SPECIAL ARTICLE
Guidelines 2000 for Colon and Rectal Cancer Surgery
Heidi Nelson, Nicholas Petrelli, Arthur Carlin, Jean Couture, James Fleshman,
Jose Guillem, Brent Miedema, David Ota, Daniel Sargent
Background: Oncologic resection techniques affect outcome
for colon cancer and rectal cancer, but standardized guide-
lines have not been adopted. The National Cancer Institute
sponsored a panel of experts to systematically review current
literature and to draft guidelines that provide uniform defi-
nitions, principles, and practices. Methods: Methods were
similar to those described by the American Society of Clini-
cal Oncology in developing practice guidelines. Experts rep-
resenting oncology and surgery met to review current litera-
ture on oncologic resection techniques for level of evidence
(IV, where I is the best evidence and V is the least compel-
ling) and grade of recommendation (AD, where A is based
on the best evidence and D is based on the weakest evidence).
Initial guidelines were drafted, reviewed, and accepted by
consensus. Results: For the following seven factors, the level
of evidence was II, III, or IV, and the findings were generally
consistent (grade B): anatomic definition of colon versus rec-
tum, tumornodemetastasis staging, radial margins, adju-
vant R0 stage, inadvertent rectal perforation, distal and
proximal rectal margins, and en bloc resection of adherent
tumors. For another seven factors, the level of evidence was
II, III, or IV, but findings were inconsistent (grade C): lap-
aroscopic colectomy; colon lymphadenectomy; level of
proximal vessel ligation, mesorectal excision, and extended
lateral pelvic lymph node dissection (all three for rectal can-
cer); no-touch technique; and bowel washout. For the other
four factors, there was little or no systematic empirical evi-
dence (grade D): abdominal exploration, oophorectomy, ex-
tent of colon resection, and total length of rectum resected.
Conclusions: The panel reports surgical guidelines and defi-
nitions based on the best available evidence. The availability
of more standardized information in the future should allow
for more grade A recommendations. [J Natl Cancer Inst
2001;93:58396]
During 2000, in the United States, 130 200 new cases of
colon cancer and rectal cancer were reported (1). On the basis
of past experience, an estimated 90%92% of patients with co-
lon cancer and 84% of patients with rectal cancer are treated
surgically (2,3). Although surgery may be performed for pallia-
tive control of symptoms in advanced cases, in most circum-
stances, it is performed with curative intent. Surgery, in fact,
remains the primary modality of treatment for malignancies of
the lower gastrointestinal tract, and standard resection is the only
therapy required for early-stage cancer. As the stage of the tumor
increases in terms of depth of penetration and lymph node in-
volvement, the chance of cure with surgery alone diminishes;
rates of local recurrence and survival are dependent on the tu-
mornodemetastasis (TNM) stage. Adjuvant therapies have
been shown to increase the probability of cure in surgically
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
treated patients who have a high risk of recurrence (4). Parallel
to the efforts in adjuvant therapies, there is renewed interest in
examining whether surgical techniques have been fully opti-
mized. Could improvements in surgery accomplish further gains
in cancer outcome?
It is well established that surgical variation exists and can be
measured for rates of both local recurrence and survival. Nu-
merous studies (59) have reported local recurrence rates for
rectal cancer ranging from as low as 4% to as high as 55% based
solely on surgeon differences. Even within U.S. cooperative
groups, modest degrees of surgeon variability have been re-
ported (10).
Ample evidence exists to support the premise that surgical
techniques clinically significantly affect cancer outcome, yet no
standardized and accepted guidelines have ever been proposed.
If improvements in surgical outcomes are to be achieved, it
is essential that the components of surgery that contribute
to local and systemic treatment failure be critically examined.
Toward that end, the National Cancer Institute (Bethesda, MD)
sponsored a panel of experts to systematically review the litera-
ture and to draft guidelines. These guidelines are intended to
enhance surgical quality control and to facilitate the homogene-
ity of groups in clinical trials. Guidelines are needed to help
reduce surgical variation and to help standardize documentation
to minimize inconsistencies in staging patients with colorectal
cancer.
The attitudes toward and methods for practice guidelines
were followed as described previously by the American
Society of Clinical Oncology (11). It must be recognized that
there are limitations in the level of evidence supporting specific
surgical practices, since not all variables discussed are well
critiqued with the use of a single level of evidence scoring
system. Therefore, it is the intent of this article to provide a
framework of uniform definitions, principles, and practices of
oncologic colon and rectal resection, including documentation.
For areas in which evidence is insufficient for the definitive
recommendation of guidelines, future research should be con-
sidered.
Affiliations of authors: H. Nelson, D. Sargent, Mayo Clinic, Rochester, MN;
N. Petrelli, Roswell Park Cancer Institute, Buffalo, NY; A. Carlin, Wayne State
University, Detroit, MI; J. Couture, Mount Sinai Hospital, Toronto, ON, Canada;
J. Fleshman, Barnes-Jewish Hospital, St. Louis, MO; J. Guillem, Memorial
Sloan-Kettering Cancer Center, New York, NY; B. Miedema, University of
Missouri, Columbia; D. Ota, Ellis Fischel Cancer Center, Columbia, MO. (These
authors make up the Writing Committee on behalf of the Expert Panel. All
members of the Expert Panel and their institutional and Cancer Cooperative
Group affiliations are listed in Appendix 1.)
Correspondence to: Heidi Nelson, M.D., Mayo Clinic, 200 First St., S.W.,
Rochester, MN 55905 (e-mail: nelsonh@mayo.edu).
See Notes following References.
Oxford University Press
SPECIAL ARTICLE 583
METHODS
Methods similar to those used by the American Society of Clinical Oncology
in developing practice guidelines (12) were used. These methods are described
in detail below.
Panel Composition
The guidelines were developed by a panel of surgeons representing each of the
National Cancer Institute-sponsored adult cancer cooperative groups (see Ap-
pendix 1). In addition, each of the three major surgical societies (Society for
Surgery of the Alimentary Tract, American Society of Colon and Rectal Sur-
geons, and Society of Surgical Oncology) and the National Cancer Institute were
represented. Because a secondary goal of this initiative was the development of
surgical data collection forms, biostatisticians and data managers from coopera-
tive group operations offices were included.
Process Overview
The guidelines were developed initially during a 2-day meeting and were
formalized through a series of subsequent discussions devoted to resolving re-
maining issues. Before the initial meeting, a list of guidelines to be developed,
as well as the data collection forms for surgically related data from each of the
cooperative groups, was circulated to the panel members.
Review of Available Data
To evaluate the available evidence, the panel followed the process for guide-
line development established by the American College of Chest Physicians
(13,14); this process was used previously for developing the American Society
of Clinical Oncology guidelines for colorectal cancer surveillance (11). The
process involves a systematic consideration of the level and grade of evidence
(IV) available for each issue (Table 1) (13,14). Outcomes of primary interest in
determining guidelines were overall survival and local tumor recurrence; con-
sideration was also given to the patients quality of life and the cost and feasi-
bility of implementing any guideline.
