Complications After

P a n c re a t i c o d u o d e n e c t o m y
Robert Simon, MD

KEYWORDS
 Pancreaticoduodenectomy  Whipple  Complications  Pancreatic fistula
 Delayed gastric emptying  Informed consent

KEY POINTS
 Mortality rate for pancreaticoduodenectomies has decreased drastically over the years,
but morbidity remains high.
 Grading systems are important to ensure uniform complication assessment and guide
therapy.
 Pancreatic fistula is one of the most dreaded complications after
pancreaticoduodenectomy.
 Understanding the potential complications is imperative to patient education to set expec-
tations and provide better informed consent.

INTRODUCTION

The first pancreaticoduodenectomy was performed in 1909 by Dr Kausch.1 The pro-

cedure was adapted and popularized by Dr Allen Oldfather Whipple in 1935, who per-
formed only 37 in his career.2 Pancreaticoduodenectomy was initially performed in a
2-stage operation. The first was the anastomosis stage wherein a cholecystogastros-
tomy was formed as well as a gastrojejunostomy. The common bile duct was then
transected during this stage. Approximately 4 weeks later, the patient was brought
back to the operating room for the resection stage of the operation. The duodenum,
pancreatic head, and common bile duct were resected, and the pancreatic duct
was oversewn.3 This procedure was performed infrequently because of high in-
hospital mortality rate, which approached 25%. In the 1980s the procedure increased
in popularity as surgical techniques improved. As surgeon experience went up, the
morbidity and mortality rates went down, and although the mortality rate is low,
approximately 1% in high-volume centers, there continues to be a high morbidity

General Surgery, Department of Hepatopancreaticobiliary Surgery, Digestive Disease and Sur-

gery Institute, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195, USA
E-mail address: [email protected]

Surg Clin N Am 101 (2021) 865–874

https://doi.org/10.1016/j.suc.2021.06.011 surgical.theclinics.com
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866 Simon

rate that approaches 50%.4,5 Understanding the potential complications is important

so that one can help recognize when complications do arise and better treat the pa-
tient. In addition, it is imperative when having discussions with patients and their fam-
ilies preoperatively to help them truly make an informed decision about whether or not
they want to move forward with surgery.
The classic Whipple procedure that is performed to today is a single-stage opera-
tion wherein the pancreatic head, duodenum, and common bile duct are resected
and 3 new anastomoses are performed with a pancreaticojejunostomy, hepaticojeju-
nostomy, and gastrojejunostomy. There are a few variations on the Whipple operation
that have been developed over the years. The primary one is a pylorus-preserving
Whipple procedure, wherein the duodenum is transected immediately distal to the py-
lorus and a duodenojejunostomy is performed. This variation was first described in the
1970s by Traverso and Longmire6 to try and prevent postgastric symptoms and was
popularized in the 1980s.7–9

SURGICAL SITE INFECTIONS

After pancreaticoduodenectomy, surgical site infections are one of the most common
complications, listed as high as 23.5%, but in the United States, they tend to be lower,
around 7% to 13%.10 Although deep surgical site infections are usually amenable to
percutaneous drainage by interventional radiology, sometimes surgery is needed to
washout the surgical field. Preoperative bile duct cannulation has been shown to in-
crease the risk of infectious complications; this is likely due to seeding of the bile
with enteric bacteria that causes bacteremia, potentially leading to infections. In one
study, patients who underwent preoperative stenting of their biliary tree had infectious
complications 41% of the time, whereas those who did not undergo stenting had in-
fectious complications only 25% of the time.11 Another study found that those who
were stented preoperatively had an odds ratio of 3.4 for an infectious complication.12
Although preoperative stenting of the bile duct is technically a modifiable risk factor for
infections, it is often unavoidable. If a patient is jaundiced and about to undergo neo-
adjuvant chemotherapy, a stent is a must, not only to prevent cholangitis but also to
make the patients themselves more comfortable as well as improve their nutritional
status. Even in patients who are going to receive upfront surgery, if wait times are pro-
longed then preoperative stenting is indicated.
In terms of preventing infectious complications, wound protectors have been shown
to decrease the rate of surgical site infections. A recent article using the American Col-
lege of Surgeons National Surgical Quality Improvement Program database of more
than 11,000 pancreaticoduodenectomies showed that wound protectors decreased
the rate of superficial and deep surgical site infections from 9.5% to 5.7%. In those
who had preoperative stents placed, the rate dropped from 12.2% to 6.6%, and in
those without stenting, the rate dropped from 6.5% to 4.6%.13 Proper antibiotic selec-
tion has also been shown to decrease infections. Ideally, a second-/third-generation
cephalosporin combined with metronidazole should be used. When cohorts were
compared, those that received the second-/third-generation cephalosporin and
metronidazole had fewer overall surgical site infections, 14.8% versus 26.4%. The
rate of Clostridium difficile also decreased from 8.1% to 1.9% using this novel anti-
biotic prophylaxis regimen.14 Changing gloves and suction tips after all anastomoses
are completed, combined with irrigating the abdomen with warm saline, has also been
shown to decrease wound complications. Last, there is also some evidence that using
negative pressure wound therapy on the incision can reduce the infection rate after
pancreaticoduodenectomy.15

