Seminars in Colon and Rectal Surgery 24 (2013) 125–131

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Seminars in Colon and Rectal Surgery

journal homepage: www.elsevier.com/locate/yscrs

Modern rectal cancer surgery—Total mesorectal excision—The standard of care

Leander Grimm Jr., MD, and James W. Fleshman, MD, FACS, FASCRSn
Department of Surgery, Baylor University Medical Center at Dallas, 3500 Gaston Ave, 1st Floor, Roberts Hospital, Dallas, TX

a b s t r a c t

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
In the early 19th century, rectal cancer was not considered a
surgically curable disease; therefore, the surgical treatment of
rectal cancer was primarily via palliative defunctioning colostomy,
as described by the French surgeon Jean Zulema Amussat in 1839.1
Jacques Lisfranc is credited with performing the first actual
resection of rectal cancer in 1826, when he removed only a few
centimeters of the very distal rectum via a perineal approach.2 For
the rest of the 19th century and up through the 1930s, most
surgeons thus adopted a 2-stage approach to rectal cancer, with a
first-stage defunctioning colostomy followed by a perineal rectal
resection in symptomatic patients. The large perineal wound was
left open and allowed to heal by secondary intent. Not surprisingly,
rectal resections using the perineal-only approach carried a 480%
local recurrence (LR) rate and a 8%–20% operative mortality.3,7
Dissatisfied with an outcome of LR of 95% and the lack of a
possible surgical cure with the perineal approach, Sir Ernest Miles
in 1908 published his seminal paper from St. Mark's Hospital in
London in which he described a radical combined abdominoper-
ineal (APR) approach to rectal cancer.4 Miles postulated that LR
could be prevented and rectal cancer resected with intent to cure
by removing as much of the pelvic lymphatics as possible. He
identified 3 zones of potential spread of rectal cancer along the
pelvic lymphatics: upward, downward, and lateral. He considered
removal of the upward zone most vital. This was only technically
feasible from an anterior abdominal approach that included
primarily blunt dissection of the rectum and its associated lym-
phatics followed by the perineal resection.4 Miles was able to show
n
Corresponding author. Tel.: þ 1 214 820 2468; fax: þ 1 214 820 4538.
E-mail address: James.Fleshman@baylorhealth.edu (J.W. Fleshman).
an impressive decrease in LR to only 29.5% while causing a 31%
operative mortality, primarily due to blood loss and infection.5,6
Despite the superior oncologic outcomes compared to the perineal
approach, the associated mortality prevented the APR from
becoming the standard of care until advances in anesthesia and
blood transfusions helped lower the mortality rate to less than 20%
in the 1940s.6,7
Lloyd-Davies at St. Mark's Hospital in 1939 described a two-
team approach to APR with the patient in lithotomy-
Trendelenburg position.8 Cuthbert Dukes reported downward
and lateral spread to be much less important than Miles believed,
and documented the majority of lymphatic spread to be proximal
or cephalad to the primary site.9 This knowledge led surgeons to
begin advocating anterior resection of mid- and upper-rectal
cancers without removing the distal rectum, provided a 5-cm
distal margin was obtained. These advances eliminated the peri-
neal proctectomy and the APR-associated morbidity and mortality
for mid- and upper-rectal tumors.10
The dogmatic belief that a 5-cm distal margin was necessary
from an oncologic standpoint also began to be challenged, provid-
ing greater opportunity for restorative operations.11 The develop-
ment and adoption of circular staplers for colorectal anastomosis
in the late 1970s and recognition that a distal margin of 2 cm
rather than 5 cm was oncologically safe allowed more frequent
restorative low anterior resections to be performed.12,13 Great
emphasis was placed on a negative distal margin as vital to good
oncologic outcomes for rectal cancer, as less importance was given
to the radial or circumferential margin (CRM). A small case series
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
at CRM in the specimen. Over time, the presence of tumor at the
lateral surgical margin became a clear indication of poor outcome.

