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: [email protected]
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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