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Perspective
The quality of total mesorectal excision specimen: A review of its
macroscopic assessment and prognostic significance
Shi-Bo Song
a,b
, Guo-Ju Wu
a
, Hong-Da Pan
a
, Hua Yang
a
, Mao-Lin Hu
a,b
,
Qiang Li
a,b
, Qiu-Xia Yan
a,b
, Gang Xiao
a,
*
a
Department of Gastrointestinal Surgery, Beijing Hospital, National Center of Gerontology, Beijing 100730, China
b
Peking University Fifth School of Clinical Medicine, Beijing 100730, China
Received 20 September 2017
Available online 12 March 2018
Abstract
As a surgical procedure which could significantly lower the recurrence rate of cancers, total mesorectal excision (TME) has
been the gold standard for middle and lower rectal cancer treatment. However, previous studies have shown that the procedure did
not achieve the ideal theoretical local recurrence rates of rectal cancers. Some researchers pointed out it was very likely that not all
so-called TME treatments completely removed the mesorectum, implying that some of these TME surgical treatments failed to
meet oncological quality standards. Therefore, a suitable assessment tool for the surgical quality of TME is necessary. The notion
of “macroscopic assessment of mesorectal excision (MAME)”was put forward by some researchers as a better assessment tool for
the surgical quality of TME and has been confirmed by a series of studies. Besides providing rapid and accurate surgical quality
feedbacks for surgeons, MAME also effectively assesses the prognosis of patients with rectal cancer. However, as a new
assessment tool used for TME surgical quality, MAME has an only limited influence on the current guidelines and is yet to be
widely applied in most countries. The aims of this review are to provide a detailed introduction to MAME for clinical practice and
to summarize the current prognostic significance of MAME.
©2018 Chinese Medical Association. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This
is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords: Macroscopic assessment of mesorectal excision (MAME); Quality control; Total mesorectal excision (TME); Coning
Introduction
In 1982, Heald et al
1
proposed the notion of total
mesorectal excision (TME) from the perspective of
embryological anatomy; this led to a deeper under-
standing of the rectal anatomic structure and made
scientific and standardized assessments and control of
the rectal cancer surgery possible. The local recurrence
rates (LRRs) have been reduced from 20%e45% using
traditional surgical treatments to less than 10% using
*Corresponding author.
E-mail address: xgbj@sina.com (G. Xiao).
Peer review under responsibility of Chinese Medical Association.
Production and Hosting by Elsevier on behalf of KeAi
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TME.
2,3
For patients receiving neoadjuvant radio-
therapy together with TME, the LRRs could be further
reduced to 5%.
4
As a surgical procedure which could
significantly lower the recurrence rate of cancers, TME
has been the gold standard for middle and lower rectal
cancer surgical treatment.
However, not all reported LRRs after TME were
lower than 10%; in some studies,
5,6
the LRRs were
11%e19%. Some researchers pointed out it was very
likely that not all so-called TME procedures completely
removed the mesorectum, which means that some of
these TME surgical treatments failed to meet onco-
logical quality standards.
7
García-Granero et al
8
suggested that the TME
quality could be assessed in terms of two aspects: (1)
involvement of the circumferential resection margin
(CRM) and (2) integrity of the TME specimen.
Although the importance of CRM involvement on the
prognosis requires no more emphasis, it is very easy
for CRM to be affected by the depth of tumor invasion
or tumor-node-metastasis (TNM) stage when used for
reflecting the surgical quality.
9
Furthermore, if the
integrity of the mesorectum cannot be guaranteed even
if the CRM was negative for tumor cells, there still
may be some micro tumor deposits or positive lymph
nodes in the residual mesorectum, which might in-
crease the risk of cancer recurrence. Numerous studies
have confirmed the correlation between the prognosis
of patients with tumors and the integrity of mesorectal
specimens evaluated macroscopically.
