D2 Nodal Dissection
Mitsuru Sasako, MD
Gastric cancer seldom produces distant metastases un-til the primary becomes a T3 tumor (Table 1).1 On
the other hand, the incidence of lymph node metastasis is
already evident in early stages of the disease (Table 2).1
Local control of lymph node metastases is, therefore, es-
sential if cure is to be obtained. Until recently, operative
resection was the only effective method for local control.
Adjuvant chemotherapy has not been shown to increase
survival for gastric cancer in any large trials, although
radio-chemotherapy, as adjuvant treatment, demon-
strated better results than surgery alone in a randomized
controlled trial, Intergroup 0116 (SWOG 9008), suggest-
ing the importance of local control of this malignancy.2
However, the surgical treatment applied in this trial was
gastrectomy with a limited lymph node dissection in 90%
of patients, and in addition, retrospective analysis of this
trial demonstrated that surgical undertreatment under-
mined survival.3 Therefore, it is questionable whether
adequate lymph node dissection can be replaced by radio-
chemotherapy. The Dutch Gastric Cancer Trial compar-
ing D1 versus D2 dissection did not prove beneficial ef-
fects of a D2 dissection, principally due to an excessive
postoperative mortality of 10%.4 This trial highlighted
the importance of surgical experience in gastrectomy for
cancer. Thus far, no trial comparing D1 versus D2 has
been performed after sufficient pretrial training or a phase
II feasibility study. The only phase II study in the history
of D2 dissection was that in the Italian Gastric Cancer
Trials, in which the postoperative mortality was lower at
3%.5 Following this study, the same group of surgeons are
conducting a phase III trial comparing D1 versus D2 re-
sections.
SPLENECTOMY AND PANCREATECTOMY
IN D2 DISSECTION
Historically, when D2 dissection was initially performed
in the 1940s through 1950s, many curable tumors were
either T4 or had large nodal metastases in the supra-
pancreatic area adherent to the pancreas. The body and
tail of the pancreas and the spleen often had to be resected
en bloc with the tumor to achieve an R0 resection, ie,
complete macroscopic clearance of the tumor. In the
1980s, Maruyama advocated the advantage of pancreas
preservation in D2 dissections. With this modification,
the tail of the pancreas is preserved but the splenic artery
and the spleen are resected as in a traditional pancreati-
From the Gastric Surgery Division, National Cancer Center Hospital, Tokyo,
Japan.
Address reprint requests to Mitsuru Sasako, MD, Professor of Surgery, Chief,
Gastric Surgery Division, National Cancer Center Hospital, 5-1-1, Tsukiji, Chuo-
ku, Tokyo, 104-0045, Japan.
Terminology: D1 dissection, lymph node dissection limited to perigastric area;
D2 dissection, lymph node dissection including both perigastric and suprapan-
creatic nodes (common hepatic, celiac, left gastric and splenic artery nodes).
Supported in part by the New 10-year Strategy for Cancer Control of the
Ministry of Health, Labor and Welfare of Japan.
© 2003 Elsevier Inc. All rights reserved.
1524-153X/03/0501-0133$30.00/0
doi:10.1053/otgn.2003.35357
Table 2. Pathologic N-stage Distribution According to the
Tumor Depth Among 4683 Patients Who Underwent
Laparotomy at NCCH Between 1972-1991
Depth N0 N1 N2 N3 N4
T1 mm 96.7 2.2 1.1 0 0
sm 82.5 12.2 4.9 0.3 0.1
T2 mp 53.0 27.0 16.8 1.8 1.4
ss 36.3 29.8 25.8 2.5 5.5
T3 se 19.5 24.4 40.1 6.9 9.2
T4 si 7.8 11.6 33.6 21.7 25.2
Total 51.7 15.7 20.3 5.5 6.8
mm, mucosa and muscularis mucosa; sm, submucosal; mp, muscularis
propria; ss, subserosal; se, serosal; si, surrounding organ invasion.
Reproduced with permission from Sasako M: Surgical management of
gastric cancer: The Japanese experience. IN: Daly JM, Hennesy TPH,
Reynolds JV (eds): Management of Upper Gastrointestinal Cancer. Lon-
don, WB Saunders, 1999, pp 107-22.
