected, five patients had masses (4 of which were at the anastomosis site) and all where adenocarcinoma on histopathology, an adenoma without dysplasia was found in 11.3%, hyperplastic polyps in 4.2%, anastomotic stenosis in 1.4%, while 4.2% had nonspecific findings [Figure 4].

Timing and results of the third surveillance colonoscopy

Only ten patients had undergone a third surveillance colonoscopy at the time of the study at 6 months (1 patient), 1 (5 patients), 2 (1 patient), 3 (1 patient), and 5 years (2 patients) from the second surveillance colonoscopy [Figure 3]. Nine of the ten had normal colonoscopies, while one had adenocarcinoma [Figure 4].


  Discussion Top


Colonoscopy is an indispensable tool in the screening of colon cancer but has limitations including the imperfect sensitivity either due to patient factors (including the bowel preparation),[22],[23] the operator and setting[24],[25] as well as a myriad of other factors. These factors could result in missed lesions, or after resection of colon cancer, recurrent tumors. Patients who had undergone resection of a colon cancer are at a higher risk of recurrence of cancer when compared to the general population[26],[27] with a standardized incidence ratio of 1.3 (95% CI: 1.1–1.5) and the risk is highest in the first 3 years.[26] The cumulative incidence of recurrent colorectal cancer after treatment has been reported in the Rotterdam Cancer Registry in The Netherlands to be 1.1% at 3 years, 2.0% at 6 years, and 3.1% at 10 years.[26]

After curative resection of colon cancer, the recommendations of the American Cancer Society and the USMSTF on Colorectal Cancer[28] are to have a repeat colonoscopy 1 year after resection, then after 3 years, and then every 5 years if normal which the National Comprehensive Cancer Network has also recommended in their guidelines[29] and is somewhat similar to the European Society for Medical Oncology (ESMO) guidelines where they recommended a colonoscopy at 1 year then every 3–5 years thereafter.[30] The American Society of Clinical Oncology (ASCO) recommended a colonoscopy at 1 year after surgery and if normal every 5 years thereafter[31] [Table 1].

While for rectal cancer, the recommendations from the USMSTF were to perform a flexible sigmoidoscopy or endoscopic ultrasound every 3–6 months for the first 2–3 years after surgery for patients at high risk for local recurrence.[28] This is different from the ESMO guidelines, which recommended a colonoscopy every 5 years up to age 75 in those with rectal cancer.[32] ASCO recommended a proctosigmoidoscopy every 6 months for 2–5 years if the patient did not receive pelvic radiotherapy [Table 1].

To have a procedure performed in accordance with the international guidelines for postcolorectal cancer resection surveillance, a recommendation to a patient has to be made. It is clear from the literature that a recommendation from the managing physician in cases of postpolypectomy surveillance is not made or is not in accordance with the recommended guideline timeframe in a large proportion of cases (41%–86%).[33],[34] We perceive that this would be less of a case in the situation of colon cancer as the stakes are higher for both patients and managing physicians. Yet, in our study, it appears that 17.9% did not attend their first surveillance colonoscopy and 2.1% refused. Whether these patients have truly forgone their surveillance colonoscopy is difficult to ascertain, and they might have opted to have these procedures at other centers for whatever reason. Even then, the rate of adherence to postcolorectal cancer resection surveillance has been low in numerous studies, for example, a study in Australia demonstrated that adherence was <30%.[13]

One of the limitations of our study is the lack of data on the comorbidities and functional status of these patients was at the time of the diagnosis and after undergoing curative therapy. This might have influenced the decision of either the patient/family members or the health-care provider to forgo surveillance, correctly, if the perceived risks outweigh the potential benefits. There has been a recent challenge to the blanket policy of screening individuals for colorectal cancer based on the sole criterion of age and rather to use a more individualized risk-stratified approach.[35] This has sparked a large debate,[36],[37],[38] but this could also spill over to the realm of surveillance postcolon cancer treatment. To prove a mortality benefit for postcolon cancer resection, surveillance procedures for a large sample size of patients are required coupled with a prolonged follow-up period, such a study is not possible in a controlled trial setting, and a registry-based study would be most practical. A study utilizing the Surveillance, Epidemiology, and End Results-Medicare database where the association between adherence to postsurveillance recommendations and 5-year survival was performed which included 17,860 Stage II and III patients with colon cancer, demonstrated that there was no difference in the overall survival between those who were more adherent or less adherent posttreatment surveillance testing (hazard ratio [HR]: 1.04, 95% CI: 0.98–1.10).[39] A similar finding was found in a randomized trial that looked into the more frequent use of computerized tomography and carcinoembryonic antigen every 6, 12, 18, 24, and 36 months after surgery or low frequency at 12 and 36 months after surgery, and there was no difference in the colon cancer-specific recurrence risk with a risk difference of 2.2% (95% CI: ‒1.0%–5.4%).[40] These patients had to have a colonoscopy within 3 months of surgery as an inclusion criterion, which would reduce the likelihood of a missed concurrent lesion during the initial diagnosis.[41],[42]In two other randomized trials there was no improvement in overall survival which was also found in two meta-analyses where intense surveillance had no effect on overall survival and found no benefit.[43],[44]