Information from the published literature as of April 1999 was synthesized for
the creation of these guidelines. All relevant literature, both prospective and
retrospective, was included in the review. Unpublished data from several sources
were included as well, and attention was given to the appropriate weight such
evidence should warrant. Before the meeting, panel members comprehensively
reviewed the published works on each of the predefined topics.
Initial guidelines were developed by working groups focused on colon and
rectal issues. These initial guidelines were circulated and reviewed by the entire
panel before a joint meeting of the working groups. At this joint meeting,
recommendations were reviewed and revised. Revised guidelines were circu-
Table 1. Levels of evidence and grades of recommendation*
Level Source of evidence
I Meta-analysis of multiple well-designed, controlled studies;
randomized trials with low false-positive and low false-negative
errors (high power)
II At least one well-designed experimental study; randomized trials
with high false-positive or high false-negative errors or both
(low power)
III Well-designed, quasi-experimental studies, such as nonrandomized,
controlled, single-group, preoperativepostoperative comparison,
cohort, time, or matched casecontrol series
IV Well-designed, nonexperimental studies, such as comparative and
correlational descriptive and case studies
V Case reports and clinical examples
Grade Grade of recommendation
A Evidence of type I or consistent findings from multiple studies of
type II, III, or IV
B Evidence of type II, III, or IV and generally consistent findings
C Evidence of type II, III, or IV but inconsistent findings
D Little or no systematic empirical evidence
*Data from Cook et al. (13) and Sackett (14).
584 SPECIAL ARTICLE
lated through several iterations, and all panel members had the opportunity to
comment on the final recommendations.
Data Collection Forms
A secondary goal of the conference was to standardize the process of collect-
ing surgically relevant data on National Cancer Institute-sponsored cooperative
group clinical trials. The decision was made to classify trials as to whether a
surgical question was the primary or the secondary hypothesis, with a different
level of data collection for each. Data forms were developed on the basis of
integrating the new guidelines into the various current cooperative group data
collection systems. Data elements defined as a result of the guidelines are in the
process of being incorporated into the National Cancer Institutes Common Data
Elements initiative.
ANATOMIC DEFINITIONS: COLON VERSUS RECTUM
Guidelines: There are many discrepancies in the literature for
defining the junction of the colon and rectum. This situation
creates uncertainties when assigning patients to colon or rectal
protocols. The following definitions are preferred: for colon,
greater than 12 cm from anal verge by rigid proctoscopy; for
rectum, 12 cm or less from anal verge by rigid proctoscopy.
Level of evidence: IVV.
Grade of recommendation: B.
Rationale: These definitions are based on the finding that
colorectal cancers located above 12 cm from the anal verge have
a local recurrence rate more consistent with patterns of recur-
rence in the colon than in the rectum. In the study by Pilipshen
et al. (15), the local recurrence rate was 9.6% for lesions located
above 12 cm compared with 30.1% and 30.7% for mid- and
low-rectal cancers, respectively. Several retrospective studies
(1521) support this observation.
Anatomic definition of the rectum is highly variable. Both
endoscopic and intraoperative criteria are used. For intraopera-
tive definitions, the beginning of the rectum or the end of the
colon has been descriptive and imprecise. The end of the taeniae
coli or peritoneal reflection has been used to determine that
location, but both are highly variable owing to differences in
age, sex, and gynecologic and obstetric conditions. Flexible sig-
moidoscopy introduces variability in the level of the rectum due
to technique. Rigid proctoscopy (suggested in the left decubitis
position) is thought to be a highly reproducible method of de-
termining the level of the rectum and is less dependent on the
operator or on the technique. The anal verge is the preferred anal
landmark, since the edge of the tumor and the verge can be
visualized simultaneously during rigid proctoscopy.
STAGING
TNM Staging
Guidelines: The TNM classification of tumors described by
the American Joint Committee on Cancer (AJCC) (22) is rec-
ommended for tumor staging (standard AJCC language for tu-
mor depth was accepted) (Table 2).
Extent of Resection (R)
Guidelines: In addition to tumor stage, any tumor not re-
moved intraoperatively strongly influences prognosis and
therapy. The absence or presence of residual tumor after surgical
treatment is described by the letter R. Accepted guidelines from
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
 Table 2. TNM staging definitions* have an incomplete resection for cure. Incomplete resection (R1
and R2) does not change the TNM stage, but it does affect
Stage Definition
curability.
Primary tumor (T) Level of evidence: III.
TX Primary tumor cannot be assessed Grade of recommendation: B.
T0 No evidence of primary tumor
Tis Carcinoma in situ: intraepithelial or invasion Rationale: Numerous studies, including the landmark study
of lamina propria by Quirke et al. (23) in 1986, clearly demonstrate the importance
T1 Tumor invades submucosa of optimal pathologic assessment of lateral, radial, and, most
T2 Tumor invades muscularis propria recently, circumferential margins of resection, since margins
T3 Tumor invades through muscularis propria into
the subserosa or into nonperitonealized positive for disease have been clearly associated with an in-
pericolic or perirectal tissues creased rate of local and distal treatment failure. In various stud-
T4 Tumor perforates visceral peritoneum or ies (2325), the local recurrence rate after resection of a rectal
directly invades other organs or structures
cancer was 29%, 78%, and 85% for cases with margins positive
Regional lymph nodes (N) for disease compared with 3%, 8%, and 10%, respectively, for
NX Regional lymph nodes could not be assessed
N0 No regional lymph node metastases cases with margins negative for disease.
N1 Metastases in one to three regional lymph Furthermore, Hall et al. (26) suggest that, after a total meso-
nodes rectal excision, both disease-free survival and mortality were
N2 Metastases in four or more regional lymph
nodes
clinically significantly related to margin involvement.
Distant metastases (M) Adjuvant R0 Stage
MX Distant metastases could not be assessed
M0 No distant metastases Guidelines: Adjuvant therapies requiring complete resec-
M1 Distant metastases tion should refer to surgical cases that are strictly R0. A case
Extent of resection (R) would not be considered R0 (i.e., a complete resection) if any
RX Presence of residual tumor cannot be assessed of the following are evident from the surgical or pathology
R0 No residual tumor
R1 Microscopic residual tumor reports: non-en-bloc resection, radial margin positive for dis-
R2 Macroscopic residual tumor ease, bowel margin positive for disease, residual lymph node
disease, or NX (incomplete staging). R definitions are based
*Standard American Joint Committee on Cancer language was accepted. on the accepted AJCC Prognostic Factors Consensus Confer-
A tumor nodule greater than 3 mm in diameter in perirectal or pericolic ence Colorectal Working Group definitions (27).
adipose tissue without histologic evidence of a residual lymph node in the nodule
Level of evidence: IV.
is classified as residual lymph node metastases; however, a tumor nodule up
to 3 mm in diameter is classified in the T category as discontinuous extension Grade of recommendation: B.