1043-1489/$ - see front matter & 2013 Elsevier Inc. All rights reserved.
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126 L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131

2. Total Mesorectal Excision (TME)

In the 1980s, an educational effort in Europe and Scandanavia

led by Professor Richard (Bill) Heald facilitated the adoption of
total mesorectal excision (TME) and recognition of the importance
of a negative CRM. In 1986, Quirke et al. reported a positive CRM in
27% of rectal specimens (14/52) resected by conventional blunt
techniques. This resulted in an 86% (12/14) LR, suggesting that a
positive CRM is the major predictor of LR.14 Adam et al. prospec-
tively showed that patients with a positive CRM are 12 times more
likely to have LR and 3 times more likely to die from rectal cancer
than patients with a negative CRM after a curative resection of
rectal cancer.15
Heald first described a total mesorectal excision (TME) in 1979
and the “holy plane” in 1988.16,17 TME can very simply be defined
as sharp dissection and “complete removal of the lymph node-
bearing mesorectum along with its intact enveloping fascia.”18 In
1982, Heald reported 5 instances of tumor deposits in the
mesorectum distal to the primary tumor.19 Additionally, his report
of a prospective series of patients treated with TME for mid- to
lower-rectal cancer showed a LR of 3.7%.20
The operative steps of TME are en bloc rectal excision includ-
ing (1) ligation of the Inferior Mesenteric Artery (IMA) at its
origin, (2) mobilization of the splenic flexure, (3) transection of
the left colon at the descending-sigmoid junction, (4) sharp
dissection in the avascular plane into the pelvis—anterior to the
presacral fascia-parietal fascia and outside the fascia propria or
enveloping visceral fascia (Fig. 1), (5) division of lymphatics and
middle hemorrhoidal vessels anterolaterally at the level of the
pelvic floor, and (6) inclusion of all pelvic fat and lymphatic
material to the level of the anorectal ring (puborectalis bundle of
the levator ani pelvic floor).
Several retrospective studies without adjuvant therapy com-
paring TME to intramesorectal dissection support the superiority
of TME. Arbman et al. reported a LR of 14% prior to TME and 6%
with TME. They showed an improvement in 4-year survival from
50% prior to TME to 70% with TME in 262 patients in the United
Kingdom with rectal cancer treated with curative intent.21 Kock-
erling et al., in Germany, reported a retrospective review of 1581
patients treated for rectal cancer with curative intent, which
showed improvement in LR from 39.4% to 9.8% and a 5-year
survival from 50% to 71% with the use of TME rather than
conventional blunt techniques.22
An audit of a prospective series of 135 patients with Dukes
B2 or C rectal cancer in Basingstoke treated with TME without
adjuvant therapy showed a LR of 5% and 5-year survival of 78%.
Fig. 1. The correct planes in total mesorectal excision. Reprinted with permission
MacFarlane et al. conclude “most carcinomas that recur ini- from Lin AY.66
tially within the pelvis could probably have been cured by
better surgery.” 23 In a prospective series of 118 patients in TME, rather, portends a worse overall prognosis, with increased
Norway treated with TME for rectal cancer, Bjerkeset et al. development of distant recurrence (DR) and decreased 5-year
achieved a 5-year LR of 14% overall, 7% in the “resectable” survival (TME and þCRM ¼ 35% DR and 48% 5-year survival;
group, and 4% in the “curable” group. This resulted in a 5-year TME and −CRM ¼ 22% DR and 70% 5-year survival). They
cancer-specific survival of 90% and overall 5-year survival of concluded that “when a mesorectal excision is performed, circum-
67%. 24 Arenas et al. prospectively studied 65 patients with ferential margin involvement is more an indicator of advanced
rectal cancer who were treated with TME þ /− adjuvant disease than inadequate local surgery” and argued that it should
therapy (depending on stage) at the University of Chicago. A play a role in staging.26
LR of 6.2% overall and 3.1% if the tumor was “curable” corre- Nagtegaal et al. retrospectively performed a pathological anal-
lated well with a 5-year survival of 88% for Stage I/II cancers ysis of the TME-only arm of the Dutch randomized controlled trial
