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Does peritoneal perforation affect short- and long-term outcomes
after transanal endoscopic microsurgery?
Mario Morino •Marco Ettore Allaix •
Federico Famiglietti •Mario Caldart •
Alberto Arezzo
Received: 4 February 2012 / Accepted: 21 May 2012 / Published online: 21 June 2012
ÓSpringer Science+Business Media, LLC 2012
Abstract
Background Peritoneal perforation (PP) is frequently
reported as a complication of transanal endoscopic micro-
surgery (TEM). Nevertheless, these concerns have only
rarely been addressed in the literature, with no mention of
the long-term oncologic consequences of PP.
Methods A prospective database was analyzed with the
intent to evaluate the influence of PP on the short- and
long-term outcomes for patients undergoing TEM.
Results Peritoneal perforation occurred in 28 (5.8 %) of
481 patients who underwent TEM for a rectal neoplasm.
The conversion rate to abdominal surgery was 10.7 %
(3/28). All the conversions occurred during the first 100
TEM procedures (3/100 vs 0/381; p=0.007). The postop-
erative morbidity rate was 3.6 % (1/28), and the 30-day
mortality was nil. Compared with the group of patients who
had no peritoneal perforation, the PP group showed a sig-
nificantly longer operating time (120 vs 60 min; p\0.001)
and a significantly longer hospital stay (6 vs 4 days;
p=0.003). Nevertheless, the global morbidity rate and the
type of complications according to Dindo’s classification
were similar. In the multivariate analysis, the only inde-
pendent predictor of PP was tumor distance from the anal
verge (p=0.010). During a median follow-up period of
48 months (range, 12–150 months), no liver or peritoneal
metastases were detected in 13 patients with rectal cancer.
Conclusions Peritoneal perforation does not seem to
affect short-term or oncologic outcomes for patients sub-
mitted to TEM with full-thickness resection for upper
rectum neoplasms. The use of TEM to resect rectal lesions
involving the intraperitoneal rectum may therefore repre-
sent an intermediate step toward the development of
transrectal natural orifice translumenal endoscopic surgery
(NOTES) techniques.
Keywords Full-thickness excision Morbidity
Peritoneal perforation Rectal neoplasm Transanal
endoscopic microsurgery
Routine excision of the intact mesorectum for cancer of the
mid and low rectum has resulted in the lowest incidence of
local recurrences ever reported [1]. Nevertheless, total
mesorectal excision (TME) is associated with high rates of
genitourinary dysfunctions [2–5], anastomotic leakage [6],
and long-term functional bowel discomfort [7].
Proposed by Buess et al. [8,9] nearly 30 years ago,
transanal endoscopic microsurgery (TEM) combines the
advantages of minimally invasive local treatment with
large full-thickness local resection and improved visuali-
zation. It rapidly became the standard of treatment for large
rectal adenomas [10,11].
More recently, TEM has become a viable alternative in
the management of selected early rectal cancer [12,13].
Combined with neoadjuvant treatment, TEM is progres-
sively extending its indications because of its mild impact
on patient recovery [14].
Originally, TEM was devised to remove extraperitoneal
lesions. A peritoneal perforation (PP) was frequently
M. Morino M. E. Allaix (&)F. Famiglietti
M. Caldart A. Arezzo
Digestive, Colorectal, Oncologic and Minimally Invasive
Surgery, Dipartimento di Discipline Medico-Chirurgiche,
University of Torino, Corso A. M. Dogliotti 14, 10126 Torino,
Italy
e-mail: Marcoettore_allaix@yahoo.it
M. Morino
e-mail: mario.morino@unito.it
123
Surg Endosc (2013) 27:181–188
DOI 10.1007/s00464-012-2418-x
and Other Interventional Techniques
reported as a complication of TEM, and tumors of the
upper rectum, particularly when located on the anterior or
lateral portion of the rectum, were considered a contrain-
dication to TEM [15–18]. Peritoneal perforation makes it
difficult or impossible to maintain a stable pneumorectum,
often creating a formidable technical challenge for the
surgeon. Furthermore, insufflation of carbon dioxide (CO
2
)
from the rectum into the peritoneum is considered a
potential cause of clinical and oncologic complications.
