Review
Dig Surg 1999;16:297304
Standard Kausch-Whipple
Pancreatoduodenectomy
Lucie Jones a Chris Russell b Franco Mosca c Ugo Boggi c Robert Sutton a
John Slavin a Mark Hartley a John P. Neoptolemos a
a Department of Surgery, University of Liverpool, Royal Liverpool University Hospital, Liverpool;
b Middlesex Hospital, London, UK, and c Divisione di Chirurgia Generale, Dipartimento di Oncologia,
Universit di Pisa, Italia
Key Words
Pancreatic cancer W Lymph nodes W Metastases W
Pancreatic resection W Pancreatoduodenectomy
Summary
Despite the increasing number of clinical trials in pan-
creatic cancer there are no widely accepted definitions of
different types of resection for pancreatic cancer. An
agreed definition of the standard Kausch-Whipple pan-
creatoduodenectomy was derived by a group of interna-
tional experts at a meeting in Castelfranco Veneto, Italy,
in May 1998. The lymph node groups to be removed en
bloc with the pancreatoduodenectomy and described
using the Japanese Pancreas Society classification were
as follows: 13a and 13b; 17a and 17b; 12b1, 12b2 and
12c; and 14a and 14b. Limited segmental major venous
resection and adjacent organ resection, if required, may
be included as part of a standard pancreatoduodenecto-
my. The pylorus-preserving procedure also may be in-
cluded as part of standard resection, but not for tumours
of the anterior-superior part of the head of the pancreas.
Wider adoption of the definition of standard Kausch-
Whipple resection will enable a more objective compara-
tive analysis of the radicality of resection between insti-
tutions and permit a more coherant analysis on the type
of surgery undertaken in multicentre adjuvant studies.
1999 S. Karger AG, Basel
ABC 02534886/99/01640297$17.50/0
Fax + 41 61 306 12 34
E-Mail karger@karger.ch Accessible online at:
www.karger.com http://BioMedNet.com/karger
Introduction
In 1912 Kausch reported the first successful two-stage
pancreatoduodenectomy for an ampullary carcinoma. In-
itially a cholecystoenterostomy was constructed to relieve
the jaundice. Subsequently, a gastroenterostomy and pan-
creatoduodenectomy were performed anastamosing the
pancreas to the jejunum similar to the modern-day dunk
procedure [1].
In 1934, Whipple resected an ampullary cancer using
catgut suture for the reconstruction; at 48 h there was
anastamotic rupture resulting in death. Five months later,
the operation was performed using silk sutures and pan-
creatic anastamosis was avoided; the patient survived [2].
Whipples first 3 cases were performed in two stages. At
the first operation, a gastrojejunostomy and cholecysto-
gastrostomy were undertaken followed several weeks later
by pancreatoduodenectomy with separate closure of the
duodenal and pancreatic stumps. Because the patient
developed cholangitis, the cholecystogastrostomy was
modified in subsequent procedures to a Roux-en-Y chole-
cystojejunostomy. This original operation did not include
either a gastric resection or a pancreaticoenteric anasto-
mosis [2, 3]. Five years later, Whipple undertook a one-
stage resection which was modified to include a pancreati-
cojejunal anastomosis; it is this procedure described in
1946 that is now known by his name [4]. The operation
Prof. J.P. Neoptolemos
University Department of Surgery, Royal Liverpool University Hospital
UCD Building, 5th Floor, Daulby Street
Liverpool L69 3GA (UK)
Tel. +44 151 706 4175, Fax +44 151 706 5798
Table 1. Japanese Pancreas Society classification of abdominal has been increased interest in the role of lymphadenecto-
lymph nodes [31] my. Ishikawa et al. [13] reported in a retrospective study
an apparently better 5-year survival rate after an extended
Group Lymph nodes
lymphadenectomy. In the only randomised study per-
1 Right gastric cardia formed, there was no improvement in 5-year survival
2 Left gastric cardia with extended lymphadenectomy, although patients with
3 Gastric lesser curve lymph node metastases had improved survival on post
4 Gastric greater curve hoc analysis [14]. This study highlighted the need for a
5 Suprapyloric
6 Infrapyloric
definition of the modern standard Kausch-Whipple resec-
7 Left gastric artery tion including the extent of lymph node dissection.
8 Common hepatic artery Recently the details of the dissection and extent of lym-
9 Coeliac trunk phadenectomy were agreed at the European Consensus
10 Hilus of the spleen Conference held in Castelfranco Veneto, Italy, on May 30,
11 Along the splenic artery
12 Hepatoduodenal ligament
1998 [15]. Adoption of a standard technique is important
12h Hepatic hilum for outcome comparisons between institutions and is
12a1 Superior to hepatic artery essential for prospective randomised trials comparing dif-
12a2 Inferior to hepatic artery ferent radicalities of operation as well as adjuvant therapy
12p1 Superior to portal vein studies.
12p2 Inferior to portal vein
12b1 Superior to bile duct
12b2 Inferior to bile duct
12c Around cystic duct Modern Standard Pancreatoduodenectomy
13 Posterior pancreatoduodenal (PPD) nodes
13a PPD nodes superior to ampulla of Vater
Preoperative Assessment
13b PPD nodes inferior to ampulla of Vater
14 Superior mesenteric artery (SMA)
History and examination, abdominal ultrasound (US)
14a Origin of the SMA and computed tomography (CT) [16] are all valuable in
14b Origin of inferior pancreatoduodenal artery assessing the resectability of a pancreatic tumour; laparos-
14c Origin of middle colic artery copy and laparoscopic US may improve further pre-oper-
14d Origin of jejunal arteries ative staging [1719]. Endoscopic biliary drainage may
15 Middle colic artery
16 Para-aortic nodes
facilitate scheduling of surgery; in comparison to percuta-
16a1 Above the origin of coeliac axis neous biliary drainage [2022] endoscopic stenting does
16a2 Coeliac axis and left renal artery not increase complications [23]. Selective angiography is
16b1 Left renal artery and inferior mesenteric artery unreliable for routine staging, although it is helpful in
16b2 Inferior mesenteric artery to aortic bifurcation identifying aberrant hepatic vasculature [24, 25]. In con-
17 Anterior pancreatoduodenal (APD) nodes
17a APD nodes superior to ampulla Vater
trast to patients with advanced disease [26], percutaneous
17b APD nodes inferior to ampulla Vater tumour biopsy/cytology should be avoided in patients
18 Inferior border of body and tail of pancreas with a potentially resectable tumour as the sampling error
is high and needling may disseminate the tumour with
reduced long-term survival [2730].

