ORIGINAL ARTICLE

Pancreatic thickness as a predictive factor for postoperativepancreatic fistula after distal pancreatectomy using an endopathstapler

Keiichi Okano • Minoru Oshima • Keitaro Kakinoki • Naoki Yamamoto •

Shintaro Akamoto • Shinichi Yachida • Masanobu Hagiike • Hideki Kamada •

Tsutomu Masaki • Yasuyuki Suzuki

Received: 29 July 2011 / Accepted: 15 December 2011 / Published online: 11 July 2012

� Springer 2012

Abstract

Purpose No consistent risk factor has yet been estab-

lished for the development of pancreatic fistula (PF) after

distal pancreatectomy (DP) with a stapler.

Methods A total of 31 consecutive patients underwent DP

with an endopath stapler between June 2006 and December

2010 using a slow parenchymal flattening technique. The

risk factors for PF after DP with an endopath stapler were

identified based on univariate and multivariate analyses.

Results Clinical PF developed in 7 of 31 (22 %) patients

who underwent DP with a stapler. The pancreata were

significantly thicker at the transection line in patients with

PF (19.4 ± 1.47 mm) in comparison to patients without PF

(12.6 ± 0.79 mm; p = 0.0003). A 16-mm cut-off for

pancreatic thickness was established based on the receiver

operating characteristic (ROC) curve; the area under the

ROC curve was 0.875 (p = 0.0215). Pancreatic thickness

(p = 0.0006) and blood transfusion (p = 0.028) were

associated with postoperative PF in a univariate analysis.

Pancreatic thickness was the only significant independent

factor (odds ratio 9.99; p = 0.036) according to a multi-

variate analysis with a specificity of 72 %, and a sensitivity

of 85 %.

Conclusion Pancreatic thickness is a significant inde-

pendent risk factor for PF development after DP with an

endopath stapler. The stapler technique is thus considered

to be an appropriate modality in patients with a pancreatic

thicknesses of \16 mm.

Keywords Distal pancreatectomy � Stapler �Pancreatic thickness � Pancreatic fistula

Introduction

Distal pancreatectomy (DP) is performed for various

indications including benign and malignant neoplasms of

the pancreas, chronic pancreatitis, and pancreatic paren-

chymal damage after abdominal trauma [1]. The rate of

perioperative complications ranges from 29 to 57 % after

DP [1–7]. The most common postoperative complication

following DP is pancreatic fistula (PF) [1, 2]. The surgical

technique is thought to be an important risk factor for the

development of PF. Various surgical techniques to reduce

the occurrence of fistulas after parenchymal transection and

closure of the pancreatic remnant have been described.

These techniques include stapled closures [1, 3, 8–10],

sutured closures [5, 11, 12], ultrasonic dissection [13],

bipolar scissors dissection [14], sealing with fibrin glue

[15, 16], seromuscular flaps [17, 18], pancreaticoenteric

anastomosis [19, 20], and ligation of the main pancreatic

duct at the transection line [17, 21–23]. The soft coagula-

tion technique on the cut surface of the pancreas followed

by the application of polyglycolic acid felt and fibrin glue

has been reported as new strategy for reducing PF after DP

[24].

A meta-analysis found no significant difference between

suture and staple closure of the pancreatic remnant with

respect to PF or intra-abdominal abscess after DP; how-

ever, staple closure is suggested to be superior to suture

K. Okano (&) � M. Oshima � K. Kakinoki � N. Yamamoto �S. Akamoto � S. Yachida � M. Hagiike � Y. Suzuki

Department of Gastroenterological Surgery,

Faculty of Medicine, Kagawa University, 1750-1 Ikenobe,

Miki-cho, Kita-gun, Kagawa 761-0793, Japan

e-mail: kokano@kms.ac.jp

H. Kamada � T. Masaki

Department of Gastroenterology and Neurology,

Faculty of Medicine, Kagawa University, Kagawa, Japan

123

Surg Today (2013) 43:141–147

DOI 10.1007/s00595-012-0235-4

closure [25, 26]. It is therefore tempting to speculate that

the perfection of a given technique at individual institutions

is just as important as the decision of which technique to

apply. A multicenter randomized trial was designed to

assess the effect of stapler versus hand-sewn closure on the

formation of PF after DP in Europe [27]. The PF rate did

not differ between a stapler (32 %) and hand-sewn closure

(28 %). This trial strongly suggested that new strategies,

including innovative surgical techniques, need to be

developed to reduce the occurrence of PF after DP.

