Research Article| Volume 36, SUPPLEMENT 1, S64-S73, September 2010

Download started.


Disparities in quality of care for colon cancer between hospitals in the Netherlands



      Aim of this study was to describe treatment patterns and outcome according to region, and according to hospital types and volumes among patients with colon cancer in the Netherlands.


      All patients with invasive colon carcinoma diagnosed in the period 2001–2006 were selected from the Netherlands Cancer Registry. Logistic regression analyses were performed to examine the influence of relevant factors on the odds of having adequate lymph node evaluation, receiving adjuvant chemotherapy and postoperative mortality. Relative survival analysis was used to estimate relative excess risk of dying according to hospital type and volume.


      In total, 39 907 patients were selected. Patients diagnosed in a university hospital had a higher odds (OR 2.47; 95% CI 2.19–2.78) and patients diagnosed in a hospital with >100 colon carcinoma diagnoses annually had a lower odds (OR 0.70; 95% CI 0.64–0.77) of having ≥10 lymph nodes evaluated. The odds of receiving adjuvant chemotherapy was lower in patients diagnosed in teaching hospitals (OR 0.85; 95% CI 0.73–0.98) and university hospitals (OR 0.56; 95% CI 0.45–0.70) compared to patients diagnosed in non-teaching hospitals. Funnel plots showed large variation in these two outcome measures between individual hospitals. No differences in postoperative mortality were found between hospital types or volumes. Patients diagnosed in university hospitals and patients diagnosed in hospitals with >50 diagnoses of colon carcinoma per year had a better survival.


      Variation in treatment and outcome of patients with colon cancer in the Netherlands was revealed, with differences between hospital types and volumes. However, variation seemed mainly based on the level of the individual hospital.


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to European Journal of Surgical Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Hewitt M.
        • Simone J.
        Ensuring quality cancer care.
        National Academy Press, Washington DC1999
        • Birkmeyer J.D.
        • Siewers A.E.
        • Finlayson E.V.
        • et al.
        Hospital volume and surgical mortality in the United States.
        N Engl J Med. 2002; 346: 1128-1137
        • Birkmeyer J.D.
        • Stukel T.A.
        • Siewers A.E.
        • Goodney P.P.
        • Wennberg D.E.
        • Lucas F.L.
        Surgeon volume and operative mortality in the United States.
        N Engl J Med. 2003; 349: 2117-2127
        • Chowdhury M.M.
        • Dagash H.
        • Pierro A.
        A systematic review of the impact of volume of surgery and specialization on patient outcome.
        Br J Surg. 2007; 94: 145-161
      1. Comprehensive Cancer Centres. <> [accessed 18.5.2009].

      2. Statistics Netherlands. <> [accessed 3.5.2009].

        • Benson III, 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
        • 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
        • Johnson P.M.
        • Porter G.A.
        • Ricciardi R.
        • Baxter N.N.
        Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer.
        J Clin Oncol. 2006; 24: 3570-3575
      3. National Working Group on Gastrointestinal Cancers. Guideline: colon cancer, <> [accessed 16.10.2009].