Nevertheless, these concerns have only rarely been
addressed in the literature, with no mention of the long-
term oncologic consequences of PP.
However, the recent introduction of natural orifice
translumenal endoscopic surgery (NOTES) techniques as
means of access to the peritoneum through the rectum has
aroused controversy about the safety and efficacy of such a
proposal [19]. We believe that with an analysis of the
clinical consequences resulting from PP during TEM, some
points in the debate could be clarified and that the current
technical and clinical limitations of local excision of rectal
neoplasms by TEM could be elucidated.
Thus, this study aimed to evaluate the influence of PP on
the short- and long-term outcomes for patients undergoing
TEM and to compare our results with evidence from the
literature.
Material and methods
This study was a retrospective analysis of a prospective
database created in January 1993. Patients in whom a PP
occurred during a TEM procedure were identified from the
data on the operative report. The indications for TEM were
benign rectal lesions judged unsuitable for endoscopic
removal, early rectal cancer, and invasive or metastatic
rectal carcinoma treated with palliative intent.
A rigid rectoscopy was routinely performed to locate the
lesion along the circumference and to measure its distance
from the anal verge. The preoperative workup and surgical
technique have been described previously [20].
The procedure was performed with the patient under
general anesthesia in all cases. Until 2008, we routinely
used Richard Wolf (Knittingen, Germany) TEM equipment
conceived by Buess [8]. Afterward, we used transanal
endoscopic operation (TEO) instrumentation (Karl Storz
GmbH, Tuttlingen, Germany).
When the original Richard Wolf TEM equipment was
used, patient positioning was varied to keep the lesion in
the inferior part of the surgical field. Since we began to use
the TEO instrumentarium, the patient ordinarily is placed
supine due to the particular shape of the TEO rectoscope
tip, which allows tissue handling over the entire surgical
field, including its superior quadrant. Nevertheless, for
treating lesions in the upper rectum and large neoplasms
involving the anterior rectal wall, which are at risk for PP,
the patient is placed prone to reduce gas losses and to help
to maintain a stable pneumorectum if a PP occurs.
Since 2008, when we began to use the TEO, and with
increasing surgical experience, a more liberal policy
toward lesions located higher has been adopted. In all cases
in this series, a full-thickness excision was made on the
rectal wall to the perirectal fatty tissue, and the wound was
closed with one or more running sutures secured with
dedicated silver clips (Richard Wolf). The same technique
was used to close the peritoneum and to reconstruct the
rectum if PP occurred.
We analyzed patient characteristics, operative data, and
the short- and long-term outcomes of two groups: the no
peritoneal perforation (NPP) group and the PP group. The
patient characteristics were age, gender, and preoperative
indication for TEM. The operative data included length of
the operative procedure and rate of conversion to abdom-
inal surgery. The short-term outcomes were defined as
postoperative morbidity according to Dindo’s classification
[21], 30-day mortality, and length of hospital stay. The
long-term outcomes were defined as the local tumor
recurrence rate and the incidence of distant metastases.
Follow-up assessment involved digital examination,
rectoscopy, and tumor marker testing (in case of malignant
lesions) every 3 months for the first 2 years, then every
6 months thereafter. A full colonoscopy was performed at
12, 36, and 60 months. In case of malignancy in NPP group
and in all cases of PP, abdominal and pelvic computed
tomography (CT) scans also were obtained at 6, 12, and
24 months for early detection of peritoneal seeding (of
adenomatous or cancer tissue) and liver metastases.
Quantitative data are given as median and range.
Chi-square tests were used to compare proportions. The
Student’s t-test was used to compare normally distributed
variables.
A stepwise logistic regression analysis was performed to
identify factors predictive of PP. The variables potentially
related to PP with a pvalue of 0.200 or less in the univariate
analysis were entered into a multivariate analysis. The pre-
dictor variables used were patient age, gender, tumor diam-
eter, tumor distance from the anal verge, and tumor
localization on the rectal wall. A level of 5 % was set as the
criterion for statistical significance. The data were entered on
an Excel spreadsheet. The statistical analysis was performed
using SPSS Software (SPSS Inc., Chicago, IL, USA).
