Lymphadenectomy—D1, D2, and D3

Fig. 13.1

Lymph node stations as described by the JRSGC

Table 13.1

Lymph node stations and their anatomical borders [5]

Station	Description	Anatomical border
1	Right cardiac	Perigastric nodes on the right side of the cardia. Nodes along the cardioesophageal branch of the left gastric artery, from its origin to the esophageal hiatus
2	Left cardiac	Perigastric nodes on the left side of the cardia
3	Lesser curvature	Nodes along the inferior branch of the left gastric artery and along the right gastric artery distal to the first gastric branch
4	Greater curvature	This location is divided into a left (s) and a right (d) part defined by the water shed. The left part is divided into a proximal (sa) and a distal part (sb). 4sa is located around the short gastric arteries and 4sb are the nodes along the left gastroepiploic artery. 4d is located along the right gastroepiploic artery distal to the first gastric branch
5	Suprapyloric	Nodes at the origin of the right gastric artery including the first gastric branch
6	Infrapyloric	Perigastric nodes on the greater curvature of the pylorus. Nodes along the gastroepiploic vessels from their origin to their first gastric branches. The origin of the vein is situated just after the gastrocolic trunk
7	Root left gastric artery	Nodes on the left gastric artery from its origin to the bifurcation into the cardioesophageal and lower branch
8	Common hepatic artery	Nodes around the common hepatic artery from the celiac trunk to the branching off of the gastroduodenal artery
9	Celiac axis	All nodes on the celiac axis including the origins of the common hepatic and splenic artery
10	Splenic hilum	All nodes at the splenic hilus, distal to the pancreas tip. At the lower pole, the first gastric branch of the left gastroepiploic artery defines the border between 10 and 4sb
11	Splenic artery	Nodes along the splenic vessels up to the distal end of the pancreas tail. These nodes are divided into proximal (p) and distal (d) nodes
12	Hepatoduodenal ligament	Group number 12 is divided up in three parts: 1. left side of the hepatic artery (12a), 2. right side of the ligament and posterior to the choledochal duct (12b) and 3, just posteriorly to the portal vein (12p)
13	Retropancreatic	Nodes along the superior and inferior posterior pancreaticoduodenal arteries on the posterior side of the pancreas. The portal vein marks the lateral left border of this location. The upper border of location 13 coincides with 12b and 12p
14	Root of mesentery	Nodes along the superior mesenteric vessels. The lateral border is confined by the bifurcation of the gastrocolic trunk, the lower border by the branching off of the jejunal veins and the upper border is typified by the origin of the superior mesenteric artery
15	Middle colic vein	Nodes in the transverse mesocolon
16	Para-aortic	Nodes around the abdominal aorta and inferior caval vein. Right and left border are defined as the hili of the left and right kidney

Regional lymph nodes are further classified into four groups, based on the location of the primary tumor. Nodes closest to the tumor are classified as N1, followed by N2 nodes further away from the primary tumor, followed by N3 and N4. The N type of lymph node station also depends on the primary location of the tumor, which is specified in Table 13.2.

Table 13.2

Lymph node groups by tumor location [4]

Lymph node station	Location	LMU/MUL MLU/UML	LD/L	LM/M/ML	MU/UM	U	E+
No. 1	Rt paracardial	1	2	1	1	1
No. 2	Lt paracardial	1	M	3	1	1
No. 3	Lesser curvature	1	1	1	1	1
No. 4sa	Short gastric	1	M	3	1	1
No. 4sb	Lt gastroepiploic	1	3	1	1	1
No. 4d	Rt gastroepiploic	1	1	1	1	2
No. 5	Suprapyloric	1	1	1	1	3
No. 6	Infrapyloric	1	1	1	1	3
No. 7	Lt gastric artery	2	2	2	2	2
No. 8a	Ant comm hepatic	2	2	2	2	2
No. 8b	Post comm hepatic	3	3	3	3	3
No. 9	Celiac artery	2	2	2	2	2
No. 10	Splenic hilum	2	M	3	2	2
No. 11p	Proximal splenic	2	2	2	2	2
No. 11d	Distal splenic	2	M	3	2	2
No. 12a	Lt hepatoduodenal	2	2	2	2	3
No. 12b,p	Post hepatoduod	3	3	3	3	3
No. 13	Retropancreatic	3	3	3	M	M
No. 14v	Sup mesenteric v.	2	2	3	3	M
No. 14a	Sup mesenteric a.	M	M	M	M	M
No. 15	Middle colic	M	M	M	M	M
No. 16a1	Aortic hiatus	M	M	M	M	M
No. 16a2,b1	Para-aortic, middle	3	3	3	3	3
No. 16b2	Para-aortic, caudal	M	M	M	M	M
No. 17	Ant pancreatic	M	M	M	M	M
No. 18	Inf pancreatic	M	M	M	M	M
No. 19	Infradiaphragmatic	3	M	M	3	3	2
No. 20	Esophageal hiatus	3	M	M	3	3	1
No. 110	Lower paraesophag	M	M	M	M	M	3
No. 111	Supradiaphragmatic	M	M	M	M	M	3
No. 112	Post mediastinal	M	M	M	M	M	3