and 65% in Stage III cancers. The overall LR was 8.3% in patients of TME þ /− preoperative radiotherapy for rectal cancer, using a
who underwent TME without adjuvant therapy, and 0% in the “bread loaf slicing” protocol developed by Quirke at the University
“curable” group, further supporting the effectiveness of TME in of Leeds in order to better define involvement of the CRM at the
decreasing LR. 25 outer extent of the mesorectal fat along the fascial envelope.14,27
Hall et al. showed in a prospective study of 152 patients that a They concluded that invasion of the tumor to within 2 mm of the
positive CRM in the setting of a proper TME does not increase the CRM should be considered positive or involved. They reported a
risk of LR as it does in intramesorectal resection (TME and þ CRM ¼ significantly higher LR (16%) than in patients with CRM 4 2 mm
15% LR; TME and −CRM ¼ 14% LR). A positive CRM after complete (5.8%). They also concluded that a CRM o 1 mm carries with it
 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
decreased survival, suggesting that CRM is an important prognos-
tic indicator.28
A large meta-analysis of all reports from 1982 to 1992 that
included at least 50 patients with “curable” rectal cancer with TME
or intramesorectal resection alone showed an overall LR of 18.5%:
23% with conventional resection (7%–50%), 12.4% with extended
pelvic lymphadenectomy (includes en bloc resection of the inter-
nal iliac nodes), and 7.1% with TME. McCall et al. concluded that
“the wide range of LR rates with surgery alone indicate that rectal
cancer should be treated by surgeons with a special interest and
training in the management of this disease.”29
3. Adjuvant therapy and TME
It has been postulated that the use of TME would potentially
obviate the need for adjuvant radiotherapy, arguing that radio-
therapy compensated for poor surgery before TME. However,
radiotherapy may still play an important role in reducing LR
even with TME. The Dutch multicenter randomized trial
randomized 1805 patients with potentially curable rectal
cancer to receive TME with or without preoperative radio-
therapy. Kapiteijn et al. reported an overall LR of 5.3% at 2 years
but no change in overall survival in the 1748 patients that
underwent a macroscopically complete TME. Interestingly, the
TME-alone group had a LR of 8.2%, while the TME þ radio-
therapy group had a LR of 2.4%, thus supporting the role of
radiotherapy combined with TME. 30 The question remains on
how to select those individuals who would benefit most from
radiotherapy.
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.
127
4. Non-oncologic advantages of TME
Other non-oncologic yet still important advantages of TME
include less blood loss through sharp dissection in avascular
planes, as well as less sexual and urinary dysfunction. Conven-
tional intramesorectal resection yields an incidence of impotence
and/or retrograde ejaculation after surgery varying from 25% to
75% while reports after TME place the incidence at 10%–29%. This
improvement is felt to be due to the precise, sharp, nerve-sparing
dissection in the correct avascular plane.31,32
5. Disadvantages of TME
5.1. Anastomotic leak
Despite all of the reported oncologic benefits, TME carries some
important drawbacks. Some may argue that TME is associated with
longer operative time, but TME's major disadvantage is its associ-
ation with an increased rate of anastomotic leak. Increased
anastomotic leak rates have been associated with an anastomosis,
with or without TME, close to the anal verge.33-36 A recent single-
institution retrospective review of 1014 patients undergoing
resection and stapled colorectal anastomosis for any indication
revealed an overall clinically apparent anastomotic leak rate of
2.9%, which increased to 7.7% for anastomoses within 7 cm of the
anal verge.35 By definition, restorative TME requires a low pelvic
anastomosis near the pelvic floor in order to remove the entire
mesorectum. Attempts to leave distal rectum without mesorectum
after resection of high rectal tumors have led to devascularized
and ischemic rectal stumps. In a prospective study of 219 patients
undergoing TME for rectal cancer, Karanjia and Heald et al.
128 L. Grimm Jr., J.W. Fleshman / Seminars in Colon and Rectal Surgery 24 (2013) 125–131

