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Prognostic Roles and Survival Benefits of Endoscopic Resection Versus Surgical Resection in the Management of Malignant Colon Polyps

Abstract

Background

Due to few sufficient data regarding the comparison between endoscopic and surgical resection of malignant colorectal polyps regarding outcomes and survival benefits, there are no clear guidelines of management strategies of malignant colorectal polyps.

The aims of the present study were to compare endoscopic resection alone and surgical resection in patients with malignant polyps in the colon (T1N0M0) readings advantages, disadvantages, recurrence risks, survival benefits, and long-term prognosis to detect how management strategy affects outcome.

Patients and methods

we included 350 patients. All included patients were divided into 2 groups; the first group included 100 patients who underwent only endoscopic polypectomy and the second group included 250 patients who underwent endoscopic polypectomy followed by definitive surgical resection after histopathological diagnosis.

We followed all patients for about 5 years, ranging from 18 to 55 months.

The primarily evaluated parameters are surgical consequences and patients' morbidity. The secondary evaluated parameters are recurrence risks, recurrence free survival, and overall survival rates.

Results

The age of patients who underwent polypectomy is usually younger than the surgical group, males have more liability to polypectomy in comparison with females.

Patients with tumors in the left colon have more liability to polypectomy in comparison with the right colon (p< 0.0001). Tumor factors associated with more liability to surgical resection are presence of lymphovascular invasion, high grade, and poor tumor differentiation (p< 0.0001).

The management strategy was the most significant predictor of overall and recurrence free survival rates in patients with malignant colon polyps (p< 0.001).

Conclusions

We found that survival benefits and lower incidence of recurrence are detected in the surgical resection group more than in the polypectomy group.

Keywords
malignant colon polyps; surgical resection; polypectomy; survival

Introduction

Colon cancer is still considered the third commonest cancer worldwide, but its fatality has declined. This was explained by many parameters, such as advancement in screening methods, which leads to early detection and removal of adenomatous polyps before progression to cancer.11 Mandic O, Jovanovic I, Cvetkovic M, et al. Factors Predicting Malignant Occurrence and Polyp Recurrence after the Endoscopic Resection of Large Colorectal Polyps: A Single Center Experience. Medicina (Kaunas) 2022;58(10):1440, 22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187

Malignant colorectal polyps which were appearing grossly as benign adenomatous polyp but microscopically contain a malignant focus which invades the muscularis mucosae and submucosa. These polyps correspond to 2 to 5% of all removed polyps.33 Zammit AP, Hooper JD, Brown I, Clark DA, Riddell AD. In comparison with polypectomy, colorectal resection is associated with improved survival for patients diagnosed with malignant polyps. Colorectal Dis 2022

Management of these polyps is still challenging, with two main scenarios of management: either follow-up after the initial endoscopic resection/polypectomy or performing surgical resection/colectomy. It was hypothesized that complete resection of these polyps until reaching a clear safety margin of ∼ 1 to 2 mm away from the excised edge, good or moderate differentiation of the cancer and absence of lymphovascular invasion, favor performing polypectomy alone, while presence of invaded margins, poorly differentiated carcinoma, presence of lymphovascular invasion, deep submucosal invasion or tumor budding favor performing colon resection.44 Quirke P, Risio M, Lambert R, von Karsa L, Vieth M. Quality assurance in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 2011;458 (01):1–19, 55 Williams JG, Pullan RD, Hill J, et al; Association of Coloproctology of Great Britain and Ireland. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013;15(Suppl 2):1–38

Although polypectomy has the risks of low morbidity, particularly in elderly patients who could not afford surgery, in comparison to surgical excision but has the risks of early recurrences due to incomplete removal, repeated costly manipulations, delay in radical management with risks of presence of nodal metastases even in T1 colon cancer that was reported in about 15% of cases.66 Komeda Y, Watanabe T, Sakurai T, et al. Risk factors for local recurrence and appropriate surveillance interval after endoscopic resection. World J Gastroenterol 2019;25(12):1502–1512

Due to few sufficient data regarding the comparison between endoscopic and surgical resection regarding outcomes and survival benefits, there are no clear guidelines of management strategies.77 Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD. Longterm recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population based study. Clin Gastroenterol Hepatol 2017;15(03):403–411.e1, 88 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659 Moreover, the results of performed studies are conflicting.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187, 99 Fischer J, Dobbs B, Dixon L, Eglinton TW, Wakeman CJ, Frizelle FANew Zealand Malignant Polyp Study (NZ MAPS) group. Management of malignant colorectal polyps in New Zealand. ANZ J Surg 2017;87(05):350–355

