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MACROSCOPIC AND HISTOLOGICAL ANALYSIS ON ENDOSCOPICALLY RESECTED RECTAL LESIONS

ANÁLISE MACROSCÓPICA E HISTOLÓGICA DE LESÕES RETAIS ENDOSCOPICAMENTE RESSECADAS

ABSTRACT

BACKGROUND:

Colorectal cancer is among the most common malignancies worldwide. Colonoscopy is the examination of choice for the prevention of CRC because of its great diagnostic and, especially, therapeutic capacity in relation to adenomatous lesions.

AIMS:

This study aimed to analyze the prevalence, macroscopic, and histological characteristics of polypoid rectal lesions resected through endoscopic techniques and assess whether endoscopic therapy is safe and efficient for treating lesions located in the rectum.

METHODS:

This is a retrospective observational study with an analysis of the medical records of all patients undergoing resection of rectal polyps.

RESULTS:

A total of 123 patients with rectal lesions were evaluated, with 59 men and 64 women of mean age 56 years. All patients underwent endoscopic resection: 70% with polypectomy and 30% with wide mucosectomy. Complete colonoscopy with removal of the entire rectal lesion occurred in 91%, while in 5% the preparation was inadequate and poor clinical conditions were an impeditive factor, and in 4% surgical treatment was indicated because there was an infiltrative lesion with central ulceration. Histological evaluation showed adenomas in 3.25%, hyperplasia in 7.32%, and hamartoma in 0.81%; low-grade dysplasia was identified in 34.96%, high-grade dysplasia in 51.22%, and adenocarcinoma in 1.63%, while one case (0.81%) was classified as erosion.

CONCLUSIONS:

Polyps in the rectum are common and were found in 37% of these colonoscopies. Adenomas with dysplasia were the most common form of Colorectal cancer . Therapeutic colonoscopy proved to be a safe and efficient method for the complete treatment of rectal lesions.

HEADINGS:
Colorectal neoplasms; Adenoma; Endoscopic mucosal resection

RESUMO

RACIONAL:

O câncer colorretal (CCR) está entre as neoplasias mais comuns em todo o mundo. A colonoscopia é o exame de escolha para prevenção por sua grande capacidade diagnóstica e, principalmente, terapêutica em relação às lesões adenomatosas.

OBJETIVOS:

Analisar a prevalência, as características macroscópicas e histológicas das lesões polipoides retais ressecadas por técnicas endoscópicas e avaliar se a terapia endoscópica é segura e eficaz para o tratamento de lesões localizadas no reto.

MÉTODOS:

Estudo observacional retrospectivo com análise dos prontuários de todos os pacientes submetidos à ressecção de pólipos retais.

RESULTADOS:

Foram avaliados 123 pacientes com lesões retais: 59 homens e 64 mulheres com idade média de 56 anos. Todos os pacientes foram submetidos à ressecção endoscópica: 70% com polipectomia e 30% com mucosectomia ampla. A colonoscopia completa com retirada de toda a lesão retal ocorreu em 91%, enquanto em 5% o preparo foi inadequado e as más condições clínicas foram fator impeditivo, e em 4% o tratamento cirúrgico foi indicado por haver lesão infiltrativa com ulceração central. A avaliação histológica mostrou adenomas em 3,25%, hiperplasia em 7,32% e hamartoma em 0,81%; displasia de baixo grau foi identificada em 34,96%, displasia de alto grau em 51,22% e adenocarcinoma em 1,63%, enquanto um caso (0,81%) foi classificado como erosão.

CONCLUSÕES:

Pólipos no reto são comuns e foram encontrados em 37% das colonoscopias. Adenomas com displasia foram a forma mais comum de câncer colorretal. A colonoscopia terapêutica mostrou-se método seguro e eficiente para o tratamento completo das lesões retais.

DESCRITORES:
Neoplasias colorretais; Adenoma; Ressecção endoscópica de mucosa

INTRODUCTION

Colorectal cancer (CRC) is the third leading cause of death in the United States. In Brazil, according to the annual report available on the website of the National Cancer Institute1515 Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17-48. https://doi.org/10.3322/caac.21763
https://doi.org/10.3322/caac.21763...
, it is the second in incidence and the third in mortality, in both men and women. Its incidence has increased over the last 15 years worldwide. It is believed that diets rich in animal fat and increased consumption of processed and manufactured foods, together with low fiber intake and sedentary lifestyles, have contributed to this increase33 Bielemann RM, Motta JV, Minten GC, Horta BL, Gigante DP. Consumption of ultra-processed foods and their impact on the diet of young adults. Rev Saúde Pública. 2015;49:28. https://doi.org/10.1590/s0034-8910.2015049005572
https://doi.org/10.1590/s0034-8910.20150...
.

