ANNALS
OF
SURGERY
Vol.
223,
No.
2,
194-198
©
1996
Lippincott-Raven
Publishers
Pancreatoduodenectomy
with
Preservation
of
the
Pylorus
and
Gastroduodenal
Artery
Hideo
Nagai,
M.D.,
Jun
Ohki,
M.D.,
Yasuo
Kondo,
M.D.,
Toshihiko
Yasuda,
M.D.,
Kogoro
Kasahara,
M.D.,
and
Kyotaro
Kanazawa,
M.D.
From
the
Department
of
Surgery,
Jichi
Medical
School,
Tochigi,
Japan
Objective
The
authors
evaluated
the
rationale
for
and
feasibility
of
gastroduodenal
artery
preservation
in
pylorus-preserving
pancreatoduodenectomy
(PPPD)
for
periampullary
cancer
in
which
the
pancreatic
remnant
maintains
a
normal
function
and
morphologic
characteristics.
Summary
Background
Data
Pylorus-preserving
pancreatoduodenectomy
has
become
one
of
the
standard
treatments
used
for
benign
and
malignant
diseases
of
the
pancreatoduodenal
region,
surpassing
ordinary
pancreatoduodenectomy
in
terms
of
technical
ease,
mortality
rate,
and
postoperative
nutrition.
Pylorus-preserving
pancreatoduodenectomy
is
usually
associated
with
gastroduodenal
artery
division,
which
presents
potential
risks
of
insufficient
duodenal
vascularity
and
lethal
postoperative
bleeding
from
the
gastroduodenal
artery
stump.
The
latter
complication
particularly
occurs
after
resection
of
bile
duct
or
ampullary
cancer
in
a
patient
whose
pancreas
remains
functionally
and
morphologically
normal
to
have
much
more
pancreatic
secretion
than
the
fibrotic
pancreas
seen
in
pancreatic
cancer.
According
to
the
authors'
data
on
the
volume
of
secretion
from
the
residual
pancreas
via
a
stent
tube
after
pancreatoduodenectomy,
the
sclerotic
pancreas,
as
seen
in
cancer
of
the
pancreatic
head,
secretes
only
20
to
50
mL/day,
whereas
the
secretion
from
the
soft
pancreas,
as
seen
in
bile
duct
cancer,
amounts
to
300
to
600
mL/day,
even
during
the
period
of
nothing
by
mouth.
Methods
Retrospectively,
we
made
a
histopathologic
study
of
eight
specimens
of
distal
bile
duct
and
ampullary
cancer
resected
by
pancreatoduodenectomy
or
PPPD
with
gastroduodenal
artery
division.
Prospectively,
we
performed
gastroduodenal
artery-preserving
PPPD
for
10
patients
with
distal
bile
duct,
ampullary,
and
islet
cell
cancers.
Results
The
histopathologic
study
revealed
no
invasion
or
metastasis
around
the
gastroduodenal
artery.
Clinical
application
of
gastroduodenal
artery-preserving
PPPD
showed
no
technical
difficulty,
and
neither
severe
complications
nor
recurrence
around
the
gastroduodenal
artery
were
observed
for
up
to
22
months
after
surgery.
Conclusions
Gastroduodenal
artery-preserving
PPPD
might
be
recommended
as
a
safe
procedure
for
patients
who
have
a
functionally
and
morphologically
normal
pancreas.
194
Gastroduodenal
Artery-Preserving
PPPD
195
Pylorus-preserving
pancreatoduodenectomy
(PPPD)
has
become
one
of
the
standard
treatments
used
for
be-
nign
and
malignant
diseases
of
the
pancreatoduodenal
region,
surpassing
ordinary
pancreatoduodenectomy
in
terms
of
technical
ease,
mortality
rate,
and
postoperative
nutrition.`13
In
PPPD,
the
gastroduodenal
artery
usually
is
divided
at
its
origin
from
the
common
hepatic
artery.
This
divi-
sion,
however,
poses
two
disadvantages.
First,
it
often
causes
poor
circulation
at
the
duodenal
stump,
leading
to
occasional
anastomotic
stenosis
or
dehiscence.
In
our
experience
with
22
cases
of
PPPD,
we
have
encountered
one
patient
who
demonstrated
necrosis
of
the
duodenal
stump
and
who
underwent
conversion
to
an
ordinary
pancreatoduodenectomy
with
resection
of
the
distal
stomach.
