Keywords
pancreas - pancreatic resection - pancreaticoduodenectomy - pancreaticojejunostomy
- postoperative complications - pancreas - CT-spiral - surgery - fistula - hemorrhage
Introduction
Pancreatic surgery is mainly performed to treat pancreatic cancer and cystic tumors,
distal cholangiocarcinoma, and complications of chronic pancreatitis. In Germany,
approximately 10 000 pancreatic surgeries are performed each year [1]. Pancreatic surgeries to treat a primary malignancy of the pancreas or the extrahepatic
bile ducts are among the most complex surgical procedures in visceral tumor medicine
[2]. The mortality rate in a Germany-wide study was 7.3 % for proximal pancreatectomy
and 22.9 % for total pancreatectomy with splenectomy [3]. The mortality and morbidity rates fluctuate depending on the experience of the
surgeon, the operation volume of the hospital, and the ability of the center to manage
complications [4]
[5]. The Germany-wide results differ significantly from the published results of individual
centers with a 30-day mortality rate of less than 3 % [2]. It must be taken into consideration in the international comparison that postoperative
mortality also includes patients after more than 30 days of inpatient care [5]. In spite of improvements in surgical techniques and peri- and postoperative care
after partial pancreatic resection, the postoperative morbidity rate even at specialized
centers is still high (30 %) resulting in long hospital stays [6]. The most common complications are pancreatic fistulas (10–35 %), bile leaks (3–9 %),
bleeding, and acute pancreatitis [7]
[8]
[9]
[10]. Relaparotomy is needed in approximately 5–10 % of cases [1].
In the case of a postoperative complication, detection as early as possible and targeted
management are essential to minimize problems. Postoperative imaging is extremely
important for further categorization of patients and determination of treatment. Computed
tomography (CT) is the method of first choice here [11]
[12]. Other imaging methods like magnetic resonance imaging (MRI) and fluoroscopy are
less helpful and are only used in individual cases. Knowledge of surgical methods,
postoperative anatomy, and the spectrum of complications is decisive for the interpretation
of radiological images. The goal of this article is to describe typical resection
methods and normal postoperative anatomy and to present typical postoperative findings,
common complications, and their management.
Surgery
Depending on the type of underlying lesion and its location, different surgical resection
methods are used. The most common resections are proximal pancreatic resection with
duodenectomy (pancreaticoduodenectomy) and distal pancreatic resection. Central pancreatectomy
is a rare operation and is performed in the case of benign lesions or low malignant
potential tumors. The pancreatic duct and cut surface of the body of the pancreas
are oversewn. The tail of the pancreas is drained via a jejunal loop.
Distal pancreatectomy is performed in the case of malignancies in the body or tail
of the pancreas. The distal part of the pancreas is resected to the left of the superior
mesenteric vein ([Fig. 1a]). Distal pancreatectomy typically also includes a splenectomy. This procedure does
not involve any anastomoses and the postoperative anatomy is almost normal.
Fig. 1 Surgical methods of partial pancreatic resection. a Distal pancreatic resection: the pancreatic head remains in place. The pancreatic
body and tail are resected, anastomoses are not necessary. b Pancreaticoduodenectomy as a classic Whipple operation: the pancreatic head, gastric
antrum, duodenum, proximal jejunum, and gallbladder are resected. The remaining pancreas
is anastomosed to the jejunum in the form of a pancreaticojejunostomy (1). Bile is
drained via a hepaticojejunostomy (2). The gastric antrum is connected to the jejunum
(3) distal to the biliodigestive anastomosis. c Pylorus-preserving pancreaticoduodenectomy (PPPD): the stomach and pylorus are preserved
and a duodenojejunostomy (4) is created. The pancreas is anastomosed to a jejunum
loop. d Using both procedures, the residual pancreas can be inserted into the stomach as
a pancreaticogastrostomy (5). In this case the proximal jejunum is closed as a blind
loop (6). Source: Maike Venhofen
Proximal resection is performed in malignant diseases like periampullary neoplasms,
cancer of the head of the pancreas, distal cholangiocarcinoma, and chronic pancreatitis.
Resection of the head of the pancreas is the most common intervention since two thirds
of pancreatic malignancies affect the head of the pancreas. The classic Kausch-Whipple
procedure includes resection of the head of pancreas, the distal stomach, the duodenum,
the gallbladder, the distal bile duct, the proximal jejunum, and the regional lymph
nodes. This extensive resection requires multiple reconstructions.
