Original article doi:10.1111/codi.

12381

Completion surgery following transanal endoscopic

microsurgery: assessment of quality and short- and long-term
outcome
R. Hompes*, R. McDonald*, C. Buskens†, I. Lindsey*, N. Armitage‡, J. Hill§, A. Scott¶,
N. J. Mortensen* and C. Cunningham* on behalf of the Association of Coloproctology of Great
Britain and Ireland Transanal Endoscopic Microsurgery Collaboration
*Department of Colorectal Surgery, Oxford University Hospitals, Oxford, UK, †Department of Surgery, Academic Medical Center, Amsterdam, The
Netherlands, ‡Department of Colorectal Surgery, Nottingham University Hospitals, Nottingham, UK, §Department of Colorectal Surgery, Central
Manchester University Hospitals, Manchester, UK and ¶Department of Colorectal Surgery, University Hospitals of Leicester, Leicester, UK

Received 9 January 2013; accepted 21 April 2013; Accepted Article online 12 August 2013

Abstract

Aim Patients with unfavourable pathology after trans-
anal endoscopic microsurgery (TEM) should be offered
completion surgery (CS) if appropriate. The aim of this
retrospective cohort study was to assess the short-term
outcome and long-term oncological results of CS and
identify factors compromising the quality of resection
specimens.
Method Data were retrieved and analysed on patients
who underwent CS from a comprehensive national
TEM database (1992–2008) and the institutional pro-
spective database from the Oxford University Hospitals
(2008–2011).
Results There were 36 patients eligible for analysis.
Postoperative complications occurred in 19 and were
minor (grade I–II) in 13 and major (grade III–V) in six
patients. The quality of the resected specimen was
graded as good in 23 (64%), moderate in six (16.6%)
and poor in seven (19.4%). Full-thickness excision by
TEM (P = 0.03), an interval to CS greater than
7 weeks (P = 0.05) and distally located lesions
(P = 0.04) were associated with increased risk for an
inferior surgical specimen. Overall survival after CS was
91% at 1 year and 83% at 5 years. Patients with a
‘good’ TME specimen had significantly improved dis-
ease-free survival compared with patients with an ‘infe-
rior’ specimen (100 vs 51%, P = 0.001).
Conclusion Patients having full-thickness TEM exci-
sion, distally placed lesions and a long interval
(> 7 weeks) to CS were likely to have an inferior TME
specimen. The results confirm that CS after TEM does
not negatively influence local recurrence and survival,
but the reduced disease-free survival in patients with an
inferior specimen is of concern.
Keywords Cancer, transanal endoscopic microsurgery
(TEM), rectum, completion surgery, recurrence
What does this paper add to the literature?
Reports of completion surgery after transanal endo-
scopic microsurgery are infrequent and predominantly
focus on oncological outcome. We report on the feasi-
bility and quality of total mesorectal excision surgery
after transanal endoscopic microsurgery. Prognostic
factors that have an impact on the difficulty of comple-
tion surgery are described and the impact on long-term
outcome is explored.

ity and poor function and the growing numbers of patients

Introduction
Rectal cancer management has been transformed in the
last two decades, with emphasis on a detailed understand-
ing of pelvic anatomy, meticulous surgery and the targeted
use of chemoradiation [1]. More recently the inherent
drawbacks of radical surgery including morbidity, mortal-
Correspondence to: Roel Hompes, Department of Colorectal Surgery, Oxford
University Hospitals, Old Road, Headington, Oxford OX3 9DU, UK.
E-mail: roelhompes@gmail.com
with early rectal cancer coming through the national
screening programmes has stimulated interest in surgeons
and patients to consider local excision more often [2–5].
Transanal endoscopic microsurgery (TEM) has proved to
be safe and effective for lesions throughout the rectum
[6].
Any method of local excision inevitably involves a
balance between oncological and clinical factors, the
latter including avoidance of peri-operative

