Surgical Science, 2011, 2, 45-51
doi:10.4236/ss.2011.22010 Published Online April 2011 (
Copyright © 2011 SciRes. SS
The Best Choice to Achieve Zer o Complications after
Shinji Osada, Hisashi Imai, Yoshiyuki Sasaki, Itaru Yasufuku, Ryuichi Asai,
Yoshihisa Tokumaru, Takuji Sakuratani, Kazuhiro Yoshida
Surgical Oncology, Gifu University School of Medicine, Gifu, Japan
September 30, 2010; revised January 21, 2011; accepted January 26, 2011
Pancreatoduodenectomy (PD) has been performed commonly, but the occurrence of pancreatic fistula (PF) is
a critical trigger of complications, which are potentially life threatening, and is also associated with markedly
prolonged hospitalization. Many techniques have been proposed for connecting the pancreatic stump with
the gastrointestinal tract, stomach vs. jejunum, etc. Among the risk factors for PF, such as general patient
factors or disease-related factors, the most important is the texture of the remnant pancreas. Surgical tech-
nique might be one improvable aspect that can reduce the pancreatic leakage rate, therefore; various methods
of managing the pancreatic remnant have been studied. Methods of reconstruction between the remnant pan-
creas and the intestine include end-to-side with/without duct-to-mucosa anastomosis or end-to-end invagina-
tion styles, has been argued. Here, we review several trials for safety and methods of treating the pancreatic
stump after PD, and demonstrate our experiences.
Keywords: Pancreatoduodenectomy, Reconstruction, Pancreatojejunostomy, Pancreatic Fistula,
Pancreatoenteric Anastomosis
1. Introduction
The indications for pancreatoduodenectomy (PD) have
expanded to encompass a broad spectrum of periampul-
lary tumors including both malignant and benign lesions,
chronic pancreatitis, and, occasionally, trauma. The oc-
currence of pancreatic fistula (PF) is a critical trigger of
complications such as intra-abdominal abscess and hem-
orrhage, which are potentially life threatening, and is
also associated with markedly prolonged hospitalization.
Many techniques have been proposed for connecting the
pancreatic stump with the gastrointestinal tract but de-
spite some success, problems remain, especially with a
soft pancreas gland with a small duct [1]. Most of the
large PD series have reported rates of PF of over 10%
[1-4]. Risk factors for PF depend upon 1) general patient
factors, including age, sex, jaundice and nutrition; 2)
disease-related factors, including pancreatic duct size,
pancreatic texture, and pathology; and 3) procedure-re-
lated factors, including blood loss, operative time, and
anastomotic method [5]. Among these risk factors, the
most important might be the texture of the remnant pan-
creas. Indeed, the occurrence of PF rises to nearly 20%
in cases of soft pancreatic texture, despite an occurrence
rate of 5% in cases of hard pancreatic tissue [2-4]. Be-
cause surgical technique might be one improvable aspect
that can reduce the pancreatic leakage rate, various me-
thods of managing the pancreatic remnant have been
studied. Methods of reconstruction between the remnant
pancreas and the intestine include end-to-side with/
without duct-to-mucosa anastomosis or end-to-end in-
vagination styles, and arguably, anastomosis of the rem-
nant pancreas with the stomach is also another method.
Here, we review several trials for safety and certain
methods of treating the pancreatic stump after PD.
2. Anastomosis Methods with Pancreas
2.1. Pancreatojejunostomy
PD consists of mainly two types of reconstruction pro-
cedures for the remnant alimentary tract: Billroth I (Im-
anaga method) with gastrojejunostomy, pancreatojeju-
nostomy, and choledochojejunostomy; and Billroth II
(Whipple and/or Child method) with pancreatojeju-
nostomy or choledochojejunostomy and gastrojeju-
Copyright © 2011 SciRes. SS
nostomy. Billroth I reconstruction has been most com-
monly performed because it is conceivable that the pas-
sage of food through the entire remnant upper small in-
testine is more physiologically normal, and the mixture
of food with bile is similar to that in normal subjects. In
fact, hepatobiliary and gastrointestinal dual scintigraphy
has demonstrated satisfactory mixing of bile and food [6].
