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Endoscopy 2013; 45(10): 827-841
DOI: 10.1055/s-0033-1344238
Original article
© Georg Thieme Verlag KG Stuttgart · New York

Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions

Steven L. Bosch
1   Department of Pathology, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands,
,
Steven Teerenstra
2   Department of Epidemiology, Biostatistics and HTA, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands,
,
Johannes H. W. de Wilt
3   Department of Surgery, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands
,
Chris Cunningham
4   Department of Colorectal Surgery, Churchill Hospital, Oxford University Hospitals, Oxford, United Kingdom
,
Iris D. Nagtegaal
1   Department of Pathology, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands,
› Institutsangaben
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Publikationsverlauf

submitted 10. Oktober 2012

accepted after revision 03. Mai 2013

Publikationsdatum:
24. Juli 2013 (online)

Auch verfügbar auf
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Background and study aim: Population screening for colorectal cancer (CRC) is expected to increase the number of pT1 CRCs. Local excision is an attractive treatment option, but is only oncologically safe in the absence of lymph node metastasis (LNM). A systematic review of the predictive value of pathological risk factors for LNM in pT1 CRC was conducted to provide data for an evidence-based decision regarding follow-up or radical surgery after local excision.

Methods: PubMed was searched for reports on predictors of LNM in pT1 CRC. Published papers written in English and containing at least 50 patients were included. Meta-analyses were performed using Review Manager 5.1.

Results: A total of 17 studies were included involving a total of 3621 patients with available nodal status. The strongest independent predictors of LNM were lymphatic invasion (relative risk [RR] 5.2, 95 % confidence interval [CI] 4.0 – 6.8), submucosal invasion ≥ 1 mm (RR 5.2, 95 %CI 1.8 – 15.4), budding (RR 5.1, 95 %CI 3.6 – 7.3), and poor histological differentiation (RR 4.8, 95 %CI 3.3 – 6.9). Limitations of the study were: results could not be stratified according to location in the colon or rectum; very early tumors removed by polypectomy without surgical resection were not included in the meta-analysis; and included studies were primarily from Asian countries and results therefore need to be verified in Western populations.

Conclusion: The absence of lymphatic invasion, budding, submucosal invasion ≥ 1 mm, and poor histological differentiation were each associated with low risk of LNM. Risk stratification models integrating these factors need to be investigated further.

Figure e2 – e8, Table e5

 

