J Gastrointest Surg

DOI 10.1007/s11605-017-3427-9

REVIEW ARTICLE

Evolution of Surgical Treatment for Rectal Cancer: a Review

Sanjeev Dayal 1 & Nick Battersby 1 & Tom Cecil 1

Received: 15 December 2016 / Accepted: 6 April 2017

# 2017 The Society for Surgery of the Alimentary Tract

Abstract Surgery that produces an optimal total mesorectal excision (TME) resection specimen remains the cornerstone of
curative rectal cancer management. In the modern era, despite the results of recent randomised trials, laparoscopic TME is a
crucial technique in the TME surgery armamentarium. Laparoscopic surgery offers the benefit of magnified views that aid sharp
and precise dissection. However operating in the confines of a narrow pelvis, particularly when the mesorectum is bulky, requires
significant technical skill. This is compounded by limited angulation of laparoscopic instruments and staplers. The final challenge
is to preserve the integrity of the mesorectum during delivery of the specimen. The principles of TME surgery, on which Bill
Heald founded the Basingstoke Colorectal unit, can equally be applied to laparoscopic, transanal and robotic TME, but great care
must be taken to preserve the key principle—that no steps are taken that have the potential to shed tumour cells or compromise the
quality of the mesorectal specimen.

Keywords Rectal cancer . Total mesorectal excision .
Laparoscopic . Transanal . Robotic
Introduction
In Charles Mayo’s review from 1903, also entitled ‘Evolution
In The Treatment Of Cancer Of The Rectum’, he stated that
‘Certain definite results are desired in operations on cancer of
the rectum, namely, permanent cure, low operative mortality
and a controllable anus, or its best substitute. These results are
modified by location, stage of progress and the age and condi-
tion of the patient’.1 In essence, this statement still summarises
the aims of rectal cancer management despite major advances
in radiology, surgery and pathology. Optimal treatment of rectal
cancer is increasingly complicated with the need for complex
multidisciplinary decisions on the role of pre-operative therapy,
* Tom Cecil
tom.cecil@nhs.net
1
Department of Surgery & Peritoneal malignancy Institute,
Basingstoke and North Hampshire Hospital, Basingstoke RG24
9NA, UK
variable access techniques and the exact surgical procedure.2
Nevertheless, in the total mesorectal excision (TME) era only,
optimal surgical resection has been robustly demonstrated to
enable curative treatment.3 Pathological staging and macro-
scopic integrity of the TME specimen are the most important
prognostic indicators and completeness of total mesorectal ex-
cision is a marker for grading surgical technique.4
Open TME
Bill Heald (RJH) first described total mesorectal excision
(TME) in 1979.5 His rationale, as described in the manual of
total mesorectal excision, stemmed from the realisation that
the rectum can be redefined as a midline gut tube surrounded
by fat and intrinsic lymphovasculature that is enveloped by a
fascial layer termed the mesorectum.6 In 1982, RJH reported
five cases where tumour deposits in the mesorectum were
found distal to the primary tumour; this led to the hypothesis
that if the rectum and mesorectum, surrounded by the
mesorectal fascia, were carefully removed en bloc, most rectal
cancers could be cured with the exception of the most ad-
vanced cases.7 This fascial layer is recognisable for surgeons
by the ‘angel hairs’ of loose areolar tissue. The distal fatty