(i.e., T3). Rationale: Prognostic profiles for tumors according to the
Cases are not considered R0 (complete resection) if the following are evi- TNM stage assume complete tumor resection (i.e., the absence
dent: non-en-bloc resection, radial or bowel margin positive for disease, residual of residual disease). The rationale for each component of com-
lymph node disease, or NX (incomplete staging). plete resection is provided below.
SURGICAL TECHNIQUESCOLON
the AJCC Prognostic Factors Consensus Conference were rec-
ommended to describe the extent of resection (Table 2). This section discusses surgical techniques relevant only to
Level of evidence: IV.1 the colon (see also Surgical TechniquesColon and Rectum
Grade of recommendation: B. below).
Rationale: The above guidelines are based on the AJCC Can-
Ideal Bowel Resection and Margins
cer Staging Manual (22) published in 1997 and approved by
national TNM committees. Guidelines: The ideal extent of a bowel resection is defined
Radial Margin by removing the blood supply and the lymphatics at the level of
the origin of the primary feeding arterial vessel. When the pri-
Guidelines: T4 lesions represent a complex group and should mary tumor is equidistant from two feeding vessels, both vessels
be considered separately from other T lesions. Radial tumor-free should be excised at their origin. Resection is substandard when
margin should be described and must be histologically free of removal of the primary tumor with its named vessel and adjacent
disease for the resection to be considered curative. lymph nodes is incomplete. Ideally, the inferior mesenteric ar-
The surgeon should be aware of the radial margins at the time tery (IMA) should be excised at its origin, but this is not man-
of the surgical procedure. The specimen should be labeled, and dated by available supportive evidence.
areas of concern should be marked so that the specimen can be Although there is some debate, 5 cm of normal bowel on
properly oriented, allowing areas of specific concern to be cor- either side of the primary colon tumor appears to be adequate to
rectly identified by the pathologist. minimize anastomotic recurrences. The length of ileum resected
Resections should be categorized as follows: R0all gross does not appear to affect local recurrence. Therefore, the shortest
disease resected by en bloc resection with margins histologically length of ileum needed to perform the surgical procedure should
free of disease; R1all gross disease resected by en bloc resec- be excised to prevent malabsorption syndromes.
tion with margins histologically positive for disease; and R2 Patients with multiple (i.e., two or more) colon cancers or
residual gross disease remains unresected. those with hereditary nonpolyposis colorectal cancer should be
Patients who do not have histologic assessment of radial tu- considered for a total abdominal colectomy with ileorectal anas-
mor margin or who had an R1 or R2 resection are considered to tomosis. Patients with ulcerative colitis should have a procto-

Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001 SPECIAL ARTICLE 585
colectomy with or without restoration. Stratification of patients
with multiple polyps or cancers is recommended for patients
entered in clinical trials.
The fresh specimen should be restored as best as possible to
its normal anatomy to allow measurement of the full-thickness
margin by the pathologist.
Level of evidence: IV.
Grade of recommendation: D; panel consensus.
Rationale: The length of bowel to be removed will be dic-
tated by the removal of the arterial supply of the colon, which
parallels the lymphatic drainage. Five to 10 cm of normal bowel
on either side of the primary tumor appears to be a minimum
length to remove the epicolic and paracolic (along the marginal
vessel) lymph nodes and to minimize anastomotic recurrences
(28,29). This length may have to be extended, depending on the
lymphadenectomy performed. A minimum length of ileum
should be resected to avoid malabsorption syndromes, because
the length of ileum resected does not appear to affect local
recurrence in tumors of the ascending colon. The basis of this
recommendation comes mainly from a retrospective analysis of
pathologic specimens and mapping of the lymphatic metastases
(30,31). Because the length of bowel resected and the extent of
lymphadenectomy performed are so closely associated, it is not
possible to assess the independent impact specifically of bowel
margins on survival or recurrence.
Lymphadenectomy
Guidelines: Lymph node resection carries with it prognostic
and therapeutic implications. An appropriate lymph node resec-
tion should extend to the level of the origin of the primary
feeding vessel. In all cases for cure, the lymph node resection
should be radical and the lymph nodes should be removed en
bloc.
Lymph nodes at the origin of feeding vessels (apical nodes)
should be removed when feasible and tagged for pathologic
evaluation. Lymph nodes suspected of being positive for disease
outside the field of resection need to be sampled or have
a biopsy. If biopsy results of the suspected lymph nodes are
positive for disease and the lymph nodes are resected along with
the apical nodes, the resection is considered to be complete (R0).
If biopsy results of the suspected lymph nodes are positive for
disease or are clinically involved and the lymph nodes are not
resected along with the positive apical nodes, the resection
is incomplete. If biopsy results of the suspected lymph nodes are
negative for disease and the apical nodes positive for disease
are resected, the resection is considered to be complete (R0).
If biopsy results for lymph nodes left behind are positive for
disease, the resection is incomplete (R2). Patients with R1 or R2
resections are not considered to be eligible for adjuvant trials.
For adjuvant trials, a minimum of one lymph node must be
examined for entry into a trial. For surgical trials or for entry into
a colon adjuvant trial in which the lymph nodes are negative for
disease, a minimum of 12 nodes must be examined. The TNM
staging system should be used for all colorectal cancer trials.
Level of evidence: IIIIV.
Grade of recommendation: C.
Rationale: Only one randomized clinical trial (32) so far has
assessed the value of a radical lymphadenectomy for left-sided
colon cancer. There was no evidence of a benefit for a wider
lymphadenectomy. Several retrospective studies (3337) have
yielded conflicting results on the value of extended lymphade-
586 SPECIAL ARTICLE
nectomy; however, if any benefit is present, it is in Dukes stage
C disease. The potential morbidity of an extended lymphade-
nectomy does not appear to be prohibitive when it is performed
by experts but remains to be explored. The panel agreed that an
important value of lymphadenectomy is in staging. The apical
node may also have prognostic significance in addition to the
number of lymph nodes positive for disease in the specimen
(38). Therefore, all lymph nodes suspected of being positive for
disease beyond the field of resection need a biopsy if feasible.
To achieve a high degree of accuracy (>90%), a minimum of 12
lymph nodes negative for disease must be examined to confirm
that the disease does not involve the nodes (39).
Laparoscopic Colectomy
Guidelines: Owing to the evolving nature of this technology
and technique, the consensus is that laparoscopic colon cancer
resection be confined to clinical trials at this time. Recurrence of
disease at trocar sites continues to be a concern. This is an
unresolved issue.
Surgeon credentialing is an important facet with this new
approach and technology. Individual experience should be docu-
mented by cases and video presentation.
Level of evidence: IVV.
Grade of recommendation: D; panel consensus.
