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Journal of Clinical Oncology, Vol 25, No 18 (June 20), 2007: pp. 2573-2579 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.11.0445 Identifying Stage III Colorectal Cancer Patients: The Influence of the Patient, Surgeon, and Pathologist
From the Cancer Epidemiology Group, Centre for Epidemiology and Biostatistics, University of Leeds; Pathology and Tumour Biology, Leeds Institute for Molecular Medicine, University of Leeds, St James's University Hospital; and the Northern and Yorkshire Cancer Registry and Information Service, Cookridge Hospital, Leeds, United Kingdom Address reprint requests to Eva Judith Ann Morris, BSc, PhD, Arthington House, Cookridge Hospital, Leeds, United Kingdom LS16 6QB; e-mail: eva.morris{at}nycris.leedsth.nhs.uk
Purpose: Nodal yields from resected colorectal cancers vary greatly. This study sought to determine what patient, tumor, and management factors influence the number of nodes retrieved and to determine if the extent of lymphadenectomy affects stage allocation and influences survival. Patients and Methods: Retrospective study of the nodal yields of 7,062 surgically resected colorectal cancer patients for whom colorectal pathology minimum data sets had been collected. The percentage of patients diagnosed as stage III was compared across nodal yield categories. A threshold for an adequate lymphadenectomy was defined as retrieval of 12 nodes. Binary logistic regression was used to determine factors associated with obtaining an adequate lymphadenectomy. Results: Median nodal yields increased over the study period from 7 (interquartile range [IQR], 4 to 11) in 1995 to 13 (IQR 8 to 19) in 2003. There was no difference in yield by cancer site or sex, but yields were lower in older patients. Yields increased with increasing local invasion and stage of tumor. The percentage of patients diagnosed as stage III increased as yields increased. Five-year survival was lower in those patients who did not have an adequate lymphadenectomy. Adequate lymphadenectomy was significantly more likely in patients with advanced tumors and when the surgery and pathology was undertaken by a specialist. Older patients were significantly less likely to receive an adequate lymphadenectomy. Conclusion: Variations in nodal yield are due to idiosyncratic patient and tumor characteristics and differences in the quality of surgery and pathology undertaken. Adequate lymphadenectomy is essential to ensure correct stage allocation and optimal survival.
Methods of treatment in colorectal cancer are determined by stage of disease. Adjuvant chemotherapy is showing increasing benefit in node-positive cases, and with improvements in survival resulting from new combinations of drugs,1 it is essential that such cases are identified. Therefore, correct classification of nodal status is important to ensure patients are given the optimal treatment for their stage of disease. The Royal College of Pathologists (London, United Kingdom) recommends that all lymph nodes draining the lymphatic field of a colorectal cancer should be harvested for histological assessment.2 However, the number of lymph nodes retrieved from resection specimens is highly variable.3-5 This is important as it has been demonstrated that the prognosis of patients from whom only a small number of lymph nodes are identified is worse than those from whom many are retrieved.6-14 This may be because lymph node metastases go unidentified in patients in whom only a small number of nodes are retrieved leading to possible understaging and, consequently, inappropriate treatment. A number of potential explanations could account for these reported differences in yield. Yield may vary due to patient factors. Studies have shown that the number and size of lymph nodes may differ in relation to age, sex, and body mass index.15-18 Tumor characteristics also are influential with variations in yield according to the size, stage, and grade of disease.5,16,19 Likewise, patients who have undergone neoadjuvant treatments may possess fewer or smaller lymph nodes.20 Therefore, there is a natural and an iatrogenic variation in the number of lymph nodes that can be identified across a population, but the evidence available to quantify this variation, as yet, is incomplete. Other factors outside this idiosyncratic variation also may be influential in determining yield, and these may be within the control of the managing medical team. For example, a few studies have demonstrated that the quality of the surgical resection and pathological examination may influence yield.3-5,21 There is a suggestion that improving the quality of care may ensure more complete lymphadenectomies, better staging, and, ultimately, better disease management. The quality of other aspects of colorectal cancer care also have been shown to be variable.15,22-23 These differences are believed to account for substantial variations in survival, and as a result, the National Health Service (NHS) in the United Kingdom has undertaken extensive reform of its colorectal cancer services with a view to ensure high-quality cancer care for all. The reforms consisted of centralizing care into the hands of site-specialist multidisciplinary teams (MDTs)24-25 in the belief that specialists in each discipline would provide a higher standard of management and improve outcomes. One area specifically highlighted in the guidance was the importance of adequate lymphadenectomy. Since 1995, pathologists have been submitting colorectal cancer pathology minimum data sets for resected tumors to the Northern and Yorkshire Cancer Registry and Information Service (NYCRIS). Details of the extent of lymphadenectomy are included in these reports. This study aims to use this information to investigate three issues: (1) to identify the relative importance of patient, tumor, and management factors on lymph node yield; (2) to determine the impact of the formation of MDTs of surgeons and pathologists on the extent and thoroughness of lymphadenectomy in colorectal cancer patients; and (3) to investigate the effect of node yield on the stage distribution of the population.