envelope that surrounds the rectum was described as the ‘holy
plane’; it is the interface between the mesorectal and parietal
fascia.8 Heald et al. reported the Basingstoke prospective se-
ries of 115 patients in the Lancet in 1986; the local recurrence
rate in patients with mid or low rectal cancer was 3.7%.9
These results were met with scepticism, but the unprecedented
step by Professor MacFarlane to take a sabbatical from
Vancouver to independently review, and confirm, these out-
comes helped legitimise and validate the TME concept.10
The fundamental principles of TME have been elucidated
by Moran in precise detail.11 These include peri-mesorectal
‘holy plane’ sharp dissection by diathermy or scissors under
direct vision with appropriate three directional traction and
counter traction. The objective is to deliver an intact
mesorectum with no naked eye or microscopic circumferential
resection margin involvement and a clear distal margin, ideal-
ly a minimum of 1 cm of normal muscle tube distal to the
tumour. It is important to recognise and preserve the autonom-
ic nerves and plexus, which are crucial for optimal bladder and
sexual function. Skilful extension of dissection into the depths
of the pelvis allows for an increase in the preservation of the
anal canal and a reduction in the need for a permanent stoma.
The excision of the TME specimen in a low rectal cancer is
aided by the Moran triple stapling technique,12 which facili-
tates cross stapling after rectal washout. Stapled low pelvic
reconstruction can then be performed after creation of a short
colon pouch or a side-to-end anastomosis to the low rectum or
a handsewn coloanal canal where necessary.
TME is associated with a symptomatic anastomotic leak-
age rate of 5–28%.13–15 The cause is multifactorial16 but a
suboptimal blood supply and proximity to the anal verge17,
18
are the key risk factors.19 The leak rates may vary in differ-
ent units according to the definition, and our preference is that
of the International Study Group of Rectal Cancer.20 We con-
tinue to use full mechanical bowel preparation for all patients
undergoing a restorative rectal cancer procedure as a proximal
stoma does not adequately protect against a faecally loaded
colon.21 We prefer to perform a defunctioning stoma to miti-
gate the consequences of a leak from a low colorectal
anastomosis.14, 22
Laparoscopic TME
On the one hand, laparoscopic surgery offers a magnified
view that can allow precise and sharp dissection, which aids
the primary objective of obtaining an optimal TME specimen.
On the other hand, operating on mid to low rectal cancers in
the confines of a narrow pelvis presents technical difficulties.
This is most apparent in the obese patient and when the tu-
mour is bulky. In addition, optimal traction and counter trac-
tion can be difficult to achieve as laparoscopic instruments and
staplers currently offer limited angulation.23
J Gastrointest Surg
For colon cancer, several international trials have reported
equivalent outcomes for open and laparoscopic surgery in
terms of safety and oncological outcomes along with
favourable morbidity for laparoscopic surgery.24–27 Rectal
cancer surgery is more challenging and although some trials
have shown comparable results for an open versus laparoscop-
ic approach, this has not been a universal finding.
The two most recent trials, the Australasian Laparoscopic
Cancer of the Rectum (ALaCaRT)28 and the ACOSOG Z6051
trial,29 failed to report ‘non-inferiority’ for laparoscopic rectal
cancer resections compared with open surgery. The conver-
sion rates in these trials were 9 and 11%, respectively. Both
trials used the same composite early endpoint whereby an
adequate surgical resection required 1 complete total
mesorectal excision, 2 a clear circumferential margin
(≥1 mm), and3 a clear distal resection margin (≥1 mm). The
ALaCaRT hypothesised from subgroup analysis that patients
who had received neoadjuvant treatment, or had larger T3
tumours, or higher BMI might have less successful outcome
in the laparoscopic group. However, they did concede that
their study was underpowered to show a significant difference
in these subgroups. There is emerging evidence that the best
oncologic outcomes from laparoscopic resections for rectal
cancer are only achieved after an experience of more than
100 cases and some have suggested that some surgeons par-
ticipating in these two trials may not have achieved the opti-
mal case volume by current standards. (November 2015, Prof
RJC Steele; ACPGBI President)
The UK CLASICC trial included 242 patients with rectal
cancer.26 Although the conversion rate was high at 34%, it
was suggested that perhaps this was because of the learning
curve in laparoscopic rectal cancer surgery. The CRM in-
volvement rate was also noted to be higher in the laparoscopic
group compared to the open group (12 vs. 6%) but this was
non-significant. The UK MRC group subsequently published
medium term follow-up of the CLASICC trial and there was
no difference in the median overall, or disease free, survival
between those who underwent laparoscopic or open surgery
for rectal cancer.30 The COLOR II trial31 included 1044 pa-
tients with rectal cancer and randomised 739 patients to the
laparoscopic arm and 364 patients to the open arm. A conver-
sion rate of 17% was reported reflecting likely technical im-
provements compared over the CLASICC trial. The CRM
involvement in both the laparoscopic and open groups was
10% (as defined by tumour within <2 mm of the resection
margin). Loco-regional recurrence at 3 years was 5% in both
groups. The COREAN trial compared 340 patients who had
received neoadjuvant treatment for stage II/III mid to low
rectal cancer and then randomised to laparoscopic or open
resection. Their earlier report in 201032 of short-term out-
comes and their more recent report in 201433 on medium-
term follow-up did not show any difference in the quality of
