Review Article
Complications in Biliopancreatic Surgery
Pasquale Cianci*, Nicola Tartaglia, Alberto Fersini, Antonio Ambrosi and Vincenzo Neri
Department of Medical and Surgical Sciences, University of Foggia, Italy
*Corresponding author: Pasquale Cianci, Department of Medical and Surgical Sciences, University of Foggia, Italy
Published: 12 Oct, 2017
Cite this article as: Cianci P, Tartaglia N, Fersini A,
Ambrosi A, Neri V. Complications in
Biliopancreatic Surgery. Clin Surg.
2017; 2: 1678.
Abstract
The complications of biliopancreatic surgery have a very variable range of incidence showing surgical
procedures with low incidence of complications such as simple cholecystectomy and complex or
very complex procedures such as pancreatic resections followed by high incidence of postoperative
complications. The purpose of this editorial is to examine a number of specific complications unique
to biliopancreatic surgery such as: pancreatic fistula in relation to the different types of pancreaticdigestive
anastomosis and biliary injuries after biliary surgery. Pancreatic and biliary surgical
complications include a large range of conditions with overlapping clinical presentations and
diverse therapeutic choices. The true incidence of pancreatic and biliary complications is difficult
to determine due to selection and reporting bias. The treatment of these complications continues to
evolve and patients may require endoscopic, surgical, and/or percutaneous techniques.
Keywords: Pancreatic surgery; Biliary surgery; Pancreatic fistula; Biliary injuries
Introduction
This editorial reviews the more common postoperative pancreatic and biliary surgical complications, their prevention and treatment. There are medical and surgical complications common to major surgical procedures but our purpose is to examine a number of specific complications unique to biliopancreatic surgery. The evaluation and study of these surgical complications should be connected with each intervention that can be related to the pathology. The specific complications of biliopancreatic surgery have a very variable range of incidence showing surgical procedures with low incidence of complications such as simple cholecystectomy and complex or very complex procedures such as pancreatic resections followed by high incidence of postoperative complications. In this manuscript we have assessed the complications with the classification proposed by Clavien- Dindo, based on the therapy used to treat the complication [1,2].
Complications in Pancreatic Surgery
Acute and chronic pancreatitis, benign and malignant tumors, may require pancreas surgery.
Surgical treatment of pancreatic disease often has very challenging steps, based on the location, the
close connections of the gland with other structures (superior mesenteric artery and vein), and the
management of the resected pancreas. Therefore the pancreatic surgery can result in complications
and high postoperative morbidity rates can occur. Pancreatic resections are the major surgical
procedures, such as duodenopancreatectomy, Frey’s intervention, etc., with operative mortality
rates less than 5%, showing a stable reduction (data referred to the last two decades), but also a
stable high morbidity rates (30-60%) [3].
The majority of perioperative complications of pancreatic surgery are not life-treatening, with
less than 10% requiring reoperation [4]. However these morbidities complicate the postoperative
period with prolonged hospital stay and delay in adjuvant therapy for cancer patients. Our study
will examine the most frequent specific complications.
Pancreatic Fistulas
Pancreatic Fistula (PF) is the most relevant complication of pancreatic surgery. A pancreaticdigestive
anastomosis typically completes the pancreatic surgery and fistula results from an
anastomotic leak. The incidence of PF range from 3 to 50%. This very variable incidence may come
from variety of assessment. In fact this variety of assessment has been in the past years the cause of
great difficulties of clinical evaluation of this morbidity. From the data of the literature there were
26 definitions of PF between 1991-2000. Each definition was arbitrarily assigned a score based on
daily fluid output criteria and timing of fistula development [5]. We can find in the literature a
very variable incidence of PF (Table 1). Then has been proposed by International Study Group on pancreatic fistula a shared definition and classification of PF [6].
The classification of PF is based on some criteria: output of fistula,
pure pancreatic fistula or mixed, side or total interruption of main
pancreatic duct.
• High output fistulas have the output in 24 hours greater
than 200 ml. On the contrary in the low output fistulas the leak is less
than 200 ml in 24 hours.
• The separation between pure and mixed fistula has very
important clinical significance. The pure fistula drains only pancreatic
juice that contains inactive pancreatic enzymes and is relatively
inert without other clinical manifestations. The mixed fistula drains
pancreatic juice with biliary and enteric juice. In the mixed fistula
there are activated proteases, which can cause some complications
such a peripancreatic necrosis, hemorrhage, etc.