        • Lemmens V.E.
        • van Lijnschoten I.
        • Janssen-Heijnen M.L.
        • Rutten H.J.
        • Verheij C.D.
        • Coebergh J.W.
        Pathology practice patterns affect lymph node evaluation and outcome of colon cancer: a population-based study.
        Ann Oncol. 2006; 17: 1803-1809
        • Van Steenbergen L.N.
        • Rutten H.J.
        • Creemers G.J.
        • Pruijt J.F.
        • Coebergh J.W.
        • Lemmens V.E.
        Large age and hospital-dependent variation in administration of adjuvant chemotherapy for stage III colon cancer in southern Netherlands.
        Ann Oncol. 2010; 21: 1273-1278
        • Chaudhry R.
        • Goel V.
        • Sawka C.
        Breast cancer survival by teaching status of the initial treating hospital.
        CMAJ. 2001; 164: 183-188
        • Cheung M.C.
        • Hamilton K.
        • Sherman R.
        • et al.
        Impact of teaching facility status and high-volume centers on outcomes for lung cancer resection: an examination of 13,469 surgical patients.
        Ann Surg Oncol. 2009; 16: 3-13
        • Holm T.
        • Johansson H.
        • Cedermark B.
        • Ekelund G.
        • Rutqvist L.E.
        Influence of hospital- and surgeon-related factors on outcome after treatment of rectal cancer with or without preoperative radiotherapy.
        Br J Surg. 1997; 84: 657-663
        • Begg C.B.
        • Cramer L.D.
        • Hoskins W.J.
        • Brennan M.F.
        Impact of hospital volume on operative mortality for major cancer surgery.
        J Am Med Assoc. 1998; 280: 1747-1751
        • Halm E.A.
        • Lee C.
        • Chassin M.R.
        Is volume related to outcome in health care? A systematic review and methodologic critique of the literature.
        Ann Intern Med. 2002; 137: 511-520
        • Simunovic M.
        • Rempel E.
        • Theriault M.E.
        • et al.
        Influence of hospital characteristics on operative death and survival of patients after major cancer surgery in Ontario.
        Can J Surg. 2006; 49: 251-258
        • Parry J.M.
        • Collins S.
        • Mathers J.
        • Scott N.A.
        • Woodman C.B.
        Influence of volume of work on the outcome of treatment for patients with colorectal cancer.
        Br J Surg. 1999; 86: 475-481
        • Harmon J.W.
        • Tang D.G.
        • Gordon T.A.
        • et al.
        Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection.
        Ann Surg. 1999; 230: 404-411
        • Hannan E.L.
        • Radzyner M.
        • Rubin D.
        • Dougherty J.
        • Brennan M.F.
        The influence of hospital and surgeon volume on in-hospital mortality for colectomy, gastrectomy, and lung lobectomy in patients with cancer.
        Surgery. 2002; 131: 6-15
        • Finlayson E.V.
        • Goodney P.P.
        • Birkmeyer J.D.
        Hospital volume and operative mortality in cancer surgery: a national study.
        Arch Surg. 2003; 138: 721-725
        • Dimick J.B.
        • Cowan Jr., J.A.
        • Upchurch Jr., G.R.
        • Colletti L.M.
        Hospital volume and surgical outcomes for elderly patients with colorectal cancer in the United States.
        J Surg Res. 2003; 114: 50-56
        • Blomqvist P.
        • Ekbom A.
        • Nyren O.
        • Krusemo U.
        • Bergstrom R.
        • Adami H.O.
        Survival after colon cancer 1973–1990 in Sweden. Convergence between catchment areas.
        Ann Surg. 1997; 225: 208-216
        • Visser O.
        • Coebergh J.W.W.
        • Van Dijck J.A.A.M.
        • Siesling S.
        Incidence of cancer in the Netherlands 1998.
        Vereniging van Integrale Kankercentra, Utrecht2002
      4. Fritz A. Percy C. Jack A. International classification of diseases for oncology. 3rd ed. WHO, Geneva2000
      5. Wittekind C. Greene F.L. Hutter R.V.P. Klimpfinger M. Sobin L.H. TNM atlas. Springer-Verlag, Berlin2004
        • Schouten L.J.
        • Jager J.J.
        • van den Brandt P.A.
        Quality of cancer registry data: a comparison of data provided by clinicians with those of registration personnel.
        Br J Cancer. 1993; 68: 974-977
        • Schouten L.J.
        • Hoppener P.
        • van den Brandt P.A.
        • Knottnerus J.A.
        • Jager J.J.
        Completeness of cancer registration in Limburg, The Netherlands.
        Int J Epidemiol. 1993; 22: 369-376
        • Agresti A.
        • Coul B.A.
        Approximate is better than “exact” for interval estimation of binomial proportions.
        Am Stat. 1998; 52: 119-126
        • Spiegelhalter D.J.
        Funnel plots for comparing institutional performance.
        Stat Med. 2005; 24: 1185-1202
        • Ederer F.
        • Heise H.
        Instructions to IBM 650 programmers in processing survival computations.
        National Cancer Institute, Bethesda, MD1959
        • 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
        • Bouhier K.
        • Maurel J.
        • Lefevre H.
        • Bouin M.
        • Arsene D.
        • Launoy G.
        Changing practices for diagnosis and treatment of colorectal cancer in Calvados: 1990–1999.
        Gastroenterol Clin Biol. 2004; 28: 371-376
        • Wright F.C.
        • Law C.H.
        • 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
        • 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
        • 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
        • Ayanian J.Z.
        • Zaslavsky A.M.
        • Fuchs C.S.
        • et al.
        Use of adjuvant chemotherapy and radiation therapy for colorectal cancer in a population-based cohort.
        J Clin Oncol. 2003; 21: 1293-1300
        • Kohne C.H.
        • Grothey A.
        • Bokemeyer C.
        • Bontke N.
        • Aapro M.
        Chemotherapy in elderly patients with colorectal cancer.
        Ann Oncol. 2001; 12: 435-442
        • Lemmens V.E.
        • van Halteren A.H.
        • Janssen-Heijnen M.L.
        • Vreugdenhil G.
        • Repelaer van Driel O.J.
        • Coebergh J.W.
        Adjuvant treatment for elderly patients with stage III colon cancer in the southern Netherlands is affected by socioeconomic status, gender, and comorbidity.
        Ann Oncol. 2005; 16: 767-772
        • Luo R.
        • Giordano S.H.
        • Zhang D.D.
        • Freeman J.
        • Goodwin J.S.
        The role of the surgeon in whether patients with lymph node-positive colon cancer see a medical oncologist.
        Cancer. 2007; 109: 975-982
      6. Surgery for colorectal cancer in elderly patients: a systematic review.
        Lancet. 2000; 356 (Colorectal Cancer Collaborative Group): 968-974
        • Koruda M.J.
        • Sheldon G.F.
        Surgery in the aged.
        Adv Surg. 1991; 24: 293-331
        • Engel A.F.
        • Oomen J.L.
        • Knol D.L.
        • Cuesta M.A.
        Operative mortality after colorectal resection in the Netherlands.
        Br J Surg. 2005; 92: 1526-1532
        • Wouters M.W.
        • Wijnhoven B.P.
        • Karim-Kos H.E.
        • et al.
        High-volume versus low-volume for esophageal resections for cancer: the essential role of case-mix adjustments based on clinical data.
        Ann Surg Oncol. 2008; 15: 80-87
        • Meyerhardt J.A.
        • Catalano P.J.
        • Schrag D.
        • et al.
        Association of hospital procedure volume and outcomes in patients with colon cancer at high risk for recurrence.
        Ann Intern Med. 2003; 139: 649-657
        • Schrag D.
        • Panageas K.S.
        • Riedel E.
        • et al.
        Surgeon volume compared to hospital volume as a predictor of outcome following primary colon cancer resection.
        J Surg Oncol. 2003; 83: 68-78