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Lymphatic spread, nodal count and the extent of lymphadenectomy in cancer of the colon

Published:October 14, 2013DOI:https://doi.org/10.1016/j.ctrv.2013.09.013

      Abstract

      In colon cancer, the biological significance of lymphatic tumour spread remains a matter of debate, which impacts on related questions such as the ideal extent of lymphadenectomy and the prognostic significance of lymph node counts. Several lines of evidence suggest that metastasis to locoregional nodes occurs early and is a stochastic, rather than a stepwise phenomenon, and in essence reflects the tumour–host–metastasis relationship. Not surprisingly, therefore, several clinical trials failed to identify a survival benefit from extensive lymphadenectomy compared to standard resection. The recently described complete mesocolic excision technique, which aims to improve survival by maximizing nodal clearance, should be subjected to a prospective randomized trial.
      There has been a fairly consistent and intriguing relation between nodal counts and survival in colon cancer. Therapeutic effects of more extensive removal of invaded nodes seem an unlikely explanation for the observed association. Similarly, several findings argue against stage migration as the only or even the most important explanation. The available literature shows an extensive array of factors confounding the nodal count–survival relationship, which are correlated to the patient’s clinical characteristics, pathology variables, and factors relating to the individual (treating surgeon and pathologist) and institutional healthcare levels. More research into the biology of nodal spread and the nodal count–survival relationship is indicated and may have important implications for therapy such as the further introduction of minimally invasive surgery and the identification of novel and potentially modifiable factors impacting on both nodal counts and survival.

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      References

        • Jemal A.
        • Bray F.
        • Center M.M.
        • Ferlay J.
        • Ward E.
        • Forman D.
        Global cancer statistics.
        CA Cancer J Clin. 2011; 61: 69-90
      1. Edge S.B. Byrd D.R. Compton C.C. Fritz A.G. Greene F.L. Trotti A. AJCC (American Joint Committee on Cancer) Cancer Staging Manual. 7th ed. Springer, New York2010
        • Hohenberger W.
        • Weber K.
        • Matzel K.
        • Papadopoulos T.
        • Merkel S.
        Standardized surgery for colonic cancer: complete mesocolic excision and central ligation – technical notes and outcome.
        Colorectal Dis. 2009; 11: 354-364
        • Stojadinovic A.
        • Nissan A.
        • Protic M.
        • et al.
        Prospective randomized study comparing sentinel lymph node evaluation with standard pathologic evaluation for the staging of colon carcinoma - Results from the United States military cancer institute clinical trials group study GI-01.
        Ann Surg. 2007; 245: 846-857
        • Klein C.A.
        Parallel progression of primary tumours and metastases.
        Nat Rev Cancer. 2009; 9: 302-312
        • Halsted W.S.
        The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June 1889 to January 1894.
        Ann Surg. 1894; 20: 497-555
        • Mareel M.
        • Oliveira M.J.
        • Madani I.
        Cancer invasion and metastasis: interacting ecosystems.
        Virchows Arch. 2009; 454: 599-622
        • Paget S.
        The distribution of secondary growths in cancer of the breast.
        Lancet. 1889; 1: 571-573
        • Hirakawa S.
        • Kodama S.
        • Kunstfeld R.
        • Kajiya K.
        • Brown L.F.
        • Detmar M.
        VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis.
        J Exp Med. 2005; 201: 1089-1099
      2. Torino F, Bonmassar E, Bonmassar L, et al. Circulating tumor cells in colorectal cancer patients. Cancer Treat Rev 2013;39:759–72

        • Rahbari N.N.
        • Bork U.
        • Motschall E.
        • et al.
        Molecular detection of tumor cells in regional lymph nodes is associated with disease recurrence and poor survival in node-negative colorectal cancer: a systematic review and meta-analysis.
        J Clin Oncol. 2012; 30: 60-70
        • Mescoli C.
        • Albertoni L.
        • Pucciarelli S.
        • et al.
        Isolated tumor cells in regional lymph nodes as relapse predictors in stage I and II colorectal cancer.
        J Clin Oncol. 2012; 30: 965-971
        • Finlay I.G.
        • Meek D.
        • Brunton F.
        • McArcle C.S.
        Growth rate of hepatic metastases in colorectal carcinoma.
        Br J Surg. 1988; 75: 641-644
        • Stoecklein N.H.