• The type of interruption of the main pancreatic duct allows
a further distinction between end and side fistula. The end fistula
is characterized by complete section of the duct. This pathological
condition is present in pancreatic-enteric anastomosis dehiscence
with the distal pancreatic stump or also in case of traumatic
disruption of main pancreatic duct. In the latter condition, that can be
termed “disconnected duct syndrome”, there are two portions of the
pancreas, both secreting, that can heal separately with great difficulty,
and for which is not applicable the conservative management. On
the contrary the end fistula from pancreatic-enteric anastomosis
leakage especially with pure output of pancreatic juice can heal
with conservative management. In the same way a side fistula, with
continuity of the pancreatic duct, has the probability of healing with
conservative treatment.
The postoperative PF usually occurs following the pancreatic
surgery: pancreticoduodenectomy, resection of distal pancreas,
resection/wirsung-jejunostomy in the treatment of chronic
pancreatitis, enucleoresection. The international assessment and
definition of PF allows an important progress in its treatment. The
definition of the International Study Group on Pancreatic Fistula
(ISGPF) is the following: “an abnormal communication between
pancreatic ductal epithelium and another epithelial surface,
containing fistulas derived enzyme rich fluid”. Beside the definition,
the classification proposes a grading system to assess the severity of
the fistula. The grading system plans three levels of severity: Grade
A, B and C. (Table 2). The grading is based on some criteria: drain
amylase level, clinical conditions, sepsis, persistent drainage longer
than 3 weeks, US/CT findings, use of specific treatment, reoperation,
readmission, signs of infection, death. For postoperative fistula due
to pancreatic anastomotic leakage after PD can be identified the risk
factors. There are three types of risk factors: patient’s related risk
factors, disease related risk factors, and surgical procedure related
risk factors.
Patients factors [5,7-17]. There are a lot of patient’s related
risk factors that have been tested in various studies. Male sex,
advanced age (> 70 years), duration of jaundice, creatinine clearance
abnormality, intraoperative blood loss, coronary disease have been
evaluated as risk factors for pancreatic fistula. The results of these
studies show [18] only a general correlation between patient’s
factors and risk of pancreatic fistula: the altered general conditions
of the patients (prolonged jaundice, abnormal creatinine clearance,
coronary disease, etc.), advanced age, intraoperative complications
may interfere with the healing of the pancreatic anastomosis. In short
these factors do not play a role quantitatively definable.
Disease factors
The risk factors for pancreatic fistula connected with pathological
features of the pancreas are in great evidence. The pancreatic
parenchyma texture can be soft, intermediate or hard, linked to
disease. The reports in the literature confirm the greater incidence
of the fistula following anastomotic leakage in the patients with
soft pancreatic parenchyma (20-30%) rather than the patients with
intermediate or hard texture [6,19-23]. A fibrotic pancreatic stump,
especially if chronic pancreatitis is present or if durable ductal
obstruction (neoplastic or not) causes the glandular sclerosis, facilitates
pancreatico-enteric anastomosis, with low risk of anastomotic
leakage. On the contrary can be difficult to perform the anastomosis
with a soft pancreatic parenchyma, characterized by high incidence
of anastomotic leakage. In fact the pancreatic or periampullary
diseases without main pancreatic duct obstruction and then without
pancreatic tissue sclerosis present high risk of anastomotic leakage:
duodenal adenocarcinoma, distal cholangiocarcinoma, benign
islet tumors, duodenal adenoma, etc: Besides the structure of the
parenchyma, should be considered for risk factor of fistula also the
size of main pancreatic duct. The size of the duct is connected with
the ductal obstruction (neoplastic or not) or the chronic flogosis.
Pancreas with dilated ducts and generally with hard parenchyma
shows less risk of anastomotic leakage and fistula; whereas if the size
of the duct is small (3 mm or less) the risk of pancreatic fistula is
higher. Other risk factors for pancreatic fistula together a small size of
pancreatic duct is a high pancreatic juice output [24].
Operative/technical factors. The pancreatic stump in the past
two decades has been submitted to various surgical procedures
that have been assessed and compared based on postoperative
fistula rates. These surgical techniques are pancreatojejunostomy,
pancreatogastrostomy, invagination of pancreatojejunal anastomosis, position of the stent in pancreatico-enteric anastomosis, etc. [5-7,19-
23,25,26]. The results of the comparison of various techniques did not
permit an unbeatable conclusion in favor of a technique or another.