reported an overall anastomotic leak rate of 17% (11% major or

clinically apparent). They concluded that a colorectal anastomosis
within 6 cm of the anal verge and use of sigmoid colon were
significant positive predictors of an anastomotic leak.36 This study
and similar ones have led many centers to routinely fashion a
protective diverting ostomy to reduce the clinical significance of
a leak.

5.2. Variability of TME quality

Variability of the quality of the TME in past randomized trials

focusing on adjuvant therapy may have resulted in false conclu-
sions regarding the benefit of the adjuvant therapy in the treat-
ment of rectal cancer. The original Swedish randomized trials
studying the value of radiotherapy utilized intramesorectal sur-
gery for rectal cancer (Stockholm I and II) and showed a reduction
in LR in the radiation groups. However, the LR and rate of APR
performed were very high in the treatment group. The Swedish
TME project utilized extensive training workshops and seminars
on correct TME technique. Martling et al. then reported a series of
381 consecutive patients undergoing curative TME, with an APR
rate of 27% and LR of 6% compared to 55%–60% and 15%,
respectively, in the Stockholm trials. They also reported a reduced
cancer-related death rate of 9% in the TME project compared to
15%–16% in the radiation group of the Stockholm trials. They
concluded that “improved TME technique as a result of a surgical
teaching initiative had a major effect on cancer outcomes.”37
Using the data from the Dutch randomized TME þ /− radio-
therapy trial, Nagtegaal et al. reported on 180 non-irradiated,
“curable” rectal cancer patients that underwent TME. Even with
vigorous surgical training and proctoring of TME technique, only Fig. 4. Nearly Complete/Intramesorectal Plane: moderate bulk to the mesorectum,
57% of specimens examined with Quirke’s “bread-loafing” protocol but irregularity of the mesorectal surface. Moderate coning of the specimen is
allowed. At no site is the muscularis propria visible, with the exception of the
insertion of the levator muscles.38 Personal communication with Quirke P,
University of Leeds.

were considered “complete” mesorectal excisions (Fig. 2), and 24%

of the specimens were judged to be “incomplete” (Fig. 3). While
there were no significant differences in local and distant recur-
rence between “complete” and “nearly complete” (Fig. 4) resec-
tions, there was a significantly increased risk in overall recurrence
(local and distant) in “incomplete” resections vs. “complete” ones
(36.1% vs. 20.3%).38,30

5.3. Functional effects

Removal of the entire rectal vault and the mesorectum has

functional effects, which impact quality of life. The “low anterior
resection syndrome” includes frequent, fractured, urgent stools,
which may be uncontrolled by the sphincter because of a lack of
reservoir and a shortened distal rectal sensory zone. The poorly
functioning anal sphincter complex multiplies the decrease in
quality of life. Temple et al. at Memorial Sloan–Kettering have
developed a scoring system that has helped grade the outcomes
and compare the function in trial settings.39