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 Complications After Pancreaticoduodenectomy 867

DELAYED GASTRIC EMPTYING

Delayed gastric emptying (DGE) is a known complication after pancreaticoduodenec-

tomy and is the main reason why nasogastric tubes (NGTs) used to routinely be placed
intraoperatively and kept postoperatively. The International Study Group of Pancreatic
Surgery (ISGPS) in 2007 developed a standard definition of DGE. In broad terminol-
ogy, DGE is defined as requiring an NGT for longer than 3 days, having to reinsert
an NGT after postoperative day 3, or the inability to tolerate an oral diet after postop-
erative day 7. DGE is further broken up into 3 grades: grade A, where an NGT is
required between 4 and 7 days, or the patient is unable to tolerate an oral diet after
7 days but is able to resume it before day 14; grade B, where an NGT is required be-
tween 8 and 14 days, or the patient is unable to tolerate an oral diet after 14 days but is
able to resume it before day 21; and last, grade C, where an NGT is required after
14 days and an oral diet is not tolerated after 21 days.16 Multiple studies have looked
into DGE, and although the incidence varies widely, it is considered to occur in about
20% to 30%5,17 of cases, representing one of the most common complications of
pancreaticoduodenectomy. The cause of DGE is multifactorial. One reason is that
there is a decrease in the amount of motilin secreted as a result of the duodenum being
resected. Another reason is that the vagal and sympathetic innervation of the antrum
and pylorus are cut by dissecting along the common hepatic artery and the lesser
omentum. Decreased blood flow to the pylorus and antrum due to dissection and
mobilization are also thought to be a contributing factor toward DGE. Finally, pancre-
atic fistulae are also thought to be a potential cause of DGE.
Treatment of DGE is usually simple because it is self-limiting. Nasojejunal feeding
tubes are often the only treatment necessary and allow enteral nutrition because the
remainder of the intestine is typically working well. Patients are able to go home
with these tubes in place and are typically well tolerated. If the patient has DGE for
a prolonged period, a gastrostomy tube with jejunal extension can be used to facilitate
the patient going home and being more comfortable.
Ultimately the best way to treat DGE is to prevent it in the first place, and there have
been a few interventions with some promising results. The first is when reconstructing
the enteric anastomosis, it should be performed in an antecolic fashion, because this
has been found to have lower rates of DGE when compared with retrocolic anastomo-
ses (9% compared with 33%).18 Another promising technique that has been sug-
gested to improve DGE rates is a Braun enteroenterostomy. The Braun
enteroenterostomy was described by Braun himself in the late 1800s with the purpose
of preventing bile reflux and helping divert food from the afferent limb of a loop gastro-
jejunostomy.19 The technical aspect involves creating a side-to-side enteroenteros-
tomy 25 cm away from the gastrojejunostomy anastomosis; this can be performed
with a stapled or a handsewn technique. A study by the University of Florida from
2010 showed that the rate of DGE decreased from 60% in those without a Braun
enteroenterostomy to 36% in those who had a Braun enteroenterostomy performed.20
A more recent meta-analysis from 2018 looked at 11 studies with more than 1600 pa-
tients undergoing pancreaticoduodenectomy. Those who had a Braun enteroenteros-
tomy performed developed DGE 11.5% of the time compared with 26.6% in those
without a Braun enteroenterostomy.21 Another technique that has been evaluated
and explored is whether or not to preserve the pylorus. In terms of oncologic out-
comes, mortality rate, and risk of other complications such as pancreatic fistulae,
there is no significant difference between the pylorus-preserving pancreaticoduode-
nectomy or the standard pancreaticoduodenectomy.22 In terms of DGE, though, it
has been suggested that resecting the pylorus leads to lower rates of DGE. In one

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868 Simon

study, pylorus resection was associated with a 15% risk of DGE compared with 42.5%
in the pylorus-preserving group.23

