Original article
Anastomotic leakage after curative anterior resection for rectal
cancer: short and long-term outcome
C. A. Bertelsen*, A. H. Andreasen†, T. Jørgensen†‡ and H. Harling* on behalf of the Danish
Colorectal Cancer Group
*Department of Surgery K, Bispebjerg University Hospital, University of Copenhagen, Copenhagen, Denmark, †Research Centre for Prevention and Health,
The Capital Region of Denmark, Glostrup, Denmark and ‡Faculty of Health Science, University of Copenhagen, Copenhagen, Denmark
Received 22 July 2008; accepted 10 February 2009; Accepted Article online 29 April 2009
Abstract
Objective The influence of symptomatic anastomotic
leakage (AL) after anterior resection (AR) for rectal
cancer on short and long-term mortality and local and
distant recurrence was analysed.
Method All patients with a first diagnosis of rectal
carcinoma were prospectively registered in a national
database. This comprised 1494 Danish citizens who had
had a curative AR between May 2001 and December
2004. Data on survival and recurrence were obtained
from the National Patient Register. Multivariate analyses
were performed.
Results Anastomotic leakage increased the 30-day mor-
tality [odds ratio (OR) 4.01 (95% CI 2.24–7.17)]. Of
other possible risk factors, only age had a significant
interaction with leakage, as the risk of death within
Introduction
Anastomotic leakage (AL) is a severe complication of
anterior resection (AR) associated with increased mor-
bidity and short-term mortality [1–3]. Its influence on
the risk of recurrence and long-term survival is contro-
versial due to contradictory results in the previously
published studies [1,4–8]. Most data on AL after AR
have been derived from single-centre studies with the
disadvantage of small patient numbers [7–9]. In a
national register, it is possible to collect data on a large
number of patients within a short time span, making the
resulting evidence based on a truly unselected population.
To our knowledge only two large multi-centre studies
[1,3] including multivariate analysis, have investigated
Correspondence to: Claus Anders Bertelsen, Georginevej 1, DK-2970 Hoersholm,
Denmark.
E-mail: cabertelsen@gmail.com
e76  2010 The Authors. Journal Compilation  2010 The Association of Coloproctology of Great Britain and Ireland. Colorectal Disease, 12, e76–e81
doi:10.1111/j.1463-1318.2009.01935.
30 days of AR decreased with increasing age. Long-term
survival decreased significantly after AL [hazard ratio
(HR) of 1.63, CI 1.21–2.19]. A total of 97 (6.7%) and
258 (18.0%) patients had local and distant recurrence
respectively in the follow-up period. The risk of local and
distant recurrence after AL was not different with HR of
1.50 (CI 0.84–2.69) and 1.13 (CI 0.76–1.69) respec-
tively. No other factors influenced the risk of recurrence
due to AL.
Conclusion Anastomotic leakage after AR for rectal
cancer increases the 30-day and long-term mortality,
but AL did not increase the risk of local and distant
recurrence.
Keywords Rectal cancer, anterior resection, anastomotic
leakage, survival, recurrence, national database
the influence of AL on the risk of death or recurrence
after AR for rectal cancer. Only one other [3] included an
unselected cohort derived nationally. We investigated the
influence of AL on 30-day mortality, long-term mortality
and local and distant recurrence after AR for rectal cancer.
Method
As reported previously [10], the study was based on the
National Register of Colorectal Cancer which included at
least 95% of all patients treated since May 2001 in
Denmark for first time colorectal adenocarcinoma. In this
study, the key event was a symptomatic anastomotic
leakage defined as peritonitis and a defect in the anasto-
mosis, or discharge of pus from the rectum, or recto-
vaginal fistula, or the passage of faeces or gas from an
abdominal drain.
The leakage had to be verified using digital examina-
tion, endoscopy, CT scan, contrast radiology or
C. A. Bertelsen et al.
reoperation. None of the participating hospitals in the
study routinely investigated for subclinical AL. Thus the
reported rate of symptomatic AL was an underestimate of
all AL.
Operative mortality was taken as 30-day mortality.
Local recurrence was defined as a pelvic or intraluminal
recurrence at the level of the anastomosis. Data regarding
recurrence were obtained from medical records and the
National Patient Register and survival data were collected
form the National Patient Register.
The study was conducted on behalf of the Danish
