location matters: ligaments and lymphatic … · location matters: ligaments and lymphatic pathways...

Jennifer J. Young, MD, MPH1, Anokh Pahwa, MD2, Maitraya Patel, MD1,2, Matilda Jude, MD2,

Monica Deshmukh, MD2, Michael Nguyen, MD2, Shaden F. Mohammad, MD2

1UCLA Department of Radiological Sciences, David Geffen School of Medicine

2Olive View-UCLA Medical Center, Department of Radiology

No relevant financial disclosures

LOCATION MATTERS: LIGAMENTS

AND LYMPHATIC PATHWAYS IN

STAGING OF GASTRIC

ADENOCARCINOMA

EDUCATIONAL GOALS AND TARGET AUDIENCE

1. Review gastric anatomy

2. Identify spread of disease via perigastric ligaments

3. Describe pathways of lymphatic involvement

4. Correlate imaging of gastric adenocarcinoma with the new

American Joint Committee on Cancer (AJCC) staging system

and summarize prognostic and management implications

• Target audience: practicing Radiologists, Gastroenterologists,

Residents and Fellows in training.

• More than 988,000 cases of gastric cancer annually worldwide. 5 th most

common cause of cancer-related mortality in Western populations.

• Adenocarcinoma is the most common histology of gastric cancer in the

United States, comprising >90% of new diagnoses.

• 65% of patients in the US present at an advanced stage (T3/T4) with nearly

85% of those accompanied by lymph node metastasis.

• CT and endoscopic ultrasound (EUS) are important tools in the preoperative

evaluation, with complete staging achieved at the time of surgery.

• Local, extra-gastric regional and distant involvement have clinical

implications in patient management and prognosis.

• It is vital for the Radiologist to be aware of the new American Joint

Committee on Cancer (AJCC) TNM (tumor, node, metastasis) staging system

for gastric cancer, to accurately stage the disease and help guide patient

management.

BACKGROUND INFORMATION

GASTRIC ANATOMY

Image courtesy of Lisa Nishiyama and Christina Ma, MD

EMBRYOLOGY OF THE STOMACH AND

LIGAMENTS

• The stomach is derived from the primitive foregut

and is suspended by the:

• Ventral mesogastrium- attaches the foregut

to the anterior abdominal wall and forms:

• Falciform ligament (FL)

• Gastrohepatic ligament (GHL)

• Hepatoduodenal ligament (HDL)

• Dorsal mesogastrium- connects the foregut

to the posterior abdominal wall and forms:

• Gastrocolic ligament (GCL)

• Gastrosplenic ligament (GSL)

• Splenorenal ligament (SRL)

Embryologic development of peritoneal

organs and ligaments

Adult position of peritoneal organs and

ligaments

GSLSRL

Liver

Stomach

Spleen

FL

GHL

Pancreas

GHL

GSL

SRL

Liver Stomach

Spleen

FL

Pancreas

EMBRYOLOGY OF THE STOMACH AND

PERIGASTRIC LIGAMENTSSagittal view shows the gastrocolic ligament,

greater omentum and transverse mesocolon.

GCL

Greater

omentum

Transverse

mesocolon

Stomach

Pancreas

Transverse colon

Stomach

Liver

GHL

HDL

The gastrohepatic and hepatoduodenal ligaments

are continuous and form the lesser omentum and

the anterior border of the lesser sac. The

hepatoduodenal ligament contains the portal triad.

PERIGASTRIC LIGAMENTS

Ligament Course Associated vasculature

Gastrohepatic ligament Left hepatic lobe to lesser

curvature of stomach

Left gastric artery and vein

Hepatoduodenal

ligament

Hepatic hilum to the lesser

curvature of the stomach

Hepatic artery, portal vein,

extrahepatic bile ducts

Gastrocolic ligament Greater curvature of the

stomach to transverse

colon

Right and left

gastroepiploic arteries

Greater omentum Fatty apron from the

transverse colon covering

the small bowel

Epiploic arteries and

branches of the


Gastrosplenic ligament Fundus and proximal body

of stomach to splenic

hilum

Short gastric and left


Splenorenal ligament Spleen to tail of pancreas Distal splenic artery and

proximal splenic vein

PERIGASTRIC LIGAMENTS ON CT

Hepatoduodenal ligament

Gastrohepatic ligament

Perigastric ligaments contain blood vessels (arteries, veins, lymphatics), lymph nodes, and nerves

Hepatoduodenal ligament Gastrocolic ligament Greater omentum

Gastrosplenic ligament Splenorenal ligament

A B C D

EF

Axial, coronal and sagittal CECT demonstrates the location of the: (A) gastrohepatic ligament with the left gastric artery as anatomic

landmark (green arrow), (B) hepatoduodenal ligament with portal vein and hepatic artery as anatomic landmarks (blue arrow), (C)

gastrocolic ligament containing gastroepiploic vessels (yellow arrow) (D) greater omentum extending from the transverse colon and

covering the small bowel (pink arrows). (E) gastrosplenic ligament containing left gastroepiploic arteries (purple arrow) and (F)

splenorenal ligament containing distal splenic artery and proximal splenic vein (orange arrow).

