Endoscopic mucosal resection for early colorectal neoplasia: Pathologic basis, procedures, and outcomes

Diseases of the Colon and Rectum

Volumn 52, Issue 8, 2009, Pages 1502-1515

  Repici, Alessandro ^a,d   Pellicano, Rinaldo ^b   Strangio, Giuseppe ^a   Danese, Silvio ^a   Fagoonee, Sharmila ^c   Malesci, Alberto ^d  

^a Istituto Ricovero Cura Carattere Scientifico Multimedica   (Italy)

^b MOLINETTE HOSPITAL   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Colonic polyps; Colorectal cancer; Colorectal neoplasia; Endoscopic mucosal resection

Indexed keywords

CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER SCREENING; CANCER STAGING; COLON POLYP; COLORECTAL CANCER; ENDOSCOPIC ECHOGRAPHY; ENDOSCOPIC MUCOSAL RESECTION; ENDOSCOPIC SUBMUCOSAL DISSECTION; HEALTH PROGRAM; HISTOPATHOLOGY; HUMAN; NONHUMAN; POLYPECTOMY; POSTOPERATIVE HEMORRHAGE; REVIEW; RISK ASSESSMENT; TREATMENT OUTCOME; COLONOSCOPY; COLORECTAL TUMOR; INTESTINE MUCOSA; METHODOLOGY; PATHOLOGY; TIME;

COLONOSCOPY; COLORECTAL NEOPLASMS; HUMANS; INTESTINAL MUCOSA; NEOPLASM STAGING; TIME FACTORS; TREATMENT OUTCOME;

EID: 68149163318     PISSN: 00123706     EISSN: 15300358     Source Type: Journal    
DOI: 10.1007/DCR.0b013e3181a74d9b     Document Type: Review

References (84)