e576 Colorectal Disease ª 2013 The Association of Coloproctology of Great Britain and Ireland. 15, 576–581
R. Hompes et al.
morbidity, long-term functional sequelae and, in
some patients, a permanent stoma. In order to mini-
mize oncological compromise, in particular local fail-
ure, patients with adverse pathological features
following local excision should have recourse to
completion surgery (CS).
Completion surgery after local excision for rectal
cancer does not appear to compromise oncological
outcome compared with radical surgery performed as
a primary treatment [7–11]. However, it is unknown
to what extent a previous local excision by TEM dis-
rupts the anatomy of the tissue planes and the
implications for the quality and outcome of CS. This
study aimed to describe the outcome of patients
undergoing CS after TEM and to identify factors
compromising the quality of resection specimens. We
also describe short-term morbidity and long-term
oncological outcome.
Method
Definition of completion surgery
We have used the term ‘completion surgery’ (CS) to
define surgery carried out after local excision to com-
plete surgical treatment of the primary tumour. This is
applied to patients with an inadequate or unclear resec-
tion margin after local excision, unfavourable pathology
according to current standards and patients with a low
risk cancer who still wish to proceed to radical surgery
after counselling.
Data collection
Data were retrieved from a comprehensive national
TEM database (http://www.temsurgery.co.uk). This
was supplemented by a comprehensive chart review by
one of the authors who visited all centres willing to
participate in the study. Additional patients from one
participating centre (Oxford) were included in the
analysis and data were gathered from the institution’s
prospective TEM database. Thirty-six patients were
eligible for analysis. Of the patient cohort (n = 487)
within the UK TEM database (1992–2008), compre-
hensive data on CS could be gathered on 29 (46%)
out of a total of 63 patients undergoing CS. For the
remaining 34 patients, no detailed surgical information
(no detailed operation note available) and no patho-
logical information (no information regarding the
quality of the resection specimen) could be retrieved
and these patients were excluded. This was mainly due
to CS being undertaken in a centre other than that
where the TEM was performed. An additional seven
Colorectal Disease ª 2013 The Association of Coloproctology of Great Britain and Ireland. 15, 576–581
Completion surgery after transanal endoscopic microsurgery
patients were identified in the Oxford patient cohort
(2008–2011).
Other data collected included details on the comple-
tion surgical procedure, morbidity and mortality
according to the Clavien–Dindo classification, hospital
stay and histopathological characteristics of the speci-
men. The long-term oncological outcome was also anal-
ysed.
TEM technique and CS (total mesorectal excision)
The standard Richard Wolf (Knittlingen, Germany)
equipment was used for TEM [7,12]. The type of CS
(anterior resection or abdominoperineal excision) was
selected on the basis of the tumour location, the
appearance of the previous resection site and the sur-
geon’s preference. In general, CS was performed when
the TEM site had completely healed, confirmed by digi-
tal rectal examination and luminal assessment, although
sometimes surgery within 2 or 3 weeks of local excision
was carried out. An open or laparoscopic approach was
undertaken according to the surgeon’s preference.
Based on subjective assessment of the operation note by
two of the authors blinded to other variables, the pro-
cedure was labelled as ‘standard’ (no difficulty at any
stage of the operation) or ‘difficult’ (difficulty as speci-
fied in the operation note). The quality of mesorectal
excision was assessed according to definitions used in
the MRC CR07 trial [13].
Follow-up
Follow-up was carried out for all patients at the time of
data collection. Patients were followed according to
local policy or National Institute for Health and Care
Excellence guidelines on rectal cancer. Data were often
recorded by specialist colorectal cancer nurses.
Statistics
Statistical analysis was performed using PASW STATISTICS
for Windows (version 18, IBM Corporation, Armonk,
NY, USA). Continuous data were given as mean  stan-
dard deviation or as median and range for non-parametric
data. Categorical data were given as frequency or percent-
age. For dichotomous outcomes, groups were compared
by the v2 or Fisher’s exact test. The t test was used to
compare means for parametric data and the Mann–
Whitney U test was used for continuous, not non-para-
metric, data. The cumulative survival rates were calculated
using the Kaplan–Meier method, and differences in
relapse rates were analysed by the log-rank test. A P value
of ≤ 0.05 was considered to be statistically significant.
e577
Completion surgery after transanal endoscopic microsurgery R. Hompes et al.

Results Table 2 Completion surgery characteristics in 36 patients.

Interval (TEM to CS), months* 2 (0.5–8.7)