F

PRE-OPERATIVE STAGING

Gastric cancer spreads through the

following mechanisms:

• 1. Regional: directly to contiguous

organs or through perigastric ligaments.

• 2. Distant: lymphatic, hematogenous, or

peritoneal

Patients are staged using a combination of:

• Endoscopic evaluation with endoscopic

ultrasound (EUS)

• CT of the chest, abdomen, and pelvis

• If results are equivocal for distant

disease:

• Staging laparoscopy

• PET-CT - not helpful for

locoregional disease, but detects

metastatic disease

AMERICAN JOINT COMMITTEE ON CANCER (AJCC): Gastric Cancer TNM

Staging System

• 7th edition released in 2009

• TNM staging system goals:

• Delineating anatomic markers for categorizing esophageal versus proximal gastric cancers

• Consistency in staging with other GI tract malignancies

• Worldwide applicability for gastric cancer cases in Asian countries and Western countries

7TH AJCC GASTRIC CANCER STAGING SYSTEM

UPDATE TO TUMOR LOCATION

• Cancers with the tumor epicenter within the

proximal 5 cm of the stomach that DO cross

the esophagogastric (EG) junction are now

staged using esophageal cancer system.

• Cancers with the tumor epicenter within the

proximal 5 cm of the stomach that DO NOT

cross the esophagogastric junction are

staged using gastric cancer system.

• Rationale: The 6th edition left the

classification of a tumor as esophageal or

gastric to the discretion of the physician.

Though controversial, the new system

standardizes the classification.

Esophageal cancer. Coronal and axial CECT demonstrate marked thickening

of the gastric cardia with extension into the distal esophagus (green arrows).

Based on the 7th AJCC, this is esophageal cancer as the tumor arises within

the proximal 5 cm of the stomach AND crosses the EG junction.


UPDATES TO TUMOR STAGING• Several Tumor (T) categories have been

upstaged.

• Rationale:

• T categories have been harmonized with

those of the esophagus, small and large

intestine.

• Tis reclassified as T1a since lymph node

metastasis may be present when tumor is

confined to the lamina propria, due to

abundance of lymphatic channels in the

gastric mucosa.

• T2b has been reclassified as T3, and T3

as T4a to reflect shorter 5-year survival for

subserosal and serosal invasion.

T-staging of gastric cancer, AJCC 7th manual.

T1a

Tumor invades the lamina propria or muscularis

mucosa. Previously Tis (in situ).

T1b Tumor invades the submucosa.

T2 Tumor invades the muscularis propria.

T3 Tumor penetrates the subserosal connective

tissue, extends into the gastrohepatic and

gastrocolic ligaments, or into the greater or lesser

omentum, without perforation of the visceral

peritoneum. Previously T2b.

T4a Tumor invades the serosa (visceral peritoneum).

Previously T3.

T4b Tumor invades adjacent structures, such as the

spleen, transverse colon, liver, diaphragm,

pancreas, abdominal wall, adrenal gland, kidney,

small intestine, and retroperitoneum.

TUMOR STAGING• Anatomically, the stomach has multiple layers,

however on CECT portal venous phase we visualize

only three layers :

• Mucosa

• Muscularis mucosa

• Submucosa

• Muscularis propria

• Subserosa

• Serosa

Enhancing layer

Enhancing layer

Hypoenhancing layer

• CT limitations:

• Limited in differentiating T1a from T1b

• Limited in differentiating T3 from T4a

• EUS is more effective for delineating these stages

Tumor (T) staging by CT:

T1a Not visible on CT.

T1b Mucosal thickening and enhancement. Preserved hypoenhancing submucosal

stripe.

T2 Loss of submucosal hypoenhancing stripe.

T3 Contiguous spread of disease into the perigastric ligaments, greater or lesser

omentum.

T4a Linitis plastica, infiltration of the surrounding peritoneal fat.