oncologic resection or medium- to long-term outcome. The
J Gastrointest Surg
CRM involvement rate was 3% with a conversion rate of only
1.5%. The mean BMI of the patients included in the
COREAN trial was 24 which is lower than that of the typical
western population and could have a bearing on the low con-
version rates.
A meta-analysis in 2015 by Arezzo et al.34 included pa-
tients from 8 randomised controlled trials (2659 patients) and
19 prospective or retrospective studies (8202 patients) who
had undergone laparoscopic or open rectal cancer resection.
CRM positivity was similar in both groups (10.3 and 11.6%,
respectively). Local recurrence for cancer within 12 cm was
3.5 and 5.6% in the laparoscopic and open groups,
respectively.
Our interpretation of these trials is that case selection is
crucial and that an ‘adapted’ incision should always be con-
sidered for oncological safety if needed.
We acknowledge that rectal division and anastomosis is
challenging laparoscopically. The reduced tactile feedback
makes it more difficult to know whether the stapler is below
the tumour. Moreover, current laparoscopic staplers have a
maximum angle of 65° so that horizontal division of the rec-
tum can be difficult from lateral ports. This often results in
multiple firings of the stapler. Three or more stapler firings
have been reported to more than double (13.2 vs. 5.8%) the
risk of anastomotic leak.35 This is probably due to an in-
creased in the risk of steps or ‘dog ears’ at the anastomosis.23
The morbidity and potential for impaired oncological out-
comes as a direct consequence of a leak are established.36, 37
Given the paramount importance of oncological outcome,
we use the triple stapling technique38 for performing distal
transection. We staple below the tumour and, in a further step
to minimise the risk of recurrence,39 we wash the rectum below
the closed staple line. Rectal division is then performed through
the washed part of the rectum. This technique, though often
feasible, can be challenging laparoscopically. An alternative
strategy is to complete the TME dissection laparoscopically
and then use TA30/45 staplers through a slightly wider
Pfannenstiel incision that required for specimen extraction.23
A similar hybrid approach has been described previously.28
This showed that the short-term benefits of laparoscopic sur-
gery are not negated when splenic flexure mobilisation and
IMA ligation are carried out laparoscopically and the critical
pelvis dissection is performed as an open procedure through a
pfannenstial/lower midline incision.
One of the explanations proposed for the findings of the
non-inferiority trials is that rectal cancer resections which are
challenging can be more difficult to perform in a deep pelvis
with in-line rigid instruments, from angles that require diffi-
cult manoeuvres to reach the most inferior limits of the
pelvis.29 There is emerging interest in the modification of
instruments and/or a different platform such as TaTME
(transanal TME) or robotic-assisted surgery which may im-
prove efficacy of minimally access techniques.
Robotic TME
Robotic surgery is another platform gaining popularity in rec-
tal cancer surgery. Robotic technology can alleviate some of
the technical limitations of loss of dexterity due to straight
laparoscopic instruments, unstable camera view and compro-
mised ergonomics. Some of the advantages of the robot in-
clude intuitive manipulation of instruments with flexible
‘wristed’ articulation, a three dimensional field view, stable
camera platform, dexterity enhancement and an ergonomic
operating environment. A further major advantage is the sur-
geon’s simultaneous control of the camera and two additional
instruments to facilitate traction and counter traction.
Nevertheless, clear benefits for robotic low rectal cancer
surgery have not been defined.40 Currently total robotic rectal
cancer surgery can be challenging with a single docking due to
the need to operate in more than one quadrant. Thus, in splenic
flexure mobilisation, there is potential for collision of robotic
arms and loss of tactile feedback, although techniques to avoid
this have been published.41 Despite these limitations, a large
robotic TME case series of 965 patients42 and several meta-
analysis43–45 have reported a reduction in the conversion rate
when compared with laparoscopic TME. It has been reported
that patients converted from lap to open resection have a higher
operative morbidity and mortality and poorer oncological out-
come compared to the laparoscopic completed or open group.46
Preliminary data from the Robotic versus Laparoscopic
Resection for Rectal cancer (ROLARR) trial has not shown
any significant difference in the conversion rate between lapa-
roscopic and robotic TME. Similar rates of CRM involvement,
30 day complications and mortality were also observed.47
There have been suggestions that skill acquisition may be faster
in robotic compared with laparoscopic surgery. A further argu-
ment in favour of robotic surgery is that the increased precision
and high-definition view will enable improve quality of life by
allowing greater nerve preservation in the pelvis. However, to
date, no prospective quality of life data has supported this ar-
gument. Although the ROLARR trial suggested that
Laparoscopic and Robotic surgery costs were equivalent,48 in
most hospitals, there are real concerns that robotic surgery is
markedly more expensive. Without robust evidence to demon-
strate significant quality of life or oncological gains, many units
may find these additional costs difficult to justify.
Transanal TME
Transanal TME (TaTME) involves a combined approach of
abdominal proximal dissection (usually performed
laparoscopically) and ligation of the IMA along with dissec-
tion in the mesorectal plane from the ‘bottom-up’.49 Two
small case series by Atallah et al. and de Lacy et al. have
suggested that this approach is safe, and the authors argue that

