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DOI: 10.3748/wjg.v22.i10.2875 © 2016 Baishideng Publishing Group Inc. All rights reserved.
TOPIC HIGHLIGHT
2016 Gastric Cancer: Global view
Gastric cancer: Current status of lymph node dissection
Maurizio Degiuli, Giovanni De Manzoni, Alberto Di Leo, Domenico D’Ugo, Erica Galasso, Daniele Marrelli,
Roberto Petrioli, Karol Polom, Franco Roviello, Francesco Santullo, Mario Morino
Maurizio Degiuli, Erica Galasso, Mario Morino, Department of different terms, provided the original work is properly cited and
Surgery, University of Turin, Citta della Salute e della Scienza, the use is non-commercial. See: http://creativecommons.org/
10126 Turin, Italy licenses/by-nc/4.0/
Giovanni De Manzoni, Department of Surgery, University of Correspondence to: Maurizio Degiuli, MD, Chirurgia Generale
Verona, Ospedale Borgo Trento, 37126 Verona, Italy Universitaria 1, Department of Surgery, University of Turin, Citta
della salute e della scienza, 10126 Turin,
Alberto Di Leo, Division of Surgery, Ospedale di Arco, 38062 Italy. dr.mauriziodegiuli@gmail.com
Arco TN, Italy Telephone: +39-335-8111286
Fax: +39-11-6336725
Domenico D’Ugo, Francesco Santullo, Department of Surgery,
University “Cattolica del Sacro Cuore”, “A.Gemelli” University Received: July 7, 2015
Hospital, 00168 Rome, Italy Peer-review started: July 8, 2015
First decision: August 26, 2015
Daniele Marrelli, Franco Roviello, Department of Surgery, Revised: October 9, 2015
University of Siena, 53100 Siena, Italy Accepted: January 17, 2016
Article in press: January 18, 2016
Roberto Petrioli, Department of Oncology, University of Siena, Published online: March 14, 2016
53100 Siena, Italy
Karol Polom, Department of Surgery, Wielkopolskie Centrum

Onkologii, 61-866 Poznan, Poland
Abstract
Author contributions: Degiuli M designed the article structure; D2 procedure has been accepted in Far East as the
Degiuli M, De Manzoni G, Di Leo A, D’Ugo D, Galasso E,
standard treatment for both early (EGC) and advanced
Marrelli D, Petrioli R, Roviello F, Santullo F and Morino M.
gastric cancer (AGC) for many decades. Recently
contributed equally to this work and wrote the paper.
EGC has been successfully treated with endoscopy
Conflict-of-interest statement: All authors certify that they by endoscopic mucosal resection or endoscopic
have no affiliations with or involvement in any organization or submucosal dissection, when restricted or extended
entity with any financial interest (such as honoraria; educational Gotoda's criteria can be applied and D1+ surgery is
grants; participation in speakers’ bureaus; membership, offered only to patients not fitted for less invasive
employment, consultancies, stock ownership, or other equity treatment. Furthermore, two randomised controlled
interest; and expert testimony or patent-licensing arrangements), trials (RCTs) have been demonstrating the non infe
or non-financial interest (such as personal or professional riority of minimally invasive technique as compared to
relationships, affiliations, knowledge or beliefs) in the subject standard open surgery for the treatment of early cases
matter or materials discussed in this manuscript.
and recently the feasibility of adequate D1+ dissection
has been demonstrated also for the robot assisted
Open-Access: This article is an open-access article which was
selected by an in-house editor and fully peer-reviewed by external technique. In case of AGC the debate on the extent
reviewers. It is distributed in accordance with the Creative of nodal dissection has been open for many decades.
Commons Attribution Non Commercial (CC BY-NC 4.0) license, While D2 gastrectomy was performed as the standard
which permits others to distribute, remix, adapt, build upon this procedure in eastern countries, mostly based on
work non-commercially, and license their derivative works on observational and retrospective studies, in the west the
WJG|www.wjgnet.com 2875 March 14, 2016|Volume 22|Issue 10|

Degiuli M et al . Lymph node dissection in gastric cancer
[2]
Medical Research Council (MRC), Dutch and Italian RCTs of the General Rules of JRSGC , which were widely
have been conducted to show a survival benefit of D2 accepted and adopted in many countries, regional
over D1 with evidence based medicine. Unfortunately lymph nodes were classified into 16 stations by their
both the MRC and the Dutch trials failed to show a location (Table 1, figure 1A).
survival benefit after the D2 procedure, mostly due to In 1997, the JRSGC was transformed into the
the significant increase of postoperative morbidity and Japanese Gastric Cancer Association and this new
mortality, which was referred to splenopancreatectomy. association has maintained its commitment to the
Only 15 years after the conclusion of its accrual, the concept of the Japanese Classification. The aim of
Dutch trial could report a significant decrease of recur
this classification is to provide a common language
rence after D2 procedure. Recently the long term
for the clinical and pathological description of gastric
survival analysis of the Italian RCT could demonstrate
cancer. In the newest classification of the Japanese
a benefit for patients with positive nodes treated with
Gastric Cancer Association (JGCA), there is a very
D2 gastrectomy without splenopancreatectomy. As
nowadays also in western countries D2 procedure can comprehensive description of regional lymph node, as
[3]
be done safely with pancreas preserving technique and follow .
without preventive splenectomy, it has been suggested
in several national guidelines as the recommended Anatomical definition of lymph nodes and lymph node
procedure for patients with AGC. regions
The regional lymph nodes of the stomach are classified
Key words: gastric cancer; lymph node dissection; into stations numbered as in Table 2, from 1 to 20,
lymphadenectomy; D2 gastrectomy; D1 gastrectomy; plus stations 110, 111 and 112. Some of lymph node
D1 plus gastrectomy; robot assisted lymphadenectomy; stations numbered from 1 to 20 have been subdivided
laparoscopic lymphadenectomy in further subsets of nodes (Figure 1b and c). Lymph
node stations 1-12 and LN station 14v are defined as
© The Author(s) 2016. Published by Baishideng Publishing
regional stations; the remnant lymph node stations are
Group Inc. All rights reserved.
considered as distant stations and metastases to these
nodes are classified as M1. Lymph nodes No. 19, 10,
Core tip: Recently early gastric cancer and advanced
110 and 111 are considered as regional lymph nodes
gastric cancer (AGC) has been successfully treated
endoscopically; surgery is offered only to patients in case of tumor invading the esophagus.
not fitted for less invasive treatment and in several lymph node metastasis (N) are classified as
guidelines D1+ (open, laparoscopic, robotic) is the follows: (1) NX: regional lymph nodes cannot be
adequate treatment. For AGC, while D2 gastrectomy assessed; (2) N0: no regional lymph nodes metastasis;
is the standard procedure in eastern countries, mostly (3) N1: metastasis in 1-2 regional lymph nodes; (4)
based on retrospective studies, in the west different N2: metastasis in 3-6 regional lymph nodes; and (5)
randomised controlled trials have been conducted to N3: metastasis in 7 or more regional lymph nodes;
demonstrate a survival benefit of D2 over D1 with N3a, metastasis in 7-15 regional lymph nodes; N3b,
evidence based medicine, with contradictory results. metastasis in > 15 regional lymph nodes. In 2011
As nowadays D2 gastrectomy can be done safely the JGCA published the Japanese gastric cancer
with pancreas and spleen preservation, it has been [4]
treatment guidelines 2010 (ver. 3) based on the 3
rd
suggested also in several western guidelines as the English edition of the Japanese Classification of Gastric
recommended procedure for patients with AGC. [3]
Carcinoma , which defined the extent of systematic
lymphadenectomy according to the type (distal or
total) of gastrectomy indicated. These guidelines
Degiuli M, De Manzoni G, Di Leo A, D’Ugo D, Galasso E,
report which lymph node stations are expected to
Marrelli D, Petrioli R, Polom K, Roviello F, Santullo F, Morino M.
Gastric cancer: Current status of lymph node dissection. World be removed to perform a correct D1, D1+ or D2 in
J Gastroenterol 2016; 22(10): 2875-2893 Available from: URL: case of both distal and total gastrectomy (see chapter
http://www.wjgnet.com/1007-9327/full/v22/i10/2875.htm DOI: “definition of different levels of lymph node dissection).
http://dx.doi.org/10.3748/wjg.v22.i10.2875
ANATOMICAL BORDERS OF LOCO-

