Pylorus-Preserving Whipple Resection

for Pancreatic Cancer

Is It Any Better?
Ameet G. Patel, FRCS; Mark T. Toyama, MD; Amy M. Kusske, MD;
Pam Alexander, RN; Stanley W. Ashley, MD; Howard A. Reber, MD

Objective: To compare the short- and long-term morbid-
ity and mortality rates ofthe standard Whipple pancreatoduo-
denectomy (SW) and its pylorus-preserving modification
(PPW) in patients with malignant periampullary disease.
Design: Retrospective medical record review and qual-
ity of life assessment by telephone interview.
Setting: University medical center.
Study Participants: Sixty-seven patients who under-
went pancreatoduodenectomy (52 SW and 15 PPW) from
June 1988 to January 1994.
Intervention: The SW and PPW.
Main Outcome Measures: Operative features and
short- and long-term complications were analyzed with
respect to the type and stage of cancer and the kind of
Results: The operative mortality rate for all patients
who had a pancreatic resection was 1.5%. The diag-
noses in the PPW vs SW groups were pancreatic can-
cer (four vs 27 patients), ampullary cancer (six vs
seven patients), duodenal cancer (zero vs six patients),
and bile duct cancer (five vs one patient). Operative
mortality rates (0% vs 1.55%) and operative times (2
minutes longer for SW) were similar. Delayed gastric
emptying (61% vs 41%) was more common in the
PPW group, resulting in a longer hospitalization (24
vs 18 days) and a greater cost in the PPW group
(P=.04). In the PPW group, a mean of five lymph
nodes was removed compared with 10 in the SW
group (P=.04).
Conclusions: The data provided no evidence of any ad-
vantage for the PPW in patients with malignant periam-
pullary tumors. We continue to advocate the SW for pan-
creatic cancer.

pancreatic resection. Mean follow-up was 32 months

(range, 1 to 5 years). (Arch Surg. 1995;130:838-843)

From the Department of
Surgery, Sepulveda Veterans
Affairs Medical Center,
Los Angeles, Calif, and the
Department of Surgery,
University of California,
Los Angeles, School of
Medicine.
The
British surgeon Wat¬
son1 firstperformed a py¬
lorus-preserving pancreato-
duodenectomy (PPW) in a
patient with carcinoma of
the ampulla of Vater and reported the case
in 1944. The operation did not receive fur¬
ther attention until 1977, when Traverso
and Longmire2 published their experience
with the procedure in two patients with
chronic pancreatitis. They hoped that the
incidence of marginal ulcer, which was as
high as 20% following the standard Whipple
pancreatoduodenectomy (SW), would be
less if the entire stomach and pylorus were
preserved. Although they originally in¬
tended that the operation only be used in
patients with benign disease, it has since
been applied at the University of Califor¬
nia, Los Angeles, (UCLA) and other insti¬
tutions to those with periampullary malig¬
4
nant neoplasms as well.3 Because of our
concern about the use of PPW in patients
with cancer, we retrospectively reviewed the
recent UCLA experience with the two op¬
erations for malignant disease.
RESULTS
Fifty-two patients underwent the SW; 15 pa¬
tients underwent the PPW. Pancreatoduo-
denectomy was performed in 43 patients
(64%) for ductal pancreatic adenocarci-
noma and in 24 patients (36%) for other as¬
sorted periampullary cancers (distal bile
duct [n=5], ampulla of Vater [n=ll], and
duodenum [n=8]). The median age of the
SW group was 63 years (range, 25-85 years) ;
there were 28 men (54%) and 24 women
(46%). The median age of the PPW group
See Patients and Methods
on next
page

Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013

 Table 1. Cases of Each Tumor According to Stage
PATIENTS AND METHODS
Pancreatoduodenectomy
r
We reviewed the medical records of 67 Standard Pylorus-Preserving
patients who Whipple Whipple
underwent pancreatoduodenectomy for malignant pan¬ Cancer Stage
creatic and periampullary neoplasms from June 1988
(11=52) (n=15)
to January 1994 at the UCLA Medical Center. Demo¬
Pancreatic cancer*
I 16
graphic information and data concerning clinical pre¬ II 3
sentation, pathological findings, the operative proce¬ III 18
dure, perioperative mortality and morbidity, and IV 0
hospital charges were examined. Gastric function was Total 37
considered delayed if patients were not tolerating oral
fluids by the seventh postoperative day. We arbi¬
Ampullary cancerf
I 6
trarily defined delayed gastric emptying in this man¬ II 0
ner because it is our impression that most patients have III 1
had their nasogastric tube removed and are taking liq¬ IV 0
uids orally by that time. Pathological staging was car¬ Total 7
ried out using the International Union Against Can¬ Bile duct cancerf
cer (UICC) classification for pancreatic cancer3 and I 0
guidelines from the American Joint Committee on Can¬ II 0
cer staging for the other neoplasms.6 Follow-up data III 1
about quality of life were obtained by telephone con¬ IV 0
tact with all living patients in January 1995. Fol¬ Total 1
Duodenal cancerf
low-up was complete, except for two patients in the I 2
SW group and three in the PPW group who were ei¬
II 1
ther unavailable or unwilling to answer any ques¬
III 4
tions. Quality of life and pain assessment scores were
IV 0
based on a questionnaire similar to that developed by Total 7
the Memorial Sloan-Kettering Cancer Center and other
standard psychological testing measures.7 All results
were expressed as mean±SEM, unless otherwise stated.
