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The literature has repeatedly shown the superiority of total mesorectal excision (TME) for rectal cancer in
reducing the incidence of local recurrence (LR) and improving long-term survival compared to conven-
tional blunt rectal dissection. This article reviews the history of surgery for rectal cancer, supports TME as
the standard of care in obtaining a negative circumferential margin (CRM) for mid- and lower-third rectal
cancers, discusses the drawbacks of TME, the role of tumor-specific mesorectal excision for upper-third
rectal cancers and laparoscopic TME, and emphasizes the need for a selective role of chemoradiation
with TME for rectal cancer. The need for standardizing TME in the United States with pathological
specimen quality analysis and reporting of the completeness of the TME specimen is also emphasized.
& 2013 Elsevier Inc. All rights reserved.
1. History of surgery for rectal cancer an impressive decrease in LR to only 29.5% while causing a 31%
operative mortality, primarily due to blood loss and infection.5,6
In the early 19th century, rectal cancer was not considered a Despite the superior oncologic outcomes compared to the perineal
surgically curable disease; therefore, the surgical treatment of approach, the associated mortality prevented the APR from
rectal cancer was primarily via palliative defunctioning colostomy, becoming the standard of care until advances in anesthesia and
as described by the French surgeon Jean Zulema Amussat in 1839.1 blood transfusions helped lower the mortality rate to less than 20%
Jacques Lisfranc is credited with performing the first actual in the 1940s.6,7
resection of rectal cancer in 1826, when he removed only a few Lloyd-Davies at St. Mark's Hospital in 1939 described a two-
centimeters of the very distal rectum via a perineal approach.2 For team approach to APR with the patient in lithotomy-
the rest of the 19th century and up through the 1930s, most Trendelenburg position.8 Cuthbert Dukes reported downward
surgeons thus adopted a 2-stage approach to rectal cancer, with a and lateral spread to be much less important than Miles believed,
first-stage defunctioning colostomy followed by a perineal rectal and documented the majority of lymphatic spread to be proximal
resection in symptomatic patients. The large perineal wound was or cephalad to the primary site.9 This knowledge led surgeons to
left open and allowed to heal by secondary intent. Not surprisingly, begin advocating anterior resection of mid- and upper-rectal
rectal resections using the perineal-only approach carried a 480% cancers without removing the distal rectum, provided a 5-cm
local recurrence (LR) rate and a 8%–20% operative mortality.3,7 distal margin was obtained. These advances eliminated the peri-
Dissatisfied with an outcome of LR of 95% and the lack of a neal proctectomy and the APR-associated morbidity and mortality
possible surgical cure with the perineal approach, Sir Ernest Miles for mid- and upper-rectal tumors.10
in 1908 published his seminal paper from St. Mark's Hospital in The dogmatic belief that a 5-cm distal margin was necessary
London in which he described a radical combined abdominoper- from an oncologic standpoint also began to be challenged, provid-
ineal (APR) approach to rectal cancer.4 Miles postulated that LR ing greater opportunity for restorative operations.11 The develop-
could be prevented and rectal cancer resected with intent to cure ment and adoption of circular staplers for colorectal anastomosis
by removing as much of the pelvic lymphatics as possible. He in the late 1970s and recognition that a distal margin of 2 cm
identified 3 zones of potential spread of rectal cancer along the rather than 5 cm was oncologically safe allowed more frequent
pelvic lymphatics: upward, downward, and lateral. He considered restorative low anterior resections to be performed.12,13 Great
removal of the upward zone most vital. This was only technically emphasis was placed on a negative distal margin as vital to good
feasible from an anterior abdominal approach that included oncologic outcomes for rectal cancer, as less importance was given
primarily blunt dissection of the rectum and its associated lym- to the radial or circumferential margin (CRM). A small case series
phatics followed by the perineal resection.4 Miles was able to show report in 1976 by Quirke et al. from Leeds University highlighted
the importance of positive CRM after rectal resection. Pelvic
recurrence occurred in 3 out of 4 patients reported with cancer
n
Corresponding author. Tel.: þ 1 214 820 2468; fax: þ 1 214 820 4538. at CRM in the specimen. Over time, the presence of tumor at the
E-mail address: James.Fleshman@baylorhealth.edu (J.W. Fleshman). lateral surgical margin became a clear indication of poor outcome.