Moreover there are other risk factors for pancreatic anastomotic
fistula related to surgical treatment: more complex intervention
for advanced stages of disease including vascular resections for
mesenteric-portal invasion, jaundice associated coagulopathy, etc. In
summary the increased intraoperative blood loss is an important risk
factor for developing PF. Intraoperative blood loss exceeding 1500 ml
increases significatively the risk of postoperative PF.
Risk of PF following enucleoresection of little nodular lesions of
the pancreas (e.g. insulinoma) and distal pancreatectomy [27,28].
The enucleoresection can cause fistula if the walls of main or other
ducts have been damaged during surgical procedure. Usually there
are partial lesions of the duct. In this case the fistula, well drained, can
be treated with conservative option. The distal resection of pancreas
with or without splenectomy can be followed by postoperative fistula.
The favorable conditions in this setting are the normal transpapillar
flow of pancreatic secretion that, if necessary can be improved with
endoscopic sphincterotomy and effective drainage of pure PF. The
conservative treatment should be the usual therapeutic choice.
Technical features of pancreatic – digestive anastomosis
The PF is a most common morbidity of pancreatic surgery with a
very variable incidence from the literature. Its incidence ranges from
6 to 30-40% [5-10,19-23,25,26]. In these same reports the mortality
ranges from 1, 4 to 5%. The clinical impact of PF consists of clinical
conditions, specific treatment required, persistence of drainage, signs
of infection, sepsis, reoperation, etc. The starting point of definition of
postoperative PF is the drain amylase level plus than 3 time’s normal
serum amylase, from the third postoperative day. The majority of
postoperative PF comes from leakage of digestive anastomosis of
remnant pancreas. Therefore the formality of pancreato-digestive
anastomosis is the first step in the prevention of anastomotic
leakage. There are two choices for pancreatic-digestive anastomosis:
pancreaticojejunostomy and pancreaticogastrostomy. In the
perspective of the safety of the anastomosis there are not the advantage
data for either type of anastomosis. The safety of anastomosis is based
on the skills of the surgeon about each specific procedure.
Pancreaticojejunostomy (PJ) can be performed such as:
• End-to-end anastomosis with some variations: one layer
(suture passage within the main duct and full thickness of the jejunal
wall); two layers (the inner layer approximates the cut pancreatic
surface passing whitin the main pancreatic duct to the full thickness
of the jejunal wall; the other layer approximates the capsule of the
pancreas to the seromuscular of the jejunum).
• End to side such as duct to mucosa anastomosis performing
two layers suture.
• End to end invagination technique. The remnant pancreas
is invaginating into the jejunum [29-34].
The comparison between these surgical techniques showed the
overlapable results based on the rate of anastomotic leakage. This
final conclusion emphasizes that the success (outcomes) of some
surgical procedures lies on the specific skill of the surgeon performing
a specific technique of pancreaticojejunal anastomosis and overall on
the pathologic characteristic of the pancreatic tissue (fibrosis or not)
and of the size of main pancreatic duct.
Pancreaticogastrostomy (PG): end to side anastomosis between the
pancreatic stump and posterior wall of the stomach. The anastomosis
can be performed following the technique of invagination of remnant
pancreas into the stomach or suturing full thickness gastric wall with
main pancreatic duct.
Several suggestions for prevention of postoperative
pancreatic fistula (POPF)
There are some options for prevention or control of
postoperative fistula. The management of pancreatic remnant after
pancreaticoduodenectomy plays a relevant role in the prevention of
POPF. Preventive function can be hypothesized for pharmacological
inhibition of exocrine pancreatic secretion in the postoperative
period. Peri-postoperative infusion of somatostatin-octreotide
may reduce the pancreatic juice secretion and consequently the
incidence of the POPF. The data of the literature about the results
of these therapeutic procedures are not overlapable [14,35-38].
Pancreaticojejunal or pancreaticogastric anastomoses are the main
surgical procedures that can condition the incidence of POPF (see
above). Some other technical detail may be important to prevent the
fistula. Main pancreatic duct stent has been proposed and employed.