Results
Between January 1993 and December 2010, 481 patients
(289 males and 192 females; median age, 68 years; range,
182 Surg Endosc (2013) 27:181–188
123
13–94 years) underwent TEM. Perforation of the perito-
neum occurred in 28 cases (5.8 %, PP group), with 14
cases (50 %) involving men (median age, 70.5 years;
range, 41–94 years). Peritoneal perforation was experi-
enced by 15 (8.5 %) of 177 patients who had surgery in the
preceding 4 years versus 13 of 304 patients (4.3 %) who
underwent surgery earlier (p=0.090). Table 1reports the
patients’ characteristics and perioperative data.
The preoperative indications were 23 adenomas and 5
carcinomas (4 uT1N0 and 1 uT2N0). The median diameter
of the rectal lesion was 5 cm (range, 3–10 cm). The dis-
tance between the lower edge of the neoplasm and the anal
verge ranged between 6 and 13 cm (median, 9 cm).
In the PP group, the neoplasm was located on the anterior
wall in ten patients (35.7 %), the lateral wall in nine patients
(32.1 %), and the posterior wall in four patients (14.3 %). It
was circumferential in five patients (17.9 %).
In 25 cases (89.3 %), the PP was sutured by TEM. In 3
cases (10.7 %), PP necessitated conversion to laparoscopic
(2 cases) or open (1 case) anterior resection. All conver-
sions occurred during the first 100 TEM procedures (3/100
vs 0/381; p=0.007). The median operating time was
120 min (range, 35–320 min). Excluding the 3 cases con-
verted to abdominal surgery, the operating time ranged
from 35 to 240 min (median, 120 min). No intraoperative
blood transfusions were required.
We observed one case of postoperative complications
(3.6 %) involving a rectovesical fistula that required sub-
sequent abdominoperineal resection. No 30-day mortality
was observed. The median hospital stay was 6 days (range,
4–14 days).
Compared with the NPP group, the PP patients showed a
significantly longer operating time (120 vs 60 min;
p\0.001) and a significantly longer hospital stay (6 vs
4 days; p=0.003). Nevertheless, the global morbidity rate
and type of complications were similar in the two groups
(Tables 1,2). Histologic examination of the surgical
specimens confirmed an adenoma in 15 cases (53.6 %),
with invaded margins in 3 cases (20 %). The rate of margin
invasion was higher than that of the 246 patients with
adenoma in the NPP group, but the difference was not
significant (20 vs 10.2 %; p=0.444). A rectal cancer was
diagnosed in the remaining 13 patients (46.4 %): 7 pT1, 5
pT2, and 1 pT3. Histology detected no margin invasion in
this group. In two cases, the margin clearance was less than
1 mm. The resection was judged to be full thickness in all
cases, and no specimen fragmentation occurred.
Table 3shows the univariate analysis for risk of PP. Of
all the variables taken into consideration, tumor distance
from the anal verge (p=0.005), tumor diameter
(p=0.038), and tumor location on the entire circumfer-
ence (p\0.001) demonstrated a statistically significant
role. The multivariate analysis of the risk for PP, also
shown in Table 3, indicates tumor distance from the anal
verge as a unique independent predictor (p=0.010).
During a median follow-up period of 72 months (range,
12–216 months), no patient with adenoma was lost to
follow-up evaluation. At this writing, all patients are dis-
ease free with no sign of local recurrence or intraperitoneal
seeding of adenomatous tissue.