* Defined
by International Union Against Cancer, in Hermanek et al5
^Defined by American Joint Committee on Cancer, in Beahrs et al6
Statistical analysis was performed using the Mann Whit¬
ney rank-sum test, \2 analysis, and Fisher's exact test.
margins, or tumor diameter in patients with pancreatic and
periampullary tumors undergoing each of the two opera¬
tions (data not shown). In the patients who underwent
was 61 years (range, 38-85 years); there were six men (40%) PPW, there was no instance in which the resection mar¬
and nine women (60%). gin of the duodenum was involved with tumor.
Preoperative laboratory data similar in both
were The complications of pancreatoduodenectomy are
groups. Both SW and PPW were performed by the same shown in Table 2. One patient died in the series, a 64-
group of surgeons. The choice of operation in each case year-old woman with extensive duodenal and retroperi-
was based on the individual preference of the operating toneal lymphoma who underwent SW. The clinical pic¬
surgeon. A total of 14 surgeons performed all the opera¬ ture was that of sepsis and respiratory failure, although
tions, but the majority (54) were done by four individu¬ infection was never proven. Reoperation was not under¬
als, and one of us (H.A.R.) performed 29 resections. taken and there was no autopsy. Thus, the operative mor¬
The cancers were staged according to currently ac¬ tality rate for all patients who underwent pancreatic
cepted conventions. According to the UICC classification resection was 1.5%.
for pancreatic cancers,5 stage I tumors are confined to the In the SW and PPW groups, there were no differ¬
pancreas and do not invade adjacent structures or other ences in operative time (508±22 vs 506±31 minutes, re¬

organs. Stage II tumors invade adjacent structures (eg, su¬
perior mesenteric-portal vein, superior mesenteric artery,
colon, and spleen). Stage III tumors are those with lymph
node métastases. There were no stage IV tumors (distant
métastases), since such extensive disease precluded a re¬
section. The cancers of the bile duct, ampulla of Vater, and
duodenum were classified according to the American Joint
Committee on Cancer staging guidelines (Table 1 ).6
The characteristics of the two groups of patients re¬
vealed that there were no significant differences in age, sex,
ethnicity, size, and total number of pancreatic and peri-
ampullary tumors. There were no significant differences
noted in the results of pathological staging, degree of tu¬
mor differentiation, involvement by tumor of the resected
spectively), estimated blood loss (799±96 vs 701 ±132
mL, respectively), and total number of units of blood trans¬
fused (1.28±0.24vs 1.5±0.32U, respectively). The only
significant differences in morbidity between the two pro¬
cedures were the pancreatic fistula rate, which was higher
in the PPW group (27% vs 6%; P=.04), and the inci¬
dence of delayed gastric emptying, which was 61% in the
PPW group compared with 41% in the SW group (Table
2) (P=.03). As a result, the PPW group had a signifi¬
cantly prolonged hospital stay (21.3 vs 15.4 days; P=.04).
The number of nodes removed with the specimen was
greater in the patients who underwent the SW (10 vs 5
nodes; P=.04).
The total charges billed to the patients associated

Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013


Table 2. Complications of Pancreatoduodenecîomy
Pancreatoduodenectomy
Standard Pylorus-Preserving
Whipple Whipple
Complications (n=52)
Pancreatic fistula 3 (6)f
Bile fistula 1 (2)
Delayed gastric emptyingf 21 (41 )f
Wound infection 3(6)
Hemorrhage 3 (6)
Intra-abdominal sepsis 3(6)
Adult respiratory
distress syndrome 3 (6)
*
Values are given as number (percent) of patients.
f P<. 05, by Fisher's exact test.