In the classic Kausch-Whipple procedure, gastrointestinal continuity is achieved by
gastrojejunostomy after resection of the gastric antrum ([Fig. 1b]). As a rule, resection of the head of the pancreas is currently performed using
a pylorus-preserving technique (PPPD) ([Fig. 1c]) so that the proximal duodenum is connected to an efferent jejunal loop. PPPD was
originally introduced with the goal of improving gastric motility by preserving the
stomach and reducing the incidence of anastomosis ulcers and alkaline gastritis. However,
this goal was not able to be achieved in practice [13]
[14]. The advantage of PPPD is the shorter operation time and the lower intraoperative
blood loss [13]
[15]. With respect to mortality, morbidity, and oncological effectiveness, a large meta-analysis
showed no differences between the two methods [16].
The remaining pancreas is either anastomosed to a jujenal loop in the form of a pancreaticojejunostomy
([Fig. 1b, c]) or is inserted into the body of the stomach as a pancreaticogastrostomy ([Fig. 1 d]). These two types of pancreatic anastomosis have comparable perioperative complication
rates. A meta-analysis showed a tendency toward a lower occurrence of pancreatic fistulas
for pancreaticogastrostomy [17]. In contrast, the prospective multicenter RECOPANC study from 14 German centers
yielded a rate of 20 % significant pancreatic fistulas for pancreaticojejunostomy
compared to 22 % for pancreaticogastrostomy [18]. Bile is drained via the biliodigestive anastomosis created by a hepaticojejunostomy
([Fig. 1]).
Patients with chronic pancreatitis can be treated with pancreaticoduodenectomy or
with a less extensive resection with preservation of the duodenum. In the case of
duodenum-preserving pancreatic head resection (DPPHR), a jejunal loop is sewn to the
anterior surface of the pancreas after excavation of the head of the pancreas and
further distal a jejunojejunostomy is performed analogously to a Roux-en-Y reconstruction
[11].
Pancreatic resection can be performed as an open, minimally invasive laparoscopic,
or robot-assisted procedure. In the data published to date, no significant differences
in overall morbidity or mortality can be seen between the procedures [19]
[20]
[21]. While open surgery is shorter, minimally invasive procedures tend to have advantages
with respect to less blood loss, fewer relevant pancreatic fistulas, and a shorter
hospital stay [21]
[22]. Left pancreatic resection has the advantage of minimally invasive surgery with
respect to reconvalescence and quality of life, but there are no significant differences
regarding the postoperative complication rate [23].
Postoperative imaging
If the early postoperative course is complication-free, there is no indication for
routine imaging. In the case of suspicion of complications, CT is typically the best
imaging modality [11]
[12]
[24]. It allows quick examination of the entire abdomen with high spatial and contrast
resolution including the vascular anatomy. In the early postoperative phase, CT should
be performed using a multiphase protocol. The non-contrast examination of the upper
abdomen is used to detect hyperdense material (clips, stents, or blood). Contrast-enhanced
imaging of the upper abdomen is performed in the late arterial phase (bolus track
in the abdominal aorta, 120 HU threshold, 15 s delay) and the venous phase (60 s delay
after the threshold is reached). Patients receive 0.4 g iodine/kg body weight in a
highly concentrated non-ionized contrast agent with an iodine delivery rate of 1.2 g
iodine/s (corresponding to approx. 120 ml of a contrast agent with 300 mg/ml iodine
and a flow rate of 4 ml/s) followed by a 50-ml saline bolus.
The late arterial phase is used to visualize the pancreatic parenchyma and vascular
and bleeding complications. The portal venous phase with visualization of the entire
abdomen is used to evaluate organ perfusion, drainage tube position, and intestinal
passage and to detect fluid collections. If the patient is capable of drinking, the
upper gastrointestinal tract is distended with 500–700 ml of water prior to the CT
examination. If the explicit goal is to visualize a fistula or gastric anastomotic
insufficiency, diluted contrast agent can be administered orally. In addition to axial
slices (3–5 mm slice thickness), additional coronal and sagittal multiplanar reconstructions
(MPRs) and maximum intensity projections (MIPs) are helpful for examining vascular
issues.