Table 1 Patient characteristics
PP (n=28) NPP (n=453) pvalue
Male gender: n(%) 14 (50) 275 (60.7) 0.356
Median age: years (range) 70.5 (41–94) 67 (13–91) 0.366
Median distance from anal verge: cm (range) 9 (6–13) 7 (2–15) \0.001
Median tumor diameter: cm (range) 5 (3–10) 4 (3–12) 0.372
Median operative time: min (range) 120 (35–320)
120 (35–240)
a
60 (15–235) \0.001
\0.001
Postoperative complications: n(%) 1 (3.6) 28 (6.2) 0.879
Median hospital stay: days (range) 6 (4–14) 4 (2–20) 0.003
PP peritoneal perforation group, NPP no peritoneal perforation group
a
Three cases of conversion to abdominal surgery were excluded
Table 2 Postoperative morbidity according to Dindo’s classification
PP
(n=28)
NPP
(n=453)
pvalue
n(%) n(%)
Postoperative
complications
1 (3.6) 28 (6.2) 0.879
Grade 1 0 6 (1.3) 0.781
Grade 2 0 9 (1.9) 0.999
Grade 3 1 (3.6) 13 (2.9) 0.716
3a 0 6 (1.3) 0.781
3b 1 (3.6) 7 (1.5) 0.934
Grade 4 0 0
Grade 5 0 0
PP peritoneal perforation group, NPP no peritoneal perforation group
Surg Endosc (2013) 27:181–188 183
123
During a median follow-up period of 48 months (range,
12–150 months), no patient with rectal cancer was lost to
follow-up evaluation. The follow-up period was longer than
3 years for 69% (9/13) of the patients, and longer than 4 years
for 46.1 % (6/13) of the patients. At this writing, all the
patients with a pT1 rectal cancer are disease free. Among the
pT2 patients, two patients underwent postoperative chemo-
radiotherapy, two patients had abdominal surgery (laparo-
scopic TME), and all are disease free at this writing. Neither
patient submitted to TME had any intraoperative evidence of
liver metastases or peritoneal carcinomatosis. Their postop-
erative course was uneventful. One pT2 patient refused any
treatment after TEM, had a local recurrence after 13 months,
underwent chemoradiotherapy, and died of lung metastases
42 months after TEM. The uT2 patient who underwent TEM
with palliative intent because of severe cardiac comorbidities
and had a postoperative diagnosis of pT3 rectal cancer locally
relapsed after 4 months, refused further treatment, and died of
lung metastases 12 months after TEM. During the follow-up
period, no liver or peritoneal metastases were detected in any
of the patients who had neoplasms treated with radical intent
in the PP group (Table 4).
Discussion
Although PP is frequently considered a complication of
TEM [18,22–34], few studies have addressed this concern
specifically to date [35–37]. With a view to clarify the
short- and long-term implications of PP during TEM, we
analyzed our series of 28 PP cases and compared the results
with the published data.
Globally, 17 studies [18,22–37] have reported the
number of PP occurrences during TEM, showing a mean
PP rate of 4.8 % (148/3100) (Table 5). The reported rate of
PP varies widely between 0 and 32.3 %, reflecting the fact
that a submucosal dissection may be preferred over a full-
thickness excision in cases at risk for PP. However, due to
the discrepancy existing between pre- and postoperative
histology and staging, our policy is to offer an appropriate
Table 3 Risk factors for peritoneal perforation
Variable n=481 Univariate analysis Multivariate analysis
OR (95% CI) pvalue
a
OR (95% CI) Pvalue
a
Age (years)
\68 240 1 0.538
C68 241 1.371 (0.637–2.944)
Gender
Female 192 1 0.356
Male 289 1.544 (0.717–3.305)
Tumor diameter (cm)
\4 271 1 0.038 1 0.235
C4 210 2.446 (1.106–5.423) 1.835 (0.801–3.276)
Distance from the anal verge (cm)
\7 198 1 0.005 1 0.010
C7 283 4.494 (1.532–13.151) 4.276 (1.488–12.266)
Rectal wall
Posterior 181 1 1
Lateral 119 2.766 (0.792–9.663) 0.180 1.833 (0.668–8.011) 0.254
Anterior 169 3.382 (0.987–10.699) 0.053 2.108 (0.880–9.049) 0.105
Circumferential 12 31.607 (14.131–70.668) \0.001 20.014 (0.910–55.467) 0.082
OR odds ratio, CI confidence interval
a
Stepwise logistic regression analysis
Table 4 Oncologic results in patients with peritoneal perforation
(PP)
Adenoma
(n=15)
Carcinoma (n=13)
pT1
(n=7)
pT2–3
(n=6)
Median follow-up: months
(range)
72 (12–216) 48 (12–150)
Local recurrence: n(%) 0 0 2 (33)
Peritoneal seeding: n(%) 0 0 0
Liver/peritoneal
metastases: n(%)
NA 0 0
Lung metastases: n(%) NA 0 2 (33)
NA not applicable
184 Surg Endosc (2013) 27:181–188
123
full-thickness excision, even in the case of anterior wall
lesions, to obtain a complete specimen and to allow a
correct pT staging.