PANCREATIC FISTULA

One of the most feared complications of pancreaticoduodenectomy is a pancreatic

fistula. The pancreas does not typically hold suture well because of its friable nature
and as a result is prone to leakage. In the most recent ISGPS guidelines, a pancreatic
fistula has been classified into 3 categories. Grade A fistula refers to a biochemical
leak defined as drain fluid amylase measured on postoperative day 3 or beyond
that is greater than 3 times the serum level and is not clinically relevant. A grade B
pancreatic fistula requires a change in the expected postoperative management of
the patient. This fistula is more specifically defined as persistent drainage greater
than 3 weeks in duration, requirement of percutaneous or endoscopic drainage of
amylase-rich fluid collection, bleeding that requires angiography, or infection. Once
organ failure occurs, this becomes a grade C pancreatic fistula. Organ failure includes
those that require reintubation, hemodialysis, or vasopressor support. In addition, a
grade C pancreatic fistula also includes those that require a reoperation for the
pancreatic leak, or those that lead to death from the leak. To reiterate, biochemical
leaks are clinically insignificant seeing because they do not change the clinical course
of the patient. Group B and C pancreatic fistulas have been grouped together into clin-
ically relevant pancreatic fistulas (CR-PF), which is important when interpreting the
literature. Although multiple techniques have been developed in an attempt to mini-
mize the incidence of pancreatic fistulae, not one is perfect.24
Pancreatic fistulas have also sparked the question of whether or not to place a drain
near the pancreatic duct anastomosis. As a result, risk calculators have been devel-
oped to help guide surgeons in this regard. The most commonly used calculator
was developed by Dr Vollmer and colleagues and uses a 10-point grading scale,
dividing patients up into negligible risk, low risk, intermediate risk, and high risk for
developing a CR-PF. The variables that go into calculating the risk score include
texture of the pancreas itself, whether the pathologic condition is pancreatic in origin
or extrapancreatic, the diameter of the main pancreatic duct, and intraoperative blood
loss.25 Those scoring 0 points were placed in the negligible-risk strata and had a 0%
risk of developing a CR-PF based on a multiinstitutional validation study. Those
scoring 1 to 2 points were in the low-risk group and had a 6.6% risk of developing
a CR-PF. Those with a score of 3 to 6 were placed in the intermediate-risk group
and had a 12.9% risk of developing a CR-PF, and finally patients scoring between 7
and 10 were placed in the high-risk group and had a 28.6% risk of developing a
CR-PF. Complications, length of stay, and readmission rates also had a positive cor-
relation with increasing risk score.26 A more recently developed pancreatic fistula risk
score was developed in 2019, which is an adaptation of the previously described risk
score wherein only 3 variables are required: pancreatic gland texture, main pancreatic
duct diameter, and body mass index. This scoring system was validated, and it was
found that the low-risk group had a less than 5% risk of a pancreatic fistula. The
intermediate-risk group had a 5% to 20% risk of a pancreatic fistula, and the high-
risk group had a greater than 20% risk of a pancreatic fistula.27 The clinical
applicability of these risk scores is their ease in calculating on the fly a patient’s risk
of pancreatic fistula formation and whether to leave a drain postoperatively.
From a technical standpoint, there is no one technique that has been shown to be
clearly superior in reducing pancreatic fistula. Ultimately it comes down to what the
particular surgeon feels comfortable with. One thing that has been shown to reduce

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 Complications After Pancreaticoduodenectomy 869

pancreatic fistula rates is proper antibiotic prophylaxis. When the antibiotic prophy-
laxis was changed to a second-/third-generation cephalosporin and metronidazole,
the rate of clinically relevant pancreatic fistulas was reduced from 23.4% to 6.0%.14

BILIARY COMPLICATIONS

One of the rarer complications after a pancreaticoduodenectomy is a biliary complica-