1. Nicholson FB, Barro JL, Atkin W, et al. Review article: population screening for colorectal cancer. Aliment Pharmacol Ther 2005;22:1069-1077 (Pubitemid 41779514)
2. Hurlstone DP, Cross SS, Adam I, et al. A prospective clinicopathologic and endoscopic evaluation of flat and depressed colorectal lesions in the United Kingdom. Am J Gastroenterol 2003;98:2543-2549
3. Japanese Society for Cancer of the Colon and Rectum. Japanese classification of colorectal carcinoma. Tokyo: Kanehara & Co., Ltd., 1997.
4. Hamilton SR, Vogelstein B, Kudo S, Riboli E, Nakamura S. Tumors of the colon and rectum. In: Hamilton SR, Aaltonen LA, eds. WHO classification of tumors. Pathology and genetics of tumors of the digestive system. Lyon: International Agency for Research on Cancer, 2000:103-143
5. Koyama Y, Kotake K. Overview of colorectal cancer in Japan: report from the Registry of the Japanese Society for Cancer of the Colon and Rectum. Dis Colon Rectum 1997;40(Suppl 10): S2-9.
6. The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003;58(Suppl 6):S3-43.
7. Church J, Muto T, Appau K. Flat lesions of the colorectal mucosa: differences in recognition between Japanese and American endoscopists. Dis Colon Rectum 2004;47:1462-1466
8. Muto T, Kamiya J, Sawada T, et al. Small "flat adenoma" of the large bowel with special reference to its clinicopathologic features. Dis Colon Rectum 1985;28:847-851
9. Kudo S, Kashida H, Nakajima T, Tamura S, Nakayo K. Endoscopic diagnosis and treatment of early colorectal cancer. World J Surg 1997;21:694-701.
10. Ajioka Y, Watanabe H, Kazama S, et al. Early colorectal cancer with special reference to the superficial nonpolypoid type from a histopathologic point of view. World J Surg 2000;24:1075-1080
11. Kariya J, Mizuno K, Mayama M. A case of early colonic cancer type IIc associated with familial polyposis coli [in Japanese]. Stomach Intest 1977;12:1359-1364
12. Rembacken BJ, Fujii T, Cairns A, et al. Flat and depressed colonic neoplasms: a prospective study of 1000 colonoscopies in the UK. Lancet 2000;355:1211-1214
13. Sakamoto N, Terai T, Ohkusa T. Distribution comparison of depressed vs. non-depressed early colorectal cancers. Aliment Pharmacol Ther 2006;24(Suppl 4):227-232
14. Kudo S, Kashida H. Flat and depressed lesions of the colorectum. Clin Gastroenterol Hepatol 2005;3:S33-6.
15. Fujimori T, Satonaka K, Yamamura-Idei Y, Nagasako K, Maeda S. Non-involvement of ras mutations in flat colorectal adenomas and carcinomas. Int J Cancer 1994;57:51-55
16. Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993;25:455-461
17. Hurlstone DP, Sanders DS, Cross SS, et al. Colonoscopic resection of lateral spreading tumors: a prospective analysis of endoscopic mucosal resection. Gut 2004;53:1334-1339
18. Kudo S, Kashida H, Tamura T, et al. Colonoscopic diagnosis and management of nonpolypoid early colorectal cancer. World J Surg 2000;24:1081-1090
19. Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H, Kitano S. Risk factors for occult lymph node metastasis of colorectal cancer invading the submucosa and indications for endoscopic mucosal resection. Dis Colon Rectum 2007;50:1370-1376
20. Ueno H, Mochizuki H, Hashiguchi Y, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 2004;127:385-394
21. Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 1995;38:1286-1295
22. Saitoh Y, Obara T, Watari J, et al. Invasion depth diagnosis of depressed type early colorectal cancers by combined use of videoendoscopy and chromoendoscopy. Gastrointest Endosc 1998;48:362-370
23. Kudo S, Rubio CA, Teixeira CR, Kashida H, Kogure E. Pit pattern in colorectal neoplasia: endoscopic magnifying view. Endoscopy 2001;33:367-373
24. Kashida H, Kudo SE. Early colorectal cancer: concept, diagnosis, and management. Int J Clin Oncol 2006;11:1-8.
25. Kiesslich R, von Bergh M, Hahn M, Hermann G, Jung M. Chromoendoscopy with indigo carmine improves the detection of adenomatous and nonadenomatous lesions in the colon. Endoscopy 2001;33:1001-1006
26. Repici A, Pagano N. Endoscopic mucosal resection-endoscopic mucosal dissection: do we really need endoscopic ultrasonography assistance? Minerva Med 2007;98:417-421
27. Harada N, Hamada S, Kubo H, et al. Preoperative evaluation of submucosal invasive colorectal cancer using a 15-MHz ultrasound miniprobe. Endoscopy 2001;33:237-240
28. Hizawa K, Suekane H, Aoyagi K, Matsumoto T, Nakamura S, Fujishima M. Use of endosonographic evaluation of colorectal tumor depth in determining the appropriateness of endoscopic mucosal resection. Am J Gastroenterol 1996;91:768-771
29. Saitoh Y, Obara T, Einami K, et al. Efficacy of high-frequency ultrasound probes for the preoperative staging of invasion depth in flat and depressed colorectal tumors. Gastrointest Endosc 1996;44:34-39
30. Uno Y, Munakata A. The non-lifting sign of invasive colon cancer. Gastrointest Endosc 1994;40:485-489