this allows easier dissection in the mesorectal plane, especially
in obese male patients.50, 51 Recently, the Bordeaux team en-
dorsed this approach in a randomised controlled trial compar-
ing laparoscopic TME with transanal TME using open surgery
via the perineal approach for rectal cancer <6 cm from the anal
verge. The CRM involvement rate was reduced in the perineal
group suggesting that the ‘bottom up’ approach may have
some advantages.52
More recently, there has been a significant improvement in
one of the technical aspects of TaTME with the introduction of
Airseal™ which is the CO2 insufflator made by SurgiQuest. It
helps limit the ‘bellowing’ or collapse and re-expansion within
the operative field with the insufflation and loss of CO2 which
is part of the cycling process, thereby providing a more stable
operating platform. The AirSeal also clears the excessive
plumes of smoke which tend to obscure the operative field very
quickly and thus provides a clearer view.53 Bill Heald, in his
editorial, ‘A new solution to some old problems: transanal
TME’49 speculated that marrying the transanal approach with
the improved gas tight seal technique along with direct ‘holy
plane’ dissection from below might revolutionise rectal cancer
surgery. It is however worth mentioning that whilst ‘pneumo-
pelvis’ works as an aid during dissection, tissue planes beyond
the correct perimesoectal plane may be opened leading the
surgeon astray. This can occur laterally at the level of the mid
rectum and posteriorly at the level of mid and upper rectum
taking the surgeon into a plane ‘too deep’ thereby entering the
presacral space. This can lead to autonomic nerve damage and
also haemorrhage from the sacral venous plexus posteriorly.53
Despite the initial interest in TaTME, there are important
questions that need to be addressed. These include selection of
rectal cancer patients most likely to benefit from this proce-
dure, long-term functional and oncological outcomes and
analysis of the factors pertaining to the learning curve to
achieve optimal performance and whether all or selected rectal
cancer surgeons should perform TaTME.54 It seems likely that
experience in TEMS/TAMIS and laparoscopic anterior resec-
tion is beneficial to the learning curve of TaTME but currently,
there is no data on key factors to limit the learning curve. It is
likely that cadaveric workshops and mentoring may be bene-
ficial. Initial experience of TaTME can be developed on be-
nign cases (such as rectal resection for inflammatory bowel
disease) and in patients with rectal cancer who do not have
locally advanced tumours. There are however some anatomi-
cal and pathological factors that influence the choice of sur-
gery in favour of TaTME. These may include the male narrow
deep pelvis, tumours in the distal third of the rectum, locally
advanced cancer, visceral obesity, prostatic hypertrophy, large
tumour diameter and post-neoadjuvant radiotherapy.54
A systematic review, mainly comprised of case reports, case
series and comparative studies, concluded that TaTME was a
feasible and reproducible technique.55 The oncologic quality of
resection was found to be comparable with other techniques as
J Gastrointest Surg
evidenced by a CRM involvement in 5% and distal resection
margin (DRM) involvement in 0.3% of cases, which is equiv-
alent to open TME outcomes (CRM involvement- 1.3-18.1%
and DRM—0 to 1.2%, respectively).55 Whilst the preliminary
data is encouraging,56 the long-term oncological outcomes for
TaTME are unavailable currently.
The actively recruiting COLOR III trial, which is an inter-
national, multicentre, superiority, RCT designed to compare
TaTME and conventional laparoscopic TME as the surgical
treatment of mid and low rectal carcinomas, may help to pro-
duce more robust TaTME evidence.57 Our practice has been to
help provide evidence for the efficacy of TaTME by entering all
patients into the TaTME registry (http://www.pelicancancer.
org/bowel-cancer-research/tatme) which is a freely available
voluntary online database that now contains over 1300
registered cases.58
The majority of surgeons have reported a significant learn-
ing curve with this new approach.54 Whilst in a systematic