The stent allows, with transjejunal or transgastric passage, the external
drainage of pancreatic juice avoiding the activation of pancreatic
enzymes by the bile. The use of T – tube transanastomotic biliary
drainage can be proposed because can establish the almost complete
separation of biliary and pancreatic secretions and an eventual POPF
should be pure fistula [39]. Other technical solutions are the use of
separate Roux-en-Y limbs for pancreatic anastomosis or with the
reduction of pancreatic remnant after duodenopancreatectomy.
The closure of pancreatic stump without digestive anastomosis has
been also proposed. In this way the purpose is to obtain a guided and
isolated PF. After ligation of the main pancreatic duct, the closure
of pancreatic stump can be performed with stitch suture or stapler
closure. Can be used also after the closure of pancreatic remnant or as
reinforcement of pancreatic anastomosis the fibrin sealant.
The treatment of POPF encompasses some therapeutic
procedures (medical or surgical) based on the type of intervention
(duodenopancreatectomy, distal pancreatectomy, enucleoresection,
etc.) and the definition and grade of this complication following on
one hand the classification proposed by Clavien, based on the therapy
used to treat the complication, and the other hand the definition and
classification proposed by International Study Group on Pancreatic
Fistula (ISGPF).
Table 1
Table 2
Complications in Biliary Surgery
Biliary surgery (gallbladder and biliary tract procedures) presents
very variable range of complexity from simple cholecystectomy to
treatment of cholangiocarcinoma or biliary tract injuries repair. The
incidence of biliary injuries relative to cholecystectomy, with open or
laparoscopic approach, range from 0.2 to 0.8% [40]. The biliary leak
after biliary surgery can be caused by a lot of factors, almost always
due to iatrogenic injuries or complications of percutaneous, surgical,
endoscopic interventions. The etiology of these complications can be
summarized as follow:
• Abdominal operations: cholecystectomy, pancreaticobiliary
resection, hepatic resection, gastroduodenal surgery, hepatic
transplantation, biliary anastomosis.
• Percutaneous procedures: transhepatic drainage/dilation,
liver biopsy, radiofrequency tumor ablation, liver biopsy.
• Endoscopic retrograde cholangiography: biliary
perforation.
The most common causes of postcholecystectomy biliary leakage
are cystic duct stump leak (frequency range from 60 to 70% of this
complication), duct of Luschka injuries (10-20%). The bile leakage
can complicate all bilioenteric anastomosis. The incidence of this
complication is not exactly established, but we can consider that its
range is from 2 to 5%. The frequency of this complication is, on the
whole, very low but in selected cases should be evaluated the employ
of biliary transanastomotic drainage such as T-tube. The most
significant complication of biliary-hepatic surgery is the bile duct
injuries. Numerous types of bile duct lesions can be considered. There
is a useful classification of common bile duct injury [41] the Way-
Stewart classification. This classification encompasses four classes of
bile duct injuries:
• Class I: common bile duct (CBD) mistaken for cystic duct
but recognized; cholangiogram incision in cystic duct extended into
CBD.
• Class II: lateral damage of common hepatic duct (CHD)
from cautery or clips placed on duct; associated bleeding, poor
visibility.
• Class III: CBD mistaken for cystic duct not recognized;
CBD, CHD, R, L hepatic ducts transected and/or resected.
• Class IV: RHD mistaken for cystic duct, RHA mistaken for
cystic artery, RHD, RHA transected. Lateral damage of the RHA from
cautery or clips placed on duct [42].
Various measures have been suggested to reduce the risk of
biliary injuries during biliary intervention, mostly cholecystectomy,
that can be very complex procedure if acute or chronic inflammation
is present in the triangle of Calot. Others risk factors are abnormal
biliary anatomy, short cystic duct and also improper surgical
maneuvers (excessive cephalad or lateral retraction of gallbladder,
excessive use of cautery, etc.). The first maneuver useful in the risk
reduction should be the antegrade dissection of gallbladder [43].
Strasberg et al. [44] have proposed the “critical view of safety”. This
method encompasses three actions:
• The triangle of Calot must be rid of fat and fibrous tissue.
• The gallbladder infundibulum should be disconnected
from the gallbladder bed.
• Only two structures can be connected with gallbladder.
These maneuvers cannot give the total certainty of avoiding
the biliary injuries but can give a considerable reduction of the risk
mostly in the complex surgical conditions.
These injuries can be recognized during operative procedures
(15-30%) or in the postoperative period, early or late.
