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Review
Br. J. Surg. 1990, Vol. 77, September,
968-974
PyIo rus prese rving
pancreatoduodenectomy: an
overview
Pylorus preserving pancreatoduodenectomy (PPPD) was reintroduced
I2 years ago. Since that time, over 400 patients have undergone PPPD
with approximately 41 per cent having chronic pancreatitis and
54 per cent having pancreatic and other periampullary malignancies.
Reported 5-year survivals in this latter group have been comparable to
those achieved by the classic Whipple procedure. The postoperative
mortality rate in 339 reported patients has been 3-8 per cent.
Postoperative morbidity, including delayed gastric emptying, has been
similar to that of the classic Whipple operation. However, PPPD has
been associated with fewer late problems with dumping, diarrhoea,
delayed gastric emptying (8.6 per cent), and marginal ulceration
(3.6 per cent). Moreover, most patients undergoing PPPD have been
able to return to their preoperative andpreillness weight. The additional
advantage of decreased operative time makes PPPD an attractive
alternative to the classic pancreatoduodenectomy.
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P. A. Grace*, H. A. P i t t t
and W. P. Longmire1
*Department of Surgery, Royal
College of Surgeons in Ireland,
Dublin, Ireland and ?Department
of Surgery, The Johns Hopkins
Medical Institutions, Baltimore,
Maryland, USA and $Department
of Surgery, UCLA Medical Center,
Los Angeles, California, USA
Correspondence to:
Mr H. A. Pitt, The Johns Hopkins
Hospital, 600 North Wolfe Street,
Blalock 688, Baltimore, Maryland
21205, USA
Keywords: Pancreatoduodenectomy, chronic pancreatitis, pancreatic carcinoma, arnpullary
carcinoma, distal bile duct carcinoma, duodenal carcinoma
The incidence of pancreatic cancer and periampullary tumours
has increased steadily over the last 40 years’ while chronic
pancreatitis, although an uncommon condition*, continues to
pose a major therapeutic challenge to the surgeon3. In recent
years a variety of new surgical approaches to pancreatic
resection have been developed. These approaches range from
the radical regional pancreatoduodenectomy advocated by
Fortner4 to the pylorus preserving pancreatoduodenectomy
( P P P D ) and duodenal preserving pancreatectomy popularized
by Longmire’ and Russell6, respectively. Local excision of
periampullary carcinomas has also had its advocates in recent
years’. The purpose of the present analysis is to review the
impact of PPPD on pancreatic surgery since its reintroduction
12 years ago.
Historical development
While there are several reports of pancreatoduodenal resections
from the end of the 19th and the beginning of the 20th
centuries8-”, it was not until 1935 that the modern era of
pancreatic surgery was inaugurated. In that year Whipple,
Parsons and M ~ l l e n s ’published
~
their report of the first
successful two-stage radical pancreatoduodenectomy for
periampullary carcinoma. In the first stage of the operation,
the patient underwent a gastrojejunostomy, ligation of the distal
common bile duct and cholecystogastrostomy. Subsequently,
the second part of the duodenum, the ampulla of Vater, the
adjacent head of the pancreas and the distal common bile duct
were removed, and the pancreatic stump was oversewn. Thus,
the antrum and pylorus were structurally preserved as a blind
stump, and the patency of the gastrointestinal tract was restored
by a gastroenterostomy.
advocated resection of the distal
In 1941 Trimble et
stomach with a Polya antecolic anastomosis, eliminating the
blind pyloric stump and the suture line in the duodenum, a
potential source of leakage. Whipple also advocated distal
gastrectomy and a choledochojejunostomy, and both Whipple
and Trimble independently reported successful one stage radical
968
pancreatoduodenectomy in 1941’4*’5. I n 1944 Watson16
described a pancreatoduodenectomy for carcinoma of the
ampulla of Vater in which he preserved the antrum, pylorus,
and 1 inch of duodenum. H e re-established alimentary
continuity with a duodenojejunostomy thus preserving in
functional continuity the antrum, pylorus, and first part of the
duodenum. Watson believed that preservation of the stomach
would lead to better digestion and that a duodenojejunostomy
would prevent anastomotic ulceration. To Watson, therefore,
must go the credit for describing the first PPPD. Watson’s
report, however, was forgotten, and gastric resection with or
without vagotomy became an integral part of the standard
The rationale for inclusion of
‘Whipple’ operation’ ’-’O.
gastrectomy and vagotomy has been to prevent marginal
ulceration and to provide adequate margins when resecting
tumours. This operation continues to be the most frequently
performed operation for resectable lesions in the head of the
pancreas.
