Skip to main content
SpringerLink
Log in

Lymphatic Staging in Colorectal Cancer: Pathologic, Molecular, and Sentinel Node Techniques

  • Current Status
  • Published:
Diseases of the Colon & Rectum

PURPOSE

Accurate staging in colorectal cancer is important to predict prognosis and identify patients who could benefit from adjuvant therapy. Patients with lymphatic metastasis, Stage III/Dukes C, are generally treated with adjuvant chemotherapy. Still, patients without lymphatic metastasis do have relapse as high as 27 percent in five years in Dukes B2. It is hypothesized that these patients have occult (micro)metastasis in their lymph nodes. If these (micro)metastasis can be identified, these patients might benefit from adjuvant therapy. We reviewed the literature on procedures to improve lymph node staging.

METHODS

An extensive literature search was performed in PubMed (www.pubmed.com). Using the reference lists, more articles were found.

RESULTS

We found 30 articles about sentinel node in colorectal cancer describing original series. Some groups reported several studies including the same patients. We reported their largest studies. For all other techniques, we only included key articles.

CONCLUSIONS

Many techniques to improve staging have been described. The finding of occult (micro)metastasis is of prognostic significance in most studies. The sentinel node technique has been recently described for use in colorectal cancer. Although it seems clear that this technique has prognostic potential, it is not yet been shown in a follow-up study. Furthermore, the finding of occult (micro)metastasis in any technique used has not been shown to be clinically significant. Whether to treat patients with adjuvant therapy if occult (micro)metastasis are found needs to be proven in future studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. CE Dukes (1932) ArticleTitleThe classification of cancer of the rectum J Pathol Bacteriol 35 323–32

    Google Scholar 

  2. CE Dukes HJ Bussey (1958) ArticleTitleThe spread of rectal cancer and its effect on prognosis Br J Cancer 12 309–20 Occurrence Handle1:STN:280:DyaG1M%2FisFyrtg%3D%3D Occurrence Handle13596482

    CAS  PubMed  Google Scholar 

  3. CE Dukes (1929) ArticleTitleThe spread of cancer of the rectum Br J Surg 17 643–8

    Google Scholar 

  4. JW Kirklin MB Dockerty JM Waugh (1949) ArticleTitleThe role of the peritoneal reflection in the prognosis of carcinoma of the rectum and sigmoid colon Surg Gynecol Obstet 88 326–31 Occurrence Handle18111779 Occurrence Handle1:STN:280:DyaH1M%2Fhtlektw%3D%3D

    PubMed  CAS  Google Scholar 

  5. VB Astler FA Coller (1954) ArticleTitleThe prognostic significance of direct extension of carcinoma of the colon and rectum Ann Surg 139 846–52 Occurrence Handle1:STN:280:DyaG2c%2FnvFWgsw%3D%3D Occurrence Handle13159135

    CAS  PubMed  Google Scholar 

  6. RB Turnbull K Kyle FR Watson J Spratt (1967) ArticleTitleCancer of the colon: the influence of the no-touch isolation technic on survival rates Ann Surg 166 420–7 Occurrence Handle6039601 Occurrence Handle10.1097/00000658-196709000-00010

    Article  PubMed  Google Scholar 

  7. FL Greene DL Page ID Fleming et al. (2002) American Joint Committee on Cancer - Cancer staging handbook, TNM classification of malignant tumors Springer-Verlag New York 129

    Google Scholar 

  8. CG Moertel TR Fleming JS Macdonald et al. (1990) ArticleTitleLevamisole and fluorouracil for adjuvant therapy of resected colon carcinoma N Engl J Med 322 352–8 Occurrence Handle1:STN:280:DyaK3c7js1Ohsw%3D%3D Occurrence Handle2300087 Occurrence Handle10.1056/NEJM199002083220602

    Article  CAS  PubMed  Google Scholar 

  9. International Multicentre Pooled Analysis of Colon Cancer Trials (IMPACT) investigators. Efficacy of adjuvant fluorouracil and folinic acid in colon cancer. International Multicentre Pooled Analysis of Colon Cancer Trials (IMPACT) investigators. Lancet 1995; 345:939-44.

    Google Scholar 

  10. International Multicentre Pooled Analysis of B2 Colon Cancer Trials (IMPACT B2) investigators. Efficacy of adjuvant fluorouracil and folinic acid in B2 colon cancer. International Multicentre Pooled Analysis of B2 Colon Cancer Trials (IMPACT B2) Investigators. J Clin Oncol 1999; 17:1356-63.

    Google Scholar 

  11. S Esser WT Reilly LB Riley C Eyvazzadeh S Arcona (2001) ArticleTitleThe role of sentinel lymph node mapping in staging of colon and rectal cancer Dis Colon Rectum 44 850–6 Occurrence Handle1:STN:280:DC%2BD3MzhvFOquw%3D%3D Occurrence Handle11391147

    CAS  PubMed  Google Scholar 

  12. JH Wong BJ Bowles R Bueno D Shimizu (2002) ArticleTitleImpact of the number of negative nodes on disease-free survival in colorectal cancer patients Dis Colon Rectum 45 1341–8 Occurrence Handle12394433

    PubMed  Google Scholar 

  13. TE Voyer ParticleLe ER Sigurdson AL Hanlon et al. (2003) ArticleTitleColon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089 J Clin Oncol 21 2912–9 Occurrence Handle10.1200/JCO.2003.05.062 Occurrence Handle1:STN:280:DC%2BD3szltlersA%3D%3D Occurrence Handle12885809