6,8,10e15
There-
fore, some researchers put forward the “macroscopic
assessment of mesorectal excision (MAME)”as a
suitable assessment tool for the integrity of meso-
rectum, which could reflect the quality of TME.
8
Nagtegaal et al
12
found that in the subgroup of pa-
tients with a negative resection margin, patients with
incomplete mesorectum resection had a higher overall
recurrence rate (ORR) than those with complete mes-
orectum resection (28.6% vs. 14.9%, P¼0.03); further,
the overall survival (OS) rate was lower in the group of
patients with incomplete mesorectum resection (76.9%
vs. 90.5%, P<0.05). Quirke et al
11
also conducted an
analysis on a subgroup of patients with negative CRMs
and found that the LRR remarkably increased in the
group of patients with incomplete mesorectum
compared with that in the group of patients with
complete mesorectum resection (12% vs. 4%). There-
fore, the integrity of the mesorectal specimen can be
regarded as an independent prognostic factor for pa-
tients who received rectal cancer resection. Moreover,
MAME is not affected by the T stage, N stage, TNM
stage, or Dukes stage, making MAME a better tool than
the CRM for TME quality assessment.
8,11,12,14,16e18
Relevant definitions
MAME
MAME is a method of assessment, by which we can
describe the integrity of the mesorectal specimen and
assess the quality of TME via visual inspection and use
of cross-sectional slices of the segment with tumor
(3e5 mm in thick).
6,8,11,12,19
The visual inspection can
provide a very clear indication of the quality of the
mesorectal specimens, and the cross-sectional slices of
the segment with tumor can provide further assessment
of the regularity of the CRM, an indicator of the ade-
quacy of the resection.
19
According to the definitions by the CR07 proto-
col,
11,15
the quality of mesorectal specimens can be
described as follows.
Mesorectal resection (MRR)/good/complete: intact
mesorectum and smooth mesorectal surface with only
minor irregularities; no defects deeper than 5 mm; no
coning of the specimen towards the distal margin; and
smooth macro-CRM on slicing.
Intramesorectal resection (IMR)/intermediate/
nearly complete: intermediate bulk of the mesorectum
with an irregular surface; a defect deeper than 5 mm,
and no visible muscularis propria other than inserted
levator; intermediate coning; intermediate irregularity
of macro-CRM on slicing.
Muscularis propria resection (MPR)/poor/incom-
plete: small bulk of the mesorectum with a very irregular
surface; defect down to the muscularis propria; severe
coning; severe irregularity of macro-CRM on slicing.
Coning
A“coning”(Fig. 1) would form if a surgeon cuts
towards the tubular rectum during distal dissection
instead of operating outside the visceral mesorectal
fascia, leaving the specimen with a tapered, conical
appearance. In the clinical practice, such a tendency
during operation is not rare, and consequently, the
surgical quality is undoubtedly suboptimal. Mean-
while, it is also unacceptable if the surgeon removes
the distal mesorectum excessively, i.e., far beyond
5 cm from the distal tumor margin, which would not
only have little help in improving the prognosis of
patients, but also increase the incidence rate of post-
operative complications.
20
Therefore, only when the
52 S.-B. Song et al. / Chronic Diseases and Translational Medicine 4 (2018) 51e58
“coning”is located within 5 cm from the distal tumor
margin will the clinical benefits become significant.
Macro-CRM
Macro-CRM can be defined as the general circum-
ferential state of the TME specimen under visual in-
spection, which is different from the counterpart of
pathological circumferential resection margin (pCRM)
under a microscope.
6,9,21,22
In MAME, macro-CRMs
are macroscopically grouped into margins with a
smooth surface, intermediate irregularity, and severe
irregularity. Furthermore, pathologists can slice through
the site of tumors at 3e5-mm intervals to examine the
circumferential margin macroscopically.
21,22
Addition-
ally, Nagtegaal and van Krieken
22
believed that if the
distance between the tumor and macroscopic CRM
under visual inspection is no less than 1 cm, the pCRM
could be considered to show a negativity.