In 1978 Traverso and Longmire5 revived the idea of
preserving the pylorus during pancreatoduodenectomy. They
reported two patients in whom the stomach, pylorus, and first
part of the duodenum were preserved and alimentary tract
continuity was re-established by end-to-side duodenojejunostomy. These authors, like Watson, reasoned that preservation
of the stomach and pylorus would eliminate the complications
of a reduced gastric reservoir and improve gastrointestinal
function. They also believed that preserving the pylorus would
prevent exposure of the jejunum to excessive amounts of acid,
thereby reducing the incidence of jejunal ulceration. Furthermore, they argued that resection of the distal stomach, pylorus,
and proximal duodenum was unnecessary in the management
of benign disease’.
Indications and survival
Traverso and Longmire’ initially performed P P P D in t w o
patients. One had chronic pancreatitis with associated
pseudocyst formation in the head of the pancreas while the
0007- 1323/90/090968- 07
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0 1990 Butterworth-Heinemann
Ltd
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Pylorous preserving pancreatoduodenectomy: P. A. Grace et al.
Table 1 Indications Jor pyrfous preserving pancreatoduodenectomy
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Authors (reference)
WatsonI6
Gall er a[.”
Mosca et
Flautner et a / . 2 3
Warshaw and TorchianaZ4
Pearlman et a[.25
Itani er a/.26
Crist et d Z 7
Eck and Murry”
Kim et
Braasch et a1.30-33
Williamson and Cooper34-36
Longmire et a/.5.3740
Hunt and McLean4’
McAfee et
Sharp et
Year
No. of
patients
Chronic
pancreatitis
Malignancy
Other
1944
1
0
1
1982
1984
18
30
18
0
0
0
0
37
0
1985
1986
1986
8
8
37
4
1
22
1985
I
1987
14
5
14
0
0
0
I
0
6
7
4
5
1987
2
1987
13
0
0
6
1988
126
41
4
82
1988
1988
1989
31
46
16
17
13
13
28
5
9
1989
1989
33
6
12
0
18
6
Total
394
163 (41)
Values in parentheses are percentages
second had a small localized carcinoma of the third part of the
duodenum. Over 160 patients have since undergone PPPD
Braasch and his
for chronic pancreatitis (Table
colleague^^^-^^ at the Lahey Clinic advocate the pylorus
preserving operation in all resections of the right side of the
pancreas for chronic pancreatitis except those patients with
duodenal ulcer disease. However, the presence of pancreatitis
throughout the gland requiring total pancreatectomy has also
been combined with PPPD24.38.The advantages of pylorus
preservation in these patients are that the patient can eat normal
sized meals, and the absence of gastrectomy diminishes the risk
of the dumping syndrome3.
Doubts have been raised as to the advisability of performing
the pylorus preserving operation for malignant disease in the
periampullary area, as the field of resection may be reduced
and survival thereby c ~ m p r o m i s e d ~Moossa4’
~ * ~ ~ . has argued
that the pylorus preservation procedure is not applicable to
cancer of the head of the pancreas or distal common bile duct
tumours since it may compromise the only chance of cure in
these patients. Sharp and his colleagues43 have also reported
tumour recurrence at the duodenal suture line. However,
Newman and associates30 have observed that the other
resection margins in pancreatoduodenectomy are much closer
to the tumour than the duodenum and antrum. Performing
frozen section of the duodenal resection margin should also
minimize this problem. Therefore, leaving the antrum, pylorus,
and first few centimetres of the duodenum is unlikely to
compromise the field of resection. Moreover, several recent
reports contain details of patients who underwent PPPD for a
variety of periampullary malignant lesions including ductal
pancreatic carcinoma with excellent long-term
A total of 213 pancreatoduodenectomies have now been
reported for malignant periampullary disease (Table I ) .