        • Klein C.A.
        Genetic disparity between primary tumours, disseminated tumour cells, and manifest metastasis.
        Int J Cancer. 2010; 126: 589-598
        • Suzuki O.
        • Sekishita Y.
        • Shiono T.
        • Ono K.
        • Fujimori M.
        • Kondo S.
        Number of lymph node metastases is better predictor of prognosis than level of lymph node metastasis in patients with node-positive colon cancer.
        J Am Coll Surg. 2006; 202: 732-736
        • Saha S.
        • Johnston G.
        • Korant A.
        • et al.
        Aberrant drainage of sentinel lymph nodes in colon cancer and its impact on staging and extent of operation.
        Am J Surg. 2013; 205: 302-305
        • Bernhoff R.
        • Holm T.
        • Sjovall A.
        • Granath F.
        • Ekbom A.
        • Martling A.
        Increased lymph node harvest in patients operated on for right-sided colon cancer: a population-based study.
        Colorectal Dis. 2012; 14: 691-696
        • Le Voyer T.E.
        • Sigurdson E.R.
        • Hanlon A.L.
        • et al.
        Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089.
        J Clin Oncol. 2003; 21: 2912-2919
        • Swanson R.S.
        • Compton C.C.
        • Stewart A.K.
        • Bland K.I.
        The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined.
        Ann Surg Oncol. 2003; 10: 65-71
        • Chen S.L.
        • Bilchik A.J.
        More extensive nodal dissection improves survival for stages I to III of colon cancer - a population-based study.
        Ann Surg. 2006; 244: 602-610
        • Parsons H.M.
        • Tuttle T.M.
        • Kuntz K.M.
        • Begun J.W.
        • McGovern P.M.
        • Virnig B.A.
        Association between lymph node evaluation for colon cancer and node positivity over the past 20 years.
        JAMA. 2011; 306: 1089-1097
        • Vather R.
        • Sammour T.
        • Kahokehr A.
        • Connolly A.
        • Hill A.
        Lymph node evaluation and long-term survival in stage II and stage III colon cancer: a national study.
        Ann Surg Oncol. 2009; 16: 585-593
        • Feinstein A.R.
        • Sosin D.M.
        • Wells C.K.
        The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer.
        N Engl J Med. 1985; 312: 1604-1608
        • Compton C.C.
        • Fielding L.P.
        • Burgart L.J.
        • et al.
        Prognostic factors in colorectal cancer – college of American pathologists consensus statement 1999.
        Arch Pathol Lab Med. 2000; 124: 979-994
        • Prandi M.
        • Lionetto R.
        • Bini A.
        • et al.
        Prognostic evaluation of stage B colon cancer patients is improved by an adequate lymphadenectomy – results of a secondary analysis of a large scale adjuvant trial.
        Ann Surg. 2002; 235: 458-463
        • Bui L.
        • Rempel E.
        • Reeson D.
        • Simunovic M.
        Lymph node counts, rates of positive lymph nodes, and patient survival for colon cancer surgery in Ontario, Canada: a population-based study.
        J Surg Oncol. 2006; 93: 439-445
        • Wong S.L.
        • Ji H.
        • Hollenbeck B.K.
        • Morris A.M.
        • Baser O.
        • Birkmeyer J.D.
        Hospital lymph node examination rates and survival after resection for colon cancer.
        JAMA. 2007; 298: 2149-2154
        • Baxter N.N.
        • Ricciardi R.
        • Simunovic M.
        • Urbach D.R.
        • Virnig B.A.
        An evaluation of the relationship between lymph node number and staging in pT3 colon cancer using population-based data.
        Dis Colon Rectum. 2010; 53: 65-70
        • Porter G.A.
        • Urquhart R.
        • Bu J.
        • Johnson P.
        • Rayson D.
        • Grunfeld E.
        Improving nodal harvest in colorectal cancer: so what?.
        Ann Surg Oncol. 2012; 19: 1066-1073
        • Berger A.C.
        • Sigurdson E.R.
        • LeVoyer T.
        • et al.
        Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes.
        J Clin Oncol. 2005; 23: 8706-8712
        • Sjo O.H.
        • Merok M.A.
        • Svindland A.
        • Nesbakken A.
        Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer.
        Dis Colon Rectum. 2012; 55: 307-315
        • Hogan N.
        • Winter D.