XDefined as failure to tolerate oral fluids by the seventh postoperative
day.
with the hospitalization (day of operation to day of dis¬
charge) for the two operations was $59 789±$5163 (for
SW) vs $85 811±$7455 (for PPW) (P=.04).
Quality of life assessment in all patients available for
interview (n=23) in January 1995 (mean follow-up, 32
months) showed no differences between the SW (n=21)
and PPW (n=2) groups (score, 8.0±0.3 vs 9±0.6, re¬
spectively; best quality of life score, 10). The SW and PPW
groups regained 92% and 96% of their preoperative
weight, respectively. One patient in the SW group had
pain; none of the patients in the PPW group did. How¬
ever, the small number of patients in the PPW group avail¬
able for quality of life assessment prevented statistically
significant comparisons between the two groups.
In the United States, about 28 000 new cases of pancre¬
atic cancer are diagnosed yearly, and almost as many pa¬
tients die of advanced disease.8 Around the world, the
SW is still the most widely performed operation in those
patients who appear to have disease resectable for cure.
Unfortunately, 5-year survival rates after the Whipple re¬
section are only about 10%, and up to 40% of these pa¬
tients eventually die of recurrent disease.8 Thus, in most
instances, this major resection, associated with
cant short- and long-term morbidity, is only a palliative
procedure. Many thoughtful surgeons have adopted the
PPW, believing that the morbidity would be less if the
gastric reservoir function was maintained. It has gener¬
ally been accepted that this did not compromise the chance
for cure of the cancer. Nevertheless, we and several other
groups have remained skeptical that the PPW repre¬
sents a significant improvement over the SW.9"11 We also
are concerned about whether it is an adequate cancer op¬
eration for most patients with cancer in the head of the
gland. The data accumulated from the present study have
strengthened our beliefs about some of these issues.
As best as can be determined in this retrospective
review, the patients in each of the two groups were com¬
parable in all important respects. Their mean ages and
gender distribution were similar. Most of the patients in
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013
the SW group had adenocarcinoma of the head of the pan¬
creas; less than half the patients in the PPW group did.
Nevertheless, the difference was not significant. The pre¬
senting complaints were the same in both groups. The
majority of the patients had obstructive jaundice and
abdominal pain and had lost some weight prior to their
(n=15)
4 (27)
surgical procedure.
The older accounts of uncontrolled diarrhea and
1 (7)
9(61)
profound weight loss that followed the SW have left a
2(1) lasting impression on many of today's surgeons.12 Thus,
0 (0) proponents of the PPW argue that digestive function is
2(1) less impaired when the gastric reservoir and antropy-
loric functions areleft intact and that patients fare bet¬
1 (7) ter nutritionally. Although a number of authors have ex¬
amined various aspects of the altered physiological features
in these patients, only rarely have they compared such
patients with patients who underwent SW. None have
looked at these issues prospectively or specifically fo¬
cused on patients with carcinoma of the head of the pan¬
creas. For example, Patti et al13 found that gastric emp¬
tying was normal in six patients, rapid in three patients,
and delayed in one patient after the PPW. Small-bowel
transit was normal in two patients, rapid in seven, and
delayed in one. In spite of these abnormalities, most pa¬
tients were without symptoms and gained weight. In their
study,13 four subjects had periampullary cancers, and four
had cancer of the head of the pancreas. The authors did
not examine subjects who had undergone the SW, so com¬
parisons were not possible.13 Braasch et alH also evalu¬
ated gastrointestinal function and weight gain in a group
of 63 patients undergoing PPW who had a variety of be¬
nign and malignant periampullary and pancreatic dis¬
eases. The patients regained 95% of their preillness weight
(median value), measured a minimum of 4 months post-
operatively. Gastric emptying of liquids and solids was
reported as normal. However, 17 patients (27%) had some
digestive complaints (six patients had abdominal pain;
eight had diarrhea despite pancreatic enzyme supple¬
mentation; two had occasional nausea and vomiting; and
one had dumping symptoms). Patients who had under¬
gone the SW were not studied in this report, either. Fink
et al15 did compare six patients who had the SW with six
who had undergone the PPW, all at least 3 years before.