When evaluating early postoperative CT examinations, surgical anastomoses of a gastrojejunostomy
or duodenojejunostomy, hepaticojejunostomy, and pancreaticojejunostomy or pancreaticogastrostomy
must be examined. After resection of the head of the pancreas, the superior mesenteric
vein and the venous confluence are to the right of the remaining pancreas and further
dorsal in the vicinity of the vena cava. In pancreaticojejunostomy, the anastomosis
is anterior to the superior mesenteric artery ([Fig. 2]). Gastrojejunostomy or duodenojejunostomy is usually performed as an antecolic procedure.
After duodenum-preserving pancreatic resection, a jejunal loop is anastomosed to the
remaining pancreas and jejunojejunostomy is performed. Anastomoses usually have edematous
changes in the early postoperative phase with corresponding thickening of the intestinal
and gastric walls. Perivascular edema around the large vessels as well as bands of
edema in the surrounding fatty tissue are also common ([Fig. 3]). Soon after the operation – particularly in the case of R0 resection – these changes
should not be evaluated as residual tumor tissue or local recurrence. After creation
of a biliodigestive anastomosis, pneumobilia, which is often more pronounced on the
left, is normal. The remaining lymph nodes can swell as a result of postoperative
reactive adenopathy and the short-axis diameter can be greater than 1 cm ([Fig. 3]). This type of reactive lymphadenopathy should resolve within 6 months at the latest.
Fluid collections in the surgical area and at the anastomoses are common findings
in the first two weeks and are seen in almost one third of patients [10]. These homogeneous water-equivalent collections are difficult to differentiate from
a pancreatic fistula or insufficiency of the hepaticojejunostomy on imaging.
Fig. 2 Pancreatic anastomoses after pancreatic head resection. a Pancreaticojejunostomy: the residual pancreas is anastomosed with a mobilized jejunum
loop. The anastomosis (arrow) is ventral to the axis of the superior mesenteric artery
at the level of the confluence venosum (*). b Pancreaticogastrostomy: the residual pancreas (small arrows) is inserted into the
posterior wall of the stomach (arrowhead). The pancreas is easily identified by the
course of the lienal vein (*).
Fig. 3 CT on the 4th postoperative day after PPPD with pancreaticogastrostomy. a Axial section at the level of the pancreaticogastrostomy. The anastomosis (arrowhead)
is edematously altered. The pancreas bulges slightly into the stomach. The gastric
lumen is marked after oral contrast administration. The fatty tissue in the surgical
area between the stomach and the hepatic orifice is edematous. b Coronary reformation at the level of the hepaticojejunostomy (arrow). The hepatic
duct is air-filled and visible. Aerobilia of the central intrahepatic bile ducts (small
arrow). Lymph nodes (black arrows) periaortic, mesenteric, and cranial to the lienal
vein are reactively enlarged and enhance after contrast medium application.
Pancreatic fistula
The most common complication after pancreatic resection is pancreatic fistula or anastomotic
insufficiency. A pancreatic fistula is clinically detected on the basis of amylase
in the fluid drained from the surgical area [7]
[25]. The incidence varies between 10 % and 35 % and is associated with the type of intervention.
Fistulas occur 10–30 % more frequently after distal pancreatic resection or enucleation
than after pancreaticoduodenectomy (10–15 %) [6]
[9]. The definition of a pancreatic fistula was standardized by the International Study
Group for Pancreatic Surgery (ISGPS) in 2005 and modified in 2016 [7]
[26]. A fistula is present when the amylase content in the drained fluid is more than
three times the maximum normal serum concentration on the third postoperative day.
Pancreatic fistulas are classified as grade A to grade C. Grade A can only be detected
as a laboratory finding due to the absence of fluid collection on CT. It does not
have any clinical consequences. Therefore, this situation is referred to as a biochemical
leak and not as a fistula in the classification that was modified in 2016. In the
case of grade B or C fistulas, CT shows peripancreatic fluid. In the case of grade
B fistulas, the patient's postoperative management must be adapted and is characterized
by drainage tubes being left in place for more than 3 weeks or by the percutaneous
or endoscopic placement of new drainage tubes. Grade C corresponds to a persistent
fistula requiring revision surgery, fistula-related organ failure, or mortality [26].
CT imaging can confirm clinical suspicion by detecting fluid near the pancreatic anastomosis,
in the pancreatic bed, and in a peripancreatic location ([Fig. 4]). After distal pancreatic resection, a fluid collection with a diameter of more
than 4 cm indicates the presence of a clinically relevant fistula [27]. In the case of major insufficiencies, peritoneal leakage of orally administered
contrast agent can be seen or contrast agent can be detected in the drainage tube
([Fig. 5]). Small air inclusions in the fluid are not pathognomonic for an infection but can
indicate a pancreatic fistula. Increases in density and a heterogeneous image are
suspicious for the presence of pancreatic fluid collections or a superinfection. Pancreatic
fistulas are treated as conservatively as possible or minimally invasively with percutaneous
or endoscopic drain placement since revision surgery is associated with a high complication
rate and mortality of up to 60 % [1].