REGIONAL LYMPH NODES
INTRODUCTION The strategy of lymph node dissection is based on
The Japanese Research Society for Gastric Cancer a perfect knowledge of the anatomy of the upper
(JRSGC) published the first edition of the General Rules abdominal vessels, which are usefull landmarks in the
[1]
for Gastric Cancer Study in 1973 . In fact, several operating fields.
lymph node studies performed in the 50’s and 60’ in We will describe systematically all the locoregional
Japan revealed pathways of lymph node drainage. lymph node stations, with particular regards to their
Following these studies, in the first English edition anatomical and vascular borders.

Table 1 Numbering of lymph nodes according to the old classification of Japanese Research Society for Gastric Cancer (1962)
Station nr Station nr
1 Right cardiac nodes 9 Nodes around the coeliac axis
2 Left cardiac nodes 10 Nodes at the splenic hilus
3 Nodes along the lesser curvature 11 Nodes along the splenic artery
4 Nodes along the greater curvature 12 Nodes in the hepatoduodenal ligament
5 Suprapyloric nodes 13 Nodes at the posterior aspect of the pancreas head
6 Infrapyloric nodes 14 Nodes at the root of the mesenterium
7 Nodes along the left gastric artery 15 Nodes in the mesocolon of the transverse colon
8 Nodes along the common hepatic artery 16 Para-aortic lymph nodes
A B APIS
AGB
AGES
VGED
VCM
VCDA
VCD
C 111
110
112
19
Figure 1 locations of lymph node station. A: Numbering and locations of lymph node station according to the first edition of the General Rules of the JRSGC; B:
Location of lymph node stations in the posterior area; C: Location of lymph node stations in subphrenic area. JRSGC: Japanese Research Society for Gastric Cancer;
APIS: arteria phrenica inferior sinistra; AGB: arteriae gastricae breves; AGES: arteria gastroepiploica sinistra; VGED: Vena gastroepiploica dextra; VCDA: Vena colica
dextra accessoria; VCM: Vena colica media; VCD: Vena colica dextra.
Location number 1 (right paracardial nodes) Location number 3 (lesser curvature nodes)
Perigastric lymph nodes on the right side of the cardia; Perigastric lymph nodes at the lesser curvature,
they are located along the cardio-esophageal branch located along the inferior (descending) branch of the
of the left gastric artery, from its origin from the left left gastric artery and along the right gastric artery
gastric artery to the oesophageal hiatus. distal to the first gastric branch.
Location number 2 (left paracardial nodes) Location number 4 (greater curvature nodes)
Perigastric lymph nodes on the left side of the cardias, Perigastric lymph nodes at the greater curvature.
located along the cardio-oesophageal branch of the left This lymph node station is divided into a left (4s) and
inferior phrenic artery. right (4d) part defined by the Von Ghoete point (the

Table 2 Anatomical definitions of lymph node stations
Nr. Definition
1 Right paracardial LNs, including those along the first branch of the ascending limb of the left gastric artery
2 Left paracardial LNs including those along the esophagocardiac branch of the left subphrenic artery
3a Lesser curvature LNs along the branches of the left gastric artery
3b Lesser curvature LNs along the 2nd branch and distal part of the right gastric artery
4sa Left greater curvature LNs along the short gastric arteries (perigastric area)
4sb Left greater curvature LNs along the left gastroepiploic artery (perigastric area)
4d Rt. greater curvature LNs along the 2nd branch and distal part of the right gastroepiploic artery
5 Suprapyloric LNs along the 1st branch and proximal part of the right gastric artery
6 Infrapyloric LNs along the first branch and proximal part of the right gastroepiploic artery down to the confluence of the right gastroepiploic
vein and the anterior superior pancreatoduodenal vein
7 LNs along the trunk of left gastric artery between its root and the origin of its ascending branch
8a Anterosuperior LNs along the common hepatic artery
8p Posterior LNs along the common hepatic artery
9 Coeliac artery
10 Splenic hilar LNs including those adjacent to the splenic artery distal to the pancreatic tail, and those on the roots of the short gastric arteries
and those along the left gastroepiploic artery proximal to its 1st gastric branch
11p Proximal splenic artery LNs from its origin to halfway between its origin and the pancreatic tail end
11d Distal splenic artery LNs from halfway between its origin and the pancreatic tail end to the end of the pancreatic tail
12a Hepatoduodenal ligament LNs along the proper hepatic artery, in the caudal half between the confluence of the right and left hepatic ducts and
the upper border of the pancreas
12b Hepatoduodenal ligament LNs along the bile duct, in the caudal half between the confluence of the right and left hepatic ducts and the upper
border of the pancreas
12p Hepatoduodenal ligament LNs along the portal vein in the caudal half between the confluence of the right and left hepatic ducts and the upper
border of the pancreas
13 LNs on the posterior surface of the pancreatic head cranial to the duodenal papilla
14v LNs along the superior mesenteric vein
15 LNs along the middle colic vessels
16a1 Paraaortic LNs in the diaphragmatic aortic hiatus
16a2 Paraaortic LNs between the upper margin of the origin of the celiac artery and the lower border of the left renal vein
16b1 Paraaortic LNs between the lower border of the left renal vein and the upper border of the origin of the inferior mesenteric artery
16b2 Paraaortic LNs between the upper border of the origin of the inferior mesenteric artery and the aortic bifurcation
17 LNs on the anterior surface of the pancreatic head beneath the pancreatic sheath
18 LNs along the inferior border of the pancreatic body
19 Infradiaphragmatic LNs predominantly along the subphrenic artery
20 Paraesophageal LNs in the diaphragmatic esophageal hiatus
110 Paraesophageal LNs in the lower thorax
111 Supradiaphragmatic LNs separate from the esophagus
112 Posterior mediastinal LNs separate from the esophagus and the esophageal hiatus
LNs: lymph nodes.
point where right and left gastropepiploic arteries Location number 7 (left gastric artery nodes)
meet each other at full channel). Furthermore the left second tier lymph nodes located along the left gastric
part is divided into a proximal (4sa) and a distal part artery, from its origin from the coeliac trunk till its
(4sb). Lymph nodes of the proximal part of left group bifurcation into the cardioesophageal (ascending) and
4 (4sa) are located around the short gastric arteries lower (descending) branches on the lesser curvature.
while lymph nodes of the distal part (4sb) are located
along the left gastroepiploic artery. Lymph nodes of Location number 8 (common hepatic artery nodes)
the right part of group 4 are located along the right second tier nodes located around the common hepatic
gastroepiploic artery, distal to the first gastric branch. artery from its origin from the coeliac trunk to the
branching off of the gastroduodenal artery. These
Location number 5 (suprapyloric nodes) lymph nodes are divided into an anterior part, 8a, and
Perigastric lymph nodes at the lesser curvature, a posterior part, 8p (Figure 2).
located at the origin of the right gastric artery including
its first gastric branch. Location number 9 (coeliac trunk nodes)
second tier lymph nodes located around at the celiac
Location number 6 (infrapyloric nodes) axis including the origins of the common hepatic artery
Perigastric lymph nodes at the greater curvature of the and splenic artery (Figure 2).
pylorus, located along the right gastroepipolic vessels
from their origin from the gastroduodenal vessels till Location number 10 (splenic hilum nodes)
their first branches directed to the gastric wall. second or third tier, or M lymph nodes, located at the