Although some of the patients undergoing SW had peri¬
ampullary tumors, none had pancreatic cancer, and all
signifi¬ in the PPW group had chronic pancreatitis. Body weights
were within normal limits in five of the six patients in
each group. Gastrointestinal symptom severity scores (eg,
nausea, vomiting, stomach fullness, gas, diarrhea, cramps,
and flushing) were the same in the two groups. Folate
and vitamin A and B12 levels were normal in all, and all
other laboratory serum values were the same in the two
groups. Gastric emptying of liquids was delayed after the
SW; it was near normal after the PPW. Solid emptying
was the same in the two groups. Thus, these authors13
were unable to substantiate significant physiological
differences between the two types of resections and
concluded that the operations were "functionally
equivalent."
Our patients were questioned between 1 and 5 years
(mean, 32 months) following their operations. The 21
patients in the SW group available for interview re-
 ported a weight gain to 92% of their preoperative weight,
compared with 96% of that weight in the two patients in
the PPW group who were assessed. The mean quality of
life index, which included questions related to gastro¬
intestinal symptoms, averaged 8.0 in the SW group and
9.0 in the PPW group. One patient in the SW group had
pain; neither of the two patients in the PPW group com¬
plained of pain. Thus, it is our impression that the pa¬
tients who underwent the SW fared well from the stand¬
point of general weight gain and nutrition, gastrointestinal
symptoms, and pain. However, because of the small num¬
ber of patients available for interview in the PPW group,
no statistical comparisons can be made.
Another argument that is often made in support of the
PPW is that the operation can be done more quickly and
that it is technically easier than the SW.3141617 Our expe¬
rience does not support those claims. There were no sig¬
nificant differences in the actual operating times, mea¬
sured blood loss, or blood replacement with the two
procedures.
The most widely recognized short-term morbidity
of the PPW is delayed gastric emptying, which our pa¬
tients also experienced to a greater degree than was seen
in the SW group (61.% vs 41%, respectively). Those pa¬
tients with delayed gastric emptying (ie, not tolerating
oral liquids by 7 days postoperatively) had no other clini¬
cal explanation for its occurrence (eg, pancreatitis, pan¬
creatic fistula, or infection). The explanation for this prob¬
lem remains unclear, but we agree with others that it is
probably associated with transient anastomotic edema
and/or an antropyloric motility disturbance.1819 Al¬
though we make every attempt to preserve a long cuff of
duodenum (3-4 cm) that is well vascularized as well as
the vagal innervation of the antrum, other unknown fac¬
tors must be involved.
In the current environment of cost consciousness
in health care, it is impressive that the average hospital
charges for the PPW group were about $26 000 greater
than for the SW group, principally because of the addi¬
tional hospitalization required until an oral diet had been
resumed. Of course, that added cost should not be a con¬
sideration if the operation itself is determined to be bet¬
ter for the patient.
Several of our findings speak indirectly to the issue
of whether the PPW is an adequate cancer operation. First,
we found no instance of tumor invasion of the duodenal
resection margin in the SW group, although it has been com¬
mented on by others.911 It is our routine to perform a fro¬
zen section examination of each resection line during the
operation and to extend the resection if tumor is present.
This practice should avoid the problem of an inadequate
resection. Second, our pathologists found an average of twice
as many lymph nodes in specimens from the SW group as
they did in the PPW group. To be sure, this does not mean
that the nodes that were left behind during the PPW con¬
tained metastatic disease, but it confirms that less lym¬
phatic tissue was removed. We are aware of the data sug¬
gesting that the lymph nodes along the greater and lesser
curves of the stomach are rarely involved by pancreatic
cancer.19
Although the small numbers of patients in our study
did not allow us to draw conclusions about whether the
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013
PPW is an adequate cancer operation, we have been im¬
pressed with the report of Roder et al.20 They analyzed
actual (not actuarial) survival for patients with ductal ad-
enocarcinoma of the head of the pancreas who under¬
went the SW (31 patients) or PPW (22 patients). Tu¬
mors were classified according to the UICC staging system.
The type of resection had no influence on survival for
patients with stage I disease; however, the SW resulted
in significantly better survival in patients with stage III
disease (P<.007). There were no differences in survival
when the two operations were compared for other peri¬
ampullary tumors. Because staging of pancreatic cancer
(ie, lymph node involvement) must generally await ex¬
amination of the Whipple specimen, these authors20 rec¬
ommended that all patients with cancer of the head of
the pancreas undergo the SW. Since most other reports
of survival include other periampullary malignant neo¬
plasms lumped together with pancreatic cancer, use sta¬
tistical techniques to estimate survival, and/or fail to stage
the disease, we find the analysis by Roder et al20 quite
persuasive.