All colorectal cancer patients for whom a NYCRIS minimum pathology data set26 was completed and submitted to the registry between 1995 and 2003 were identified. Routinely recorded information about these patients’ disease and its management were then downloaded from the main registry database and the two data sets were merged. The operating surgeon and reporting pathologist were identified for each tumor. Surgeons and pathologists were then assigned to be team or nonteam members according to the results of the National Cancer Peer Review process. This review has been undertaken by the UK Department of Health to assess the compliance of hospital cancer services to nationally agreed standards.27 One of these standards specified that specialist surgeons and pathologists should oversee the management of colorectal cancer patients. Specialist MDT surgeons are expected to annually resect a minimum of 20 colorectal tumors, whereas specialist MDT pathologists must report on the majority of colorectal cancer specimens in their hospital. Both should routinely attend MDT meetings to discuss the optimal management of each patient. The median number of nodes examined was assessed in relation to differences in patient and management characteristics. Medians were compared using the Mann-Whitney, Wilcoxon rank sum and the Kruskall-Wallis tests. Based on the literature, the threshold for an adequate lymph node evaluation was set at 12 nodes,19 and patients categorized as receiving adequate and inadequate evaluations. Follow-up for patients diagnosed before 2001 extended to 5 years, so the survival of these patients was examined in relation to the adequacy of the lymphadenectomy. Kaplan-Meier survival graphs were plotted with this grouping comparing the 5-year survival of all node-negative and node-positive patients. Log-rank tests were used to assess whether survival differences were statistically significant. A binary logistic regression model was then created with adequacy of lymphadenectomy as the dependent variable. Less than 12 nodes examined was coded as 0, and the retrieval of 12 or more nodes was coded as 1. Covariates included age, sex, year of diagnosis, cancer site, stage, maximum tumor diameter, local invasion, and the designation of the surgeon and pathologist as a team member.
Between 1995 and 2003 minimum prognostic data sets for 9,041 colorectal patients with single tumors were submitted to NYCRIS. The number of nodes retrieved was not recorded on 129 (1.4%) of these forms, and these cases were excluded. The majority of these forms (69.1%) were completed by nonspecialist pathologists. In addition, we excluded 39 patients (0.4%) who did not have a radical resection, 594 (6.6%) who received neoadjuvant therapy, and 1,217 (13.5%) who had distant metastases, leaving a study population of 7,062. Survival was assessed on 5,556 patients for whom we had at least 5 years’ follow-up (ie, diagnosed before 2001). Characteristics of the population and the median number of nodes retrieved in relation to these characteristics are presented in Table 1. The overall median was 10 nodes (interquartile range [IQR] 6 to 15). The median yield was seen to increase over time from 7 (IQR 4 to 11) in 1995 to 13 (IQR 8 to 19) in 2003. There was no difference in the median number of nodes retrieved by cancer site or by sex. Age was related to the number of lymph nodes found with increasing age being associated with a declining number of nodes identified. Lymph node yields were higher in patients with more advanced local invasion. For example, T1 tumors had a median yield of 6 nodes (IQR, 4 to 10) compared with a median yield of 11 nodes (IQR, 7 to 17) in T4 tumors. Similarly, the median lymph node yield increased with stage from 7 nodes (IQR, 4 to 11) for stage I compared with 11 nodes (IQR, 8 to 17) for stage III tumors.
To investigate how the extent of lymphadenectomy affected the staging of the population, the percentage of patients diagnosed as stage III in relation to the number of nodes retrieved was investigated (Fig 1). In patients with only one to three nodes examined, the percentage diagnosed as node-positive was 20.5%, but when more than 15 nodes were retrieved, this proportion increased to 46.4%.