Rationale: Laparoscopic colectomy for cancer is currently
undergoing rigorous study in the United States (40,41), Europe
(42), Scandinavia (40), and Australia (40). There are no results
from the randomized, prospective trials about treatment of
cancer for cureeither short-term or long-term. Several small
randomized, controlled trials (4346) have produced early data
suggesting that laparoscopic colectomy for cancer is safe, offers
improved early recovery, and has a low rate of implantation of
cancer at the trocar site. There are no randomized, controlled
trials evaluating the laparoscopic resection of rectal cancer.
There are no long-term data about disease-free survival after
laparoscopic colectomy for curable cancer.
Prospective and retrospective reviews of large series of pa-
tients who have had laparoscopic resection for colorectal cancer
(4752) suggest that implantation of cancer at trocar sites can
be maintained at a low rate, and preliminary survival rates of
patients are similar to historical series of open resections for
cancer. Even so, anecdotal reports of tumor recurrence at trocar
sites (5356) have raised the awareness of surgeons that this
technique has potentially adverse effects on outcomes. Experi-
mental models suggest that implantation of tumors at trocar sites
is related to technique and depends on the presence of free cells
within the peritoneal cavity and on the rapid distribution of
cells throughout the cavity by the pneumoperitoneum and that
implantation can be reduced by local treatment of trocar sites to
prevent tumor adherence or contamination of the wound (45,57
64). The effect of laparoscopic conditions is variable and de-
pends on the gas used, the tumor model, and the conditions of
the experiment itself (65).
The learning curve for laparoscopic colectomy has been es-
timated to be 3550 procedures (66). As young surgeons in
training gain experience in other advanced procedures, this
quantity may decrease. The current randomized, controlled
trials require credentialing of surgeons by submission of at least
20 surgical reports of laparoscopic colectomy that meet estab-
lished technical requirements, including tissue handling, intra-
corporeal vessel control with proximal vessel ligation, central
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
structure identification, resection of margins of bowel and mes-
entery, and containment of tumor spillage (41). Video documen-
tation is also required.
SURGICAL TECHNIQUESRECTUM
This section discusses surgical techniques relevant only to the
rectum (see also Surgical TechniquesColon and Rectum
below). The goal of surgery is complete removal of the primary
tumor, its named vessel(s), associated lymph nodes, and the
appropriate amount of mesorectum.
Length of Bowel
Guidelines: The length of bowel resection was reviewed, and
there were no supporting data to indicate that length of bowel
had an effect on local control and 5-year survival.
Level of evidence: IV.
Grade of recommendation: D.
Rationale: The length of bowel resected during a resection of
the rectum for a rectal cancer is influenced by the available
blood supply after appropriate vascular ligation and mesenteric
resection. After proximal margins of 5 cm and distal margins of
2 cm are obtained, there is no advantage to resecting additional
length of colon or rectum (see below) (67). The main emphasis
in determining the appropriate length of bowel resection should
be to obtain clear surgical margins and yield an R0 resection (no
residual tumor) (68).
Distal and Proximal Bowel Margins
Guidelines: The ideal distal margin length is 2 cm or greater
from the transected mucosal edge to the distal edge of the pri-
mary tumor (Table 3). This length is measured in the fresh,
anatomically restored ex vivo condition or in the formalinized,
fixed specimen with the use of a correction factor of 12% re-
duction for anatomically restored, fixed specimens compared
with 50% reduction for nonrestored, fixed specimens. The distal
edge is the transected full-thickness edge and does not include
the tissue doughnut from the endoluminal stapler. For tumors of
the distal rectum (<5 cm from the anal verge), the minimally
acceptable length of the distal margin is 1 cm in the fresh,
anatomically restored ex vivo condition or in the equivalent for-
malinized, fixed specimen. A 1-cm margin is not advised in
cases of large, bulky tumors or in cases with adverse histologic
features, such as poorly differentiated tumors or tumors with
lymphovascular or neural invasion. With regard to histologic
assessment of distal margins, all patients must have microhisto-
pathologic evaluation of the distal margin by a review of sec-
tions of either permanently fixed tissue or frozen tissue. If the
distal margin is 12 cm, an intraoperative evaluation of frozen
Table 3. Distal and proximal bowel margins for resection of rectal tumors*
Length, cm
Margin Distal Proximal
Ideal 2 5
Minimally acceptable 1 5
*Current data indicate that margin standards are equally applicable to patients
receiving preoperative radiation therapy.
For tumors of the distal rectum where sphincter preservation is an issue.
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
tissue section of the distal margin nearest to the tumor is rec-
ommended.
Level of evidence: IIIIV.
Grade of recommendation: B.
Rationale: Proximal and distal bowel margins are influenced
primarily by the level of vascular ligation and excision of distal
mesorectum in proximal rectal cancers and mid-rectal cancers.
A minimum 5-cm bowel margin has been recommended on the
basis of the work by Grinnell (67), in which intramural extension
was estimated to occur in 12% of cases. The 5-cm rule has been
questioned, especially in the distal rectal cancer in which a 5-cm
margin would necessitate excision of the anal sphincters. Several
studies (6972) have shown that distal intramural spread is rare
and is found beyond 1 cm in only 4%10% of rectal cancers.
Subsequently, survival and local recurrence have been shown to
be acceptable with a 2-cm or greater distal bowel margin (73
76). If distal spread does occur beyond 1.5 cm, it is usually from
a poorly differentiated cancer and the prognosis is poor, regard-
less of the length of the distal margin (71). Therefore, it is
currently accepted that 1) distal intramural spread beyond 1 cm
occurs rarely, 2) distal spread beyond 1 cm is associated with
tumors of advanced stage or histologically aggressive disease,
and 3) the associated poor prognosis is not improved by a longer
distal margin (77). A 1-cm distal margin may be adequate
(73,74). With preoperative radiation therapy and chemotherapy,
a simple, clear margin may be adequate, but this has not been
accepted as a general guideline (78).
Level of Proximal Lymphovascular Ligation for
Rectal Cancer
Guidelines: Available evidence suggests that an appropriate
proximal lymphatic resection for rectal cancer is provided by the
removal of the blood supply and lymphatics up to the level of
the origin of the primary feeding vessel. For rectal cancer, this is
at the origin of the superior rectal artery, which is immediately
distal to the takeoff of the left colic artery. There is a lack of
evidence about the benefit of ligating the IMA at its origin. This
is a valid statement for patients who do not have clinically
suggestive lymph node disease. In the context of lymph nodes
clinically suggestive of disease, we recommend the removal of
all lymph node disease suspicious for metastasis as is technically
possible. Suspicious periaortic nodes should have a biopsy for
staging.
Level of evidence: IIIII.
Grade of recommendation: C.