was also reported as a one-stage procedure by Trimble et
al. [5] in 1941.
Thereafter, the pancreatoduodenectomy became the
operation of choice for patients with cancer of the head of
the pancreas, ampulla, distal bile duct and duodenum [6,
7]. The development of specialist units has contributed to
a marked reduction in post-operative mortality from
around 30 to 56% or less [711].
Following findings by Cubilla et al. [12] who showed
that up to one third of patients had metastases in lymph
nodes not usually removed with standard operation, there
Laparotomy and Assessment of Lymph Node
Involvement
Lymph Node Stations. Lymph node stations are de-
scribed as in the Japanese General Rules for the study of
pancreatic cancer (table 1; fig. 13); although complex, it
enables precise definitions of the extent of lymph node
dissection [31].
Exploratory Laparotomy. Systematic palpation should
exclude the presence of hepatic and lymph node metas-
tases, whilst palpation of the pancreas, hepatoduodenal
ligament and the root of the mesentry including the liga-

298 Dig Surg 1999;16:297304 Jones/Russell/Mosca/Boggi/Sutton/Slavin/

Hartley/Neoptolemos
Fig. 1. Japanese Pancreatic Society clas-
sification of perigastric lymph nodes [31].
1 = Lymph nodes around the righ cardia;
2 = lymph nodes around the left cardia;
3 = lymph nodes along the lesser curvature;
4 = lymph nodes along the greater curvature;
5 = suprapyloric lymph nodes; 6 = infrapy-
loric lymph nodes.

Fig. 2. Japanese Pancreas Society classification of regional lymph nodes of the pancreas [31].
8 = Lymph nodes around common hepatic artery; 9 = lymph node around coeliac trunk; 10 =
lymph nodes at hilum of sleep; 11 = lymph nodes along splenic artery; 12 = lymph nodes in
hepatoduodenal ligament; 13 = posterior pancreatoduodenal; 14 = lymph nodes around the
superior mesenteric artery; 15 = lymph nodes along the middle colic artery; 16 = para-aortic
lymph nodes; 17 = anterior pancreatoduodenal; 18 = inferior border of body and tail of pan-
creas.