10 Levic K, Bulut O, Hansen TP, Gögenur I, Bisgaard T. Malignant colorectal polyps: endoscopic polypectomy and watchful waiting is not inferior to subsequent bowel resection. A nationwide propensity score-based analysis. Langenbecks Arch Surg 2019; 404(02):231–242
-1111 Senore C, Giovo I, Ribaldone DG, et al. Management of Pt1 tumours removed by endoscopy during colorectal cancer screening: Outcome and treatment quality indicators. Eur J Surg Oncol 2018;44(12):1873–1879

The aim of the present study was to compare between endoscopic resection alone and surgical resection in patients with malignant polyps in the colon (T1N0M0) readings advantages, disadvantages, recurrence risks, survival benefits and long-term prognosis to detect how management strategy affects outcome.

Patients and Methods

Inclusion Criteria

The present retrospective multicenter cohort study included all patients more than or equal to 18 years of age, with invasive adenocarcinoma discovered in colon polyps staged as T1N0M0 in the period between January 2015 and December 2020.

In General surgery Departments Faculty of Medicine Zagazig University Hospitals and Mansoura University Hospitals, Department of hepatogastroenterology and Infectious Diseases Faculty of Medicine, Alazhar University, Department of Hepatology and Gastroenterology, Theodor Bilharz, Research Institute, Department of Tropical Medicine, Faculty of Medicine, Zagazig University.

Exclusion Criteria

We excluded patients with incomplete data; patients with a positively invaded resection margin, patients with malignant rectal polyps due to different management options which is not just polypectomy or surgical resection.

After application of the inclusion criteria, we included 350 patients. All included patients were divided into 2 groups; the first group included 100 patients who underwent only endoscopic polypectomy and the second group included 250 patients who underwent endoscopic polypectomy followed by definitive surgical resection after histopathological diagnosis.

We followed all patients for about 5 years, ranging from 18 to 55 months.

Detailed histopathological data were assessed, such as; number of polyps, tumor size, tumor grade, pathological TNM stage, (pTNM), nodal status, AJCC Cancer Stage, presence of lymphovascular and perineural invasion.

Regarding site of the malignant polyps, we divided them in two main categories to facilitate statistical analysis and comparison: right colon if the malignant polyps were found in the cecum, the ascending colon, the hepatic flexure, and the transverse colon, and left colon if the malignant polyps were found in the splenic flexure, the descending, and the sigmoid colon).

Outcome Parameters

Primarily evaluated parameters are surgical consequences, patients' morbidity, hospital readmission within 30 days of discharge and 30- to 90-day mortality. Secondary evaluated parameters are recurrence risks, recurrence free survival, and overall survival rates.

Results

A total of 350 patients were included, 100 (28.6%) of them underwent only polypectomy and 250 (71.4%) of them underwent surgical resection (Figure 1).

Fig. 1
Endoscopic finding in colon cancer

Table 1 demonstrates detailed clinical, demographic, and tumor findings of all patients in association with management status.

Table 1
Comparison between the studied groups regarding baseline data

The patients who underwent polypectomy are usually younger than the surgical group, males have more liability to polypectomy in comparison with females.

There is a significant difference between groups regarding presence of comorbidity (p< 0.001), presence of lymphovascular invasion (p= 0.029), recurrence and low survival rates (p< 0.001). Both groups did not significantly differ regarding sex, histopathological subtypes, T stage, or grade (Table 1).

Patients with tumors in the left colon have more liability to polypectomy in comparison with the right colon (p< 0.0001). Tumor factors associated with more liability to surgical resection are presence of lymphovascular invasion, high grade, and poor tumor differentiation (p< 0.0001).

Regarding survival and follow-up findings; female gender, younger age, low grade tumor and absence of lymphovascular invasion were associated with improved survival. The primary tumor location was not associated with survival benefits.

Patients who underwent surgical resection have longer hospital stay time in comparison with polypectomy, have more liability to hospital readmission within 30 days, and high possibility of 30-day mortality, but there were no significant differences in 90-day mortality between both groups.

There is statistically a nonsignificant relation between overall survival and approach of colon resection, whether laparoscopic or open.

