Efficacy of intracorporeal reinforcing sutures for anastomotic leakage after laparoscopic surgery for rectal cancer

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Surgical EndoscopyAnd Other Interventional TechniquesOfficial Journal of the Society ofAmerican Gastrointestinal andEndoscopic Surgeons (SAGES) andEuropean Association for EndoscopicSurgery (EAES) ISSN 0930-2794 Surg EndoscDOI 10.1007/s00464-015-4104-2

Efficacy of intracorporeal reinforcingsutures for anastomotic leakage afterlaparoscopic surgery for rectal cancer

Kiyoshi Maeda, Hisashi Nagahara,Masatsune Shibutani, Hiroshi Ohtani,Katsunobu Sakurai, Takahiro Toyokawa,Kazuya Muguruma, et al.

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Efficacy of intracorporeal reinforcing sutures for anastomoticleakage after laparoscopic surgery for rectal cancer

Kiyoshi Maeda • Hisashi Nagahara • Masatsune Shibutani • Hiroshi Ohtani •

Katsunobu Sakurai • Takahiro Toyokawa • Kazuya Muguruma • Hiroaki Tanaka •

Ryosuke Amano • Kenjiro Kimura • Kenji Sugano • Teturo Ikeya •

Yasuhito Iseki • Kosei Hirakawa

Received: 28 October 2014 / Accepted: 27 January 2015

� Springer Science+Business Media New York 2015

Abstract

Background The aim of the present study was to inves-

tigate the efficacy of intracorporeal reinforcing sutures for

preventing anastomotic leakage (AL) after laparoscopic

surgery for rectal cancer.

Methods This was a retrospective single-institution study

consisting of 201 consecutive patients who underwent la-

paroscopic proctectomy with double-stapling anastomosis

for primary rectal cancer between August 2007 and

December 2013. The data for patients who received in-

tracorporeal reinforcing sutures were compared with those

of patients who did not receive reinforcing sutures. Patient-

, tumor- and surgery-related variables were collected and

examined using univariate and multivariate analyses.

Results The overall incidence of AL was 9.0 % (18/201).

No significant correlations were observed between the

various clinicopathological factors and the use of rein-

forcing sutures. The multivariate analyses revealed the

distance of the tumor from the anal verge, tumor size and

presence of reinforcing sutures to be independent risk

factors for AL. We classified the patients into two risk

groups using a combination of the tumor site and tumor

size: a low-risk group (patients without any risk factors,

n = 134) and a high-risk group (patients with one or two

risk factors, n = 67). The frequency of AL was sig-

nificantly lower (p \ 0.02) in the patients treated with

reinforcing sutures than in those treated without reinforcing

sutures in the high-risk group. However, no significant

differences were observed in the low-risk group.

Conclusions The use of intracorporeal reinforcing sutures

may reduce the incidence of AL. A prospective randomized

trial is required to evaluate the effects of reinforcing su-

tures in preventing AL.

Keywords Laparoscopic surgery � Rectal cancer �Anastomotic leakage � Reinforcing suture

Several recent randomized trials have demonstrated that la-

paroscopic colectomy is similar to conventional open sur-

gery in terms of oncologic safety and is associated with

improved short-term perioperative outcomes [1–3]. La-

paroscopic rectal surgery is technically more difficult than

laparoscopic colectomy, due to difficulties related to rectal

excision and anastomosis within the narrow pelvic space.

However, an increasing number of recent studies have shown

that laparoscopic rectal surgery is safe and feasible [4–6].

Anastomotic leakage (AL) is a major problem in pa-

tients undergoing rectal cancer surgery. This complication

often requires reoperation, thus resulting in a prolonged

hospital stay as well as high morbidity and mortality. The

incidence of AL has been reported to range from 3.6 to

21 % [7–15]. Leakage can be the result of a combination of

technical, local and systemic factors, and several risk fac-

tors, including old age, a male sex, smoking habit, diabetes

mellitus, obesity, intraoperative blood loss, a longer dura-

tion of surgery, the use of more than three cartridges for

rectal transection, larger tumor size, lower tumor location

and bulky tumors, have been reported [8–15]. The double-

stapled anastomotic technique is widely used in colorectal

surgery because it allows the anastomosis to be made

very low in the pelvis and preserves the anal sphincter.