Colonoscopy is certainly the most effective preventive method for directly combating preneoplastic lesions, that is, polyps of the colon and rectum1313 Risso MFA, Costa LCDS, Tercioti V Jr, Ferrer JAP, Lopes LR, Andreollo NA. The esophageal, gastric, and colorectal tumors and the esophagogastroduodenoscopies and colonoscopies by the Brazilian Unified Health system: what is the importance? Arq Bras Cir Dig. 2022;35:e1661. https://doi.org/10.1590/0102-672020210002e1661
https://doi.org/10.1590/0102-67202021000...
. The advent of image magnification and chromoscopy and the evolution of materials for endoscopic resections, along with improved training for endoscopists, have been contributing to prevention22 Averbach M, Zanoni ECA, Corrêa PAFP, Rossini G, Paccos JL, Alencar ML, et al. High resolution chromoendoscopy in the differential diagnosis of neoplastic and non-neoplastic polyps. Arq Gastroenterol. 2003;40(2):99-103. https://doi.org/10.1590/S0004-28032003000200007
https://doi.org/10.1590/S0004-2803200300...
.

Consequent to the implementation of the American Cancer Society Guidelines, which have made it routine to undergo preventive colonoscopy from the age of 50 years onward and among the direct relatives of patients with a history of CRC from the age of 40 years onward, it is believed that the incidence of this form of cancer should fall over the next few years1313 Risso MFA, Costa LCDS, Tercioti V Jr, Ferrer JAP, Lopes LR, Andreollo NA. The esophageal, gastric, and colorectal tumors and the esophagogastroduodenoscopies and colonoscopies by the Brazilian Unified Health system: what is the importance? Arq Bras Cir Dig. 2022;35:e1661. https://doi.org/10.1590/0102-672020210002e1661
https://doi.org/10.1590/0102-67202021000...
,1616 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):250-81. https://doi.org/10.3322/caac.21457
https://doi.org/10.3322/caac.21457...
.

Rectal cancer presents characteristics that differ slightly from cancer of the rest of the colon, due to its more aggressive anatomopathological peculiarities, which are associated with higher morbidity and mortality for this type of lesion66 Facciorusso A, Antonino M, Di Maso M, Barone M, Muscatiello N. Non-polypoid colorectal neoplasms: Classification, therapy and follow-up. World J Gastroenterol. 2015;21(17):5149-57. https://doi.org/10.3748/wjg.v21.i17.5149
https://doi.org/10.3748/wjg.v21.i17.5149...
.

Thus, the relevance of our current project comes from its analysis of the prevalence, size, and distribution of rectal lesions resected through endoscopy, with anatomopathological analysis, to ascertain the efficacy and safety of the treatment of the cases selected.

The aim of this study was to analyze the prevalence, size, age distribution, and anatomopathological distribution of rectal lesions resected through endoscopy and ascertain whether this method was safe and effective as a treatment for the cases selected.

METHODS

This was a retrospective, observational, and cross-sectional study in which the aim was to assess rectal lesions that underwent endoscopic resection (polypectomy and mucosectomy), at the Endoscopy Service of Hospital 9 de Julho in São Paulo, Brazil. This study was approved by the Research Ethics Committee of the Mackenzie Presbyterian Institute and registered on the Brazil Platform (n° CAAE 23424719.8.0000.0103).

Out of a total of 3,790 colonoscopies, 123 cases of rectal lesions resected through endoscopy were selected in accordance with the inclusion and exclusion criteria of the current research project. In cases of suspected lesions, the routine preparation consisted of washing with physiological serum solution followed by chromoscopy using 0.4% indigo carmine, in order to study the surface of the lesion and more accurately delimit its margins1212 Rex DK, Ahnen DJ, Baron JA, Batts KP, Burke CA, Burt RW, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012;107(9):1315-29. https://doi.org/10.1038/ajg.2012.161
https://doi.org/10.1038/ajg.2012.161...
.