  • References

  • 1 Hardcastle JD, Chamberlain JO, Robinson MH et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996; 348: 1472-1477
    CrossrefPubMedGoogle Scholar
  • 2 Kewenter J, Brevinge H, Engaras B et al. Results of screening, rescreening, and follow-up in a prospective randomized study for detection of colorectal cancer by fecal occult blood testing. Results for 68,308 subjects. Scand J Gastroenterol 1994; 29: 468-473
    CrossrefPubMedGoogle Scholar
  • 3 Kronborg O, Fenger C, Olsen J et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 1996; 348: 1467-1471
    CrossrefPubMedGoogle Scholar
  • 4 Mandel JS, Bond JH, Church TR et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 1993; 328: 1365-1371
    CrossrefPubMedGoogle Scholar
  • 5 Paimela H, Malila N, Palva T et al. Early detection of colorectal cancer with faecal occult blood test screening. Br J Surg 2010; 97: 1567-1571
    CrossrefPubMedGoogle Scholar
  • 6 Smart CR. Screening and early diagnosis. Cancer 1992; 70: 1246-1251
    CrossrefPubMedGoogle Scholar
  • 7 Takeuchi Y, Uedo N, Ishihara R et al. Efficacy of an endo-knife with a water-jet function (Flushknife) for endoscopic submucosal dissection of superficial colorectal neoplasms. Am J Gastroenterol 2010; 105: 314-322
    CrossrefPubMedGoogle Scholar
  • 8 Winde G, Nottberg H, Keller R et al. Surgical cure for early rectal carcinomas (T1). Transanal endoscopic microsurgery vs. anterior resection. Dis Colon Rectum 1996; 39: 969-976
    CrossrefPubMedGoogle Scholar
  • 9 Langer C, Liersch T, Suss M et al. Surgical cure for early rectal carcinoma and large adenoma: transanal endoscopic microsurgery (using ultrasound or electrosurgery) compared to conventional local and radical resection. Int J Colorectal Dis 2003; 18: 222-229
    PubMedGoogle Scholar
  • 10 Lee W, Lee D, Choi S et al. Transanal endoscopic microsurgery and radical surgery for T1 and T2 rectal cancer. Surg Endosc 2003; 17: 1283-1287
    CrossrefPubMedGoogle Scholar
  • 11 Wu Y, Wu YY, Li S et al. TEM and conventional rectal surgery for T1 rectal cancer: a meta-analysis. Hepatogastroenterology 2011; 58: 364-368
    PubMedGoogle Scholar
  • 12 Tada M, Inoue H, Yabata E et al. Feasibility of the transparent cap-fitted colonoscope for screening and mucosal resection. Dis Colon Rectum 1997; 40: 618-621
    CrossrefPubMedGoogle Scholar
  • 13 Lee EJ, Lee JB, Lee SH et al. Endoscopic treatment of large colorectal tumors: comparison of endoscopic mucosal resection, endoscopic mucosal resection-precutting, and endoscopic submucosal dissection. Surg Endosc 2012; 26: 2220-2230
    CrossrefPubMedGoogle Scholar
  • 14 Iversen LH, Nielsen H, Pedersen L et al. Seasonal variation in short-term mortality after surgery for colorectal cancer?. Colorectal Dis 2010; 12: e31-36
    CrossrefPubMedGoogle Scholar
  • 15 Paulson EC, Mitra N, Sonnad S et al. National Cancer Institute designation predicts improved outcomes in colorectal cancer surgery. Ann Surg 2008; 248: 675-686
    PubMedGoogle Scholar
  • 16 Vironen JH, Kairaluoma M, Aalto AM et al. Impact of functional results on quality of life after rectal cancer surgery. Dis Colon Rectum 2006; 49: 568-578
    CrossrefPubMedGoogle Scholar
  • 17 Balch GC, De Meo A, Guillem JG. Modern management of rectal cancer: a 2006 update. World J Gastroenterol 2006; 12: 3186-3195
    PubMedGoogle Scholar
  • 18 Engel J, Kerr J, Schlesinger-Raab A et al. Quality of life in rectal cancer patients: a four-year prospective study. Ann Surg 2003; 238: 203-213
    CrossrefPubMedGoogle Scholar
  • 19 Chatwin NA, Ribordy M, Givel JC. Clinical outcomes and quality of life after low anterior resection for rectal cancer. Eur J Surg 2002; 168: 297-301
    CrossrefPubMedGoogle Scholar
  • 20 Braga M, Frasson M, Zuliani W et al. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg 2010; 97: 1180-1186
    CrossrefPubMedGoogle Scholar
  • 21 Tanaka S, Oka S, Kaneko I et al. Endoscopic submucosal dissection for colorectal neoplasia: possibility of standardization. Gastrointest Endosc 2007; 66: 100-107