6. Tumor-specific mesorectal excision

The original description of TME, even for high rectal cancers,

Fig. 3. Incomplete/Muscularis Propria Plane: little bulk to mesorectum with defects
down onto muscularis propria and/or very irregular circumferential resection
margin.38 Personal communication with Quirke P, University of Leeds.
required a very low rectal anastomosis because a complete TME
resulted in a high anastomotic leak rate if the ischemic distal
rectum was not removed. In a prospective series of 45 consecutive
patients undergoing curative TME for rectal and rectosigmoid
cancer, Hainsworth et al. reported a 2-year LR of 11% and an
 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
indicated for upper and rectosigmoid cancers.40
Tumor-specific mesorectal excision has been shown to be
oncologically acceptable for upper rectal and rectosigmoid cancers.
A review of 415 patients undergoing curative surgery alone for
rectal cancer in the Department of Colorectal Surgery at the Mayo
Clinic from 1982 to 1989 showed acceptable outcomes for tumor-
specific TME. For tumors of the middle or lower rectum, patients
underwent complete TME with either coloanal anastomosis (CAA)
or APR, as necessary. Patients with upper rectal cancers underwent
anterior resection (AR) with tumor-specific mesorectal excision by
performing a mesorectal excision to 5 cm below the tumor and
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-
tively, after AR, 6% and 83% after CAA, and 4% and 80% after APR.
They concluded that “appropriate ‘tumor-specific’ mesorectal
excision during AR when the tumor is high in the rectum is
likewise consistent with a low rate of local recurrence and good
long-term survival.”41
6.1. Distal margin
Tumor-specific mesorectal excision is further supported by the
shortening of the necessary distal margin. Multiple studies have
shown that any distal intramural spread of rectal cancer is almost
always within 1.5 cm of the primary tumor, and that when there is
distal spread beyond 1.5 cm, these instances are highly associated
with high grade or widely metastatic tumors, rendering prognosis
poor and resection largely palliative in nature.42–47 The random-
ized prospective clinical trial by the National Surgical Adjuvant
Breast and Bowel Project (NSABP) R03 evaluating adjuvant therapy
in Dukes B and C rectal cancer showed no significant difference in
LR or survival in 181 patients undergoing sphincter-preserving
rectal resections, whether the distal margin was o2 cm, 2–2.9 cm,
or Z 3 cm.47
In the era of neoadjuvant chemoradiotherapy, distal margins
even r 1 cm appear sufficient. In a prospective study of 36
patients with rectal cancer r 8 cm from the anal verge who
underwent chemoradiotherapy prior to resection, Kushinoff et al.
reported no significant difference in LR or disease-free survival
Fig. 5. Tumor-specific mesorectal excision. The distal mesorectum and rectum are
transected at a right angle. Reprinted with permission from Lin AY.66
129
between patients who underwent APR or sphincter-preserving
resection with a distal margin r 1 cm. They concluded that distal
margin r 1 cm is an oncologically sound margin after neoadjuvant
chemoradiation.48 A recent literature review by Park and Kim also
concluded that a distal resection margin of r1 cm is adequate in
patients undergoing curative resection after neoadjuvant chemo-
radiotherapy.49 The American Society of Colon and Rectal Surgeons
recommends a 2-cm distal margin in its most recent Practice
Parameters for the Management of Rectal Cancer. They do state
that smaller margins can be acceptable in certain circumstances, as
the “principle objective of surgical treatment is to obtain clear
surgical margins.”50
7. Laparoscopic TME
The multicenter, randomized, prospective North American
Clinical Outcomes of Surgical Therapy (COST) Study Group and
United Kingdom Medical Research Council Conventional vs.
Laparoscopic-Assisted Surgery in Colorectal Cancer (CLASICC) trials
reported that laparoscopic surgery for colon and colorectal sur-
gery, respectively, are oncologically equivalent to open resec-
tion.51,52 Similarly, several multicenter randomized trials looking
at laparoscopic vs. open resection for rectal cancer are currently
underway, such as the European COLOR II Trial, the Japanese JCOG
study 0404, and the American College of Surgeons Oncology Group
(ACOSOG) trial Z6051.53–55 The endpoints of the European and
Japanese trials are survival and LR. The primary endpoint of the
ACOSOG Z6051 trial is the quality of the surgical specimen
measured by clear circumferential and distal margins and a
complete TME resection.55 In a single-center randomized prospec-
tive trial from Hong Kong looking at laparoscopic vs. open
resection of 403 patients with cancer of the rectosigmoid junction,