Overall and Recurrence free Survival Findings:

The management strategy was the most significant predictor of overall and recurrence free survival rates in patients with malignant colon polyps (p< 0.001) (Figure 2) (Tables 2-6).

Table 2
Comparison between the studied groups regarding different approaches of colon resection
Table 3
Correlation between OS rate and approach of colon resection
Table 4
Correlation between OS rate and type of primary operation
Table 5
Correlation between recurrence free survival and approach of colon resection
Table 6
Correlation between OS rate and type of primary operation
Fig. 2
Kaplan-Meier survival plot showing correlations between recurrence free survival rate (A) and overall survival rate (B) and type of primary operation

Absent lymphovascular invasion, conventional adenocarcinoma protect against recurrence after polypectomy, while increasing age, female sex, comorbidity, increase risk by 1.023, 1. 2.59 and 3.07 folds respectively.

T stages and grades higher indefinitely increase the risk of recurrence.

Discussion

In the present study, we showed that in patients diagnosed with malignant polyps in the colon who underwent surgical excision have more favorable RFS and OS rates and a lower incidence of recurrence than patients who underwent only polypectomy. This was similar to Lowe et al.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187

Moreover, we showed that factors that make performing polypectomy alone is more beneficial to the patients include; complete resection of the polyps until reaching free safety margins of ∼ 1 to 2 mm from the resected edge, low grade tumor (grade I and II), and absence of lymphovascular and perineural invasion, results similar to those of Quirke et al.,44 Quirke P, Risio M, Lambert R, von Karsa L, Vieth M. Quality assurance in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 2011;458 (01):1–19 and Williams et al.55 Williams JG, Pullan RD, Hill J, et al; Association of Coloproctology of Great Britain and Ireland. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013;15(Suppl 2):1–38

Lowe et al.,22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187 showed that these criteria of performing only polypectomy might be easily applied to pedunculated polyps with a stalk which could be easily resected en bloc, but might be difficult to be applied for sessile malignant polyps.

Absence of a stalk leads to a short access for malignant spread from the polyp surface to the depth of bowel wall thus leads to a higher rate of lympho-vascular invasion and metastases to regional lymph node.

In the present study, we showed that malignant proximal colon polyps are more sessile, less liable to be adequately excised, with inadequate assessment of resection margins, high rates of residual tumor, and high incidence of tumor recurrence and unfavorable survival rates. These results are similar to.55 Williams JG, Pullan RD, Hill J, et al; Association of Coloproctology of Great Britain and Ireland. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013;15(Suppl 2):1–38, 1212 Boenicke L, Fein M, Sailer M, Isbert C, Germer CT, Thalheimer A. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis 2010;25(04):433–438, 1313 Netzer P, Forster C, Biral R, et al. Risk factor assessment of endoscopically removed malignant colorectal polyps. Gut 1998; 43(05):669–674

Most of the polyps which are located in the left colon are diagnosed in old age patients, similar to what has been observed by Belderbos et al.,77 Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD. Longterm recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population based study. Clin Gastroenterol Hepatol 2017;15(03):403–411.e1, Cooper et al.,88 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659 and Wasif et al.1414 Wasif N, Etzioni D, Maggard MA, Tomlinson JS, Ko CY. Trends, patterns, and outcomes in the management of malignant colonic polyps in the general population of the United States. Cancer 2011;117(05):931–937

We performed surgical resection of polyps located in right colon than in left colon and this was similar to results of Lowe et al.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187

Our results were nearly similar to those of Cooper et al.,88 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659 who compared survival rates of patients with malignant colon polyps who underwent endoscopic resection and patients who underwent surgical excision and they found more favorable survival rates in the surgical excision group than in the polypectomy group.

Similar to our findings, Lowe et al.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187 showed that a larger number of patients underwent surgical excision in comparison with only polypectomy.

Previous data1515 National Comprehensive Cancer Network. Colon Cancer (Version 1. 2019https://www.nccn.org/professionals/physician_gls/pdf/ colon.pdf. Accessed March 19, 2019.
https://www.nccn.org/professionals/physi...
and Wasif et al.1414 Wasif N, Etzioni D, Maggard MA, Tomlinson JS, Ko CY. Trends, patterns, and outcomes in the management of malignant colonic polyps in the general population of the United States. Cancer 2011;117(05):931–937 showed increasing rates of surgical resection more than polypectomy alone.