We have no explanation for our finding that the fre¬
quency of pancreatic fistulas was higher in the PPW group,
but doubt that it represents a difference attributable to
the type of operation. We defined a pancreatic fistula as
drainage of fluid with a high amylase concentration (> 100
mL/24 h) from the pancreatic drain any time after the
second postoperative day. Since we did not routinely
sample drain fluid for its amylase content, we may have
overlooked clinically insignificant fistulas. Both groups
of procedures were performed by the same surgeons, some
of whom use pancreatic stents, and some of whom do
not. Similar techniques were used for the pancreaticoje-
junostomy anastomoses as well. Thus, the occurrence of
fistulas was not likely to have been influenced by differ¬
ences in surgical proficiency.
In summary, our retrospective review failed to pro¬
vide support for the idea that the PPW was technically easier
or could be performed more quickly. The SW group fared
well from the point of view of weight gain, pain, and qual¬
ity of life. The PPW group required longer hospitaliza-
tions at greater cost, chiefly because of the greater likeli¬
hood of delayed gastric emptying. The best data available
in the literature suggest to us that the SW is still indicated
for cancer of the head of the pancreas; the PPW may be a
satisfactory alternative for other periampullary tumors. How¬
ever, the notion that patients fare better nutritionally or en¬
joy better quality of life after this less radical operation re¬
mains to be proven.
Accepted for publication April 26, 1995.
Supported by the Veterans Affairs Merit Review Pro¬
gram (Drs Ashley and Reber).
Presented at the 66th Annual Session of the Pacific
Coast Surgical Association, Seattle, Wash, February 19,
1995.
The authors gratefully acknowledge the assistance of
Wendy Berger, MPH, for the quality of life assessments.
Reprint requests to University of California, Los
Angeles, School of Medicine, Department of Surgery (72-
215 CHS), 10833 LeConte Ave, Los Angeles, CA 90024-
6904 (Dr Reber).
 "
REFERENCES
J tric emptying. In those patients, the average length of stay was
1. Watson K. Carcinoma of ampulla of Vater: successful radical resection. Br J
Surg. 1944;31:368-373.
2. Traverso LW, Longmire WP Jr. Preservation of the pylorus in pancreaticoduo-
denectomy. Surg Gynecol Obstet. 1978;146:959-962.
3. Crist DW, Cameron JL. The current status of the Whipple operation for peri-
ampullary carcinoma. Adv Surg. 1992;25:21-49.
4. Tsao Jl, Rossi RL, Lowell JA. Pylorus-preserving pancreatoduodenectomy: is
it an adequate cancer operation? Arch Surg. 1994;129:405-412.
5. Hermanek P, Sobin LH, eds. TMN Classification of Malignant Tumours. 4th ed.
Geneva, Switzerland: International Union Against Cancer (UICC); 1987:63-71.
6. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ (American Joint Committee
on Cancer), eds. Manual for Staging of Cancer. 4th ed. Philadelphia, Pa: JB
Lippincott; 1992:69-73, 99-115.
7. Fishman B, Pasternak S, Wallenstein SL, Houde RW, Holland J, Foley KM. The
Memorial Pain Assessment Card: a valid instrument for the evaluation of can-
cer pain. Cancer. 1987;60:1151-1158.
8. Livingston EH, Welton ML, Reber HA. Surgical treatment of pancreatic cancer:
the United States experience. Int J Pancreatol. 1991;9:153-157.
9. Sharp KW, Ross CB, Halter SA, et al. Pancreatoduodenectomy with pyloric
preservation for carcinoma of the pancreas: a cautionary note. Surgery. 1989;
105:645-653.
10. McAfee MK, van Heerden JA, Adson MA. Is proximal pancreatoduodenectomy
with pyloric preservation superior to total pancreatectomy? Surgery. 1989;
105:347-351.
11. Boerma EJ, Coosemans JAR. Non-preservation of the pylorus in resection of
pancreatic cancer. Br J Surg. 1990;77:299-300.
12. Fish JC, Smith LB, Williams RD. Digestive function after radical pancreatico-
duodenectomy. Am J Surg. 1969;117:40-45.
13. Patti MG, Pelligrini CA, Way LW. Gastric emptying and small bowel transit of
solid food after pylorus-preserving pancreaticoduodenectomy. Arch Surg. 1987;
122:528-532.
14. Braasch JW, Deziel DJ, Rossi RL, Watkins E Jr, Winter PF. Pyloric and gastric
preserving pancreatic resection: experience with 87 patients. Ann Surg. 1986;
204:411-418.