    Article  CAS  PubMed  Google Scholar 

  14. NE Joseph ER Sigurdson AL Hanlon et al. (2003) ArticleTitleAccuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection Ann Surg Oncol 10 213–8 Occurrence Handle10.1245/ASO.2003.03.059 Occurrence Handle12679304

    Article  PubMed  Google Scholar 

  15. Steele, GJ (1994) “Colorectal cancer” In: McKenna, RJ, Murphy, GP (eds.), Cancer surgery, Lippincott, Philadelphia, pp 125–84

  16. KS Mainprize H Kulacoglu J Hewavisinthe A Savage N Mortensen BF Warren (1998) ArticleTitleHow many lymph nodes to stage colorectal carcinoma? J Clin Pathol 51 165–6 Occurrence Handle9602694 Occurrence Handle1:STN:280:DyaK1c3msFCjtg%3D%3D Occurrence Handle10.1136/jcp.51.2.165

    Article  PubMed  CAS  Google Scholar 

  17. JH Wong R Severino MB Honnebier P Tom TS Namiki (1999) ArticleTitleNumber of nodes examined and staging accuracy in colorectal carcinoma J Clin Oncol 17 2896–900 Occurrence Handle10561368 Occurrence Handle1:STN:280:DC%2BD3c%2FjtVSqtQ%3D%3D

    PubMed  CAS  Google Scholar 

  18. J Maurel G Launoy P Grosclaude et al. (1998) ArticleTitleLymph node harvest reporting in patients with carcinoma of the large bowel: a French population-based study Cancer 82 1482–6 Occurrence Handle1:STN:280:DyaK1c3htlWrug%3D%3D Occurrence Handle9554524

    CAS  PubMed  Google Scholar 

  19. R Tang JY Wang JS Chen et al. (1995) ArticleTitleSurvival impact of lymph node metastasis in TNM stage III carcinoma of the colon and rectum J Am Coll Surg 180 705–12 Occurrence Handle1:STN:280:DyaK2M3ptFGnsg%3D%3D Occurrence Handle7773484

    CAS  PubMed  Google Scholar 

  20. LP Fielding PA Arsenault PH Chapuis et al. (1991) ArticleTitleClinicopathological staging for colorectal cancer: an International Documentation System (IDS) and an International Comprehensive Anatomical Terminology (ICAT) J Gastroenterol Hepatol 6 325–44 Occurrence Handle1:STN:280:DyaK38%2FgtlGjtQ%3D%3D Occurrence Handle1912440

    CAS  PubMed  Google Scholar 

  21. NS Goldstein W Sanford M Coffey LJ Layfield (1996) ArticleTitleLymph node recovery from colorectal resection specimens removed for adenocarcinoma. Trends over time and a recommendation for a minimum number of lymph nodes to be recovered Am J Clin Pathol 106 209–16 Occurrence Handle1:STN:280:DyaK28zjsFShtA%3D%3D Occurrence Handle8712176

    CAS  PubMed  Google Scholar 

  22. G Cserni K Vajda M Tarjan R Bori M Svebis B Baltas (1999) ArticleTitleNodal staging of colorectal carcinomas from quantitative and qualitative aspects. Can lymphatic mapping help staging? Pathol Oncol Res 5 291–6 Occurrence Handle10.1053/paor.1999.0205 Occurrence Handle1:STN:280:DC%2BD3c%2Fns1Oruw%3D%3D Occurrence Handle10607924

    Article  CAS  PubMed  Google Scholar 

  23. L Herrera-Ornelas J Justiniano N Castillo NJ Petrelli JP Stulc A Mittelman (1987) ArticleTitleMetastases in small lymph nodes from colon cancer Arch Surg 122 1253–6 Occurrence Handle1:STN:280:DyaL1c%2FkvVyqsQ%3D%3D Occurrence Handle3675188

    CAS  PubMed  Google Scholar 

  24. L Herrera JR Villarreal (1992) ArticleTitleIncidence of metastases from rectal adenocarcinoma in small lymph nodes detected by a clearing technique Dis Colon Rectum 35 783–8 Occurrence Handle1:STN:280:DyaK38zlsVCqtg%3D%3D Occurrence Handle1644003

    CAS  PubMed  Google Scholar 

  25. MA Rodriguez-Bigas S Maamoun TK Weber RB Penetrante LE Blumenson NJ Petrelli (1996) ArticleTitleClinical significance of colorectal cancer: metastases in lymph nodes < 5 mm in size Ann Surg Oncol 3 124–30 Occurrence Handle1:STN:280:DyaK283js1Gnsg%3D%3D Occurrence Handle8646511

    CAS  PubMed  Google Scholar 

  26. NY Haboubi SA Abdalla S Amini et al. (1998) ArticleTitleThe novel combination of fat clearance and immunohistochemistry improves prediction of the outcome of patients with colorectal carcinomas: a preliminary study Int J Colorectal Dis 13 99–102 Occurrence Handle1:STN:280:DyaK1czgt1emsA%3D%3D Occurrence Handle9638496

    CAS  PubMed  Google Scholar 

  27. KW Scott RH Grace (1989) ArticleTitleDetection of lymph node metastases in colorectal carcinoma before and after fat clearance Br J Surg 76 1165–7 Occurrence Handle2688803 Occurrence Handle1:STN:280:DyaK3c%2FovF2msQ%3D%3D

    PubMed  CAS  Google Scholar 

  28. JW Pickren (1975) ArticleTitleCurrent concepts in cancer. Nodal clearance and detection JAMA 231 969–71 Occurrence Handle1:STN:280:DyaE2M7jsFyitA%3D%3D Occurrence Handle1173109