Regarding patient demographic findings and histopathological tumor data, we showed similar results to previous studies.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187, 88 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659

Lowe et al.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187 and Nfonsam et al.1616 Nfonsam VN, Jecius H, Chen D, et al. Increasing incidence of colon cancer in the young: assessing the tumor biology. J Am Coll Surg 2019;229(01):79–90 included patients with a wide age distribution and 44% of their patients were < 65 years old, which was similar to our included patients that allow more accurate correlations. This adds an important aspect to our study especially given the rising incidence of colon cancer in those < 50 years old.

Moreover, we adequately assessed the presence of lymphovascular invasion and we demonstrated its association with a high incidence of lymph node metastasis and malignant recurrence in the polyp which necessitated surgical resection later on in addition to unfavorable survival in both groups of patients. Similar findings were stated by previous studies.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187, 44 Quirke P, Risio M, Lambert R, von Karsa L, Vieth M. Quality assurance in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 2011;458 (01):1–19, 55 Williams JG, Pullan RD, Hill J, et al; Association of Coloproctology of Great Britain and Ireland. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013;15(Suppl 2):1–38

We demonstrated a survival advantage for the group that underwent surgical resection more than for the group that underwent polypectomy, which was similar to results of previous studies in which the survival rates of their patients were better in the group that had surgical resection.22 Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187, 77 Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD. Longterm recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population based study. Clin Gastroenterol Hepatol 2017;15(03):403–411.e1

8 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659

9 Fischer J, Dobbs B, Dixon L, Eglinton TW, Wakeman CJ, Frizelle FANew Zealand Malignant Polyp Study (NZ MAPS) group. Management of malignant colorectal polyps in New Zealand. ANZ J Surg 2017;87(05):350–355
-1010 Levic K, Bulut O, Hansen TP, Gögenur I, Bisgaard T. Malignant colorectal polyps: endoscopic polypectomy and watchful waiting is not inferior to subsequent bowel resection. A nationwide propensity score-based analysis. Langenbecks Arch Surg 2019; 404(02):231–242

Our cohort of patients was younger and most of them were without significant comorbidity, thus has more liability to afford surgery more than old populations. A large percentage of our patients has their polyps located in right sided colon and has ales liability to be adequately excised by polypectomy alone. Our findings were similar to results of.88 Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659, 1313 Netzer P, Forster C, Biral R, et al. Risk factor assessment of endoscopically removed malignant colorectal polyps. Gut 1998; 43(05):669–674, 1414 Wasif N, Etzioni D, Maggard MA, Tomlinson JS, Ko CY. Trends, patterns, and outcomes in the management of malignant colonic polyps in the general population of the United States. Cancer 2011;117(05):931–937

Field effect or cancerization, which is defined as the liability of normally appearing mucosa which surrounds the malignancy to transform to metachronous cancer, was detected in colon cancer.1717 Park SK, Song CS, Yang HJ, et al. Field Cancerization in Sporadic Colon Cancer. Gut Liver 2016;10(05):773–78010.5009/gnl15334
https://doi.org/10.5009/gnl15334...
So, surgical resection of the colonic segment will lead to reduction of risks of occurrence of such malignancy, thus improving survival.

Although patients who underwent surgical resection had a longer duration of postoperative hospital stay, had more liability to readmission within 30 post-operative days with increased risks of 30-day mortality, but, improving surgical techniques and using minimally invasive laparoscopic assisted approaches leads to less post-operative morbidity, rabid recovery of bowel functions and short duration of post-operative hospital stay.1818 Koopmann MC, Heise CP. Laparoscopic and minimally invasive resection of malignant colorectal disease. Surg Clin North Am 2008;88(05):1047–1072, vii All these findings and data are in favor of surgical resection more than polypectomy.

Points of Strength of the Study

Our study is a prospective large cohort and multicenter study which allows the inclusion of a large number of patients with better comparison between both techniques with a high chance of reaching accurate results.

Limitations and Points of Weakness

We have no data about family history of colon cancer or past history of colon polyps to correlate surgical techniques and recurrence with genetic basis.

Conclusion

In our study, we included a large number of patients with malignant colon polyps (T1N0M0). When we compared between both surgical resection of the colon and polypectomy alone we found that survival benefits and lower incidence of recurrence are detected in the surgical resection group more than in the polypectomy group even after adjusting all pathological, clinical, and demographic findings. Although recent studies demonstrated that malignant polyps with good histopathological prognostic findings and free resected margins can be safely managed by only polypectomy, our data stated that polypectomy has no survival or recurrence advantages over surgical resection, so it will be of no benefit.

