J Gastrointest Surg (2012) 16:16591665

DOI 10.1007/s11605-012-1932-4

ORIGINAL ARTICLE

Risk Factors for Esophagojejunal Anastomotic Leakage

After Elective Gastrectomy for Gastric Cancer
Kazuhiro Migita & Tomoyoshi Takayama &
Sohei Matsumoto & Kohei Wakatsuki & Koji Enomoto &
Tetsuya Tanaka & Masahiro Ito & Yoshiyuki Nakajima

Received: 5 April 2012 / Accepted: 30 May 2012 / Published online: 12 June 2012
# 2012 The Society for Surgery of the Alimentary Tract

Abstract
Objective The aim of this study was to investigate the correlation between intraoperative anastomotic troubles and the
incidence of esophagojejunal anastomotic leakage (EJAL), and to identify risk factors for EJAL after elective gastrectomy for
gastric cancer.
Methods This study reviewed the medical and surgical records of 327 patients who underwent elective gastrectomy followed
by esophagojejunostomy. A multivariate analysis was performed to determine the risk factors for EJAL.
Results An EJAL occurred in 19 patients (5.8 %). A multivariate analysis demonstrated that hemoglobin A1c 7.0 % (p<0.01),
chronic renal failure (p<0.01), proximal gastrectomy (p<0.05), and anastomotic trouble during construction of the esophagojejunostomy (p<0.01) were independent predictors for EJAL. Anastomotic trouble during construction of esophagojejunostomy
occurred in 20 patients (6.1 %), and EJAL occurred in 6 of these 20 patients (30 %). Four of ten patients (40 %) in whom an
incomplete anastomosis was repaired by suturing during surgery had an EJAL, while none of seven patients who underwent reanastomosis had this complication.
Conclusions EJAL is strongly associated with intraoperative technical errors. To reduce this complication, proper anastomotic
techniques are required. Re-anastomosis should be performed when an incomplete anastomosis is discovered during surgery.
Keywords Esophagojejunal anastomotic leakage .
Gastrectomy . Short-term outcome

Introduction
Automatic suturing devices have been developed and are
increasingly used for anastomoses of the gastrointestinal tract.
Accordingly, a marked reduction in esophagojejunal anastomotic leakage (EJAL) has been achieved.13 However, EJAL
is still one of the most serious complications after gastrectomy,
thus leading to poorer quality of life, prolonged hospital stay,
and increased cost and mortality.2,47 Anastomotic leakage
also has a negative impact on long-term outcomes.6,8 Some
K. Migita (*) : T. Takayama : S. Matsumoto : K. Wakatsuki :
K. Enomoto : T. Tanaka : M. Ito : Y. Nakajima
Department of Surgery, Nara Medical University,
840 Shijo-Cho,
Kashihara, Nara 634-8522, Japan
e-mail: kmigita@naramed-u.ac.jp

authors have reported the rate of EJAL to be associated with

the anastomosis techniques.1,3 However, there is so far little
information on the risk factors for EJAL in patients undergoing stapled esophagojejunostomy.6,9,10 Reports about the
impact of intraoperative technical failures of esophagojejunostomy on the occurrence of EJAL are also scarce.1,9 Furthermore, proper intraoperative management of technical
failures remains unclear. This study, therefore, investigated
the characteristics of EJAL, the correlation between intraoperative anastomotic troubles and the incidence of EJAL, and
intraoperative treatments for anastomotic troubles. This investigation also attempted to identify the risk factors for EJAL in
this group.

Patients and Methods

A total of 334 patients with gastric cancer underwent elective
gastrectomy followed by esophagojejunostomy at Nara Medical University from January 2001 to December 2011. Seven