    CAS  PubMed  Google Scholar 

  29. SJ Cawthorn NM Gibbs CG Marks (1986) ArticleTitleClearance technique for the detection of lymph nodes in colorectal cancer Br J Surg 73 58–60 Occurrence Handle3512023 Occurrence Handle1:STN:280:DyaL287jt1ensw%3D%3D

    PubMed  CAS  Google Scholar 

  30. NY Haboubi P Clark SM Kaftan PF Schofield (1992) ArticleTitleThe importance of combining xylene clearance and immunohistochemistry in the accurate staging of colorectal carcinoma J R Soc Med 85 386–8 Occurrence Handle1:STN:280:DyaK38zjtlCqsA%3D%3D Occurrence Handle1378498

    CAS  PubMed  Google Scholar 

  31. R Koren A Siegal B Klein et al. (1997) ArticleTitleLymph node-revealing solution: simple new method for detecting minute lymph nodes in colon carcinoma Dis Colon Rectum 40 407–10 Occurrence Handle1:STN:280:DyaK2s3mtVGlug%3D%3D Occurrence Handle9106688

    CAS  PubMed  Google Scholar 

  32. DN Poller (2000) ArticleTitleMethod of specimen fixation and pathological dissection of colorectal cancer influences retrieval of lymph nodes and tumour nodal stage Eur J Surg Oncol 26 758–62 Occurrence Handle1:STN:280:DC%2BD3M7jvFKntQ%3D%3D Occurrence Handle11087641

    CAS  PubMed  Google Scholar 

  33. MJ O’Brien N Zamcheck B Burke SE Kirkham CA Saravis LS Gottlieb (1981) ArticleTitleImmunocytochemical localization of carcinoembryonic antigen in benign and malignant colorectal tissues. Assessment of diagnostic value Am J Clin Pathol 75 283–90 Occurrence Handle1:STN:280:DyaL3M7lslSltQ%3D%3D Occurrence Handle7010989

    CAS  PubMed  Google Scholar 

  34. CA Makin LG Bobrow RJ Nicholls (1989) ArticleTitleCan immunohistology improve detection of lymph-node metastases in large-bowel cancer? Dis Colon Rectum 32 99–102 Occurrence Handle1:STN:280:DyaL1M7itVCksA%3D%3D Occurrence Handle2464463

    CAS  PubMed  Google Scholar 

  35. BR Davidson VR Sams J Styles C Deane PB Boulos (1990) ArticleTitleDetection of occult nodal metastases in patients with colorectal carcinoma Cancer 65 967–70 Occurrence Handle2297665 Occurrence Handle1:STN:280:DyaK3c7isVWltg%3D%3D

    PubMed  CAS  Google Scholar 

  36. AG Nicholson CG Marks MG Cook (1994) ArticleTitleEffect on lymph node status of triple levelling and immunohistochemistry with CAM 5.2 on node negative colorectal carcinomas Gut 35 1447–8 Occurrence Handle1:STN:280:DyaK2M%2FkslKqsA%3D%3D Occurrence Handle7525418

    CAS  PubMed  Google Scholar 

  37. R Cutait VA Alves LC Lopes et al. (1991) ArticleTitleRestaging of colorectal cancer based on the identification of lymph node micrometastases through immunoperoxidase staining of CEA and cytokeratins Dis Colon Rectum 34 917–20 Occurrence Handle1:STN:280:DyaK38%2Fgs12ltA%3D%3D Occurrence Handle1717210

    CAS  PubMed  Google Scholar 

  38. MD Jeffers GM O’Dowd H Mulcahy M Stagg DP O’Donoghue M Toner (1994) ArticleTitleThe prognostic significance of immunohistochemically detected lymph node micrometastases in colorectal carcinoma J Pathol 172 183–7 Occurrence Handle1:STN:280:DyaK2c3itlCmsg%3D%3D Occurrence Handle7513353

    CAS  PubMed  Google Scholar 

  39. JK Greenson CE Isenhart R Rice C Mojzisik D Houchens EW Martin (1994) ArticleTitleIdentification of occult micrometastases in pericolic lymph nodes of Duke’s B colorectal cancer patients using monoclonal antibodies against cytokeratin and CC49. Correlation with long-term survival Cancer 73 563–9 Occurrence Handle1:STN:280:DyaK2c7jtVahtA%3D%3D Occurrence Handle7507795

    CAS  PubMed  Google Scholar 

  40. G Adell B Boeryd B Franlund R Sjodahl L Hakansson (1996) ArticleTitleOccurrence and prognostic importance of micrometastases in regional lymph nodes in Dukes B colorectal carcinoma: an immunohistochemical study Eur J Surg 162 637–42 Occurrence Handle1:STN:280:DyaK2s%2Fks1Ojsw%3D%3D Occurrence Handle8891622

    CAS  PubMed  Google Scholar 

  41. R Broll V Schauer H Schimmelpenning et al. (1997) ArticleTitlePrognostic relevance of occult tumor cells in lymph nodes of colorectal carcinomas: an immunohistochemical study Dis Colon Rectum 40 1465–71 Occurrence Handle1:STN:280:DyaK1c%2FmvFyktw%3D%3D Occurrence Handle9407986

    CAS  PubMed  Google Scholar 

  42. A öberg R Stenling B Tavelin G Lindmark (1998) ArticleTitleAre lymph node micrometastases of any clinical significance in Dukes Stages A and B colorectal cancer? Dis Colon Rectum 41 1244–9 Occurrence Handle9788387

    PubMed  Google Scholar 

  43. CL Hitchcock J Sampsel DC Young EW Martin MW Arnold (1999) ArticleTitleLimitations with light microscopy in the detection of colorectal cancer cells Dis Colon Rectum 42 1046–52 Occurrence Handle1:STN:280:DyaK1MzosFeisw%3D%3D Occurrence Handle10458129