Rationale: The recommended level of proximal vascular
ligation for rectal cancer is at the origin of the primary feeding
vessel (superior rectal artery). This recommendation is based
on the same data used to recommend primary feeding vessel
ligation for colon cancer. The data from a French multicenter,
randomized trial (comparing left colectomy and ligation of the
IMA with segmental colectomy and ligation of the primary feed-
ing vessel) show no statistically significant difference in long-
term (12 years) survival (32). A large series from Columbia-
Presbyterian Hospital (New York, NY) showed improved
survival only for patients with stage II rectal cancer who had
high IMA ligation. Stage III disease was not affected by high
ligation at the IMA (79). A more accurate staging and prognosis
may be obtained by high ligation, but survival does not seem to
be affected (80). Stage migration may affect overall outcome
because of improved staging and lead time bias (81). All lymph
SPECIAL ARTICLE 587
nodes suspicious for metastasis beyond the origin of the feeding
vessel should have a biopsy or should be removed, or the level
of resection should be extended to include the worrisome lymph
nodes. Even so, a skip phenomenon (i.e., metastases beyond
an uninvolved sentinel lymph node) should be present in only
5% of cases (32).
Mesorectal Excision
Guidelines: The mesorectum is defined as the lymphovascu-
lar, fatty and neural tissue that is circumferentially adherent to
the rectum, starting at the level of the sacral promontory, where
the superior hemorrhoidal vessel divides into right and left
branches. The mesorectum tapers and then diminishes just below
Waldeyers fascia (the investing fascia of the levators) around
the levator ani muscles at the level of the distal third of the
rectum.
The goal of surgery should be to obtain radial clearance
of mesorectal tissue, including the primary tumor and lymphatic,
vascular, and perineural tumor deposits. Wide anatomic resec-
tion is accepted as the standard technique for rectal cancer pro-
cedures. Wide anatomic resection includes presacral dissection
under direct visualization, preservation of mesorectal fascia pro-
pria integrity, at least 4-cm clearance of attached mesorectum
distal to the tumor, and pathologic confirmation of mesorectum
attached to the bowel, distal to the tumor.
In surgical trials, a checklist should verify that dissection
under direct visualization has been performed. Surgical and
pathologic reports should verify a 4-cm, fresh, distal mesorectal
margin.
Level of evidence: III.
Grade of recommendation: C.
Rationale: The clinical significance of the mesorectum and of
its surgical clearance is supported by the demonstration of tumor
deposits within the mesorectum remote from the primary tumor
(82) and by the demonstration of a strong correlation between
the extent of the mesorectal tumor spread and cancer outcomes
(83).
Mesorectal spread can occur by direct tumor extension or as
lymph nodes, perineural invasion, or isolated mesenteric depos-
its (23). Mesorectal spread appears to be an important indicator
of disease severity (83), and surgical clearance of the mesorec-
tum appears to be an important technical variable. Several stud-
ies (10,24,25,84,85) have demonstrated greater rates of failure
for treating local disease in patients with lateral resection mar-
gins that are positive for disease. The fact that lateral clearance
rather than lateral spread correlated with the risk of failure for
treating local disease in a large study of patients treated in co-
operative group studies (10) supports the importance of radial
clearance techniques. Further support derives from the fact that
most failures for treating pelvic disease are extrarectal rather
than anastomotic (86) and that the practice of mesorectal clear-
ance is associated with small rates of local recurrence (8,8789).
Note that circumferential margin involvement after mesorectal
excision of rectal cancer with curative intent indicates advanced
disease, not inadequate surgery; accordingly, death from disease
typically occurs before local recurrence (26). Data from patho-
logic assessments of rectal cancer specimens with attention to
mesorectal deposits suggest that mesorectal clearance of at least
4 cm distal to the tumor should be sufficient (29,90).
A current controversy considers that proper attention to sur-
gical clearance of mesorectal tumor deposits can reduce rates of
588 SPECIAL ARTICLE
pelvic recurrence sufficient to reduce rates of pelvic irradiation.
This concept is being tested by the Dutch ColoRectal Cancer
Group (91). Patients with nonfixed, resectable cancer are being
randomly assigned to receive total mesorectal excision or total
mesorectal excision plus preoperative external beam radiation
therapy (25 Gy).
Mesorectal excision will remain controversial until scientific
evidence from randomized trials demonstrates an advantage.
Extended Lateral Pelvic Lymph Node Dissection
Guidelines: Evidence is insufficient to recommend an ex-
tended lateral lymphatic dissection for rectal cancer in the con-
text of a patient without lymph nodes that are clinically sus-
pected of having disease. In the context of clinically suspected
lateral lymph node disease, the dissection should attempt to re-
move these nodes, as is technically feasible. A biopsy of sus-
pected lymph nodes that are beyond the surgical field of resec-
tion needs to be done for staging purposes (e.g., iliac lymph
node). The apical lymph node should be tagged for pathologic
examination.
For adjuvant trials, a minimum of one lymph node must be
examined for entry into the trial. For surgical trials or for entry
into an adjuvant trial for lymph nodes negative for disease,
a minimum of four nodes must be examined.
Level of evidence: IV.
Grade of recommendation: C.
Rationale: It has long been recognized that the lymphatic
drainage of the rectum is highly variable and that dominant
patterns are dependent on the location of the tumor in the rectum
(92). In addition to longitudinal lymphatic spread along the co-
lon, tumors in the upper rectum spread mostly to the superior
pedicle and tumors in the lower rectum spread superiorly and
laterally (29,92). Involved lymph nodes can be detected along
the aorta and superior rectal vessels, as well as along iliac,
hypogastric, sacral, and inguinal nodal sites and laterally along
the middle hemorrhoidal and lateral ligaments (29,92,93). The
number and location (i.e., lateral or apical) of lymph nodes posi-
tive for disease influence outcomes, especially 5-year survival,
and have served as the basis for recommendations for extended
or lateral node dissection (38,93,94). What is not yet established
is whether the involvement of apical or lateral lymph nodes is
relevant only as an indicator of disease severity and prognosis or
whether it indicates a need for more radical lymphadenectomy.
To date, no controlled trials have demonstrated a benefit for
extended lymphadenectomy. Such trials have been difficult to
conduct for many reasons, including limitations of intraoperative
staging; e.g., the inclusion of patients with stage I or II disease
and lymph nodes negative for disease would be expected to
dilute the power of the study. Recent reports from the coopera-
tive group rectal adjuvant studies (10) demonstrate a statistically
significant effect of the percentage of lymph nodes positive for
disease. In fact, in a multivariate analysis testing the effect of
lymph nodes on local recurrence rates, the percentage of lymph
nodes positive for disease was statistically significant when the
number of nodes positive for disease was not (10). This obser-
vation suggests that surgical clearance may be an important
variable affecting rates of local disease treatment failure much
like mesorectal clearance influences local failure rates. Future
research efforts should consider reinvestigating the role of ex-
tended but selective lymphadenectomy, perhaps using modern
techniques of sentinel lymph node mapping.
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
SURGICAL TECHNIQUESCOLON AND RECTUM
See also Surgical TechniquesColon and Surgical Tech-
niquesRectum above.
