Oncology| Volume 158, ISSUE 3, P692-699, September 2015

Opportunity lost: Adjuvant chemotherapy in patients with stage III colon cancer remains underused


      There is strong evidence supporting the efficacy of adjuvant chemotherapy for patients with pathologic, stage III colon cancer. This study examines differences in adherence to evidence-based adjuvant chemotherapy guidelines for pathologic, stage III colon cancer cases across hospital and patient subgroups.


      Patients with stage III colon cancer were identified from the 2003 to 2011 National Cancer Data Base (NCDB). A logistic regression model was used to estimate the odds of receipt of adjuvant chemotherapy across varying hospital and patient characteristics. A multivariable Cox proportional hazards model was used to estimate the association between receipt of adjuvant chemotherapy and 5-year survival. Risk adjusted observed/expected (O/E) outcome ratios were calculated for each hospital to compare hospital-specific quality of care during the study period.


      A total of 124,008 patients met the inclusion criteria. Adjuvant chemotherapy was not administered to 34%. The rates of adjuvant chemotherapy have shown little improvement over time (63% in 2003 vs 66% in 2011). The Cox model indicates that patients receiving adjuvant chemotherapy had better survival (hazard ratio = 0.48, 95% confidence interval 0.47–0.49). Analysis of risk adjusted O/E ratios indicated no consistent pattern as to which hospitals were performing optimally or subopitmally over time.


      There has been no meaningful improvement in receipt of chemotherapy in patients with stage III colon cancer. The fact that chemotherapy is not being considered or offered to more than 20% of patients with node-positive colon cancer suggests that there are substantial process failures across many institutions and regions in the United States.
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        • Benson 3rd, A.B.
        • Schrag D.
        • Somerfield M.R.
        • et al.
        American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer.
        J Clin Oncol. 2004; 22: 3408-3419
        • Engstrom P.F.
        • Benson 3rd, A.B.
        • Saltz L.
        Colon cancer clinical practice guidelines in oncology.
        J Natl Compr Cancer Netw. 2003; 1: 40-53
      1. National Comprehensive Cancer Network. Available at: Accessed March 16, 2005.

        • Moertel C.G.
        • Fleming T.R.
        • Macdonald J.S.
        • et al.
        Levamisole and fluorouracil for adjuvant therapy of resected colon carcinoma.
        N Engl J Med. 1990; 322: 352-358
        • Andre T.
        • Boni C.
        • Mounedji-Boudiaf L.
        • et al.
        Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer.
        N Engl J Med. 2004; 350: 2343-2351
        • Moertel C.G.
        • Fleming T.R.
        • Macdonald J.S.
        • et al.
        Fluorouracil plus levamisole as effective adjuvant therapy after resection of stage III colon carcinoma: a final report.
        Ann Intern Med. 1995; 122: 321-326
        • Spinks T.
        • Albright H.W.
        • Feeley T.W.
        • et al.
        Ensuring quality cancer care: a follow-up review of the Institute of Medicine's 10 recommendations for improving the quality of cancer care in America.
        Cancer. 2012; 118: 2571-2582
        • Chagpar R.
        • Xing Y.
        • Chiang Y.J.
        • et al.
        Adherence to stage-specific treatment guidelines for patients with colon cancer.
        J Clin Oncol. 2012; 30: 972-979
        • Muss H.B.
        • Bynum D.L.
        Adjuvant chemotherapy in older patients with stage III colon cancer: an underused lifesaving treatment.
        J Clin Oncol. 2012; 30: 2576-2578
        • Schrag D.
        • Cramer L.D.
        • Bach P.B.
        • Begg C.B.
        Age and adjuvant chemotherapy use after surgery for stage III colon cancer.
        J Natl Cancer Inst. 2001; 93: 850-857
      2. National Comprehensive Cancer Network: NCCN Clinical Practice Guidelines in Oncology: Colon Cancer. Accessed May 13, 2015.

        • Meyerhardt J.A.
        • Mangu P.B.
        • Flynn P.J.
        • et al.
        Follow-up care, surveillance protocol, and secondary prevention measures for survivors of colorectal cancer: American Society of Clinical Oncology clinical practice guideline endorsement.
        J Clin Oncol. 2013; 31: 4465-4470
        • Boland G.M.
        • Chang G.J.
        • Haynes A.B.
        • et al.
        Association between adherence to National Comprehensive Cancer Network treatment guidelines and improved survival in patients with colon cancer.
        Cancer. 2013; 119: 1593-1601
        • Wolmark N.
        • Wieand H.S.
        • Hyams D.M.
        • et al.
        Randomized trial of postoperative adjuvant chemotherapy with or without radiotherapy for carcinoma of the rectum: National Surgical Adjuvant Breast and Bowel Project Protocol R-02.
        J Natl Cancer Inst. 2000; 92: 388
        • Bilimoria K.Y.
        • Stewart A.K.
        • Winchester D.P.
        • et al.
        The National Cancer Data Base: a powerful initiative to improve cancer care in the United States.
        Ann Surg Oncol. 2008; 15: 683-690
        • Winchester D.P.
        • Stewart A.K.
        • Phillips J.L.
        • et al.
        The national cancer data base: past, present, and future.
        Ann Surg Oncol. 2010; 17: 4-7
      3. American College of Surgeons. Facility Oncology Registry Data Standards: December 18, 2012. Available at: Accessed May 13, 2015.