Second,
it
can
be
a
potential
source
of
fatal
postopera-
tive
bleeding
in
a
case
of
disruption
of
the
pancreatic
anastomosis.
In
particular,
this
complication
occurs
af-
ter
resection
of
cancer
of
the
distal
common
bile
duct
and
the
ampulla
of
Vater,
because
the
pancreas
tends
to
constitute
a
danger
due
to
its
extreme
softness
and
secre-
tion
of
a
large
volume
of
digestive
enzymes.
We
therefore
evaluated
the
rationale
for
and
feasibility
of
gastroduodenal
artery
preservation
in
resection
of
periampullary
cancer
in
which
the
pancreatic
remnant
maintains
normal
function
and
morphologic
character-
istics.
MATERIALS
AND
METHODS
Histopathologic
Study
Retrospectively,
we
reviewed
specimens
from
eight
patients
with
relatively
small
(1.5-3
cm)
distal
common
bile
ducts
(5
cases)
or
ampullary
cancer
(3
cases)
who
underwent
resection
at
our
institution
by
either
ordinary
pancreatoduodenectomy
or
PPPD
with
gastroduodenal
artery
division
between
January
1988
and
December
1992
(Table
1).
After
surgery,
two
of
the
patients
with
common
bile
duct
cancer
had
massive
bleeding
from
the
gastroduodenal
artery
stump
after
anastomotic
de-
hiscence
of
pancreaticojejunostomy.
One
of
these
pa-
tients
died
of
the
bleeding.
The
head
of
the
pancreas
has
been
subjected
to
step-
wise
sectioning
for
routine
histopathologic
study.
The
gastroduodenal
artery
could
be
identified
in
histologic
sections
of
all
cases.
In
the
current
study,
we
investigated
histologic
sections
to
find
cancer
invasion,
lymphatic
permeation,
and
lymph
node
metastasis
around
the
gas-
troduodenal
artery.
Surgical
Study
Ten
patients
underwent
gastroduodenal
artery-pre-
serving
PPPD
from
February 1993
through
September
1994
(Table
2).
Primary
tumors
included
distal
common
bile
duct
(4
cases),
ampullary
(5
cases),
and
islet
cell
(1
case)
cancers.
All
patients
had
nonsclerotic
parenchyma
in
the
body
and
tail
of
the
pancreas
and
a
main
pancre-
atic
duct
of
small
caliber.
Gastroduodenal
artery
preservation
included
com-
plete
preservation
of
the
right
gastroepiploic
artery,
divi-
sion
of
the
anterior
superior
pancreaticoduodenal
artery,
dissection
of
the
entire
length
of
the
gastroduodenal
ar-
tery,
and
division
of
the
posterior
superior
pancreatico-
duodenal
artery.
After
resecting
the
pancreatoduodenal
specimen,
we
reconstructed
the
distal
pancreas
with
anastomosis
to
the
posterior
wall
of
the
stomach.
Technical
difficulties,
blood
flow
from
the
duodenal
stump,
postoperative
complications,
and
modes
of
re-
currence
were
evaluated.
RESULTS
Histopathologic
Study
On
histologic
examination,
none
of
the
specimens
were
shown
to
feature
cancer
permeation,
invasion,
or
metastasis
around
the
gastroduodenal
artery
(Fig.
1),
even
though
all
cases
demonstrated
lymphatic
permea-
tion
somewhere
in
histologic
sections.
Surgical
Study
Dissection
of
the
gastroduodenal
artery
from
the
pan-
creas
required
meticulous
ligation
of
three
to
five
small
branches
of
the
gastroduodenal
artery
other
than
the
an-
terior
and
posterior
superior
pancreaticoduodenal
arter-
ies
(Figs.
2,
3,
and
4).
In
all
cases,
the
duodenal
stump
had
a
sufficient
blood
supply
after
completion
of
gastro-
duodenal
artery
dissection,
as
was
shown
by
affluent
bleeding
when
the
duodenum
was
divided
approxi-
mately
3
cm
distal
to
the
pyloric
ring.
After
surgery,
none
of
the
patients
had
major
compli-
cations.
Two
patients
had
minor
leakage
from
pancrea-
togastrostomy,
which
resolved
spontaneously.
One
of
these
two
patients
had
postoperative
bleeding
of
about
300
mL
from
around
the
pancreatogastrostomy
site,
but
neither
blood
transfusion
nor
reoperation
was
required.
In
no
case
was
peritonitis
experienced,
and
no
patients
died
during
hospitalization.