T4b Contiguous spread to adjacent organs and structures.

T2 tumor: Axial CECT

shows normal layers of the

greater curvature (green

and blue arrows, yellow

star), and diffuse

enhancement and

thickening of the lesser

curvature and gastric

antrum with loss of

hypoenhancing submucosal

stripe (purple arrows).

Adenopathy is present

(white arrow).

T2 tumor: Coronal CECT demonstrates circumferential wall

thickening of the gastric antrum with loss of the normal

hypoenhancing submucosal stripe (yellow arrow). Note

normal appearance of gastric fundus (white arrow).

T2 TUMOR

Hepatoduodenal ligament

T3 tumor: Axial CECT demonstrates

diffuse gastric wall thickening with soft

tissue infiltration along the gastrocolic

ligament containing gastroepiploic vessels

(yellow arrow). There is extension into the

gastrohepatic ligament (green arrow) and

into the gastrosplenic ligament containing

short gastric arteries (orange arrow).

Gastrocolic, gastrohepatic and

gastrosplenic ligaments Gastrohepatic ligament

T3 tumor: Axial CECT demonstrates lesser

curvature thickening with extension into the

gastrohepatic ligament encasing the left

gastric artery (green arrow).

TUMOR STAGING- T3

T3 tumor: Coronal CECT demonstrates

diffuse thickening and enhancement of

the gastric fundus (white arrow) with

extensive extragastric spread of disease

including periportal extension of tumor

along the hepatoduodenal ligament to

the liver with narrowing of the portal vein

(blue arrow). Adenopathy is present

(purple arrows).

T4a tumor. Axial CECT demonstrates marked

thickening of the gastric body and soft tissue

infiltration of the peritoneal fat in the left upper

quadrant (orange arrow). Direct spread along the

gastrohepatic ligament containing left gastric

artery (green arrow), gastrosplenic ligament

containing left gastroepiploic vessels (blue arrow), and splenorenal ligament containing distal splenic

artery and proximal splenic vein (purple arrow) is

present.

TUMOR STAGING- T4A

T4a tumor: Axial CECT

demonstrates linitis plastica

with marked diffuse

thickening and

enhancement of the

stomach invading the

subserosa and serosa

without invading adjacent

structures (red arrow).

T4a tumor: Axial CECT

shows marked thickening

and enhancement of the

gastric antrum with

infiltration of the peritoneal

fat (orange arrow).

T4b tumor: Axial CECT demonstrates marked

diffuse gastric thickening invading the

pancreas (red arrow). Tumor extends along

the hepatoduodenal ligament (peach arrow).

T4b tumor: Coronal CECT

demonstrates marked diffuse gastric

thickening invading the left hepatic lobe

(yellow arrow). Tumor extends into the

gastrocolic ligament (brown arrow) and

has metastasized to the liver (pink

arrow).

TUMOR STAGING- T4B

T4b tumor: Axial CECT demonstrates

diffuse mural thickening of the stomach

with fistulization between the gastric body

and a thickened colonic splenic flexure

(green arrow).

T4b tumor: Axial CECT

demonstrates asymmetric

mural thickening of the

gastric fundus with soft

tissue infiltration along the

celiac axis (orange arrow)

and left adrenal gland (blue

arrow).

• Upstaging in number of involved lymph nodes

• Rationale: In many centers, particularly in the US and Europe,

less than 15 lymph nodes are dissected, limiting the ability to

stage patients. The new system adjusts guidelines.


UPDATES TO NODAL STAGING

N- Staging of gastric cancer, AJCC

6th manual

N N- Staging of gastric cancer, AJCC

7th manual

No regional lymph node metastasis N0 No regional lymph node metastasis

Metastasis in 1 to 6 regional lymph

nodes

N1 Metastasis in 1 to 2 regional lymph

nodes

Metastasis in 7 to 15 regional lymph

nodes

N2 Metastasis in 3 to 6 regional lymph

nodes

Metastasis in ≥16 regional lymph

nodes

N3 Metastasis in 7 or more regional lymph

nodes

NODAL STAGING

• High frequency of lymph node involvement at

diagnosis- 5-24% of early gastric cancer (T1) can

have lymph node involvement.

• Prognosis depends on the total number and

regional versus metastatic location of lymph nodes.

• Lymph nodes are divided into 23 stations by

Japanese Gastric Cancer Association (JGCA), for

purposes of staging regional (N) versus metastatic

(M) lymph nodes, and for surgical approach.