1043-1489/$ - see front matter & 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1053/j.scrs.2013.03.004
126 L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131
an increased risk of distant recurrence (37.6% vs. 12.7%) and 4. Non-oncologic advantages of TME
decreased survival, suggesting that CRM is an important prognos-
tic indicator.28 Other non-oncologic yet still important advantages of TME
A large meta-analysis of all reports from 1982 to 1992 that include less blood loss through sharp dissection in avascular
included at least 50 patients with “curable” rectal cancer with TME planes, as well as less sexual and urinary dysfunction. Conven-
or intramesorectal resection alone showed an overall LR of 18.5%: tional intramesorectal resection yields an incidence of impotence
23% with conventional resection (7%–50%), 12.4% with extended and/or retrograde ejaculation after surgery varying from 25% to
pelvic lymphadenectomy (includes en bloc resection of the inter- 75% while reports after TME place the incidence at 10%–29%. This
nal iliac nodes), and 7.1% with TME. McCall et al. concluded that improvement is felt to be due to the precise, sharp, nerve-sparing
“the wide range of LR rates with surgery alone indicate that rectal dissection in the correct avascular plane.31,32
cancer should be treated by surgeons with a special interest and
training in the management of this disease.”29
5. Disadvantages of TME
Fig. 2. Complete/Mesorectal Plane: intact mesorectum with only minor irregularities of a smooth mesorectal surface. No defect is deeper than 5 mm, and there is no coning
toward the distal margin of the specimen. There is a smooth circumferential resection margin on slicing.38 Personal communication with Quirke P, University of Leeds.
128 L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131
anastomotic leak rate of 16%. They concluded that TME is not between patients who underwent APR or sphincter-preserving
indicated for upper and rectosigmoid cancers.40 resection with a distal margin r 1 cm. They concluded that distal
Tumor-specific mesorectal excision has been shown to be margin r 1 cm is an oncologically sound margin after neoadjuvant
oncologically acceptable for upper rectal and rectosigmoid cancers. chemoradiation.48 A recent literature review by Park and Kim also
A review of 415 patients undergoing curative surgery alone for concluded that a distal resection margin of r1 cm is adequate in
rectal cancer in the Department of Colorectal Surgery at the Mayo patients undergoing curative resection after neoadjuvant chemo-
Clinic from 1982 to 1989 showed acceptable outcomes for tumor- radiotherapy.49 The American Society of Colon and Rectal Surgeons
specific TME. For tumors of the middle or lower rectum, patients recommends a 2-cm distal margin in its most recent Practice
underwent complete TME with either coloanal anastomosis (CAA) Parameters for the Management of Rectal Cancer. They do state
or APR, as necessary. Patients with upper rectal cancers underwent that smaller margins can be acceptable in certain circumstances, as
anterior resection (AR) with tumor-specific mesorectal excision by the “principle objective of surgical treatment is to obtain clear
performing a mesorectal excision to 5 cm below the tumor and surgical margins.”50
transecting the mesorectum and rectum at this point at a right
angle, avoiding “coning-in” on the rectum (Fig. 5). They reported
LR and 5-year disease-free survival rates of 7% and 78%, respec- 7. Laparoscopic TME
tively, after AR, 6% and 83% after CAA, and 4% and 80% after APR.