A simple and safe technical management technique has

been established, using a stapler for DP with a slow

parenchymal flattening technique [9, 28]. Although the

incidence of PF has declined over the past decade with the

stapler technique, approximately 20 % of patients still

develop clinical PF after DP. While there are reports that

obesity [29], patient age [7, 30], longer operation time [20],

malignancy [3], malnutrtion [31], and the texture of the

pancreatic parenchyma [5, 11] are suggested to be potential

risk factors for pancreatic resection while using several

techniques, the specific risk factors for PF after DP with a

stapler are still not well defined.

The purpose of this study was to determine the risk

factors for the formation of PF after DP with a stapler using

a slow parenchymal flattening technique.

Patients and methods

A total of 31 patients underwent DP with an endopath

stapler with a slow parenchymal flattening technique

between June 2006 and December 2010 at Kagawa Uni-

versity Hospital. The patients’ characteristics are summa-

rized in Table 1.

The technical considerations of the slow parenchymal

flattening technique for DP have been described previously

[9, 28]. The pancreas is gently compressed with an atrau-

matic intestinal clamp at the transection line for a few

minutes prior to the stapling dissection. The pancreas is

transected with an Echelon 60 stapling device (Ethicon

Endo-surgery; Johnson & Johnson, Cincinnati, OH, USA)

with a gold cartridge (compressible thickness to 1.8 mm).

The closure jaw of the Echelon 60 is closed slowly and

carefully over an interval of more than 5 min at a fixed

speed. The stapler is not released immediately after firing

and the jaws of the stapler are held shut for about 2 min, to

ensure hemostasis of the pancreatic stump. Ligation of the

main pancreatic duct is not necessary, and minor bleeding

from the stump can be easily controlled by compression or

coagulation by electrocautery. A 10-mm soft silicon drain

is placed near the stump of the remnant pancreas.

The amylase levels in the serum and drainage fluid were

measured on postoperative days 1 and 3. PF was defined

using the International Study Group on Pancreatic Fistula

(ISGPF) definition as follows [32]: drainage of any mea-

surable volume after postoperative day 3 with an amylase

content greater than 3 times the normal serum value.

Patients were categorized as having developed a clinically

significant PF on the basis of the ISPGF definitions of

grades B and C fistulas. The drain was removed on post-

operative day 4 if no clinical PFs on bacterial contamina-

tion developed [32].

The clinicopathological risk factors for PF after DP with

an endopath stapler were identified using univariate and

multivariate models. The patient data including demo-

graphics, comorbidities, additional procedures, body mass

index (BMI), preoperative albumin, operative time, blood

loss, pathology, and postoperative complications were

Table 1 Background of 31 patients underwent DP using endopath

stapler

Variables Values

Number of patients 31

Age

Mean 65.5 ± 2.3

Range 24–82

Gender

Female 13

Male 18

BMI (kg/m2) 21.5 ± 0.48

Preoperative albumin (mg/dl) 3.66 ± 0.11

Indication for DP

Ductal adenocarcinoma 13

Endocrine neoplasia 5

Cystic neoplasm 4

Gastric adenocaricinoma 2

Metastatic renal cell carcinoma 2

Acinar cell carcinoma 2

Retension cyst 1

Intrapancreatic accessory spleen 1

Splenectomy 1

Operative time (min) 300.8 ± 15.5

Blood loss (ml) 683.9 ± 126.2

Site of transection

Thickness of pancreas (mm)*

Head 16 (12.9 ± 1.2)

Body 7 (15.3 ± 1.7)

Tail 8 (16.1 ± 1.6)

Clinical pancreatic fistula (ISGPF) 7

Grade B 6

Grade C 1

BMI body mass index, DP distal pancreatectomy, ISGPF Interna-

tional study group on pancreatic fistula

* There is no siginificant difference in the thickness of pancreas at site

of transection

142 Surg Today (2013) 43:141–147

123

collected from the electronic hospital records and chart

reviews. Pancreatic thickness at the resection line was

estimated by preoperative and postoperative CT as a can-

didate factor. Pancreatic texture at the transection line was

estimated to be soft or hard by the attending surgeons (K.O.

and Y.S.).