Patient and tumour/TEM characteristics Procedures
Ultra-low AR 1
The clinico-pathological characteristics of the 36
Open AR 18
patients are summarized in Table 1. The indications for Laparoscopic AR 12
CS were adenocarcinoma (11) and adenoma (25). No APE 4
patient with adenocarcinoma had received any form of Hartmann 1
chemoradiotherapy. A full-thickness excision was per- Operation time, min* 200 (120–360)
formed in all malignant lesions with sampling of the Blood loss, ml* 300 (120–1800)
mesorectum in one case. For the 25 presumed benign Morbidity/mortality (Dindo–Clavien)
lesions a full-thickness excision was performed in 14, Minor (I–II) 13
and a partial thickness and a combination of partial and Major (III–IV) 5
full thickness was carried out in seven and four patients. Mortality (V) 1
Hospital stay, days* 10 (6–76)
The final histology of the TEM specimen revealed one
Final staging after CS†
(3%) patient with a large severely dysplastic adenoma,
Stage I 19
16 (43%) with a pT1 lesion and 19 (54%) with a more Stage II 4
advanced lesion. Stage IIIa 5
Stage IIIb 7
Stage IIIc 0
Completion surgery
TEM, transanal endoscopic microsurgery; CS, completion sur-
Based on the current guidelines proposed in the UK
gery; AR, anterior resection; APE, abdominoperineal excision.
and USA, two patients had CS for an early rectal cancer
*Values are median number with ranges in parentheses.
that had undergone a potentially curative local excision,
†American Joint Committee on Cancer Staging system.
a so-called low risk tumour [7,14]. The other pT1
tumours all contained one or more accepted high risk
defunctioning loop ileostomy in 25/31. In one patient
features and these patients were counselled to have
severe intra-operative bleeding led to conversion of an
completion major surgery, as were the patients with a
open low anterior resection to a low Hartmann’s proce-
pT2–3 tumour.
dure. The procedure was graded as ‘difficult’ in 53% (19/
For the single patient with a severely dysplastic ade-
36) of cases, mostly due to bleeding and/or fibrosis/
noma, CS was performed owing to the possibility of
adhesions at the TEM site. Operation time and total
malignant invasion (Table 2). In 31 (86%) patients a
blood loss were significantly higher in this group of
sphincter-preserving procedure was performed, with a
patients compared with the ‘standard’ cases (230.3 
62.3 min vs 187.5  27.2 min, P = 0.02; and 721.9 
Table 1 Patient and initial tumour characteristics at TEM in
562.4 ml vs 286.9  139.7 ml, P = 0.008, respectively).
36 patients subsequently requiring completion surgery.
Three (9.7%) patients developed a clinically signifi-
Sex, M:F 19:17 cant postoperative anastomotic leak and underwent
Age, years* 64 (39–84) Hartmann’s procedure. Two patients returned to theatre
BMI, kg/m2* 27 (21–40)
for postoperative bleeding and revision of a retracted
Tumour distance from anal verge, cm* 5 (14%)
ileostomy. The median hospital stay was 10 (6–76) days
Tumour location (cm)
Lower rectum (0–6) 9 (2–15)
and six patients were readmitted within 30 days for
Mid rectum (7–11) 25 (69%) pulmonary embolus (n = 1), small bowel obstruction
Upper rectum (12–16) 6 (17%) (n = 3) and stoma related problems (n = 2).
Tumour surface, cm2* 7.2 (0.5–57) The final histology report of the total mesorectal
Specimen surface, cm2* 18 (3.1–142.5) excision specimen showed residual tumour in 17 (47%)
Tumour stage after TEM patients. These included seven with residual tumour
T0 1 (3%) and involved lymph nodes, five with isolated tumour
T1 16 (43%) and five with isolated lymph node involvement. In all
T2 12 (33%) but two patients a microscopically clear excision margin
T3 7 (21%)
resection (R0) was obtained. A total mesorectal excision
TEM, transanal endoscopic microsurgery; BMI, body mass Grade 3 specimen (good) was achieved in 23 (64%)
index. patients, a Grade 2 specimen in six (16.6%) and a Grade
*Value or median number with range in parentheses. 1 specimen (poor) in seven (19.4%) Although there was

e578 Colorectal Disease ª 2013 The Association of Coloproctology of Great Britain and Ireland. 15, 576–581
R. Hompes et al. Completion surgery after transanal endoscopic microsurgery

no correlation between grade of specimen and the type
of resection, specimens with a lower grade were more
frequently found after full-thickness TEM, in distal
lesions and after an interval from TEM to CS of more
than 7 weeks (Table 3). All 13 ‘inferior’ specimens were
in the ‘difficult’ surgery category.
Outcome
Adjuvant chemotherapy or radiotherapy was adminis-
tered in 11 (30.5%) patients after CS. The overall sur-
Table 3 Patient, tumour and procedure related characteristics.
Good Inferior
specimen specimen
(n = 23) (n = 13)
vival at 1 year was 91 and 83% at 5 years. After a
median follow-up of 49.2 (3–137) months, the relapse
rate was 16.7% (6/36) with 1- and 5-year disease-spe-
cific survival rates of 91 and 74%. Only one patient (3%)
developed local recurrence (at 39 months after CS) and
five (14%) developed distant metastases without signs of
local recurrence at a mean follow-up of 33.2 months.
Patients with a ‘good’ total mesorectal excision speci-
men had significantly improved 5-year disease-free
survival compared with patients with an ‘inferior’ speci-
men (100 vs 51%, P = 0.001, log-rank test) (Fig. 1).
Although the number of patients was too small to per-
form a multivariate analysis, no significant correlation
between other prognostic parameters (e.g. pT, pN and
Dukes staging) and reduced disease-free survival could
be demonstrated.
P value