They concluded that “appropriate ‘tumor-specific’ mesorectal The multicenter, randomized, prospective North American
excision during AR when the tumor is high in the rectum is Clinical Outcomes of Surgical Therapy (COST) Study Group and
likewise consistent with a low rate of local recurrence and good United Kingdom Medical Research Council Conventional vs.
long-term survival.”41 Laparoscopic-Assisted Surgery in Colorectal Cancer (CLASICC) trials
reported that laparoscopic surgery for colon and colorectal sur-
6.1. Distal margin gery, respectively, are oncologically equivalent to open resec-
tion.51,52 Similarly, several multicenter randomized trials looking
Tumor-specific mesorectal excision is further supported by the at laparoscopic vs. open resection for rectal cancer are currently
shortening of the necessary distal margin. Multiple studies have underway, such as the European COLOR II Trial, the Japanese JCOG
shown that any distal intramural spread of rectal cancer is almost study 0404, and the American College of Surgeons Oncology Group
always within 1.5 cm of the primary tumor, and that when there is (ACOSOG) trial Z6051.53–55 The endpoints of the European and
distal spread beyond 1.5 cm, these instances are highly associated Japanese trials are survival and LR. The primary endpoint of the
with high grade or widely metastatic tumors, rendering prognosis ACOSOG Z6051 trial is the quality of the surgical specimen
poor and resection largely palliative in nature.42–47 The random- measured by clear circumferential and distal margins and a
ized prospective clinical trial by the National Surgical Adjuvant complete TME resection.55 In a single-center randomized prospec-
Breast and Bowel Project (NSABP) R03 evaluating adjuvant therapy tive trial from Hong Kong looking at laparoscopic vs. open
in Dukes B and C rectal cancer showed no significant difference in resection of 403 patients with cancer of the rectosigmoid junction,
LR or survival in 181 patients undergoing sphincter-preserving Leung et al. showed that laparoscopic resection of rectosigmoid
rectal resections, whether the distal margin was o2 cm, 2–2.9 cm, cancers was technically possible and oncologically safe.56 Separate
or Z 3 cm.47 prospective studies in England and France both concluded that
In the era of neoadjuvant chemoradiotherapy, distal margins laparoscopic TME was technically feasible and oncologically safe in
even r 1 cm appear sufficient. In a prospective study of 36 the treatment of rectal cancer.57–58
patients with rectal cancer r 8 cm from the anal verge who Zhou et al. prospectively randomized 171 patients with curable
underwent chemoradiotherapy prior to resection, Kushinoff et al. low rectal cancers in a single Chinese institution to either laparo-
reported no significant difference in LR or disease-free survival scopic or open TME with anal sphincter preservation and anasto-
mosis Z2 cm, o 2 cm, or 0 cm above the dentate line. They
reported no significant difference between the laparoscopic and
open groups in operative time, days requiring parenteral analgesia,
start of a diet, LR, and operative mortality (0 in both); however,
there were significant differences in the open vs. laparoscopic
groups in operative blood loss (92 mL vs. 20 mL, respectively), days
to first bowel movement (2.7 d vs. 1.5 d), hospitalization (13.3 d vs.
8.1 d), and overall complications (12.4% vs. 6.1%). They concluded
that laparoscopic TME is an oncologically feasible operation with
significant short-term postoperative benefits.59 In Milan, Braga
et al. randomized 168 patients with rectal cancer to either
laparoscopic or open resection and reported that laparoscopic
resection significantly reduced the length of hospital stay from
13.6 to 4.9 days, improved the first-year quality of life after
surgery, and increased the total hospital cost by $351. There were
no significant differences between LR and 5-year survival.60
With the evidence showing the value of TME and the CRM,
pathologists, led by Quirke and Nagtegaal, have standardized the
Fig. 5. Tumor-specific mesorectal excision. The distal mesorectum and rectum are reporting of the macroscopic quality of the TME and the micro-
transected at a right angle. Reprinted with permission from Lin AY.66 scopic CRM.38,61–64 With supporting photo-documented evidence,
130 L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131
Table 1 articles in colonic and rectal surgery. Jean Zulema Amussat 1796–1855. Dis
The effect of quality of TME and preoperative short-course radiotherapy (PRE) on Colon Rectum 26: 483–487, 1983].
3-year LR and disease-free survival (DFS). POST ¼ selective postoperative chemor- 2. Lisfranc J. Memoire sur l'excision de la partie inferieure du rectum devenue
adiotherapy if involved CRM; HR ¼ Hazard Ratio.65 carcinomateuse. Mem Ac R Chir. 1833;3:291–302 [Reprinted in Corman ML ed.