Table 1. Incidence of Nodal, Hepatic, and Peritoneal
Metastases (%) According to Tumor Depth Among 4683
Patients Who Underwent Laparotomy at National Cancer
Center Hospital (NCHH) Between 1972-1991
Depth Lymph Node Liver Peritoneum No. of Patients
T1 mm 3.3 0 0 1063
sm 17.5 0.1 0 881
T2 mp 46.8 1.1 0.5 436
ss 63.7 3.4 2.2 325
T3 se 79.9 6.3 17.8 1232
T4 si 89.8 15.5 41.6 724
Total 47.7 4.5 11.5 4683
mm, mucosa and muscularis mucosa; sm, submucosal; mp, muscularis
propria; ss, subserosal; se, serosal; si, surrounding organ invasion
Reproduced with permission from Sasako M: Surgical management of
gastric cancer: The Japanese experience. IN: Daly JM, Hennesy TPH,
Reynolds JV (eds): Management of Upper Gastrointestinal Cancer. Lon-
don, WB Saunders, 1999, pp 107-22.
36 Operative Techniques in General Surgery, Vol 5, No 1 (March), 2003: pp 36-49
cosplenectomy.6 In many specialist centers in both Eu-
rope and Japan, pancreas-preserving total gastrectomy is
the standard procedure for a D2 total gastrectomy,5,7,8
although disadvantages to splenectomy have been sug-
gested.9 In particular, the two large clinical trials compar-
ing D1 to D2 dissection strongly suggested a negative
effect of splenectomy on both postoperative morbidity
and mortality.4,10 As these trials were not designed to
compare patients with or without splenectomy, a new
trial comparing D2 with or without splenectomy needs to
be performed to provide a definitive answer to this ques-
tion. Such a trial has, in fact, been started by the Japanese
Clinical Oncology Group in 2002 with the accrual of 500
patients planned11 in an attempt to prove the advantages/
disadvantages of splenic preservation. As the results of
this randomized controlled trial are pending, a pancreas-
preserving total gastrectomy with a D2 nodal dissection is
described as the standard surgical technique in this con-
tribution.
CANDIDATES FOR PANCREAS
PRESERVING D2 TOTAL GASTRECTOMY
Any T1 tumor requiring a total gastrectomy should be
treated without performing a splenectomy.12 Any curable
T4 tumor invading the tail of the pancreas should be
treated by total gastrectomy with a pancreaticosplenec-
tomy.1 In patients who have macroscopically metastatic
nodes adherent to the pancreas, the involved portion of
the gland and the remainder of the distal pancreas should
be resected with the spleen. Other curable advanced tu-
mors are candidates for this procedure.
Surgical Procedure
The incision of choice is either an upper midline, or the
so-called Mercedes incision, which includes bilateral sub-
costal incisions plus a high midline incision over the
xiphoid process (Fig 1).
1 The xiphoid process should be resected at the xiphi-sternal junction to obtain clear visualization of the esophageal hiatus.
Following laparotomy, the entire peritoneal surface including the pouch of Douglas should be inspected and palpated, after which
a sample for lavage cytology is taken from the pouch of Douglas or the left subphrenic space. The liver is inspected and palpated to
exclude previously undetected metastases. A Kocher maneuver is performed to access the para-aortic area. If there are suspicious
metastatic nodes, they should be removed and sent for frozen section analysis. If these evaluations reveal no distant metastasis, a
curative operation is initiated.
37D2 Nodal Dissection
2 The greater omentum is dissected from the transverse colon together with the anterior sheet of the mesocolon (lesser sac). It
is unclear whether a complete omentectomy and bursectomy is necessary for T2 tumors, but it is important for T3 tumors that may
invade the lesser sac. Many tumors invading or adherent to the anterior sheet of the mesocolon can be resected completely with
resection of this sheet only but without a transverse colectomy. The second assistant should spread the transverse colon so that the
operator can dissect the anterior sheet from the underlying tissue easily. This procedure is started from both the hepatic and the
splenic flexures toward the middle of the colon, where dissection is the most difficult. Dissection is continued cranially from the
colon toward the pancreatic body and tail. The dissection should be stopped close to the inferior border of the pancreas. On the
right, the anterior sheet of the mesocolon continues onto the duodenum and the head of the pancreas.
38 Mitsuru Sasako
3 While dissecting this sheet, the right accessory colic vein is found and followed cranially to the point where it joins Henle’s
surgical trunk. The origin of the gastroepiploic vein can then be identified. This vein is ligated and divided at its origin.
39D2 Nodal Dissection
4 As the mesocolon contains vessels which emerge from behind the pancreas, cranial continuation of the dissection of the
anterior sheet of mesocolon leads to a plane behind the pancreas. Therefore, the layer of dissection has to change from the posterior
to the anterior surface of the pancreas. Several small vessels passing from behind the pancreas should be ligated and divided. The
anterior sheet of the mesocolon continues as the pancreatic capsule, which is now dissected from the underlying pancreatic
parenchyma. This dissection is performed from the inferior to the superior border of the pancreas and from the middle of the
pancreas toward the duodenum, until the gastroduodenal artery is found. This artery is followed caudally to the right gastroepiploic
artery, which is doubly ligated and divided at its origin.