16a1
11p 16a1
12a 9
16a2
8a
16b1
12p 8p
12b 16b2
Figure 2 Complete lymph node removal along the hepatic pedicle (lymph Figure 3 Anatomical borders of lymph node station nr 16.
node station nr 12a, 12b and 12p), common hepatic artery (lymph node
station nr 8a and 8p), splenic artery (lymph node station nr 11p), coeliac
axis (lymph node station nr 9). site of the primary tumor) along the origin of the
superior mesenteric vein (VMS) (14 v) and M nodes
along the origin of the superior mesenteric artery (AMS),
splenic hilus, distal to the tip of the pancreas tail. At
at the root of the mesenterium. The lateral border is
the lower pole of the spleen, the first gastric branch
represented by the branching of the gastrocolic vein
of the left gastroepiploic artery defines the vascular
(TGC); the lower border is located at the branching off
border between 10 and 4sb lymph nodes.
of the middle colic vein from the VMS and the upper
border is represented by the origin of the AMS at the
Location number 11 (splenic artery nodes) lower hedge of the pancreas.
Second tier nodes located along the splenic artery.
These nodes have been divided into a proximal part,
Location number 15 (middle colic nodes)
11p, located around the splenic artery, from its origin
M nodes located in the transverse mesocolon around
from the celiac axis, till the branching off of the posterior
the middle colic vessels, from their origin from the
gastric artery; and into a distal part, 11d, located
superior mesenteric vessels, till the mesocolic hedge of
around the splenic artery from the branching off of the
the transverse colon.
posterior gastric artery to the tip of the pancreas tail
(Figure 2).
Location number 16 (aortic hiatus -a1, middle -a2/b1 and
caudal -b2 paraaortic nodes)
Location number 12 (hepatoduodenal ligament nodes) Location number 16 includes in fact 4 separate groups
second and third tier nodes (according to the site of
of lymph nodes. All of them are nodes around the
the primary tumor) at the hepatoduodenal ligament.
abdominal aorta and inferior vena cava. The groups are
These nodes have been divided into 3 parts: left
the following: 16a1, M nodes around the aortic hiatus,
hepatoduodenal ligament nodes (12a), located at the
over the anterior side of the aorta, from the inferior
left side of the proper hepatic artery; and posterior
hedge of the hiatus to the upper border of the coeliac
hepatoduodenal ligament nodes (12b and 12p), again
trunk; 16a2, M nodes located over the anterior side of
divided into nodes located at the right and posterior
the aorta, from the coeliac trunk to the lower hedge of
side of the common hepatic duct (12b) and into nodes
the left renal vein; 16b1, third tier nodes located around
located posteriorly to the portal vein (12p) (Figure 2).
the anterior face of the aorta and vena cava, from the
lower hedge of the left renal vein to the upper border of
Location number 13 (retropancreatic nodes) the inferior mesenteric artery; right and left border are
third tier and M nodes, (according to the site of
defined by the right hedge of the inferior vena cava and
the primary tumor), along the superior and inferior
by the left ovarian (spermatic) vessels; 16b2, M nodes
branches of the posterior pancreaticoduodenal artery,
located around the anterior face of the aorta and vena
located over the posterior side of the pancreas head.
cava, from the upper border of the inferior mesenteric
The left lateral border of this location is marked by the
artery to the aortic bifurcation (Figure 3).
portal vein, while the upper border is represented by
the origin of locations 12b and 12p.
DEFINITIONS OF DIFFERENT LEVELS OF
Location number 14 (superior mesenteric vein and
artery nodes) LYMPH NODE DISSECTION
second and third tier and M nodes (according to the In the Japanese gastric cancer treatment guidelines

rd
2010 (ver. 3) based on the 3 English edition of the which involves the removal of stations 12a and 11p in
Japanese Classification of Gastric Carcinoma, the JGCA subtotal gastrectomy, and stations 12a, 11d and 10 in
[4]
defined the extent of systematic lymphadenectomy total gastrectomy .
[4]
according to the type of gastrectomy indicated . In South Korea the treatment approach to early
[10]
For total gastrectomy, the lymph nodes stations forms is similar . In a recent study from Seoul
to be dissected in D1 lymphadenectomy are stations National University Hospital (SNUH) the appropriate
from No.1 to 7; D1+ includes D1 stations plus stations extent of lymph node (LN) dissection in lower third
No.8a, 9, and 11p, and D2 includes D1 stations plus was evaluated analysing LN metastasis patterns
stations No.8a, 9, 10, 11p, 11d, and 12a. For tumors from a prospective topographic database, using
[11]
invading the esophagus, D1+ includes N0. 110 and D2 the Maruyama Index of unresected disease . The
includes Nos. 19,20,110 and 111. evaluated risk of lymph node metastasis in stations
For distal gastrectomy, the lymph nodes stations 8-12 led the Authors to conclude that the D1 dissection
to be dissected in D1 lymphadenectomy are stations plus stations 7 and 8a for mucosal cancer, and an
No.1, 3, 4sb, 4d, 5, 6 and 7; D1+ includes D1 stations expanded dissection to the D2 level for submucosal
plus stations No.8a, and 9, and D2 includes D1 cancer should be considered to ensure complete
stations plus stations No.8a, 9, 11p, and 12a. removal of metastatic LNs.
In the West, the clinical setting is rather different
from East Asia. In a large series of resected EGC from
LYMPH NODE DISSECTION FOR EARLY the Italian Research Group for Gastric Cancer (GIRCG)
GASTRIC CANCER database, submucosal invasion, Lauren diffuse/mixed
type, Kodama Pen A type and tumor size were found
The extent of lymphadenectomy in early gastric to be associated with an increased risk of lymph node
cancer (EGC) is strongly dependent from lymph [12]
metastases . The risk of positive nodes is particularly
nodal spread of early forms. It is well known that high in diffuse-mixed type, an aggressive form of
the probability of lymph node metastasis in EGC gastric cancer with special propensity to lymph node
is much lower than in advanced forms. However, metastasis and peritoneal dissemination in advanced
the risk ranges notably according to pathological [13]
forms . In the West, the decreasing incidence of
characteristics of EGC. Invasion of submucosa, tumor gastric cancer is mainly due to the decreasing number
grading, size, macroscopic appearance, and lympho- of intestinal type tumors of the distal third; as such,
vascular invasion have been identified as strong risk proximal tumors and diffuse-mixed type show a
[5]
factors for lymph node metastases in EGC . As a relative increase, and surgeons will more frequently
consequence, these factors are taken into account for face with this aggressive form of gastric cancer
[14,15]
.
establishing the indications to endoscopic resection Furthermore, endoscopic resections, which are
procedures (endoscopic mucosal resection, EMR, or treatment but also staging procedures, are much less
endoscopic submucosal dissection, ESD) in the JGCA adopted in the West, even if their implementation in
[4-6]
guidelines . According to these predictive factors, clinical practice is increasing, above all in specialized
subgroups of patients with virtual no risk of lymph [16]
centers ; as a consequence the diagnosis of EGC
node metastases have been identified. The resection is is clinically-based in most cases. Despite the recent
judged as curative when all of the following conditions advancement of staging procedures (CT scan,
are fulfilled: en-bloc resection, tumor size not greater endoscopic US), the risk of a clinical understaging is
than 2 cm, histology of intestinal-differentiated-type, still considerable, and this may be associated with a
pT1a, negative horizontal (lateral) margin, negative potentially fatal undertreatment, as the probability
vertical margin, and no lymphovascular invasion. The of advanced nodal status in non-early forms of
JGCA “expanded” criteria tend to include larger tumor gastric cancer in Western patients is notable . For
[15]
size, ulcerated or submucosal invading forms, and these reasons, the GIRCG guidelines advice a D2
selected undifferentiated tumors in the indications to lymphadenectomy in clinically early forms not suitable
[7,8]
endoscopic treatment . However, expanded criteria [17]
for endoscopic treatment . Special attention should
are not universally accepted and need validation in be given to the removal of infra-pyloric nodes (number
[9]
series outside East Asia . 6), which are the most commonly involved in EGC
In early forms not suitable for endoscopic treat of the distal stomach, above all in the diffuse-mixed
ment, the JGCA guidelines advice a D1 or D1 plus type, and to station 1 (in subtotal gastrectomy) as well
lymphadenectomy in cases with clinically negative as to lymph node stations from 7 to 12 (station 10 is
[4]
nodes . The D1 lymphadenectomy involves the optional). The D2 dissection is associated with a limited
removal of perigastric lymph nodes and station risk of complications and postoperative mortality in
number 7, whereas in the D1 plus the lymph node the West, above all when performed in specialized
stations 8a and 9 for subtotal gastrectomy, with the centers and when avoiding unnecessary splenectomy
[14,18]
addition of station 11p for total gastrectomy, should or spleno-pancreatectomy . Only in selected
be dissected. When lymph nodes are clinically positive, cases (high-risk patients, early forms with favourable
JGCA treatment guidelines advice a D2 dissection, pathological characteristics) more limited procedures