    CrossrefPubMedGoogle Scholar
  • 22 Cahill RA, Leroy J, Marescaux J. Localized resection for colon cancer. Surg Oncol 2009; 18: 334-342
    CrossrefPubMedGoogle Scholar
  • 23 Kato H, Haga S, Endo S et al. Lifting of lesions during endoscopic mucosal resection (EMR) of early colorectal cancer: implications for the assessment of resectability. Endoscopy 2001; 33: 568-573
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 24 Mellgren A, Sirivongs P, Rothenberger DA et al. Is local excision adequate therapy for early rectal cancer?. Dis Colon Rectum 2000; 43: 1064-1071 ; discussion 1071-1064
    CrossrefPubMedGoogle Scholar
  • 25 Tanaka S, Haruma K, Teixeira CR et al. Endoscopic treatment of submucosal invasive colorectal carcinoma with special reference to risk factors for lymph node metastasis. J Gastroenterol 1995; 30: 710-717
    CrossrefPubMedGoogle Scholar
  • 26 Kobayashi H, Mochizuki H, Morita T et al. Characteristics of recurrence after curative resection for T1 colorectal cancer: Japanese multicenter study. J Gastroenterol 2011; 46: 203-211
    CrossrefPubMedGoogle Scholar
  • 27 Coverlizza S, Risio M, Ferrari A et al. Colorectal adenomas containing invasive carcinoma. Pathologic assessment of lymph node metastatic potential. Cancer 1989; 64: 1937-1947
    CrossrefPubMedGoogle Scholar
  • 28 Kitamura K, Taniguchi H, Yamaguchi T et al. Clinical outcome of surgical treatment for invasive early colorectal cancer in Japan. Hepatogastroenterology 1997; 44: 108-115
    PubMedGoogle Scholar
  • 29 Graham RA, Garnsey L, Jessup JM. Local excision of rectal carcinoma. Am J Surg 1990; 160: 306-312
    CrossrefPubMedGoogle Scholar
  • 30 Brodsky JT, Richard GK, Cohen AM et al. Variables correlated with the risk of lymph node metastasis in early rectal cancer. Cancer 1992; 69: 322-326
    CrossrefPubMedGoogle Scholar
  • 31 Blumberg D, Paty PB, Guillem JG et al. All patients with small intramural rectal cancers are at risk for lymph node metastasis. Dis Colon Rectum 1999; 42: 881-885
    CrossrefPubMedGoogle Scholar
  • 32 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
    CrossrefPubMedGoogle Scholar
  • 33 National Cancer Institute. Rectal Cancer Treatment (PDQ®). 2011 Available from: http://www.cancer.gov/cancertopics/pdq/treatment/rectal/HealthProfessional Accessed: 17 February 2012
    PubMedGoogle Scholar
  • 34 The Association of Coloproctology of Great Britain and Ireland. Guidelines for the management of colorectal cancer. edn 2007 3rd. Available from: http://www.acpgbi.org.uk/wp-content/uploads/2007-CC-Management-Guidelines.pdf Accessed: 17 February 2012
    PubMedGoogle Scholar
  • 35 Oncoline. Cancer clinical practice guidelines. Rectal cancer. Version: 2.0. 2008 Available from: http://oncoline.nl/index.php?pagina=/richtlijn/item/pagina.php&richtlijn_id=615 Accessed: 17 February 2012
    PubMedGoogle Scholar
  • 36 Japanese Society for Cancer of the Colon and Rectum. Japanese guidelines for the treatment of colorectal carcinoma. Tokyo: Kanehara Shuppan Co; 2010: 42-43
    Google Scholar
  • 37 Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993; 25: 455-461
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 38 Yamamoto S, Watanabe M, Hasegawa H et al. The risk of lymph node metastasis in T1 colorectal carcinoma. Hepatogastroenterology 2004; 51: 998-1000
    PubMedGoogle Scholar
  • 39 Sakuragi M, Togashi K, Konishi F et al. Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum 2003; 46: 1626-1632
    CrossrefPubMedGoogle Scholar
  • 40 Endreseth BH, Myrvold HE, Romundstad P et al. Transanal excision vs. major surgery for T1 rectal cancer. Dis Colon Rectum 2005; 48: 1380-1388
    CrossrefPubMedGoogle Scholar
  • 41 Haggitt RC, Glotzbach RE, Soffer EE et al. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology 1985; 89: 328-336
    CrossrefPubMedGoogle Scholar
  • 42 Ueno H, Mochizuki H, Hashiguchi Y et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 2004; 127: 385-394