    CAS  PubMed  Google Scholar 

  44. J Tschmelitsch DS Klimstra AM Cohen (2000) ArticleTitleLymph node micrometastases do not predict relapse in Stage II colon cancer Ann Surg Oncol 7 601–8 Occurrence Handle1:STN:280:DC%2BD3cvltVGktw%3D%3D Occurrence Handle11005559

    CAS  PubMed  Google Scholar 

  45. S Noura H Yamamoto T Ohnishi et al. (2002) ArticleTitleComparative detection of lymph node micrometastases of Stage II colorectal cancer by reverse transcriptase polymerase chain reaction and immunohistochemistry J Clin Oncol 20 4232–41 Occurrence Handle10.1200/JCO.2002.10.023 Occurrence Handle1:CAS:528:DC%2BD38XnsFyqsb0%3D Occurrence Handle12377967

    Article  CAS  PubMed  Google Scholar 

  46. M Shimoyama T Yamazaki T Suda K Hatakeyama (2003) ArticleTitlePrognostic significance of lateral lymph node micrometastases in lower rectal cancer: an immunohistochemical study with CAM5.2 Dis Colon Rectum 46 333–9 Occurrence Handle12626908

    PubMed  Google Scholar 

  47. PJ Diest Particlevan HL Peterse PJ Borgstein O Hoekstra CJ Meijer (1999) ArticleTitlePathological investigation of sentinel lymph nodes Eur J Nucl Med 26 S43–9 Occurrence Handle10199932

    PubMed  Google Scholar 

  48. M Sasaki H Watanabe JR Jass et al. (1997) ArticleTitleOccult lymph node metastases detected by cytokeratin immunohistochemistry predict recurrence in “node-negative” colorectal cancer J Gastroenterol 32 758–64 Occurrence Handle1:STN:280:DyaK1c%2FptFynug%3D%3D Occurrence Handle9430013 Occurrence Handle10.1007/BF02936951

    Article  CAS  PubMed  Google Scholar 

  49. N Hayashi I Ito A Yanagisawa et al. (1995) ArticleTitleGenetic diagnosis of lymph-node metastasis in colorectal cancer Lancet 345 1257–9 Occurrence Handle1:STN:280:DyaK2M3msVyitw%3D%3D Occurrence Handle7746054

    CAS  PubMed  Google Scholar 

  50. R Rosenberg A Hoos J Mueller et al. (2002) ArticleTitlePrognostic significance of cytokeratin-20 reverse transcriptase polymerase chain reaction in lymph nodes of node-negative colorectal cancer patients J Clin Oncol 20 1049–55 Occurrence Handle11844829

    PubMed  Google Scholar 

  51. Y Fujiwara DD Chi H Wang et al. (1999) ArticleTitlePlasma DNA microsatellites as tumor-specific markers and indicators of tumor progression in melanoma patients Cancer Res 59 1567–71 Occurrence Handle1:CAS:528:DyaK1MXisVWkurg%3D Occurrence Handle10197630

    CAS  PubMed  Google Scholar 

  52. X Chen H Bonnefoi S Diebold-Berger et al. (1999) ArticleTitleDetecting tumor-related alterations in plasma or serum DNA of patients diagnosed with breast cancer Clin Cancer Res 5 2297–303 Occurrence Handle10499596 Occurrence Handle1:CAS:528:DyaK1MXmsFyjsr0%3D

    PubMed  CAS  Google Scholar 

  53. JL Bos (1989) ArticleTitleRas oncogenes in human cancer: a review Cancer Res 49 4682–9 Occurrence Handle1:CAS:528:DyaL1MXltlWksL4%3D Occurrence Handle2547513

    CAS  PubMed  Google Scholar 

  54. JM Nigro SJ Baker AC Preisinger et al. (1989) ArticleTitleMutations in the p53 gene occur in diverse human tumour types Nature 342 705–8 Occurrence Handle1:CAS:528:DyaK3cXkvFyhug%3D%3D Occurrence Handle2531845

    CAS  PubMed  Google Scholar 

  55. M Mori K Mimori H Inoue et al. (1995) ArticleTitleDetection of cancer micrometastases in lymph nodes by reverse transcriptase-polymerase chain reaction Cancer Res 55 3417–20 Occurrence Handle1:CAS:528:DyaK2MXnt1antrs%3D Occurrence Handle7542169

    CAS  PubMed  Google Scholar 

  56. M Futamura Y Takagi H Koumura et al. (1998) ArticleTitleSpread of colorectal cancer micrometastases in regional lymph nodes by reverse transcriptase-polymerase chain reactions for carcinoembryonic antigen and cytokeratin 20 J Surg Oncol 68 34–40 Occurrence Handle10.1002/(SICI)1096-9098(199805)68:1<34::AID-JSO8>3.0.CO;2-M Occurrence Handle1:STN:280:DyaK1c3nt1WqsA%3D%3D Occurrence Handle9610661

    Article  CAS  PubMed  Google Scholar 

  57. M Mori K Mimori H Ueo et al. (1998) ArticleTitleClinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription-polymerase chain reaction in patients with gastrointestinal or breast carcinomas J Clin Oncol 16 128–32 Occurrence Handle9440733 Occurrence Handle1:STN:280:DyaK1c7gtFKrsQ%3D%3D