When the definition for an adequate lymphadenectomy was set at 12 nodes, 41.7% of the population received an acceptable nodal assessment. The proportions of patients according to stage who received an adequate lymphadenectomy according to this standard are shown in Figure 2. Over the study period, the overall percentage of patients receiving adequate assessment increased year over year from 19.8% in 1995 to 56.6% in 2003. In all years, however, the proportion of patients receiving an adequate lymph node assessment was greatest in the higher stage patients. Even in 2003, only 35.7% of stage I patients obtained an adequate lymphadenectomy according to the 12-node standard.
Figure 3 shows the survival difference between patients who did or did not receive a lymphadenectomy of at least 12 nodes. Across all patients, there was a 5.5% 5-year survival difference between those who did or did not receive an adequate lymphadenectomy—53.4% (95% CI, 51.7% to 55.0%) versus 58.8% (95% CI, 56.8% to 61.0%; P < .001). This effect also was consistent across both the node-positive and node-negative population, with a 5.0% (P < .001) and 7.0% (P < .001) difference in 5-year survival, respectively.
The results of the model assessing the odds of an adequate lymph node resection in relation to patient, tumor, and management factors are presented in Table 2. Increasing age was associated with a 2% decrease per year in the odds of retrieving at least 12 lymph nodes. Females had an increase of 19% in the odds of having an adequate lymphadenectomy when compared with males. The odds also were significantly increased for larger and more advanced tumors and those in whom positive nodes were identified. Management factors also were significantly related to the odds of an adequate lymphadenectomy. MDT surgeons offered a 40% increase in the odds of retrieving at least 12 nodes (odds ratio [OR], 1.40; 95% CI, 1.24 to 1.58), whereas the odds for MDT pathologists was more than twice that of nonspecialist pathologists (OR, 2.16; 95% CI, 1.93 to 2.41). Year of diagnosis was also important, with a 17% increase in the odds of a patient attaining an adequate lymphadenectomy for each year of the study (OR, 1.17; 95% CI, 1.14 to 1.19).
Lymph node status is a strong predictor of colorectal cancer survival and frequently dictates treatment methods. As adjuvant therapy becomes increasingly effective, this becomes of greater importance to patient care. Cure achieved through adjuvant treatment is also cost-effective, as failures may require further use of multiple expensive drugs in the palliative metastatic setting. Therefore, adequate assessment of this pathological feature is vital, but lymph node yields are seen to vary. Across this population, survival was associated with the extent of lymphadenectomy, and this effect was consistent across both the node-positive and node-negative population. Lymph node yield was found to be associated with many factors. Increasing patient age was negatively associated with yield, whereas the increasing size and stage of the tumor were associated with higher yields. The biggest effects on yield were seen, however, in relation to management factors, with it increasing significantly over time and being greatest when the patient was managed by specialist surgeons and pathologists. The analyses looking at the odds of adequate lymphadenectomy found similar trends. Again, increasing age was associated with a reduced odds, and increasing tumor size and stage with an increased odds, of adequate lymphadenectomy. Female patients were more likely to receive adequate lymphadenectomies, too. These effects remained after adjustment for casemix factors. Management factors also were important and existed despite adjustment for patient and tumor casemix factors. The odds of an adequate lymphadenectomy increased by 17% for each advancing year of the study, and management by specialist surgeons and pathologists was associated with an increase in odds of 40% and 116%, respectively. These results are supported by other published studies. Increasing age has been associated with decreased lymph node yields,16,19 but the reasons for this are unclear. There is evidence to suggest that the size of nodes reduces as patients get older, and this may make it harder to identify and retrieve them.28 Alternatively, it may be related to greater comorbidity in older patients making surgical retrieval more pressured. However, no difference in the mean specimen length or stage at diagnosis was observed between the different age categories (data not shown) suggesting surgeons were able to undertake resections of a similar extent in all patients. The difference in the median lymph node yield between the sexes approached statistical significance in this study, and the odds of adequate lymphadenectomy were increased in female patients. Again, this effect has been seen in other studies, but the reasons for this are unclear.16,19 A possible explanation is the sex differences in pelvic anatomy that affect the ease of surgical clearance.29-30 Anatomic site has been shown to relate to the extent of lymphadenectomy,6,19 but the effect has not been universally observed21 and was not seen in this population, though we could only distinguish between colon and rectal tumors. Theories of why a cancer site should influence yield often center on the technical difficulties of different surgical procedures. Right-sided resection specimens are stated to be longer than left-sided resections15-31 because of the anatomy of the bowel, and this may make it easier to identify more nodes. Our study does not, however, support this effect, and further work is required to delineate the impact tumor location has on yield. Ours, like other studies,17,19 demonstrated that lymph node yield is associated with T stage with an increase in yield from T1 to T4. This effect persisted when