are adviced by the GIRCG group (D1 plus). has always raised great interest. In Asian countries
In any case, long term results reported in extended lymphadenectomy seems to give superior
[38-42]
previous studies should be considered to optimize results in terms of survival and recurrence :
treatment approach. Surgical treatment with adequate this could be explained by the Asian larger surgical
[18,38,43-46]
lymphadenectomy could offer a high probability of experience with this kind of dissection and by
cure even in Western patients. Survival rates in early the younger age of Asian patients, who therefore have
[38,47]
stages reported from specialized Western centers are fewer comorbidities , and less abdominal fat with
[19,20] [46]
very similar to those obtained in Eastern series . a consequent easier feasibility of the procedure .
Selected forms can be treated by endoscopic approach, A criticism that Western surgeons have advocated is
in accordance with the JGCA criteria, with acceptable that Japanese- and Asian in general-results were often
results even in the West
[16,21]
. However, it should be provided by retrospective surveys and non-randomized
[38,45,48]
emphasized that lymph node status is the strongest studies .
prognostic factor for EGC. Whereas 5-year and On the contrary in Western countries D2 lympha
10-year cancer-related survival of 98% and 95% can denectomy was not considered a standard procedure
[27,35,43]
be achieved in pT1N0 cases treated with appropriate in the clinical practice : the lower incidence of
lymphadenectomy, these rates fall to 70%-80% in this tumour and the consequent less confidence of
pT1N1/N2, and less than 30% when more than 6 western surgeons in this procedure is surely one of
lymph node are involved
[12,20]
. In T1N3a cases, the the reasons. D2 is a complicated and challenging
risk of recurrence could exceed 50%, reaching 80% in surgical technique and a proper training is mandatory.
[22]
pT1N3b . In Western patients, EGC with advanced In addition, according to former studies [mainly
[38,45,46,49]
nodal status should be considered very aggressive Western randomized clinical trials (RCTs) and
[50-54]
forms, requiring appropriate surgical and adjuvant subsequent reviews ] D2 seemed associated with
treatments. higher rate of surgical complications and higher peri-
Early forms could also be treated by minimally- operative mortality, without a real survival benefit.
invasive (laparoscopic or robotic) approach, which Driven by these results, Western surgeons have always
demonstrated non-inferior oncological results than preferred the limited dissection.
open surgery in recent studies
[23,24]
. However, it should Recent data have undermined this historical
be emphasized that oncological criteria regarding preference and started to change Western point of
resection margin and lymph node dissection need to view on D2 lymphadenectomy. In fact it has been
[28,45-48,55-58]
be carefully followed in minimally-invasive procedures. demonstrated that the higher rate of
mortality and surgical complications with D2 procedure
were mostly related to distal pancreatectomy and/
D2 LYMPH NODE DISSECTION FOR or splenectomy, which previously were included in
the standard D2 lymphadenectomy and considered
ADVANCED GASTRIC CANCER necessary for an adequate nodal dissection. Older
Gastric cancer is one of the leading causes of death for studies
[18,36,44,47-52]
included in the D2 group all patients
[25,26]
cancer worldwide . In the latest decades in Eastern treated with distal pancreatectomy and splenectomy:
countries national screening programs have brought these patients had a higher mortality rate and a
to earlier and widespread diagnosis while in Western higher incidence of surgical complications (such as
countries diagnosis is often late, due to the lack of fistulas, re-intervention, anastomotic leakage etc.)
[27]
surveillance strategies . In all the cases surgery is which influenced their outcome. On the contrary in
indeed the standard of care for all resectable tumours: more recent studies
[18,28,43,44,53]
subsites of patients that
radical gastrectomy with regional lymphadenectomy is underwent splenopancreatectomy and patients with
[28]
considered the adequate treatment . spleen and/or pancreas preservation are analysed
Gastric cancer has a high tendency to lymph separately.
nodes involvement and local spread: the deeper is the Furthermore it has been shown that even in
[29]
extension of the tumour the more they are invaded . Western countries, after a proper training, surgeons
Nodal spreading gradually takes place radiating from can safely perform a D2 gastrectomy when spleen and
[30,31]
the primary site and nodal involvement is one of pancreas are preserved, leading to lower morbidity
the most important prognostic factors. It is therefore and mortality rates and to a safer lymph node
[18,44,58]
clear the reason why surgeons have always given dissection .
so much importance to lymphadenectomy and its Last but not least the 15 year-follow up of the
[28]
extension famous Dutch study has demonstrated that loco-
In fact, lymph node dissection has been debated for regional recurrence rate is significantly lower in
several years by surgeons: as a result, two different patients treated with D2 lymphadenectomy vs patients
[32,33]
schools have developed . In Eastern countries who underwent D1 dissection, showing a survival
D2 lymphadenectomy has been considered the benefit with the enlarged dissection.
[34,35]
standard procedure since the 60’s , in particular in Here after some of the most significant studies,
[1,36,37]
Japan , where the high incidence of this tumour RCTs, reviews and meta-analysis -over D1 vs D2 are