Table 2. Lymph node involvement in

Lymph Nagakawa 1994 [33] Nakao 1995 [32] Ishikawa 1997 [34] Total lymph
patients with cancer of the head of pancreas
node group lymph nodes lymph nodes lymph nodes nodes involved/
in three recent series involved/patients involved/patients involved/patients total patients

1 Not examined 0/90 0/81 0/171 (0%)

2 Not examined 0/90 0/81 0/171 (0%)
3 Not examined 0/90 0/81 0/171 (0%)
4 Not examined 0/90 0/81 0/171 (0%)
5 Not examined 0/90 0/81 0/171 (0%)
6 1/42 13/90 4/81 18/213 (8%)
7 0/42 0/90 2/81 2/213 (1%)
8 6/42 12/90 9/81 27/213 (13%)
9 2/42 2/90 2/81 6/213 (3%)
10 0/42 1/90 1/81 2/213 (1%)
11 2/42 16/90 6/81 24/213 (11%)
12 9/42 17/90 12/81 38/213 (18%)
13 29/42 46/90 40/81 115/213 (54%)
14 16/42 21/90 38/81 75/213 (35%)
15 0/42 0/90 5/81 5/213 (2%)
16 7/42 23/90 15/81 45/213 (21%)
17 22/42 35/90 30/81 87/213 (41%)
18 5/20 3/90 4/81 12/191 (6%)