the number of positive nodes identified was controlled. The reasons for this association are unclear. It may be that tumor-draining nodes undergo reactive changes that make them larger and easier to identify or that new lymph nodes appear due to the antigenic challenge of a larger tumor. Alternatively, it may be that as more advanced tumors are more likely to have positive nodes, surgeons attempt greater clearance. Both this study and others19,32-34 have demonstrated that tumor stage is related to the extent of lymphadenectomy. The median number of nodes examined increased with stage, and the proportion of patients diagnosed with a stage III tumor was greater in patients who had large numbers of nodes retrieved and assessed. Retrieving a higher number of nodes increases the probability that, if present, positive lymph nodes will be detected. Thus, it is perhaps not surprising that patients with stage III disease had a higher average lymph node yield than their lower stage counterparts. The number of patients misclassified as stage II remains unclear, but based on the node-positive rate of 45.9% in those with higher than 12 nodes, compared with 37.2% in patients who did not receive an adequate lymphadenectomy, it is possible that approximately 9% of our population were misstaged. This relates to 636 patients who, potentially, were denied their indicated chemotherapy. Over the study period, the median number of nodes retrieved increased significantly. A similar trend has been demonstrated in other studies.14 Over this time, colorectal cancer care in England has undergone dramatic reform, and it is possible this has influenced nodal yields. The production of guidance documents,24-25 the centralization of services, and the national educational Pelican MDT-TME program35 have raised awareness about the importance of adequate staging and teamwork in the multidisciplinary management of colorectal cancer and emphasized the value of discussion and feedback between MDT members. The resulting increased awareness of adequate pathological staging may account for the improved yields observed. This theory is supported by other studies that have demonstrated an increased node retrieval rate following educational initiatives34 and that have demonstrated that changes in the way cancer care services are organized can improve the quality of cancer care.36 Surgeon factors, such as procedure volume and specimen length, have previously been correlated with lymph node retrieval,15,31 and institutional differences also have been observed,15,21 but the effect has not been seen universal.5,37 Our data show that MDT surgeons offered a 40% increase in the odds of a patient receiving an adequate lymphadenectomy after controlling for all other patient, tumor, and management casemix factors. Numerous studies have shown that high surgeon workload and surgical specialization improve outcomes in colorectal cancer22,38,39 through improved surgical technique and management. Likewise, pathologists who belonged to MDTs had higher median lymph node yields and were significantly more likely to retrieve greater than 12 nodes from a specimen than pathologists who were not team members. Although differences in pathological techniques used may account for some of the observed variation, it seems likely that the most influential factor is the effort and diligence of the reporting pathologist. MDT pathologists appear most likely to undertake the meticulous assessment of the resected specimen required to maximize yield. This is supported by other studies that have shown a difference in pathologist retrieval rates,4,40 though the evidence is not conclusive.31 The number of lymph nodes required for an adequate lymphadenectomy is contentious. Many studies offer evidence that different thresholds are required,9-10,14,32,41-42 and in this data set, the proportion of patients diagnosed as being node-positive continued to increase in patients in whom more than 12 nodes were retrieved. The concept of an adequate lymphadenectomy having occurred in patients with 12 or more lymph nodes appears simplistic and, in practice, is often ignored by the pathological community.19,33,40 If a 12-node threshold were applied to our data in the early years of our study, more than half our population would be Nx (ie, they would have nodes that cannot be assessed).43 It is known that the higher the number of nodes retrieved, the greater the percentage of node-positive disease, but the chances of retrieving 12 lymph nodes is dependant on many factors. An elderly patient with early-stage disease managed by a nonspecialist surgeon and pathologist is much less likely to yield as many nodes as a late-stage tumor in a young person managed by a specialist team. Therefore, a threshold of 12 nodes is arbitrary. The UK National Institute for Health and Clinical Excellence recommendations on colorectal lymphadenectomy for England and Wales simply state that as many nodes as possible should be removed,25 but that 12 or more nodes should normally be examined, and if the median is consistently below this, then both pathologist and surgeon should discuss their techniques. We support this recommendation. Adequate assessment of lymph node status is vital to ensure the best treatment strategy is adopted and to obtain the optimal survival. Assessing as many lymph nodes from the resected specimen as possible is important, but yields will vary in relation to many factors. They can, however, be maximized through high-quality surgery and diligent pathological examination. The UK government's recent reorganization of NHS cancer services focused the care of colorectal cancer patients into the hands of specialist MDTs. This study provides evidence to demonstrate that lymph node yield is greater when patients are managed by such teams, and this offers cautious support for the current NHS cancer reforms.