These findings challenge the current practice of surveillance, but in a meta-analysis that stratified the overall survival in the included studies comparing the use of usual colonoscopy surveillance to no colonoscopy, there was an overall survival benefit (four studies) with a HR of 0.65 (95% CI: 0.53–0.81), but the use of more intensive colonoscopy surveillance as compared to usual surveillance was not associated with an overall survival benefit with a HR of 0.86 (95% CI: 0.69–1.06).[45]

The British Society of Gastroenterology/Association of Coloproctology of Great Britain and Ireland/Public Health England had recently published a guideline that used the Grading of Recommendations, Assessment, Development, and Evaluations (GRADE) methodology and had recommended that after a potentially curative colorectal cancer resection, individuals should have a clearance colonoscopy within a year of their diagnosis and a next surveillance colonoscopy should be performed after an interval of 3 years, both these recommendations were of low evidence based on GRADE but were strong recommendations.[46] What is interesting in this guideline is that surveillance is halted after the second colonoscopy and thereafter the patient returns to the regular pool of screening. Furthermore, not only has the movement of guidelines for colorectal cancer screening been individualized based on a persons risk but more recently ASCO has issued guidelines looking into methods of screening to be offer to people based on the resources available to health-care providers.[47] Interestingly, important findings were detected in each round of surveillance colonoscopy and there were cases of adenocarcinoma detected in each of these rounds. This might be due to unmeasured confounders that might have led to adherence to surveillance colonoscopy recommendations or even the more frequent intense use of surveillance colonoscopy as shown by the repeated procedures in some patients before the recommended intervals by published guidelines. There is also the possibility of attrition bias due to the high proportion of patients who were not accounted.

We also lacked data on the residence of patients who were included in our study as both centers do not have a defined catchment area for the population they serve and, as such, might provide health care to patients presenting from remote areas. In a study, those with Stage I disease were more likely not to be adherent to surveillance (51.8%), as opposed to Stage II (18.0%) or Stage III (12.8%) (P < 0.01) as well as those who required to travel a distance of more than 40 miles (46.2%) as opposed to those less (18.7%) (P < 0.01).[48] These factors might have played a role in the adherence to surveillance colonoscopy, assuming that it was offered to them.

A cost-effective analysis that looked into the detection of metachronous colorectal cancer in the 1st year after resection found that 143 were needed to detect one colorectal cancer while 926 were needed to prevent one colorectal cancer-related death.[49] It also found the incremental cost-effectiveness ratio (ICER) of the early 1-year colonoscopy as compared to not performing it was $40,313 per life-year gained, but if the prevalence decreased from 0.7% to 0.19%, the ICER would be higher than $150,000/life-year gained.[49] Given the low age-adjusted incidence of colon cancer in Saudi Arabia compared to the world average, this might make a structured surveillance colonoscopy program challenging. This is even more true given the lack of a known willingness to pay threshold for life-years gained that is agreed on by health-care payers and regulators in the country.

Nonetheless, we believe that despite its limitations, this study provides an important milestone in the understanding the natural history and real-life practice in the management of patients with colon cancer in our community and we recommend that proper registries be created to capture patients' data and to inform policymakers and health-care providers with the aim of making informed decisions and recommendations that would improve important patient outcomes.

Conclusion

This study demonstrates that in a real world setting that the attrition rate and deviation from timing of surveillance colonoscopies is high. Also, the yield of surveillance colonoscopies for important findings is clinically relevant in the real world setting even with all the limitations which emphasis its importance.

Ethical approval

This study was approved by the institutional review board of both hospitals.

Financial support and sponsorship

The authors extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding of this research through the Research Group Project number RGP-279.

Conflicts of interest

There are no conflicts of interest.



 
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