reported. treatment for patients with resectable gastric cancer

[59]
Dent et al in 1988 described the first RCT (Table 3).
[38]
recruiting 43 patients, 22 with D1 and 21 with D2 In the British study , whose short term survival
dissection: the D2 group showed a higher rate of results were published in 1996, 400 patients, 200 with
perioperative complications without any significant D1 and 200 with D2, were recruited. The D2 group
benefit in survival after a follow up of three years. had greater postoperative mortality (13% vs 6.5%, p
In the 90’s two multicentre European RCTs, the = 0.04), higher overall postoperative morbidity (46%
Dutch and the MRC trials, almost simultaneously, vs 28%, p < 0.001) and longer hospitalization. Also
[49]
published their results comparing short and long-term Cuschieri et al investigated the adverse effects of
outcomes after D1 and D2 LN dissection. In the Dutch distal pancreatico-splenectomy, reporting that the
[45]
trial , which randomised 711 patients (380 to D1 and disadvantages of D2 gastrectomy (i.e., higher mortality
331 to D2), the D2 group showed a higher mortality and morbidity) might be the result of the additional
rate (10% vs 4%, p = 0.004), a higher frequency of pancreatectomies and splenectomies performed. The
postoperative complications (43% vs 25%, p < 0.001) same authors in 1999 published the 5-year survival
[49]
and a longer hospital stay (median 25 d vs 18 d, p results of their trial without showing any significant
[46]
< 0.001). In 1999 the same authors reported the difference in the overall survival (35% in D1 and
5-year survival results: survival rates were similar in 33% in D2). In multivariate analysis clinical stages Ⅱ
the two groups (45% in D1 vs 47% in D2). The risk and Ⅲ, male sex, old age and especially resection of
of relapse after 5 years was 43% for the D1 group spleen and pancreas were found to have a significant
and 37% for the D2 group; the difference suggested influence on survival. The authors concluded that D2
only a trend of survival benefit for the D2 group (p gastrectomy did not offer any advantage in terms of
= 0.22). In addition, patients who needed resection survival over D1 gastrectomy and that pancreatico-
of the spleen or of the distal pancreas had a lower splenectomy should not be considered a part of D2
survival rate compared to those who did not require dissection unless a direct involvement of the disease
it; splenectomy was found to be an independent risk into the pancreas was suspected (Table 3).
[60]
factor for surgical complications and was associated In 1998 the Italian Gastric Cancer Study Group
with decreased survival in both D1 and D2 procedures. published the results of a prospective multicentre
The authors concluded that splenectomy should not be phase 2 study on feasibility of D2 gastrectomy with
[61-63]
a routine part of the standard gastrectomy. spleen and pancreas preservation : pancreatico-
In 2004 the Dutch Gastric Cancer Group published splenectomy was not performed unless a direct
[48]
the long-term outcome of their trial after 11 years involvement of the pancreas by the tumour was
follow-up: no overall survival benefit was demonstrated suspected. The authors showed that D2 gastrectomy
with D2 lymphadenectomy (30% with D1 vs 35% with with spleen and pancreas preservation could be done
D2, p = 0.53) and only in subgroup analysis patients even in Western countries, in specialized centres,
with N2 disease showed higher survival rate after D2 with a strict quality control and a after a period of
than after D1procedure. The authors concluded that adequate training. Mortality and morbidity rates
no overall survival benefit had been demonstrated were comparable to those of standard resection and
with an extended dissection as the associated higher even better, reaching figures similar to the Japanese
postoperative mortality may had offset D2 long-term ones. After these first cheering results, a randomised
[58]
benefit in survival; for that reason D2 dissection could controlled trial was set up in 1998 , in order to
have been of benefit only if mortality and morbidity compare the short- and long-term outcome of D1 and
could have been avoided. D2 nodal dissection. A total of 267 patients with gastric
In 2010 the results of 15-year follow-up of the cancer were randomly assigned to either a D1 (133)
[28]
same trial were published. D2 lymphadenectomy or a D2 (134) procedure with preservation of pancreas
was finally associated with lower loco-regional and spleen, in five specialized centres over a period of
recurrence and gastric-cancer-related death rates, 6 years. In 2010 the Authors reported the short-term
as compared to those of D1 (p = 0.01). Significantly results. In the intention-to-treat analysis, the overall
lower overall survival was noticed in patients who morbidity rate after D2 and D1 dissections were 17.9%
underwent splenectomy and pancreatectomy in both and 12.0% respectively (p = 0.178). The postoperative
D1 and D2 groups. Subgroup analysis of patients who in-hospital mortality rate was 3.0% in the D1 group
did not undergo pancreatectomy and splenectomy and 2.2% after D2 gastrectomy (p = 0.722). The
showed significantly higher overall 15-year survival Authors concluded that in specialized centres the rate
rate in the D2 group (35% vs 22%). The authors of complications following D2 dissection was much
[61,62]
concluded that, since other studies had recently lower than in published randomized Western trials
demonstrated that even in Europe trained surgeons and therefore D2 dissection, in an appropriate setting,
could safely perform D2 lymphadenectomy with could be considered as a safe option for the radical
spleen and pancreas preservation and that D2 showed management of gastric cancer in Western patients. In
more favourable recurrence pattern and cancer- 2014 the Italian Gastric cancer Study Group published
[18]
related survival, D2 seemed to be the recommended the long-term results of this RCT . The five-year

Table 3 Results of randomised controlled trials on D1 vs D2 gastrectomy
RCT Nr. pts Morbidity (%) Mortality (%) Survival (%)

D1 D2 D1 D2 D1 D2 D1 (OS) D2 (OS)
Bonenkamp et al[45,46] 380 331 25 43 4 10 45 (5 yr) 47 (5 yr)
p < 0.001 p = 0.04 P = 0.99
30 (11 yr) 35 (11 yr)
p = 0.53
21 (15 yr) 35 (15 yr)
P = 0.03
Cuschieri et al[38,49] 200 200 28 46 6.5 13 35 (5 yr) 33 (5 yr)
P < 0.001 P = 0.04 P = 0.43
Wu et al[55,56] 110 111 17.1 7.3 0 0 59.5 (5 yr) 53.3 (5 yr)
P = 0.012 P = 0.041
Degiuli et al[18, 58] 133 134 12 17.9 3 2.2 66.5 (5 yr) 64.2 (5 yr)
P = 0.178 P = 0.722 P = 0.695
38 (DSS 5 yr 59.0 (DSS 5 yr
T2-T4 N+) T2-4 N+)
P = 0.055
RCT: randomised controlled trial; OS: overall survival; DSS: disease specific survival; N+: node positive patients.
overall survival (OS) and disease-specific survival even if D3 lymphadenectomy was associated with
(DSS) rates were respectively 66.5% and 71% for a higher morbidity, due to its surgical complexity, it
D1 and 64.2% and 72.6% for D2, with no significant had a significant long-term survival benefit over D1
difference between the two groups (OS p = 0.695, dissection (Table 3).
[57]
DSS p = 0.916). Subgroup analysis showed a trend Seevaratnam et al in 2012 analysed 5 randomized
towards benefit of D2 dissection in patients with locally trials involving 1642 patients (845 D1 and 797 D2)
advanced gastric cancer (DSS 55% for D1 vs 69% enrolled from 1982 to 2005; the authors highlighted
for D2 with p = 0.143) and in patients with positive the differences among earlier (considering procedures
lymph nodes (OS rate 35% for D1 vs 51% for D2 and with spleen and pancreas removal) and more recent
DSS rate 38% for D1 vs 59% for D2). This survival trials (with spleen and pancreas preservation). As
benefit was even greater and close to reaching a concerns the short-term outcomes, overall hospital
statistical significance in the subgroup of patients with mortality was significantly higher for D2 patients (7.5%
both these two variables (T2-T4, N positive): 5-year vs 3.8% with RR of 2.02, p = 0.002); subsite analysis
OS rate was 35 % for D1 and 51% for D2, with p = showed that hospital mortality was still significantly
0.078, while 5-year DSS was 38% for D1 and 59% for higher for D2 patients in early trials (10.5% vs 4.6%,
D2 (p = 0.055). Therefore the authors concluded that p = 0.0003), while it was similar in recent trials (1.5%
D2 might be a better choice in patients with advanced for D1 vs 1.2% for D2, p = 0.70).
disease and lymph nodes metastasis (Table 3). The overall 5-year survival rate showed similar
[55]
Wu et al in 2004 published the first results of a results for D1 and D2 patients (43.5% and 44.9%,
trial comparing 110 patients undergoing D1 dissection p = 0.58). In subgroup analysis no significant
and 111 undergoing D3 resection and their respective difference was found between T1/T2 patients (55.4%
morbidity and mortality rates. The postoperative for D1 and 52.3% for D2, p = 0.46) while a trend
hospital stay was longer for D3 patients [mean (SD) of survival benefit in favour of D2 was identified for
19.6 (13.9) (range 10-98) d vs 15.0 (4.0) (range more advanced tumours (13.5% for D1 vs 19.5% for
10-30) d, p = 0.001]. Morbidity rate was higher in D2 in patients with T3/T4). In addition, the subgroup
the D3 group (17.1% vs 7.3%, p = 0.012), mainly of patients with spleen and pancreas preservation
due to a high incidence of abdominal abscess after showed a trend towards better survival rate with D2
D3 resection (8.1% vs 0%, p = 0.003). Patients with compared to D1 (54.9% vs 43.0%). The authors
hemipancreaticosplenectomy had a higher morbidity concluded that while older trials favoured D1, the more
rate (35.7% vs 10.6%, p = 0.017). In both group recent trials did not show any significant differences in
there was no operative mortality. The study confirmed mortality between the two procedures, demonstrating
the higher risk of complications after that extensive that D2 gastrectomy could be performed safely, mostly
dissections and suggested that extensive lymph node due to the preservation of spleen and pancreas.
[35]
dissection should be done by surgeons thoroughly In 2014 Jiang et al analysed 8 RCTs published
experienced in the technique. In 2006 the same between 1988 and 2010, with a total of 2044 patients
[56]
authors published the 5-year survival results: overall (1042 D1 and 1002 D2). D2 gastrectomy resulted
5-year survival was higher for D3 patients (59.5% associated with significantly greater morbidity in
vs 53.3%, p = 0.041). The authors concluded that terms of anastomotic leakage, pancreatic leakage,