1660

patients who underwent an additional surgical procedure for

another disease at the time of gastrectomy were excluded;
these included esophageal carcinoma in three patients, and
hepatocellular carcinoma, renal cell carcinoma, intraductal
papillary neoplasm of the pancreas, and abdominal aortic
aneurysm. Therefore, 327 patients remained and were analyzed in this study.
Surgical Technique
Reconstruction was performed by Roux-en Y esophagojejunostomy after total gastrectomy in 317 patients and by
jejunal interposition after proximal gastrectomy in ten
patients. All esophagojejunal anastomoses were performed
with a circular stapler. A suitable sized stapler for the esophageal and jejunal lumen was selected by the surgeons
discretion. The stapled esophageal and jejunal doughnuts
were examined for completeness of anastomosis. No supplementary sutures were performed routinely to strengthen
the anastomosis. The esophagojejunal anastomosis was not
routinely tested for air leaks during surgery.
Definition of Esophagojejunal Anastomotic Leakage
The integrity of the esophagojejunal anastomosis was routinely
examined with water-soluble contrast medium after a median
of six postoperative days (range, 420 days). An EJAL was
diagnosed with extravasation of contrast material during radiologic examination and/or with discharge of saliva or gastrointestinal content through a drain or during re-laparotomy.
Clinical leakage was defined as the presence of either clinical
symptoms or signs suggesting potential leakage such as abdominal pain, fever, leukocytosis, and abnormal drain discharge. Our definition of an EJAL was the clinical leakage.
Two cases of asymptomatic leakage that were only radiographically diagnosed were not included in the EJAL group.
Data
The patient clinicopathological characteristics and surgical
variables were obtained retrospectively from the medical
records and evaluated as risk factors for the incidence of
EJAL. The anastomotic trouble during construction of
esophagojejunostomy and intraoperative treatments for the
trouble were also obtained from the surgical records.
The patient clinicopathological characteristics included
age, sex, body mass index (BMI), American Society of
Anesthesiologists (ASA) score (<3 versus 3), presence of
cardiovascular disease, hemoglobin A1c (HbA1c; <7.0 versus 7.0 %), presence of chronic renal failure, corticosteroid
therapy in the past 30 days for a chronic condition, serum
albumin (3.5 versus <3.5 g/dl), hemoglobin (10 versus
<10 g/dl), preoperative chemotherapy, and pathological

J Gastrointest Surg (2012) 16:16591665

stage of gastric cancer. No patients had undergone any

preoperative radiotherapy. Chronic renal failure was defined
as a chronic kidney disease stage 4 or an end-stage renal
failure requiring dialysis.11
The surgical variables included the presence of macroscopic esophageal invasion, the type of procedure (total
versus proximal gastrectomy) and approach (open versus
laparoscopic), duration of the operation, blood loss, perioperative allogenic blood transfusion, extent of lymph node
dissection (D0, D1 versus D2 or more), combined organ
resection, surgeons experience (<10 versus 1014 versus
15 years), and the anastomotic trouble during construction
of the esophagojejunostomy. Total gastrectomy included
total gastrectomy and total resection of the gastric remnant.
The stage of gastric cancer was classified according to the
seventh edition of the American Joint Committee on Cancer
TNM classification system.12 The extent of lymph node
dissection was based on the Japanese Gastric Cancer Treatment Guidelines 2010 (version 3).13
The outcome parameters were also evaluated in this
study, including the length of postoperative hospital stay
and inhospital mortality. The requirement for performing a
second procedure, including percutaneous drainage or reoperation, was also assessed. The severity of surgical complications was defined according to the ClavienDindo
classification.14
Statistical Analysis
All patients were divided into two groups according to
whether or not they had postoperative EJAL. The categorical variables were presented as numbers and percentages,
and the groups were compared using the chi-square test or
Fishers exact test. Continuous variables were expressed as
the median with range, and groups were compared using the
MannWhitney U test. Moreover, some continuous variables were converted to dichotomous variables for convenience, including the duration of operation (<300 versus
300 min) and blood loss (<500 versus 500 g). All variables with a p value <0.2 in the univariate analysis were
entered into a multivariate analysis. The multivariate analysis used a logistic regression model to investigate the factors
associated with the incidence of EJAL. A p value <0.05 was
considered to be statistically significant.