40 Mitsuru Sasako
5 After division of the gastroepiploic artery, the gastroduodenal artery is followed cranially until the common and proper hepatic
arteries are recognized. There is usually one large lymph node lying in the triangle formed by the gastroduodenal and common
hepatic arteries and the superior border of the pancreas. This node is classified as a suprapancreatic node, but recent studies have
shown that it is often one of the sentinel nodes from tumors in the gastric antrum. The stomach is pulled caudally by the assistant
so that the lesser omentum and the serosa covering the esophageal hiatus are stretched. The lesser omentum is then divided 1 cm
caudal to the attachment to the lateral sector of the liver. In many cases, there is an accessory left hepatic artery (occasionally a
replaced left hepatic artery) crossing the lesser omentum to the liver, which requires special attention. Whether this artery to the
liver from the left gastric artery should be preserved or not is decided by the stage of tumor (incidence of metastasis to this area) and
the size of the artery. When the intrahepatic anastomosis between the branches of the proper hepatic artery and an aberrant left
hepatic artery is poorly developed, partial liver necrosis in the lateral segments may occur. This line of division just below the liver
should be continued on to the hepatoduodenal ligament to the patient’s left side of the hepatic duct. The serosa of the ligament is
incised caudally toward the duodenum. This defines the area of dissection of the hepatoduodenal ligament. Several supraduodenal
vessels, most of which originate from the gastroduodenal artery, are ligated on the first part of the duodenum. After completing this
step, the gastroduodenal artery and the surface of the neck of the pancreas are clearly seen, as the duodenum is already detached
from the pancreas along the gastroduodenal artery. Tissue in the hepatoduodenal ligament is dissected along the gastroduodenal
artery and then along the proper hepatic artery from the duodenum toward the liver.
41D2 Nodal Dissection
6 The proximal ends of the supraduodenal arteries are ligated at their origin from the gastroduodenal artery. Dissection of the
hepato-duodenal ligament is to the bifurcation of the proper hepatic artery near the hepatic hilum. The right and left hepatic arteries
are recognized at this level and tissues are dissected caudally and from the right to the left. The right gastric artery is found arising
from either the gastroduodenal or proper hepatic artery in most cases. Occasionally the right gastric artery can arise from the left
hepatic artery when it has bifurcated low from the proper hepatic artery.
42 Mitsuru Sasako
7 After ligation and division of the right gastric artery, the duodenum is divided in the first portion. Before starting the dissection
of the suprapancreatic nodes, lymph nodes to the left and behind the portal vein are dissected, exposing the left and the posterior
sides of the portal vein. Dissection of the suprapancreatic nodes, ie, common hepatic, celiac, left gastric and splenic artery nodes,
is now performed from right to left, from the portal vein to the middle of the splenic artery. The adipose tissue cranial to the pancreas
contains many lymph nodes. This tissue is loosely attached to the pancreatic parenchyma in most cases and therefore can be
separated from the pancreas without difficulty. However, in patients who have a history of pancreatitis or who have fatty
degeneration of the pancreas, dissection between the pancreatic parenchyma and the suprapancreatic adipose tissue is difficult
andoften bloody. The pancreas is, therefore, easily damaged, and this may result in pancreatic leakage.
43D2 Nodal Dissection
8 The left gastric vein crossing over the common hepatic or the splenic artery and entering the splenic vein is sometimes
encountered (approximately one-third of cases) during this stage of the procedure. This vein should be ligated and divided near the
superior border of the pancreas. The adipose tissue containing lymph nodes in this area is then carefully dissected from the arteries
and surrounding nerve tissue in a cranial direction. If there are no obvious nodal metastases, the nerve structures surrounding the
arteries including bilateral celiac ganglia should be preserved. The posterior border of this adipose tissue is the respective
diaphragmatic crus on each side of the celiac artery. On the right, there are many lymph nodes behind the common hepatic artery,
which continue caudally as the para-aortic nodes. When these nodes are dissected, the left gastric vein is seen entering the portal
vein near the spleno-portal junction (approximately two-thirds of cases) shown in the figure. After dissection of this tissue from the
right crus, the right side of the celiac artery and the root of the left gastric artery can be recognized from its right side. The left gastric
artery is surrounded by thick nerve tissue, mainly celiac branches of the vagal nerves. Together with the nerve, the artery is ligated
and divided near its origin.