Classic articles in colonic and rectal surgery. Jacques Lisfranc 1790–1847. Dis
Plane of surgery LR at 3 years DFS at 3 years Colon Rectum 26: 694–695, 1983].
3. Graney MJ, Graney CM. Colorectal surgery from antiguity to the modern era. Dis
N PRE POST HR PRE POST HR Colon Rectum. 1980;23:432–441.
(%) (%) (%) (%) 4. Miles WE. A method of performing abdomino-perineal excision for carcinoma
of the rectum and of the terminal portion of the pelvic colon. Lancet.
1908;2:1812–1813.
Mesorectal plane/Complete 596 1 6 4.47 87 80 1.53
5. Miles WE. Cancer of the rectum (Lettsomian lectures). Trans Med Soc Lond.
Intramesorectal plane/Nearly 382 6 12 2.02 78 75 1.13
1923;46(127): [Reprinted in Miles WE. Cancer of the rectum: being the
Complete
Lettsomian lectures delivered before the medical society of London on February
Muscularis propria plane/ 141 9 29 2.76 79 65 1.75
19th, March 7th, and March 26, 1923, London, Harrison and Sons, 1926].
Incomplete 6. Lange MM, Rutten HJ, van de Velde CJ. One hundred years of curative surgery
for rectal cancer: 1908–2008. Eur J Surg Oncol. 2009;35:456–463.
7. Ruo L, Guillem JG. Major 20th-century advancements in the management of
it is recommended that all rectal specimens be graded by specif- rectal cancer. Dis Colon Rectum. 1999;42:563–578.
ically trained pathologists for macroscopic quality of the TME as 8. Lloyd-Davies OV. Lithotomy-Trendelenburg position for resection of rectum and
“complete” (Mesorectal Plane, Fig. 2), “nearly complete” (Intra- lower pelvic colon. Lancet. 1939;237:74–76.
9. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol. 1932;35
mesorectal Plane, Fig. 3), or “incomplete” (Muscularis Propria (3):323–332 [Reprinted in Corman ML ed. Classic articles in colonic and rectal
Plane, Fig. 4).38,61,63,64 The CRM is then microscopically assessed surgery. The classification of cancer of the rectum. Dis Colon Rectum 23(8):
via the “bread loaf slicing” technique developed by Quirke.14,27,61 605–611, 1980].
10. Dixon CF. Anterior resection for malignant lesions of the upper part of the
In a recent abstract on the 3-year results from the ongoing rectum and lower part of the sigmoid. Ann Surg. 1948;128(3):425–442.
Medical Research Council (MRC) CR07 trial that randomized 11. Goligher JC, Dukes CE, Bussey HJ. Local recurrences after sphincter saving
patients with rectal cancer to either short-course preoperative excisions for carcinoma of the rectum and rectosigmoid. Br J Surg.
radiotherapy (PRE) or selective postoperative chemoradiotherapy 1951;39:199–211.
12. Fain SN, Patin CS, Morgenstern L. Use of a mechanical suturing apparatus in low
if the CRM is involved (POST), Quirke et al. prospectively assessed colorectal anastomosis. Arch Surg. 1975;110(9):1079–1082.
the CRM in 1232 patients and the plane of surgery (quality of TME) 13. Pollet WG, Nicholls RJ. The relationship between the extent of distal clearance
in 1119 patients. Adhering to his well-documented pathological and survival and local recurrence rates after curative anterior resection for
carcinoma of the rectum. Ann Surg. 1983;198(2):159–163.
inspection guidelines, Quirke reported a strong association with 14. Quirke P, Durdey P, Dixon MF, et al. Local recurrence of rectal adenocarcinoma
both decreased LR and increased 3-year disease-free survival (DFS) due to inadequate surgical resection. Histopathological study of lateral tumour
with both the higher quality of surgery and the use of preoperative spread and surgical excision. Lancet. 1986;2(8514):996–999.