The author(s) indicated no potential conflicts of interest.
Conception and design: Eva Judith Ann Morris, Nicola Joanne Maughan, David Forman, Philip Quirke Collection and assembly of data: Eva Judith Ann Morris, Nicola Joanne Maughan, David Forman, Philip Quirke Data analysis and interpretation: Eva Judith Ann Morris, Nicola Joanne Maughan, David Forman, Philip Quirke Manuscript writing: Eva Judith Ann Morris, Nicola Joanne Maughan, David Forman, Philip Quirke Final approval of manuscript: Eva Judith Ann Morris, Nicola Joanne Maughan, David Forman, Philip Quirke
We thank the Yorkshire pathologists for completing the pathology proformas and making this study possible.
Supported by the National Translational Research Cancer Program (N.J.M.), the Pelican Cancer Foundation (E.J.A.M.), and Yorkshire Cancer Research (P.Q.). Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
1. Andre T, Boni C, Mounedji-Boudiaf L, et al: Oxaliplatin, fluorouracil and leucovorin as adjuvant treatment for colon cancer. N Engl J Med 350:2343-2351, 2004 2. Quirke P, Williams GT: Minimum Dataset for Colorectal Cancer Histopathology Reports. London, United Kingdom, Royal College of Pathologists, 2000, pp 2-3 3. Bull AD, Biffin AHB, Mella J, et al: Colorectal cancer pathology reporting: A regional audit. J Clin Pathol 50:138-142, 1997 4. Pheby DFH, Levine DF, Pitcher RW, et al: Lymph node harvest directly influences the staging of colorectal cancer: Evidence from a regional audit. J Clin Pathol 57:43-47, 2004 5. Thorn CC, Woodcock NP, Scott N, et al: What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 6:356-361, 2004[CrossRef][Medline] 6. Prandi M, Lionetto R, Bini A, et al: Prognostic evaluation of Stage B colon cancer patients is improved by an adequate lymphadenectomy. Ann Surg 235:458-463, 2002[CrossRef][Medline] 7. Johnson PM, Porter GA, Ricciardi R, et al: Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol 24:3570-3575, 2006 8. Jestin P, Pahlman L, Glimelius B, et al: Cancer staging and survival in colon cancer is dependent on the quality of the pathologists’ specimen examination. Eur J Cancer 41:2071-2078, 2005[CrossRef][Medline] 9. Le Voyer TE, Sigurdson ER, Hanlon AL, et al: Colon cancer survival is associated with increasing number of lymph nodes analyzed: A secondary survery of Intergroup trial INT-0089. J Clin Oncol 21:2919, 2003 10. Tepper JE, O'Connell MJ, Niedzwiecki D, et al: Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 19:157-163, 2001 11. Cianchi F, Palomba A, Boddi V, et al: Lymph node recovery from colorectal tumour specimens: Recommendation for a minimum number of lymph nodes to be examined. World J Surg 26:384-389, 2002[CrossRef][Medline] 12. Caplin S, Cerottini JP, Bosman FT, et al: For patients with Dukes’ B (TNM stage II) colorectal carcinoma, examination of six or fewer lymph nodes is related to poor prognosis. Cancer 83:666-672, 1998[CrossRef][Medline] 13. Pocard M, Panis Y, Malassagne B, et al: Assessing the effectiveness of mesorectal excision in rectal cancer: Prognostic value of the number of nodes found in resected specimens. Dis Colon Rectum 41:839-845, 1998[CrossRef][Medline] 14. Goldstein NS: Lymph node recoveries from 2427 pT3 colorectal resection specimens spanning 45 years: Recommendations for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 26:179-189, 2002[CrossRef][Medline] 15. Wright FC, Law HL, Last L, et al: Lymph node retrieval and assessment in stage II colorectal cancer: A population based study. Ann Surg Oncol 8:903-909, 1910 16. Sarli L, Bader G, Iusco D, et al: Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer 41:272-279, 2005[CrossRef][Medline] 17. Leibl S, Tsybrovsky O, Denk H: How many lymph nodes are necessary to stage early and advanced adenocarcinoma of the sigmoid colon and upper rectum? Virchows Arch 443:133-138, 2003[CrossRef][Medline] 18. Gorog D, Nagy P, Peter A, et al: Influence of obesity on lymph node recovery from rectal resection specimens. Pathol Oncol Res 9:180-183, 2003[Medline] 19. Baxter NN, Virnig DJ, Rothenberger DA, et