15. Fink AS, DeSouza LR, Mayer EA, Hawkins R, Longmire WP Jr. Long-term evalu-
ation of pylorus preservation during pancreaticoduodenectomy. World J Surg.
1988;12:663-670.
16. Itani KM, Coleman RE, Meyers WC, Akwari OE. Pylorus-preserving pancreatoduo-
denectomy: a clinical and physiologic appraisal. Ann Surg. 1986;204:655-664.
17. Grace PA, Pitt HA, Longmire WP. Pylorus preserving pancreatoduodenec-
tomy: an overview. Br J Surg. 1990;77:968-974.
18. Warshaw AL, Torchiana DL. Delayed gastric emptying after pylorus preserving
pancreaticoduodenectomy. Surg Gynecol Obstet. 1985;160:1-4.
19. Cubilla AL, Fortner J, Fitzgerald PJ. Lymph node involvement in carcinoma of
the head of the pancreas area. Cancer. 1978;41:880-887.
20. Roder JD, Stein HJ, Huttl W, Siewert JR. Pylorus-preserving versus standard
pancreaticoduodenectomy: an analysis of 110 pancreatic and periampullary car-
cinomas. Br JSu1992;79:152-155.
rg.
¡^ DISCUSSION J tomosis, and how do you define a pancreatic leak or fistula?
Charles F. Frey, MD, Sacramento, Calif: In comparing the two
operations, the authors considered the speed of operation, blood
loss, suture line involvement with tumor, performance status, weight
gain, abdominal complaints, and found no differences between these
two operations. However, they did find differences in the incidence
of pancreatic fistulas or leaks at the pancreaticojejunostomy anas¬
tomosis. The incidence of leaks was 27% in patients with pylorus-
preserving pancreaticoduodenectomy and only 6% in patients with
standard pancreaticoduodenectomy. They also noted an increased
incidence of delayed gastric emptying in patients with pylorus-
preserving pancreaticoduodenectomy—61% vs 41% for patients
with a standard Whipple. Delayed gastric emptying as they defined
it was inability to tolerate oral liquids on the seventh postopera¬
tive day. The length of hospital stay was also increased with pa¬
tients with pylorus-preserving pancreaticoduodenectomy, from
21.3 days vs 15.4 days. The cost was also increased to $26 000 per
patient in the pylorus-preserving pancreaticoduodenectomy.
Why did you choose 7 days as your criteria for delayed
gastric emptying? Other authors have been less rigorous when
examining this topic. For example, Miedema and his col¬
leagues at the Mayo Clinic, in reporting their experience with
delayed gastric emptying in 279 patients, used inability to take
solid food at 14 days as their criterion. They reported 23% of
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013
their patients after pancreaticoduodenectomy had delayed gas¬
prolonged to 23 days, which is not dissimilar from the 21.3 days
reported by Dr Reber and his colleagues.
Going back to the issue of how to define delayed gastric emp¬
tying, it seems arbitrary. If we use 5 days as our standard, we could
have almost 95% delayed gastric emptying. If we went out to 20
days, the percentage would probably be about 5%. The real im¬
portance of delayed gastric emptying, no matter how defined, is
how it affects the length of hospital stay and the cost of hospital¬
isation. In this regard, the average length of stay between the pa¬
tients reported by Dr Reber and the Mayo experience was very
similar. There was one big difference between these two excel¬
lent studies. The Mayo group found no difference in the inci¬
dence of delayed gastric emptying between the pylorus-
preserving pancreaticoduodenectomy and the standard Whipple.
What is the cause of delayed gastric emptying after pancre¬
aticoduodenectomy? I am sure there are a variety of reasons. One
of them has been cited by the Mayo Clinic group, in which they
noted the incidence of a pancreatic leak or fistula was 54% in pa¬
tients with delayed gastric emptying and 17% in those without a
leak or fistula. My second question to the authors of this study: Is
the incidence of pancreatic fistula or leak at the pancreaticojeju¬
nostomy anastomosis higher in the patients witb delayed gastric
emptying? We have done approximately 15 of the pylorus-preserving
Whipples and about 15 of the standard pancreaticoduodenecto-
mies in the last 2 years. It is my impression, and we have not spe¬
cifically studied this issue, that we had no appreciable difference
in the incidence of delayed gastric emptying between the two pro¬
cedures. I know we have not had any of these patients in the hos¬
pital longer than 18 days, which is less than the average figure in
those patients who had delayed gastric emptying in either the UCLA
or Mayo experience. In part I attribute this to the fact that we had
only one leak which did not require reoperation from the duct-to-
mucosa pancreaticojejunostomy anastomosis among these 30 pa¬
tients, which has a lower leak rate than is associated with the stuff¬
ing pancreaticojejunostomy. We keep a Jackson-Pratt drain near
the pancreaticojejunostomy anastomosis and obtain daily drain
amylase levels. By day 6, the amylase level should be equivalent
to serum. Those who do not measure the drain amylase levels will
not know whether they have a leak or not.