review, the peri-operative morbidity and the rate of intra-
operative rectal perforation in TaTME were comparable to
open and laparoscopic TME;55 the risk of urethral injury in
TaTME warrants discussion. Urethral injury is a serious com-
plication specific to the TaTME approach and rarely if ever
occurs in open or laparoscopic TME, though of course is well
described as a possible complication in APE surgery. The risk
of urethral injury is increased at the level of the post-prostatic
urethra particularly in anterior tumours treated by neoadjuvant
therapy and is a consequence of the prostate being inadvertent-
ly pulled down into the plane of dissection. Despite small num-
bers of urethral injury during TaTME were reported in
literature,55 some of whom may be part of the initial learning
curve; urethral injury remains a real risk with potentially seri-
ous consequences. We suggest that adequately supervised,
technically adept surgeons and minimal access trained surgeons
should undertake TaTME and that high-quality data is collected
to allow safe and responsible introduction of this procedure.54
Finally, there is concern about neorectal function where the
majority of patients undergoing TaTME have had pre-
operative radiotherapy, a low anastomosis and trauma to the
sphincter complex and further long-term follow-up are
awaited. Simultaneous combined abdominal laparoscopic
and perineal surgery has the potential for shorter operating
times.56 However, caution is needed to ensure that the poor
outcomes of ‘synchronous APE’ are not repeated with
TaTME. TaTME may allow transanal extraction of the speci-
men, though this may not always be possible especially if the
mesorectum is bulky, the pelvis is narrow or there is a large
prostate.54 This can result in a tear in the mesorectum, produc-
ing a suboptimal specimen and potentially shedding tumour
cells. We favour transabdominal extraction using an Alexis
retractor.
In summary, TaTME has the potential to define distal and
radial margins of the lower rectum more clearly and precisely.
J Gastrointest Surg
This may be beneficial, for example, in a male, obese patient
who has had pre-operative radiotherapy for a tumour in the
lower third of the rectum, where laparoscopic, robotic or open
surgery may be difficult.59 The distal margin in TaTME is
assessed at the beginning and this may improve sphincter
preservation rates.53
Multimodal Approach
Combinations of technology, through the abdomen or via the
transanal route with individualised case selection, are likely to
be the future in rectal cancer surgery. In the French study
comparing the need for transanal completion of surgery using
a transanal endoscopic operation device (TEO) in robotic ver-
sus laparoscopic TME for sphincter saving surgery; robotic
TME allowed complete abdominal rectal dissection more of-
ten than laparoscopic TME. The conversion rate to open sur-
gery was low in both groups (3.2 vs. 4.7%, respectively). The
rate of transanal completion was 1.7% in the robotic TME
group and 16.7% in the Lap TME group (p = 0.004). The
authors concluded that whilst robotic TME may allow com-
plete rectal dissection by the abdominal route, laparoscopic
TME requires transanal completion more often in difficult
cases.40
Training and Mentorship
The evolution and revolution of surgical techniques in the
treatment of rectal cancer are exciting. A recent survey of
ACPGBI members on training needs reported TATME as
the foremost area of interest and development. The challenge
for the surgical community is how to safely introduce novel
techniques.
The UK Lapco training programme for laparoscopic colo-
rectal surgery which ran between 2008 and 2013 changed
adoption rates in the UK from 8 to 40%.60 The key to the
programme was surgical mentorship with expert surgeons
providing hands on experience to trainee surgeons. This not
only increased procedural adoption but allowed training to be
performed with excellent outcomes. Thus, conversion to open
rates between 5 and 10% were maintained when trainees
adopted independent laparoscopic practice.61
Additionally, as part of this programme, a Lapco ‘Train the
trainers’ programme (Lapco TT), specific to laparoscopic sur-