reoperation rates, wound infection and pulmonary further evaluations before definitively rule out the
complications. The overall 5-year survival rate did PAN dissection by therapeutic options for treatment of
[88,89]
not show any significant difference between the advanced gastric cancer .
two groups. Overall postoperative mortality was Interestingly, in a recent phase Ⅱ trial from the
significantly lower in the D1 group (RR = 0.58, 95%CI: Stomach Cancer Study Group of the Japan Clinical
[90]
0.47-0.71, p < 0.001) but in subgroup analysis no Oncology Group , patients with locally advanced
difference was found between patients with pancreas gastric cancer with extensive regional (N2) nodes
and spleen preservation in D1 and D2 groups (RR = and/or PAN metastases were treated with neo-
1.35, 95%CI: 0.45-4.05 for pancreas resection; RR = adjuvant chemotherapy (S-1 plus cisplatin) followed
0.85, 95%CI: 0.47-1.54 for spleen resection), showing by extended surgery with PAN dissection. The 3- and
that the higher mortality associated with D2 in older 5-year overall survival rates were of 59 and 53 per
trials was highly influenced by spleen and/or pancreas cent, respectively.
resection. The authors reported also a trend towards Based on these results, Japanese surgeons are
a lower risk of gastric cancer-related death in D2 now suggesting that extended D2 plus PAN dissection
patients with spleen and pancreas preservation. after neo-adjuvant chemotherapy could be considered
Anyway, in the latest years the consensus on D2 as a promising treatment for patients with clinically
[28,57,64-78]
lymphadenectomy has increased worldwide , detected PAN involvement or with extensive N2 nodal
[91]
since a trend of improved survival among D2 patients metastases .
was recorded and published mainly due to spleen and Anyway, we need further evaluations regarding
pancreas preservation and to the increase of skillness the benefit of dissecting nodal stations other than PAN
and experience on D2 technique in high volume whose removal is currently no more indicated, and the
reference hospital. identification of subgroups of advanced gastric patients
evidence based medicine (EBM) and practical who may definitely benefit from D2+ dissection after
surgical experience seem now to move towards an neo-adjuvant chemotherapy.
international agreement: nowadays D2 procedure Indeed, according to the last version of Japanese
[4]
is recommended as the standard procedure by the guidelines , the standard D2 dissection does not
[3] [10] [79] [80] [81]
Japanese , Korean , German , British , Italian , include the removal of lymph nodes along the superior
[82]
European Society for Medical Oncology (ESMO) and mesenteric vein (No. 14v). Of note, No. 14v station
the joint ESMO- ESSO (European Society of Surgical was comprised in the N2 compartment for lower third
Oncology)- ESTRO (European Society of Radiotherapy gastric tumours in the second edition of Japanese
[83] [3]
and Oncology) guidelines ; in addition, more recently Classification and was part of the D2 dissection for
[84]
NCCN recommends D1+ or modified D2 also in the distal tumours in the JCOG9501 trial.
United States. But, even in the lack of specific evidences a D2+
No 14v nodes is, currently, considered only in case
of tumours with apparent metastases to infra-pyloric
D2+ FOR ADVANCED GASTRIC CANCER nodes. Recently, a Korean study
[92]
showed that 14v
Whether the extension of lymphadenectomy beyond lymph node dissection was an independent prognostic
the standard D2 dissection could add any benefit in the factor in patients with clinical stage Ⅲ /Ⅳ gastric
treatment of advanced gastric cancer, is a controversial cancer of the middle and lower third, therefore future
issue. investigations on this topic are necessary.
The routine lymphadenectomy of para-aortic Also, the dissection of posterior nodal stations (No.
nodes (PAN), which has been practiced extensively by 8p, 12p, 13), which were routinely removed during a
Japanese surgeons and in specialized Western centres super-extended (D3) lymphadenectomy and, in case
in the past decades, is currently no more indicated of retro-pancreatic (No. 13) nodes, were comprised
after the publication of the Japan Clinical Oncology in the standard D2 dissection for distal tumours in the
[85]
Group (JCOG) 9501 trial . Indeed, the results of the JCOG trial, is at present, no more indicated.
Japanese trial showed no survival benefit after D2 plus In a recent observational study of our GIRCG
PAN dissection compared to D2 lymphadenectomy group, super-extended (D3) lymphadenectomy
alone in advanced gastric cancer without clinical which included the systematic removal of posterior
[85]
suspicion of PAN metastases . stations (8p, 12p, 13, 16a2 and 16b1), was
Nevertheless, in the JCOG9501 trial, a rather high associated with a significant lower incidence of loco-
5-year survival (18.2%) was reported in patients regional relapses when compared to the standard
with positive PAN after a prophylactic PAN dissection. D2 dissection in advanced gastric cancer with
[93]
Also, similarly, in some Eastern and Western series, mixed-diffuse histology . These results suggest a
including cases with clinical involvement of PAN, long- possible therapeutic role of the dissection of posterior
term survivals were reported, after PAN dissection, in stations other than PAN (8p, 12p. 13). Moreover, we
[86]
patients with pathologically positive PAN , especially observed that subgroups of tumours with a greater
[87]
in the absence of incurable factors . lymphotropism are better controlled by a super-
Therefore, some authors suggested the need of extended lymphadenectomy. In our study none of the