The inclusion criteria were that the rectal lesions should be greater than or equal to 10 mm in diameter, without endoscopic signs suggestive of submucosal infiltration, which were resected by means of endoscopy (polypectomy or mucosectomy). The exclusion criteria were situations of rectal lesions smaller than 10 mm in diameter, or lesions larger than 10 mm with endoscopic signs suggestive of submucosal infiltration or that did not rise after injection of saline solution into the submucosa to attempt mucosectomy. Such cases were referred for a more individualized investigation and appropriate treatment. Advanced tumors and other inflammatory lesions of the rectum were also excluded.

Procedures

A Pentax EPKi endoscope with image magnification accessories and digital chromoscopy (i-Scan) was used. Indigo carmine was used to stain the lesions. Physiological solution and, if necessary, adrenaline 1-10000u were used for infiltration of the submucosa, in order to elevate the lesions and enable complete resection or resection in pieces (master pieces) using a conventional polypectomy loop. Te lesions were classified macroscopically in accordance with the Paris classification system99 Kudo Se, Lambert R, Allen JI, Fujii H, Fujii T, Kashida H, et al. Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc. 2008;68(Suppl 4):S3-47. https://doi.org/10.1016/j.gie.2008.07.052
https://doi.org/10.1016/j.gie.2008.07.05...
and anatomopathologically in accordance with the Vienna classification system55 Dixon MF. Gastrointestinal epithelial neoplasia: Vienna revisited. Gut. 2002;51(1):130-1. https://doi.org/10.1136/gut.51.1.130
https://doi.org/10.1136/gut.51.1.130...
,1414 Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47(2):251-5. https://doi.org/10.1136/gut.47.2.251
https://doi.org/10.1136/gut.47.2.251...
.

Statistical analysis

The data from the patients and their polyps were compiled in Excel and shared in the Epi Info software for analysis of the variables presented in the results.

RESULTS

A total of 123 cases of rectal lesions greater than or equal to 10 mm in diameter were collected and analyzed. There were slightly more cases among women (52.03%) than among men (47.97%) over the period studied. However, this difference in proportions was only a numerical difference of five cases (i.e., men accounted for only five cases fewer).

Regarding age groups, the patients were categorized into six groups, as follows: group 1: 30–40 years; group 2: 41–50 years; group 3: 51–60 years; group 4: 61–70 years; group 5: 71–80 years; and group 6: 81 years or older.

Table 1 presents the analysis on the rectal lesions greater than or equal to 10 mm in diameter that were resected by means of endoscopy, according to age group.

Table 1
Distribution according to age group.

Although the guidelines (clinical protocol) recommend that preventive action through colonoscopy should only start to be implemented above the age of 50 years, it should be noted that the present study revealed that 25% of the cases occurred at less than 50 years of age, which was a proportion similar to that of the group aged 61-70 years.

Regarding the data on lesion size that were collected, the patients were categorized into six groups as follows: group 1: 10 mm; group 2: 11–20 mm; group 3: 21–30 mm; group 4: 31–40 mm; group 5: 41–50 mm; and group 6: 51 mm (Table 2).

Table 2
Lesion size.

Overall, regarding lesion sizes, lesions of sizes 10–30 mm were present in much higher quantities (84.55% of the total), and the highest proportion was the size range 11–20 mm (38.21%) (Figure 1).

Figure 1
Lesion sizes.

The lesions were endoscopically classified using the Paris classification system66 Facciorusso A, Antonino M, Di Maso M, Barone M, Muscatiello N. Non-polypoid colorectal neoplasms: Classification, therapy and follow-up. World J Gastroenterol. 2015;21(17):5149-57. https://doi.org/10.3748/wjg.v21.i17.5149
https://doi.org/10.3748/wjg.v21.i17.5149...
(Table 3).

Table 3
Type of lesion according to the Paris classification system6.

We considered lesions of types 0-LST and 0-IIa (of the Paris classification66 Facciorusso A, Antonino M, Di Maso M, Barone M, Muscatiello N. Non-polypoid colorectal neoplasms: Classification, therapy and follow-up. World J Gastroenterol. 2015;21(17):5149-57. https://doi.org/10.3748/wjg.v21.i17.5149
https://doi.org/10.3748/wjg.v21.i17.5149...
) together as superficially elevated lesions. Their surfaces were classified as granular when they presented mucosal granulation of up to 6 mm in diameter; nodular or mixed when one or more nodules of more than 6 mm in diameter were present; or smooth when the surfaces were smooth.