Braasch and associate^^^^^^ have reported actuarial 5 year
survival rates of 65 per cent for ampullary adenocarcinoma,
45 per cent for bile duct carcinoma, and 20 per cent for
adenocarcinoma of the head of the pancreas following PPPD.
These figures compare favourably with published survival rates
following the standard Whipple resection: 37 per cent46 to
60 per cent47 for ampullary carcinoma; 17 per cent46 to
30 per cent3’ for carcinoma of the distal common bile duct; and
6 per ~ e n t to~ 18~per- centz7
~ ~ for pancreatic adenocarcinoma.
In a previous analysis from the University of California at
Los Angeles, the present authors compared survival in a group
Br. J. Surg., Vol. 77, No. 9, September 1990
2
213 (54)
0
3
3
1
0
zy
18 (5)
of 26 patients with histologically proven adenocarcinoma of
the head of the pancreas who were treated with either a PPPD
( n = 13) or a classical Whipple resection ( n = 13)39. The two
groups of patients were comparable in terms of age, sex,
preoperative laboratory data, and tumour staging. The
actuarial survival rate was 25 per cent at 5 years for the pylorus
preserving group compared with 12 per cent at 3 years for the
classic Whipple group. Thus, patient survival appears not to
be compromised following PPPD for adenocarcinoma of the
head of the pancreas. We, therefore, agree with Braasch and
co-authors who advocate PPPD in all patients with pancreatic
and periampullary tumours except those cancers of the
duodenum or bile duct that are in close proximity to the first
centimetre of the d u o d e n ~ m ~ ~ . ~ ~ .
Operative technique
Adequate exposure is essential for assessment of resectability
of the pancreas and subsequent pancreatoduodenectomy. The
head of the pancreas is best approached through a right
subcostal incision. This incision can easily be converted to a
bilateral subcostal incision if a resection is to be undertaken.
In a thin patient with a narrow costal angle, a midline upper
abdominal incision also provides good exposure. In a patient
with malignant disease, a full and comprehensive laparotomy
is performed initially to detect metastases in the liver, lymph
nodes, peritoneum, or omentum. A Kocher manoeuvre is
performed and the head of the pancreas evaluated for size and
location of the primary lesion. Invasion of contiguous structures
such as the portal or superior mesenteric veins, the superior
mesenteric artery, and the common hepatic artery can now also
be assessed.
If a preoperative histological diagnosis has not been made,
biopsy of the primary lesion and any lymph nodes can be
undertaken. Biopsy material can be obtained by open scalpel
biopsy of any superficial lesion, transduodenal Tru-CutQneedle
(Travenol Laboratories Inc., Deerfield, Illinois, USA) biopsy
of the pancreatic mass or fine needle aspiration cytology
of the lesion. The common duct may also be opened and
curettage biopsy material obtained from the distal common
bile duct. Controversy exists, however, as to whether
histological proof of carcinoma of the head of the pancreas is
necessary before embarking on pancreatoduodenectomy.
Longmire and Traverse" have suggested that if the possibility
969
Pylorous preserving pancreatoduodenectomy: P. A. Grace et al.
of a resection for benign disease has been discussed with the
patient, it is acceptable to perform pancreatectomy without
tissue diagnosis. Thus, a potentially curable occult lesion is not
overlooked. Others have argued that if pancreatitis is severe
enough to be confused with malignancy, pancreatectomy is
probably indicated in any case4’.
An assessment of resectability is now undertaken. The
dissection is carried along the third part of the duodenum to
expose the superior mesenteric vein at the point where it crosses
the duodenum and passes under the neck of the pancreas. A
critical determination of resectability is the ability to separate
the portal and superior mesenteric veins from the adjacent
pancreas. Major tributaries usually do not enter the portal vein
on its ventral surface behind the pancreatic neck, and it should
be possible to develop a plane between these two structures. If
this manoeuvre can be achieved, resection is usually feasible.