    PubMed  CAS  Google Scholar 

  58. GJ Liefers AM Cleton-Jansen CJ Velde Particlevan de et al. (1998) ArticleTitleMicrometastases and survival in stage II colorectal cancer N Engl J Med 339 223–8 Occurrence Handle10.1056/NEJM199807233390403 Occurrence Handle1:STN:280:DyaK1czivVKhuw%3D%3D Occurrence Handle9673300

    Article  CAS  PubMed  Google Scholar 

  59. J Gunn JL McCall K Yun PA Wright (1996) ArticleTitleDetection of micrometastases in colorectal cancer patients by K19 and K20 reverse-transcription polymerase chain reaction Lab Invest 75 611–6 Occurrence Handle1:CAS:528:DyaK28XmvFWms7c%3D Occurrence Handle8874391

    CAS  PubMed  Google Scholar 

  60. S Dorudi E Kinrade NC Marshall R Feakins NS Williams SA Bustin (1998) ArticleTitleGenetic detection of lymph node micrometastases in patients with colorectal cancer Br J Surg 85 98–100 Occurrence Handle9462394 Occurrence Handle1:STN:280:DyaK1c7itl2ntA%3D%3D

    PubMed  CAS  Google Scholar 

  61. J Weitz P Kienle A Magener et al. (1999) ArticleTitleDetection of disseminated colorectal cancer cells in lymph nodes, blood and bone marrow Clin Cancer Res 5 1830–6 Occurrence Handle10430088 Occurrence Handle1:STN:280:DyaK1MzlslWmtQ%3D%3D

    PubMed  CAS  Google Scholar 

  62. AE Merrie K Yun AM Rij Particlevan JL McCall (1999) ArticleTitleDetection and significance of minimal residual disease in colorectal cancer Histol Histopathol 14 561–9 Occurrence Handle1:STN:280:DyaK1M3ivFarug%3D%3D Occurrence Handle10212818

    CAS  PubMed  Google Scholar 

  63. LS Wong JE Cantrill S Odogwu AG Morris IA Fraser (1997) ArticleTitleDetection of circulating tumour cells and nodal metastasis by reverse transcriptase-polymerase chain reaction technique Br J Surg 84 834–9 Occurrence Handle9189103 Occurrence Handle1:STN:280:DyaK2szjt12nsw%3D%3D

    PubMed  CAS  Google Scholar 

  64. Y Ichikawa T Ishikawa N Momiyama et al. (1998) ArticleTitleDetection of regional lymph node metastases in colon cancer by using RT-PCR for matrix metalloproteinase 7, matrilysin Clin Exp Metastasis 16 3–8 Occurrence Handle9502072 Occurrence Handle1:CAS:528:DyaK1cXhvVyit78%3D

    PubMed  CAS  Google Scholar 

  65. SA Waldman B Cagir J Rakinic et al. (1998) ArticleTitleUse of guanylyl cyclase C for detecting micrometastases in lymph nodes of patients with colon cancer Dis Colon Rectum 41 310–5 Occurrence Handle1:STN:280:DyaK1c7ntlelsg%3D%3D Occurrence Handle9514425

    CAS  PubMed  Google Scholar 

  66. A Bernini M Spencer S Frizelle et al. (2000) ArticleTitleEvidence for colorectal cancer micrometastases using reverse transcriptase-polymerase chain reaction analysis of MUC2 in lymph nodes Cancer Detect Prev 24 72–9 Occurrence Handle1:CAS:528:DC%2BD3cXit1Khu7o%3D Occurrence Handle10757125

    CAS  PubMed  Google Scholar 

  67. AJ Bosma B Weigelt AC Lambrechts et al. (2002) ArticleTitleDetection of circulating breast tumor cells by differential expression of marker genes Clin Cancer Res 8 1871–7 Occurrence Handle12060630 Occurrence Handle1:CAS:528:DC%2BD38Xlt1Crur4%3D

    PubMed  CAS  Google Scholar 

  68. DL Morton DR Wen JH Wong et al. (1992) ArticleTitleTechnical details of intraoperative lymphatic mapping for early stage melanoma Arch Surg 127 392–9 Occurrence Handle1:STN:280:DyaK383hsFWjsw%3D%3D Occurrence Handle1558490

    CAS  PubMed  Google Scholar 

  69. LR Braithwaite (1923) ArticleTitleFlow of lymph from ileocaecal angle Br J Surg 11 7–26

    Google Scholar 

  70. J Weinberg EM Greaney (1951) ArticleTitleThe use and toxicity of pontamine sky blue Science 114 41–2 Occurrence Handle1:STN:280:DyaG3M%2FosVCntg%3D%3D Occurrence Handle14854894

    CAS  PubMed  Google Scholar 

  71. J Weinberg EM Greaney (1950) ArticleTitleIdentification of regional lymph nodes by means of a vital staining dye during surgery of gastric cancer Surg Gynecol Obstet 90 561–7 Occurrence Handle1:STN:280:DyaG3c%2FivVSmtQ%3D%3D Occurrence Handle15418425

    CAS  PubMed  Google Scholar 

  72. IJ Cohn W Leon LH Strug (1958) ArticleTitleVital staining of the thoracic duct Ann Surg 148 867–70 Occurrence Handle13606738

    PubMed  Google Scholar 

  73. RM Cabañas (1977) ArticleTitleAn approach for the treatment of penile carcinoma Cancer 39 456–66 Occurrence Handle1:STN:280:CSiC3MzntlY%3D Occurrence Handle837331

    CAS  PubMed  Google Scholar 

  74. JH Wong LA Cagle DL Morton (1991) ArticleTitleLymphatic drainage of skin to a sentinel lymph node in a feline model Ann Surg 214 637–41 Occurrence Handle1:STN:280:DyaK38%2FmtFaluw%3D%3D Occurrence Handle1953118