Leung et al. showed that laparoscopic resection of rectosigmoid
cancers was technically possible and oncologically safe.56 Separate
prospective studies in England and France both concluded that
laparoscopic TME was technically feasible and oncologically safe in
the treatment of rectal cancer.57–58
Zhou et al. prospectively randomized 171 patients with curable
low rectal cancers in a single Chinese institution to either laparo-
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
8. Near future: Quality analysis and grading of the TME
specimen
With the evidence showing the value of TME and the CRM,
pathologists, led by Quirke and Nagtegaal, have standardized the
reporting of the macroscopic quality of the TME and the micro-
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
The effect of quality of TME and preoperative short-course radiotherapy (PRE) on
3-year LR and disease-free survival (DFS). POST ¼ selective postoperative chemor-
adiotherapy if involved CRM; HR ¼ Hazard Ratio.65
Plane of surgery LR at 3 years DFS at 3 years
N PRE POST HR PRE POST HR
(%) (%) (%) (%)
Mesorectal plane/Complete 596 1 6 4.47 87 80 1.53
Intramesorectal plane/Nearly 382 6 12 2.02 78 75 1.13
Complete
Muscularis propria plane/ 141 9 29 2.76 79 65 1.75
Incomplete
it is recommended that all rectal specimens be graded by specif-
ically trained pathologists for macroscopic quality of the TME as
“complete” (Mesorectal Plane, Fig. 2), “nearly complete” (Intra-
mesorectal Plane, Fig. 3), or “incomplete” (Muscularis Propria
Plane, Fig. 4).38,61,63,64 The CRM is then microscopically assessed
via the “bread loaf slicing” technique developed by Quirke.14,27,61
In a recent abstract on the 3-year results from the ongoing
Medical Research Council (MRC) CR07 trial that randomized
patients with rectal cancer to either short-course preoperative
radiotherapy (PRE) or selective postoperative chemoradiotherapy
if the CRM is involved (POST), Quirke et al. prospectively assessed
the CRM in 1232 patients and the plane of surgery (quality of TME)
in 1119 patients. Adhering to his well-documented pathological
inspection guidelines, Quirke reported a strong association with
both decreased LR and increased 3-year disease-free survival (DFS)
with both the higher quality of surgery and the use of preoperative
short-course radiotherapy (Table 1). He concluded that “for
patients with rectal cancer short-course preoperative radiotherapy
and good quality surgery can almost completely eliminate local
recurrence.”65
These standardized quality measures are a vital part of the
ongoing multicenter, randomized American College of Surgeons
Oncology Group (ACOSOG) trial Z6051 looking at laparoscopic vs.
open TME for curable rectal cancer. Surgeons are credentialed in
this study by review of their operative videos and documentation
of TME in their operative notes. The 3 primary endpoints of this
study are a CRM 4 1 mm, a negative distal margin, and the quality
of the TME. One-third of the TME quality endpoint is based on the
macroscopic photos of the TME.55
9. Summary
Complete, disease-specific mesorectal excision is the standard of
care in the current treatment of rectal cancer. In instances of mid-
and low-rectal cancers, this generally requires total mesorectal
excision. TME plays a vital role in obtaining a negative circum-
ferential resection margin, which significantly decreases local
recurrence and is a valuable prognostic indicator for disease-free
survival and likely overall survival. In the era of TME, selective
neoadjuvant and adjuvant therapy continues to play an important
role. Laparoscopic TME appears to be feasible and oncologically
safe, and several multicenter, randomized trials studying it look to
be completed soon. Finally, TME performed by experts and eval-
uated and reported according to rigorous, standardized patholog-
ical protocols provides significantly improved outcomes and drives
better-informed decision making in regard to adjuvant therapy.
References
1. Amussat JZ. Notes on the possible establishment of an artificial anus in the
lumbar region without entering the peritoneal cavity [in French]. Paris: Lu a
L’Academie Royale de Medecine. 1839 [Reprinted in Corman ML ed. Classic
articles in colonic and rectal surgery. Jean Zulema Amussat 1796–1855. Dis
Colon Rectum 26: 483–487, 1983].
2. Lisfranc J. Memoire sur l'excision de la partie inferieure du rectum devenue
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
Colon Rectum 26: 694–695, 1983].
3. Graney MJ, Graney CM. Colorectal surgery from antiguity to the modern era. Dis
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.
5. Miles WE. Cancer of the rectum (Lettsomian lectures). Trans Med Soc Lond.
1923;46(127): [Reprinted in Miles WE. Cancer of the rectum: being the
Lettsomian lectures delivered before the medical society of London on February