• 1-6 are perigastric

• 7-18 are adjacent to major vessels, behind the

pancreas, and along the aorta

• 19-20 and 110-112 are around the diaphragm,

supradiaphragmatic, and paraesophageal

• CT characteristics of abnormal

lymph nodes:

• ≥ 8 mm in short axis

• round shape

• marked or heterogeneous

enhancement

• cluster of 3+ nodes in a

lymph node station

JGCA LYMPH NODE

STATIONS

Group LN station Location

1

Perigastric lymph nodes

1 Right paracardial

2 Left paracardial

3 Lesser curvature

4 Greater curvature

5 Suprapyloric

6 Infrapyloric

Group LN station Location

2

7 Left gastric artery trunk

8 Common hepatic artery

9 Celiac artery

10 Splenic hilar

11 Splenic artery

3

12* Hepatoduodenal ligament

13 Posterior surface of the pancreatic head

14v Superior mesenteric vein

415 Middle colic

16 Paraaortic

17 Anterior surface of the pancreatic head

beneath the pancreatic sheath

18 Inferior border of pancreatic body

19 Infradiaphragmatic LNs along

subphrenic artery

20 Paraesophageal LNs in diaphragmatic

hiatus

110 Paraesophageal LNs in lower thorax

111 Supradiaphragmatic

112 Posterior mediastinal

Regional lymph nodes (LNs) (in gray,

classified as N disease): 1-11, 14v

• Jejunal LNs adjacent to gastrojejunostomy

anastomosis in recurrent cancer after

partial gastrectomy

Distant LNs (in orange, classified as M

disease): 13, 15-20, 110-112

• 12*: Hepatoduodenal lymph nodes are

regional by JGCA, but distant by AJCC.

• Lymphatic involvement correlates with

the degree of gastric wall invasion.

• Lymphatic drainage of the stomach is

complex and multidirectional.

• The distribution of nodal metastasis is

variable.

• Depending on the location of the primary

tumor – upper, middle and lower third,

certain lymph node stations have a

higher frequency of involvement.

• Skip metastasis may occur, with

uninvolved perigastric lymph nodes and

involved metastatic distant lymph nodes.

• Upper and middle third tumors have a

higher incidence of skip metastasis.

Frequently involved lymph nodes by tumor location

Portion of

stomach

Perigastric lymph

nodes

Non-perigastric

lymph nodes

Upper third - lesser curvature

- paracardial

- celiac artery

- left gastric artery

- splenic hilum

- para-aortic

Middle third - lesser curvature

- greater curvature

- right paracardial

- splenic hilum

- para-aortic

Lower third - infrapyloric

- lesser curvature

- greater curvature

- common hepatic

artery

- celiac artery

NODAL STAGING

Station 4. Axial CECT demonstrates diffuse wall

thickening of the proximal two thirds of the

stomach, and enlarged greater curvature lymph

nodes (yellow arrow).

Station 3. Axial CECT demonstrates wall

thickening and enhancement of the proximal

lesser curvature, with enlarged lesser curvature

lymph nodes (blue arrow).

NODAL STAGING (N) – REGIONAL GROUP 1

Stations 5 and 6. Coronal CECT in a patient with

diffuse gastric wall thickening due to chronic

gastritis and a malignant ulcer along the lesser

curvature (green arrow). There is station 5

suprapyloric (pink arrow) and station 6

infrapyloric (orange arrow) adenopathy. An air

and fluid collection is seen subdiaphragmatically

due to perforation (red arrow).

NODAL STAGING (N) – REGIONAL GROUP 2

Station 7. Axial CECT in a patient with

adenocarcinoma of the gastric antrum (not

shown) demonstrates enlarged lymph nodes

along the left gastric artery (green arrow). A

gallbladder mass is present.

Stations 8, 10 and 11. Axial CECT

demonstrates irregular thickening and

enhancement of the lower third of the

stomach (white arrow). There is station 8

common hepatic artery (yellow arrow),

station 10 splenic hilum (green arrow) and

station 11 splenic artery (orange arrows)

adenopathy, as well as right portal vein

thrombosis (blue arrow), and liver metastasis

(red arrow).

Station 9. Axial CECT demonstrates

diffuse thickening of the middle third

of the stomach (white arrow) and

celiac axis adenopathy (peach arrow).

Station 12. Coronal CECT demonstrates diffuse wall

thickening and enhancement of the upper two thirds

of the stomach (white arrow), and hepatoduodenal

adenopathy (blue arrow). Regional (N) lymph nodes

are seen in the celiac axis (peach arrow) and

infrapyloric (orange arrow) stations.