15. Adam IJ, Mohamdee MO, Martin IG. Role of circumferential margin involve-
short-course radiotherapy (Table 1). He concluded that “for
ment in the local recurrence of rectal cancer. Lancet. 1994;344
patients with rectal cancer short-course preoperative radiotherapy (8924):707–711.
and good quality surgery can almost completely eliminate local 16. Heald RJ. A new approach to rectal cancer. Br J Hosp Med. 1979;22(3):277–281.
recurrence.”65 17. Heald RJ. The ‘Holy Plane’ of rectal surgery. J R Soc Med. 1988;81(9):503–508.
18. Nogueras JJ. Open low anterior resection. In: Wexner SD, Fleshman JW, Fischer
These standardized quality measures are a vital part of the JE, (eds): Master Techniques in General Surgery: Colon and Rectal Surgery:
ongoing multicenter, randomized American College of Surgeons Abdominal Operations. Philadelphia, PA: Lippincott Williams & Wilkins; 2012.
Oncology Group (ACOSOG) trial Z6051 looking at laparoscopic vs. p. 127–131.
19. Heald RJ, Husband EM, Ryall RDH. The mesorectum in rectal cancer surgery—
open TME for curable rectal cancer. Surgeons are credentialed in
the clue to pelvic recurrence? Br J Surg. 1982;69:613–616.
this study by review of their operative videos and documentation 20. Heald RJ, Ryall RDH. Recurrence and survival after total mesorectal excision for
of TME in their operative notes. The 3 primary endpoints of this rectal cancer. Lancet. 1986;327(8496):1479–1482.
21. Arbman G, Nilsson E, Hallbook, et al. Local recurrence after total mesorectal
study are a CRM 4 1 mm, a negative distal margin, and the quality
excision for rectal cancer. Br J Surg. 1996;83(3):375–379.
of the TME. One-third of the TME quality endpoint is based on the 22. Kockerling F, Reymond MA, Altendorf-Hofmann A, et al. Influence of surgery on
macroscopic photos of the TME.55 metachronous distant metastases and survival in rectal cancer. J Clin Oncol.
1998;16(1):324–329.
23. MacFarlane JK, Ryall RDH, Heald RJ. Mesorectal excision for rectal cancer.
Lancet. 1993;341(8843):457–460.
9. Summary
24. Bjerkeset T, Edna TH. Rectal cancer: the influence of type of operation on local
recurrence and survival. Eur J Surg. 1996;162(8):643–648.
Complete, disease-specific mesorectal excision is the standard of 25. Arenas RB, Fichera A, Mhoon D, et al. Total mesorectal excision in the surgical
care in the current treatment of rectal cancer. In instances of mid- treatment of rectal cancer. Arch Surg. 1998;133(6):608–612.
26. Hall NR, Finan PJ, Al-Jaberi T, et al. Circumferential margin involvement after
and low-rectal cancers, this generally requires total mesorectal mesorectal excision of rectal cancer with curative intent. Predictor of survival
excision. TME plays a vital role in obtaining a negative circum- but not local recurrence? Dis Colon Rectum. 1998;41(8):979–983.
ferential resection margin, which significantly decreases local 27. Quirke P, Dixon MF. How i do it: the prediction of local recurrence in rectal
adenocarcinoma by histopathological examination. Int J Colorectal Dis. 1988;3
recurrence and is a valuable prognostic indicator for disease-free (2):127–131.
survival and likely overall survival. In the era of TME, selective 28. Nagtegaal ID, Marijnen CA, Kranenbarg EK, et al. Circumferential margin
neoadjuvant and adjuvant therapy continues to play an important involvement is still an important predictor of local recurrence in rectal
carcinoma: not one millimeter but two millimeters is the limit. Am J Surg
role. Laparoscopic TME appears to be feasible and oncologically
Pathol. 2002;26(3):350–357.
safe, and several multicenter, randomized trials studying it look to 29. McCall JL, Cox MR, Wattchow DA. Analysis of local recurrence rates after
be completed soon. Finally, TME performed by experts and eval- surgery alone for rectal cancer. Int J Colorectal Dis. 10(3):126–132.
uated and reported according to rigorous, standardized patholog- 30. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy
combined with total mesorectal excision for resectable rectal cancer. N Engl J
ical protocols provides significantly improved outcomes and drives Med. 2001;345(9):638–646.
better-informed decision making in regard to adjuvant therapy. 31. Bleday R, Brindzei N. Surgical treatment of rectal cancer. In: Beck DE, Roberts
PL, Saclarides TJ, et al.,(eds): The ASCRS Textbook of Colon and Rectal Surgery. 2nd
References ed.,New York, NY: Springer; 2011. p. 747–750.