An intact neurovascular supply to the pylorus and the first
part of the duodenum is essential for the success of the pylorus
preserving operation. The right gastric artery is preserved, and
the gastroduodenal artery is isolated and divided at the junction
with the hepatic artery. The gastroepiploic vessels along the
entire greater curvature of the stomach are carefully preserved
as is the vagal innervation of the pylorus and antrum. The right
gastroepiploic artery is divided at its origin from the anterior
pancreaticoduodenal artery on the head of the pancreas
(Figure I ) .
The common hepatic duct should be divided just proximal
to the cystic duct and a cholecystectomy performed. The
duodenum is divided 2 cm distal to the pylorus. Unless a total
pancreatectomy is being undertaken, the pancreas should be
transected across the surgical neck. Transfixion sutures placed
along the upper and lower margins of the pancreas on either
side of the line of transection will reduce bleeding from the cut
surface of the pancreas. Division of the small bowel distal to
the ligament of Treitz will facilitate dissection of the uncinate
process. Division of arterial and venous branches close to the
jejunum at the ligament will help to avoid injury to the superior
mesenteric artery. Bringing the divided jejunum to the patient’s
right at this stage is also often a helpful manoeuvre. The
uncinate process should now be carefully dissected from behind
the superior mesenteric vein. Several small veins in this region
must be individually ligated. The uncinate process may now
be freed completely by dividing the remaining retroperitoneal
tissues and branches to the superior mesenteric artery.
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Choledochojejunostomy
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Hepatic a r t e r y
i
‘Duodenojejunostomy
Paediatric feeding t u b e
Figure 2 End-to-side duodenojejunostomy with the pancreaticojejunostomy and choledochoduodenostomy pluced proximally. A long
paediatric feeding tube splints the pancreatojejunal anastomosis. (from
Grace et
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Coeliac a r t e r
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Reconstructive methods
Reconstruction of the alimentary tract is now undertaken. Two
different methods of duodenojejunostomy have been described.
Watson performed an end-to-end duodenojejunostomy in his
operation 16, a technique also favoured by Flautner and
colleague^^^, while Traverso and Longmire’ described an
end-to-side anastomosis of the duodenal segment to a loop of
jejunum. A variety of methods of managing the pancreatic
stump have also been advocated. These include ligation of the
pancreatic stumpL6,pancreatic duct occlu~ion’~,
pancreaticojejunostomy’, and pancreaticoga~trostomy~~-~~.
Pancreatic
duct ligation is not to be recommended as it leads to a high
incidence of fistula f ~ r m a t i o n ’ ~ . ’Pancreatic
~.
duct occlusion
also has the long-term problem of assuring pancreatic exocrine
insufficiency and the need for enzyme replacement.
To help neutralize gastric acid, the pancreaticojejunostomy
and the choledochojejunostomy are placed proximal to the
duodenojejunostomy. Placing the pancreaticojejunostomy
proximal to the choledochojejunostomy also facilitates
reoperation if resection is required for a leak at the
pancreaticojejunostomy. A number of methods of pancreaticojejunostomy are available. If the pancreas is soft with a small
pancreatic duct, as is often the case with malignant disease, the
transected pancreatic stump can be invaginated into the
proximal jejunum. This procedure is called the ‘dunking’
pancreaticojejunostomy and was originally described by
Desjardins in 19079. However, if the duct is dilated and
thickened from chronic pancreatitis, a mucosa-to-mucosa
anastomosis between the pancreatic duct and the jejunum
should be performed (Figure 2)54. Either an end-to-side or
lateral pancreaticojejunostomy as described by Traverso and
Longmire’ in their patient with pancreatitis can be undertaken.
Stenting this anastomosis may reduce the incidence of
postoperative pancreatic fistula38. Braasch and co-workers
have indicated that in patients who d o not have chronic
pancreatitis long-term patency of the pancreatic anastomosis
may be better following the dunking procedure than after the
end-to-side anastomosis3I .