Discussion
Clinical presentation
The surgical drain, if present, can show the evident biliary
component. If there isn’t the drain, the bile leakage forms a collection,
usually in the surgical site, or widespread in the peritoneal cavity. The
clinical presentation ranges from general discomfort to abdominal
pain, fever, septic conditions, expected evolution of bile peritonitis.
Diagnosis
The first diagnostic step is the suspicion based on the alteration
of normal postoperative course. The diagnostic phase can employ the
common exams. Laboratory data can show serum bilirubin increase
and leukocytosis. At imaging exams (US, CT) can be detected
intrabdominal fluid collection. An important diagnostic exam
for postoperative bile leakage is the cholangiography performed
by different ways: operative drain, if present; biliary drainage
(T-tube), endoscopic retrograde cholangiography, percutaneous
transhepatic cholangiography. The access to biliary three in some
cases allows several therapeutic actions (simple drainage, prosthesis,
stent, etc.). A noninvasive imaging exam is the magnetic resonance
cholangiopancreatography that cannot have therapeutic role.
Management
The minor bile leaks, usually after cholecystectomy can be
treated with decompression of biliary tree by ERCP and endoscopic
sphincterotomy with or without biliary stent. In some cases should
be necessary percutaneous drainage of intrabdominal fluid biliary
collections. If the transpapillary access is not possible can be employed
the percutaneous way (PTC) to biliary tree. The major bile duct injury
usually requires surgical intervention. The timing of treatment can
be conditioned by several factors: time of recognition of lesion, the
type of lesions, the skills of the surgeons. The lesion detected at time
of intervention (e.g. laparoscopic cholecystectomy) should be treated
with primary repair or hepaticojejunostomy (usually end to side
Roux-en-Y loop). On the other hand if the injury has been detected in
the early postoperative period with CT scan the first step of treatment
is the (percutaneous) drain collections. The following step is the
anatomical definition of biliary lesion by PTC with biliary drainage. In
this way we can control the biliary leak that allows waiting 4-6 weeks
to organize the definitive repair as hepaticojejunostomy. In any case
the biliary injury can be followed by long-term morbidity, multiple
radiological and surgical procedures and also mortality. Clinical
manifestations due to biliary injuries in the later postoperative period
are biliary strictures and cholangitis. Biliary strictures can be due
also to bilio-digestive anastomosis following biliary resections for
malignant or benign diseases. Biliary lithiasis can be complicated by
retained stones following surgical treatments such as cholecystectomy
or choledocolithotomy. Moreover biliary pancreatitis, sometime
recurrent, may be the complication of incomplete treatment of
papillary stenosis due to stones passage through duodenal papilla.
Finally postoperative pancreatitis can occur following biliary
surgery. The other specific complications of pancreatic surgery are
the following: delayed gastric emptying after PD (incidence 20-40%),
postoperative hemorrhage (incidence 2-15%) following pancreatic
resection in the immediate postoperative period or delayed 10-15
days after surgery. Gastrojejunal anastomosis fistulas after PD with
incidence 0.4-7.4%, enteric fistulas after laparotomies/relaparotomies
as treatment of infected pancreatic necrosis (high incidence 41-
75%), intrabdominal abscess following necrosectomy for infected
pancreatic necrosis after acute pancreatitis (incidence 13-26%), after
PD (incidence 11%) and pancreatic-enteric anastomosis (incidence
7%).
Conclusion
Pancreatic and biliary surgical complications include a large range of conditions with overlapping clinical presentations and diverse therapeutic choices. The true incidence of pancreatic and biliary complications is difficult to determine due to selection and reporting bias. The treatment of these complications continues to evolve and patients may require endoscopic, surgical, and/or percutaneous techniques.
References
- Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205-13.
- Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187-96.
- Ho CK, Kleeff J, Friess H, Büchler MW. Complications of pancreatic surgery. HPB (Oxford). 2005;7(2):99-108.
- Ushigome H, Sakai K, Suzuki T, Nobori S, Yoshizawa A, Ikoma H, et al. Biliary anastomosis and biliary complications following living donor liver transplantation. Transplant Proc. 2008;40(8):2537-8.
- Bassi C, Butturini G, Molinari E, Mascetta G, Salvia R, Falconi M, et al. Pancreatic fistula rate after pancreatic resection. The importance of definitions. Dig Surg. 2004;21(1):54-9.
- Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. International Study Group on Pancreatic Fistula Definition. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138(1):8-13.