    CrossrefPubMedGoogle Scholar
  • 43 Son HJ, Song SY, Lee WY et al. Characteristics of early colorectal carcinoma with lymph node metastatic disease. Hepatogastroenterology 2008; 55: 1293-1297
    PubMedGoogle Scholar
  • 44 Egashira Y, Yoshida T, Hirata I et al. Analysis of pathological risk factors for lymph node metastasis of submucosal invasive colon cancer. Mod Pathol 2004; 17: 503-511
    CrossrefPubMedGoogle Scholar
  • 45 Ishii M, Ota M, Saito S et al. Lymphatic vessel invasion detected by monoclonal antibody D2-40 as a predictor of lymph node metastasis in T1 colorectal cancer. Int J Colorectal Dis 2009; 24: 1069-1074
    CrossrefPubMedGoogle Scholar
  • 46 Ishikawa Y, Akishima-Fukasawa Y, Ito K et al. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer 2008; 112: 924-933
    CrossrefPubMedGoogle Scholar
  • 47 Kitajima K, Fujimori T, Fujii S 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: 534-543
    PubMedGoogle Scholar
  • 48 Masaki T, Matsuoka H, Sugiyama M et al. Actual number of tumor budding as a new tool for the individualization of treatment of T1 colorectal carcinomas. J Gastroenterol Hepatol 2006; 21: 1115-1121
    CrossrefPubMedGoogle Scholar
  • 49 Nascimbeni R, Burgart LJ, Nivatvongs S et al. Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 2002; 45: 200-206
    CrossrefPubMedGoogle Scholar
  • 50 Oh-e H, Tanaka S, Kitadai Y et al. Angiogenesis at the site of deepest penetration predicts lymph node metastasis of submucosal colorectal cancer. Dis Colon Rectum 2001; 44: 1129-1136
    CrossrefPubMedGoogle Scholar
  • 51 Okabe S, Shia J, Nash G et al. Lymph node metastasis in T1 adenocarcinoma of the colon and rectum. J Gastrointest Surg 2004; 8: 1032-1039 ; discussion 1039-1040
    CrossrefPubMedGoogle Scholar
  • 52 Rasheed S, Bowley DM, Aziz O et al. Can depth of tumour invasion predict lymph node positivity in patients undergoing resection for early rectal cancer? A comparative study between T1 and T2 cancers. Colorectal Dis 2008; 10: 231-238
    CrossrefPubMedGoogle Scholar
  • 53 Suzuki T, Sadahiro S, Mukoyama S et al. Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt's level 4 invasion: image analysis of submucosal layer invasion. Dis Colon Rectum 2003; 46: 203-208
    CrossrefPubMedGoogle Scholar
  • 54 Tsuruta O, Tsuji Y, Kawano H et al. Indication for endoscopic resection of submucosal colorectal carcinoma: special reference to lymph node metastasis. Diagn Ther Endosc 2000; 6: 101-109
    CrossrefPubMedGoogle Scholar
  • 55 Wang HS, Liang WY, Lin TC et al. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum 2005; 48: 1182-1192
    CrossrefPubMedGoogle Scholar
  • 56 Suzuki A, Togashi K, Nokubi M et al. Evaluation of venous invasion by Elastica van Gieson stain and tumor budding predicts local and distant metastases in patients with T1 stage colorectal cancer. Am J Surg Pathol 2009; 33: 1601-1607
    CrossrefPubMedGoogle Scholar
  • 57 Blenkinsopp WK, Stewart-Brown S, Blesovsky L et al. Histopathology reporting in large bowel cancer. J Clin Pathol 1981; 34: 509-513
    CrossrefPubMedGoogle Scholar
  • 58 Thomas GD, Dixon MF, Smeeton NC et al. Observer variation in the histological grading of rectal carcinoma. J Clin Pathol 1983; 36: 385-391
    CrossrefPubMedGoogle Scholar
  • 59 Bosman FT. World Health Organization, International Agency for Research on Cancer. WHO classification of tumours of the digestive system. 4th. edn. Lyon: International Agency for Research on Cancer; 2010
    Google Scholar
  • 60 Vieth M, Quirke P, Lambert R et al. Annex to Quirke et al. Quality assurance in pathology in colorectal cancer screening and diagnosis: annotations of colorectal lesions. Virchows Arch 2011; 458: 21-30
    CrossrefPubMedGoogle Scholar
  • 61 Nakadoi K, Tanaka S, Kanao H et al. Management of T1 colorectal carcinoma with special reference to criteria for curative endoscopic resection. J Gastroenterol Hepatol 2012; 27: 1057-1062
    CrossrefPubMedGoogle Scholar