Results
Incidence and Characteristics of Esophagojejunal
Anastomotic Leakage
An EJAL occurred in 19 of 327 patients, and the rate was
5.8 %. The leakage was diagnosed at a median of 7 days

J Gastrointest Surg (2012) 16:16591665

1661

after gastrectomy (range, 316 days). Twelve patients

(63.2 %) presented with elevated white blood cell counts
or C-reactive protein, 12 (63.2 %) with discharge of gastrointestinal content or turbid effluent from the abdominal
drain, 10 (52.6 %) with fever, and 4 (21.1 %) with abdominal pain.
Risk Factors for Esophagojejunal Anastomotic Leakage
Table 1 shows the clinicopathological characteristics of the
patients and the incidence of EJAL. The patients with
HbA1c 7.0 % had a higher rate of EJAL than those without
it (23.1 versus 5.1 %, p<0.05). There were no significant
differences between the groups in terms of age, sex, BMI,
ASA score, cardiovascular disease, chronic renal failure,
corticosteroid therapy, serum albumin, hemoglobin,

Table 1 Clinicopathological
characteristics of the patients
with esophagojejunal anastomotic leakage

BMI body mass index, ASA

American Society of Anesthesiologists, CTx chemotherapy
a

Values are expressed as the median with range

Variables
Age (years)a
Sex
Male
Female
BMI
<25
25
ASA score
<3
3
Cardiovascular disease
Absent
Present
Hemoglobin A1c (%)
<7.0
7.0
Chronic renal failure
Absent
Present
Corticosteroid therapy
Absent
Present
Serum albumin (g/dl)
3.5
<3.5
Hemoglobin (g/dl)
10
<10
Preoperative CTx
Not performed
Performed
Pathological stage
I, II
III, IV

preoperative chemotherapy, and pathological stage of gastric cancer.

The surgical variables and the incidence of EJAL are
compared in Table 2. The rate of EJAL was significantly
higher in patients with macroscopic esophageal invasion
than in those without it (15.8 versus 4.5 %, p<0.05). The
patients with EJAL had a significantly longer median duration of operation than those without it (330 versus 290 min,
p<0.05). The patients with EJAL also had greater blood loss
than those without it (820 versus 425 g, p<0.05). There
were no significant differences between the groups in terms
of the type of procedure and approach, allogenic blood
transfusion, extent of lymph node dissection, combined
organ resection, and surgeons experience. Anastomotic
troubles during construction of the esophagojejunostomy
occurred in 20 patients (6.1 %), and postoperative EJAL

Total (N)

Leakage (), %

Leakage (+), %

p value

69 (3389)

64 (5288)

0.2629

241
86

227 (94.2)
81 (94.2)

14 (5.8)
5 (5.8)

>0.9999

276
51

262 (94.9)
46 (90.2)

14 (5.1)
5 (9.8)

302
25

284 (94)
24 (96)

18 (6)
1 (4)

>0.9999

187
140

178 (95.2)
130 (92.9)

9 (4.8)
10 (7.1)

0.5137

314
13

298 (94.9)
10 (76.9)

16 (5.1)
3 (23.1)

0.0329

320
7

303 (94.7)
5 (71.4)

17 (5.3)
2 (28.6)

0.0565

322
5

303 (94.1)
5 (100)

19 (5.9)
0 (0)

>0.9999

294
33

278 (94.6)
30 (90.9)

16 (5.4)
3 (9.1)

0.4225

295
32

280 (94.9)
28 (87.5)

15 (5.1)
4 (12.5)

0.1021

298
29

283 (95)
25 (86.2)

15 (5)
4 (13.8)

0.0757

192
135

183 (95.3)
125 (92.6)

9 (4.7)
10 (7.4)

0.4261

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Table 2 Surgical variables and
esophagojejunal anastomotic
leakage

J Gastrointest Surg (2012) 16:16591665

Variables
Macroscopic esophageal invasion
Absent
Present
Procedure
Total gastrectomya
Proximal gastrectomy
Approach
Open
Laparoscopic
Duration of operation (min)b
<300
300
Blood loss (g)b
<500
500
Transfusion
Not performed
Performed
Lymph node dissection
D0, D1
D2 or more
Combined organ resection
Not performed
Performed
Surgeons experience (years)