Nine
months
after
surgery,
one
patient
demonstrated
recurrence
in
the
abdominal
wall
at
the
site
of
previous
Address
reprint
requests
to
Hideo
Nagai,
M.D.,
Department
of
Sur-
gery,
Jichi
Medical
School,
Minamikawachi,
Tochigi,
329-04
Ja-
pan.
Accepted
for
publication
April
10,
1995.
Vol.
223
*
No.
2
196
Nagai
and
Others
Table
1.
PD/PPPD
WITH
DIVISION
OF
GDA:
PATHOLOGIC
FINDINGS
Around
GDA
Patient
Age
Size
Lymphatic
No.
(yr)
Gender
Cancer
(cm)
Permeation
Invasion
LN
Metastases
1
2
3
4
5
6
7
8
73
57
56
82
55
76
73
63
F
M
M
M
M
M
M
M
CBD
CBD
CBD
CBD
CBD
Amp
Amp
Amp
3.0
2.5
1.8
2.0
1.5
2.5
2.0
3.0
++
++
++
++
++
++
PD
=
pancreatoduodenectomy;
PPPD
=
pylorus-preserving
pancreatoduodenectomy;
GDA
=
gastroduodenal
artery;
CBD
=
distal
common
bile
duct
cancer;
Amp
=
ampullary
cancer.
percutaneous
transhepatic
biliary
drainage.
This
was
re-
sected,
and
he
is
well
and
without
cancer.
No
other
re-
currence
has
been
observed
during
follow-up
for
22
months.
All
of
the
patients
are
now
living
satisfactory
lives.
DISCUSSION
Pylorus-preserving
pancreatoduodenectomy
has
gained
wide
recognition
in
pancreatobiliary
surgery
since
the
report
of
Traverso
and
Longmire
in
1978.4
With
its
simpler
technique,
greater
physiologic
function,
and
improved
postoperative
nutrition,
PPPD
appears
to
be
superior
to
the
conventional
Whipple
procedure.
1,2,'
Although
disturbance
of
gastric
emptying
has
been
mentioned
as
one
disadvantage
of
pylorus
preservation,
many
investigators
have
failed
to
observe
much
differ-
ence
in
the
incidence
of
gastric
stasis
between
patients
undergoing
PPPD
or
the
ordinary
Whipple
procedure.
Even
if
delayed
gastric
emptying
occurs,
it
is
not
pro-
longed
beyond
the
immediate
postoperative
period.6
Peptic
ulcer
at
the
anastomotic
site,
once
suspected
as
a
troublesome
complication
of
pylorus
preservation,
has
been
reported
to
be
less
common
than
or
equal
to
that
after
standard
pancreatoduodenectomy
with
gastric
re-
section."13
According
to
the
recent
literature,"7'8
the
mortality
rate
after
pancreatoduodenectomy,
whether
with
or
without
pylorus
preservation,
is
less
than
5%.
In
a
survey
of
the
literature,
Grace
et
al.9
reported
that
13
of
3339
PPPD
patients
died
while
hospitalized.
Two
of
the
deaths
were
procedure
related:
one
patient
died
after
de-
hiscence
of
duodenojejunal
anastomosis,
and
the
other
died
of
a
pancreatic
fistula.
To
take
greatest
advantage
of
the
PPPD
procedure,
one
should
endeavor
to
avoid
severe
morbidity
and
at-
Table
2.
GDA-PRESERVING
PPPD
Patient
Age
Size
Lymphatic
No.
(yr)
Gender
Cancer
(cm)
Permeation
Outcome
(mo)
Alive,
22
CA(-)
Recurrence(+)
resected
Alive,
18
CA(-)
Alive,
13CA(-)
Alive,
4
CA(-)
Alive,
21
CA(-)
Alive,
17
CA(-)
Alive,
12
CA(-)
Alive,
10
CA(-)
Alive,
10
CA(-)
Alive,
12
CA(-)
GDA
=
gastroduodenal
artery;
PPPD
=
pylorus-preserving
pancreatoduodenectomy;
CBD
=
distal
common
bile
duct
cancer;
Amp
=
ampullary
cancer;
Islet
=
islet
cell
cancer
of
the
pancreas;
CA
=
recurrence
of
cancer.
2
65
77
3
4
5
6
7
8
9
10
77
69
48
79
79
55
79
54
F
M
F
M
F
F
M
F
M
M
CBD
CBD
CBD
CBD
Amp
Amp
Amp
Amp
Amp
Islet
2.0
2.0
2.0
4.0
2.0
1.0
1.5
3.0
2.0
3.0
++
++
++
+
++
++
Ann.