K. Maeda (&) � H. Nagahara � M. Shibutani � H. Ohtani �K. Sakurai � T. Toyokawa � K. Muguruma � H. Tanaka �R. Amano � K. Kimura � K. Sugano � T. Ikeya � Y. Iseki �K. Hirakawa

Department of Surgical Oncology, Graduate School of Medicine,

Osaka City University, 1-4-3 Asahimachi, Abeno-ku, Osaka,

Japan

e-mail: [email protected]

123

Surg Endosc

DOI 10.1007/s00464-015-4104-2

and Other Interventional Techniques

Author's personal copy

However, this technique creates stapled corners known as

‘‘dog ears,’’ which are made by crossing at least two staple

lines, potentially forming vulnerable areas. The staple line

may also become weakened via friction created by hard

stools, thus increasing the risk of anastomotic failure. In

order to address this problem, various methods have been

suggested, including the placement of intracorporeal rein-

forcing sutures at the staple line. We hypothesized that

placing the sutures to support the circular-stapled anasto-

mosis may reduce AL.

Patients and methods

Patients

We retrospectively collected and reviewed patient charac-

teristics and perioperative data after obtaining approval

from our institutional review board. Between August 2007

and December 2013, a total of 201 consecutive patients

who underwent laparoscopic proctectomy with double-

stapling anastomosis for primary rectal cancer at the

Department of Surgical Oncology, Osaka City University

Hospital, were evaluated. The location of each tumor was

within 15 cm from the anal verge. The eligibility criteria

included rectal cancer with histologically proven adeno-

carcinoma. The exclusion criteria were as follows: ab-

dominoperineal resection, Hartman’s procedure, creation

of a diverting stoma at the time of surgery, emergency

surgery, intersphincteric resection and trans-anal hand-

sewn anastomosis, total abdominal colectomy and

ileorectal anastomosis, and a history of preoperative che-

motherapy or radiation therapy. We divided the eligible

201 patients into two groups: comprising those who re-

ceived reinforcing sutures (n = 91) and those who did not

(n = 110).

Surgical procedure

All procedures were performed or supervised by two senior

surgeons (K.M. and H.N.) specialized in laparoscopic

colorectal surgery. We have routinely utilized intracorpo-

real reinforcing sutures since April 2011. Therefore, most

of the patients with reinforcing sutures underwent surgery

between 2012 and 2013. A schematic view of the rein-

forcing suture technique is shown in Fig. 1. Following

rectal division using an endo-linear stapler, end-to-end

anastomosis was performed using a circular stapler and

reinforcing sutures using 4-0 PDS (Ethicon Inc, New Jer-

sey, USA) were placed intracorporeally. Two to four in-

terrupted sutures were placed along the staple line, and the

two corners made by crossing the circular and linear staple

lines were always included. The distance from the anal

verge was determined on colonoscopy. Air leakage tests

were performed in all patients following anastomosis and

placement of the reinforcing sutures. A temporary diverting

stoma was considered in patients with several risk factors,

such as a positive air leakage test, incomplete circular

stapling donut or doubtful blood supply.

According to our hospital protocol, the patients under-

went mechanical preparation, regardless of whether the

procedure was emergent or elective. A second-generation

cephalosporin was used as a prophylactic antibiotic

(20 mg/kg). The antibiotic was administered 30 min before

surgery and thereafter every 3 h during the procedure.

Definition of anastomotic leakage

Clinical AL was defined as the presence of signs of leakage

(ex, discharge of gas, pus or feces through the pelvic drain,

peritonitis or pus discharge through the rectum) and con-

firmed on diagnostic imaging modalities, such as computed

tomography or retrograde colonography using water-sol-

uble contrast medium. Asymptomatic AL was not assessed

because routine contrast enemas were not performed after

Fig. 1 Intracorporeal view of the anastomosis and reinforcing

sutures. A Reinforcing sutures were placed at the crossing point of

the staple lines. Black arrow anastomosis White Arrow staple line.