32. Masui H, Ike H, Yamaguchi S, et al. Male sexual function after autonomic nerve-
preserving operation for rectal cancer. Dis Colon Rectum. 1996;39
1. Amussat JZ. Notes on the possible establishment of an artificial anus in the (10):1140–1145.
lumbar region without entering the peritoneal cavity [in French]. Paris: Lu a 33. Goligher JC, Graham NG, DeDombal FT. Anastomotic dehiscence after anterior
L’Academie Royale de Medecine. 1839 [Reprinted in Corman ML ed. Classic resection of rectum and sigmoid. Br J Surg. 1970;57(2):109–118.
L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131 131
34. Fielding LP, Stewart-Brown S, Blesovsky L, et al. Anastomotic integrity after 50. Tjandra JJ, Kilkenny JW, Buie WD, et al. Practice parameters for the manage-
operations for large-bowel cancer: a multicentre study. Br Med J. 1980;281 ment of rectal cancer. Dis Colon Rectum. 2005;48(3):411–423 [Revised].
(6237):411–414. 51. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparos-
35. Vignali A, Fazio VW, Lavery IC, et al. Factors associated with the occurrence of copically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350
leaks in stapled rectal anastomoses: a review of 1014 patients. J Am Coll Surg. (20):2050–2059.
1997;185(2):105–113. 52. Jayne DG, Guillou PJ, Thorpe H. Randomized trial of laparoscopic-assisted
36. Karanjia ND, Corder AP, Bearn P, et al. Leakage from stapled low anastomosis resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial
after total mesorectal excision for carcinoma of the rectum. Br J Surg. 1994;81 Group. J Clin Oncol. 2007;25(21):3061–3068.
(8):1224–1226. 53. Buunen M, Bonjer HJ, Hop WC, et al. COLOR II. A randomized clinical trial
37. Martling AL, Holm T, Rutqvist LE, et al. Effect of a surgical training programme comparing laparoscopic and open surgery for rectal cancer. Dan Med Bull.
on outcome of rectal cancer in the County of Stockholm. Stockholm Colorectal 2009;56(2):89–91.
Cancer Study Group, Basingstoke Bowel Cancer Research Project. Lancet. 54. Kitano S, Inomata M, Sato A, et al. Randomized controlled trial to evaluate
2000;356(9224):93–96. laparoscopic surgery for colorectal cancer: Japan Clinical Oncology Group Study
38. Nagtegaal ID, van de Velde CJ, van der Worp E, et al. Macroscopic evaluation of JCOG 0404. Jpn J Clin Oncol. 2005;35(8):475–477.
rectal cancer resection specimen: clinical significance of the pathologist in 55. Fleshman J. American College of Surgeons Oncology Group (ACOSOG)-Z6051. A
quality control. J Clin Oncol. 2002;20(7):1729–1734. phase III prospective randomized trial comparing laparoscopic-assisted resec-
39. Temple LK, Bacik J, Savatta SG, et al. The development of a validated instrument tion versus open resection for rectal cancer. Available at: 〈http://clinicaltrials.
to evaluate bowel function after sphincter-preserving surgery for rectal cancer. gov/ct2/show/NCT00726622〉.