31. Kobayashi N, Saito Y, Sano Y, et al. Determining the treatment strategy for colorectal neoplastic lesions: endoscopic assessment or the non-lifting sign for diagnosing invasion depth? Endoscopy 2007;39:701-705
32. Machida H, Sano Y, Hamamoto Y, et al. Narrow-band imaging in the diagnosis of colorectal mucosal lesions: a pilot study. Endoscopy 2004;36:1094-1098
33. Cho E, Uno K, Tanaka K, Yasuda K, Nakajima M. Clinical use-fulness of endoscopic optimal coherence tomography (EOCT) in the diagnosis of colorectal diseases: a comparative study with EUS using ultrasonic probe. Gastrointest Endosc 2003;57:T1461.
34. Hurlstone DP, Tiffin N, Brown SR, Barraza W, Thomson M, Cross SS. In vivo confocal laser scanning chromo-endomicroscopy of colorectal neoplasia: changing the technological paradigm. Histopathology 2008;52:417-426
35. Waye JD. Endoscopic mucosal resection of colon polyps. Gastrointest Clin N Am 2001;3:537-548
36. Deyle P, Largiader F, Jenny S, Fumagalli I. A method for endoscopic electroresection of sessile colonic polyps. Endoscopy 1973;5:38-40.
37. Sato T. A novel method of endoscopic mucosal resection assisted by submucosal injection of autologous blood (blood patch EMR). Dis Colon Rectum 2006;49:1636-1641
38. Van Gossum A, Cozzoli A, Adler M, Taton G, Cremer M. Colonoscopic snare polypectomy: analysis of 1485 resections comparing two types of current. Gastrointest Endosc 1992;38: 472-475
39. Inoue H, Takeshita K, Hori H, Muraoka Y, Yoneshima H, Endo M. Endoscopic mucosal resection with a cap-fitted panendoscope for esophagus, stomach, and colon mucosal lesions. Gastrointest Endosc 1993;39:58-62.
40. Inoue H, Kawano T, Tani M, Takeshita K, Iwai T. Endoscopic mucosal resection using a cap: techniques for use and preventing perforation. Can J Gastroenterol 1999;13:477-480
41. Soehendra N, Binmoeller KF, Bohnacker S, et al. Endoscopic snare mucosectomy in the esophagus without any additional equipment: a simple technique for resection of flat early cancer. Endoscopy 1997;29:380-383
42. Tada M, Inoue H, Yabata E, Okabe S, Endo M. Colonic mucosal resection using a transparent cap-fitted endoscope. Gastrointest Endosc 1996;44:63-65
43. Conio M, Repici A, Demarquay JF, Blanchi S, Dumas R, Filiberti R. EMR of large sessile colorectal polyps. Gastrointest Endosc 2004;60:234-241
44. Yoshikane H, Hidano H, Sakakibara A, Niwa Y, Goto H. Efficacy of a distal attachment in endoscopic resection of colorectal polyps situated behind semilunar folds. Endoscopy 2001;33:440-442
45. Sadahiro S, Ishida H, Tokunaga N, et al. Experimental assessment of endoscopic mucosectomy with a cap-fitted panendoscope. Endoscopy 1998;30:713-717
46. Brooker JC, Saunders BP, Suzuki N, Sibbons P. Twin-endoscope scissors resection (T-ESR): a new minimally invasive technique for performing colonic mucosectomy. Surg Endosc 2001;15: 1463-1466
47. Hosokawa K, Yoshida S. Recent advances in endoscopic mucosal resection for early gastric cancer. Gan To Kagaku Ryohio 1998;25:476-483
48. Ohkuwa M, Hosokawa N, Boku N, Ohtu H, Tajiri H, Yoshida S. New endoscopic treatment for intramucosal gastric tumors using an insulated-tip diathermic knife. Endoscopy 2001;33: 221-226
49. Yamamoto H. Endoscopic submucosal dissection of early cancers and large flat adenomas. Clin Gastroenterol Hepatol 2005; 3(7 Suppl 1):S74-6.
50. Lee SH, Cho WY, Kim HJ, et al. A new method of EMR: submucosal injection of a fibrinogen mixture. Gastrointest Endosc 2004;59:220-224
51. Gotoda T, Kondo H, Ono H, et al. A new endoscopic mucosal resection procedure using an insulation-tipped electrosurgical knife for rectal flat lesions. Report of two cases. Gastrointest Endosc 1999;50:560-563
52. Akahoshi K, Kubokawa M, Fujimaru T, et al. Endoscopic resection of a large pedunculated colonic polyp using an insulated-tip diathermy knife. Endoscopy 2005;37:405-406
53. Fujishiro M, Yahagi N, Nakamura M, et al. Endoscopic submucosal dissection for rectal epithelial neoplasia. Endoscopy 2006; 38:493-497 (Pubitemid 43744708)
54. Tanaka S, Oka S, Kaneko I, et al. Endoscopic submucosal dissection for colorectal neoplasia: possibility of standardization. Gastrointest Endosc 2007;66:100-107 (Pubitemid 46962498)
55. Kessler WR, Rex DK. Impact of bending section length on insertion and retroflexion properties of pediatric and adult colonoscopes. Am J Gastroenterol 2005;100:1290-1295
56. Matsui Y, Inomata M, Izumi K, et al. Hyaluronic acid stimulates tumor cell proliferation at wound sites. Gastrointest Endosc 2004;60:539-543
57. Fujishiro M, Yahagi N, Nakamura N, et al. Successful outcomes of a novel endoscopic treatment for GI tumors: endoscopic submucosal dissection with a mixture of high-molecular-weight hyaluronic acid, glycerin, and sugar. Gastrointest Endosc 2006;63: 243-249