B Two to four interrupted sutures were placed along the staple line.

Black arrows reinforcing sutures

Surg Endosc

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surgery. All patients diagnosed with AL in this study were

identified within 14 days.

Variables

The following 21 parameters were evaluated as potential

risk factors for AL: age at the time of surgery (C75 or

\75 years), gender, body mass index (BMI C25 or

\25 kg/m2), ASA score, past history of previous laparo-

tomy, presence of myocardial infarction, chronic obstruc-

tive pulmonary disease (COPD), diabetes mellitus, tumor

site (]5 or\5 cm from the anal verge), tumor size (C4 or

\4 cm in diameter), depth of tumor invasion, regional

lymph node metastasis, operative time (C240 or

\240 min), amount of intraoperative blood loss (C600 or

\600 ml), number of stapler firings, ligation of the left

colic artery, preoperative serum C-reactive protein (CRP)

level (C1.0 or \1.0 g/ml), preoperative serum albumin

level (C3.5 or\3.5 g/ml) and the placement of reinforcing

sutures at the staple line.

All blood samples were collected either 1 or 2 weeks be-

fore surgery. The cutoff levels for the operative time and

amount of intraoperative blood loss, tumor site (distance from

the anal verge) and tumor size (tumor maximal diameter) were

determined as median values. A BMI of C25 kg/m2 is con-

sidered to reflect obesity in Japanese patients [16]; therefore,

the cutoff value for the BMI was set at 25 kg/m2.

Statistical analysis

The statistical analyses were performed using the JMP 10

software program (SAS Institute Japan, Tokyo, Japan).

Univariate analyses were performed using the Chi-square

test, Fisher’s exact test and the Mann–Whitney U test. All

variables with a p value of\0.05 in the univariate analyses

were included in a multivariate logistic regression analysis.

A p value of \0.05 was considered to be statistically

significant.

Results

Patient characteristics

The clinical characteristics of the 201 patients are sum-

marized in Table 1. The mean age at surgery was 67 years

(range 31–90). The majority of patients were classified as

having an ASA of 1 or 2 (94.5 %). A preoperative BMI of

more than 25 was observed in 46 (22.9 %) patients. With

respect to comorbidities, ischemic heart disease was

Table 1 Patient characteristics

Number

of patients

Age (years)

Median (range) 67 (31–90)

Gender

Male 118

Female 83

BMI

Median (range) 22.8 (14.3–32.8)

ASA score

1, 2 190

3 11

Previous laparotomy

Absent 163

Present 38

Myocardial infarction

Absent 182

Present 19

Chronic obstructive pulmonary disease

Absent 194

Present 7

Diabetes mellitus

Absent 159

Present 42

Tumor site (from anal verge, cm)

Median (range) 5.1 (3.0–13.5)

Tumor size (diameter, cm)

Median (range) 39.5 (4.0–90.0)

Depth of tumor invasion

T1, 2 76

T3, 4 125

Lymph node metastases

Absent 132

Present 69

Intra-operative blood loss (ml)

Median (range) 60.6 (5–960)

Number of stapler firing

C3 6

\3 195

Ligation of left colic artery

No 83

Yes 118

Operation time (min)

Median (range) 238 (131–425)

Preoperative serum CRP level (g/dl)

C1 13

\1 188

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observed in 19 (9.5 %) patients, diabetes mellitus was

observed in 42 (20.9 %) patients and chronic obstructive

pulmonary disease was observed in seven (3.5 %) patients.

Forty-five patients (22.1 %) presented with rectal cancer

within 5 cm from the anal verge.

The correlations between the various clinicopathological

factors and the presence of reinforcing sutures are shown in

Table 2. There were no significant differences between the

two groups.