Billroth I reconstruction also enables endoscopic study of
the patency of the pancreatic and bile ducts in conjunc-
tion with evaluation of exocrine function [7]. However,
another study demonstrated no benefit to nutritional
status and quality of life after Billroth I [8]. Furthermore,
in consideration of early postoperative complications,
more frequent anastomotic failure of the pancreatojeju-
nostomy using the Billroth I method has been reported
than with other procedures [9]. Although the cause of
this failure remains unclear, the angularity of the jejunal
loop might be related to these problems [10] and, as de-
scribed previously, we suspect the mixture of bile and
pancreatic juice-induced enzyme activation to be associ-
ated with damage to the tissue [11]. Delayed gastric
emptying (DGE), which is critical for the determination
of nutritional status, has also been a concern following
Billroth I reconstruction. The cause of DGE has been
indicated to relate not only to anastomotic leakage [12]
but also to disruption of the gastroduodenal neural con-
nection by PD or to residual pancreatic fibrosis [13].
However, a disadvantage of Billroth II reconstruction is
that bile leakage tends to occur more frequently [14]. In
fact, biliogastric reflux after the type II operation is
problematic in the late postoperative period [15]. As a
consequence, abnormal motility of the afferent jejunum
due to dietary moderation indu ces bile statu s, resulting in
a high prevalence of bile leakage.
Continuous duct-to-mucosa anastomosis was de-
scribed as being safer and as having a significantly lower
leakage rate [16,17]. However, a prospective randomized
clinical trial found it to be favored in low-risk patients
with a dilated pancreas duct or firm fibrotic pancreas,
whereas the invagination technique was better for high-
risk patients with small ducts or a soft friable pancreas
[18]. In addition, in an analysis of the occurrence of PF
in pancreatojejunostomy, 40% originated from the pa-
renchyma or a small side branch duct and appeared to be
as common as duct-to-mucosa anastomosis [19]. In par-
ticular, for a soft pancreas, no pancreatic duct dilatation
is usually detected; thus, duct-to-mucosa anastomosis
might be difficult.
2.2. Pancreatogastrostomy
Since several retrospective studies reported that pan-
creatogastrostomy (PG) reduces the occurrence of PF
after PD [20,21], there has been trend toward increasing
use of this type of an astomosis. However, the results of a
prospective randomized trial comparing PG with pan-
creatojejunostomy showed that the overall incidence of
PF was 11.7%, and the condition occurred with similar
frequency after pancreatojejunostomy (11.1%) and after
PG (12.3%) [20,22]. Length of postoperative hospital
stay also did not differ between the two procedures. Be-
cause the objective safety of PG was not supported by
the data from these prosp ective studies an d meta-ana lysis
[23], the best method for dealing with the pancreatic
stump after PD remains in question. In addition, disad-
vantages of PG have been identified, including an in-
creased incidence of DGE and of pancreatic duct ob-
struction due overgrowth by the gastric mucosa [13]. In
theory, PG has several advantages over pancreatojeju-
nostomy as the preferred method of reconstruction after
PD. First, a low incidence of pancreatic leakage seems
likely because the anastomosis is made with the thick
and richly vascular gastric wall. Second, PG is known to
suppress activation of proteolytic enzymes. Enterokinase
in particular is required to convert trypsinogen to the
active form, trypsin, and is present in small intestine
mucosa but not in gastric mucosa. This activation also
requires a neutral pH. Therefore, even if leakage does
occur, it does not lead to life-threatening complications
because the pancreatic enzymes are hardly activated.
Indeed, a comparative clinical study found that PG is
safer than pancreatojejunostomy, particularly with regard
to the incidence of PF [20,21]. However, questions re-
main regarding the long-term endocrine and exocrine
function of the pancreas after PG. Available data on
hormone levels indicate that endocrine function appears
to be equal, but exocrine function appears to be worse
after PG than after pancreatojejunostomy [24], resulting
in severe atrophic changes in the remnant pancreas [25].