CT studies were performed with an Aquilion (Toshiba,

Tokyo, Japan) scanner. Contrast enhancement dynamic

multidetector CT (MDCT) scans were obtained both pre-

and postoperatively for each patient. The preoperative and

the postoperative MDCT were usually performed

1–2 weeks before operation and 1 week after operation.

The thickness of the pancreas at the cutting line was

measured on axial images of preoperative multi-planar

reformation MDCT (Fig. 1a, c). The cutting line was

estimated based on postoperative MDCT images (Fig. 1b,

d). The pancreatic parenchymal phase of dynamic MDCT

was used to measure the pancreatic thickness to discrimi-

nate the pancreatic parenchyma from these surrounding

tissues.

Statistical analysis

The parametric data are expressed as the mean ± SEM and

compared using Student’s t test. All other comparisons

between groups were performed using the Chi-squared test.

Variables including age, body mass index (BMI), preop-

erative albumin, operative time and thickness of pancreas

were dichotomized according to the results of the receiver

operating characteristic (ROC) curve for univariate analy-

sis. The sensitivities and specificities for different cut-off

points were calculated within the group of patients with PF

and without PF for the ROC analysis. Those variables with

p values B0.07 in the univariate analysis were entered into

multivariate analyses in a backward stepwise manner until

all variables remaining in the model were significant. The

odds ratios are presented with their respective 95 % con-

fidence intervals. Pancreatic thickness was considered a

continuous value in the logistic regression analysis, and an

arbitrary cut-off based on the ROC curve was inserted.

Statistical significance was set at p \ 0.05. All computa-

tions were performed using the JMP software� package

(SAS International Inc., Cary, NC, USA).

Results

Eighteen of the 31 patients enrolled in the study were male

and 13 female (mean age 65.5 ± 2.3 years). The indica-

tions for surgical resection and other parameters of

Fig. 1 Representative preoperative and postoperative MDCT images

to measure the thickness of the pancreas. A 68-year-old male received

distal pancreatectomy for ductal adenocarcinoma of the pancreas

body. The pancreatic transection was performed using a stapler along

right border of SMV. The pancreatic thickness of the cutting line

measured by preoperative MDCT (a) in reference to the postoperative

MDCT (b) was 8.5 mm. A 73-year-old male received distal

pancreatectomy for endocrine neoplasm of the pancreas tail. The

pancreatic thickness of the cutting line measured by preoperative

MDCT (c) in reference to the postoperative MDCT (D) was 26.5 mm.

The dotted line indicates pancreatic thickness of the transection line

Surg Today (2013) 43:141–147 143

123

background are described in Table 1. No significant dif-

ference was observed in the thickness of the pancreas at the

site of transection (i.e., head, body, or tail of the pancreas).

Clinical PF developed in 7 of 31 (22 %) patients after DP

with a stapler. There were no mortalities, although 1 patient

developed a severe PF (ISGPF grade C) with an infection

and required re-operation for necrosectomy.

A comparative analysis of patients with and without PF

revealed that the pancreata were significantly thicker in

patients with PF (19.4 ± 1.47 mm) than in those without

PF (12.6 ± 0.79 mm; p = 0.0003). A 16-mm cut-off for

pancreatic thickness was established for the univariate and

multivariate analyses. The area under the ROC curve was

0.875 (p = 0.0215; Fig. 2). The cut-off value of pancreatic

thickness exhibited a specificity of 72 %, sensitivity of

85 %, positive predictive value of 66 %, and negative

predictive value of 95 % for clinical PF development.