        A nodal positivity constant: new perspectives in lymph node evaluation and colorectal cancer.
        World J Surg. 2013; 37: 878-882
        • Rouffet F.
        • Hay J.M.
        • Vacher B.
        • et al.
        Curative resection for left colonic carcinoma: hemicolectomy vs. segmental colectomy. A prospective, controlled, multicenter trial. French association for surgical research.
        Dis Colon Rectum. 1994; 37: 651-659
        • Tagliacozzo S.
        • Tocchi A.
        Extended mesenteric excision in right hemicolectomy for carcinoma of the colon.
        Int J Colorectal Dis. 1997; 12: 272-275
        • Tentes A.-A.K.
        • Mirelis C.
        • Karanikiotis C.
        • Korakianitis O.
        Radical lymph node resection of the retroperitoneal area for left-sided colon cancer.
        Langenbecks Arch Surg. 2007; 392: 155-160
        • West N.P.
        • Hohenberger W.
        • Weber K.
        • Perrakis A.
        • Finan P.J.
        • Quirke P.
        Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon.
        J Clin Oncol. 2010; 28: 1763-1769
        • Hashiguchi Y.
        • Hase K.
        • Ueno H.
        • Mochizuki H.
        • Shinto E.
        • Yamamoto J.
        Optimal margins and lymphadenectomy in colonic cancer surgery.
        Br J Surg. 2011; 98: 1171-1178
        • West N.P.
        • Kobayashi H.
        • Takahashi K.
        • et al.
        Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation.
        J Clin Oncol. 2012; 30: 1763-1769
        • Ikeda Y.
        • Shimabukuro R.
        • Saitsu H.
        • Saku M.
        • Maehara Y.
        Influence of prophylactic apical node dissection of the inferior mesenteric artery on prognosis of colorectal cancer.
        Hepatogastroenterology. 2007; 54: 1985-1987
        • Cirocchi R.
        • Trastulli S.
        • Farinella E.
        • et al.
        High tie versus low tie of the inferior mesenteric artery in colorectal cancer: A RCT is needed.
        Surg Oncol. 2012; 21: e111-e123
        • Baxter N.N.
        • Virnig D.J.
        • Rothenberger D.A.
        • Morris A.M.
        • Jessurun J.
        • Virnig B.A.
        Lymph node evaluation in colorectal cancer patients: a population-based study.
        J Natl Cancer Inst. 2005; 97: 219-225
        • Chen S.L.
        • Steele S.R.
        • Eberhardt J.
        • Zhu K.
        • Bilchik A.
        • Stojadinovic A.
        Lymph node ratio as a quality and prognostic indicator in stage III colon cancer.
        Ann Surg. 2011; 253: 82-87
        • Chou J.F.
        • Row D.
        • Gonen M.
        • Liu Y.-H.
        • Schrag D.
        • Weiser M.R.
        Clinical and pathologic factors that predict lymph node yield from surgical specimens in colorectal cancer a population-based study.
        Cancer. 2010; 116: 2560-2570
        • Hsieh M.-C.
        • Velasco C.
        • Wu X.-C.
        • Pareti L.A.
        • Andrews P.A.
        • Chen V.W.
        Influence of socioeconomic status and hospital type on disparities of lymph node evaluation in colon cancer patients.
        Cancer. 2012; 118: 1675-1683
        • Maurel J.
        • Launoy G.
        • Grosclaude P.
        • et al.
        Lymph node harvest reporting in patients with carcinoma of the large bowel – a French population-based study.
        Cancer. 1998; 82: 1482-1486
        • Morris E.J.A.
        • Maughan N.J.
        • Forman D.
        • Quirke P.
        Identifying stage III colorectal cancer patients: the influence of the patient, surgeon, and pathologist.
        J Clin Oncol. 2007; 25: 2573-2579
        • Nash G.M.
        • Row D.
        • Weiss A.
        • et al.
        A predictive model for lymph node yield in colon cancer resection specimens.
        Ann Surg. 2011; 253: 318-322
        • Sarli L.
        • Bader G.
        • Iusco D.
        • et al.
        Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer.
        Eur J Cancer. 2005; 41: 272-279
        • Steele S.R.
        • Chen S.L.
        • Stojadinovic A.
        • et al.
        The impact of age on quality measure adherence in colon cancer.
        J Am Coll Surg. 2011; 213: 95-103
        • Rhoads K.F.