- Pecorelli N, Balzano G, Capretti G, Zerbi A, Di Carlo V, Braga M. Effect of surgeon volume on outcome following pancreaticoduodenectomy in a high-volume hospital. J Gastrointest Surg. 2012;16(3):518-23.
- Lowy AM, Lee JE, Pisters PW, Davidson BS, Fenoglio CJ, Stanford P, et al. Prospective, randomized trial of octreotide to prevent pancreatic fistula after pancreaticoduodenectomy for malignant disease. Ann Surg. 1997;226(5):632-41.
- Strasberg SM, Linehan DC, Clavien PA, Barkun JS. Proposal for definition and severity grading of pancreatic anastomosis failure and pancreatic occlusion failure. Surgery. 2007;141(4):420-6.
- Lin JW, Cameron JL, Yeo CJ, Riall TS, Lillemoe KD. Risk factors and outcomes in postpancreaticoduodenectomy pancreaticocutaneous fistula. J Gastrointest Surg. 2004;8(8):951-9.
- van Berge Henegouwen MI, De Wit LT, Van Gulik TM, Obertop H, Gouma DJ. Incidence, risk factors, and treatment of pancreatic leakage after pancreaticoduodenectomy: drainage versus resection of the pancreatic remnant. J Am Coll Surg. 1997;185(1):18-24.
- Yeo CJ, Cameron JL, Lillemoe KD, Sauter PK, Coleman J, Sohn TA, et al. Does prophylactic octreotide decrease the rates of pancreatic fistula and other complications after pancreaticoduodenectomy? Results of a prospective randomized placebo-controlled trial. Ann Surg. 2000;232(3):419-29.
- Matsusue S, Takeda H, Nakamura Y, Nishimura S, Koizumi S. A prospective analysis of the factors influencing pancreaticojejunostomy performed using a single method, in 100 consecutive pancreaticoduodenectomies. Surg Today. 1998;28(7):719-26.
- Poon RT, Lo SH, Fong D, Fan ST, Wong J. Prevention of pancreatic anastomotic leakage after pancreaticoduodenectomy. Am J Surg. 2002;183(1):42-52.
- Yeh TS, Jan YY, Jeng LB, Hwang TL, Wang CS, Chen SC, et al. Pancreaticojejunal anastomotic leak after pancreaticoduodenectomy--multivariate analysis of perioperative risk factors. J Surg Res. 1997;67(2):119-25.
- Ishikawa O, Ohigashi H, Imaoka S, Teshima T, Inoue T, Sasaki Y, et al. Concomitant benefit of preoperative irradiation in preventing pancreas fistula formation after pancreatoduodenectomy. Arch Surg. 1991;126(7):885-9.
- Hoffman J. Does prior adjuvant chemoradiotherapy lead to a safer pancreatoduodenectomy? Ann Surg Oncol. 2006;13(1):7-9.
- Machado NO. Pancreatic fistula after pancreatectomy: definitions, risk factors, preventive measures, and management-review. Int J Surg Oncol. 2012;2012:602478.
- Callery MP, Pratt WB, Vollmer CM Jr. Prevention and management of pancreatic fistula. J Gastrointest Surg. 2009;13(1):163-73.
- Yang YM, Tian XD, Zhuang Y, Wang WM, Wan YL, Huang YT. Risk factors of pancreatic leakage after pancreaticoduodenectomy. World J Gastroenterol. 2005;11(16):2456-61.
- Shrikhande SV, D'Souza MA. Pancreatic fistula after pancreatectomy: evolving definitions, preventive strategies and modern management. World J Gastroenterol. 2008;14(38):5789-96.
- Lai EC, Lau SH, Lau WY. Measures to prevent pancreatic fistula after pancreatoduodenectomy: a comprehensive review. Arch Surg. 2009;144(11):1074-80.
- Cameron JL, Riall TS, Coleman J, Belcher KA. One thousand consecutive pancreaticoduodenectomies. Ann Surg. 2006;244(1):10-5.
- Hamanaka Y, Nishihara K, Hamasaki T, Kawabata A, Yamamoto S, Tsurumi M, et al. Pancreatic juice output after pancreatoduodenectomy in relation to pancreatic consistency, duct size, and leakage. Surgery. 1996;119(3):281-7.
- Schmidt CM, Powell ES, Yiannoutsos CT, Howard TJ, Wiebke EA, Wiesenauer CA, et al. Pancreaticoduodenectomy: a 20-year experience in 516 patients. Arch Surg. 2004;139(7):718-25; discussion 725-7.