En Bloc Resection of Adherent Tumors
Guidelines: En bloc resection is the ideal surgical method
to manage locally advanced, adherent colorectal tumors. If
margins achieved with en bloc resection are histologically nega-
tive for disease, they are adequate. If a tumor is transected at
the site of local adherence rather than en bloc, resection is
not complete. En bloc resection is considered to be the mini-
mum extent of resection to achieve a complete resection for
lesions that are T4 clinically and pathologically. Tumors are
considered to be R0 if adjacent structures involved by direct
extension of the primary tumor are removed en bloc and if, in
the judgment of the surgeon and when confirmed on histologic
examination (i.e., the margins of resection are not involved),
the resection is considered to be curative. Lesions that are clini-
cally treated as T4 lesions by en bloc resection but that contain
only inflammatory adhesions are not considered to be T4 le-
sions.
Level of evidence: III.
Grade of recommendation: B.
Rationale: An en bloc excision of the colorectal cancer and
adjacent organs must be performed so as not to compromise
curability. Colorectal cancer adherence to adjacent intra-
abdominal organs or structures is encountered in 15% of patients
with colorectal cancer (95). Rectal carcinoma most often in-
volves the uterus, adnexa, posterior vaginal wall, and bladder
(96). Hence, aggressive surgical procedures are needed because
of the direct extension of tumor into these adjacent structures.
Importantly, tumor adherence to adjacent organs can represent
malignant invasion or simply inflammatory adhesions (96100).
The critical issue is that one cannot determine reliably before
resection whether tumor involvement of contiguous organs is the
result of an inflammatory process or of malignant invasion.
Hence, extended resection of structures adherent to the carci-
noma is the most appropriate surgical management. The reported
incidence of histologically proved, malignant adhesions is 49%
84% (101107). In a collective review of 248 patients who
underwent total pelvic exenteration for rectosigmoid cancer,
Lopez and Monafo (108) reported a 40% incidence of malig-
nant adhesions. In these patients, resection that was less than
en bloc not only compromised the survival but also increased
the recurrence rate. In a group of 43 patients with adjacent
organ involvement reported by Hunter et al. (109), the 5-year
survival rate was 61% and the local recurrence rate was 36%
for individuals who underwent an en bloc resection compared
with 23% 5-year survival and 77% local recurrence rates for
those who had their adhesions surgically separated. Other
reports in the literature (95,96,106,110112) have shown
improved survival in similar-stage colorectal tumors when en
bloc resection is performed. Even for patients with regional
lymph node metastases (the most important prognostic factor
after potentially curative resection for colorectal carcinoma and
adjacent organ involvement), an en bloc resection is warranted
because approximately 25% of these patients will survive
5 years (108).
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
The urinary bladder is the organ most frequently involved by
locally advanced colorectal carcinoma (113). Extended resection
may include a partial or a total cystectomy as part of the en bloc
resection. For such procedures, morbidity rates are increased
compared with the standard surgical resections for colorectal
carcinoma because of the complications associated with the
urinary diversion or bladder repair (114). Results reported by
Talamonti et al. (113) confirm that resection of an advanced
carcinoma of the colon and rectum with en bloc removal of all
or part of the urinary bladder can prolong survival when resec-
tion margins are negative for tumor.
In conclusion, en bloc removal of adjacent organs locally
invaded by cancers of the colon or rectum can achieve survival
rates similar to those of patients with tumors that do not invade
an adjacent organ. To achieve this result, resection margins
negative for tumor are required.
Inadvertent Perforation
Guidelines: Inadvertent perforation of the rectum during
surgery must be documented. Even though patients with inad-
vertent perforation have a high risk for recurrence, these patients
are considered to have complete resection (R0). No data show
an advantage to any management technique for inadvertent
perforation involving rectal cancer. The AJCC should con-
sider classifying a rectal tumor as T4 when inadvertent full-
thickness perforation of the rectum occurs during resection. Fur-
ther data may provide justification for considering perforated
cases as R1.
Level of evidence: III.
Grade of recommendation: B.
Rationale: Inadvertent perforation is not uncommon, espe-
cially in resection of rectal carcinomas. It has been reported in
7.7%25.6% of cases (115). The documentation of intraopera-
tive colorectal perforation is paramount, owing to the negative
implications for local recurrence and survival. Several retrospec-
tive studies (115118) have consistently demonstrated the sta-
tistically significant reduction in 5-year survival and the increase
in local recurrence rates. In addition, perforation at the site of
cancer, as opposed to an area remote from the tumor, has an even
greater impact on survival and local recurrence, as demonstrated
by Slanetz (117). Documentation of intraoperative spillage of
tumor must be considered in a statistical comparison of different
treatment groups, because this spillage has an independent effect
on prognosis. Also, these patients may be candidates for adju-
vant radiotherapy to reduce rates of local recurrence.
No-Touch Technique
Guidelines: The value of the no-touch technique in colon
surgery is debated; the one randomized study of this topic indi-
cates no advantage to support the routine use of the no-touch
technique.
Level of evidence: II.
Grade of recommendation: C.
Rationale: Concern about dislodgment of tumor emboli dur-
ing resection of colorectal carcinomas was the stimulus for the
introduction of the no-touch technique. In a retrospective analy-
sis, Turnbull et al. (119) demonstrated a difference in 5-year
survival; however, there were serious problems with the design
of this study, especially involving more extended resections
SPECIAL ARTICLE 589
in the no-touch group. In the only prospective, randomized trial
evaluating 236 patients, Wiggers et al. (120) demonstrated
no statistically significant difference in 5-year survival with the
use of the no-touch technique. The absolute 5-year survival rates
were 56.3% and 59.8% in the conventional arm and no-touch
surgical groups, respectively. In the conventional group, more
patients had liver metastases and the time to metastasis was
shorter, but differences in survival were not statistically signifi-
cant.
No conclusive data demonstrate that, during surgical manipu-
lation of colorectal tumors, the detachment and circulation of
tumor cells increase in the peripheral circulation. In fact, in
a study by Garcia-Olmo et al. (121), only one in 18 patients had
carcinoembryonic antigen products in the blood of a peripheral
vein detected postoperatively by reverse transcription
polymerase chain reaction; this patient was also one of two in
whom the products were identified preoperatively. In addition,
only one patient was found to have carcinoembryonic antigen
products in the main drainage vein of the colorectal cancer dur-
ing the resection. Hayashi et al. (122) used mutant-allele-
specific amplification to demonstrate that the no-touch tech-
nique may prevent cancer cells from being shed into the portal
circulation. However, this was in a small series of only 18 pa-
tients with colorectal cancer, and the clinical significance of
these experimental findings remains unclear.
Bowel Washout
Guidelines: Studies have shown that viable tumor cells exist
in the lumen of the colon and rectum. Rectal washout may have
value; however, no information exists to suggest any benefit in
the management of colon cancer.