    CAS  PubMed  Google Scholar 

  75. JC Alex DL Weaver JT Fairbank BS Rankin DN Krag (1993) ArticleTitleGamma-probe-guided lymph node localization in malignant melanoma Surg Oncol 2 303–8 Occurrence Handle1:STN:280:DyaK2c7jvVGhsw%3D%3D Occurrence Handle8305972

    CAS  PubMed  Google Scholar 

  76. DN Krag DL Weaver JC Alex JT Fairbank (1993) ArticleTitleSurgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe Surg Oncol 2 335–9 Occurrence Handle10.1016/0960-7404(93)90064-6 Occurrence Handle1:STN:280:DyaK2c7nslegtQ%3D%3D Occurrence Handle8130940

    Article  CAS  PubMed  Google Scholar 

  77. AE Giuliano DM Kirgan JM Guenther DL Morton (1994) ArticleTitleLymphatic mapping and sentinel lymphadenectomy for breast cancer Ann Surg 220 391–8 Occurrence Handle8092905 Occurrence Handle1:STN:280:DyaK2cznvFyksA%3D%3D

    PubMed  CAS  Google Scholar 

  78. PR Kelemen AJ Herle ParticleVan AE Giuliano (1998) ArticleTitleSentinel lymphadenectomy in thyroid malignant neoplasms Arch Surg 133 288–92 Occurrence Handle1:STN:280:DyaK1c7ns12hsw%3D%3D Occurrence Handle9517742

    CAS  PubMed  Google Scholar 

  79. C Levenback TW Burke DM Gershenson M Morris A Malpica MI Ross (1994) ArticleTitleIntraoperative lymphatic mapping for vulvar cancer Obstet Gynecol 84 163–7 Occurrence Handle1:STN:280:DyaK2czhs1eksg%3D%3D Occurrence Handle8041523

    CAS  PubMed  Google Scholar 

  80. AJ Bilchik A Giuliano R Essner et al. (1998) ArticleTitleUniversal application of intraoperative lymphatic mapping and sentinel lymphadenectomy in solid neoplasms Cancer J Sci Am 4 351–8 Occurrence Handle1:STN:280:DyaK1M%2FntVantw%3D%3D Occurrence Handle9853133

    CAS  PubMed  Google Scholar 

  81. JJ Joosten LJ Strobbe CA Wauters M Pruszczynski T Wobbes TJ Ruers (1999) ArticleTitleIntraoperative lymphatic mapping and the sentinel node concept in colorectal carcinoma Br J Surg 86 482–6 Occurrence Handle10.1046/j.1365-2168.1999.01051.x Occurrence Handle1:STN:280:DyaK1M3jtlOlsQ%3D%3D Occurrence Handle10215818

    Article  CAS  PubMed  Google Scholar 

  82. DA Wiese S Saha J Badin (1999) ArticleTitleSentinel lymph node mapping in staging of colorectal carcinoma Am J Clin Pathol 112 542

    Google Scholar 

  83. S Saha D Wiese J Badin et al. (2000) ArticleTitleTechnical details of sentinel lymph node mapping in colorectal cancer and its impact on staging Ann Surg Oncol 7 120–4 Occurrence Handle1:STN:280:DC%2BD3c3it1ChtQ%3D%3D Occurrence Handle10761790

    CAS  PubMed  Google Scholar 

  84. GJ Tsioulias TF Wood DL Morton AJ Bilchik (2000) ArticleTitleLymphatic mapping and focused analysis of sentinel lymph nodes upstage gastrointestinal neoplasms Arch Surg 135 926–32 Occurrence Handle10.1001/archsurg.135.8.926 Occurrence Handle10922254 Occurrence Handle1:STN:280:DC%2BD3cvhs12rsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  85. GS Waters KR Geisinger DD Garske BW Loggie EA Levine (2000) ArticleTitleSentinel lymph node mapping for carcinoma of the colon: a pilot study Am Surg 66 943–5 Occurrence Handle1:STN:280:DC%2BD3M7mtFWrtg%3D%3D Occurrence Handle11261621

    CAS  PubMed  Google Scholar 

  86. TF Wood GJ Tsioulias DL Morton et al. (2000) ArticleTitleFocused examination of sentinel lymph nodes upstages early colorectal carcinoma Am Surg 66 998–1003 Occurrence Handle1:STN:280:DC%2BD3M%2FmvVCntg%3D%3D Occurrence Handle11090005

    CAS  PubMed  Google Scholar 

  87. DA Wiese S Saha J Badin et al. (2000) ArticleTitlePathologic evaluation of sentinel lymph nodes in colorectal carcinoma Arch Pathol Lab Med 124 1759–63 Occurrence Handle11100053 Occurrence Handle1:STN:280:DC%2BD3M%2FpsVyqsg%3D%3D

    PubMed  CAS  Google Scholar 

  88. Y Kitagawa H Fujii M Mukai et al. (2000) ArticleTitleThe role of the sentinel lymph node in gastrointestinal cancer Surg Clin North Am 80 1799–809 Occurrence Handle1:STN:280:DC%2BD3M%2FoslSgug%3D%3D Occurrence Handle11140874

    CAS  PubMed  Google Scholar 

  89. S Saha D Nora JH Wong D Weise (2000) ArticleTitleSentinel lymph node mapping in colorectal cancer–a review Surg Clin North Am 80 1811–9 Occurrence Handle1:STN:280:DC%2BD3M%2FoslSguw%3D%3D Occurrence Handle11140875