- Bassi C, Falconi M, Salvia R, Mascetta G, Molinari E, Pederzoli P. Management of complications after pancreaticoduodenectomy in a high volume centre: results on 150 consecutive patients. Dig Surg. 2001;18(6):453-7; discussion 458.
- Sledzianowski JF, Duffas JP, Muscari F, Suc B, Fourtanier F. Risk factors for mortality and intra-abdominal morbidity after distal pancreatectomy. Surgery. 2005;137(2):180-5.
- Pannegeon V, Pessaux P, Sauvanet A, Vullierme MP, Kianmanesh R, Belghiti J. Pancreatic fistula after distal pancreatectomy: predictive risk factors and value of conservative treatment. Arch Surg. 2006;141(11):1071-6; discussion 1076.
- Grace PA, Pitt HA, Tompkins RK, DenBesten L, Longmire WP Jr. Decreased morbidity and mortality after pancreatoduodenectomy. Am J Surg. 1986; 151:141-9.
- Matsumoto Y, Fujii H, Miura K, Inoue S, Sekikawa T, Aoyama H, et al. Successful pancreatojejunal anastomosis for pancreatoduodenectomy. Surg Gynecol Obstet. 1992;175(6):555-62.
- Howard JM. Pancreatojejunostomy: leakage is a preventable complication of the Whipple resection. J Am Coll Surg. 1997;184(5):454-7.
- Hosotani R, Doi R, Imamura M. Duct-to-mucosa pancreaticojejunostomy reduces the risk of pancreatic leakage after pancreatoduodenectomy. World J Surg. 2002;26(1):99-104.
- Tsuji M, Kimura H, Konishi K, Yabushita K, Maeda K, Kuroda Y. Management of continuous anastomosis of pancreatic duct and jejunal mucosa after pancreaticoduodenectomy: historical study of 300 patients. Surgery. 1998;123(6):617-21.
- Hwang TL, Jan YY, Chen MF. Secural pancreaticojejunal anastomosis for the pancreaticoduodenectomy. Hepatogastroenterology. 1996;43(7):275-7.
- Büchler M, Friess H, Klempa I, Hermanek P, Sulkowski U, Becker H, et al. Role of octreotide in prevention of post operative complications following pancreatic resection. Am J Surg. 1992;163(1):125-30.
- Pederzoli P, Bassi C, Falconi M, Camboni MG. Efficacy of octreotide in the prevention of complications of elective pancreatic surgery. Italian Study Group. Br J Surg. 1994;81(2):265-9.
- Montorsi M, Zago M, Mosca F, Capussotti L, Zotti E, Ribotta G, et al. Efficacy of octreotide in the prevention of pancreatic fistula after elective pancreatic resections: a prospective, controlled, randomized clinical trial. Surgery. 1995;117(1):26-31.
- Friess H, Beger HG, Sulkowski U, Becker H, Hofbauer B, Dennler HJ, et al. Randomized controlled multicentre study of the prevention of complications by octreotide in patients undergoing surgery for chronic pancreatitis. Br J Surg. 1995;82(9):1270-3.
- Cianci P, Giaracuni G, Tartaglia N, Fersini A, Ambrosi A, Neri V. Use of t-tube biliary drainage during reconstruction after pancreaticoduodenectomy. A single institution experience. Ann Ital Chir. 2017;88.
- Anderson CD, Scoggins CR, Chari RS. Reoperative hepatobiliary Surgery. In: Mark P Callery, ed. Handbook of Reoperative General Surgery. Malden, Blackwell Publishing Inc., 2006;1-16.
- Way LW, Stewart L, Gantert W, Liu K, Lee CM, Whang K, et al. Causes and prevention of laparoscopic bile duct injuries: analysis of 252 cases from a human factors and cognitive psychology perspective. Ann Surg. 2003;237(4):460-9.
- Stewart L, Way LW. Bile duct injuries during laparoscopic cholecystectomy. Factors that influence the results of treatment. Arch Surg. 1995;130(10):1123-8; discussion 1129.
- Neri V, Ambrosi A, Fersini A, Tartaglia N, Valentino TP. Antegrade dissection in laparoscopic cholecystectomy. JSLS. 2007;11(2):225-8.
- Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg. 1995;180(1):101-25.