Including total gastrectomy and

total resection of gastric remnant

Values are expressed as the median with range

<10
1014
15
Anastomotic trouble
Absent
Present

occurred in 6 (30 %) of these 20 patients. This rate was

significantly higher than that of 4.2 % in patients without
anastomotic troubles (p<0.0001).
Table 3 shows the results of the multivariate analysis for
the risk factors of EJAL. HbA1c 7.0 % (p<0.01), chronic
renal failure (p<0.01), proximal gastrectomy (p<0.05), and
anastomotic troubles (p<0.01) were identified as independent factors for predicting the incidence of EJAL.
Inhospital Mortality and Postoperative Hospital Stay
Thirteen of the 19 EJAL were treated conservatively, and 3
were successfully managed with image-guided percutaneous
drainage. Three EJAL required drainage by laparotomy due to
uncontrolled peritonitis or mediastinitis. Two of these three
patients who underwent reoperation required only drainage.
The anastomosis was reinforced with drainage in the remaining patient. A second procedure was performed more frequently in patients with EJAL than in those without it (31.6

Total (N)

Leakage (), %

Leakage (+), %

p value

289
38

276 (95.5)
32 (84.2)

13 (4.5)
6 (15.8)

0.0151

317
10

300 (94.6)
8 (80)

17 (5.4)
2 (20)

0.1089

281
46

16 (5.7)
3 (6.5)
330 (205520)
5 (2.9)
14 (9.1)
820 (802,397)
6 (3.4)
13 (8.8)

0.7384

179
148

265 (94.3)
43 (93.5)
290 (145631)
168 (97.1)
140 (90.9)
425 (152,907)
173 (96.6)
135 (91.2)

207
120

198 (95.7)
110 (91.7)

9 (4.3)
10 (8.3)

0.2148

183
144

176 (96.2)
132 (91.7)

7 (3.8)
12 (8.3)

0.1355

158
169

152 (96.2)
156 (92.3)

6 (3.8)
13 (7.7)

0.2046

19
136
172

18 (94.7)
127 (93.4)
163 (94.8)

1 (5.3)
9 (6.6)
9 (5.2)

0.8705

307
20

294 (95.8)
14 (70)

13 (4.2)
6 (30)

<0.0001

173
154

0.0416
0.0311
0.0286
0.0639

versus 6.2 %, p<0.01). The reoperation rate in patients with

EJAL was also significantly higher in comparison to those
without it (15.8 versus 2.3 %, p<0.05). The ClavienDindo
classification showed that the severity of complications was
grade II in 13 patients, IIIa in 1, IIIb in 3, and V in 2.
Overall, 1.8 % of patients (6 of 327 patients) died during
their hospitalization. These included 3 of 21 patients who
developed an EJAL. The causes of death were multiple
organ failure secondary to sepsis, cerebral bleeding, and
progression of gastric cancer in the three patients with
EJAL. Two of the three patients without EJAL died of
progression of gastric cancer, and one patient died of peritonitis due to a pancreatic fistula. Inhospital mortality rate
was significantly higher in patients with EJAL than in those
without it (15.8 versus 1.0 %, p<0.01).
The median length of postoperative hospital stay of patients
with EJAL and without it was 60 days (range, 20148 days)
and 24 days (range, 999 days), respectively. This difference
was statistically significant (p<0.0001).

J Gastrointest Surg (2012) 16:16591665

Table 3 Multivariate analysis of
the risk factors for esophagojejunal anastomotic leakage

Variables
Hemoglobin A1c (%)
7.0
Chronic renal failure
Present
Hemoglobin (g/dl)
<10
Preoperative CTx
Performed
Macroscopic esophageal invasion
Present
Procedure
Proximal gastrectomy
Duration of operation (min)
300

CI confidence interval, CTx

chemotherapy

Blood loss (g)

500
Lymph node dissection
D2 or more
Anastomotic trouble
Present

Anastomotic Troubles
The anastomotic troubles during construction of the esophagojejunostomy included partial dehiscence of the anastomosis in seven patients, positive air leak test without
macroscopic dehiscence of the anastomosis in six, jejunal
tear, an incomplete esophageal and/or jejunal doughnut
without macroscopic dehiscence of the anastomosis, and
injury of the esophageal mucosa at the time of insertion of
anvil head in two each, and difficulty in fixing the anvil
head in one. Treatment for the anastomotic trouble and the
occurrence of postoperative EJAL are shown in Table 4.
Although four of ten patients (40 %) in whom an incomplete
anastomosis was repaired by additional suturing had a postoperative EJAL, none of the seven patients who underwent
re-anastomosis had this complication (p00.1029).