        • Cullen J.
        • Ngo J.V.
        • Wren S.M.
        Racial and ethnic differences in lymph node examination after colon cancer resection do not completely explain disparities in mortality.
        Cancer. 2012; 118: 469-477
        • Nathan H.
        • Shore A.D.
        • Anders R.A.
        • Wick E.C.
        • Gearhart S.L.
        • Pawlik T.M.
        Variation in lymph node assessment after colon cancer resection: patient, surgeon, pathologist, or hospital?.
        J Gastrointest Surg. 2011; 15: 471-479
        • Schofield J.B.
        • Mounter N.A.
        • Mallett R.
        • Haboubi N.Y.
        The importance of accurate pathological assessment of lymph node involvement in colorectal cancer.
        Colorectal Dis. 2006; 8: 460-470
        • Shia J.
        • Wang H.
        • Nash G.M.
        • Klimstra D.S.
        Lymph node draging in colorectal cancer: revisiting the benchmark of at least 12 lymph nodes in R0 resection.
        J Am Coll Surg. 2012; 214: 348-355
        • Tekkis P.P.
        • Smith J.J.
        • Heriot A.G.
        • et al.
        A national study on lymph node retrieval in resectional surgery for colorectal cancer.
        Dis Colon Rectum. 2006; 49: 1673-1683
        • Morikawa T.
        • Tanaka N.
        • Kuchiba A.
        • et al.
        Predictors of lymph node count in colorectal cancer resections data from US nationwide prospective cohort studies.
        Arch Surg. 2012; 147: 715-723
        • McBride R.B.
        • Lebwohl B.
        • Hershman D.L.
        • Neugut A.I.
        Impact of socioeconomic status on extent of lymph node dissection for colon cancer.
        Cancer Epidemiol Biomarkers Prev. 2010; 19: 738-745
        • Cone M.M.
        • Shoop K.M.
        • Rea J.D.
        • Lu K.C.
        • Herzig D.O.
        Ethnicity influences lymph node resection in colon cancer.
        J Gastrointest Surg. 2010; 14: 1752-1757
        • Belt E.J.T.
        • Velde E.A.T.
        • Krijgsman O.
        • et al.
        High lymph node yield is related to microsatellite instability in colon cancer.
        Ann Surg Oncol. 2012; 19: 1222-1230
        • Bilimoria K.Y.
        • Palis B.
        • Stewart A.K.
        • et al.
        Impact of tumor location on nodal evaluation for colon cancer.
        Dis Colon Rectum. 2008; 51: 154-161
        • Snaebjornsson P.
        • Jonasson L.
        • Jonsson T.
        • Moller P.H.
        • Theodors A.
        • Jonasson J.G.
        Colon cancer in Iceland-a nationwide comparative study on various pathology parameters with respect to right and left tumor location and patients age.
        Int J Cancer. 2010; 127: 2645-2653
        • Cucino C.
        • Buchner A.M.
        • Sonnenberg A.
        Continued rightward shift of colorectal cancer.
        Dis Colon Rectum. 2002; 45: 1035-1040
        • George S.
        • Primrose J.
        • Talbot R.
        • et al.
        Will Rogers revisited: prospective observational study of survival of 3592 patients with colorectal cancer according to number of nodes examined by pathologists.
        Br J Cancer. 2006; 95: 841-847
        • Schwitalle Y.
        • Kloor M.
        • Eiermann S.
        • et al.
        Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers.
        Gastroenterology. 2008; 134: 988-997
        • Eveno C.
        • Nemeth J.
        • Soliman H.
        • et al.
        Association between a high number of isolated lymph nodes in T1 to T4 N0M0 colorectal cancer and the microsatellite instability phenotype.
        Arch Surg. 2010; 145: 12-17
        • Soreide K.
        • Nedrebo B.S.
        • Soreide J.A.
        • Slewa A.
        • Korner H.
        Lymph node harvest in colon cancer: influence of microsatellite instability and proximal tumor location.
        World J Surg. 2009; 33: 2695-2703
        • MacQuarrie E.
        • Arnason T.
        • Gruchy J.
        • Yan S.
        • Drucker A.
        • Huang W.
        Microsatellite instability status does not predict total lymph node or negative lymph node retrieval in stage III colon cancer.
        Hum Pathol. 2012; 43: 1258-1264
        • Ogino S.