Recently, a number of authors have advocated pancreatogastrostomy as an ideal complement to PPPD for chronic
p a n ~ r e a t i t i s ~ ~ ~ Flautner
”~”.
and his colleagues23 argue that
pancreatogastrostomy is technically easier than pancreatojejunostomy and that during the postoperative period the
anastomosis may be easily examined by endoscopy or
radiology. Furthermore, the alimentary tract is restored so that
a blind intestinal segment does not remain. Recent evidence
also suggests that pancreatogastrostomy may give better relief
,
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gastroepiploic
aRight
rtery divided
A n t e r i o r a n d p o s t e r i o r pancreaticoduodenal a r t e r i e s
Figure 1 Preseming the blood supply to the pylorus. The right gastric
artery is preserved. The gustroduodenal artery is divided at its junction
ivith the hepatic artery. The right gastroepiploic artery is dioided at its
origin ,from the anterior pancreatoduodenal artery preserving the
gastroepiploic vessels along the greater curvature of‘ the stomach.
(from Grace et
970
Br. J. Surg.. Vol. 77, No. 9. September 1990
Pylorous preserving pancreatoduodenectorny: P. A. Grace e t al.
of pain than pancreatojejunostomy in patients with chronic
p a n ~ r e a t i t i s ~This
~ . procedure has the significant potential
disadvantage, however, of leading to both a pancreatic and
gastric fistula when an anastomotic leak occurs. Whenever
possible, a small plastic catheter should be placed into the
pancreatic duct to act as a splint for the pancreatic anastomosis.
An end-to-side choledochojejunostomy is then created. Soft,
closed suction drains are placed adjacent to the pancreatic and
biliary anastomoses before closing the abdomen.
z
Hopkins also failed to observe any difference in the incidence
of delayed gastric emptying between patients undergoing the
pylorus preserving procedure or partial gastric resection (29
uersus 28 per cent)27.Similarly, McAfee et al.42from the Mayo
Clinic found no differences between the PPPD and the classic
Whipple operation with respect to mean days of nasogastric
suction (7.6 uersus 7.9) or percentage of patients with early
gastric stasis (28 uersus 33 per cent). Moreover, Hunt and
McLean4’ have suggested that delayed gastric emptying in the
early postoperative period is usually associated with another
intra-abdominal complication. In the authors’ experience early
Postoperative mortality
delayed gastric emptying is most often associated with a leak
In recent years, a substantial improvement in operative
at the pancreatojejunal anastomosis or with postoperative
mortality has been reported following pancreatoduodenectomy .
pancreatitis.
Twenty-two years ago,
was able to report 41
Several investigators have studied gastric function in detail
consecutive Whipple procedures without mortality. However,
following pylorus preserving pancreatectomy in both humans
his experience was unique as contemporary reports recorded
and experimental animals. Traverso and Longmire3’, in a
operative mortality rates of 20-40 per cent57-59. During the
detailed study of gastric function using pyloric fluoroscopy and
last decade, operative mortality rates decreased to 1&12 per
gastric barium emptying, found normal gastric emptying in all
cent in tertiary referral centre^^^,^^.^'. However, Herman in
eight patients studied 2 to 12 months following pancreatic
197862, combining the results of 1005 Whipple procedures
resection. Braasch and colleagues3 using isotopes to measure
performed by 18 surgeons, reported an overall surgical
gastric emptying of liquids and solids found no differences
mortality rate of 20 per cent. Current reports suggest that
between five control subjects and five patients following PPPD.
pancreatoduodenectomy carries an operative mortality rate of
Patti and c o - ~ o r k e r sin~ ~San Francisco measured gastric
less than 5 per ~ e n t ~ ~ PPPD
* ~ ~ is. ~associated
~ . ~ ~with
.
emptying and small bowel transit in ten patients following
comparable operative mortality rates. Among 339 patients
PPPD. They found that the rate of gastric emptying was normal
in the recent literature, 13 perioperative deaths were
in six patients, faster than normal in three, and abnormally
reported for an operative mortality rate of 3.8 per cent
slow in a single patient who was subsequently found to have
(Table 2)21-28.g0-35*41-43.