Therefore, pancreatojejunostomy may be preferable to
maintain activation of the pancreatic enzymes for more
physiologic digestion and absorption.
3. Reducing Problms of Anastomosis with
the Pancreas Stump
In the past several years, increased intraoperative blood
loss has been recognized as a predictive factor for PF [26,
27]. Because an adequate blood supply to the stump of
the pancreas is critical to wound healing, the next step
leading to a successful anastomosis [28], postoperative
infusion planning must be supported. The use of soma-
tostatin analogue has also been focused on to prevent PF
[29], but its use is still not accepted as a consensus [30,
31]. The risk of developing a PF is known to be signifi-
cantly associated with the final histopathological d iagno-
Copyright © 2011 SciRes. SS
sis of the resected specimen, with lower risk in adeno-
carcinoma and higher risk in cystic neoplasms or disease
originating from the bile duct [32,33]. This might be due
to the fact that pancreatic adenocarcinoma usually oc-
cludes the main pancreatic duct, causing duct dilatation
and distal inflammation. Included as a possibility is can-
cer occurring in chronic pancreatitis, where a fibrotic
hard remnant pancreas is easily anastomosed, but a soft
pancreas remains at risk of PF due to its fragility and its
secretion of a high amount of pancreatic juice [18].
Many surgeons have used a stent across the pan-
creaticoenterostomy to prevent PF, and a stent may be
useful for diversion of pancreatic juice from the pancre-
atic anastomotic site, decompression of the re mnant pan-
creas, and patency of the main pancreatic duct. Reported
findings show no significant difference between internal
and external stenting [34], whereas placement of drain-
age tube was associated with a clearly lower PF rate
compared with nonstented patients [3]. Due to the con-
cern about length of hospital stay, shorter postoperative
length is not only considered a predictor of less-invasive
surgical procedures but also forces evaluation of the ne-
cessity of wound treatment or external tube placement.
Potential complication s associated with stent removal are
also argued because local peritonitis after stent removal
has been reported [35]. To reduce postoperative compli-
cations, placement of a stent may be critical, and the in-
ternal type might be better than external, then internal
lost tube might be best.
4. Novel Modified Reconstruction Method
4.1. Background
As suggested by the pathogenesis of the congenital cho-
ledochal cyst, reflux of pancreatic juice into the biliary
tree could have an adverse effect on the bile duct wall. In
particular, lysolecithin, which is converted from bile le-
cithin by pancreatic juice components including phos-
pholipase A, causes severe cellular in jury. Phospholipase
A itself is activated by lysolecithin, and these enzymes
strongly interact. In Child’s type reconstruction, one of
the most common reconstruction methods, the hepatoje-
junostomy site is several centimeters distal to the pan-
creatojejunostomy site. Once leakage develops at the
hepatojejunostomy site, the presence of pancreatic juice
will exacerbate the leakage problem. A similar problem
occurs with the Whipple method, in which the hepato-
and pancreato-jejunostomy anastomoses are reversed.
Thus, the association of pancreatojejunostomy with
life-threatening postoperative complications can be ex-
plained by the enzyme activation theory. Therefore, the
safest type of anastomosis is one in which the mixture of
pancreatic and biliary enzymes is contained, such as in a
jejunojejunostomy. A novel modified type of reconstruc-
tion, the separated loop (SL) method, which prevents
pancreatic leakage and critical secondary complications,
has been well tolerated (Figure 1).
Biliary or pancreas duct drainage tubes are not neces-
sary, and just one drainage tube is placed that is pulled
out within 4 days after surgery to reduce in tra-abdominal
infection induced by long-term tube placement [36]. The
full details were described previously [11].