al: Lymph node evaluation in colorectal cancer patients. J Natl Cancer Inst 97:219-225, 2005 20. Scott N Thorne C, Jayne D: Lymph node retrieval after neoadjuvant radiotherapy for rectal adenocarcinoma. J Clin Pathol 57:335-336, 2004 21. Miller EA, Woosley J, Martin CF, et al: Hospital-to-hospital variation in lymph node detection after colorectal resection. Cancer 101:1065-1071, 2004[CrossRef][Medline] 22. Halm EA, Lee C, Chassin MR: Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med 137:511-520, 2002 23. NHS Executive. Guidance on commissioning cancer services: Improving outcomes in colorectal cancer: The research evidence. Leeds, United Kingdom, Department of Health, 1997 24. NHS Executive. Guidance on commissioning cancer services: Improving outcomes in colorectal cancer: The manual. Leeds, United Kingdom, Department of Health, 1997 25. NHS Executive: Guidance on commissioning cancer services: Improving outcomes in colorectal cancer: The manual update. Leeds, United Kingdom, Department of Health, 2004 26. Northern and Yorkshire Cancer Registry and Information Service: Colorectal histopathology form. http://www.nycris.org.uk 27. UK Department of Health: Manual of Cancer Service Standards. London, United Kingdom, UK Department of Health, 2001 28. Baxendall M, Lewis F, Guillou, et al: Disappearing lymph nodes: One explanation for the fall in number with increasing age. J Pathol 208:29A, 2005 (suppl 1) 29. Marr R, Birbeck K, Garvican J, et al: The modern abdominoperineal excision: The next challenge after total mesorectal excision. Ann Surg 242:74-82, 2005[CrossRef][Medline] 30. Nagtegaal ID, van da Velde CJH, Marijnen CAM, et al: Low rectal cancer: A call for a change of approach in abdominoperineal resection. J Clin Oncol 23:9257-9264, 2005 31. Johnson PM, Malatjalian D, Porter GA: Adequacy of nodal harvest in colorectal cancer: A consecutive cohort study. J Gastrointest Surg 6:883-890, 2002[CrossRef][Medline] 32. Wong JH, Severino R, Honnebier B, et al: Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 17:2896-2900, 1999 33. 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 82:1482-1486, 1998[CrossRef][Medline] 34. Smith AJ, Law CH, Khalifa MA, et al: Multimodal CME for surgeons and pathologists improves colon cancer staging. J Cancer Educ 18:81-86, 2003[CrossRef][Medline] 35. Pelican Cancer Foundation: National MDT TME programme. http://www.pelicancancer.org/index.php?page=pages&menu=36&submenu=198&page_id=198 36. Morris E, Haward RA, Gilthorpe MS, et al: The impact of the Calman-Hine report on the processes and outcomes of care for Yorkshire's colorectal cancer patients. Br J Cancer 95:979-985, 2006[CrossRef][Medline] 37. Jha MK, Koreli A, Corbett WA, et al: When is a ‘Dukes’ B’ a Dukes’ B? An analysis of lymph node retrieval and reporting in colorectal cancer. Colorectal Dis 4:8, 2002 (suppl 1; abstr O22) 38. Schrag D, Panageas KS, Riedel E, et al: Hospital and surgeon procedure volume as predictors of outcome following rectal cancer resection. Ann Surg 236:583-592, 2002[CrossRef][Medline] 39. Smith JA, King PM, Lane RH, et al: Evidence of the effect of specialization on the management, surgical outcome and survival from colorectal cancer in Wessex. Br J Surg 90:583-592, 2003[CrossRef][Medline] 40. Wright FC, Law CHL, Last LD, et al: Barriers to optimal assessment of lymph nodes in colorectal cancer specimens. Am J Clin Pathol 121:663-670, 2004[CrossRef][Medline] 41. Joseph NE, Sigurdson ER, Hanlon AL, et al: Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol 10:213-218, 2003 42. Cserni S, Vinh-Hung V, Burzykowski T, et al: Is there a minimum number of lymph nodes that should be histologically assessed for a reliable nodal staging of T3N0M0 colorectal carcinomas? J Surg Oncol 81:63-69, 2002[CrossRef][Medline] 43. Sobin L, Wittekind C: TNM Classification of Malignant Tumours. New York, NY, Wiley & Sons, 1997 Submitted January 31, 2007; accepted April 2, 2007. 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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