Surg.
*
February
1996
Gastroduodenal
Artery-Preserving
PPPD
197
Figure
1.
Histologic
view
of
gastroduodenal
artery
(arrow)
in
patient
5
(see
Table
1).
No
cancer
metastasis
or
invasion
can
be
seen
around
the
artery.
D:
duodenum;
P:
pancreas.
(H
&
E,
original
magnification
X
50).
Figure
3.
Gastroduodenal
artery
(arrowheads)
detached
from
head
of
pancreas
(P)
during
surgery
for
patient
10
(see
Table
2).
Arrow
indicates
right
gastroepiploic
artery
and
vein.
tain
a
near-zero
mortality
rate.
We
have
paid
special
at-
tention
to
preservation
of
the
gastroduodenal
artery
for
the
purpose
of
improving
PPPD
safety.
As
with
conventional
pancreatoduodenectomy,
al-
most
all
surgeons
routinely
divide
and
resect
the
gastro-
duodenal
artery
along
with
the
tumor
in
PPPD.
This
di-
vision
of
the
gastroduodenal
artery
appears
to
pose
two
problems.
First,
it
often
causes
poor
circulation
at
the
duodenal
stump.
After
dividing
the
gastroduodenal
ar-
tery
and
the
right
gastroepiploic
artery,
we
usually
ob-
serve
discoloration
of
the
duodenum
and
fail
to
see
an
active
flow
of
fresh
blood
from
the
cut
end
of
the
duode-
nal
wall.
Even
under
these
circumstances,
leakage
from
or
stenosis
of
the
duodenal
anastomosis
is
rare.
Nonethe-
less,
it
does
occur,
as
seen
in
our
pancreatoduodenec-
AE%S
4:A,
Figure
2.
Schema
of
gastroduodenal
artery
dissection
from
pancreas
and
severance
of
duodenum.
ASPD:
anterior
superior
pancreaticoduode-
nal
artery;
CHA:
common
hepatic
artery;
GDA:
gastroduodenal
artery;
PHA:
proper
hepatic
artery;
PSPD:
posterior
superior
pancreaticoduode-
nal
artery;
RGEA:
right
gastroepiploic
artery.
Figure
4.
Postoperative
celiac
angiogram
of
patient
3
(see
Table
2)
shows
preserved
gastroduodenal
artery
and
right
gastroepiploic
artery
(ar-
rowheads).
Arrow
indicates
right
gastric
artery
anomalously
derived
from
gastroduodenal
artery.
Vol.
223
*
No.
2
.:A
V.
i.
..L-.
198
Nagai
and
Others
tomy
series
and
as
reported
by
Grace
et
al.9
Preservation
of
the
gastroduodenal
artery
guarantees
a
sufficient
sup-
ply
of
blood
to
the
duodenal
stump.
Second,
postoperative
hemorrhaging
sometimes
oc-
curs
after
pancreatic
resection.
Although
the
number
of
deaths
due
to
pancreatoduodenectomy
and
PPPD
has
decreased
considerably
in
recent
years,
a
discussion
of
pancreatic
resection
morbidity
and
death
should
include
the
functional
and
morphologic
characteristics
of
the
pancreatic
remnant
subjected
to
anastomosis
with
the
gastrointestinal
tract.
The
immediate
postoperative
re-
sults
of
either
pancreatoduodenectomy
or
PPPD
for
pan-
creatic
cancer
have
been
excellent
due
to
the
usual
pres-
ence
of
the
fibrosclerotic
parenchyma,
dilated
pancreatic
duct,
and
reduced
secretory
capacity
of
the
remaining
pancreas,
all
of
which
are
caused
by
obstruction
of
the
main
pancreatic
duct
in
the
head
of
the
pancreas.
In
contrast,
however,
when
a
soft
pancreas
without
dila-
tion
of
the
duct
system
is
to
be
reconstructed,
as
in
the
case
of
distal
common
bile
duct,
ampullary,
duodenal,
and
pan-
creatic
islet
tumors,
the
surgeon
must
be
prepared
for
a
high
rate
of
leakage
from
the
pancreatic
anastomosis
and
for
sub-
sequent,
often
lethal,
hemorrhaging
caused
by
erosion
of
major
vessels.8"0"'
In
this
situation,
the
most
common
source
of
hemorrhaging
is
the
gastroduodenal
artery
stump."