    CAS  PubMed  Google Scholar 

  90. AJ Bilchik S Saha D Wiese et al. (2001) ArticleTitleMolecular staging of early colon cancer on the basis of sentinel node analysis: a multicenter phase II trial J Clin Oncol 19 1128–36 Occurrence Handle1:STN:280:DC%2BD3M3gsFagtA%3D%3D Occurrence Handle11181678

    CAS  PubMed  Google Scholar 

  91. TF Wood S Saha DL Morton et al. (2001) ArticleTitleValidation of lymphatic mapping in colorectal cancer: in vivo, ex vivo, and laparoscopic techniques Ann Surg Oncol 8 150–7 Occurrence Handle10.1245/aso.2001.8.2.150 Occurrence Handle1:STN:280:DC%2BD3Mzgt1agtw%3D%3D Occurrence Handle11258780

    Article  CAS  PubMed  Google Scholar 

  92. AE Merrie AM Rij Particlevan LV Phillips JI Rossaak K Yun JL McCall (2001) ArticleTitleDiagnostic use of the sentinel node in colon cancer Dis Colon Rectum 44 410–7 Occurrence Handle1:STN:280:DC%2BD3M7pvFyruw%3D%3D Occurrence Handle11289289

    CAS  PubMed  Google Scholar 

  93. JH Wong S Steineman C Calderia J Bowles T Namiki (2001) ArticleTitleEx vivo sentinel node mapping in carcinoma of the colon and rectum Ann Surg 233 515–21 Occurrence Handle10.1097/00000658-200104000-00006 Occurrence Handle1:STN:280:DC%2BD3M3kvVajsA%3D%3D Occurrence Handle11303133

    Article  CAS  PubMed  Google Scholar 

  94. JC Paramo J Summerall C Wilson et al. (2001) ArticleTitleIntraoperative sentinel lymph node mapping in patients with colon cancer Am J Surg 182 40–3 Occurrence Handle11532413 Occurrence Handle1:STN:280:DC%2BD3MvovFOnsQ%3D%3D

    PubMed  CAS  Google Scholar 

  95. TF Wood M Spirt D Rangel et al. (2001) ArticleTitleLymphatic mapping improves staging during laparoscopic colectomy for cancer Surg Endosc 15 715–9 Occurrence Handle1:STN:280:DC%2BD3MrksV2ktg%3D%3D Occurrence Handle11591974

    CAS  PubMed  Google Scholar 

  96. BW Feig S Curley A Lucci et al. (2001) ArticleTitleA caution regarding lymphatic mapping in patients with colon cancer Am J Surg 182 707–12 Occurrence Handle10.1016/S0002-9610(01)00803-0 Occurrence Handle11839343 Occurrence Handle1:STN:280:DC%2BD387gvVWgsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  97. S Saha A Bilchik D Wiese et al. (2001) ArticleTitleUltrastaging of colorectal cancer by sentinel lymph node mapping technique–a multicenter trial Ann Surg Oncol 8 94S–8S Occurrence Handle1:STN:280:DC%2BD3Mrlt12rtg%3D%3D Occurrence Handle11599912

    CAS  PubMed  Google Scholar 

  98. TL Fitzgerald MA Khalifa M Zahrani ParticleAl CH Law AJ Smith (2002) ArticleTitleEx vivo sentinel lymph node biopsy in colorectal cancer: a feasibility study J Surg Oncol 80 27–32 Occurrence Handle10.1002/jso.10091 Occurrence Handle1:STN:280:DC%2BD383osVaqtQ%3D%3D Occurrence Handle11967903

    Article  CAS  PubMed  Google Scholar 

  99. W Evangelista MA Satolli A Malossi B Mussa S Sandrucci (2002) ArticleTitleSentinel lymph node mapping in colorectal cancer: a feasibility study Tumori 88 37–40 Occurrence Handle12004848

    PubMed  Google Scholar 

  100. JC Paramo J Summerall R Poppiti TW Mesko (2002) ArticleTitleValidation of sentinel node mapping in patients with colon cancer Ann Surg Oncol 9 550–4 Occurrence Handle10.1245/aso.2002.9.6.550 Occurrence Handle12095970

    Article  PubMed  Google Scholar 

  101. Gandy CP, Biddlestone LR, Roe AM, O’Leary DP. Intra-operative injection of Patent Blue V dye to facilitate nodal staging in colorectal cancer. Colorectal Dis 2002; 4:447–9.

    Google Scholar 

  102. AJ Bilchik D Nora RA Tollenaar et al. (2002) ArticleTitleUltrastaging of early colon cancer using lymphatic mapping and molecular analysis Eur J Cancer 38 977–85 Occurrence Handle10.1016/S0959-8049(02)00058-8 Occurrence Handle1:STN:280:DC%2BD383ktVyqtw%3D%3D Occurrence Handle11978523

    Article  CAS  PubMed  Google Scholar 

  103. GJ Tsioulias TF Wood M Spirt DL Morton AJ Bilchik (2002) ArticleTitleA novel lymphatic mapping technique to improve localization and staging of early colon cancer during laparoscopic colectomy Am Surg 68 561–5 Occurrence Handle12132733

    PubMed  Google Scholar 

  104. Y Bendavid JF Latulippe RJ Younan et al. (2002) ArticleTitlePhase I study on sentinel lymph node mapping in colon cancer: a preliminary report J Surg Oncol 79 81–4 Occurrence Handle11815993

    PubMed  Google Scholar 

  105. TF Wood DT Nora DL Morton et al. (2002) ArticleTitleOne hundred consecutive cases of sentinel lymph node mapping in early colorectal carcinoma: detection of missed micrometastases J Gastrointest Surg 6 322–9 Occurrence Handle12022982