Colorectal Cancer Group and was approved by The
Danish Data Protection Agency and the National Ethics
Committee of Science.
Patients
Data on the 1495 patients in the register who under-
went a curative anterior resection for rectal adenocarci-
noma between May 2001 and December 2004 have
been reported previously [10]. One patient was not a
Danish resident and was excluded from the study. Two
were lost to follow up and were excluded from the
analysis of long-term survival and recurrence. Follow up
with respect to recurrence and survival was terminated
by the end of February 2007 and the end of June 2007
respectively.
Statistical analysis
The influence of possible risk factors on 30-day mortal-
ity after anterior resection was investigated in a univar-
iate analysis using a v2 test for categorical variables and a
Wilcoxon test for continuous variables. The long-term
survival and local and distant recurrence were investi-
gated for patients alive at day 30 in univariate analyses
using the log rank test for categorical predictors and
Cox-regression models for continuous variables. The
influence of possible confounding factors on 30-day
mortality, long-term survival and recurrence was analy-
sed using logistic regression analysis for the 30 day
mortality and Cox regression analysis with time from day
30 after surgery. These variables were included stepwise
in models 1 to 5 as follows: Model 1: Anastomotic
leakage; Model 2 (Patient factors): Model 1 + age and
gender; Model 3 (Process factors): Model 2 + peroper-
ative bleeding, preoperative radiotherapy, coloanal
pouch (any kind), faecal diversion and surgery per-
formed or supervised by a surgeon specialized in GI
surgery; Model 4 (Disease factors): Model 3 + tumour
stage according to Dukes and tumour distance from the
anal verge; and Model 5 (Comorbidity factors): Model 4
+ ASA score.
 2010 The Authors. Journal Compilation  2010 The Association of Coloproctology of Great Britain and Ireland. Colorectal Disease, 12, e76–e81
Leakage after rectal resection: outcome
The design of the multivariate analyses was based on a
priori clinical consideration but, due to the limited
number of 30-day deaths and of local recurrences, the
models had to be adjusted for these two end-points. For
30-day mortality models 3, 4 and 5 were added to model
2 and tested in separate models for each variable. In the
analyses of local recurrence the analyses had to be
performed as shown in Table 5.
The analyses included tests for possible interactions
between AL and each of the other variables in the
models. In patients with AL, only age had a significant
influence on risk of death within 30 days and was
therefore included in the succeeding models. The
results are presented as odds ratios (OR) for 30-day
mortality and hazard ratios (HR) for recurrence and
long-term survival after AL with 95% confidence inter-
vals (CI). All tests were two-sided with a significance
level of 0.05.
Results
Thirty-day mortality
Anastomotic leakage occurred in 163 (10.9%) of the
1494 patients. The overall 30-day mortality was 3.9%,
eighteen (11%) of the 163 patients with AL died within
30 days of surgery and 27 (17%) before discharge. AL,
high age, male sex, peroperative bleeding and ASA score
> 2 increased the risk of postoperative death (Table 1).
In a multivariate analysis, AL increased the risk of
death during the first 30 days [OR 4.01, 2.24–7.17 (95%
CI)]. Gender did not change the effect of AL, whereas a
significant interaction between age and leakage was
observed in the analysis, thus the risk of dying after AL
decreased with increasing age (Table 2). The inclusion of
preoperative blood loss and ASA score showed no
significant change of dying within 30 days of AR due to
AL (Table 2). Inclusion of the remaining variables from
models 3 to 5 resulted in insignificant changes in the
influence of AL, and the results are not shown.
Long-term survival
Mean follow up was 3.77 (range 0.09–6.18) years. In the
univariate analysis patients who suffered from AL had a
poorer long-term survival rate compared with patients
without this complication (Fig. 1). Male sex, high age,
perioperative bleeding, surgery by a nonspecialist, ad-
vanced Dukes’ stage and ASA score > 2 also were
significantly associated with decreased long-term survival
(Table 1). Multivariate analysis (Table 3) showed AL to
be an independent risk factor of increased long-term
mortality.
e77
Leakage after rectal resection: outcome C. A. Bertelsen et al.