Evolution of MAME
As early as 1998, Quirke et al
11
first introduced
three grades of mesorectal surgical quality that assess
the quality of TME in the international multicenter
CR07 and National Cancer Institute of Canada Clinical
Trials Group (NCIC-CTG) CO16 trial, i.e., good, in-
termediate, and poor; they also analyzed the prognostic
differences among these patients with different MAME
grades and reported a significant correlation between
the LRR and MAME grade.
Subsequently, Nagtegaal et al
12
systematically
described the macroscopic quality of the mesorectal
specimens by classifying them into three groups:
complete, nearly complete, and incomplete according
to the definitions by the CR07 protocol; they further
confirmed a significant correlation between the quality
of the TME specimens and the prognosis of patients
after rectal cancer resection.
11,12
In recent years, some researchers proposed the
concept of “TME scores”
14
or “MAME.”
8
They
preferred the more descriptive and objective evalua-
tion of the mesorectal quality based on the surgical
plane of resection in which three grades of TME had
been defined, including mesorectal plane of resection,
intramesorectal plane of resection and muscularis
propria plane of resection.
8,10,11,13,15
In addition, Leonard et al
15
found that for prediction,
both two-grade (grade of MRR vs. combined grade of
IMR and MPR) and three-grade scoring systems func-
tioned well; however, the former was more significantly
associated with the OS and the risk of distant metas-
tasis. Although the names of grades are different, the
contents are consistent. Moreover, MAME based on the
surgical plane of resection is more objective and
widespread; therefore, MAME was used as follows.
10
Method of MAME
According to the National Comprehensive Cancer
Network (NCCN) Guidelines Version 3.2017,
23
the
status of the proximal and distal circumferential (radial)
and mesenteric margins should be reported, and the
pathologists should evaluate the quality (completeness)
of the mesorectum. Although increasing attention has
been paid to MAME, there is no international consensus
on its assessment methods and criteria.
21,22,24,25
Therefore, it is necessary to develop an objective and
repeatable standard of MAME and standardize the
method of MAME, which is important for the prognosis
assessment, postoperative decision-making, and early
feedback provision on the surgical quality for surgeons.
The method and process of MAME combined with the
surgical principles of TME from a pathology perspec-
tive are listed below. Further, the detailed process of
MAME is summarized in Fig. 2.
To start with, it should be clear that the TME
specimens for optimal macroscopic evaluation should
Fig. 1. “Coning”: the tendency to cut towards the tubular rectum
during distal dissection. If the integrity of the mesorectum cannot be
guaranteed, even though the mrCRM and pCRM are negative, there
may still be some micro tumor deposits or positive lymph nodes in the
residual mesorectum, which would increase the risk of local recurrence
in patients who received TME. mrCRM: magnetic resonance imaging-
assessed circumferential resection margin; pCRM: pathological
circumferential resection margin; TME: total mesorectal excision.
53S.-B. Song et al. / Chronic Diseases and Translational Medicine 4 (2018) 51e58
be received instantly after surgical removal, while
unfixed and unopened.
21,22
Prior to the assessment,
photographic documentation of the circumferential and
distal margins of a fresh mesorectal specimen is
desirable, which would serve as the evidence for
macroscopic evaluation and review in the future.
6,21,22
The integrity of the mesorectum will be assessed in
accordance with the contents described in MAME. The
macroscopic state of the mesorectal specimen should
be evaluated first. It is necessary to carefully record
whether the mesorectum is complete and smooth and
whether there are any defects. If the specimen surface
is not smooth or has any defects, the depth of defects
should be measured. An optimal mesorectum specimen
should have a smooth and intact surface, while a poor-
quality specimen has a small bulk in the mesorectum,
deep defects reaching the muscularis propria, or even a
perforation.