However, only two of the deaths
diffuse carcinomatosis. Small bowel transit was found to be
were procedure related. One patient died following dehiscence
increased in seven patients, which Patti and his associates
of the duodenojejunal anastomosis” while the second patient
attributed to loss of exposure of the duodenum to food.
died following a pancreatic fistula34.Furthermore, the reported
Recent studies by Fink et al?’ by Hunt and McLean4’, and
incidence of pancreatic f i s t ~ l a ~ ~biliary
- ~ ~f .i ~ t~u l. a~~~’and
.,~ ~ , by Cooper et a1.66 confirm that the majority of patients have
enteric fistula” following PPPD is in the same range as after
normal gastric emptying after PPPD. In comparison with
the classic Whipple procedure. Moreover, these reports indicate
patients undergoing the classic Whipple procedure, Cooper et
that PPPD is a safe operation carrying with it a low operative
a1.66found no significant differences. In the study by Fink and
mortality.
his ~ o l l e a g u e s gastric
~ ~ , emptying of liquids was normal after
PPPD but delayed after the standard Whipple. Thus, of 58
patients without recurrent cancer who have had gastric
Gastric and small bowel function
emptying studies many months after surgery, only five
One of the concerns expressed about the pylorus preserving
(9 per cent) have had delayedemptying (Table 2)31*37.40*41.65.66.
operation has been whether the stomach would empty
Itani and colleagues67 studied the effects of duodenosatisfactorily following the procedure. In reviewing the
jejunostomy on gastric emptying and on gastric motility in
collected experience of 284 patients, transient delay in gastric
dogs. These investigators found no significant difference in
emptying was found to occur in 27.1 per cent of patients
gastric emptying in either control or duodenojejunostomy
animals during the 3-month period of observation. Similarly,
(Table 2)22-24*27,30*31*34-38.39*41.42,
Braasch and his colleagues3’
gastric myoelectric activity was unaltered by duodenonoted that 50 per cent of their patients required gastric suction
for more than 7 days. Similarly, Warshaw and T ~ r c h i a n a ~ ~ jejunostomy. PPPD does not remove the natural duodenal
pacemaker which is located approximately 0.5 cm distal to the
observed a significant delay in achieving full diet in patients
pylorus68. Altered small bowel motility has been demonstrated
following the pylorus preserving procedure compared with the
in patients following the classic pancreatodu~denectomy~~.
classical Whipple procedure (16 days uersus 9.8 days). Mosca
However, dumping and diarrhoea have not been long-term
and his colleagues22 reported the resumption of normal
problems following PPPD.
gastrojejunal emptying around the tenth postoperative day,
Despite normal gastric myoelectric activity, Itani and
while 8 days was the longest period of nasogastric aspiration
colleagues67 observed profound alterations in proximal small
in Williamson and Cooper’s e ~ p e r i e n c e ~ ~ .
bowel myoelectric activity following duodenojejunostomy in
In a previous analysis, however, the present authors found
dogs. Specifically, they observed a significant decrease in
that postoperative nasogastric intubation was required for a
pacesetter potential frequency in the bowel distal to the site of
similar period in both pylorus preserving (6.7 days) and classical
duodenal transection. The physiology of gastrointestinal
Whipple (7.7 days) patientsg8. A recent study from Johns
motility following PPPD remains to be completely elucidated.
The role of hormones, gut peptides, and neurological factors
Table 2 Postoperative mortality and morbidity rates
in the regulation of gastrointestinal motility following
pancreatoduodenectomy needs further study. The evidence to
No. of
date supports the view that in the majority of patients no
patients
Total
significant long-term alterations in upper gastrointestinal
Postoperative mortality rate
13
339 (3.8)
motility occur following PPPD. Although delayed gastric
emptying may be seen in a quarter of the patients in the early
Delayed gastric emptying rate
postoperative period, this problem is often related to a
77
284 (27.1)
Postoperative
pancreatic fistula or pancreatitis.
Long-term
5
58 (9)
A number of investigators have observed enterogastric reflux
Marginal ulceration rate
12
331 (3.6)
in some patients following PPPD. Braasch et aL3’ using 99mTc
bound to iminodiacetic acid calculated an enterogastric reflux
Values in parentheses are percentages
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Br. J. Surg., Vol. 77, No. 9, September 1990
971
Pylorous preserving pancreatoduodenectomy: P. A. Grace et al.
index which reflected the percentage of pancreatobiliary and
jejunal contents that reflux into the stomach over a period
following injection of the isotope. Although two of five patients
showed evidence of reflux, they noted a wide divergence of
reflux values following pyloric preservation. The other three
patients studied had reflux curves similar to normal controls.