tion. These complications are mainly divided into early complications, manifested as a
bile leak, and late complications, manifested as bile duct strictures at the hepaticoje-
junostomy anastomosis. The rate of bile leaks is generally considered low at less than
5%.28,29 Owing to it being a rare complication, it is difficult to find statistically signifi-
cant risk factors, although one study found that small-diameter bile ducts (<5 mm) was
a risk factor for bile leaks. In this study, about one-half of the bile leaks sealed spon-
taneously and did not require any intervention. About one-third of these leaks required
a percutaneous drain to be placed into the biloma, and only about one-fourth required
a reintervention, either by interventional radiology or reoperation.28 Another study
found that bile leaks resolved spontaneously in about 56% of patients.29
Biliary strictures are a rare complication as well, occurring in less than 5% of pan-
creaticoduodenectomies. It is generally thought that bile leaks can result in the future
development of biliary strictures. In one study, one-third of patients with biliary stric-
tures were found to have postoperative bile leaks and the remaining patients were
found to have recurrence of their cancer.30 Another study found that biliary strictures
were more common in those who had preoperative percutaneous biliary diversion via
a transhepatic catheter, thought to be due to inflammation of the bile duct.31
In addition to general principles of performing any anastomosis, such as tension free
and ensuring a good blood supply, technical aspects that can minimize bile leaks and
strictures are to evenly space the sutures and avoid unnecessary throws into the bile
duct. The suture path should be planned well so that the bile duct is not stabbed, and if
the suture spacing is inadequate, the needle should be removed and placed in a
different spot. It is also important to get good healthy bites of the bile duct so that
the suture does not pull through and tear the bile duct.

HEMORRHAGE

Bleeding remains one of the more common complications after pancreaticoduode-

nectomies. The ISGPS has again helped us develop a grading scale and universal defi-
nition, and this helps ensure that surgeons and clinicians are on the same page when
discussing patients and reviewing the literature. There are 3 parameters that help
define postoperative hemorrhage after pancreaticoduodenectomy. The first param-
eter is onset of the bleeding, early versus late, early being defined by bleeding within
the first 24 hours of the operation and late being greater than 24 hours after the oper-
ation. Early bleeding tends to be related to inadequate hemostasis during the index
operation or an underlying coagulopathy. Late bleeding tends to result from intestinal
ulcerations, erosion of blood vessels from a pancreatic fistula, a tie becoming dis-
lodged, or development of a pseudoaneurysm. The location of the bleeding can be
grouped as being intraluminal or extraluminal. Potential intraluminal sources of
bleeding can be hemobilia from biliary stents placed preoperatively, bleeding from
enteric staple lines or anastomoses, or ulcer formation. Potential extraluminal sources
of bleeding can be raw surfaces from dissection planes or pseudoaneurysms.
Bleeding severity is classified into 2 groups. Mild hemorrhage does not have any clin-
ical impairment. Severe hemorrhage requires 4 or more units of packed red blood cells

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870 Simon

to be transfused within a 24-hour period, a hemoglobin level drop greater than 4 g/dL,
or an operation or interventional angiography for control.32
Understanding the onset, location, and severity of the hemorrhage helps the clini-
cian best treat the patient. For example, many patients are jaundiced or malnourished
preoperatively, and this can lead to them being coagulopathic. Therefore recognizing
this coagulopathy and treating with vitamin K is critical. If a patient has intraluminal
bleeding, then an endoscopy could be warranted, but if the bleeding is extraluminal
then endoscopy is unnecessary. It has been shown that pancreatic fistulae, especially
combined with a bile leak, can predispose to a gastroduodenal artery stump blowout.
Therefore, if bile is noted in the drain with a high amylase level, there should be a high
suspicion of a GDA stump.

CHYLE LEAK

Chyle leaks are another complication that the ISGPS has defined, and it has devel-
oped a classification system. The definition of a chyle leak is milky fluid output after
postoperative day 2 with a triglyceride level greater than or equal to 110 mg/dL. A
grade A chyle leak is classified as one that is not clinically relevant, meaning that it
does not prolong the hospital length of stay and improves with conservative dietary
modifications. A grade B chyle leak is one that requires one of 3 interventions, one be-
ing nasojejunal nutrition or total parental nutrition, a second being placement of a
percutaneous drain or maintenance of the surgically placed drain for longer than
planned, and a third being the use of octreotide. A grade C chyle leak is one that re-
quires invasive treatment; this includes operative exploration for the chyle leak, inten-
sive care unit admission, or interventional radiology involvement for lymphatic
embolization. If mortality occurs that is directly related to the chyle leak, this would
be classified as a grade C chyle leak.33
The occurrence of chyle leaks has been reported in various studies, ranging from as
low as 1.3% to as high as 10.4%.34,35 The clinical relevance of chyle leaks depends on
if the chyle leak is contained or if it is causing diffuse ascites. Hospital length of stay is
longer in those with chyle leaks, and of those with chyle leaks, it is longer if there is
diffuse ascites. Most importantly, though, chylous ascites has been shown to have
a lower overall survival, whereas those with contained chyle leaks have a similar over-
all survival compared with patients with no chyle leak. Risk factors for chyle leaks
include higher lymph node harvest and vascular reconstruction.34
Frequently chyle can be seen intraoperatively during the dissection, and when this
happens, the most important thing is to make an attempt at locating the source and
oversewing it. It is often easy to control with 1 or 2 interrupted sutures. Other times,
though, there is no chyle seen intraoperatively, and when patients start getting enteral
nutrition, milky chylous fluid is seen in the drains. Most chylous leaks resolve after
placing patients on a low-fat diet, in particular limiting them to medium-chain fatty
acids. According to various studies, this treatment is effective in about 75% to 85%
of patients.34,36,37 Resolution of the chyle leak is confirmed by seeing the drain output
turn serous. One can then start reintroducing fats into the patient’s diet to ensure that
the drain fluid remains serous. Once this occurs, the drain can be safely removed.