Table 1 Thirty-day mortality and long-term mortality in 1494 patients having curative anterior resection for rectal cancer in Denmark
(May 2001 to December 2004).

30-day mortality (n = 1494) Long-term mortality* (n = 1434)

Dead £ 30 Alive > 30 Dead > 30 Alive at P Log-rank

days after AR days after AR P (v2) days after AR follow up test
n = 58 n = 1436 Wilcoxon n = 357 n = 1077 Cox-
No. of patients (3.9%) (96.1%) ( ) (24.9%) (75.1%) regression ( )

Leakage 18 (31.0%) 145 (10.1%) < 0.0001 50 (14.0%) 95 (8.8%) 0.0013

Age (median, range), years 75 (50–89) 67 (30–93) < 0.0001  71 (42–93) 65 (30–91) < 0.0001  
Male 43 (74.1%) 819 (57.0%) 0.0079 225 (63.0%) 592 (55.0%) 0.0042
Peroperative blood loss 600 (100–4400) 400 (0–7190) 0.019  500 (0–7190) 400 (0–5000) 0.0001  
(median, range), ml
Preoperative radiotherapy 6 (10.7%) 247 (17.5%) 0.17 48 (13.7%) 199 (18.7%) 0.22
Coloanal pouch 6 (10.3%) 205 (14.3%) 0.38 47 (13.2%) 158 (14.7%) 0.67
Diverting stoma 31 (53.4%) 808 (56.3%) 0.67 209 (58.5%) 597 (55.4%) 0.32
Surgery by specialist 44 (75.9%) 1172 (81.6%) 0.29 267 (74.8%) 905 (84.0%) 0.0010
Dukes’ stage 0.83 < 0.0001
A 12 (21.1%) 336 (23.7%) 49 (13.9%) 287 (27.0%)
B 25 (43.9%) 538 (38.0%) 108 (30.7%) 428 (40.3%)
C 20 (35.1%) 543 (38.3%) 195 (55.4%) 348 (32.7%)
Tumour level (median 11 (3–15) 11 (1–15) 0.93  10 (3–15) 11 (1–15) 0.60  
and range), cm
ASA score < 0.0001 < 0.0001
ASA I-II 35 (64.8%) 1226 (88.5%) 286 (82.4%) 939 (90.6%)
ASA III-IV 19 (35.2%) 159 (11.5%) 61 (17.6%) 97 (9.4%)

*In patients alive 30 days after surgery.

 Peroperative blood loss, tumour level and age are measured continually.

Table 2 Multivariate analysis of 30-day mortality in 1494 patients after curative anterior resection for rectal cancer according to age.

Odds Ratio of 30-day mortality (95% CI) Age (y) Interaction

between
No. of leakage
patients 60 65 70 75 80 and age

Model 2 (leakage 1494 10.4 (3.76–28.7) 6.96 (3.19–15.2) 4.66 (2.47–8.82) 3.13 (1.63–5.98) 2.09 (0.93–4.70) P = 0.018
+ age and gender)
Model 2 + blood 1443 11.8 (4.09–34.3) 7.56 (3.35–17.1) 4.82 (2.50–9.31) 3.08 (1.59–5.97) 1.96 (0.86–4.48) P = 0.011
loss
Model 2 + blood 1439 12.5 (4.25–36.9) 8.09 (3.54–18.5) 5.23 (2.68–10.2) 3.38 (1.73–6.62) 2.19 (0.95–5.05) P = 0.015
loss + ASA score