19th, March 7th, and March 26, 1923, London, Harrison and Sons, 1926].
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
rectal cancer. Dis Colon Rectum. 1999;42:563–578.
8. Lloyd-Davies OV. Lithotomy-Trendelenburg position for resection of rectum and
lower pelvic colon. Lancet. 1939;237:74–76.
9. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol. 1932;35
(3):323–332 [Reprinted in Corman ML ed. Classic articles in colonic and rectal
surgery. The classification of cancer of the rectum. Dis Colon Rectum 23(8):
605–611, 1980].
10. Dixon CF. Anterior resection for malignant lesions of the upper part of the
rectum and lower part of the sigmoid. Ann Surg. 1948;128(3):425–442.
11. Goligher JC, Dukes CE, Bussey HJ. Local recurrences after sphincter saving
excisions for carcinoma of the rectum and rectosigmoid. Br J Surg.
1951;39:199–211.
12. Fain SN, Patin CS, Morgenstern L. Use of a mechanical suturing apparatus in low
colorectal anastomosis. Arch Surg. 1975;110(9):1079–1082.
13. Pollet WG, Nicholls RJ. The relationship between the extent of distal clearance
and survival and local recurrence rates after curative anterior resection for
carcinoma of the rectum. Ann Surg. 1983;198(2):159–163.
14. Quirke P, Durdey P, Dixon MF, et al. Local recurrence of rectal adenocarcinoma
due to inadequate surgical resection. Histopathological study of lateral tumour
spread and surgical excision. Lancet. 1986;2(8514):996–999.
15. Adam IJ, Mohamdee MO, Martin IG. Role of circumferential margin involve-
ment in the local recurrence of rectal cancer. Lancet. 1994;344
(8924):707–711.
16. Heald RJ. A new approach to rectal cancer. Br J Hosp Med. 1979;22(3):277–281.
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
JE, (eds): Master Techniques in General Surgery: Colon and Rectal Surgery:
Abdominal Operations. Philadelphia, PA: Lippincott Williams & Wilkins; 2012.
p. 127–131.
19. Heald RJ, Husband EM, Ryall RDH. The mesorectum in rectal cancer surgery—
the clue to pelvic recurrence? Br J Surg. 1982;69:613–616.
20. Heald RJ, Ryall RDH. Recurrence and survival after total mesorectal excision for
rectal cancer. Lancet. 1986;327(8496):1479–1482.
21. Arbman G, Nilsson E, Hallbook, et al. Local recurrence after total mesorectal
excision for rectal cancer. Br J Surg. 1996;83(3):375–379.
22. Kockerling F, Reymond MA, Altendorf-Hofmann A, et al. Influence of surgery on
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.
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.
25. Arenas RB, Fichera A, Mhoon D, et al. Total mesorectal excision in the surgical
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
mesorectal excision of rectal cancer with curative intent. Predictor of survival
but not local recurrence? Dis Colon Rectum. 1998;41(8):979–983.
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
(2):127–131.
28. Nagtegaal ID, Marijnen CA, Kranenbarg EK, et al. Circumferential margin
involvement is still an important predictor of local recurrence in rectal
carcinoma: not one millimeter but two millimeters is the limit. Am J Surg
Pathol. 2002;26(3):350–357.
29. McCall JL, Cox MR, Wattchow DA. Analysis of local recurrence rates after
surgery alone for rectal cancer. Int J Colorectal Dis. 10(3):126–132.
30. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy
combined with total mesorectal excision for resectable rectal cancer. N Engl J
Med. 2001;345(9):638–646.
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
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
(10):1140–1145.
33. Goligher JC, Graham NG, DeDombal FT. Anastomotic dehiscence after anterior
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
34. Fielding LP, Stewart-Brown S, Blesovsky L, et al. Anastomotic integrity after
operations for large-bowel cancer: a multicentre study. Br Med J. 1980;281
(6237):411–414.
35. Vignali A, Fazio VW, Lavery IC, et al. Factors associated with the occurrence of
leaks in stapled rectal anastomoses: a review of 1014 patients. J Am Coll Surg.
1997;185(2):105–113.
36. Karanjia ND, Corder AP, Bearn P, et al. Leakage from stapled low anastomosis
after total mesorectal excision for carcinoma of the rectum. Br J Surg. 1994;81
(8):1224–1226.
37. Martling AL, Holm T, Rutqvist LE, et al. Effect of a surgical training programme
on outcome of rectal cancer in the County of Stockholm. Stockholm Colorectal
Cancer Study Group, Basingstoke Bowel Cancer Research Project. Lancet.
2000;356(9224):93–96.
38. Nagtegaal ID, van de Velde CJ, van der Worp E, et al. Macroscopic evaluation of
rectal cancer resection specimen: clinical significance of the pathologist in
quality control. J Clin Oncol. 2002;20(7):1729–1734.
39. Temple LK, Bacik J, Savatta SG, et al. The development of a validated instrument
to evaluate bowel function after sphincter-preserving surgery for rectal cancer.
Dis Colon Rectum. 2005;48(7):1353–1365.