Standard Kausch-Whipple Dig Surg 1999;16:297304 299

Pancreatoduodenectomy

Fig. 3. Japanese Pancreas Society classification of para-aortic lymph
nodes [31]. 16a = Lymph nodes above the coeliac axis; 16b1 = lymph
nodes between coeliac axis and renal artery; 16b2 = between renal
artery and inferior mesenteric artery.
ment of Treitz should exclude infiltration by the primary
tumour. The size and position of the cancer in the head of
the pancreas helps to determine the suitability of a pylo-
rus-preserving pancreaticoduodenectomy. Studies by Na-
kao et al. [32], Nagakawa et al. [33] and Ishikawa et al.
[34] showed the absence of lymph node metastases of the
suprapyloric group of nodes and an average of 8% had
lymph node metastases of the infrapyloric group (table 2).
Thus pylorus-preserving pancreatoduodenectomy should
be avoided in cases where the tumour lies close to the
superior border of the head of the pancreas. Lymph nodes
which are removed en bloc during the standard Kausch-
Whipple procedure include the anterior pancreatoduo-
denal nodes (13a, 13b); lymph nodes on the right side of
the hepatoduodenal ligament (12b1, 12b2, 12c); the nodes
to the right side of the superior mesenteric artery, from
the origin of the superior mesenteric artery at the aorta to
the inferior pancreaticoduodenal artery (14a, 14b), and
the anterior pancreaticoduodenal nodes (17a, 17b; ta-
ble 3). Lymph nodes around the common hepatic artery
(8a and 8p) are not removed routinely en bloc as part of
the standard Kausch-Whipple resection; lymph node 8a
can be removed for staging purposes.
Although para-aortic nodes (fig. 3) are removed as part
of the radical pancreatoduodenectomy and extended pan-
creatoduodenectomy (table 2), they are not removed as
part of the standard Kausch-Whipple resection [15].
300 Dig Surg 1999;16:297304
Table 3. Lymph nodes resected during the standard Kausch-Whip-
ple operation (group 8 for staging biopsy only)
Lymph nodes resected % involvement in patients
with carcinoma of the head
of the pancreas [3234]
Group 13a, b posterior pancreatoduodenal 54
Group 17a, b anterior pancreatoduodenal 41
Group 12b1, 12b2, 12c hepatoduodenal 18
Group 14a, b superior mesenteric 35
Group 8 common hepatic artery 13
Mobilisation
The hepatic flexure of the colon is mobilised to expose
fully the duodenum and head of pancreas. The duodenum
and head of the pancreas then are mobilised by Kochers
manoeuvre. Dissection along the fascia of Treitz (dorsal
pancreatic fascia) separates the duodenum and pancreas
from Gerotas fascia posteriorly on the right, then the
inferior vena cava and right ovarian/testicular vein, the
left renal vein and the abdominal aorta up to the superior
mesenteric artery on the left. In order to obtain a tumour-
free posterior pancreatic margin it may be necessary on
occasions to include the supero-anterior part of Gerotas
fascia. The gastrocolic ligament is dissected from the
transverse colon opening the lesser sac, fully exposing the
head of the pancreas and permitting identification of the
superior mesenteric vein.
Cholecystectomy and Dissection of the
Hepatoduodenal Ligament
The gallbladder is dissected in continuity with the
main extrahepatic bile duct. The common hepatic duct is
so divided as to leave a short bile stump with a good blood
supply for the subsequent biliary anastomosis. The main
bile duct is dissected distally together with the lymphoid
tissue lateral to the portal vein and artery (fig. 4). Care
must be taken as abnormal hepatic arterial vasculature is
common. The lesser curve of the stomach is mobilised by
dividing the lesser omentum. The common hepatic artery
is identified and mobilised along its horizontal course and
the gastroduodenal artery and small right gastric artery
identified. The gastroduodenal artery is divided. For the
pylorus-preserving procedure preservation of the right
gastric artery may not be necessary, provided there is only
a short (12 cm) duodenal stump [35]. Identification of
the hepatic portal vein at the superior border of the head
and neck of the pancreas may be performed at this stage.
Jones/Russell/Mosca/Boggi/Sutton/Slavin/
Hartley/Neoptolemos
Fig. 4. Dissection of the hepatoduodenal ligament. Removal of lym-
phatics from the right lateral border of the hepatic portal vein.
Mobilisation and Division of the Neck of the Pancreas
The right gastro-epiploic vein and the branch from the
right colon draining into Henles trunk are divided.
Henles trunk is ligated and divided as it drains into the
superior mesenteric vein. The neck of the pancreas is
divided as it lies on the hepatic portal and superior mes-
enteric veins. Using blunt dissection in the main, a tunnel
is created between the neck of the pancreas and the anteri-
or walls of the superior mesenteric and hepatic portal
veins. If the tumour appears to reach the resection mar-
gin, the pancreatectomy should be extended towards the
left. If there is any doubt a frozen section should be per-
formed, although if the tumour has been breached, a more
extended resection is unlikely to improve survival.
Partial Gastrectomy/Duodenectomy
The gastrocolic ligament and greater omentum are dis-
sected up to the greater curve of the stomach. For a distal
gastrectomy the left gastric artery and the right gastro-epi-
ploic artery are divided at the junction of the antrum and
body of the stomach. For the pylorus-preserving proce-
dure the duodenum is dissected and divided 12 cm dis-
tal to the pylorus. Sparing the stomach during pancreato-
duodenectomy does not limit the possibility of achieving
an adequate lymphadenectomy [36]. In contrast to the
standard Kausch-Whipple procedure, the lymph nodes
around the pylorus and along the lesser and greater curva-
tures of the gastric antrum are left in the pylorus-preserv-
ing pancreatoduodenectomy. These lymph nodes rarely
contain metastases unless the tumour is situated at the
anteriosuperior border or is so advanced that surgery is
not indicated anyway [32, 37].
Standard Kausch-Whipple
Pancreatoduodenectomy
Fig. 5. Dissection of the superior mesenteric vessels.
Division of the Jejunum
The ligament of Treitz is divided and the whole of the
duodenum is mobilised. The first part of the jejunum is
dissected and divided leaving a suitable vascular arcade.
Dissection off the Mesenteric Vessels
The whole specimen is retracted en bloc to the right.
This places mild traction on the plane between the pan-
creas and the mesenteric vessels to the left (fig. 5). Each
connecting vessel including the inferior and superior pan-
creatoduodenal veins and arteries are identified individu-
ally by direct vision, ligated and divided. Lymphatic tis-
sue in the dorsal pancreatic fascia (of Treitz) and along the
right lateral border of the superior mesenteric artery is
included with the resected specimen. Lymphatic tissue to
the left of the superior mesenteric vessels remains behind.
Skeletonising the superior mesenteric artery of all lym-
phatic tissue also results in denervation with the risk of
severe post-operative diarrhoea [38].
If the hepatic portal vein/superior mesenteric vein
encasement is relatively short (!1 cm) and involving less
than 50% of the circumference, it is acceptable to resect
the involved segment en bloc with the tumour. The defect
can be closed usually with primary suture, either a side
closure or end-to-end anastomosis, making sure that the
splenic vein/portal vein junction remains intact. If the
defect cannot be closed, an appropriate vein graft is per-
formed: the long saphenous vein may be used to patch the
vein or the internal jugular vein is used as a graft. One or
both main trunks of the coronary vein may enter the por-
tal system (hepatic portal vein or splenic vein) in the field
of dissection. At least one of these main trunks along with
Dig Surg 1999;16:297304 301
Table 4. Mortality and survival rates after
Kausch-Whipple (KW) and pylorus- Reference Number of Mortality 5-year Median
preserving pancreatoduodenectomy (PPPD) resections survival survival
excluding series with patients who have % % months
received adjuvant treatment
Trede et al. [7], 1989 118 0 24
Gall et al. [41], 1991 138 6 16 11
Geer and Brennan [42], 1993 146 3.4 24
Nitecki et al. [43], 1995 186 3 6.8
Russell [44], 1996 61 8 13
Sperti et al. [45], 1996 113 15 12
UKPACA [8], 1996 421 5.9
Mosca et al. [35], 1997 221 8.2 (KW) 9.6
7.0 (PPPD)