patients had received preoperative chemotherapy. 1500 laparoscopic and 1500 open gastrectomies over
Based on these findings, dedicated randomized a 7-year period), comparing the long-term results of
[96]
trials are needed to provide specific evidences on laparoscopic with open approach .
the optimal extension and the indications of D2+ In this study, at a median follow-up of 70.8 mo
lymphadenectomy after neo-adjuvant chemotherapy the overall survival, disease-specific survival, and
in advanced gastric cancer. recurrence-free survival were not statistically different
except for patients with stage IA disease treated with
laparoscopic surgery, who showed an increased overall
LAPAROSCOPIC LYMPH NODE survival rate (laparoscopic group; 95.3%, open group:
DISSECTION 90.3%; P < 0.001) probably attributable to selection
bias.
In recent years, through the development of minimally
It is well known that the number of lymph nodes
invasive techniques and improvement of the devices
for laparoscopic surgery, several surgeons have started removed during gastrectomy is to be correlated with
applying laparoscopic assisted gastrectomy (LAG) for the prognosis of gastric cancer. In past years the
gastric cancer. number of lymph nodes collected during laparoscopic
Although several potential benefits of LAG compared lymphadenectomy was lower compared to open
to conventional open procedure - such as less post- lymphadenectomy. In recent years, through the
operative pain, cosmetics, less blood loss, faster improvement of laparoscopic surgical techniques and
recovery, and shorter hospital stay - minimal invasive skills of surgeons, the number of dissected lymph
surgery for gastric cancer has not yet achieved a nodes has gradually increased, reaching that observed
solid evidence-based validation; up to 2010, the after open gastrectomy.
[97]
Japanese Gastric Cancer Treatment Guidelines did not Ohtani et al in a meta-analysis conducted on
[97-100]
recommend LAG in a curative cancer resection setting, four randomized control studies comparing
but indicated laparoscopic gastrectomy just as an laparoscopic distal gastrectomy LADG with open
[4]
investigational procedure eligible for clinical trials . distal gastrectomy (ODG) for EGC, has shown that
To date, two prospective trials (KLASS 01, JCOG the number of harvested lymph nodes was higher
0703)
[94,95]
and several retrospective studies argue in the ODG group than in the LADG group, although
the safety and oncological feasibility of laparoscopic this difference was not statistical significant except
surgery for the treatment of EGC. The results of these in one of the four studies. A recent meta-analysis of
studies demonstrate both the reliability of laparoscopic eight case-control studies has revealed that there is
lymphadenectomy in terms of oncological radicality as no evident difference in the number of lymph nodes
[101]
well as the absence of differences in the complication dissected, between LADG and ODG . The mean
rate and short-term results between laparoscopic and operative time for LADG is significantly higher than
[102]
open surgery. Therefore, along with the demonstration ODG. Kodera et al has shown that the mean
that the number of harvested lymph nodes by LAG to operating time in the LADG group ranged from 196 to
date has increased up to reach that observed during 348 min, that appears to be certainly longer than the
open gastrectomy, laparoscopic gastric surgery has time needed to accomplish an ODG in all studies. This
now to be considered at least as “feasible”. finding could be due to the reduction of the field of
Most recent reports investigating the short-term view, lack of tactile sensation, and the steep learning
results of laparoscopic gastric surgery refer to EGC; curve needed for LADG. In the near future, with the
these data obviously can not be directly transferred to advancements in surgical techniques and laparoscopic
what is expected for advanced gastric cancer (AGC) devices, the time required for laparoscopic-assisted
and it is extremely important to differentiate the gastrectomy is probably going to decrease.
results related to early tumors from those related to
advanced tumors. Laparoscopic total gastrectomy
Differently from LADG, techniques for laparoscopic
EGC total gastrectomy (LTG) has not yet been standardized,
As concerns early gastric cancer a phase Ⅲ multicenter therefore it remains a challenging procedure. Some
[94]
prospective randomized trial (KLASS Trial) has technical difficulties involved in D2 lymphadenectomy,
concluded that there is no significance difference in such as a safe dissection of the No. 10 lymph nodes,
morbidity and mortality between laparoscopy assisted and a standardized laparoscopic anastomosis technique,
distal gastrectomy and open distal gastrectomy. may constitute an obstacle in applying laparoscopic
Possible disadvantages are the longer operative time surgery for proximal cancer.
[103]
and the steep learning curve for laparoscopic surgery. A recent metanalysis including eight non-RCTs
The same group to provide background data was published. There were compared the short term
for KLASS trial, present one of the largest case- results of 314 LTG and 384 open total gastrectomy
matched series, comprising about 3000 patients with (OTG) in patients with gastric cancer. In hospital
surgically resectable gastric cancer (approximately mortality rates were comparable between two groups

(LTG 0.9% - OTG 1.8%). denectomy in terms of oncological appropriateness and

Patients in LTG group, despite a longer operative the absence of differences as regards the incidence of
time, seem to have less intraoperative blood loss, less complications and short-term results between laparoscopic
postoperative complications, and shorter hospital stay and open approach, have allowed the transferral of
compared with OTG. the many advantages of mini-invasiveness to the
The results of this metanalysis showed that LTG treatment of early gastric cancer. This has been made
has better short-term outcomes compared with OTG. possible through the development of newly designed
Despite these encouraging results data on LTG are still operative techniques and the introduction of better
limited. In South Korea, a multicenter phase Ⅱ trial technological devices for laparoscopic surgery together
(KLASS-03) trying to assess the feasibility of LTG for with the undoubted improvement of surgical skills.
stage I gastric cancer is currently ongoing. Up to date laparoscopy assisted gastrectomy with D2
lymph node dissection for the treatment of advanced
AGC gastric cancer is a promising oncological procedure with
Another issue requiring further clarification is the adequate lymph node harvesting. The advantages of
application of laparoscopic surgery in AGC. Thus, if minimal invasion, including the reduced risks of surgical
laparoscopy gastrectomy (LADG) has been increasingly related trauma, the containment of blood loss, less
used for EGC and T1-T2 tumors, still it has been less postoperative pain and earlier recovery could lead to
investigated as regards AGC; it is currently matter a reduction in complications for difficult patients such
for debate if LAG with D2 lymphadenectomy should as those with advanced gastric cancer. Confirmation of
represent an appropriate treatment for an AGC as the appropriateness and safety of laparoscopic assisted
well
[104,105]
. Challenging technical issues could be gastrectomy for patients with advanced gastric cancer
represented by large-size tumors or tumors that are expected from the results of different prospective
require multiorgan resection. studies comparing the short- and long-term outcomes
To date, short-term results and complication (KLASS 02, CLASS 01, JLSSG 0901), which are
rate of laparoscopic gastrectomy with D2 lymph currently in progress.
nodes dissection for advanced gastric cancer are
still controversial. Many authors have reported no
ROBOT ASSISTED LYMPH NODE
difference between laparoscopic and open procedures
in terms of number of harvested lymph nodes
[106-108]
. DISSECTION
[109]
Shuang et al has reported a median number of Modern oncology offers a huge step forward in
35 lymph nodes dissected in the laparoscopic group more effective treatment of a cancer using modern
vs 38 in the open group, which is comparable to the and advanced equipment to improve the quality of
number reported by other authors who performed care
[116-120]
. The role of robotic gastric cancer surgery
[107,110,111]
laparoscopic surgery for AGC . Analyzing the is increasing, but still no strong and clear evidence
data in literature the postoperative morbidity rates of has been reported to support the superiority of this
LAG for advanced gastric cancer ranges from 7.7% approach over others. Clearly it shows advantages in
[94,112,113] [114]
to 31.5% . Cai et al has reported that comparison with laparoscopic by the use of twisted
the overall morbidity rates were 12.24% in the LAG instruments with 7 degrees of freedom and motion
and 19.15% in the OG groups, with no significant scaling, tremor filtering and 3D visualization images
difference. However, respiratory complications were of high resolution. It is clear that laparoscopy led us
more frequent in the OG group. with magnifying anatomical structures to perform
more precise lymphadenectomy. Using laparoscopical
Learning Curve approach surgeons had to face with limitation of
Another important issue for laparoscopic lympha movements, linear laparoscopic tools, tremor transfer
denectomy is the learning curve. In a recent korean of the surgeon’s hand to the tip of the forceps, and 2D
series, in order to improve lymphadenectomy skills visualization without proper sense of depth. Robotic
and decrease complications at least 42 gastrectomies surgery seems to solve all of these disadvantages. The
[96]
were required . high resolution image with 3D visualization technology
Therefore, an extensive case-load is required is especially useful in infrapyloric, suprapancreatic area
to individual surgeons in order to perform a safe and splenic hilum, where an adequate recognition of
laparoscopy assisted gastrectomy; a precise standar tiny anatomical structures during lymphadenectomy is
dization of laparoscopic procedures together with of the highest importance. The endowrist instruments
a considerable number of cases are needed for an might be especially helpful during lymphadenectomy
efficient educational system. Only the high-volume in suprapancreatic area where it seems to be more
certified centers can provide the number required to difficult in laparoscopic setting using linear instruments.
the clinical application and teaching of laparoscopic In retrospective studies in majority from eastern
[115]
techniques for gastric cancer . countries they compare laparoscopic and robotic
The achievement of reliability of laparoscopic lympha approach sometimes also with open technique. Woo et