Mosca and his colleagues2’ in an analysis of 14 patients
post-pylorus preservation recorded biliogastric reflux in six
patients. However, in only two patients was reflux marked and
prolonged. Cooper et ~ 1 . ~ ‘have also documented that
enterogastric reflux is more common after the classic Whipple
procedure than after PPPD. B r a a ~ c hhas
~ ~even suggested that
preservation of the pylorus by preventing alkaline reflux and
antral stimulation may prevent peptic ulcer formation.
However, the significance of reflux in patients following pylorus
preservation is difficult to determine as it has been postulated
that duodenogastric reflux is a physiological phenomenon in
man”. Moreover, Fink and associates4’ found no mucosal
lesions in their P P P D patients who underwent postoperative
endoscopy.
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marginal ulceration demonstrated. Similarly, neither Flautner
and his associates23, Perlman and his colleague^^^, nor Kim
et a/.29reported marginal ulceration in a total of 60 patients.
Crist and colleagues2’ reported a single case of upper
gastrointestinal bleeding following PPPD among 14 patients
(7 per cent). Warshaw and TorchianaZ4observed a single case
ofjejunal ulceration in their series ofeight patients (12 per cent).
This patient required antrectomy and vagotomy. McAfee et
a/.4’ reported marginal ulceration in four of 31 patients
(13 per cent). Hunt and McLean41 have reported the highest
incidence of marginal ulceration with three of 16 patients
(19 per cent) developing this problem.
Thus, of 331 patients who have undergone PPPD, twelve
(3.6 per cent) have had postoperative problems suggestive of
marginal ulceration (Table 2)22-2 7 . 2 9 . 3 3 . 4 0 . The incidence of
this problem has ranged from zero to 19 per cent which is in
the same range as has been reported for the classic
pancreatoduodenectomy which includes a vagotomy. Moreover,
most patients with marginal ulceration after P P P D have been
easily controlled with medical management.
A number of authors have studied the effects of pancreatic
resection on acid and gastrin production. Traverso and
Longmire3’ studied basal and stimulated acid output in eight
patients at a mean of six months following PPPD. They
observed low-normal basal (0-4.1 mmol/h) and stimulated
(0.1-224 mmol/h) acid production. Pearlman and his associates2’
also reported similar findings. Pearlman and associates reported
a variable stimulated gastrin response after P P P D but persistent
hypergastrinaemia was not seen28. Sudo and colleagues’’
analysed gastrin production before and after a standard
Whipple resection. They found that both fasting and stimulated
gastrin levels were reduced following pancreatoduodenectomy.
Takuda and associate^'^ compared 20 patients with P P P D , 27
patients with the classic Whipple procedure, and eight healthy
controls. They found that postprandial gastrin and secretin
were normal after P P P D but significantly diminished after the
classic Whipple. Similarly, Kim et a/.29found that serum gastrin
and gastric acid were normal after their modification of the
P P P D and decreased with the classic Whipple operation. Thus,
both experimental and clinical evidence suggest that the PPPD
is not an ulcerogenic procedure.
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Marginal ulceration
Marginal ulceration has posed a considerable problem
following classic pancreatoduodenectomy. Owens in 1948”
reported three patients with peptic ulcer following Whipple
operations and advised that the gastroenterostomy should be
placed distal to the pancreatic and biliary anastomoses. Ten
years later, Porter reported three marginal ulcers which
occurred despite distal placement of the gastroenter~stomy’~.
He advocated hemigastrectomy for prevention of the problem
while Elliot73 argued that pancreatoduodenectomy inevitably
led to gastric hyperacidity unless an antrectomy was performed.
Grant and van Heerden” in an analysis of 297 patients who
had undergone pancreatoduodenal resection at the Mayo Clinic
observed anastomotic ulceration in 18 patients (6 per cent) of
whom seven had undergone total pancreatectomy. These
authors observed that total pancreatectomy was more
ulcerogenic than a Whipple procedure and that a 50 per cent
gastric resection was inadequate to prevent marginal ulceration.