Fig. 4 Patient with superinfected pancreatic fistula after distal pancreatectomy. a With elevated inflammation lab results 12 days after surgery and wound drains already
removed, there is a homogeneous fluid accumulation (*) in the pancreatic bed. The
infected fluid was drained percutaneously with CT-guided puncture. b After 4 weeks of drainage treatment, there is only a small residual cavity (arrow)
and the drain was removed.
Fig. 5 Patient after PPPD and pancreaticogastrostomy with persistent pancreatic fistula
and elevated amylase in the drainage fluid. a Coronary reformation of a CT scan after oral contrast administration. The pancreas
is visible as a protrusion in the gastric lumen (arrow). A fine contrast medium extraluminate
lies at the level of the anastomosis (arrowhead). b Contrast medium leakage via the indwelling drain (arrow).
Biliary fistula
Insufficiency of a biliodigestive anastomosis is primarily the result of surgical-technical
problems. It is diagnosed clinically when the bilirubin concentration in the drained
fluid is three times higher than the normal serum bilirubin concentration three days
after surgery. The incidence is between 3 % and 9 % of patients with hepaticojejunostomy
[1]. Patients show clinical signs of biliary peritonitis and homogeneous fluid collections
on CT ([Fig. 6]) primarily in the vicinity of the biliodigestive anastomosis [12]. Finally, reliable differential diagnosis between biliary fistula and pancreatic
fistula on imaging is difficult without a clinical correlation due to the close vicinity
to the anastomoses. Treatment must be determined on an interdisciplinary basis. In
addition to creation of a new biliodigestive anastomosis, an attempt can be made to
cure the fistula after the fluid is drained via CT-guided drainage or by percutaneous
transhepatic cholangiodrainage (PTCD).
Fig. 6 Patient after PPPD and pancreaticogastrostomy. Elevated bilirubin concentration in
the drained fluid on day 5. a The pancreas (arrowhead) inserts into the posterior wall of the stomach. Some fluid
is evident perigastrically and peripancreatically. Fluid retention at the porta hepatis
and between the vena cava and the aorta (small arrows). b Fluid is seen next to a jejunal loop and along the course of the extrahepatic portal
vein (small arrow) in the coronary reformation. A surgical drain is depicted caudal
to the liver (arrow).
Postoperative bleeding
Bleeding occurs in 2–16 % of cases and is a serious complication with a high mortality
rate [9]
[28]. In a prospective study, relevant bleeding complications were seen in 9 % of pancreaticogastrostomies
compared to 4 % of pancreaticojejunostomies [18]. Early postoperative bleeding complications within 24 hours of the intervention
are usually due to surgical-technical problems and are typically treated surgically
[29]. Later bleeding due to inflammatory vascular erosion or pseudoaneurysms ([Fig. 7]) is rarer (1.5–5 %) but more complicated with a mortality rate of greater than 60 %.
Extraluminal retroperitoneal bleeding with blood loss via the drainage tube is most
common. Intraluminal bleeding is rarer and manifests as hematemesis or melena. On
non-contrast CT, bleeding is visible as an intraluminal or extraluminal fluid collection
with increased density. A pseudoaneurysm or extravasation can be detected on contrast-enhanced
imaging [24]. Late bleeding is often also treated surgically. Particularly in the case of hemodynamically
stable patients, interventional treatment should be attempted due to the high technical
success rate and the 50 % lower mortality rate [30]
[31]
[32].
Fig. 7 Patient after PPPD with active bleeding via the drain. a CT in arterial phase shows a false aneurysm (arrow) at the origin of the cystic artery
with surrounding hematoma. b The bleeding was successfully controlled by coil embolization.
Circulatory disorder
Ischemic complications are usually the result of surgery-related occlusion of the
hepatic artery or the celiac trunk or more rarely the portal vein [33]. Increasing age of surgical patients results in an increase in the prevalence of
arteriosclerotic vascular changes with involvement of the celiac trunk or the inferior
mesenteric artery and thus the risk for postoperative intestinal ischemia or hepatic
infarction even without intraoperative vascular occlusion [12]. A hepatic infarction is seen as a non-contrast-enhanced parenchyma typically extending
to the liver capsule without signs of a space-occupying lesion ([Fig. 8]).