[121]
al showed that robotic approach is associated with from robotic gastric cancer surgery. In paper by Suda
[132]
longer operative time. From the other hand less blood et al in comparison of laparoscopic with robotic
loss was observed during robotic surgery. Analyzing approach the local complications rate (robotic vs lap
morbidity (11%) and mortality (0.4%) there were 1.1% vs 9.8%, p = 0.007) and morbidity (2.3% vs
no difference between both techniques (p > 0.05). 11.4%, p = 0.009) were statistically significantly lower
Also the numbers of dissected lymph nodes were as robotic technique was used. These authors underline
[122]
similar. In paper by Kim et al that compared overall the fact that in their series no pancreatic fistulas were
complications, reoperation and mortality rates were reported. It is probably because of better anatomy
similar in open, laparoscopic and robotic approach. The visualization during lymphadenectomy and less
only difference was observed in anastomotic leakage traumatic access to the pancreatic parenchyma during
which was more common in minimally invasive than robotic tissue preparation. In multicentric prospective
in open approach (p = 0.017). It is probably because study from South Korea the authors compared robotic
[133]
of usage staplers that were not used in minimally with laparoscopic gastrectomy . The complications
invasive techniques. rates were similar, without mortality in both arms.
Currently we have few reviews and meta-analysis Robotic approach was associated with longer time of
that analyzed problem of advantages in using robotic operation and higher costs. The authors conclude that
[123-127]
surgery during gastrectomy . The results showed perioperative surgical outcomes in robotic technique
[134]
a lower amount of blood loss, but with longer time of are not superior to laparoscopic one. Noshiro et al
operation. An explanations underline that the docking analyzed using a monopolar scalpel in robotic lymph
time might be responsible for prolonging the operation, node dissection. They underlined a stable visualization of
and stable grasping and tissue retracting may help in the operative field that can help in better understanding
better recognition of anatomical structures that lead to of the anatomy and proposed to use a term “robotically-
safer and less bloody procedure. The prolonged time enhanced surgical anatomy”. The authors proved that
of operation is also associated with more complicated robotic operation was associated with lower blood loss
lymphadenectomy especially with comparison to and lower rate of pancreatic fistula.
open technique. It is worth to note that no significant The most difficult part of widely usage a laparo
difference was observed according to the number scopic approach in gastric surgery is a complicated
of harvested lymph nodes. Also no difference was lymphadenectomy, and it is difficult to implement
[135]
seen when analyzing overall complications rate and that into a routine practice . It seems that usage
mortality. of robotic may help in standardization of gastric
Analyzing survival we have only 2 non randomized cancer lymphadenectomy. The robotic approach may
studies that compare robotic with open approach and probably help in more precise and safer operation
one non-randomized study that compare laparoscopic especially of some most critical lymph nodes stations
[128-130]
and robotic one . In publication by Caruso et like No. 6, 5, 1, 14v, and suprapancreatic area with
[130] [136,137]
al no significant differences in overall survival rates stations 7, 8a and 9 . The greatest attention
[128]
was observed. Pernazza et al proved that robotic is directed to station nr 6 and suprapancreatic area
surgery was associated with improved survival in because of its dissection is close to anterior surface of
comparison with open technique. This improvement the pancreas. The anatomical differences in this area
[138]
was observed especially in advanced gastric cancer presented by Haruta et al might be responsible for
[129]
patients. In paper by Pugliese et al 5-years survival technical problems in this area. Any mistake in this
was 85% for robotic and 75% for laparoscopic but area may lead to pancreatic parenchyma penetration
without statistical significance. followed by pancreatitis with local fistula and even a
[127] [138]
Marano et al analyzed technical benefits of robotic leakage if the duodenal stump . Another difficult
approach in gastric cancer surgery. They emphasized lymph node station dissection is number 10 in splenic
the improvement in performing lymphadenectomy in hilum. Problems with bleeding in this area often lead
infrapyloric, suprapancreatic region, in splenic hilum to perform splenectomy. Robotic approach probably
[131]
and superior mesenteric vein. In paper by Son et al might help in better recognition of the anatomical planes
where they compared spleen preserved robotic and and safer dissection even in mostly dangerous areas.
laparoscopic D2 gastrectomy no difference between Another point of interest is a usage of robotic
these two approaches was observed in terms of technique in obese patients especially that in western
number of dissected lymph nodes, complications countries many patients show high body mass index
rate, and mortality rate. Interestingly they observed (BMI) status. Theoretically obese patients may have a
higher number of retrieved lymph nodes along splenic benefit form robotic approach because of technically
artery and splenic hilum in robotic approach. Higher demanding D2 lymphadenectomy especially around
number of retrieved lymph nodes was not associated vessels when a fatty tissue might be a problem in
with improvement in survival but of course led to adequate exposition of the surgical field. In paper by
[139]
improvement in staging of the disease. Seems that Park et al patients were classified to obese and
lower morbidity might be the most important benefit non-obese group according to visceral fat area (VFA).

Interestingly the complete number of total and N2 area and retrospective studies, in the west three RCTs (MRC,
lymph node number was higher in non-obese patients Dutch and IGCSG trials) have been conducted to show
2
with VFA < 100 cm . There were no differences a survival benefit of D2 over D1 with EBM. While the
in obese patients. Statistically significant robotic MRC trial failed to show a survival benefit after the
approach was associated with lower rate of severe D2 procedure, mostly due to the significant increase
complications after total gastrectomy in non-obese of postoperative morbidity and mortality, which was
patients. The problem of obesity was also analyzed referred to splenopancreatectomy, the Dutch trial
[140]
by Lee et al . They compared subtotal gastrectomy could report a significant decrease of recurrence after
with D2 lymphadenecotmy in laparoscopic and D2 procedure at 15 years from the conclusion of its
robotic approach in patients of different BMI status. accrual. Recently, also the long term survival analysis
In different BMI groups no significant difference in the of the Italian RCT could demonstrate a benefit for
rate of dissection of more than 25 nodes was observed patients with AGC and positive nodes treated with D2
between two techniques, but it is worth not note that gastrectomy without splenopancreatectomy.
laparoscopic approach had a significantly lower rate of As nowadays also in western countries D2 pro
retrieving more than 25 nodes in high BMI patients (p cedure can be done safely with pancreas preserving
= 0.006). In high BMI patients the complications rate technique and without preventive splenectomy, it has
was comparable. been suggested in several national guidelines as the
Even as the role of extended lymphadenectomy recommended procedure for patients with AGC.
in gastric cancer is still under debate no doubts this
technique requires high level of experience. The full
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P- Reviewer: Ohkohchi N S- Editor: Gong ZM L- Editor: A

E- Editor: Zhang DN

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com/esps/ World J Gastroenterol 2016 March 14; 22(10): 2875-2893

2016 Gastric Cancer: Global view

Gastric cancer: Current status of lymph node dissection

Karol Polom, Department of Surgery, Wielkopolskie Centrum

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ANATOMICAL BORDERS OF LOCO-

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Table 2 Anatomical definitions of lymph node stations

LNs: lymph nodes.

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reported. treatment for patients with resectable gastric cancer

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Table 3 Results of randomised controlled trials on D1 vs D2 gastrectomy

RCT Nr. pts Morbidity (%) Mortality (%) Survival (%)

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(LTG 0.9% - OTG 1.8%). denectomy in terms of oncological appropriateness and

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65-72 [PMID: 20954197 DOI: 10.1002/bjs.7266] 10.3748/wjg.v20.i14.3880]

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