Dukes' Classification of Rectal Cancer

DEBA P. SARMA, MD, New Orleans, La

DUKES' CLASSIFICATION is the most commonly used staging system for colorectal cancer. The classification is based on findings from pathologic examination of the resected bowel specimen, reflecting the extent of spread of the cancer. Dr. Cuthbert E. Dukes, a pathologist at St. Mark's Hospital in London, had proposed the classification because it had prognostic significance. Although physicians, especially pamologists and surgeons, have been using Dukes' classification of colorectal cancer for more than 40 years, confusion and misinterpretation of the system have not resolved. As late as 1975 an editorial in the British Medical Journal1 described an incorrect Dukes' classification. Probably the most dramatic examples of incorrect interpretation of Dukes' classification have been reported in two widely read national publications, Newsweek2 and Time,3 after the news of President Reagan's colon cancer. I have reviewed various articles written either by Dr. Dukes alone or with coauthors, starting with one article published in 1929 in the Journal of British Surgery.4 This was the first article in which Dr. Dukes described a classification for rectal cancer as follows:
All cases of cancer of the rectum at St. Mark's Hospital are classified for the purpose of prognosis according to the depth of spread within the rectal wall. The system adopted is a modification of a clinical classification into A, B, and Ceases (Fig. 390), suggested by Lockhart-Mummery.1 A cases are malignant tumours in which the growth extends into the submucosa, but not into the muscle coat (Fig. 391). B cases are malignant tumours in which the growth extends into the muscle coat, but has not spread by direct continuity into the perirectal tissues (Fig. 392). C cases are malignant tumours which have spread by direct continuity into the perirectal tissues (Figs. 393-395). B cases may be further subdivided into El in which the circular muscle is the limit of growth, and B2 in which the longitudinal muscle has been reached. C cases may also be subdivided into Cl without glandular involvement, and C2 with metastasis in the lymphatic glands. This classification is made after microscopic examination of
From the Department of Pathology, Veterans Administration Medical Center and Louisiana State University Medical School, New Orleans. Reprint requests to Deba P. Sarma, MD, 1601 Perdido St, New Orleans, LA 70146.

big sections through the fixed and hardened tissue.

Three years later (1932), in an article in the Journal of Pathology and Bacteriology, Dukes abandoned his earlier (1929) classification and proposed the following:
A cases are those in which the carcinoma is limited to the wall of the rectum, there being no extension into the extra-rectal tissues and no metastases in lymph nodes, B cases those in which the carcinoma has spread by direct continuity to the extra-rectal tissues but has not yet invaded the regional nodes, and C cases those in which metastases are present in the regional lymph nodes.

Dukes had intended very specifically to follow this classification. 5 He wrote:

When instituted six years ago this method of classification was a development of a clinical grouping of cases introduced by Lockhart-Mummery (1926-27) and as first used all cases were grouped as C in which there was extra-rectal spread (GordonWatson and Dukes). Increasing experience, however, showed the desirability of a change to the present standards, particularly where the remarkable differences in the survival period of the three classes began to be apparent.

The difference between the original (1929) and the second (1932) classification by Dukes is remarkable:
Dukes' A 1932 1929 Cancer limited to Cancer extending into submucosa, but not into the rectal wall, no extrarectal spread, the muscle. no lymph node metastasis. Cancer into muscle coat, but not extending Cancer extends into into perirectal tissues. perirectal tissues, no lymph node Cancer extends into perirectal tissue (Cl metastases. Metastases are no lymph node present in the metastasis, C2with lymph node metastasis). lymph nodes.

Dukes' B Dukes' C

After 1932, Dr. Dukes referred to his 1932 classification in various publications 6 12 ; however, never in any writing did he mention his original (1929) classification. Dr. Dukes had subdivided the C cases into Cl

Reprinted from the Southern Medical Journal, Journal of the Southern Medical Association, Volume 81, Number 3, March 1988, Pages 407-408, Copyright 1988 by Southern Medical Association, Birmingham, Alabama

and C2 in a 1935 article in the British Journal of Surgery6:

Those cases in which the glandular spread has reached up to the level of the point of ligature of the blood-vessels we classify as C2 cases. In these cases the prognosis is bad, there being reason to suspect that glands at a higher level are affected. On the other hand, cases in which the regional lymph glands only are involved, or those in which the upward spread has not yet reached the glands at the point of ligature of the bloodvessels, we classify as Cl (Fig. 262). The prognosis is much better for this group, since the disease does not yet appear to have spread by lymphatic channels to the limits of the tissue removed.