        • Deyo R.A.
        • Cherkin D.C.
        • Ciol M.A.
        Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases.
        J Clin Epidemiol. 1992; 45: 613-619
        • Mack C.D.
        • Carpenter W.
        • Meyer A.M.
        • Sanoff H.
        • Stürmer T.
        Racial disparities in receipt and comparative effectiveness of oxaliplatin for stage III colon cancer in older adults.
        Cancer. 2012; 118: 2925-2934
        • Haas J.S.
        • Brawarsky P.
        • Iyer A.
        • Fitzmaurice G.M.
        • Neville B.A.
        • Earle C.
        Association of area sociodemographic characteristics and capacity for treatment with disparities in colorectal cancer care and mortality.
        Cancer. 2011; 117: 4267-4276
        • Potosky A.L.
        • Harlan L.C.
        • Kaplan R.S.
        • et al.
        Age, sex, and racial differences in the use of standard adjuvant therapy for colorectal cancer.
        J Clin Oncol. 2002; 20: 1192-1202
        • Gorey K.M.
        • Haji-Jama S.
        • Bartfay E.
        • Luginaah I.N.
        • Wright F.C.
        • Kanjeekal S.M.
        Lack of access to chemotherapy for colon cancer: multiplicative disadvantage of being extremely poor, inadequately insured and African American.
        BMC Health Serv Res. 2014; 14: 133
        • Landrum M.B.
        • Keating N.L.
        • Lamont E.B.
        • Bozeman S.R.
        • McNeil B.J.
        Reasons for underuse of recommended therapies for colorectal and lung cancer in the Veterans Health Administration.
        Cancer. 2012; 118: 3345-3355
        • El Shayeb M.
        • Scarfe A.
        • Yasui Y.
        • Winget M.
        Reasons physicians do not recommend and patients refuse adjuvant chemotherapy for stage III colon cancer: a population based chart review.
        BMC Res Notes. 2012; 5: 269
        • André T.
        • Boni C.
        • Navarro M.
        • et al.
        Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial.
        J Clin Oncol. 2009; 27: 3109-3116
        • Obias V.J.
        • Reynolds H.L.
        Multidisciplinary teams in the management of rectal cancer.
        Clin Colon Rectal Surg. 2007; 20: 143-147
        • Davies A.R.
        • Deans D.A.
        • Penman I.
        • et al.
        The multidisciplinary team meeting improves staging accuracy and treatment selection for gastro-esophageal cancer.
        Dis Esophagus. 2006; 19: 496-503
        • Taylor C.
        • Munro A.J.
        • Glynne-Jones R.
        • Griffiths C.
        • Trevatt P.
        • Richards M.A.
        • et al.
        Multidisciplinary team working in cancer: where are we now?.
        BMJ. 2010; 340: c951
        • Lamb B.
        • Brown K.
        • Nagpal K.
        • Vincent C.
        • Green J.S.A.
        • Sevdalis N.
        Team decision making by cancer care multidisciplinary teams: a systematic review.
        Ann Surg Oncol. 2011; 18: 2116-2125
        • Lindskog E.B.
        • Gunnarsdóttir K.Á.
        • Derwinger K.
        • Wettergren Y.
        • Glimelius B.
        • Kodeda K.
        A population-based cohort study on adherence to practice guidelines for adjuvant chemotherapy in colorectal cancer.
        BMC Cancer. 2014; 14: 948
        • MacDermid E.
        • Hooton G.
        • MacDonald M.
        • McKay G.
        • Grose D.
        • Mohammed N.
        • et al.
        Improving patient survival with the colorectal cancer multi-disciplinary team.
        Colorectal Dis. 2009; 11: 291-295
        • Freund K.M.
        • Battaglia T.A.
        • Calhoun E.
        • et al.
        Impact of patient navigation on timely cancer care: the Patient Navigation Research Program.
        J Natl Cancer Inst. 2014; 106: dju115
        • Ko N.Y.
        • Darnell J.S.
        • Calhoun E.
        • et al.
        Can patient navigation improve receipt of recommended breast cancer care? Evidence from the National Patient Navigation Research Program.
        J Clin Oncol. 2014; 32: 2758-2764
        • Vincent C.A.
        Patient safety.
        Elsevier Churchill Livingstone, Edinburgh2006
        • Stump S.
        Re-engineering the medication error-reporting process: removing the blame and improving the system.
        Am J Health Syst Pharm. 2000; 57: S10-S17
        • Bonnabry P.
        • Despont-Gros C.
        • Grauser D.
        • Casez P.
        • Despond M.
        • Pugin D.
        • et al.
        A risk analysis method to evaluate the impact of a computerized provider order entry system on patient safety.
        J Am Med Inform Assoc. 2008; 15: 453-460