the splenic vein should be preserved. The specimen is
removed en bloc.
Reconstruction
Reconstruction begins with the pancreatojejunostomy.
A variety of reconstructions are possible which are associ-
ated with relatively low leak rates [39, 40]. An end-to-side
hepaticojejunostomy is performed with a single layer of
interrupted sutures. With a pylorus-preserving procedure
an end-to-side duodenojejunostomy is performed. For a
Kausch-Whipple resection a Roux-en-Y reconstruction
may be used.
Results
Post-operative mortality rates are around 58% in
experienced centres; although the median survival is only
1113 months and 5-year survival varies from 7 to 24%
(table 4). There is no significant difference in either mor-
tality, morbidity or long-term survival between the pylo-
rus-preserving and the standard pancreatoduodenectomy
[8, 35, 4145].
Discussion
Since the development of the Kausch-Whipple proce-
dure there has been much debate surrounding the role of
the pancreatoduodenectomy. During the 1960s and 1970s
the Whipple procedure became unpopular due to the
associated high mortality and poor 5-year survival [46,
47]. Some even rejected resection as a treatment for can-
cer of the head of the pancreas [4850]. Improvements in
operative and peri-operative management have signifi-
cantly lessened the risks of pancreatoduodenectomy [51].
Recent reports have documented an operative mortality
of 6% or less in specialist units [811], significantly lower
than in units in which resection is undertaken by general
surgeons [10, 11, 52]. Acceptable mortality and morbidity
rates in specialist centres justify pancreatoduodenectomy
in any fit patient with a potentially resectable tumour;
indeed resection is the best means of palliation and pro-
longation of life even in the absence of a prospect of cure.
The median survival times following surgery are still
poor, being between 10 and 18 months with 5-year surviv-
al rates of 724% [7, 34, 4145, 53, 54]. It has been shown
that the percentage of resected pancreas specimens with
lymph node involvement is around 5679% [32, 33, 55].
From the theoretical point of view, more extensive sur-
gery might improve the long-term survival rate.
The most significant factors in predicting patient out-
come are tumour grade, stage and resection margin status
[41, 56, 57]; those patients with negative resection mar-
gins and stage-I and II disease demonstrate superior sur-
vival rates [7, 58]. The survival rates in patients with neg-
ative resection margins (the potentially curative resec-
tions) are still, however, poor [56]. This is due to the high
rates of local recurrence (5080%) and hepatic metastases
(4090%). The early appearance of liver metastases fol-
lowing resection probably indicates the presence of dis-
seminated disease at the time of surgery. Lymph node
metastasis is usually an indicator of poor prognosis [13,
42], but some studies have shown little relationship be-
tween lymph node involvement and survival [57, 58].
Although some retrospective studies appear to show
improved survival from extended lymphadenectomy,
they are subject to retrospective analysis and stage migra-
tion [13, 5961]. Eighty-three patients were recently re-
cruited into a prospective randomised clinical trial of tra-
ditional or extended lymphadenectomy by 6 centres, 5 in
Italy and 1 in the USA [14]. The results showed no signifi-

302 Dig Surg 1999;16:297304 Jones/Russell/Mosca/Boggi/Sutton/Slavin/

Hartley/Neoptolemos
cant survival difference in the 2 groups overall, but a
question remained regarding the role of extended lym-
phadenectomy as post hoc analysis revealed survival ad-
vantage in patients with involved lymph nodes. This
raised the need for a further larger trial of extended lym-
phadenectomy. Moreover, the lack of a clear definition of
a standard Kausch-Whipple operation was also apparent.
The increasing interest in adjuvant treatment [6265]
also requires a more inherent understanding of the opera-
tions being undertaken. The European Study Group for
Pancreatic Cancer (ESPAC) is currently undertaking an
adjuvant study comparing radiochemotherapy or chemo-
therapy or a combination of both with no treatment [65].
At present over 470 patients have been recruited but
unfortunately prospective data on the extent of surgery
has not been collected. Once recruitment to ESPAC-1 has
closed, ESPAC-3 will compare adjuvant 5FU/folinic acid
with gemicitabine or no treatment which will require
recruitment of 760 patients; in this study the type of sur-
gery defined by the Castelfranco Veneto classification will
be collected.
In conclusion, standardisation of operations will allow
a more objective comparison between procedures of vary-
ing radicality and permit a greater understanding as to the
extent of surgery with adjuvant therapy.
Acknowledgments
We are grateful to Belinda Theis for checking the manuscript.
ESPAC-1 and ESPAC-3 are funded by clinical project grants from
the Cancer Research Campaign and supported by the European Pan-
creatic Club.

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