To date, no study has assessed the risk factors for PP. In
our series, in the multivariate analysis, a tumor distance of
7 cm or more from the anal verge was the unique inde-
pendent predictor of PP, whereas the tumor location on the
anterior rectal wall or on the entire circumference showed a
statistical trend toward an increased risk for PP (p=0.105
and p=0.082, respectively).
We observed a trend toward a higher rate of PP in our
series over the last 4 years compared with the preceding
period (8.5 vs 4.3 %, p=0.090), reflecting the extension
of indications to larger and more proximal lesions. The
extension of indications for TEM in our series derived not
only from increased surgical experience and dexterity but
also from the use of the TEO instrument (Karl Storz
GmbH), which allows manipulation and suturing of the
rectal wall on a 360°surface, thanks to the particular shape
of the rectoscope tip.
Concerning intraoperative outcomes, we found that PP
was associated with a significantly longer operative time,
mainly related to the proximal location of the lesion and
closure of the defect, which are technically challenging,
rather than to the learning curve of the surgeon. The
learning curve and the case volume of the surgical centre
Table 5 Peritoneal perforation during transanal endoscopic microsurgery (TEM): review of the literature
Author (year) No. of
TEMs
No. of
PPs (%)
No. of
conversions
(%)
No. of
stomas (%)
Postoperative
morbidity (%)
Median
postoperative stay
(days)
Local
recurrence
(%)
Distant
metastasis
(%)
Demartines
et al [18]
50 2 (4) 1 (50) 1 (50) NA NA NA NA
Cocilovo et al
[22]
56 1 (1.8) 1 (100) 0 NA NA NA NA
Dafnis et al
[23]
58 1 (1.7) 1 (100) 0 NA NA NA NA
Meng et al
[24]
31 2 (6.5) 0 0 0 NA NA NA
Palma et al
[25]
100 8 (8) 1 (12.5) 0 0 NA NA NA
Platell et al
(2004) [26]
113 3 (2.7) 0 0 0 NA NA NA
Whitehouse
et al [27]
146 20 (13.6) 0 6 (30) 0 4.5 NA NA
Ganai et al
(2006) [28]
144 9 (6) 0 0 NA NA NA NA
Zacharakis
et al [29]
76 3 (3.9) 2 (66.6) 1 (33.3) NA NA NA NA
Serra-Aracil
et al [30]
96 1 (1) 0 0 0 NA NA NA
Ramirez et al
[31]
173 7 (4) 1 (14.3) 0 NA NA NA NA
de Graaf et al
[32]
353 28 (8.7) 0 0 0 NA NA NA
Guerrieri et al
[33]
402 13 (3.2) 0 0 NA NA NA NA
Le
´onard et al
[34]
123 2 (1.6) 1 (0.8) 0 0 NA NA NA
Gavagan et al
[35]
34 11 (32.3) 0 0 45 NA NA NA
Ramwell et al
[36]
257 15 (5.8) 5 (33.3) 6 (40) 27 8 NA NA
Baatrup et al
[37]
888 22 (2.5) 0 0 4.5 7 10 14
Global 3100 148 (4.8) 13 (8.8) 14 (9.4)
Current series 481 28 (5.8) 3 (10.7) 1 (3.6) 3.6 6 7 0
PP peritoneal perforation, NA not available
Surg Endosc (2013) 27:181–188 185
123
are two main factors that can influence the treatment
strategy to be adopted when PP occurs. It is noteworthy
that conversion to laparotomy was reported in 50–100 % of
PP cases only in a series with fewer than 100 patients,
whereas it ranged between 0 and 40 % in larger series
(Table 5).
These data confirm the results obtained by Salm et al.