40. Hainsworth PJ, Egan MJ, Cunliffe WJ. Evaluation of a policy of total mesorectal
excision for rectal and rectosigmoid cancers. Br J Surg. 1997;84(5):652–656.
41. Zaheer S, Pemberton JH, Farouk R, et al. Surgical treatment of adenocarcinoma
of the rectum. Ann Surg. 1998;227(6):800–811.
42. Black WA, Waugh JM. The intramural extension of carcinoma of the descending
colon, sigmoid, and rectosigmoid; a pathologic study. Surg Gynecol Obstet.
1948;87(4):457–464.
43. Quer EA, Dahlin DC, Mayo CW. Retrograde intramural spread of carcinoma of
the rectum and rectosigmoid; a microscopic study. Surg Gynecol Obstet.
1953;96(1):24–30.
44. Grinnell RS. Distal intramural spread of carcinoma of the rectum and recto-
sigmoid. Surg Gynecol Obstet. 1954;99(4):421–430.
45. Williams NS, Dixon MF, Johnston D. Reappraisal of the 5 centimetre rule of
distal excision for carcinoma of the rectum: a study of distal intramural spread
and of patients' survival. Br J Surg. 1983;70(3):150–154.
46. Madsen PM, Christiansen J. Distal intramural spread of rectal carcinomas. Dis
Colon Rectum. 1986;29(4):279–282.
47. Wolmark N, Fisher B. An analysis of survival and treatment failure following
abdominoperineal and sphincter-saving resection in Dukes' B and C rectal
carcinoma. A report of the NSABP clinical trials. National Surgical Adjuvant
Breast and Bowel Project. Ann Surg. 1986;204(4):480–489.
48. Kushinoff B, Maghfoor I, Miedema B, et al. Distal margin requirements after
preoperative chemoradiotherapy for distal rectal carcinomas: are o or ¼ 1 cm
distal margins sufficient? Ann Surg Oncol. 2001;8(2):163–169.
49. Park IJ, Kim JC. Adequate length of the distal resection margin in rectal cancer:
from the oncological point of view. J Gastrointest Surg. 2010;14(8):1331–1337.
131
50. Tjandra JJ, Kilkenny JW, Buie WD, et al. Practice parameters for the manage-
ment of rectal cancer. Dis Colon Rectum. 2005;48(3):411–423 [Revised].
51. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparos-
copically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350
(20):2050–2059.
52. Jayne DG, Guillou PJ, Thorpe H. Randomized trial of laparoscopic-assisted
resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial
Group. J Clin Oncol. 2007;25(21):3061–3068.
53. Buunen M, Bonjer HJ, Hop WC, et al. COLOR II. A randomized clinical trial
comparing laparoscopic and open surgery for rectal cancer. Dan Med Bull.
2009;56(2):89–91.
54. Kitano S, Inomata M, Sato A, et al. Randomized controlled trial to evaluate
laparoscopic surgery for colorectal cancer: Japan Clinical Oncology Group Study
JCOG 0404. Jpn J Clin Oncol. 2005;35(8):475–477.
55. Fleshman J. American College of Surgeons Oncology Group (ACOSOG)-Z6051. A
phase III prospective randomized trial comparing laparoscopic-assisted resec-
tion versus open resection for rectal cancer. Available at: 〈http://clinicaltrials.
gov/ct2/show/NCT00726622〉.
56. Leung KL, Kwok SP, Lam SC. Laparoscopic resection of rectosigmoid carcinoma:
prospective randomised trial. Lancet. 2004;363(9416):1187–1192.
57. Hartley JE, Mehigan BJ, Qureshi AE, et al. Total mesorectal excision: assessment
of the laparoscopic approach. Dis Colon Rectum. 2001;44(3):315–331.
58. Bretagnol F, Rullier E, Couderc P, et al. Technical and oncological feasibility of
laparoscopic total mesorectal excision with pouch coloanal anastomosis for
rectal cancer. Colorectal Dis. 2003;5(5):451–453.
59. Zhou ZG, Hu M, Li Y, et al. Laparoscopic versus open total mesorectal excision
with anal sphincter preservation for low rectal cancer. Surg Endosc. 2004;18
(8):1211–1215.
60. Braga M, Frasson M, Vignali A. Laparoscopic resection in rectal cancer patients:
outcome and cost-benefit analysis. Dis Colon Rectum. 2007;50(4):464–471.
61. Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the
modern treatment of rectal cancer? J Clin Oncol. 2008;26(2):303–312.
62. Hoorens A, De Ridder M, Jouret-Mourin A, et al. Pathological assessment of the
rectal cancer resection specimen. Bel J Med Oncol. 2009;3(6):251–260.
63. Parfitt JR, Driman DK. The total mesorectal excision specimen for rectal cancer:
a review of its pathological assessment. J Clin Pathol. 2007;60(8):849–855.
64. Jass JR, O'Brien MJ, Riddell RH. Recommendations for the reporting of surgically
resected specimens of colorectal carcinoma. Hum Pathol. 2007;38(4):537–545.
65. Quirke P, Sebag-Montefiore D, Steele R, et al. Local recurrence after rectal
cancer resection is strongly related to the plane of surgical dissection and is
further reduced by preoperative short course radiotherapy: preliminary results
of the MRC CR07 trial. J Clin Oncol. 2006;24:149s [suppl; abstr 3512].
66. Lin AY. Open low anterior resection of rectum. In: Fleshman JW, (ed). Atlas of
Surgical Techniques for the Colon, Rectum, and Anus. Philadelphia, PA: Elsevier
Saunders; 2013. p. 156–177.