How did you monitor your pancreaticojejunostomy anas¬
tomosis to identify a leak? Do you keep a drain near the anas¬
The authors have pointed out that the effect of the pylorus-
preserving Whipple on survival in patients with pancreatic ad-
enocarcinoma could not be answered from this study. The lower
yield of lymph nodes in patients undergoing the pylorus-
preserving Whipple is of concern. Taken together with a report
which Dr Reber cited in his article by Roder in which they found
a significant difference in survival among patients with stage III
pancreatic adenocarcinoma, it certainly seems that we should be
cautious in employing the pylorus-preserving Whipple in pa¬
tients with adenocarcinoma of the pancreas. The same prohibi¬
tions do not seem to apply to patients with ampullary lesions.
L. William Traverso, MD, Seattle, Wash: Dr Patel and col¬
leagues have shown a higher incidence of pancreatic fistula and
delayed gastric function with the pylorus-preservingWhipple over
that of the standard Whipple. Pancreatic fistula, at least in the ab¬
stract, was observed in three of 13 patients with pylorus-preserving
Whipple and in four of 38 patients with the standard Whipple. In
my opinion, the reason for the pancreatic fistula in any patient is
not the dissection differences between these two operations but
rather the experience of the surgeon. With increasing experience,
surgeons eventually tumble on an anastomotic technique that works
for them. We studied the factors that led to a successful pancre¬
aticojejunostomy in the laboratory and found the tiny canine
pancreatic duct could routinely be connected to a jejunal limb with-
 out fistula or leak by using a compulsively constructed mucosa-
to-mucosa anastomosis with surgical loopsor a surgical microscope.
Superb visualization was the key, regardless of whether you used
a stent or what type of anastomosis that you might want to do that
works for you. This study appeared in the May 1992 issue of the
American Journal of Surgery.
What was your experience and the type of technique you
used? From one slide, it seemed like half of the pylorus-
preserving procedures were performed by one surgeon, the group
that has the highest incidence of pancreatic fistulas in your study.
A contributing factor in their analysis may be their low num¬
bers with the pylorus-preserving Whipple and the low abso¬
lute numbers of pancreatic fistula in the study. My own x2 test
and, probably more appropriate, the Fisher's exact test indi¬
cate the figures in the abstract were not statistically significant
in regards to delayed gastric emptying after the Whipple pro¬
cedure. My experience, the Hopkins' group experience, and the
Mayo Clinic's experience found that all Whipple procedures
do not open up very quickly, that is to say they all open up later
than say a standard Billroth II gastrectomy.
When gastrointestinal function does not return, say after
12 or 14 days, then invariably a pancreatic leak under the stom¬
ach is brewing. Percutaneous drainage of the leak results in re¬
sumption of gastrointestinal function.
I would like to point out a landmark article published in
the May issue of the 1994 Journal of the American College of
Surgeons. Professor Kozuschek of Ruhr University in Ger¬
many published his experience with pancreatic cancer in pa¬
tients treated with either a pylorus-preserving Whipple or the
standard Whipple. There was no difference in long-term sur¬
vival. However, twice the number of patients were able to gain
weight after a pylorus-preserving Whipple than after the stan¬
dard Whipple. Pylorus-preserving Whipple allows for better nu¬
trition but still is not enough treatment to improve survival be¬
cause its weakness is the same as that of the standard Whipple,
ie, in the posterior pancreatic head in the retroperitoneum over
the vena cava. This has nicely been shown by Dr Warshaw to
be the most common place for positive surgical margins. It makes
no sense to have a few millimeters of margin in this area and
have a foot-long margin of gastric antrum. Do the authors have
long-term follow-up for their patients' ability to gain weight,
and what was the average long-term follow-up in their study
of the patients who you were able to contact by telephone? I
would like to use this opportunity to call for a sharing of in¬
formation, finding common ground on pancreatic cancer, and
then proceeding away from differences of resection toward other
things that we can do to make the prognosis of this disease with
surgery better. Clearly surgery alone is not the answer.