        • Galon J.
        • Fuchs C.S.
        • Dranoff G.
        Cancer immunology-analysis of host and tumor factors for personalized medicine.
        Nat Rev Clin Oncol. 2011; 8: 711-719
        • Rondelli F.
        • Trastulli S.
        • Avenia N.
        • et al.
        Is laparoscopic right colectomy more effective than open resection? A meta-analysis of randomized and nonrandomized studies.
        Colorectal Dis. 2012; 14: e447-e469
        • Wu Z.
        • Zhang S.
        • Aung L.H.H.
        • Ouyang J.
        • Wei L.
        Lymph node harvested in laparoscopic versus open colorectal cancer approaches: a meta-analysis.
        Surg Laparosc Endosc Percutan Tech. 2012; 22: 5-11
        • Antoniou S.A.
        • Antoniou G.A.
        • Koch O.O.
        • Pointner R.
        • Granderath F.A.
        Robot-assisted laparoscopic surgery of the colon and rectum.
        Surg Endosc. 2012; 26: 1-11
        • Nissan A.
        • Protic M.
        • Bilchik A.J.
        • Howard R.S.
        • Peoples G.E.
        • Stojadinovic A.
        United States military cancer institute clinical trials group (USMCI GI-01) Randomized controlled trial comparing targeted nodal assessment and ultrastaging with standard pathological evaluation for colon cancer.
        Ann Surg. 2012; 256: 412-427
        • van der Pas M.H.G.M.
        • Meijer S.
        • Hoekstra O.S.
        • et al.
        Sentinel-lymph-node procedure in colon and rectal cancer: a systematic review and meta-analysis.
        Lancet Oncol. 2011; 12: 540-550
        • van der Zaag E.S.
        • Bouma W.H.
        • Tanis P.J.
        • Ubbink D.T.
        • Bemelman W.A.
        • Buskens C.J.
        Systematic review of sentinel lymph node mapping procedure in colorectal cancer.
        Ann Surg Oncol. 2012; 19: 3449-3459
        • Hutteman M.
        • Choi H.S.
        • Mieog J.S.D.
        Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light.
        Ann Surg Oncol. 2011; 18: 1006-1014
        • Quirke P.
        • Steele R.
        • Monson J.
        • et al.
        Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG CO16 randomised clinical trial.
        Lancet. 2006; 373: 821-828
        • West N.P.
        • Morris E.J.A.
        • Rotimi O.
        • Cairns A.
        • Finan P.J.
        • Quirke P.
        Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study.
        Lancet Oncol. 2008; 9: 857-865
        • Bertelsen C.A.
        • Bols B.
        • Ingeholm P.
        • Jansen J.E.
        • Neuenschwander A.U.
        • Vilandt J.
        Can the quality of colonic surgery be improved by standardization of surgical technique with complete mesocolic excision?.
        Colorectal Dis. 2011; 13: 1123-1129
        • Hogan A.M.
        • Winter D.C.
        Complete mesocolic excision (CME): a “novel” concept?.
        J Surg Oncol. 2009; 100: 182-183
        • Shen S.S.
        • Haupt B.X.
        • Ro J.Y.
        • Zhu J.
        • Bailey H.R.
        • Schwartz M.R.
        Number of lymph nodes examined and associated clinicopathologic factors in colorectal carcinoma.
        Arch Pathol Lab Med. 2009; 133: 781-786
        • Jakub J.W.
        • Russell G.
        • Tillman C.L.
        • Lariscy C.
        Colon cancer and low lymph node count who is to blame?.
        Arch Surg. 2009; 144: 1115-1120
        • Barbas A.
        • Turley R.
        • Mantyh C.
        • Migaly J.
        Advanced fellowship training is associated with improved lymph node retrieval in colon cancer resections.
        J Surg Res. 2011; 170: e41-e46
        • Bilimoria K.Y.
        • Bentrem D.J.
        • Stewart A.K.
        • et al.
        Lymph node evaluation as a colon cancer quality measure: a national hospital report card.
        J Natl Cancer Inst. 2008; 100: 1310-1317
        • Miller E.A.
        • Woosley J.
        • Martin C.F.
        • Sandler R.S.
        Hospital-to-hospital variation in lymph node detection after colorectal resection.
        Cancer. 2004; 101: 1065-1071
        • Wright F.C.
        • Law C.H.L.
        • Last L.