Discussion
The present study clearly demonstrated that EJAL was strongly associated with intraoperative technical errors of esophagojejunostomy, and that the intraoperative proper treatment for
an incomplete anastomosis could avoid postoperative EJAL.
EJAL occurred in 5.8 % of the patients in the present study.
T h e r a t e s o f E J A L v a r y, r a n g i n g f r o m 1 . 0 t o
11.5 %.1,3,4,6,7,9,10,15,16 The leakage rate reported from Japanese high-volume centers is 1.0 and 2.1 %.3,10 Most EJAL is

1663

Odds ratio (95 % CI)

p value

10.885 (2.05257.739)

0.005

16.115 (2.238116.049)

0.0058

2.3 (0.5559.532)

0.2507

2.624 (0.59811.517)

0.2012

3.088 (0.86511.022)

0.0823

12.98 (1.507111.766)

0.0196

1.614 (0.4525.77)

0.461

1.627 (0.4465.933)

0.4609

2.216 (0.6018.167)

0.2318

8.061 (2.23929.018)

0.0014

likely to result from intraoperative technical failures. It is also

important that technical failures that are not detected during
surgery lead to postoperative EJAL.1 Taken together, the rate
of EJAL might decrease to nearly zero by the prevention and
the proper intraoperative management of an incomplete anastomosis, and detail observations of the anastomosis site.
The impact of the anastomotic trouble on the occurrence
of EJAL indicates that prevention is crucial to reduce this
complication. Some authors have highlighted that the rate of
EJAL is associated with an experience of the surgeon.13
However, the experience of the surgeon was not a significant variable relating to the incidence of the anastomotic
trouble in the current series, nor the development of EJAL.
Anastomotic troubles occurred in 7.6 % of cases (13 out of
172 cases) performed by surgeons with 15 years of experience, in 4.4 % of cases (6 out of 136 cases) performed by
surgeons with 1014 years of experience, and in 5.3 % of
cases (1 out of 19 cases) performed by surgeons with less
than 10 years of experience. These differences were not
statistically significant (p00.513). This is probably because
at least one expert surgeon participated in all gastrectomy as
a surgeon or an assistant surgeon, and suggests that skills of
surgical teams, rather than individual surgeons, are important when considering surgical quality. On the other hand,
we found that blood loss was significantly greater in gastrectomy in which the anastomotic trouble occurred than in
gastrectomy without it (783 versus 423 g, p<0.05). Furthermore, gastrectomy with anastomotic trouble tended to have

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J Gastrointest Surg (2012) 16:16591665

Table 4 Treatments and occurrence of esophagojejunal anastomotic leakage in patients with anastomosis troubles during construction of
esophagojejunostomy
Patient No.

Troubles

Treatment

Postoperative leakage

1
2
3
4
5
6
7
8
9
10
11
12
13

Positive air leak testa

Partial dehiscence of anastomosis
Partial dehiscence of anastomosis
Incomplete doughnutb
Positive air leak testa
Positive air leak testa
Positive air leak testa
Positive air leak testa
Partial dehiscence of anastomosis
Incomplete doughnutb
Esophageal mucosal tear during insertion of anvil head
Difficulty in fixing anvil head
Esophageal mucosal tear during insertion of anvil head

Suturing
Suturing
Suturing
Suturing
Suturing
Suturing
Suturing
Suturing
Suturing
Suturing
Reinsertion of anvil head
Reinsertion of anvil head
Reinsertion of anvil head

Yes
Yes
Yes
Yes
No
No
No
No
No
No
Yes
Yes
No

14
15
16
17
18
19
20

Positive air leak testa

Partial dehiscence of anastomosis
Partial dehiscence of anastomosis
Partial dehiscence of anastomosis
Partial dehiscence of anastomosis
Jejunal tear
Jejunal tear

Re-anastomosis
Re-anastomosis
Re-anastomosis
Re-anastomosis
Re-anastomosis
Re-anastomosis
Re-anastomosis