Level of evidence: III.
Grade of recommendation: C.
Rationale: No data conclusively demonstrate reduction of
local recurrence or anastomotic implantation with colon or rectal
washout. However, exfoliated malignant cells have been found
in the effluent of resection margins, in rectal stumps, and
on circular stapling devices (123125). Furthermore, the via-
bility, ability to proliferate, and metastatic potential of
exfoliated malignant colorectal cells have been illustrated
(124,125). Different chemical washout solutions, including nor-
mal saline, have been shown to eliminate exfoliated malignant
cells in the doughnut of rectal tissue from a circular stapler
(126). Despite the evidence for potential anastomotic implanta-
tion, no conclusive evidence supports bowel washout, and no
data support its use in colon cancer. However, with no risk and
minimal cost, it may have some utility in the management of
rectal cancer, where the proximity of the anastomotic site and
the cancer is close; furthermore, it may reduce the microbial
concentration.
Oophorectomy
Guidelines: Direct extension of the tumor to the ovary or a
grossly abnormal ovary should result in en bloc or com-
plete resection of the ovary. Data do not exist to support
routine prophylactic oophorectomy. However, oophorec-
tomy may be offered as an option to standard-risk patients who
receive preoperative radiation therapy or who are postmeno-
pausal.
Level of evidence: IV.
Grade of recommendation: D; panel consensus.
590 SPECIAL ARTICLE
Rationale: There is general agreement among surgeons that
grossly abnormal ovaries should be removed. In addition, meta-
chronous ovarian lesions should be resected, because removal of
all gross disease can provide a clinically significant survival
advantage (127). En bloc resection is the ideal surgical method
to manage locally advanced adherent colorectal cancers. For
further details, see the previous section, En Bloc Resection of
Adherent Tumors.
Ovarian metastases from colorectal carcinoma occur in up
to 6% of patients and are associated with a poor prognosis
and usually with widespread disease (128). Thus, several inves-
tigators have advocated prophylactic oophorectomy to address
this issue and to prevent the risk of primary ovarian carcinoma.
Although no randomized studies have addressed prophylactic
oophorectomy, two studies have retrospectively compared
survival in patients with and without prophylactic oopho-
rectomy. Cutait et al. (129) compared 201 women who had
prophylactic oophorectomy with 134 women who did not.
No statistically significant difference in survival occurred,
and the survival curves of the patients with oophorectomy
were slightly worse. Ballantyne et al. (130) retrospectively
analyzed the impact of oophorectomy on survival and on re-
currence-free survival in women with colon cancer. No statisti-
cally significant difference occurred in patients undergoing
bilateral oophorectomy compared with those not undergo-
ing oophorectomy, although a 5% improvement in survival
favored the oophorectomy group. Thus, no data demon-
strate a survival advantage with prophylactic oophorectomy.
Because of the low risk and potential advantage, this procedure
still is considered to be an option in postmenopausal patients,
although dysfunctional uterine bleeding can occur as a compli-
cation.
Abdominal Exploration
Guidelines: Review of surgical reports has indicated an in-
creasing reliance on preoperative staging techniques, such as
ultrasonography and computerized axial tomography (CT). The
standard should remain a thorough intraoperative exploration for
metastatic and locally advanced primary and lymph node dis-
ease. The patient is entitled to an intraoperative exploration that
is as thorough as the anatomy and prior surgical procedures
permit without increasing the risk to the patient. A thorough
examination includes inspection and palpation of the liver, peri-
toneal surface, omentum, retroperitoneum, and ovaries, if pre-
sent. The primary tumor should be assessed for local adherence.
Palpation of the periaortic, celiac, and portohepatic lymph
nodes, when accessible, is important for documentation. Details
of the exploration should be part of the surgical note, and the
presence of metastatic disease should be documented, preferably
histologically.
Alternatives to direct inspection of the liver include intraop-
erative ultrasonography, bimanual examination of the liver, and
preoperative CT. Eligibility requirements for clinical trials are
established by each clinical trials group. A reasonable require-
ment for entry is that all patients at the time of the surgical
procedure have a documented abdominal exploration based on
the above criteria. CT alone is not a substitute for a thorough
abdominal exploration to satisfy eligibility criteria for clinical
trial entry.
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
 Level of evidence: V.
Grade of recommendation: D; panel consensus.
Rationale: No data demonstrate that a less-than-thorough ex-
ploration affects survival. However, accuracy of overall staging
is greatly dependent on a thorough, systematic exploration of
potential metastatic sites. Histologic confirmation of any meta-
static disease would greatly affect staging and eligibility for
adjuvant therapy.
The surgical guidelines are summarized in Table 4.
SURGICAL DOCUMENTATION
Ideal Surgical Report
The ideal surgical report for colorectal cancer should provide
all of the diagnostic, staging, prognostic, and technical aspects of
the procedure that may influence outcome.
Documentation should include the following:
1) Preoperative treatments, including chemotherapy, radiation
therapy, and immunotherapy.
2) The site, size, and adherence of the primary tumor(s); ob-
struction or perforation if present.
3) Staging for metastatic disease (liver, peritoneum, omentum,
or ovaries) and nonmesenteric lymph nodes (celiac, porto-
hepatic, periaortic, or iliac); the extent and means (manual,
bimanual, or sonographic) of liver exploration; the presence
or absence of ascites and whether fluid was sent for cyto-
logic examination; the description of any compromise of the
Table 4. Summary of surgical guidelines
Location
of cancer Surgical guideline and grade of recommendation
Colon Lymphadenectomy should extend to the level of the origin of
the primary feeding vessel; suspected positive lymph nodes
outside the standard resection should be removed when
feasible (grade C).
Bowel margins 5 cm proximally and distally should be used
(grade D).
Laparoscopic colectomy for cancer should be confined to
clinical trials (grade D).
Rectum The ideal bowel margin is 2 cm distally and 5 cm
proximally, measured fresh with the use of full thickness; the
minimally acceptable distal margin for sphincter preservation
is 1 cm (grade B).
Lymphovascular resection of the rectum should include a wide
anatomic resection of the mesorectum, including the
mesorectal fascia propria and 4 cm of clearance distal to
the tumor and proximal ligation of the primary feeding
vessel (grade C).
Extended lateral lymphatic dissection cannot be supported on
current evidence (grade C).
Length of bowel cannot be supported as an important surgical
variable (grade D).
Colon and En bloc resection should be performed for tumors adherent to
rectum local structures (grade B).
Inadvertent bowel perforation increases the risk of recurrence
and should be avoided (grade B).
Thorough abdominal exploration for metastatic and locally
advanced primary and lymph node disease should be
performed (grade D).
The no-touch technique is debated with little evidence to
support it (grade C).
Bowel washout may have theoretical benefits in rectal cancer,
but such benefits have not been proven (grade C).