Pancreatic thickness (p = 0.0006) and blood transfusion

(p = 0.028) were associated with postoperative PF in the

univariate analysis (Table 2). Pancreatic thickness, blood

transfusion, and age C70 years (p = 0.062) were examined

as risk factors in the multivariate analysis. Pancreatic

thickness (C16 mm) was the only significant independent

factor (odds ratio 9.99; p = 0.036) according to a multi-

variate analysis (Table 3).

An individual analysis of each of the cases involving

complications revealed the cut-off value (C16 mm) of

pancreatic thickness to be sufficient for 6 of the 7 patients

(85 %) who developed clinical PF. In addition, only 1 case

of clinical PF (4.7 %) was detected among the 21 patients

with pancreatic thicknesses of \16 mm at the resection

line. One patient with an ISGPF grade C fistula underwent

Fig. 2 Receiver operating characteristic (ROC) curve based on

pancreatic thickness for clinical pancreatic fistula after distal pancre-

atectomy using a stapler; area under the curve = 0.875

Table 2 Univariate analysis of preoperative risk factors for clinical

PF after DP using endopath stapler

Clinical PF (%) p value

Sex

Female 3/13 (23) 0.955

Male 4/18 (22)

Age (years)

C70 6/17 (35) 0.062

\70 1/14 (7.1)

Diabetes

Yes 1/4 (25) 0.901

No 6/27 (22)

BMI (kg/m2)

C22 3/13 (23) 0.955

\22 4/18 (22)

Preoperative albumin (mg/dl)

C3.7 3/18 (16) 0.354

\3.7 4/13 (30)

Texture

Soft 6/28 (21) 0.639

Hard 1/3 (33)

Lymph node clearance

Yes 3/13 (23) 0.955

No 4/18 (22)

Malignancy

Yes 3/18 (16) 0.354

No 4/13 (30)

Multi visceral resection

Yes 2/12 (16) 0.531

No 5/19 (26)

Preserving spleen

Yes 2/5 (40) 0.309

No 5/26 (19)

Operative time (min)

[300 4/15 (26) 0.598

\300 3/16 (18)

Blood loss (ml)

C1000 3/6 (50) 0.07

\1000 4/25 (16)

Blood transfusion

Yes 3/5 (60) 0.028

No 4/26 (15)

Thickness of pancreas (mm)

C16 6/10 (60) 0.0006

\16 1/21 (4.7)

Site of transection

Head 4/16 (25) 0.837

Body 1/7 (14)

Tail 2/8 (25)

BMI body mass index, DP distal pancreatectomy

144 Surg Today (2013) 43:141–147

123

reoperation. The patient had a hard and thick pancreas, and

subsequently experienced pancreatic tissue crushing during

transection with the stapler. The patient recovered after

necrosectomy, including drainage of the infectious necrotic

tissue associated with PF.

Discussion

The optimal surgical technique for both pancreatic tran-

section and closure of the pancreatic remnant is still under

debate. Several surgical techniques and instruments have

been proposed for reducing the occurrence of PF. The most

frequently used techniques are suture and staple closures of

the pancreatic remnant. A recent meta-analysis concluded

that there are no significant differences between suture and

staple closure with respect to PF or intra-abdominal

abscesses after distal pancreatectomy, although there is a

trend favouring staple closure [25, 26]. A lot of conflicting

data can still be found in the literature, including results

from high-volume centers. These findings suggest the

importance of nominal differences in surgical technique or

devices in both suture and staple closures.

The ISGPF criteria define grade A PF as subclinical,

whereas grades B and C are clinical [32]. It is very

important for surgeons to identify risk factors for clinical

PF and reduce them preoperatively, which is the same

procedure followed when developing safe surgical tech-

niques and instruments. Some authors report a number of

risk factors for increased rates of PF after DP other than the

surgical closure technique, including soft pancreatic tex-

ture, long operation time, obesity, malnutrition, age, and

extended lymphadenectomy. However, a multivariate

analysis performed in the present study does not indicate

that any of these factors increases the risk of clinical PF.