NUTRITION

Two of the main functions of the pancreas are insulin production and pancreatic
enzyme production. Taking part of the pancreas puts patients at risk of developing
diabetes mellitus and exocrine pancreatic insufficiency (EPI). Diabetes mellitus after
partial pancreatectomy is also called type 3c diabetes, or pancreatogenic diabetes,

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 Complications After Pancreaticoduodenectomy 871

and has been reported to be as high as 22% or even 37% after pancreaticoduodenec-
tomy in some studies.38,39 It is known that the risk of developing diabetes increases
with time. As one gets further and further away from their operation, their risk of devel-
oping type 3c diabetes increases. In one study by the Mayo Clinic on the development
of immediate postresection diabetes after pancreaticoduodenectomy, the investiga-
tors found that the incidence was only 4%.40 It is generally known that the incidence
of type 3c diabetes after distal pancreatectomy is higher than after pancreaticoduode-
nectomy. In studies looking at resections for chronic pancreatitis, the incidence of
new-onset diabetes after a distal pancreatectomy was 85% and only 40% after a pan-
creaticoduodenectomy.41,42 Even in patients who have normal pancreatic tissue, dia-
betes after distal pancreatectomy has been found to be as high as 60%.43 The reason
for the lower incidence after pancreaticoduodenectomies could be related to the dis-
tribution of beta islet cells, the insulin-producing cell of the pancreas. A cadaveric
study examining the islet cell concentrations throughout the pancreas found that
the head and body had similar concentrations, whereas the tail had more than 2 times
the amount of islet cells.44
EPI is found in about 36% of patients after pancreatic resections, with higher inci-
dences after pancreaticoduodenectomies compared with distal pancreatectomies.
On average, these patients developed EPI 14 months from surgery.45 This observation
stresses the importance of following these patients long term postoperatively and
screening them at every visit for steatorrhea and malabsorption to ensure that they
do not require pancreatic enzyme supplementation. Fecal elastase levels can be
checked as well to not only help diagnose these patients but also help get insurance
approval for the pancreatic enzymes. Also of note, pancreatic enzymes are broken
down by acid, and therefore proton pump inhibitors are usually required to help
improve the efficacy of the enzymes and reduce the amount of pancreatic enzymes
taken by patients. In addition, it is imperative to properly educate patients on the pur-
pose of the enzymes and the correct way to take them. Patients should be instructed
to take half of their dose with the first bite of their meal and the remainder halfway
through their meal. If they forget to take them, they should not take them after the
meal, because it is a waste of the medication. I also tell them that the purpose is to
help digest grease and fat, therefore if they are eating a particularly greasy, fatty
meal, they may need to take an extra pill or two to help them digest it properly.

SUMMARY

When the pancreaticoduodenectomy was first described and developed in the 1960s
and the 1970s, the mortality rate was as high as 25%. In subsequent years, the mor-
tality rate has been lowered significantly, and now it is thought to be around 1.5%; this
is thought to result only partially from better operative techniques and skill. Consid-
ering that the morbidity rate of pancreaticoduodenectomies remains high, nearing
50% in some studies, a more important aspect of the improvement in mortality is likely
due to better postoperative care and management of postoperative complications.46
For example, silastic drains, feeding tubes, antibiotics, and better percutaneous tech-
niques to control fluid collections and hemorrhage are imperative in taking care of
these complex patients.

CLINICS CARE POINTS

 Pancreaticoduodenectomies are a complex operation with a high morbidity rate

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872 Simon

 Having an understanding of the definitions is imperative to recognizing and treating

complications
 DGE and pancreatic fistulas are among the most common complication after
pancreaticoduodenectomies and result in the highest amount of resource use of any of
the other complications

DISCLOSURE

The author has nothing to disclose.

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