Clinico-pathological parameters Discussion

Age (mean, years)* 64.9  10.7 62.8  14.2 0.6
Sex Large data sets on CS after TEM are lacking and the
Male 11 8 0.4 outcome focuses predominantly on survival with accept-
Female 12 5 able local/distant recurrence rates [7–10]. Anecdotal
Location lesion evidence suggests that this type of surgery is difficult
Anterior 5 6 0.1 and may result in a higher permanent stoma rate
Posterior 7 3 [15,16]. The data presented here show that CS after
Lateral 11 4 TEM is feasible with acceptable postoperative morbidity
Anterior vs posterior 5 vs 18 6 vs 7 0.07 and low mortality. In addition, the reported leak rate of
and lateral
under 10% is comparable with that reported for anterior
Distance anus
Upper 4 2 0.2
Mid 17 7
Lower 2 4
1.0
Lower vs upper and 2 vs 21 4 vs 9 0.04
mid
TEM thickness
Probability of disease-free survival

0.8
Partial 7 0 0.03
Full 16 13
Time to surgery 9.5  7.2 11.7  9.5 0.2
(mean, weeks)* 0.6
≤ 7 weeks 12 3 0.05
> 7 weeks 11 10
Closure TEM defect 0.4
No 14 10 0.3
Yes 9 3
TEM complication 0.2
No 18 11 0.6
Yes 5 2
Type of surgery 0.0
AR 22 9 0.08
0.00 2.00 4.00 6.00 8.00 10.00 12.00
APE 1 3
Follow up in years
Hartmann 0 1
Figure 1 Kaplan–Meier curves of 36 patients having comple-
TEM, transanal endoscopic microsurgery; AR, anterior resec- tion surgery after transanal endoscopic microsurgery. There is a
tion; APE, abdominoperineal excision. Bold font denotes significant difference in disease-free survival between patients
significant values. with ‘good’ (solid line) or ‘inferior’ (dotted line) resection
*Values are mean  SD. specimens (100 vs 51%, P = 0.001, log-rank test).