The overall incidence of AL was 9.0 % (18/201).

Among these patients, re-laparotomy was required in five

cases; all five patients received a protective stoma and then

quickly recovered. The remaining 13 patients recovered

with conservative treatment. The median time to hospital

discharge was 37 days (range 21–67), and there were no

deaths related to AL.

We classified the patients into two groups based on the

period in which the surgery was performed. One hundred

and eleven patients who underwent surgery between 2007

and 2011 were classified into the early period group, and

the other 90 patients who underwent surgery between 2012

and 2013 were classified into the late period group

(Table 3). The median operative time for reinforcing su-

tures and the frequency of AL were compared among these

groups. As a result, the operative time for reinforcing su-

tures tended to be shorter in the late period group than in

the early period group; however, there were no significant

differences between the two groups. Otherwise, although

the frequency of AL was lower in the late period group

than in the early period group, there were no significant

differences between the two groups.

The results of univariate analyses of the risk factors

potentially associated with AL are shown in Table 4. Ten

factors (BMI of C25, diabetes mellitus, tumor site from the

anal verge of C5 cm, tumor diameter of C4 cm, operative

time of C4 h, operative blood loss of C60 ml, number of

stapler firings C3, depth of tumor invasion CT3 and use of

reinforcing sutures) were found to be significantly corre-

lated with AL. Regarding the correlation between the in-

cidence of AL and the presence of reinforcing sutures, the

rate of AL was 3.3 % (3/91) in the patients treated with

reinforcing sutures, which was significantly (p \ 0.01)

lower than that observed in the patients without reinforcing

sutures (13.6 %, 15/110). Meanwhile, the multivariate

Table 1 continued

Number

of patients

Preoperative serum albumin level (g/dl)

C3.5 189

\3.5 12

BMI body mass index

Table 2 Correlations between various clinicopathological factors

and the use of reinforcing sutures

Variables Reinforcing sutures p value

Yes No

(n = 91) (n = 110)

Age (years)

C75 24 24 0.45

\75 67 86

Gender

Male 52 66 0.68

Female 39 44

BMI

C25 17 29 0.2

\25 74 81

ASA score

1, 2 87 103 0.76

3 4 7

Previous laparotomy

Absent 74 89 0.94

Present 17 21

Myocardial infarction

Absent 83 99 0.77

Present 8 11

COPD

Absent 89 105 0.60

Present 2 5

Diabetes mellitus

Absent 76 83 0.16

Present 15 27

Tumor site (from anal verge, cm)

C5 66 90 0.12

\5 25 20

Tumor size (cm)

C4 20 23 0.85

\4 71 87

Depth of tumor invasion

T1, 2 38 38 0.29

T3, 4 53 72

Lymph node metastases

Absent 61 71 0.71

Present 30 39

Intra-operative blood loss (ml)

C60 16 25 0.37

\60 75 85

Number of stapler firing

C3 1 5 0.31

\3 90 105

Ligation of left colic artery

No 43 40 0.12

Yes 48 70

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analyses revealed a tumor site from the anal verge of

B5 cm, tumor size of C4 cm and the absence of reinforc-

ing sutures to be independent risk factors for AL (Table 5).

We classified the patients into two risk groups using a

combination of tumor-related risk factors (tumor site from

the anal verge of B5 cm and tumor size of C4 cm). The

patients were classified into the low-risk group (patients

without any risk factor, n = 134) and high-risk group

(patients with one or two risk factors, n = 67). Moreover,

the frequency of AL was compared between the patients

treated with and without reinforcing sutures (Table 6). The

frequency of AL was significantly lower (p \ 0.02) in the

patients treated with reinforcing sutures than in the patients

treated without reinforcing sutures in the high-risk group.

However, there were no differences in the low-risk group.