        • et al.
        Lymph node retrieval and assessment in stage II colorectal cancer: A population-based study.
        Ann Surg Oncol. 2003; 10: 903-909
        • Elferink M.A.G.
        • Siesling S.
        • Visser O.
        • et al.
        Large variation between hospitals and pathology laboratories in lymph node evaluation in colon cancer and its impact on survival, a nationwide population-based study in The Netherlands.
        Ann Oncol. 2011; 22: 110-117
        • Rajput A.
        • Romanus D.
        • Weiser M.R.
        • et al.
        Meeting the 12 lymph node (LN) benchmark in colon cancer.
        J Surg Oncol. 2010; 102: 3-9
        • Senthil M.
        • Trisal V.
        • Paz I.B.
        • Lai L.L.
        Prediction of the Adequacy of lymph node retrieval in colon cancer by hospital type.
        Arch Surg. 2010; 145: 840-843
        • Lemmens V.E.
        • van Lijnschoten I.
        • Janssen-Heijnen M.L.
        • Rutten H.J.
        • Verheij C.D.
        • Coebergh J.W.W.
        Pathology practice patterns affect lymph node evaluation and outcome of colon cancer: a population-based study.
        Ann Oncol. 2006; 17: 1803-1809
        • Choi H.K.
        • Law W.L.
        • Poon J.T.C.
        The optimal number of lymph nodes examined in stage II colorectal cancer and its impact of on outcomes.
        BMC Cancer. 2010; 10: 267
        • Scott K.W.M.
        • Grace R.H.
        Detection of lymph node metastases in colorectal carcinoma before and after fat clearance.
        Br J Surg. 1989; 76: 1165-1167
        • Brown H.G.
        • Luckasevic T.M.
        • Medich D.S.
        • Celebrezze J.P.
        • Jones S.M.
        Efficacy of manual dissection of lymph nodes in colon cancer resections.
        Mod Pathol. 2004; 17: 402-406
        • Maerkl B.
        • Kerwel T.G.
        • Jaehnig H.G.
        • et al.
        Methylene blue-assisted lymph node dissection in colon specimens.
        Am J Clin Pathol. 2008; 130: 913-919
        • Iversen L.H.
        • Laurberg S.
        • Hagemann-Madsen R.
        • Dybdahl H.
        Increased lymph node harvest from colorectal cancer resections using GEWF solution: a randomised study.
        J Clin Pathol. 2008; 61: 1203-1208
        • Dawson K.
        • Wiebusch A.
        • Thirlby R.C.
        Preoperative tattooing and improved lymph node retrieval rates from colectomy specimens in patients with colorectal cancers.
        Arch Surg. 2010; 145: 826-830
        • Johnson P.M.
        • Malatjalian D.
        • Porter G.A.
        Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study.
        J Gastrointest Surg. 2002; 6: 883-888
        • Galvis C.O.
        • Raab S.S.
        • D’Amico F.
        • Grzybicki D.M.
        Pathologists’ assistants practice: a measurement of performance.
        Am J Clin Pathol. 2001; 116: 816-822
        • Ostadi M.A.
        • Harnish J.L.
        • Stegienko S.
        • Urbach D.R.
        Factors affecting the number of lymph nodes retrieved in colorectal cancer specimens.
        Surg Endosc. 2007; 21: 2142-2146
        • Bull A.D.
        • Biffin A.H.B.
        • Mella J.
        • et al.
        Colorectal cancer pathology reporting: a regional audit.
        J Clin Pathol. 1997; 50: 138-142
        • Jestin P.
        • Pahlman L.
        • Glimelius B.
        • Gunnarsson U.
        Cancer staging and survival in colon cancer is dependent on the quality of the pathologists’ specimen examination.
        Eur J Cancer. 2005; 41: 2071-2078
        • Rieger N.A.
        • Barnett F.S.
        • Moore J.W.E.
        • et al.
        Quality of pathology reporting impacts on lymph node yield in colon cancer.
        J Clin Oncol. 2007; 25: 463
        • Baxter N.N.
        Is lymph node count an ideal quality indicator for cancer care?.
        J Surg Oncol. 2009; 99: 265-268
        • West N.
        Commentary: lymph node retrieval in colorectal cancer specimens: National standards are achievable, and low numbers are associated with reduced survival.
        Colorectal Dis. 2010; 12: 309-311