21,22
Thereafter, the degree of coning in the
distal end of the mesorectum will be assessed. In
partial mesorectal excision (PME), whether the distal
transection is in a plane of 90to the rectal wall should
be assessed. The distal transection must be performed
at the same distance (over 5 cm) from the gross distal
tumor margin on the rectal wall and both inner and
outer mesorectum, which could avoid the formation of
coning.
6
The circumferential margin in a gross mesorectal
specimen is painted using ink, including all non-
Entire (fresh)
mesorectal specimen
Cross-sectional
slices
Obtain photographs, and assess the integrity of
the mesorectum according to the contents
described in MAME
Ink the non-peritonealized bare areas of the
specimen
Open the specimen, leaving the segments 2 cm
above and below the tumor intact
Pin the s
p
ecimen on a corkboard
Place formalin-soaked gauze wicks into the
lumen of the unopened segment
Fix the specimen for at least 48 hours
Transversely slice the unopened segment of the
rectum at 3–5-mm intervals, and place the slices
on the work surface
Obtain photographs, and further assess the
integrity of the mesorectum according to the
contents described in MAME
Fig. 2. Summary of the process for macroscopic pathological assessment. MAME: macroscopic assessment of mesorectal excision.
54 S.-B. Song et al. / Chronic Diseases and Translational Medicine 4 (2018) 51e58
peritonealized surfaces anteriorly and posteriorly.
26
It
should be kept in mind that the serosal surfaces should
not be inked, especially for the anterior part, because it
might be difficult to identify the serosal involvement.
26
After inking of the gross specimen, the rectal tube
and mesorectum should be opened anteriorly, leaving
the flanking region extending 2 cm beyond the tumor
margin (where the specimen would be preserved
intact), together with the tumor mass, untouched.
21
The
tumor size should also be recorded as an element in
tumor documentation.
21
The specimen should be pin-
ned on a corkboard to prevent shrinkage artefacts, and
a loose, formalin-soaked gauze wick should be placed
within the lumen of the unopened segment to optimize
fixation.
27
Subsequently, the specimen should be fixed
for at least 48 hours. Although the duration is longer
than that in fixation in many hospitals, this is vital for
the serial cross-sectional slicing of the unopened
segment.
21,22,27
Finally, the unopened segment of the fixed spec-
imen will be transversely sliced into thin sections
(3e5 mm).
21,22
All the cross-sectional rings should be
laid out to assess the mesorectal quality and macro-
CRM further.
21,22
These thin sections will also lay
the foundation for the subsequent microscopic exami-
nation. Photographic documents are necessary, espe-
cially in cases of a poor TME or positive macro-CRM.
After the macroscopic assessment, the slices showing
the closest relationship of tumor or a positive node to
the circumferential margin should be further made into
microscopic slices to examine the pCRM. Nagtegaal
and van Krieken
22
believed that if the distance between
the tumor and resection margin under visual inspection
was over 1 cm as per the macroscopic pathological
assessment, MAME would be enough to support the
judgement of a negative pCRM. In sum, both the whole
specimen (fresh) and cross-sectional slices (after
fixing) should be examined for an adequate
assessment.
Prognostic significance of MAME
Local recurrence
TME reduces the LRR for patients with rectal
cancer. Primarily being employed to assess the local
surgical quality, the prognostic value of MAME is
mainly manifested in the relationship between different
mesorectal grades and the LRR.
Quirke et al
11
were the first to group the mesorectal
specimens into groups using three different grades in
the CR07 trial, and they found that the 3-year LRRs in
the three groups were 4% for good, 7% for interme-
diate, and 13% for poor (P¼0.0039), which suggested
a significant correlation between the LRR and MAME
grade. Nagtegaal et al
12
analyzed the data of 180 non-
irradiated patients with detailed descriptions of the
specimens in their pathology reports in the Dutch
multicenter trial. In the group with an incomplete
mesorectum, the LRR after 25.8 months of follow-up
was 15.0% compared with 8.7% in the group with a
nearly complete mesorectum (P¼0.01).