Discussion

Anastomotic leakage is a major problem in rectal cancer

surgery, and it is associated with both postoperative mor-

bidity and mortality. Even now, the effects of leakage on

the oncologic outcomes are not clear, although some re-

ports have suggested that AL results in increased rates of

local recurrence and a poor survival [16–18]. Several risk

factors for AL in patients with laparoscopic rectal surgery

have been identified in previous reports [8–15]. In the

current study, we found the tumor size, tumor site from the

anal verge and use of reinforcing sutures to be independent

risk factors for symptomatic AL.

Various methods have been applied to reduce the inci-

dence of AL in patients with these risk factors. Park et al.

[14] and Tan et al. [19] reported that diverting stomas are

mandatory in patients with two or more risk factors.

Meanwhile, Ito et al. [20] reported that vertical rectal

transection via an additional suprapubic site could be used

to avoid multiple stapler firings, resulting in a decreased

rate of AL, and Xiao et al. [21], Zhao et al. [22] and

Nishigori et al. [23] reported that trans-anal decompression

tubes are useful for preventing AL. Recently, Gadiot et al.

[24] examined patients who undergoing left-sided colec-

tomy, sigmoidectomy and anterior resection and reported

that the placement of sutures at the site of anastomosis to

reduce traction resulted in a reduction of AL. All of these

reports examined patients treated with double-stapling

anastomosis. Double-stapling anastomosis is a widely used

and useful technique; however, it creates weak points,

made by crossing staple lines. In the present study, we

examined the efficacy of placing intracorporeal reinforcing

sutures at the crossing staple line for reducing the rate of

AL. As a result, although there were no significant differ-

ences in the low-risk group, the frequency of AL was

significantly lower in the patients treated with reinforcing

sutures than in those treated without reinforcing sutures in

the high-risk group. Therefore, reinforcing sutures are

thought to be useful for reducing AL in the high-risk pa-

tients, although they may be unnecessary in the low-risk

patients. In the case of open surgery, it is difficult to apply

reinforcing sutures, especially in patients treated with very

low anterior resection, due to the limited visual field re-

sulting from the narrow pelvic field. Otherwise, laparo-

scopic surgery has the advantage of providing better

magnified visualization with endoscopy; therefore, it is

easier to place reinforcing sutures under laparoscopic ver-

sus open surgery. Even under laparoscopic visualization,

placing reinforcing sutures is technically difficult in some

cases, especially in high-risk patients. Although the use of

a diverting stoma requires at least once additional surgery,

which can impact the patient’s quality of life, several

studies [14, 19] reported that the frequency of AL is sig-

nificantly lower in patients with a diverting stoma. There-

fore, a diverting stoma should be created in patients whom

reinforcing sutures cannot be accomplished.

The present study has several limitations. First, this

study was not randomized, and there may have been se-

lection bias in the decision to place reinforcing sutures. A

prospective randomized trial is, therefore, needed to eval-

uate the effects of reinforcing sutures on AL. Second, most

of the patients with reinforcing sutures belonged to the late

Table 2 continued

Variables Reinforcing sutures p value

Yes No

(n = 91) (n = 110)

Operation time (min)

C240 39 49 0.81

\240 52 61

Preoperative CRP level (g/dl)

C1 6 7 0.82

\1 85 103

Preoperative serum albumin level (g/dl)

C3.5 85 104 0.97

\3.5 6 6

BMI body mass index

Table 3 Median operative time for reinforcing sutures and frequency

of anastomotic leakage subdivided by the treatment period

Years n Median

operative time

for reinforcing

sutures (second;

range)

p value Number

of patients

with AL

(%)

p value

2007–2011 111 403 (258–622) 0.13 13 (11.7) 0.20

2012–2013 90 384 (214–710) 5 (5.6)

Surg Endosc

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period group. The laparoscopic surgical skills may have

been better in the late period than in the early period.

Although the learning curve for laparoscopic surgery may

have slightly affected to the reduction in the frequency of

AL in the late period group, the rate of AL was not sig-

nificantly different between the early period group and the

late period group.