Preservation
of
the
gastroduodenal
artery
will
re-
duce
the
possibility
of
this
formidable
complication.
The
mode
of
reconstruction
of
the
pancreatic
remnant
also
has
much
to
do
with
postoperative
complications
that
occur
after
proximal
pancreatectomy.
In
our
early
series
of
pancreaticojejunostomy
in
51
cases
of
pancreatoduodenal
region
cancer,
we
encountered
major
anastomotic
insuffi-
ciency,
massive
intra-abdominal
bleeding,
and
hospital
deaths
in
10,
8,
and
5
cases,
respectively.
These
major
post-
operative
complications
were
associated
with
cases
of
com-
mon
bile
duct,
duodenal,
and
periampullary
cancers
that
featured
a
soft
gland
and
a
main
pancreatic
duct
of
small
caliber.
We
thereafter
abandoned
pancreaticojejunostomy
for
soft-pancreas
cases
and
adopted
pancreatogastrostomy.
To
date,
we
have
performed
pancreatic
anastomosis
with
the
stomach
for
28
patients,
including
those
who
underwent
the
gastroduodenal
artery-preserving
PPPD
discussed
in
the
current
study.
Among
these,
anastomotic
dehiscence
oc-
curred
in
three
cases
(minor
3,
major
0),
intra-abdominal
hemorrhage
in
two
cases
(minor
2,
major
0),
and
hospital
deaths
in
zero
cases.
We
therefore
believe,
as
do
many
other
authors,8"12-'6
that
pancreatogastrostomy
is
much
safer
than
pancreaticojejunostomy.
Even
with
pancreatogastrostomy,
however,
leakage
and
bleeding
do
sometimes
occur.
We
must
pursue
measures
to
combat
major
bleeding
in
the
event
of
pancreatic
leakage.
Our
histologic
study
did
not
show
direct
invasion,
lym-
phatic
permeation,
or
lymph
node
metastasis
around
the
gastroduodenal
artery
in
specimens
of
common
bile
duct
or
Ann.
Surg.
*
February
1996
ampullary
cancer
resected
by
conventional
pancreatoduo-
denectomy
or
PPPD.
We
have
therefore
left
the
gastroduo-
denal
artery
unresected
without
impairing
the
radicality
of
resection
of
tumors
confined
in
the
pancreatoduodenal
re-
gion,
thus
avoiding
the
chance
of
massive
bleeding
from
an
eroded
arterial
stump.
Although
the
operative
procedure
for
dissecting
the
gastroduodenal
artery
from
the
anterior
surface
of
the
pancreas
required
a
half-hour
of
meticulous
division
of
tiny
branches,
it
proved
technically
possible
within
an
acceptable
operating
time.
In
conclusion,
we
strongly
advocate
gastroduodenal
artery-preserving
PPPD
for
resection
of
confined
tu-
mors
in
the
duodenum
and
pancreatobiliary
region
that
have
a
dangerous
pancreatic
remnant.
References
1.
Braasch
JW,
Gagner
M.
Pylorus-preserving
pancreatoduodenec-
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technical
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Langenbecks
Arch
Chir
1991;
376:50-58.
2.
Crist
DW,
Cameron
JL.
The
current
status
of
the
Whipple
opera-
tion
for
periampullary
carcinoma.
Adv
Surg
1992;
25:21-49.
3.
Traverso
LW.
Preservation
of
the
pylorus
during
pancreaticoduo-
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and
current
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J
Hep
Bil
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Surg
1994;
4:329-334.
4.
Traverso
LW,
Longmire
WP.
Preservation
of
the
pylorus
in
pan-
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Surg
Gynecol
Obstet
1978;
146:959-962.
5.
Takada
T,
Yasuda
H,
Uchiyama
K,
et
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pan-
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cancer
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surgical
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1994;
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367-371.
6.
Braasch
JW.
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of
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of
the
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of
the
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J
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1994;
4:342-348.
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JL,
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HA,
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CJ,
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and
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consecutive
pancreaticoduodenectomy
without
mortality.
Ann
Surg
1993;
5:430-438.
8.
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FG,
Arnone
GB,
Ravera
G,
et
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fistula
and
relative
mortality
in
malignant
disease
after
pancreaticoduodenec-
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Br
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10.
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DR,
Beart
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Jr.,
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Brodsky
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Arch
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126:1037-
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12.
Delcore
R,
Thomas
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Pierce
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13.
Ramesh
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Thomas
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