Local recurrence Distant recurrence

Mean follow up was 3.42 (range 0.08–5.83) years. A
total of 97 (6.7%) patients developed local recurrence.
Advanced Dukes’ stage, peroperative bleeding, tumour
level above anal verge and the presence of a diverting
stoma were associated with an increase in the rate of local
recurrence in the univariate analysis (Table 4). There was
no significant association between AL and local recurrence
in the univariate or multivariate analyses (Tables 4 and 5).
Mean follow up was 3.31 (range 0.77–5.83) years. A total
of 258 (18.0%) patients developed distant recurrence.
There was an increased incidence of distant recurrence
with more advanced Dukes’ stage, age, peroperative
bleeding and the presence of a diverting stoma (Table 4)
in univariate analysis. There was no association between
AL and the risk of distant recurrence in the univariate or
multivariate analysis (Tables 4 and 6).

e78  2010 The Authors. Journal Compilation  2010 The Association of Coloproctology of Great Britain and Ireland. Colorectal Disease, 12, e76–e81
C. A. Bertelsen et al. Leakage after rectal resection: outcome

100% observation would have been expected, as elderly patients

90%
would be expected to be less capable of surviving a major
complication. We cannot offer an obvious explanation,
80% but the presence of selection bias is a possible reason.
70% Surgeons might prefer Hartmann’s resection to avoid
60% an anastomosis in the most fragile elderly patients while
Survival

undertaking sphincter preserving surgery in all younger

50%
patients. Fit elderly patients may have been more suitable
40% to survive leakage compared with unfit younger patients.
30% ASA score is supposed to reflect the risk of surgery, but in
the multivariate analysis we did not find any significant
20% Leakage association between ASA score and the risk of death due
10% No leakage to AL.
0% We have previously reported [10] that peroperative
0 1 2 3 4 5 6 bleeding is a risk factor of AL. In this study peroperative
Years
blood loss caused only insignificant changes in the risk of
Figure 1 Kaplan–Meier survival analysis after curative anterior dying due to AL even though blood loss was a significant risk
resection for rectal cancer, with or without anastomotic leakage factor for short-term mortality in the univariate analysis.
(AL). Log-rank-test P = 0.0013.
We observed that AL independently increased long-
term mortality, as reported in some previous studies
Table 3 Multivariate analysis of long-term mortality of 1434 [5,8,13,14], but in contrast to others [1,6,11,15–17].
patients alive 30 days after curative anterior resection for rectal McArdle et al. [13] and Walker et al. [14] reported
cancer. comparable excess long-term mortality after AL in
colorectal cancer patients with HR of 1.6.
Long-term
No. of mortality [Hazard In our study, the increased long-term mortality was
patients Ratio (95% CI)] not related to complications after closure of the defunc-
tioning stoma, because no deaths occurred after such
Model 1: Anastomotic leakage 1434 1.63 (1.21–2.19) procedures in the AL group (unpublished data).
Model 2: Model 1 + age and 1434 1.59 (1.18–2.15) The number of patients in the database with complete
gender data on preoperative weight loss, smoking, alcohol
Model 3: Model 2 + peroperative 1364 1.59 (1.17–2.18) consumption, diabetes and self-reported physical fitness
blood loss, preoperative was unfortunately limited and a valid multivariate analysis
radiotherapy, could not be performed. The role of smoking is of
coloanal pouch, diverting stoma interest; it increased the rate of leakage in our cohort
and specialization of the surgeon
[10], but it is disappointing that we are not presently able
Model 4: Model 3 + Dukes’ 1343 1.51 (1.11–2.07)
to analyse long-term survival in smokers following AL.
stage and tumour level above
anal verge (cm)
The effect of AL on the risk of local recurrence is
Model 5: Model 4 + ASA score 1300 1.54 (1.12–2.10) controversial. Some studies have shown an increased risk of
up to four times [1,4,5,11,15]. Ptok et al. [1] reported an
increased risk of recurrence in patients with leakage
requiring reoperation compared with AL patients managed
Discussion
without it. They suggested that more marked inflamma-
This study showed that anastomotic leakage (AL) after tion occurs if AL requires surgical revision and that more
curative anterior resection for rectal cancer increased the pronounced immunosuppression is caused by reoperation.
30-day mortality rate, with the highest mortality in In addition, transmission of viable exfoliated cancer cells
younger patients. AL was an independent predictor of during further surgery might be responsible for an
reduced long-term survival, but had no significant increased risk of local recurrence but there are no data on
influence on local or distant recurrence rates. this. However, in accordance with other authors [3,6,16–
Other studies have previously shown increased 30-day 19] we did not observe a significant increase in local
mortality after AL [1,3,11–13]. Surprisingly, we observed recurrence in AL patients. While the number of patients
that the risk of 30-day mortality decreased significantly included in our study exceeds what is reported in most of
with increasing age. This finding persisted when other the previously published studies [4,6,11,15,19], our rate
possible confounding factors were added. The reverse of local recurrence is generally lower [4,8,11,15,16].