In an attempt to reduce the incidence of anastomotic ulceration,
Scott and his colleague^'^ advocated truncal vagotomy with
pancreatoduodenectomy. In an analysis of 41 pancreatoduodenectomies, they observed anastomotic ulceration in
36 per cent of patients without vagotomy compared with no
ulceration in patients who had undergone vagotomy. However,
Walsh and associate^'^ found that antrectomy alone was
associated with a marginal ulcer rate of 12 per cent compared
with 9 per cent when vagotomy was added. These findings have
since been substantiated by Grace and associates38 and Crist
and colleagues27 who found that the incidence of marginal
ulceration was similar for antrectomy alone or antrectomy plus
vagotomy.
Watson’‘ and Traverso and Longmire’ believed that
preserving the pylorus during pancreatic resection would
decrease the postoperative incidence of jejunal ulceration. The
clinical experience to date would support their hypothesis.
Braasch and associates33 in their series of 126 patients reported
six patients ( 5 per cent) in whom the diagnosis of marginal
ulceration was suggested either radiologically o r by endoscopy.
Four patients were managed successfully by medical means
while two underwent operation. Grace et ul. observed no upper
gastrointestinal bleeding in the immediate postoperative period
in 39 patients following PPPD. but two patients ( 5 per cent)
presented at 16 and 61 months after operation. One was found
to have a marginal ulcer which required gastric resection while
the other had non-specific upper gastrointestinal bleeding
probably related to portal hypertension. In a later follow-up
of this series by Fink et a/.40 two of 46 patients (5 per cent)
had developed marginal ulceration.
All 30 patients in the series by Mosca er a / . 2 2underwent
upper gastrointestinal endoscopy. Five patients had moderate
inflammation of the antral mucosa but in no patient was
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Postoperative nutrition
One of the theoretical advantages of P P P D is improved
nutrition. Most patients who undergo the classic Whipple
procedure are unable to achieve their preoperative weight3’.
However, Braasch and his colleague^^^^'^ have documented
that patients undergoing P P P D regained a median of 101 per
cent of preoperative weight and 95 per cent of preillness weight.
Fink and his associates4’ also studied serum levels of vitamins A
and B , 2 . iron, total iron-binding capacity, carotene. and folate
in both P P P D and classic Whipple patients. N o differences
were noted between the two groups, and vitamins A, B I Zand
folate levels were normal in all patients. Of six patients
undergoing PPPD, serum iron levels were low in two, total
iron-binding capacity was increased in three, and serum
carotene levels were low in five. However, similar abnormalities
were observed in classic Whipple patients. Thus, current data
suggest that weight and the majority of nutritional parameters
are normal after PPPD.
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Conclusion
P P P D represents one of the most significant recent advances
in pancreatic surgery. The operation can be performed with a
very low mortality and morbidity and is technically easier than
the standard Whipple resection. Gastric emptying may be
prolonged transiently in the immediate postoperative period.
However, this complication is easily managed and is not a
long-term problem. In addition, P P P D has a lower incidence
of enterogastric reflux. dumping, and diarrhoea when compared
with the classic Whipple procedure. Clinical and experimental
zyxwvutsrqpo
972
Br. J. Surg., Vol. 77, No. 9, September 1990
zyx
P y l o r o u s preserving p a n c r e a t o d u o d e n e c t o m y : P. A. G r a c e et al.
evidence has substantiated the hypothesis that preservation of
the pylorus would reduce the incidence of marginal ulceration
following pancreatectomy. Moreover, patients undergoing
PPPD are m o re likely t o regain their preoperative a n d preillness
weight.
Pancreatoduodenectomy with preservation of the pylorus
may be the procedure of choice for chronic pancreatitis
involving the head of the pancreas. Initial concerns a b o ut the
use of this procedure in malignant disease have n o t been born
out, a nd its use should be considered for curative or palliative
resections of pancreatic and periampullary malignancies.
Surgery is the only method of treatment which provides the
chance of cure in patients with such pancreatic an d
periampullary neoplasms, and may also provide the best
palliation in terms of survival and quality of life. Thus, we
believe that PPPD has a significant role to play in the
management of patients with pancreatic a n d periampullary
neoplasms.
24.
25.
26.
27.
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28.
29.
30.
31.
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76.
Paper accepted 9 April 1990
Br. J. Surg., Vol. 77, No. 9. September 1990