Norman M. Christensen, MD, Eureka, Calif: One thing
that bothers me about this paper is that there were 61 pancre-
atectomies and one surgeon did 28 of them. As I recall the slides,
he did the standard Whipple. Clearly, with almost 50% of the
total number done by one surgeon, that would skew the out¬
comes and therefore the conclusions. We all know the impor¬
tance of the learning curve in pancreatic surgery.
John A. Butler, MD, Orange, Calif: I wonder whether
the increased incidence of fistula formation has to do with the
fact that patients with the pylorus-preserving technique have
tumors that are heavily weighted toward distal common bile
duct and small periampullary tumors, where you are dealing
with a pancreas that is normal in consistency and has a normal-
sized duct, vs the Whipple, where you have a markedly fi-
brotic pancreas with an enlarged pancreatic duct. How many
of those patients required operation for closure of the fistula,
and did it in fact cause prolonged hospitalization?
Dr Reber: I appreciate the effort the discussants put into
a critical analysis of our data. First, let me address some of Dr
Frey's points. I agree that the definition of delayed gastric emp-
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Massachusetts User on 09/19/2013
tying is entirely arbitrary. One should choose a time that co¬
incides with when most patients had their nasogastric tube re¬
moved and have begun to tolerate liquids. Two weeks is really
too long; our experience has been that by a week most pa¬
tients have had their nasogastric tube removed.
I agree that a pancreatic fistula might cause delayed gastric
emptying, but we found no such relationship in our patients. All
of the pancreaticojejunostomies were done in a similar way by
the same surgeons doing both of the operations. Some of them
do use stents routinely; others do not. We were not able to find
any relationship between the use of a stent and the development
of a fistula.
Dr Butler made an excellent suggestion about why pancre¬
atic fistulas were more common in the pylorus-preserving group.
It may very well be that the pancreas was more normal in con¬
sistency and held sutures less well so that the likelihood of fis¬
tula formation was higher. It is important to stress that we do not
believe that the pylorus-preserving operation itself is more likely
to result in the development of a pancreatic fistula.
Dr Frey also asked about how we make the diagnosis of pan¬
creatic fistula and how we manage the drains. As you saw, there
were a number of different surgeons, and I can't speak for all of them,
but the majority handle the issue the same way. I leave a Silastic
drain close to the pancreaticojejunostomy, taking pains not to place
it right on the anastomosis. In most cases, I remove that drain about
10 days postoperatively. This is roughly the time that most of the
patients who have had an uncomplicated recovery are eating sol¬
ids, and I am ready to send them home in another day or two.
The diagnosis of a pancreatic fistula is not based particu¬
larly on the volume of fluid which comes out of the drain. Most
of our patients early in their recovery drain somewhere between
25 or 50 cc over a 24-hour period. However, we don't send the
drain fluid for an amylase determination unless there is some other
reason to be concerned. The presence of amylase in high con¬
centrations in that fluid is the basis for the diagnosis of a fistula.
Dr Traverso, you have talked a bit about the technique in¬
volved and whether we consider it important to do a duct-to-
mucosa anastomosis. Some of the surgeons do routinely try to
do such an anastomosis and some do not. There is no uniform
approach. I personally do not have an incidence of pancreatic fis¬
tula in my own series, which is about 5%. So I don't think it an
important thing to do. You're quite right in saying that probably
the most important thing is the experience of the surgeon and
his or her being comfortable with whatever the technique is that
they have evolved over a period of years.
The follow-up where we reported the weight gain and qual¬
ity of life issues was a minimum of 1 year and a mean of 27 months.
There is no question that longer follow-up is desirable, and we are
continuing to follow these patients. I would also point out to you
that virtually all of the data currently in the literature (and the
present study is no different) represent a retrospective analysis of
these issues. We need a prospective study, and we have undertaken
such a study at UCLA. We are looking primarily at quality of life
issues, nutritional differences, if any, between the two operations,
weight gain, and so forth. I began to accrue patients into the study
about 4 or 5 months ago. We now have four patients in each of the
two arms, ie, four standard Whipples and four pylorus-preserving
ones.
Dr Christensen, you expressed some concern about half of
the operations were done by one surgeon. You wondered whether
some of the complications occurred at the hands of the surgeons
who were doing fewer resections. Let me assure you that the sur¬
geons who did the smaller number of operations in our present
study were nevertheless surgeons with considerable experience with
the Whipple. Over the years, their case numbers far exceeded what
you saw quoted in this study. So, while I would certainly agree that
the experience of the surgeon is important, I think that is not likely
to be a problem in the present series.