In conclusion, our findings demonstrate that the use of

intracorporeal reinforcing sutures may reduce the incidence

Table 4 Univariate analyses according to the correlations between

various clinicopathological factors and the presence of anastomotic

leakage

Variables Anastomotic leakage p value

Present Absent

(n = 18) (n = 183)

Age (years)

C75 15 78 0.22

\75 3 105

Gender

Male 15 138 0.45

Female 3 45

BMI

C25 10 145 0.02

\25 8 38

ASA score

1, 2 16 174 0.27

3 2 9

Previous laparotomy

Absent 19 149 0.80

Present 5 34

Myocardial infarction

Absent 15 167 0.27

Present 3 16

COPD

Absent 18 178 0.40

Present 0 5

Diabetes mellitus

Absent 10 149 0.01

Present 8 34

Tumor site (from anal verge; cm)

C5 8 148 0.004

\5 10 35

Tumor size (cm)

C4 12 71 0.02

\4 6 112

Depth of tumor invasion

T1, 2 0 75 0.006

T3, 4 18 108

Lymph node metastases

Absent 10 121 0.35

Present 8 61

Intra-operative blood loss (ml)

C60 8 33 0.0008

\60 10 150

Number of stapler firing

C3 3 3 0.0004

\3 15 180

Ligation of left colic artery

No 4 76 0.23

Yes 14 107

Table 4 continued

Variables Anastomotic leakage p value

Present Absent

(n = 18) (n = 183)

Operation time (min)

C240 16 72 \0.0001

\240 2 111

Reinforcing suture of the staple line

No 15 95 0.01

Yes 3 88

Preoperative serum CRP level (g/dl)

C1 0 13 0.24

\1 18 110

Preoperative serum albumin level (g/dl)

C3.5 16 173 0.33

\3.5 2 10

BMI body mass index

Table 5 Multivariate analyses according to the correlations between

various clinicopathological factors and the presence of anastomotic

leakage

Variables Multivariate analysis p value

Odds ratio 95 % CI

BMI

C25 versus \25 1.80 0.58–5.63 0.31

Diabetes mellitus

Present versus absent 2.07 0.65–6.52 0.21

Tumor site (from anal verge, cm)

\5 versus C5 7.13 2.61–17.4 0.01

Tumor size (cm)

C4 versus \4 4.89 1.36–8.87 0.02

Depth of tumor invasion

T3, 4 versus T1, 2 2.69 0.73–9.86 0.12

Operation time (min)

C240 versus \240 2.24 0.61–8.28 0.22

Number of stapler firing

C3 versus \3 1.16 0.15–7.73 0.88

Reinforcing suture of the staple line

No versus yes 4.65 1.36–13.2 0.02

BMI body mass index

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of AL. However, a prospective randomized trial is still

needed to evaluate the effects of reinforcing sutures for

preventing AL.

Disclosures Drs Kiyoshi Maeda, Hisashi Nagahara, Masatsune

Shibutani, Hiroshi Otani, Kenji Sugano, Ikeya Tetsuro, Yoshihito

Iseki, Katsunobu Sakurai, Takahiro Toyokawa, Kazuya Muguruma,

Hiroaki Tanaka, Ryosuke Amano, Kenjiro Kimura and Kosei Hi-

rakawa have no conflicts of interest or financial ties to disclose.

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Table 6 Correlations between

the frequency of anastomotic

leakage and use of reinforcing

sutures subdivided according to

the risk group

AL anastomotic leakage

Reinforcing suture AL Frequency of AL (%) p value

Present Absent

High risk

Yes 2 32 5.9

No 10 23 30.3 0.02

Low risk

Yes 2 55 3.5

No 4 73 5.2 0.88

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23. Nishigori H, Ito M, NIshizawa Y, Kobayashi A, Sugito M, Saito

N (2014) Effectiveness of a transanal tube for the prevention of

anastomotic leakage after rectal cancers surgery. World J Surg

38:1843–1851

24. Gadiot RPM, Dunker MS, Mearadji A, Hannaerts GHH (2011)

Reduction of anastomotic failure in laparoscopic antitraction

sutures. Surg Endosc 25:68–71

Surg Endosc

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