12
Nagtegaal
et al
10,12,22
believed that the integrity of the mesorectal
specimens is not only an important predictor of local
recurrence of rectal cancer but also provides reliable
feedback on the surgeon's performance.
Maslekar et al
16
revealed significant differences
among the LRRs of MRR, IMR, and MPR (1.6%,
5.7%, and 41%, respectively; P<0.0001), which
strongly confirmed the prognostic value of the grades
of the mesorectum. Although Jeyarajah et al
14
failed to
reveal the correlation between the LRR and the grade
of MRR, they found that the pCRM-negative patients
were more likely to have a higher TME score
(P¼0.0001). Leite et al
17
(P<0.01) and García-
Granero et al
8
(P¼0.003) also reported a significant
impact of the grades of the mesorectum on the LRR.
Most of these studies, pooled in a meta-analysis by
Bosch and Nagtegaal
10
and including over 2174 pa-
tients, found that patients with an MPR had a signifi-
cantly higher LRR than patients with the other two
grades (either IMR or MRR) (P¼0.005); moreover,
the LRR in patients with either an MPR or an IMR was
significantly higher than that in patients with an MRR
(P¼0.04). Therefore, it could be practical to employ
the grades of the mesorectum as an indicator for the
risk of local recurrence among patients who received
rectal cancer resection.
Furthermore, in the pCRM-negative subgroup based
on the data of Quirke et al,
11
the statistical difference
in the 3-year LRR was significant (12% for MPR vs.
4% for MRR), while that in the 3-year disease-free
survival (DFS) rate was subtle (74% for MPR vs.
81% for MRR); this indicated MAME as an indepen-
dent prognostic factor for the LRR.
Another sub-analysis performed by Quirke et al
11
showed that short-course preoperative radiotherapy
reduced the 3-year LRR (P<0.0001) and improved the
3-year DFS rate (P¼0.013) for all three grades;
however, the benefit of short-course preoperative
radiotherapy did not differ among the three grades
(P¼0.30 for trend). Leonard et al
18
found that patients
who did not show downstaging after long-course che-
moradiotherapy (CRT) had a higher incidence of MPR
55S.-B. Song et al. / Chronic Diseases and Translational Medicine 4 (2018) 51e58
than patients who showed downstaging (P¼0.0005).
Kiehlmann et al
28
analyzed the prognosis of patients
who underwent preoperative long-term CRT and TME
and found that the 5-year LRR was 6.7% in patients
with either an MRR or an IMR compared with the LRR
of 50% in the patients with an MPR (P¼0.015).
Therefore, neoadjuvant radiotherapy could improve the
local prognosis of patients planned to undergo resec-
tion. However, even after neoadjuvant CRT, it should
not be ignored that the quality (completeness) of the
mesorectum still has a strong influence on local recur-
rence in patients with rectal carcinoma.
28
Overall recurrence
Nagtegaal et al
12
showed that the ORR also
significantly increased in the MPR group compared
with that in the MRR group (35.5% vs. 21.5%,
P¼0.01). Moreover, pCRM-negative patients showed
an ORR of 14.9% in the MRR and IMR groups
compared with the ORR of 28.6% in the MPR group
(P¼0.03), which was statistically different and indi-
cated MAME as a reflection of the risk of overall
recurrence among patients with rectal cancer, espe-
cially for pCRM-negative patients.
Maslekar et al
16
showed remarkable differences in
the ORR (1.6% for MRR, 17% for IMR, and 59% for
MPR; P<0.0001). García-Granero et al
8
also showed
a statistical difference (1.6% for MRR, 17% for IMR,
59% for MPR; P¼0.032). Moreover, the patients with
rectal cancer and MPR in the meta-analysis by Bosch
and Nagtegaal
10
had higher ORRs than the patients in
the other two groups (P¼0.01); however, there was no
significant difference between the groups of patients
with either an MPR or an IMR and the group of pa-
tients with an MRR (P¼0.07).