[38] in a survey of 1,900 TEM procedures performed in
Germany in 1994. They reported that the rate of conversion
to laparotomy during TEM for all causes, including inad-
vertent transrectal opening of the peritoneal cavity,
decreased with experience from 11.6 % (1 to 10 TEM
procedures) to 1.2 % ([100 TEM procedures). In our ser-
ies, three conversions were performed during the first 100
TEMs compared with 0/381 in more recent years
(p=0.007), confirming the crucial role that experience
plays in the management of PP.
Only a few studies [24–27,30,32,34–37] have reported
a specific postoperative morbidity rate (range, 0–27 %). No
cases of pelvic sepsis or infectious complications after PP
have been reported. In our series, we observed no statisti-
cally significant difference in the overall complication rate
(3.6 vs 6.2 %) or the degree of severity according to
Dindo’s classification between the PP and NPP groups
(3.6 % of grade 3b complications in the PP group vs 1.5 %
in the NPP group). A longer hospital stay (6 vs 4 days) was
observed for the PP patients, mainly due to a more con-
servative postoperative management.
This study had some limitations, including the retro-
spective design and the relatively small sample size of the
PP group.
However, according to the results of our series, TEM
seems not to be associated with a higher risk for pelvic
infections or other complications when a PP occurs. Fur-
thermore, the low morbidity rate and the absence of pelvic
infectious complications in our series demonstrate that a
nonfunctioning stoma generally is not necessary in high-
volume institutions (Table 5).
To our knowledge, the only study to evaluate the on-
cologic results of patients undergoing TEM with an inad-
vertent PP was that by Baatrup et al. [37], who reported 22
perforations into the peritoneal cavity during a total of 888
TEM procedures for rectal cancer performed at four
European centers. During a median follow-up period of
36 months (range, 3–164 months), local recurrence devel-
oped in one pT1 patient (7 %) and in one pT2 patient
(25 %), whereas distant metastases were detected in three
patients.
In our series, at this writing, during a median follow-up
period longer than 4 years, all the patients who experienced
a PP during TEM for adenoma or pT1 rectal cancer are
disease free, with no sign of intraperitoneal seeding of
adenomatous or cancer tissue. Four pT2 patients who
underwent laparoscopic TME or chemoradiotherapy and
remain disease free. Local recurrence developed only in the
pT2 and pT3 patients who did not receive further treatment
after TEM. No patient with PP has experienced liver or
peritoneal metastases. Therefore, although a limited num-
ber of patients were evaluated and in a retrospective way,
PP does not seem to correlate with an increased risk of
local recurrence or liver/peritoneal metastasis.
In the NOTES era, transrectal access to the peritoneal
cavity has been variously described [39–42], taking into
consideration feasibility and risk for fecal contamination of
the abdomen. In an experimental trial, Denk et al. [43]
demonstrated the feasibility of some transrectal NOTES
procedures (diagnostic peritoneoscopy, liver biopsy, sig-
moid resection) using TEM instrumentation, suggesting
TEM as a portal for NOTES.
The experience gained in handling PP with TEM and the
good results of the current series could enhance confidence
in the management of such situations. The use of TEM to
resect rectal lesions involving the intraperitoneal rectum
may therefore represent an intermediate step toward the
development of transrectal NOTES techniques [19].
However, we believe that the application of the transanal
approach to NOTES may be limited in the future to
selected centers with tremendous experience in TEM to
minimize the risks of conversion to abdominal surgery,
stoma, and perioperative complications. From analysis of
the published data, we found that a stoma was more fre-
quently performed (30–50 %) in series with fewer than 100
TEM procedures [18,29] or by surgeons not particularly
skilled in endoscopic closure of the peritoneal defect [36]
(Table 5).
In our series, no stoma was performed intraoperatively
for PP. Only one patient (3.6 %) had a stoma for treatment
of a postoperative rectovesical fistula after a TEM proce-
dure for a lesion on the anterior rectal wall.
In conclusion, evidence from the literature and our per-
sonal experience suggest that when TEM is performed at
expert centers, indications for TEM can be safely extended
to selected lesions in the upper rectum with no further risk
of conversion to abdominal surgery or a nonfunctioning
stoma and with good early and late oncologic results.
Disclosures The authors Mario Morino, Marco Ettore Allaix,
Federico Famiglietti, Mario Caldart, and Alberto Arezzo have no
conflicts of interest or financial ties to disclose.
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