Ovaries grossly involved with tumor should be removed;
prophylactic oophorectomy cannot be supported (grade D).
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
exploration due to adhesions or concomitant disease(s); the
site of biopsy of any areas suspected of having metastatic
disease; the rationale if a biopsy specimen of the metastatic
disease was not obtained.
4) The site and treatment of any metastatic disease.
5) The presence or absence of mesenteric lymph nodes (en-
larged or firm) suspected of having disease; the site of any
suspected lymph nodes left after the procedure is com-
pleted; the site of biopsy of any suspected lymph node(s)
outside the mesenteric resection.
6) The extent of resection, including level of transected feed-
ing vessel(s); description of removal of adjacent structures
or organs.
7) Any departure from an en bloc resection; any spillage of
tumor or stool; site of placement of clips to aid in radiation
therapy.
8) The marking of any radial margins suspected of having
disease, especially rectal cancer; the extent of mesorectal
excision.
9) Any frozen sections submitted for examination; other inter-
action with a pathologist.
10) Clinical classification of tumor resection as R0, R1, or R2.
11) The distal rectal mucosal and mesenteric margins.
Explanation of Surgical Checklist
The surgical checklist (see Appendix 2) can be used to
evaluate patients for clinical trial eligibility and to aid in obtain-
ing complete information for the surgical note. This list is a
compromise between obtaining the majority of important data
and developing an exhaustive list for every eventuality. This list
complements but does not replace the surgical note, in which the
variations and nuances in the individual patient are best docu-
mented.
The surgical report can be supplemented with a drawing
of the colon with its mesentery and arterial supply. This draw-
ing can give important quality control by providing addi-
tional information or clarifying written information in the re-
port.
The exact surgical procedure should be detailed. An extended
right colectomy extends distal to the middle colic artery. A low
anterior resection refers to mobilization of the rectum from its
pelvic attachments and anastomosis below the pelvic perito-
neum. In a high anterior resection, all of the dissection and the
anastomosis are done above the peritoneal reflection. If a low
anterior resection of the rectum and sigmoid colon is done, in-
dicate both sigmoidectomy and low anterior resection or
sphincter-preserving rectal resection. Any other procedure
performed, such as oophorectomy, hysterectomy, or partial cys-
tectomy, should be indicated.
An en bloc resection means that the tumor and attached mes-
entery, tissue, or organs are removed as a whole. Thus, if a tumor
is shaved off the bladder and then the attached portion of the
bladder is removed later, the resection is no longer en bloc. If a
rectal tumor is transected and then additional rectal tissue is
excised to obtain a margin negative for disease, the resection is
no longer en bloc. If the specimen is removed and then addi-
tional lymph nodes positive for disease are removed, the resec-
tion is not en bloc.
The feeding vessels, such as ileocolic, middle colic, left colic,
sigmoid, superior rectal, inferior mesenteric, or middle rectal
SPECIAL ARTICLE 591
 APPENDIX 1
The following are members of the Expert Panel and their institutions and group associations:

Name and degree Institution

Heidi Nelson, M.D., Chair Mayo Clinic, Rochester, MN

North Central Cancer Treatment Group
Robert W. Beart, Jr., M.D. University of Southern California, Los Angeles, CA
Southwest Oncology Group
Arthur Carlin, M.D. Wayne State University, Detroit, MI
Society for Surgery of the Alimentary Tract
Barbara Conley, M.D. National Cancer Institute, Rockville, MD
Cancer Therapy and Evaluation Program
Jean Couture, M.D. Mount Sinai Hospital, Toronto, Ontario
National Institute of Canada Clinical Trials Group
Norman Estes, M.D. University of Illinois College of Medicine, Peoria, IL
Southwest Oncology Group
James Fleshman, M.D. Barnes-Jewish Hospital, St. Louis, MO
Radiation Therapy Oncology Group
Jose Guillem, M.D. Memorial Sloan-Kettering Cancer Center, New York, NY
American Society of Colon and Rectal Surgeons
Smita Hastak Oracle Corporation, Reston, VA
Linda Healy Mayo Clinic, Rochester, MN
North Central Cancer Treatment Group
Judy Jones, M.S. NSABP Biostatistical Center, Pittsburgh, PA
National Surgical Adjuvant Breast and Bowel Program
Thomas Julian, M.D. Allegheny Cancer Center, Pittsburgh, PA
National Surgical Adjuvant Breast and Bowel Program
Brent Miedema, M.D. University of Missouri, Columbia, MO
Cancer and Leukemia Group B
David Ota, M.D. Ellis Fischel Cancer Center, Columbia, MO
Society of Surgical Oncology
Nicholas Petrelli, M.D. Roswell Park Cancer Institute, Buffalo, NY
National Surgical Adjuvant Breast and Bowel Program
Maryanne Nicosia ECOG Coordinating Center, Brookline, MA
Eastern Cooperative Oncology Group
Daniel Sargent, Ph.D. Mayo Clinic, Rochester, MN
North Central Cancer Treatment Group
Elin Sigurdson, M.D. Fox Chase Cancer Center, Philadelphia, PA
Eastern Cooperative Oncology Group and Radiation Therapy Oncology Group
Jay Stauffer, M.D. Hill Country General and Oncology Surgical Associates, Fredericksburg, TX
Southwest Oncology Group
Edward Trimble, M.D. National Institutes of Health, Rockville, MD
National Cancer Institute
Sam Wells, Jr., M.D. American College of Surgeons, Chicago, IL
American College of Surgeons Oncology Group

arteries, should be identified. A clinical evaluation of residual FUTURE DIRECTIONS

tumor should be documented.
The distal mesorectal margin should be measured in the fresh
specimen, preferably with the specimen pinned. The mesorectal
distal margin is measured horizontally from the distal edge of the
tumor.
Any areas suspected of having metastatic disease should have
a biopsy unless the risk is not justified. If there is a suspicion of
liver and extrahepatic metastatic disease, both sites should have
a biopsy because the results may influence liver-directed
therapy.
Using an established methodology, the panel of experts re-
viewed current literature and drafted guidelines as the first step
in promoting consistency in oncologic surgical practices. The
limiting factor in developing evidence-based recommendations
was the paucity of evidence of levels I and II. The vision of the
panel is that future efforts be focused on the collection of data in
a standardized manner in large groups of patients. Only coordi-
nated efforts of this sort will generate the data necessary to
support grade A recommendations.

592 SPECIAL ARTICLE Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001
 APPENDIX 2
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NOTES
1
Considered to be category I as prognostic factors by the College of Ameri-
can Pathologists Consensus Statement 1999 (68): Definitively proven to be of
prognostic import based on evidence from multiple statistically robust published
trials and generally used in patient management.
Sponsored by the National Cancer Institute.
Manuscript received October 25, 2000; revised February 6, 2001; accepted
February 15, 2001.
Journal of the National Cancer Institute, Vol. 93, No. 8, April 18, 2001