 2010 The Authors. Journal Compilation  2010 The Association of Coloproctology of Great Britain and Ireland. Colorectal Disease, 12, e76–e81 e79
Leakage after rectal resection: outcome C. A. Bertelsen et al.

Table 4 Local recurrence and distant recurrence of 1434 patients alive 30 days after curative anterior resection for rectal cancer.

Local No local P Distant No distant P

recurrence recurrence Log-rank test recurrence recurrence Log-rank test
n = 97 (6.7%) n = 1337 Cox-regression (*) n = 258 (17.3%) n = 1234 Cox-regression (*)

Leakage 13 (13.4%) 132 (9.9%) 0.17 27 (10.5%) 118 (10.3%) 0.54

Age (median and 64 (37–84) 67 (30–93) 0.055* 64 (30–88) 67 (34–93) 0.028*
range), years
Male sex 55 (56.7%) 762 (56.9%) 0.89 150 (58.1%) 667 (56.7%) 0.44
Peroperative blood 605 (50–4600) 400 (0–7190) < 0.0001* 500 (0–4000) 400 (0–7190) 0.010*
loss (median and
range), ml
Preoperative radiotherapy 11 (11.6%) 236 (17.9%) 0.15 50 (19.6%) 197 (17.0%) 0.17
Coloanal pouch 11 (11.3%) 194 (14.5%) 0.37 40 (15.5%) 165 (14.0%) 0.61
Diverting stoma 70 (72.2%) 736 (55.0%) 0.0010 164 (63.6%) 642 (54.6%) 0.0066
Surgery by specialist 74 (76.3%) 1098 (82.1%) 0.13 206 (79.8%) 966 (82.1%) 0.42
Dukes’ stage < 0.0001 < 0.0001
Dukes A 4 (4.2%) 332 (25.2%) 21 (8.2%) 315 (27.2%)
Dukes B 29 (30.5%) 507 (38.4%) 67 (26.1%) 469 (40.5%)
Dukes C 62 (65.3%) 481 (36.4%) 169 (65.8%) 374 (32.3%)
Tumour level (median 10 (3–15) 11 (1–15) 0.0012* 10 (4––15) 11 (1–15) 0.062*
and range), cm
ASA score 0.94 0.77
ASA I-II 85 (89.5%) 1140 (88.5%) 226 (90.4%) 999 (88.2%)
ASA III-IV 10 (10.5%) 148 (11.5%) 24 (9.6%) 134 (11.8%)

*Peroperative blood loss, tumour level and age are measured continually.

Table 5 Multivariate analysis of local recurrence of 1434 Table 6 Multivariate analysis of distant recurrence of 1434
patients alive 30 days after curative anterior resection for rectal patients alive 30 days after curative anterior resection for rectal
cancer. cancer.