44 Mitsuru Sasako
9 The adipose tissue on the left side of the celiac artery is now dissected from the left crus surrounding the esophageal hiatus and
from the left side of Gerota’s membrane more laterally. This tissue contains the splenic artery nodes and dissection of these nodes
is continued along the anterior surface of the splenic artery until the posterior gastric vessels are encountered and ligated at their
origin from the splenic artery. The great pancreatic artery (arteria pancreatica magna) branches off at the same point from the
splenic artery, which is ligated and divided distal to the great pancreatic artery. In the original Maruyama’s pancreas preserving D2
total gastrectomy, the splenic artery was ligated near its origin, but in Sasako’s modification, the position of ligation is distal to the
great pancreatic artery to improve blood supply to the tail of the pancreas. The splenic vein should be preserved as far as the tip of
the pancreas and as many tributaries from the pancreas as possible should be preserved.
45D2 Nodal Dissection
10 The body of the pancreas is mobilized from the retroperitoneum on Toldt’s fascia. Dissection is started near the middle of the
gland from the inferior border of the pancreas toward the superior border and then laterally from middle part toward the spleen.
Complete mobilization of the body and tail of the pancreas together with the spleen enables thorough lymph node dissection of
splenic artery and splenic hilar nodes. All the connective tissue surrounding the tail of the pancreas, splenic vein and artery is
cleared. At this stage, the stomach, the spleen, and the omentum with surrounding connective tissue, including many regional
lymph nodes, are pulled up and the cardio-esophageal branch of the inferior phrenic vessels, branching to the left side of the cardia,
is ligated and divided at its origin. The lymph nodes at the origin of the phrenic vessels are included in the left pericardiac nodes in
the Japanese Classification of the Gastric Carcinoma. The vagal trunks are divided at a suitable level based on the proximal
extension of the tumor. The abdominal esophagus is then divided with a safe surgical margin.
46 Mitsuru Sasako
11 Our preferred reconstruction is a stapled Roux-en-Y esophagojejunostomy. The Roux limb (jejunum) should be placed
through a slit of mesocolon just to the right of the middle colic vessels. The length of jejunum above the mesocolon should be as
short as 10 cm to avoid kinking and adhesion to the dissected surface. We prefer an end-to-side esophagojejunostomy for safety,
being careful to make the jejunal stump small to avoid a blind loop and stasis of food. The Roux limb is fixed to the transverse
mesocolon with closure of the defect. We strongly favor a retrocolic Roux-en-Y technique.
47D2 Nodal Dissection
POSTOPERATIVE CARE
Table 3 shows the incidence of postoperative compli-
cations after D2 or D3 dissections in the clinical trial
JCOG 9501. Total and distal subtotal gastrectomy are
included. The most frequent complication is intra-ab-
dominal abscess, which is usually subphrenic. If the
morbidity after subtotal and total gastrectomy is com-
pared, pancreatic fistula is notably more frequent after
total gastrectomy, but there is little difference in other
complications (Table 4). Anastomotic leakage at the
esophagojejunostomy has decreased from more than
10% to 1 to 2% because of the use of surgical staples.1,13
The most frequent life-threatening complication fol-
lowing D2 total gastrectomy is pancreatic leakage, usu-
ally accompanied by intra-abdominal abscess when
contaminated. As this contamination occurs even in
patients without drainage tubes, the most likely route
for contamination is reflux of duodenal content
through the Papilla of Vater. To avoid septic complica-
tions requiring reoperation, insertion of prophylactic
drainage tubes into the left subphrenic space is recom-
mended. Separate drains are placed (laterally) in the
subphrenic space and (anteriorly) along the tail of the
pancreas. Amylase concentration of the fluid from
these drainage tubes is measured daily until it de-
creases to less than 1000 international units per milli-
liter. If the amylase concentration remains more than
2000 IU/mL after 4 to 5 days, pancreatic leakage is
occurring.14 If the level is more than 5000 IU/mL,
continuous suction is recommended. If the amylase
level is less than 5000 IU/mL and the patient does not
have features of sepsis, the drainage tubes are kept in
place for 12 to 14 days when fistulography through the
tubes is performed. If there is a large cavity or an
insufficiently drained space, continuous irrigation
should be started. Drainage of contaminated pancreatic
leakage is often so viscous that drains are easily oc-
cluded. In such cases, the drains need to be aspirated
frequently with large caliber suction catheters. Ulti-
mately the drains should be changed to a large double
lumen (usually 28 French gauge) drain to allow effec-
tive continuous irrigation. Contamination of pancre-
atic juice activates pancreatic enzymes and may cause
pseudoaneurysms of hepatic, splenic, celiac arteries, or
their ligated stumps. As with patients who develop
anastomotic leakage, continuous aggressive irrigation
is the only way to prevent such life-threatening occur-
rences.15
SURVIVAL RESULTS
The survival results of D2 gastrectomy are summarized
i
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