However, in a recent prospective study with a long-
term follow-up (5 years, n¼121) by Madbouly et al,
29
no remarkable difference among different mesorectal
grades in terms of the LRR or ORR was found in either
all patients or in pCRM-negative patients only.
Although there is still a lack of sufficient evidence
for the correlation between the grades of the meso-
rectum and the risk of overall recurrence, it is still of
some practical significance in the clinical practice and
could somehow be considered as a parameter of
prognosis for patients after rectal cancer resection.
Survival
Nagtegaal et al
12
demonstrated an association be-
tween MPR and a lower OS (76% for MPR and 86%
for MRR, P<0.05) and a similar result in their
pCRM-negative group (76.9% for MPR and 90.5% for
MRR, P<0.05). Leite et al
17
found that the 5-year
cancer-free survival rate was 65% in their MRR
group and 47% in their MPR group (P<0.05).
However, neither did Quirke et al
11
find any correlation
between mesorectal grading and 3-year DFS rate (79%
in MRR patients, 75% in IMR patients, and 70% in
MPR patients, P¼0.14), nor did Maslekar et al
16
find
any correlation with the survival rates (P¼0.17).
Most of the studies consistently showed that
avoiding MPR could significantly reduce the recur-
rence risk after TME surgery, and an optimal plane
(MRR) of TME also could significantly improve the
LRR and ORR compared with a poor plane (IMR or
MPR).
10
However, owing to the lack of sufficient data
to validate the prognostic value, there was seemingly a
trend that a better survival was associated with an
optimal plane (MRR).
10,11,16,17
TME-quality assessment instrument
Although MAME has been classified as a routine
part of the pathological review in some countries, a
convenient and united method of evaluation is still not
globally available. To utilize the tool conveniently
and uniformly, Simunovic et al
30
designed an assess-
ment instrument TME-Quality Assessment (TME-QA)
based on the Quirke classification system. After they
compared the average scores for macroscopic spec-
imen quality evaluated by different pathological pro-
fessionals with TME-QA, including gold standard
assessors, pathologists, and pathology assistants, the
results showed an acceptable internal consistency (0.75
for the gold standard assessors, 0.63 for the patholo-
gists, and 0.60 for the pathology assistants). However,
the interrater reliability for macroscopic specimen
quality among these three pathological professions was
not sufficient (0.45 for the pathology assistants, 0.80
for the pathologists, and 0.86 for the gold standard
assessors), which limits its popularization and appli-
cation. By combining the instrument with the above-
mentioned assessment methods, we may be able to
design a direct, rapid, and reliable evaluation for
specimens to assess the quality of TME for surgeons
and the prognosis of patients.
Conclusion
Most of the current studies showed that complete
resection of the mesorectum can significantly reduce
the risk of recurrence. Both MAME and CRM are key
56 S.-B. Song et al. / Chronic Diseases and Translational Medicine 4 (2018) 51e58
prognostic factors for patients after rectal cancer
resection. Furthermore, MAME can provide rapid and
accurate feedback on surgical quality to guide surgeons
and improve surgical techniques, which is vital for the
quality control of TME. Although the TME-QA was
good for MAME to some extent, it was not very easy to
be handled by pathology assistants. We believe that
MAME could be a direct, rapid, and reliable method of
assessment for TME quality if we put more effort into
designing a practical assessment instrument.
With MAME, we can rapidly identify the quality of
TME, predict the outcomes of patients, and take further
actions to manage a poor prognosis. However, tech-
niques to prevent or manage the poor prognosis of an
incomplete mesorectum need further investigation. The
measures may include neoadjuvant radio-
chemotherapy, adjuvant radiochemotherapy, improve-
ment of operation, or other treatments; however,
relevant data are insufficient, and further studies and
joint efforts of surgeons, pathologists, oncologists, and
other medical professionals are needed.
Conflicts of interest
None.
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Edited by Pei-Fang Wei
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