With the evolution of concepts and with technological improvements, endoscopists have begun to diagnose more and more nonpolypoid or superficial lesions (superficially elevated, flat, or depressed) and lesions or tumors with spreading or lateral growth (laterally spreading tumors [LST]). These tend to grow laterally in relation to the surface of the colon or rectum, and by definition have a diameter greater than 10 mm99 Kudo Se, Lambert R, Allen JI, Fujii H, Fujii T, Kashida H, et al. Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc. 2008;68(Suppl 4):S3-47. https://doi.org/10.1016/j.gie.2008.07.052
https://doi.org/10.1016/j.gie.2008.07.05...
,1010 Lambert R, Tanaka S. Laterally spreading tumors in the colon and rectum. Eur J Gastroenterol Hepatol. 2012;24(10):1123-34. https://doi.org/10.1097/MEG.0b013e328355e2d9
https://doi.org/10.1097/MEG.0b013e328355...
. In the present study, the prevalence of LST was 24.64%. These lesions invade the submucosa and therefore already present neoplastic cells; hence, they can no longer be treated endoscopically (Figures 2 and 3).

Figure 2
Rectal laterally spreading tumor (chromoscopy, Parada et al.1111 Parada AA, Venco FE, Varca-Neto MR, El Ibrahim R, Poletti PB, Brito HP, et al. Which lesions are at higher risk of developing colorectal carcinomas: superficially elevated serrated lesions or depressed lesions? Arq Bras Cir Dig. 2023;35:e1716. https://doi.org/10.1590/0102-672020220002e1716
https://doi.org/10.1590/0102-67202022000...
).
Figure 3
(A) Mucosectomy using rectal laterally spreading tumor loop. (B) Mucosa with margin.

According to the Vienna classification system55 Dixon MF. Gastrointestinal epithelial neoplasia: Vienna revisited. Gut. 2002;51(1):130-1. https://doi.org/10.1136/gut.51.1.130
https://doi.org/10.1136/gut.51.1.130...
,1414 Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47(2):251-5. https://doi.org/10.1136/gut.47.2.251
https://doi.org/10.1136/gut.47.2.251...
(Table 4), these lesions are histopathologically classified into the following five types:

Table 4
Anatomopathological categories according to the Vienna classification system5,14.
  1. negative for dysplasia/neoplasia (includes reactive lesions);

  2. undefined regarding dysplasia/neoplasia;

  3. noninvasive low-grade intraepithelial neoplasia (LG-IEN), equivalent to low-grade dysplasia and corresponding to mild and moderate dysplasia in the three-grade system, that is, low-grade adenoma/dysplasia;

  4. noninvasive high-grade intraepithelial neoplasia (HG-IEN), equivalent to high-grade dysplasia: adenoma with high-grade dysplasia or intense dysplasia in the three-grade system, noninvasive in situ carcinoma, and intramucosal carcinoma invading the lamina propria; and

  5. invasive neoplasia, which invades as far as the submucosa or even more deeply55 Dixon MF. Gastrointestinal epithelial neoplasia: Vienna revisited. Gut. 2002;51(1):130-1. https://doi.org/10.1136/gut.51.1.130
    https://doi.org/10.1136/gut.51.1.130...
    ,1414 Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47(2):251-5. https://doi.org/10.1136/gut.47.2.251
    https://doi.org/10.1136/gut.47.2.251...
    .

The HG-IEN was found in 51.22% of the cases, and four with adenocarcinoma were referred for complementary treatment (Figure 3).

From the point of view of treatment, patients whose lesions were limited to the mucosa can be considered to have been cured, strictly speaking. The risk of lymph node metastases increases with the depth of invasion of the submucosa99 Kudo Se, Lambert R, Allen JI, Fujii H, Fujii T, Kashida H, et al. Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc. 2008;68(Suppl 4):S3-47. https://doi.org/10.1016/j.gie.2008.07.052
https://doi.org/10.1016/j.gie.2008.07.05...
,88 Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol. 2004;39(6):534-43. https://doi.org/10.1007/s00535-004-1339-4
https://doi.org/10.1007/s00535-004-1339-...
.

DISCUSSION

Colonoscopy has been shown to be a very safe and effective method for diagnosing rectal lesions, as well as for implementing definitive treatment for the vast majority of lesions. It can be used for performing polypectomy and mucosectomy safely, with high technical quality1313 Risso MFA, Costa LCDS, Tercioti V Jr, Ferrer JAP, Lopes LR, Andreollo NA. The esophageal, gastric, and colorectal tumors and the esophagogastroduodenoscopies and colonoscopies by the Brazilian Unified Health system: what is the importance? Arq Bras Cir Dig. 2022;35:e1661. https://doi.org/10.1590/0102-672020210002e1661
https://doi.org/10.1590/0102-67202021000...
.