Colorectal Disease ª 2013 The Association of Coloproctology of Great Britain and Ireland. 15, 576–581 e579
Completion surgery after transanal endoscopic microsurgery
resections [17]. In all but one patient the procedure
could be completed according to the preoperative plan
and in the majority (86%) of patients a sphincter-
preserving procedure was achieved.
In over half of the cases the dissection was difficult
owing to the disruption of the normal tissue planes.
This is reflected by the significantly higher intra-opera-
tive blood loss and operating time. Platell et al. [15]
found that, in patients proceeding to a more radical
procedure within 2–6 weeks after TEM, disruption of
the normal pelvic dissection planes added significantly
to the technical difficulty. The compromised mesorectal
plane and the weakened rectal wall also increase the risk
of disruption of the surgical specimen. Similar to our
results, Levic et al. [8] reported an intra-operative rectal
perforation rate of 20%, all at the previous TEM site.
Thus, violation of the surgical planes not only poten-
tially renders radical surgery after TEM more difficult
but also significantly increases the risk of producing an
inferior specimen. However, these risks have to be con-
sidered against the potential benefits of full-thickness
TEM as a means of offering cure for early stage rectal
neoplasia compared with submucosal excision. The rea-
sons for this decreased survival remain speculative.
Unfortunately, the patient group was too small to
perform a multivariate analysis, but no association with
T-stage and N-stage could be demonstrated. The strong
correlation between survival and an inferior specimen
suggests a potential direct oncological effect related to
difficult surgery (e.g. increased blood loss: 0.7 l vs 0.3 l,
increased tumour spill and circulating tumour cells,
decreased immune system). Overall, the long-term out-
come of patients after CS is acceptable in this popula-
tion, with a 1-year and 5-year disease-free survival of 91
and 74% respectively.
It is striking that only one patient developed local
recurrence and that almost all patients with disease
relapse had metastatic disease. Doornebosch et al. [18]
described a similar outcome in patients following sal-
vage surgery for local recurrence after TEM for T1 rec-
tal cancers; only one patient had a further local
recurrence but seven had distant metastases. They spec-
ulated that these patients represent a different biological
group and that salvage therapy should be intensified
with the inclusion of neoadjuvant radiotherapy and/or
adjuvant chemotherapy in an effort to improve out-
comes. In the study by Levic et al. [8] one patient
developed distal metastasis and no local recurrence was
observed in 25 patients, although the median follow-up
period of 25 months was short.
Various factors were analysed that may contribute to
difficult surgery and an inferior resection specimen. As
expected, an association between a full-thickness TEM
e580 Colorectal Disease ª 2013 The Association of Coloproctology of Great Britain and Ireland. 15, 576–581
R. Hompes et al.
and an inferior total mesorectal excision specimen
could be demonstrated. The same association was
found for distally located lesions with a similar ten-
dency towards an increased chance of obtaining an
inferior specimen in patients with an anterior lesion.
This is in keeping with the anatomical characteristics of
the distal mesorectum, described as the bare area by
Morson et al. [19]. The mesorectal fat peters out dis-
tally as it does for anterior located lesions. These obser-
vations suggest that there might be a greater need for
abdominoperineal excision after TEM of a tumour in
the lower third of the rectum. This might reduce the
chance of a poor or perforated surgical specimen. An
alternative approach to avoid a difficult dissection from
the abdomen is to attempt a perianal disconnection via
a lower third intersphincteric dissection. Clearly, what-
ever approach is chosen, potentially difficult surgery
should be anticipated and an experienced surgical team
should be available. The risk of converting a potential
sphincter-preserving procedure (as primary treatment)
into an abdominoperineal excision needs to be part of
the discussion with the patient before considering
TEM.
There is no consensus regarding the timing of CS.
Examining the impact of various TEM to CS intervals,
we found that an interval longer than 7 weeks signifi-
cantly increased the risk for an inferior specimen. The
cut-off point at 7 weeks is more likely to reflect infec-
tion or dehiscence at the TEM site.
One of the weaknesses of this study is the inevitable
selection bias of the study population. Only 36 patients
were eligible for analysis out of a potential study popu-
lation of 70 patients. The retrospective nature of the
study with strict inclusion criteria led to the exclusion
of 34 patients. Our findings are thus based on a small
group of patients and there is therefore a possibility of
type II error. Furthermore the absence of a common
protocol for the management of these patients and the
impact of surgical experience (with TEM and CS) of
each centre will need to be considered when interpret-
ing the results. While these shortcomings may hamper
strong conclusions, this series is one of the largest series
available and helps to identify risk factors for less
favourable outcomes after CS following TEM.
Transanal endoscopic microsurgery has been a rela-
tively niche subspecialty in colorectal surgery; however,
the increasing incidence of early stage rectal cancer and
the greater availability of transanal minimally invasive
surgery are likely to see it enter mainstream practice
over the next few years as clinicians and patients opt for
organ preservation in favour of radical surgery. In addi-
tion, various national randomized controlled trials com-
paring radical surgery with local excision for rectal
R. Hompes et al.
cancer will also increase patient numbers (TREC trial,
UK; CARTS study, The Netherlands; GRECCAR 2
trial, France). This should be good news for patients,
but one must be cognizant of the pitfalls and challenges
of local excision. These approaches will need to be part
of a strategy for early rectal cancer management that
include CS, careful surveillance and salvage surgery
along with the use of neoadjuvant and other adjuvant
therapy.
In conclusion, CS after TEM is feasible in most
patients without significant morbidity and acceptable
permanent stoma rates. Our results confirm those of
other studies that CS after TEM does not negatively
influence local recurrence and survival, but the reduced
disease-free survival in patients with an inferior speci-
men is of concern. Completion surgery after full-
thickness TEM excision within the distal and/or ante-
rior rectum deserves special consideration. In this group
there may be a role for neoadjuvant and adjuvant treat-
ment strategies combined with CS in an effort to
improve survival.
Author contributions
The concept for this paper was designed by the lead
author and C. Cunningham. Analysis of the data was
performed by C. Buskens and interpretation thereafter
was done by the lead author, C. Cunningham and C.
Buskens. The other authors were crucial for accurate
and detailed data collection and on revision made sug-
gestions regarding the interpretation of the data. The
main draft was written by the lead author with major
input from C. Cunningham. All other authors critically
revised the content and approved the final version of
the paper.
Funding
None declared.
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