    PubMed  Google Scholar 

  106. Y Kitagawa M Watanabe H Hasegawa et al. (2002) ArticleTitleSentinel node mapping for colorectal cancer with radioactive tracer Dis Colon Rectum 45 1476–80 Occurrence Handle12432294

    PubMed  Google Scholar 

  107. G Broderick-Villa A Ko TX O’Connell JM Guenther T Danial LA DiFronzo (2002) ArticleTitleDoes tumor burden limit the accuracy of lymphatic mapping and sentinel lymph node biopsy in colorectal cancer? Cancer J 8 445–50 Occurrence Handle12500853 Occurrence Handle10.1097/00130404-200211000-00008

    Article  PubMed  Google Scholar 

  108. AJ Bilchik DT Nora S Saha et al. (2002) ArticleTitleThe use of molecular profiling of early colorectal cancer to predict micrometastases Arch Surg 137 1377–83 Occurrence Handle1:CAS:528:DC%2BD38Xpslens7o%3D Occurrence Handle12470104

    CAS  PubMed  Google Scholar 

  109. AM Lacy JC Garciá-Valdecasas S Delgado et al. (2002) ArticleTitleLaparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial Lancet 359 2224–9 Occurrence Handle10.1016/S0140-6736(02)09290-5 Occurrence Handle12103285

    Article  PubMed  Google Scholar 

  110. AM Cohen EW Martin I Lavery et al. (1991) ArticleTitleRadioimmunoguided surgery using iodine 125 B72.3 in patients with colorectal cancer Arch Surg 126 349–52 Occurrence Handle1:STN:280:DyaK3M7ltFaksA%3D%3D Occurrence Handle1998477

    CAS  PubMed  Google Scholar 

  111. F Aftab HS Stoldt A Testori et al. (1996) ArticleTitleRadioimmunoguided surgery and colorectal cancer Eur J Surg Oncol 22 381–8 Occurrence Handle1:STN:280:DyaK28znslynug%3D%3D Occurrence Handle8783657

    CAS  PubMed  Google Scholar 

  112. RJ Cote DP Houchens CL Hitchcock et al. (1996) ArticleTitleIntraoperative detection of occult colon cancer micrometastases using 125 I-radiolabled monoclonal antibody CC49 Cancer 77 613–20 Occurrence Handle1:STN:280:DyaK287os1ynsQ%3D%3D Occurrence Handle8616751

    CAS  PubMed  Google Scholar 

  113. A Renda F Iovino L Capasso L Ricciardelli V Tammaro W Acampa (1998) ArticleTitleRadioimmunoguided surgery in colorectal cancer: a 6-year experience with four different technical solutions Semin Surg Oncol 15 226–30 Occurrence Handle1:STN:280:DyaK1M%2FksVynsA%3D%3D Occurrence Handle9829377

    CAS  PubMed  Google Scholar 

  114. G Tsavellas H Patel TG Allen-Mersh (2001) ArticleTitleDetection and clinical significance of occult tumour cells in colorectal cancer Br J Surg 88 1307–20 Occurrence Handle11578283 Occurrence Handle1:STN:280:DC%2BD3Mrjt1Snsg%3D%3D

    PubMed  CAS  Google Scholar 

  115. LJ Van’t Veer H Dai MJ Vijver Particlevan de et al. (2002) ArticleTitleGene expression profiling predicts clinical outcome of breast cancer Nature 415 530–6 Occurrence Handle10.1038/415530a Occurrence Handle11823860 Occurrence Handle1:CAS:528:DC%2BD38Xht1Giu7k%3D

    Article  PubMed  CAS  Google Scholar 

  116. A Ahr T Karn C Solbach et al. (2002) ArticleTitleIdentification of high risk breast-cancer patients by gene expression profiling Lancet 359 131–2 Occurrence Handle11809257

    PubMed  Google Scholar 

  117. PJ Borgstein R Pijpers EF Comans PJ Diest Particlevan RP Boom S Meijer (1998) ArticleTitleSentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection J Am Coll Surg 186 275–83 Occurrence Handle10.1016/S1072-7515(98)00011-8 Occurrence Handle1:STN:280:DyaK1c7mvFSktQ%3D%3D Occurrence Handle9510258

    Article  CAS  PubMed  Google Scholar 

  118. Suga K, Okuda J, Yamamoto T, Nishiguchi K, Toyoda M, Tanigawa N. Lateral lymph node dissection for lower rectal cancer in terms of sentinel node concept. The third international sentinel node congress, Yokohama, Japan (abstract book). Tokyo: Keio University Press, 2003, p 219

  119. Bembenek A, Rau B, Ulmer C, et al. Sentinel lymph node in rectal cancer: research for a difficult indication. The third international sentinel node congress, Yokohama, Japan. Tokyo: Keio University Press, 2003, p 168

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Isala Klinieken, Zwolle, The Netherlands

    A. E. Braat M.D., J. W. A. Oosterhuis M.D., Ph.D. & J. E. de Vries M.D., Ph.D.

  2. Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands

    R. A. E. M. Tollenaar M.D., Ph.D.

Authors
  1. A. E. Braat M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. W. A. Oosterhuis M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. E. de Vries M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. A. E. M. Tollenaar M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. E. Braat M.D..

About this article

Cite this article

Braat, A., Oosterhuis, J., de Vries, J. et al. Lymphatic Staging in Colorectal Cancer: Pathologic, Molecular, and Sentinel Node Techniques. Dis Colon Rectum 48, 371–383 (2005). https://doi.org/10.1007/s10350-004-0796-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10350-004-0796-4

Key words

Search

Navigation