This subdivision into Cl and C2 had been subsequently cited several times by Dr. Dukes.7'1012 Dr. Dukes never described a "stage D" of colo-rectal carcinoma. However, in one article published in 1947 in the Bulletin of the International Association of Medical Museums,10 Dr. Dukes mentioned a "fourth stage": "The fourth stage is reached when the malignant disease has spread to distant organs and can no longer be eradicated by surgery."
COMMENT

The ABC classification of rectal cancer, based on the extent of spread, as intended by Dr. Cuthbert Dukes, is a practical method of summarizing a pathology report on a resected rectal specimen. Prognosis of rectal cancer is largely dependent on the extent of spread at the time of surgical excision, and the excised specimen is best evaluated by a thorough pathologic study. A cases are those in which the cancer is limited to rectum, with no extrarectal spread and no lymph node metastasis; in B cases the cancer has directly spread to the extrarectal tissues, but there is no lymph node metastasis; and C cases are those with lymph node metastasis. The Dukes' classification is based on pathologic study of the resected rectal specimen, but the same classification has been applied for all intestinal carcinomas, as was recommended by Dr. Dukes himself. 5 7 1 It is very clear from Dukes' writing and illustrations that when he says the growth is limited to the rectum (A cases), he means that the cancer has not extended beyond the muscularis propria. He considers the outer border of the rectal wall as identical with the outer surface of the muscularis propria. When used for other parts of the colon, the same rule must apply, ie, Dukes' A for a colonic cancer should mean that the cancer has not extended beyond the muscularis propria of the colon. Similarly, the Dukes' B classification (cancer spreading to extrarectal tissues) when applied to the rest of the colon should mean that the cancer has spread beyond the muscularis propria into the pericolonic tissue. As for Dukes' C cases, there is no room for confusion when it is applied

to other colonic cancers because the cancer has to be metastatic in the lymph nodes to be classified as C. Dukes' classification has been used for colorectal cancers surgically resected with curative purpose. In advanced cancer when bowel can be resected only partially, leaving behind tumor at the excision site, or when bowel is excised for palliation only in cases with systemic metastases, such specimens cannot be or should not be classified by Dukes' method. Various modifications of Dukes' classification have been proposed and used over the years. 1316 Many authors are confused by various modified Dukes' classifications (eg, Turnbull's, Astler-Coller's, etc) and call them Dukes' classification. When we classify a resected colorectal cancer by Dukes' method we should use strictly Dukes' 1932 version of the ABC classification. If any modified versions are used, it must be specifically stated, such as "Astler-Coller's modification of Dukes' stages" or "Turnbull's modification of Dukes' stages." For a pathologist, minimal information on the pathology report of a resected colorectal specimen should specifically include (1) how far the cancer has extended (whether the tumor extends into the muscularis propria or beyond the muscularis propria into the fibroadipose tissue), and (2) whether there is any metastasis in the lymph nodes. With this information any physician should be able to classify cancer by the Dukes' system.
References
1. Search for presypmptomatic large bowel cancer (Editorial). Br Med J 4:605-606, 1975 2. A President's cancer scare (National affairs). Newsweek 22:14-21, July 1985 3. What the diagnosis means (Nation). Time 29:22, 1985 4. Gordon-Watson C, Dukes C: The treatment of carcinoma of the rectum with radium with an introduction on the spread of cancer of the rectum. BrJSurg 17:643-648, 1929 5. Dukes CE: The classification of cancer of the rectum. J Path Bad 85:323-332, 1932 6. Gabriel WB, Dukes C, Bussey HJR: Lymphatic spread in cancer of the rectum. Br J ^23:395-413, 1935
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8. 9. 10. 11. 12. 13. 14. 15. 16.

Dukes C, Bussey HJR: Preparation and mounting of museum specimens of intestinal tumours. J Tech Methods 15:44-48, 1936 Dukes C: Histological grading of rectal cancer. Proc R Sue Med 30:371-376, 1937 Dukes CE: Cancer of the rectum: an analysis of 1000 cases. J Path Bad 50:527-539, 1940 Dukes CE, Bussey HJR, Lamb GW: The examination and classifica tion of operation specimens of intestinal cancer. Bull Int Assoc Med Mus 27:55-65, 1947 Dukes CE, Bussey HJR: The spread of rectal cancer and its effect on prognosis. Br J Cancer 12:309-320, 1958 Dukes CE: The pathology of rectal cancer. Neoplastic Disease at Various Sites. Smithers DW (gen ed). Cancer oj the Rectum. Dukes CE (ed). Edin burgh, Livingstone, Vol 3, 1968, pp 59-68 Turnbull RB, Kyle K, Watson FR, et ah Cancer of the colon: the in fluence of the no-touch isolation technic on survival rates. Ann Surg 166:420-427, 1967 Kirklin JW, Dockerty MB, Waugh JM: Role of peritoneal reflection in prognosis of carcinoma of rectum and sigmoid colon. Surg Gynecol Obstet 88:326-331, 1949 Astler VB, Coller FA: Prognostic significance of direct extension of car cinoma of colon and rectum. Ann Surg 139:846-852, 1954 Eker R: Some prognostic factors for carcinomas of the colon and rec tum. Ada Cfitr Scand 126:636-656, 1963

Sarma DP(1988): Dukes classification of rectal cancer. South Med J 81: 407-408. PMID: 3279538 [PubMed - indexed for MEDLINE]