Dis Colon Rectum. 2005;48(7):1353–1365. 56. Leung KL, Kwok SP, Lam SC. Laparoscopic resection of rectosigmoid carcinoma:
40. Hainsworth PJ, Egan MJ, Cunliffe WJ. Evaluation of a policy of total mesorectal prospective randomised trial. Lancet. 2004;363(9416):1187–1192.
excision for rectal and rectosigmoid cancers. Br J Surg. 1997;84(5):652–656. 57. Hartley JE, Mehigan BJ, Qureshi AE, et al. Total mesorectal excision: assessment
41. Zaheer S, Pemberton JH, Farouk R, et al. Surgical treatment of adenocarcinoma of the laparoscopic approach. Dis Colon Rectum. 2001;44(3):315–331.
of the rectum. Ann Surg. 1998;227(6):800–811. 58. Bretagnol F, Rullier E, Couderc P, et al. Technical and oncological feasibility of
42. Black WA, Waugh JM. The intramural extension of carcinoma of the descending laparoscopic total mesorectal excision with pouch coloanal anastomosis for
colon, sigmoid, and rectosigmoid; a pathologic study. Surg Gynecol Obstet. rectal cancer. Colorectal Dis. 2003;5(5):451–453.
1948;87(4):457–464. 59. Zhou ZG, Hu M, Li Y, et al. Laparoscopic versus open total mesorectal excision
43. Quer EA, Dahlin DC, Mayo CW. Retrograde intramural spread of carcinoma of with anal sphincter preservation for low rectal cancer. Surg Endosc. 2004;18
the rectum and rectosigmoid; a microscopic study. Surg Gynecol Obstet. (8):1211–1215.
1953;96(1):24–30. 60. Braga M, Frasson M, Vignali A. Laparoscopic resection in rectal cancer patients:
44. Grinnell RS. Distal intramural spread of carcinoma of the rectum and recto- outcome and cost-benefit analysis. Dis Colon Rectum. 2007;50(4):464–471.
sigmoid. Surg Gynecol Obstet. 1954;99(4):421–430. 61. Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the
45. Williams NS, Dixon MF, Johnston D. Reappraisal of the 5 centimetre rule of modern treatment of rectal cancer? J Clin Oncol. 2008;26(2):303–312.
distal excision for carcinoma of the rectum: a study of distal intramural spread 62. Hoorens A, De Ridder M, Jouret-Mourin A, et al. Pathological assessment of the
and of patients' survival. Br J Surg. 1983;70(3):150–154. rectal cancer resection specimen. Bel J Med Oncol. 2009;3(6):251–260.
46. Madsen PM, Christiansen J. Distal intramural spread of rectal carcinomas. Dis 63. Parfitt JR, Driman DK. The total mesorectal excision specimen for rectal cancer:
Colon Rectum. 1986;29(4):279–282. a review of its pathological assessment. J Clin Pathol. 2007;60(8):849–855.
47. Wolmark N, Fisher B. An analysis of survival and treatment failure following 64. Jass JR, O'Brien MJ, Riddell RH. Recommendations for the reporting of surgically
abdominoperineal and sphincter-saving resection in Dukes' B and C rectal resected specimens of colorectal carcinoma. Hum Pathol. 2007;38(4):537–545.
carcinoma. A report of the NSABP clinical trials. National Surgical Adjuvant 65. Quirke P, Sebag-Montefiore D, Steele R, et al. Local recurrence after rectal
Breast and Bowel Project. Ann Surg. 1986;204(4):480–489. cancer resection is strongly related to the plane of surgical dissection and is
48. Kushinoff B, Maghfoor I, Miedema B, et al. Distal margin requirements after further reduced by preoperative short course radiotherapy: preliminary results
preoperative chemoradiotherapy for distal rectal carcinomas: are o or ¼ 1 cm of the MRC CR07 trial. J Clin Oncol. 2006;24:149s [suppl; abstr 3512].
distal margins sufficient? Ann Surg Oncol. 2001;8(2):163–169. 66. Lin AY. Open low anterior resection of rectum. In: Fleshman JW, (ed). Atlas of
49. Park IJ, Kim JC. Adequate length of the distal resection margin in rectal cancer: Surgical Techniques for the Colon, Rectum, and Anus. Philadelphia, PA: Elsevier
from the oncological point of view. J Gastrointest Surg. 2010;14(8):1331–1337. Saunders; 2013. p. 156–177.