Fig. 8 Patient with signs of inflammation and liver failure on day 10 after PPPD and pancreaticogastrostomy.
a Axial contrast-enhanced CT in portal venous phase showing hypodensity of the functional
left hepatic lobe and free fluid ventral to the liver. The residual pancreas inserts
into the posterior wall of the stomach (arrow). b MIP reconstruction of the arterial phase. The common hepatic artery is ligated proximal
to the gastroduodenal artery (arrowhead). The left hepatic artery is not perfused.
The arterial supply to the right lobe of the liver is via the right hepatic artery
with the origin from the superior mesenteric artery.
Abscesses
An abscess is usually the result of a superinfection of an undrained or insufficiently
drained pancreatic fistula and can be diagnosed on imaging as a fluid collection with
a thickened and enhanced wall in a patient with signs of infection. The incidence
is around 6 % [1]
[9]
[24]. The treatment of choice is CT-guided puncture and percutaneous drainage.
Impaired gastric emptying
With up to 60 %, impaired gastric emptying is the most common complication after pancreatic
head resection [12]. Current data from a German registry (StuDoQ Pancreas Registry) including 5080 patients
yielded an incidence of 20.6 % for postoperative impaired gastric emptying [14]. Risk factors for the development of postoperative impaired gastric emptying were
advanced age, long operation duration, and reconstruction with pancreaticogastrostomy.
The term impaired gastric emptying is used when a patient cannot consume any solid
food a week after surgery, or the patient has not been able to fully return to solid
food by the 14th day after surgery. Impaired gastric emptying is detected endoscopically
or dynamically under fluoroscopy as small bowel transit using a water-soluble contrast
agent ([Fig. 9]). CT can be performed to rule out a pancreatic fistula or an abscess.
Fig. 9 Dynamic gastric contrast study using fluoroscopy with oral application of a water
soluble contrast agent on the seventh day after PPPD in a patient with vomiting. The
stomach is distended and atonic. The contrast medium is slowly emptying into the attached
jejunum.
Late complications
With a frequency of 4–8 %, the most common late complication is a stricture of the
pancreaticojejunostomy or the hepaticojejunostomy due to scarring with a frequency
of 4–8 % [24]. CT shows dilation of the intrahepatic bile ducts or the pancreatic duct with increasing
parenchymal atrophy of the remaining pancreas. MRI with MRCP is the most suitable
method for visualizing the ducts and anastomoses. Fibrosis must be differentiated
from a duct obstruction due to tumor recurrence. Local recurrence is seen in one third
of cases. Infiltrating growth of soft tissue in the pancreatic bed in the region of
the anastomoses or around the superior mesenteric artery or the celiac trunk is a
typical finding ([Fig. 10]). New lymph node enlargement is also suspicious for lymphogenic recurrence. Distant
hematogenous metastases primarily affect the liver and later the lungs.
Fig. 10 Patient three years after PPPD and new weight loss. a Axial CT shows soft tissue around the superior mesenteric artery (arrow). b Coronary reformation depicts the extensive tumor recurrence along the superior mesenteric
artery and at the level of the venous confluence with obstruction of the superior
mesenteric vein. The celiac trunk is also encased (small arrow).
Conclusion
Globally, pancreatic cancer has one of the worst prognoses and only few patients can
be treated surgically or with a curative approach at the time of diagnosis. Major
pancreatic surgery continues to be associated with a high morbidity rate [18], with early detection of complications and inclusion of interventional-radiological
options being essential for targeted complication management [3]
[4]. Imaging is an important part of the postoperative evaluation of complications after
pancreatic resection. Due to the fast examination and the good spatial and contrast
resolution, CT continues to be the most important and best method particularly for
early postoperative imaging, making it possible to respond quickly, safely, and successfully
to potentially life-threatening complications. The interpreting radiologist must be
familiar with the postoperative anatomy, normal postoperative findings, and manifestation
of typical complications. Many imaging findings must be interpreted in the clinical
context and together with the laboratory results, particularly when diagnosing anastomotic
insufficiency. Therefore, close collaboration between radiology and visceral medicine
is essential for good management. In the case of persistent fistulas or abscesses
as well as in the case of bleeding complications, interventional radiology treatment
options are characterized by high efficiency with a low complication rate.