No
No
No
No
No
No
No

Defined as positive air leak test without macroscopic dehiscence of anastomosis

Defined as an incomplete esophageal and/or jejunal doughnut without macroscopic dehiscence of anastomosis

a longer median duration of operation in comparison to that

without it (351 versus 290 min, p00.0682). These results
indicate that more complicated gastrectomy is associated
with the incidence of the anastomotic trouble. Surgical
teams should maintain their concentration during construction of the esophagojejunostomy, even in complicated gastrectomy cases, to avoid anastomotic troubles.
The method selected to repair an incomplete anastomosis
during surgery is also considered to be important. Incomplete anastomoses that are discovered during surgery force
the surgeon to decide whether to perform suturing or reanastomosis to treat it, particularly when the site of an
incomplete anastomosis is obvious. The re-anastomosis is
generally complicated in comparison to the repair by suturing. Ten patients with an incomplete anastomosis underwent
repair by suturing in the current series, while seven patients
underwent re-anastomosis. As a result, four of ten patients
(40 %) who underwent repair by suturing experienced postoperative EJAL, while none of the patients who underwent
re-anastomosis had this complication. Among the four
patients who had postoperative EJAL after undergoing repair procedures by suturing, the site of the incomplete
anastomosis was identified during surgery in three patients.
These results suggest that repair by suturing may be insufficient to treat an incomplete anastomosis. Re-anastomosis

without hesitation is recommended when an incomplete

anastomosis is discovered. When re-anastomosis cannot be
performed, then the surgeon is prepared to encounter some
degree of the occurrence of postoperative EJAL. Moreover,
an incomplete anastomosis that is not discovered during
surgery can also lead to postoperative anastomotic leakage.1
Detailed observations of the anastomosis site and doughnuts
are therefore needed to discover an incomplete anastomosis
during surgery.
On the other hand, three of the patients had anastomotic
troubles during the insertion of anvil head. Although reinsertion of the anvil head was performed in all patients, two
patients (66.7 %) experienced postoperative EJAL. This is
probably due to a weakness or minimal tear of the distal
esophagus, which was overlooked during surgery. Therefore, detailed observations of distal esophagus and the anastomotic site were also required in patients who had difficulty
in inserting the anvil head.
The complete prevention of EJAL has not been achieved,
thus patient-related factors may be associated with the incidence of EJAL. Diabetes mellitus is known to impair wound
healing, including not only incisional wounds,17 but also
intestinal anastomosis.18 However, the impact of diabetes
mellitus on the incidence of anastomotic leakage still
remains controversial. Some authors have reported that

J Gastrointest Surg (2012) 16:16591665

diabetes mellitus is independently associated with the incidence of anastomotic leakage in colorectal anastomosis.19,20
On the other hand, this correlation has not been demonstrated in esophagojejunal anastomosis.4,6,10 Preoperative poor
diabetic control (HbA1c 7.0 %) was an independent risk
factor for EJAL in the current study. Four of 46 diabetic
patients (8.7 %) with HbA1c of <7.0 % had an EJAL. This
rate was not significantly higher in comparison to the rate of
4.5 % in patients without diabetes mellitus (p00.2675).
These results suggest that the preoperative glucose control
level is a more important predictor for anastomotic leakage
than the prevalence of diabetes mellitus. The preoperative
improvement in diabetes control is necessary in patients
undergoing gastrectomy to reduce EJAL.
Apart from preoperative diabetes control levels, another
factor that was significantly associated with the development of EJAL was the prevalence of chronic renal failure.
This is the first study that has demonstrated that chronic
renal failure is an independent predictor for EJAL. Renal
insufficiency is associated with an increased postoperative
morbidity, including anastomotic leakage, in various types
of gastrointestinal surgery.2123 This increased risk is related
not only to advanced atherosclerosis, metabolic disorders,
and uremia-related coagulopathy, but also to the comorbid
other medical disease.21,23 Indeed, all seven patients with
chronic renal failure in the present study had other medical
disorders. Six patients (85.7 %) had cardiovascular disease,
and four (57.1 %) had diabetes mellitus. Meticulous anastomosis techniques and careful postoperative management
are needed in patients with chronic renal failure.
In conclusion, this study demonstrated the occurrence of
EJAL to be strongly associated with intraoperative technical
errors. Proper anastomotic techniques and detailed observation of the anastomosis are therefore required to reduce this
complication. Re-anastomosis should be performed when an
incomplete anastomosis is discovered during surgery.

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