Local recurrence Distant

No. of Hazard Ratio recurrence
patients (95% CI) No. of Hazard Ratio
patients (95% CI)
Model 1: Anastomotic leakage 1434 1.50 (0.84–2.69)
Model 2: Model 1 + age and gender 1434 1.48 (0.82–2.66) Model 1: Anastomotic leakage 1434 1.13 (0.76–1.69)
Model 3: Model 2 + peroperative 1364 1.46 (0.79–2.68) Model 2: Model 1 + age and 1434 1.12 (0.75–1.66)
blood loss, preoperative gender
radiotherapy, coloanal pouch, Model 3: Model 2 + peroperative 1364 1.10 (0.73–1.66)
diverting stoma and specialization blood loss, preoperative
of the surgeon radiotherapy,
Model 4: Model 2 + Dukes’ stage 1391 1.29 (0.71–2.33) coloanal pouch, diverting stoma
and tumour level above anal verge and specialization of the surgeon
Model 5: Model 4 + ASA score 1344 1.31 (0.72–2.37) Model 4: Model 3 + Dukes’ stage 1343 1.06 (0.71–1.60)
and tumour level above anal verge
Model 5: Model 4 + ASA score 1300 1.05 (0.70–1.60)
In Denmark, the reporting of cancer and cancer
recurrence to the National Patients Register is highly
accurate and we are confident that we did not miss any length of follow up in this study compared with other
recurrence. Differences in the length of follow up studies [4,5] might therefore explain why we observed
between studies could explain the different recurrence fewer recurrences. Nevertheless, the mean follow up in
rates. The majority of patients were offered follow up on a this study was 3.42 years and the majority of recurrences
regularly basis for a period of a minimum of 5 years and it were likely to have already occurred.
is quite possible that some patients may have died outside Furthermore, we found no relationship between AL
the hospital with an undiagnosed recurrence. A shorter and distant recurrence. No previous study has addressed

e80  2010 The Authors. Journal Compilation  2010 The Association of Coloproctology of Great Britain and Ireland. Colorectal Disease, 12, e76–e81
C. A. Bertelsen et al.
this topic. Given the absence of any relationship between
AL and these cancer-specific outcomes, a late excess
mortality caused by recurrence probably did not contrib-
ute significantly to reduced long-term survival in patients
experiencing AL.
In conclusion, AL is an independent risk factor
influencing short- and long-term mortality. Recognized
risk factors of leakage should be taken into account when
deciding for or against an anastomosis after anterior
resection.
Acknowledgements
Jens Gustafsen, Rigshospitalet; Peer Wille-Jorgensen,
Bispebjerg Hospital; Steffen Bülow, Hvidovre Hospital;
Uhle Wied, Amager Hospital; Hans Henrik Raskov, Kbh.
Amts Sygehus i Gentofte; Poul Crone, Kbh. Amts Sygehus
i Glostrup; Claus Ronholt, Kbh. Amts Sygehus i Herlev.
Ole Hart Hansen and Per Jess, Hillerod Sygehus; Lene
Kirkeby, Roskilde Amts Sygehus, Roskilde; Esben Iversen,
Roskilde Amts Sygehus, Koge; Troels Haakansson, Syge-
hus Vestsjaelland; Ole Bjorn Andersen, Storstrommens
Sygehus; Jens Nymark, Centralsygehuset Nykobing Fal-
ster; Otto Lawaetz, Bornholms Centralsygehus; Hans
Rahr and Peter Madsen, Odense Universitetshospital; Per
V. Andersen, Sygehus Fyn Svendborg; Niels Buch, Syge-
hus Fyn Nyborg; Peter Teglaard, Sonderborg Sygehus;
Karl Erik Juul Jensen, Esbjerg Centralsygehus; Vagn Berg,
Grindsted Sygehus; Henrik Thomsen, Horsens Sygehus;
Michael Klaerke, Kolding Sygehus; Claus Bisgaard, Vejle
Sygehus; Henrik Sloth, Holstebro Sygehus; Mogens
Rorbaek Madsen, Herning Sygehus; Gunnar Madsen,
Silkeborg Centralsygehus; Henrik Christensen, Aarhus
Amtssygehus; Jesper Dan Nielsen, Randers Centralsyge-
hus; Mads Mark, Sygehus Viborg; Hans Henrik Lausten-
Thomsen, Sygehus NORD, Nykobing-Thisted; Per Gand-
rup, Aalborg Sygehus; Niels Lauesen, Hobro ⁄ Terndrup
Sygehus; Eskild Lundhus, Sygehus Vendsyssel; Niels
Malling, Aabenraa Sygehus.
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