NODAL STAGING (M) – DISTANT LYMPH NODES

Station 15. Axial CECT demonstrates focal

thickening of the distal third of the stomach

(white arrow) and middle colic adenopathy (red

arrows).

Station 16. Coronal CECT demonstrates

diffuse wall thickening of the gastric cardia and

proximal stomach (white arrows), and

extensive paraaortic adenopathy (green

arrows).

LYMPH NODE DISSECTION TYPES

• D0 dissection- fewer lymph nodes than D1

• D1 dissection- Group 1 nodes (gray nodes)

• D2 dissection- Group 1 and 2 nodes (orange nodes

part of D1+ dissection, red nodes included in D2)

• D3 dissection- Group 1, 2, and 3 nodes

• D4 dissection- Group 1, 2, 3, and 4 nodes

• Depending on the type of gastrectomy (distal vs

total), the lymph nodes removed may be modified.

• Typically the more extended dissections (D2 or D3

and beyond) are performed in Japan and may

account for better survival rates as compared to

Western countries, however, others argue that

extended lymph node dissection is associated with

higher post-operative morbidity and mortality.

4

6

4

4

2

5

3

71

12 11d11p8 9

Stomach

Pancreas

Duodenum

Spleen

M-staging of gastric cancer, American Joint

Committee on Cancer 7th manual

M0 No distant metastases

M1 Metastasis:

-Distant metastasis

-Involvement of hepatoduodenal, retropancreatic,

mesenteric, retroperitoneal, and para-aortic lymph

nodes are considered distant metastases

-Peritoneal carcinomatosis/ positive peritoneal

washing cytology New from prior system

• Peritoneal carcinomatosis/ + peritoneal washing cytology is now M1 disease.

• Only M1 patients may be classified as Stage IV.

• Rationale: patients with peritoneal disease and patients with M1 disease have

significantly worse survival.

Stage groupings

N0 N1 N2 N3

T1 IA IB IIA IIB

T2 IB IIA IIB IIIA

T3 IIA IIB IIIA IIIB

T4a IIB IIIA IIIB IIIC

T4b IIIB IIIB IIIC IIIC

M1 (any T or N) IV


UPDATES TO METASTASIS AND TNM STAGING

METASTASIS STAGING

• Distant metastases occur through multiple mechanisms:

• Hematogenous: liver is the most common site, other sites include lung, bones, and adrenal glands

• Lymphatic: distant nodal stations, lymphangitic spread of tumor

• Peritoneal: ascites, soft tissue plaques or nodules, peritoneal fat stranding, thickening or enhancement, Krukenberg tumor

Hematogenous metastases. Anterior and posterior

Tc99m MDP bone scan images demonstrate multiple

areas of increased radiotracer uptake consistent with

diffuse bone metastases.

METASTASIS STAGING

Lymphatic metastases. Coronal PET and

axial CECT images demonstrate FDG-

avid gastric mass (green arrow) and

enlarged Virchow nodes in the left axillary

and supraclavicular stations (orange

arrows), consistent with Stage IV disease.

Peritoneal carcinomatosis. Axial CECT

demonstrates omental plaques and

nodules (red arrows) in a patient with

gastric adenocarcinoma, consistent

with stage IV cancer.Peritoneal metastases. Coronal CECT

demonstrates a large pelvic mass (purple

arrow) from gastric adenocarcinoma

metastasis to the right ovary (Krukenberg

tumor), and ascites, consistent with Stage

IV disease.

Lymphangitic carcinomatosis. Axial

CECT demonstrates nodular septal

thickening in a patient with gastric

adenocarcinoma, consistent with

Stage IV disease.

5-year survival rate by stage

N0 N1 N2 N3

T1 71% 57% 46% 33%

T2 57% 46% 33% 20%

T3 46% 33% 20% 14%

T4a 33% 20% 14% 9%

T4b 14% 14% 9% 9%

M1 (any T or N) 4%

MANAGEMENT AND PROGNOSIS• Accurate staging influences management and is

an important prognostic indicator.

• Localized disease is treated with endoscopy,

surgery, and lymph node dissection.

• Locally advanced and systemic disease with

distant metastases is not curable and requires

a combination of surgery, chemotherapy, and

radiation.

Resection options: Indications:

Endoscopic mucosal resection or endoscopic submucosal

dissection

For early gastric cancer (EGC)- gastric cancer that invades no deeper

than the submucosa, regardless of lymph node metastasis (T1, any N).