gery, was developed. This course has been evaluated by
Kirkpatrick’s four levels of evaluation which includes (a)
pre- and post-course interviews, (b) a training quality assess-
ment during the course (STTAR Tool), interviews after 4–
6 months, (c) course delegates training performance rated by
their trainees (mini-STTAR) and (d) assessing competence
gain by trainees before and after their trainer (delegate)
attended the course.62
The output of the Lapco training programme and Lapco TT
course is demonstrating that hands-on mentorship works to
allow adoption of new techniques and unsurprisingly both
training experts, and surgeons in training, can further improve
their performance and ability to mentor trainees. As new tech-
niques for rectal cancer emerge, the old adage of ‘See one, do
one and teach one’ can no longer apply and is not appropriate
and acceptable for our patients.
Multi-Disciplinary Team
The management of rectal cancer is increasingly complex with
advances in pre-operative imaging, selective neoadjuvant che-
motherapy alone or chemo radiotherapy and surgical tech-
nique. Multidisciplinary team (MDT) practice appears to im-
prove outcomes63 with evidence for increased rates of sphinc-
ter preservation64 and TME quality,64 and improved oncolog-
ical outcomes.65, 66 Consequently, it is now internationally
recognised that the multidisciplinary team meeting is a crucial
forum for the decision-making process in the management of
rectal cancer.67 This is well summarised by the LOREC (Low
Rectal Cancer English National Development) programme
which concluded that‘Decisions are more important than
incisions’.68
Optimal rectal cancer management requires a MDT that
can facilitate complex decisions for individual patients.
Personalising the operative modality to the patient, selecting
when open or laparoscopic or robotic and/or transanal options
are appropriate, forms one of these important decisions.
Conclusion
Rectal cancer should be managed by teams with experience
and a dedication to develop new skills and remain up to date
with all options for their patients. Indeed, in 1957, Cuthbert
Dukes when asked about the merits of four different opera-
tions for rectal cancer replied ‘I should not choose the opera-
tion but I should choose the surgeon, and I should choose him
with very great care’ This remains pertinent today but perhaps
not only to the surgeon but to the MDT as a whole.
Laparoscopic surgery can be particularly challenging for low
rectal cancer but in the appropriately selected patient can pro-
duce good outcomes. It should be part of the armamentarium
in units who have the appropriate case load for treating rectal
cancer, as opposed to the ‘be all and end all’ approach. This is
especially relevant when approaches like TaTME and robotic
TME are evolving. These approaches certainly have technical
and ergonomic advantages, which can increase the chances of
obtaining an optimal TME specimen in difficult cases. Whilst
surgical training and experience are crucial to technique and
outcomes, case selection is essential in the choice of the access
technique, whether open, laparoscopic, transanal or robotic

TME. Ultimately, the key quality control in all techniques for
TME must be the aspiration to produce the ‘perfect TME
resected specimen’—the technical approach that achieves this
is secondary.
Compliance with Ethical Standards
Grant Assistance Not applicable.
Confirmation of Authorship This is to confirm that Sanjeev Dayal,
Nick Battersby and Tom Cecil meet the following guidelines as per the
International Committee of Medical Journal Editors (ICMJE) for author-
ship of this article:
1. Substantial contributions to the conception and design of the work,
analysis and interpretation of data both from personal experience and
literature
2. Drafting the work or revising it critically for important intellectual
content
3. Final approval of the version to be published
4. Agreement to be accountable for all aspects of the work in ensuring
that questions related to the accuracy or integrity of any part of the
work are appropriately investigated and resolved
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