This document discusses the lymphatic drainage systems of the stomach and classifications of lymph nodes that drain the stomach. It describes the Japanese classification system for lymph nodes in detail. It then discusses staging systems used for gastric cancer and the importance of lymph node metastasis as a prognostic factor. The major focus is on the extent of lymph node dissection for gastric cancer, including definitions of D1, D1+, D2, and D3 dissection. It provides details on the lymph nodes dissected for different types of gastrectomy and indications for different levels of lymph node dissection.

1. MANAGEMENT OF METASTATIC
LYMPH NODES IN GASTRIC
CANCER
BY
DR. HAYTHAM FAYED
A. PROFESSOR OF SURGICAL ONCOLOGY
ALEXANDRIA UNIVERSITY

2. Gastric lymphatics
The lymphatics of the stomach can
be divided into three systems:
1. Intramural.
2. Intermediary.
3. Extramural.

3. Gastric lymphatics
Extramural system
Zone 1.
Zone 2.
Zone 3.
Zone 4

4. Japanese classification of lymph nodes draining the stomach
No 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

5. Japanese classification of lymph nodes draining the stomach
No definition
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
12d 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

6. Japanese classification of lymph nodes draining the stomach
No definition
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

7. Japanese classification of lymph nodes draining the stomach
No definition
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

8. Staging Systems of gastric carcinoma
Two major staging systems are commonly used in gastric cancer, as follows:
• The tumor-node-metastasis (TNM) system, developed by the International
Union Against Cancer (UICC) and the American Joint Committee on Cancer
(AJCC)
• The Japanese Research Society staging, is more elaborate and is based on
anatomic involvement, particularly the lymph node stations..
• Both the NCCN and ESMO use the TNM system for staging

10. • In gastric cancer, the presence or absence of lymph node metastasis is
one of the most important prognostic indicators in patients following
curative resection.
• More than 50% of gastric cancer patients have lymph node
metastases at diagnosis, which lead to a 5-year survival rate < 30%.

11. Although several investigators reported that the minority of lymph
node-negative gastric cancer patients had recurrence and poor
survival, most investigators demonstrated that the prognosis of
lymph node-negative gastric cancer patients was significantly better
than that of lymph node-positive patients

12. The major controversy in gastric cancer surgery now is in
regard to the extent of lymph node dissection
necessary to accomplish cure

13. • D2 lymph node dissection in gastric cancer achieves better
locoregional tumor control than limited (D1) lymphadenectomy, but
its influence on survival is controversial.
• The value of D2 resection is unproven in randomized trials.
Evidence of survival benefit of extended (D2) lymphadenectomy in Western patients with gastric cancer based on a new concept: A
prospective long-term follow-up study
Dimitrios H. Roukos, MD, Mathias Lorenz, MD, and Albrecht Encke, MD, Ioannina, Greece, and Frankfurt, Germany

14. Gastrectomy plus extended removal of 2nd station lymph nodes (D2)
lymphadenectomy has been accepted as the standard surgical
procedure for potentially curative resection in Eastern countries,
especially Japan
Meta-Analysis of Effectiveness and Safety of D2 Plus Para-Aortic Lymphadenectomy for Resectable Gastric Cancer
Xin-Zu Chen, MD, Jian-Kun Hu, MD, PhD, Zong-Guang Zhou, MD, PhD, FACS, Yuan-Yi Rui, MD, Kun Yang, MD, LiWang, PhD, Bo Zhang,
MD, PhD, Zhi-Xin Chen, MD, Jia-Ping Chen, MD

15. • To date, little evidence exists from prospective randomized trials to
confirm the advantage of extended lymph node dissection compared
to limited lymphadenectomy.
• Despite that, long-term results after D2 and D2+ lymphadenectomy
reported by Japanese as well as by dedicated Western centers are
definitely better compared to European and US results.
Super-extended (D3) lymphadenectomy in advanced gastric cancer
F. Roviello a, C. Pedrazzani a,*, D. Marrelli a, A. Di Leo b, S. Caruso a, S. Giacopuzzi b, G. Corso a, G. de Manzoni b
EJSO 36 (2010) 439e446

16. • Recently a Cochrane review concluded that “randomised studies
show no evidence of overall survival benefit” after D2 dissection, “but
possible benefit in T3+ tumors.
• These results may be confounded by surgical learning curves.
Risk factors for operative mortality and morbidity in gastric cancer undergoing D2-gastrectomy
Ferda N. Koksoy*, Dogan Gonullu, Oguz Catal, Erol Kuroglu
Ministry of Health, Taksim Training and Research Hospital, Department of Surgery, Istanbul, Turkey

17. Lymph node dissection
Extent of lymph node dissection
• The extent of systematic lymphadenectomy is defined as follows
according to the type of gastrectomy conducted.
• When the extent of lymphadenectomy performed does not fully
comply with the D level criteria, the lymph node station that has been
additionally resected or left in situ could be recorded as in the
following examples: D1 (?No. 8a), D2 (-No. 10).