This suggests that some specific critical risk factor-asso-

ciated staple closure may thus be overlooked.

Stapler transection of the pancreas has been found to be

a simple and quick method for closing the proximal

pancreas. However, the incidence of PF after distal pan-

createctomy with a stapler device ranges from 3 to 26 %

[5, 8–10, 20, 28, 33, 34]. This large variation might reflect

differences in the technical management of stapling or the

stapler device. The most important and technically difficult

step of stapler dissection is to prevent pancreatic tissue

tears during compression. The importance of the com-

pression speed of the closure jaw during pancreatic tran-

section with the stapler has been previously described. A

slow parenchymal stapler technique for DP is applied. The

pancreas is gently and slowly compressed with an Echelon

60 stapler, which provides precise and uniform wide

compression throughout the length of the closure jaw, for

5 min to prevent tearing the pancreatic tissue. The 31

patients in this series that underwent standardized manip-

ulation with the same stapler experienced a clinical PF rate

of 22 %, which is unsatisfactory according to the ISPGF

classification, in spite of the fact that there was no

mortality.

The primary aim of the current study was to determine

the influence of operative factors on the incidence of PF

after DP with a stapler. The study focused on the pancreatic

thickness at the resection line. Eguchi et al. [30] report a

similar incidence of PF in 48 patients who received hand-

sewn or staple closure after undergoing DP. They identified

younger age and the thickness of the pancreatic remnant as

independent risk factors for PF using a logistic regression

analysis for all patients. Half of the 22 patients in the

stapler group with a thick pancreas developed PF, while no

patients with a thin pancreas developed PF. The results of

the present study strongly suggest that a thick pancreas is a

critical risk factor for PF after DP with a stapler. A staple

closure seems to be suitable for patients with a pancreatic

thicknesses of \16 mm. Other strategies, such as sero-

muscular flaps [17, 18], pancreaticoenteric anastomosis

[20], or ligation of the main pancreatic duct at the tran-

section line [21–23], are candidates for safe distal pan-

createctomy in patients with a thick pancreas. Covering the

stapled pancreatic remnants with a seromuscular patch may

be a simple method that can decrease the rate of compli-

cations including PF after DP [17].

The texture of the pancreatic parenchyma is reported to

be an important risk factor associated with the development

of postoperative PF in DP [5, 11] and pancreatoduode-

nectomy. Fibrotic pancreatic tissue is believed to be less

likely to leak than soft pancreatic parenchymal tissue as

long as the continuity of the main pancreatic duct is not

compromised. Pancreatic parenchymal texture was not

identified as a risk factor in the current series. One patient

with an ISGPF grade C PF required reoperation in the

present study. Interestingly, the patient had a hard and thick

pancreas, and subsequently experienced pancreatic tissue

crushing during transection with the stapler. Although the

objective evaluation of the pancreatic texture was not

consistent, a hard pancreas may therefore be another risk

factor, which requires special caution to prevent tissue

crushing during stapling for DP.

Table 3 Multivariate logistic regression analysis of preoperative risk

factors for clinical PF after DP using endopath stapler

Varable Odds

ratio

95 % confidence

interval

p value

Thickness of pancreas C16 mm 9.99 1.14–224.55 0.036

Blood transfusion 5.28 0.53–130.03 0.161

Age C70 years 3.96 0.37–50.99 0.248

DP Distal pancreatectomy

Surg Today (2013) 43:141–147 145

123

The thickness of the pancreatic parenchyma appears to

be related to the formation of clinical PF after DP with a

stapler. This series suggests that a 16-mm cut-off for

pancreatic thickness has a clinical impact on minimizing

the formation of PF. Staple closure seems to be suitable for

patients with a pancreatic thicknesses of \16 mm. Con-

versely, the establishment of safe strategies for closure of a

thick pancreas is expected in the future. Additional pro-

spective randomized studies stratified by pancreatic thick-

ness are therefore needed to determine the optimal surgical

technique for parenchymal transection and remnant closure

during DP to minimize the occurrence of postoperative PF.

Conflict of interest The authors declare no conflicts of interest.

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