58. Repici A, Conio M, De Angelis C, et al. Insulated-tip knife endoscopic mucosal resection of large colorectal polyps unsuitable for standard polypectomy. Am J Gastroenterol 2007;102: 1617-1623
59. Yamamoto S, Watanabe M, Hasegawa H, et al. The risk of lymph node metastasis in T1 colorectal carcinoma. Hepatogastroenterology 2004;51:998-1000.
60. Yokota T, Sugihara K, Yoshida S. Endoscopic mucosal resection for colorectal neoplastic lesions. Dis Colon Rectum 1994; 37:1108-1111
61. Bergmann U, Beger HG. Endoscopic mucosal resection for advanced non-polypoid colorectal adenoma and early stage carcinoma. Surg Endosc 2003;17:475-479
62. Bories E, Pesenti C, Monges G, et al. Endoscopic mucosal resection for advanced sessile adenoma and early-stage colorectal carcinoma. Endoscopy 2006;38:231-235
63. Iishi H, Tatsuta M, Iseki K, et al. Endoscopic piecemeal resection with submucosal saline injection of large sessile colorectal polyps. Gastrointest Endosc 2000;51:697-700.
64. Katsinelos P, Kountouras J, Paroutoglou G, Zavos C, Rizos C, Beltsis A. Endoscopic mucosal resection of large sessile colorectal polyps with submucosal injection of hypertonic 50 percent dextrose-epinephrine solution. Dis Colon Rectum 2006;49: 1384-1392
65. Su MY, Hsu CM, Ho YP, et al. Endoscopic mucosal resection for colonic non-polypoid neoplasms. AmJ Gastroenterol 2005;100: 2174-2179
66. Arebi N, Swain D, Suzuki N, Fraser C, Price A, Saunders BP. Endoscopic mucosal resection of 161 cases of large sessile or flat colorectal polyps. Scand J Gastroenterol 2007;42:859-866
67. Tamegai Y, Saito Y, Masaki N, et al. Endoscopic submucosal dissection: a safe technique for colorectal tumors. Endoscopy 2007;39:418-422
68. Walsh RM, Ackroyd FW, Shellito PC. Endoscopic resection of large sessile colorectal polyps. Gastrointest Endosc 1992;38: 303-309
69. Hurlstone DP, Sanders DS, Thomson M, Cross SS. "Salvage" endoscopic mucosal resection in the colon using a retroflexion gastroscope dissection technique: a prospective analysis. Endoscopy 2006;38:902-906
70. Yoshikane H, Hidano H, Sakakibara A, et al. Endoscopic resection of laterally spreading tumors of the large intestine using a distal attachment. Endoscopy 1999;31:426-430
71. Ahmad NA, Kochman ML, Long WB, et al. Efficacy, safety, and clinical outcomes of endoscopic mucosal resection: a study of 101 cases. Gastrointest Endosc 2001;55:390-396
72. Uraoka T, Saito Y, Matsuda T, et al. Endoscopic indications for endoscopic mucosal resection of laterally spreading tumors in the colorectum. Gut 2006;55:1592-1597
73. Mana F, De Vogelaere K, Urban D. Iatrogenic perforation of the colon during diagnostic colonoscopy: endoscopic treatment with clips. Gastrointest Endosc 2001;54:258-259
74. Matsuda T, Fujii T, Emura F, et al. Complete closure of large defect after EMR of a lateral spreading colorectal tumor when using a two-channel colonoscope. Gastrointest Endosc 2003;57: 836-838
75. Hurlstone DP, Lobo AJ. A new technique for endoscopic resection of large lateral spreading tumors of the colon: dual intubation colonoscopy with endoclip-assisted 'loop suturing' method. Am J Gastroenterol 2002;97:2931-2932
76. Kunihiro M, Tanaka S, Haruma K, et al. Electrocautery snare resection stimulates cellular proliferation of residual colorectal tumor: an increasing gene expression related to tumor growth. Dis Colon Rectum 2000;43:1107-1115
77. Bedogni G, Bertoni G, Ricci E, et al. Colonoscopic excision of large and giant colorectal polyps. Technical implication and result over eight years. Dis Colon Rectum 1986;29:831-835
78. Noshirwani KC, van Stolk RU, Rybicki LA, Beck GJ. Adenoma size and number are predictive of adenoma recurrence: implications for surveillance colonoscopy. Gastrointest Endosc 2000; 51:433-437
79. Brooker JC, Saunders BP, Shah SG, Thapar CJ, Suzuki N, Williams CB. Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations. Gastrointest Endosc 2002;55:371-375
80. Zlatanic J, Waye JD, Kirn PS, Baiocco PJ, Gleim GW. Large sessile colonic adenomas: use of argon plasma coagulator to supplement piecemeal snare polypectomy. Gastrointest Endosc 1999;49:731-735
81. Regula J, Wronska E, Polkowski M, et al. Argon plasma coagulation after piecemeal polypectomy of sessile colorectal adenomas: long-term follow-up study. Endoscopy 2003;35:212-218
82. Prohm P, Weber J, Bonner C. Laparoscopic-assisted colonoscopic polypectomy. Dis Colon Rectum 2001;44:746-748
83. Mal F, Perniceni T, Levard H, Boudet MJ, Levy P, Gayet B. Colonic polyps considered unresectable by endoscopy. Removal by combinations of laparoscopy and endoscopy in 65 patients. Gastroenterol Clin Biol 1998;22:425-430
84. Le Picard P, Vacher B, Pouliquen X. Laparoscopy-assisted colonic polypectomy or how to be helped by laparoscopy to prevent colectomy in benign polyps considered to be unresectable by colonoscopy. Ann Chir 1997;51:986-989