The present study demonstrated the aggressiveness of polypoid lesions of the rectum, with special attention to LST lesions, which are more likely to be more aggressive. LST lesions are typically larger than 10 mm in diameter.

Among the 123 patients analyzed, despite the fact that colonoscopy is a very safe and effective method, the characteristic that drew our attention most was their age. 25% of these patients studied were between 30 and 50 years of age and had been asymptomatic. Therefore, endoscopic evaluation for these patients would not be prescribed, according to current guidelines. However, it is still worth mentioning that 50% of this sample was 50–70 years of age. Regarding the size of the lesions, we took into consideration lesions that were at least 10 mm in diameter. This minimum diameter accounted for 37.4% of the sample. Lesions larger than 51 mm accounted for 4.07%. The mean size was 11–20 mm (38.21%). These findings are in agreement with those found in other similar studies, such as that of Heo et al.77 Heo J, Jeon SW, Jung MK, Kim SK, Kim J, Kim S. Endoscopic resection as the first-line treatment for early colorectal cancer: comparison with surgery. Surg Endosc. 2014;28(12):3435-42. https://doi.org/10.1007/s00464-014-3618-3
https://doi.org/10.1007/s00464-014-3618-...
, in which the mean size was 19.8±12.1 mm.

Intraepithelial neoplasia is a denomination introduced through the Vienna consensus of 2002 to replace the terms adenoma and dysplasia. It is subdivided into high and low grades. According to the WHO, in situ and intramucosal carcinoma should be classified as dysplasia or HG-IEN, because the repercussions of the lesions are exactly the same, that is, none of them have the potential to send metastases to other organs and lymph nodes12.

The precursor lesions include superficially elevated, flat, depressed, excavated, and lateral-growth lesions44 Diger NR, Kubrusly LF, Nassif PAN, Parada AA, Bolsi GT, Teixeira HCB, et al. Is superficial colorectal lesions with low and high grades intraepithelial neoplasms more prevalent in older above 65 years? Arq Bras Cir Dig. 2019;32(4):e1478. https://doi.org/10.1590/0102-672020190001e1478
https://doi.org/10.1590/0102-67202019000...
. In the literature, it is stated that flat lesions have a higher chance of progression to HG-IEN, predominantly in the right colon and usually with a thickness of less than 1 cm. These present higher risk of infiltrative growth than sessile adenomas of the same size, especially in depressed lesions11 Assis RVB. Tracking and surveillance of colorectal: guidelines world. GED Gastroenterol Endosc Dig. 2011;30(2):62-74..

In a study by Diger et al.44 Diger NR, Kubrusly LF, Nassif PAN, Parada AA, Bolsi GT, Teixeira HCB, et al. Is superficial colorectal lesions with low and high grades intraepithelial neoplasms more prevalent in older above 65 years? Arq Bras Cir Dig. 2019;32(4):e1478. https://doi.org/10.1590/0102-672020190001e1478
https://doi.org/10.1590/0102-67202019000...
, out of the 200 patients evaluated, 21% of the colonic lesions and 56% of the rectal lesions were of high grade, compared with 51.22% of the rectal lesions that were of high grade in the present study. Among our patients who were identified as having HG-IEN, adenocarcinoma was found in 4 (3.25%). These patients were referred for further treatment. This number is slightly lower than that found in a study by Heo et al.77 Heo J, Jeon SW, Jung MK, Kim SK, Kim J, Kim S. Endoscopic resection as the first-line treatment for early colorectal cancer: comparison with surgery. Surg Endosc. 2014;28(12):3435-42. https://doi.org/10.1007/s00464-014-3618-3
https://doi.org/10.1007/s00464-014-3618-...
, in which 8.9% of the patients required additional treatment after endoscopic treatment.

In general, the results from studying these 123 patients were quite balanced in relation to the worldwide literature. Reiterating, there were no significant differences between the sexes, and the main point that needs to be highlighted is the issue that 25% of the cases were less than 50 years of age.

As demonstrated, among the 63 patients who benefited from endoscopic resection, 51.22% had HG-IEN, and 4 of them already had adenocarcinoma and were referred for complementary treatment. It is thus evident that colonoscopy is a method that should be increasingly used and, if possible, earlier.

CONCLUSION

Colonoscopy, used in association with endoscopic mucosectomy, is a safe and very effective practice for diagnosing, treating, and following up rectal lesions.