Lymph node involvement affects decision for chemotherapy.

Surgical Total Gastrectomy

- Proximal or upper 1/3 tumors

- Large midgastric or infiltrative tumor (linitis plastica)

Partial/subtotal gastrectomy

- Lower two-third tumors

MANAGEMENT- UNRESECTABLE CANCER

• Unresectable cancers are not curable and typically undergo local or

systemic therapy, or a combination of both, for palliation.

• Features of unresectability:

• Distant metastases

• Invasion of a major vascular structure, such as the aorta

• Disease encasement or occlusion of the hepatic artery or

celiac axis/proximal splenic artery

• Lymph nodes in the aortocaval region, mediastinum, porta hepatis,

or behind or inferior to the pancreas are usually considered

outside of the surgical field

• Linitis plastica

• Imaging plays an essential role in the TNM staging of gastric

adenocarcinoma based on updated criteria of AJCC.

• Radiologist knowledge of common patterns of disease spread

based on locoregional pathways and metastatic spread is

essential for management and prognosis.

CONCLUSION

REFERENCES

1. De Sol, A. et al. Requirement for a standardised definition of advanced gastric cancer. Oncol Lett 7, 164–170 (2014).

2. De Manzoni, Giovanni, Franco Roviello, and Walter Siquini. "Lymphatic Spread, Lymph Node Stations, and Levels of Lymphatic Di ssection in Gastric

Cancer." In Surgery in the Multimodal Management of Gastric Cancer, 15-23. 2012.

3. Kadowaki, K. et al. Helical CT imaging of gastric cancer: normal wall appearance and the potential for staging. Radiat Med 18, 47–54 (2000).

4. Karpeh, M. S., Leon, L., Klimstra, D. & Brennan, M. F. Lymph Node Staging in Gastric Cancer: Is Location More Important Than Number? Ann Surg

232, 362–371 (2000).

5. Kwon, S. J. Evaluation of the 7th UICC TNM Staging System of Gastric Cancer. J Gastric Cancer 11, 78–85 (2011).

6. Le, O. Patterns of peritoneal spread of tumor in the abdomen and pelvis. World J Radiol 5, 106–112 (2013).

7. Lim, J. S. et al. CT and PET in stomach cancer: preoperative staging and monitoring of response to therapy. Radiographics 26, 143–156 (2006).

8. Lee, S. L. et al. Relevance of hepatoduodenal ligament lymph nodes in resectional surgery for gastric cancer. Br J Surg 101, 518–522 (2014).

9. Marrelli, D. et al. Prognostic value of the 7th AJCC/UICC TNM classification of noncardia gastric cancer: analysis of a large series from special ized

Western centers. Ann. Surg. 255, 486–491 (2012).

10. Schmidt, B. & Yoon, S. S. D1 Versus D2 Lymphadenectomy for Gastric Cancer. J Surg Oncol 107, 259–264 (2013).

11. Tamura, S. et al. Lymph Node Dissection in Curative Gastrectomy for Advanced Gastric Cancer, Lymph Node Dissection in Curative Gastrectomy for

Advanced Gastric Cancer. International Journal of Surgical Oncology, International Journal of Surgical Oncology 2011, 2011, e748745 (2011).

12. Tan, C. H., Peungjesada, S., Charnsangavej, C. & Bhosale, P. Gastric cancer: Patterns of disease spread via the perigastric liga ments shown by CT.

AJR Am J Roentgenol 195, 398–404 (2010).

13. Japanese Gastric Cancer Association. "Japanese Classification of Gastric Carcinoma: 3rd English Edition." Edited by Takeshi Sano and Y asuhiro

Kodera. Gastric Cancer, no. 14 (2011): 101-12. Accessed November 10, 2015. doi:10.1007/s10120-011-0041-5.

14. Japanese Gastric Cancer Association, Takeshi Sano, and Yasuhiro Kodera. "Japanese Gastric Cancer Treatment Guidelines 2010 (ver. 3)." Gastric

Cancer, no. 14 (2011): 113-23. Accessed November 10, 2015. doi:10.1007/s10120-011-0042-4.

15. "Survival Rates for Stomach Cancer, by Stage." American Cancer Society. March 16, 2015. Accessed December 13, 2015.

http://www.cancer.org/cancer/stomachcancer/detailedguide/stomach-cancer-survival-rates.

Contact information: [email protected]

location matters: ligaments and lymphatic … · location matters: ligaments and lymphatic pathways...

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