4.2. Outcome
The SL method, as a Billroth II reconstruction, was eva-
luated at a single institution by comparison to PG or the
Imanaga method, as Billroth I reconstructions, according
to postoperative patien t condition determined from blood
test values and complications incurred [11, 37]. Of 107
patients undergoing PD, 31 were selected for PG, 26 for
the Imanaga method, and 38 for the SL method. PG was
achieved with an invagination anastomosis, which was
constructed with two layers of interrupted sutures from
an anterior gastrotomy and a pancreatic duct tube exiting
through the stomach and abdominal wall.
There were no significant differences between PG and
the Imanaga and SL methods in terms of mean total
blood loss, operation time, or changes in patient body
Figure 1. Schema of separated loop reconstruction method.
(The jejunum is reflected upward through an inci sion in the
transverse mesocolon, and anastomosed end-to-side with
the choledochus. At 20 cm distal to this biliary anastomosis,
the jejunum is interrupted and the end of the pancreas is
inserted into the bowel by means of an invagination tech-
nique. At 20 cm distal to this pancreatojejunostomy, the
jejunum is anastomosed to the stomach in an end-to-side
fashion. Approximately 20 cm distal to the gastrostomy, a
Y-type reconstruction of the jejunum is made with the dis-
tal end of the biliary route).
Copyright © 2011 SciRes. SS
weight. However, DGE was the most frequent cause of
morbidity and was observed exclusively among patients
undergoing PG (12.9%). Of the patients undergoing the
Imanaga method, 19.2% showed a high amylase level in
their drainage fluid, with 3.7% mortality due to abdomi-
nal bleeding after postoperative day 52. In 6.5% and
5.2% of the patients undergoing PG or the SL method,
respectively, a high amylase level was detected, but no
problematic clinical events were observed. No patient
required re-operation. Compared with the IM method
and PG, values of postoperative blood tests were more
favorable for the SL method. The postoperative condi-
tion of our patients who underwent SL reconstruction
was good, suggesting that this method reduces the inci-
dence of serious complications immediately after surgery.
In the SL method, suturing of the anterior outer layer can
lead to pancreas injury, especially with soft pancreas
tissue; therefore, in recent cases, the anterior layer is
made in single for incomplete invagination (Figure 2).
Before beginning anterior layer suturing, two transpan-
creatic U-sutures are placed with 4-0 PDS suture. The
U-suture needle is inserted from the anterior outside of
the jejunum about 1 cm distal to the cut edge and is then
withdrawn from the inside of the jejunum lumen. Liga-
tion of the U-suture leads the pancreas stump into the
jejunum with no strain on the edge of the pancreas. We
experienced no PF in 12 other patients with incomplete
invagination of the pancreas stump. And patients who
survive for long periods after standard pancreatojeju-
nostomy might be at risk of developing secondary cho-
ledochal or pancreatic cancer, as observed in patients
with anomalous arrangement of the pancreaticobiliary
ductal system [38]. Thus, the SL reconstruction method
could potentially prevent both short-term postoperative
complications and future secondary carcinogenesis. A
greater number of cases must be accumulated to confirm
our findings and determine long-term outcomes.
5. Conclusion
Certain reports have shown no clear evidence for or
against one particular method of pancreaticoenteric an-
astomosis [39,40]. The choice of pancreatic anastomotic
method might be based on individual experience and
adherence to basic principles such as good exposure and
visualization; fine, nonstrangulating suture placement to
produce a patent, watertight anastomosis; and preserva-
tion of the blood supply [41]. As long as PD is per-
formed, the argument for safety should be continued, and
for even non-expert surgeons or in cases of soft pancreas
texture, a favorite method that causes the surgeon no
anxiety will be chosen. There is still no agreement as to
which of the reconstruction me t hods i s best , but early -t erm
Figure 2. Recent modified pancreatojejunostomy, incom-
plete invagination. (Before anterior layer suturing, placed
two transpancreatic U-sutures (a). The U-suture was nee-
dled from the anterior outside of jejunum about 1cm distal
to the cut edge, then withdrawing from the inside of the
jejunum lumen. Ligation of the U-suture leads the pancreas
stump (dot area) into the jejunum without any strain for
pancreas edge (b)).
observation after PD indicates that the SL method might
be superior to the other methods.
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