18. Lymph node dissection
Extent of lymph node dissection
Total gastrectomy
D0: Lymphadenectomy less than D1.
D1: Nos. 1–7.
D1+: D1 + No. 8a, 9, 11p.
D2: D1 + No. 8a, 9, 10, 11p, 11d, 12a.
For tumors invading the esophagus, D1+
includes: No. 110*, D2 includes No. 19, 20,
110 and 111.
The extent of lymphadenectomy after total
gastrectomy. The numbers correspond to the
lymph node station as defined in the Japanese
Classification of Gastric Carcinoma
Complete dissection of the nodes in blue
denotes D1 dissection, the nodes in orange
D1+ and the nodes in red D2

19. Lymph node dissection
Extent of lymph node dissection
Distal gastrectomy
D0: Lymphadenectomy less than D1.
D1: No. 1, 3, 4sb, 4d, 5, 6, 7
D1+: D1 + No. 8a, 9
D2: D1 + No. 8a, 9, 11p, 12a.
The extent of lymphadenectomy after distal
gastrectomy. The numbers correspond to the
lymph node station as defined in the Japanese
Classification of Gastric Carcinoma.
Complete dissection of the nodes in blue
denotes D1 dissection, the nodes in orange
D1+ and the nodes in red D2

20. Lymph node dissection
Extent of lymph node dissection
Pylorus-preserving gastrectomy
D0: Lymphadenectomy less than D1.
D1: No. 1, 3, 4sb, 4d, 6, 7.
D1+: D1 + No. 8a, 9 The extent of lymphadenectomy after pylorus-
preserving gastrectomy. The number
correspond to the lymph node station as
defined in the Japanese Classification of
Gastric Carcinoma.
Complete dissection of the nodes in blue
denotes D1 dissection and the nodes in
orange D1+

21. Lymph node dissection
Extent of lymph node dissection
Proximal gastrectomy
D0: Lymphadenectomy less than D1.
D1: No. 1, 2, 3a, 4sa, 4sb, 7.
D1+: D1 + No. 8a, 9, 11p.
For tumors invading the esophagus, D1 + includes No.
110*.
No. 110 lymph nodes (lower thoracic para-esophageal
nodes) in gastric cancer invading the esophagus are
those attached to the lower part of the esophagus that
is removed to obtain a sufficient resection margin.
The extent of lymphadenectomy after
proximal gastrectomy. The numbers
correspond to the lymph node station as
defined in the Japanese Classification of
Gastric Carcinoma. Complete dissection of the
nodes in blue denotes D1 dissection and the
nodes in orange D1+

22. Lymph node dissection
Extent of lymph node dissection
Indications for lymph node dissection
In principle, a D1 or a D1+ lymphadenectomy is indicated for cT1N0
tumors and D2 for cN+ or cT2-T4 tumors.
Since the pre- and intraoperative diagnoses of lymph node
metastases remain unreliable, a D2 lymphadenectomy should be
performed whenever nodal involvement is suspected.

23. Lymph node dissection
Extent of lymph node dissection
Indications for lymph node dissection
D1 lymphadenectomy
A D1 lymphadenectomy is indicated for T1a tumors that do not
meet the criteria for EMR/ ESD, and for cT1bN0 tumors that are
histologically of differentiated type and 1.5 cm or smaller in
diameter

24. Lymph node dissection
Extent of lymph node dissection
Indications for lymph node dissection
D1+ lymphadenectomy
A D1+ lymphadenectomy is indicated for cT1N0 tumors other than
the above.

25. Lymph node dissection
Extent of lymph node dissection
Indications for lymph node dissection
D2 lymphadenectomy
A D2 lymphadenectomy is indicated for potentially curable T2-T4 tumors as well as
cT1N+ tumors.
The role of splenectomy for complete resection of Nos. 10 and 11 nodes had long
been an issue of controversy, and the final results of a randomized trial (JCOG 0110)
are awaited.
In the meantime, complete clearance of No. 10 nodes by splenectomy should be
considered for potentially curable T2-T4 tumors invading the greater curvature of the
upper stomach

26. Lymph node dissection
Extent of lymph node dissection
Indications for lymph node dissection
D2+ lymphadenectomy
Gastrectomy with extended lymphadenectomy beyond D2 is
classified as a non-standard gastrectomy.