Recommendations

We recommend performing large studies including many patients with malignant colon polyps who underwent both surgical techniques considering the collection of genetic data and family history of colon cancer for better stratification of patients.

References

  • 1
    Mandic O, Jovanovic I, Cvetkovic M, et al. Factors Predicting Malignant Occurrence and Polyp Recurrence after the Endoscopic Resection of Large Colorectal Polyps: A Single Center Experience. Medicina (Kaunas) 2022;58(10):1440
  • 2
    Lowe D, Saleem S, Arif MO, Sinha S, Brooks G. Role of Endoscopic Resection Versus Surgical Resection in Management of Malignant Colon Polyps: a National Cancer Database Analysis. J Gastrointest Surg 2020;24(01):177–187
  • 3
    Zammit AP, Hooper JD, Brown I, Clark DA, Riddell AD. In comparison with polypectomy, colorectal resection is associated with improved survival for patients diagnosed with malignant polyps. Colorectal Dis 2022
  • 4
    Quirke P, Risio M, Lambert R, von Karsa L, Vieth M. Quality assurance in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 2011;458 (01):1–19
  • 5
    Williams JG, Pullan RD, Hill J, et al; Association of Coloproctology of Great Britain and Ireland. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013;15(Suppl 2):1–38
  • 6
    Komeda Y, Watanabe T, Sakurai T, et al. Risk factors for local recurrence and appropriate surveillance interval after endoscopic resection. World J Gastroenterol 2019;25(12):1502–1512
  • 7
    Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD. Longterm recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population based study. Clin Gastroenterol Hepatol 2017;15(03):403–411.e1
  • 8
    Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a populationbased analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118(03):651–659
  • 9
    Fischer J, Dobbs B, Dixon L, Eglinton TW, Wakeman CJ, Frizelle FANew Zealand Malignant Polyp Study (NZ MAPS) group. Management of malignant colorectal polyps in New Zealand. ANZ J Surg 2017;87(05):350–355
  • 10
    Levic K, Bulut O, Hansen TP, Gögenur I, Bisgaard T. Malignant colorectal polyps: endoscopic polypectomy and watchful waiting is not inferior to subsequent bowel resection. A nationwide propensity score-based analysis. Langenbecks Arch Surg 2019; 404(02):231–242
  • 11
    Senore C, Giovo I, Ribaldone DG, et al. Management of Pt1 tumours removed by endoscopy during colorectal cancer screening: Outcome and treatment quality indicators. Eur J Surg Oncol 2018;44(12):1873–1879
  • 12
    Boenicke L, Fein M, Sailer M, Isbert C, Germer CT, Thalheimer A. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis 2010;25(04):433–438
  • 13
    Netzer P, Forster C, Biral R, et al. Risk factor assessment of endoscopically removed malignant colorectal polyps. Gut 1998; 43(05):669–674
  • 14
    Wasif N, Etzioni D, Maggard MA, Tomlinson JS, Ko CY. Trends, patterns, and outcomes in the management of malignant colonic polyps in the general population of the United States. Cancer 2011;117(05):931–937
  • 15
    National Comprehensive Cancer Network. Colon Cancer (Version 1. 2019https://www.nccn.org/professionals/physician_gls/pdf/ colon.pdf Accessed March 19, 2019.
    » https://www.nccn.org/professionals/physician_gls/pdf/colon.pdf
  • 16
    Nfonsam VN, Jecius H, Chen D, et al. Increasing incidence of colon cancer in the young: assessing the tumor biology. J Am Coll Surg 2019;229(01):79–90
  • 17
    Park SK, Song CS, Yang HJ, et al. Field Cancerization in Sporadic Colon Cancer. Gut Liver 2016;10(05):773–78010.5009/gnl15334
    » https://doi.org/10.5009/gnl15334
  • 18
    Koopmann MC, Heise CP. Laparoscopic and minimally invasive resection of malignant colorectal disease. Surg Clin North Am 2008;88(05):1047–1072, vii

Publication Dates

  • Publication in this collection
    04 Aug 2023
  • Date of issue
    Apr-Jun 2023

History

  • Received
    16 Feb 2023
  • Accepted
    19 Apr 2023
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