  • Financial source: This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) (Code 001).
  • Editorial Support: National Council for Scientific and Technological Development (CNPq).
  • Central Message
    Colonoscopy is certainly the most effective preventive method for directly combating preneoplastic lesions, that is, polyps of the colon and rectum. The advent of image magnification and chromoscopy and the evolution of materials for endoscopic resections, along with improved training for endoscopists, have been contributing to prevention. Rectal cancer presents characteristics that differ slightly from cancer of the rest of the colon, due to its more aggressive anatomopathological peculiarities, which are associated with higher morbidity and mortality for this type of lesion.
  • Perspectives
    Polyps in the rectum are common and were found in 37% of these colonoscopies. Adenomas with dysplasia were the most common form of colorectal cancer. Therapeutic colonoscopy has proven to be a safe and efficient method for complete treatment of rectal lesions.

REFERENCES

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    Bielemann RM, Motta JV, Minten GC, Horta BL, Gigante DP. Consumption of ultra-processed foods and their impact on the diet of young adults. Rev Saúde Pública. 2015;49:28. https://doi.org/10.1590/s0034-8910.2015049005572
    » https://doi.org/10.1590/s0034-8910.2015049005572
  • 4
    Diger NR, Kubrusly LF, Nassif PAN, Parada AA, Bolsi GT, Teixeira HCB, et al. Is superficial colorectal lesions with low and high grades intraepithelial neoplasms more prevalent in older above 65 years? Arq Bras Cir Dig. 2019;32(4):e1478. https://doi.org/10.1590/0102-672020190001e1478
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    Facciorusso A, Antonino M, Di Maso M, Barone M, Muscatiello N. Non-polypoid colorectal neoplasms: Classification, therapy and follow-up. World J Gastroenterol. 2015;21(17):5149-57. https://doi.org/10.3748/wjg.v21.i17.5149
    » https://doi.org/10.3748/wjg.v21.i17.5149
  • 7
    Heo J, Jeon SW, Jung MK, Kim SK, Kim J, Kim S. Endoscopic resection as the first-line treatment for early colorectal cancer: comparison with surgery. Surg Endosc. 2014;28(12):3435-42. https://doi.org/10.1007/s00464-014-3618-3
    » https://doi.org/10.1007/s00464-014-3618-3
  • 8
    Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol. 2004;39(6):534-43. https://doi.org/10.1007/s00535-004-1339-4
    » https://doi.org/10.1007/s00535-004-1339-4
  • 9
    Kudo Se, Lambert R, Allen JI, Fujii H, Fujii T, Kashida H, et al. Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc. 2008;68(Suppl 4):S3-47. https://doi.org/10.1016/j.gie.2008.07.052
    » https://doi.org/10.1016/j.gie.2008.07.052
  • 10
    Lambert R, Tanaka S. Laterally spreading tumors in the colon and rectum. Eur J Gastroenterol Hepatol. 2012;24(10):1123-34. https://doi.org/10.1097/MEG.0b013e328355e2d9
    » https://doi.org/10.1097/MEG.0b013e328355e2d9
  • 11
    Parada AA, Venco FE, Varca-Neto MR, El Ibrahim R, Poletti PB, Brito HP, et al. Which lesions are at higher risk of developing colorectal carcinomas: superficially elevated serrated lesions or depressed lesions? Arq Bras Cir Dig. 2023;35:e1716. https://doi.org/10.1590/0102-672020220002e1716
    » https://doi.org/10.1590/0102-672020220002e1716
  • 12
    Rex DK, Ahnen DJ, Baron JA, Batts KP, Burke CA, Burt RW, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012;107(9):1315-29. https://doi.org/10.1038/ajg.2012.161
    » https://doi.org/10.1038/ajg.2012.161
  • 13
    Risso MFA, Costa LCDS, Tercioti V Jr, Ferrer JAP, Lopes LR, Andreollo NA. The esophageal, gastric, and colorectal tumors and the esophagogastroduodenoscopies and colonoscopies by the Brazilian Unified Health system: what is the importance? Arq Bras Cir Dig. 2022;35:e1661. https://doi.org/10.1590/0102-672020210002e1661
    » https://doi.org/10.1590/0102-672020210002e1661
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Publication Dates

  • Publication in this collection
    30 June 2023
  • Date of issue
    2023

History

  • Received
    13 Sept 2022
  • Accepted
    20 Dec 2022
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