U upper 1/3, M middle 1/3, L lower 1/3

The type of lymphadenectomy depends on the lymph node stations that are removed. In a limited D1 dissection, the stomach with the primary tumor and perigastric (N1) lymph nodes are removed. For a D2 lymphadenectomy, the nodes along the left gastric, the common hepatic, the splenic, and the left hepatoduodenal artery are also removed, as well as some stations that differ for proximal, middle, and distal tumors (N2 nodes). In previous versions, it was recommended to perform a distal pancreaticosplenectomy with every D2 dissection. This has been abandoned and is now only advised for tumors with invasion of the greater curvature. With a D4 dissection, the N1 and N2 nodes are removed with the para-aortic nodes.

Randomized Controlled Trials on the Extent of Lymph Node Dissection

The key point of the debate on the extent of lymphadenectomy for gastric cancer has always been the balance between maximum locoregional control and acceptable morbidity and mortality . In Japan, an extended D2 lymph node dissection has been the standard of care for decades and is generally performed by experienced surgeons in specialized centers. Western surgeons have lower annual caseloads (except for a few high-volume centers) and mostly performed a more limited D1 dissection because of the higher morbidity and mortality associated with extended lymphadenectomy performed in low volumes. As Japanese long-term survival results were impressively better compared with those of the West [6], several groups decided to perform trials comparing a D1 with D2 lymphadenectomy. A summary of all described trials is given in Table 13.3 .

Table 13.3

Randomized studies on the extent of lymph node dissection in gastric cancer

Trial	Country	N	Comparison	Morbidity	Mortality	Overall survival
Dent [7]	South Africa	43	D1 versus D2	–	0 versus 0 %	At 3.1 years: 82 versus 77 % not significant
Robertson [8]	Hong Kong	55	D1 versus D2	0 versus 23 % relaparotomies	0 versus 3 %	At 4.1 years: 46 versus 38 % P = 0.04
Cuschieri [9, 10]	UK	400	D1 versus D2	28 versus 46 % P < 0.001	6.5 versus 13 % P = 0.04	At 5 years: 35 versus 33 % not significant
Bonenkamp [11, 13, 14]	Netherlands	711	D1 versus D2	25 versus 43 % P < 0.001	4 versus 10 % P = 0.004	At 15 years: 21 versus 29 % P = 0.34 Gastric cancer specific survival 48 versus 37 % P = 0.01
Wu [16]	Taiwan	221	D1 versus D3	7.3 versus 17.1 %	0 versus 0 %	At 5 years: 53.6 versus 59.5 % P = 0.041
Sano [1818, 19]	Japan	523	D2 versus D2+ para-aortic	20.9 versus 28.1 % P = 0.067	0.8 versus 0.8 %	At 5 years: 69.2 versus 70.3 % P = 0.85
Degiuli[20, 21]	Italy	267	D1 versus D2^a	12.0 versus 17.9 % P = 0.178	3.0 versus 2.2 % P = 0.722	At 5 years: 66.5 versus 64.2 % P = 0.695

^a D2 without routine distal pancreaticosplenectomy

South Africa

Dent et al. performed the first study between 1982 and 1987 in South Africa. In this randomized trial, 403 patients were evaluated for surgery. The majority of patients were ineligible due to advanced disease, and 43 patients were randomized between a D1 resection and a D2 resection. Although there was no in-hospital mortality, patients in the D2 group had a significantly longer operating time, a greater blood transfusion requirement, and had a longer hospital stay. With a median follow-up of 3.1 years, no differences in survival were detected between the two study arms. The authors concluded that a D2 lymphadenectomy should not be performed in daily clinical practice [7].

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