Japanese classification of gastric carcinoma: 3rd English edition
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- Japanese Gastric Cancer Association Gastric Cancer (2011) 14: 101. doi:10.1007/s10120-011-0041-5
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Clinical and pathological classification
Clinical classification (c)
Pathological classification (c)
Physical examination, imaging studies, endoscopic, laparoscopic and surgical findings, biopsy, cytology, biochemical and biological investigations.
Histological examination of surgically or endoscopically resected specimens; peritoneal lavage cytology.
Histological tumor findings are recorded in the following order: tumor location, macroscopic type, size, histological type, depth of invasion, cancer–stroma relationship, pattern of infiltration, lymphatic invasion, venous invasion, lymph node metastasis, and resection margins. For example: L, Less, Type 2, 50 × 20 mm, tub1 > tub2, pT2, int, INFb, ly1, v1, pN1 (2/13), pPM0, pDM0 (see subsequent text for an explanation of the abbreviations).
Anatomical extent and stage of gastric carcinoma
Description of the primary tumor
Size and number of lesions
The two greatest dimensions should be recorded for each lesion. Where there are multiple lesions, the tumor with the most advanced T category (or the largest lesion where the T stage is identical) is classified.
The three gastric regions and the esophagogastric junction
The area extending 2 cm above to 2 cm below the esophagogastric junction (EGJ) is designated the EGJ area. Tumors having their epicenter in this area are designated EGJ carcinomas irrespective of histological type. The location of an EGJ carcinoma is described using the symbols E (proximal 2 cm segment) and G (distal 2 cm segment), with the dominant area of invasion described first, i.e., E, EG, E=G (both areas equally involved), GE, or G. The distance between the tumor center and the EGJ is recorded.
The EGJ is defined as the border between the esophageal and gastric muscles. Clinically this is identified by one of the following: (a) the distal end of the longitudinal palisading small vessels in the lower esophagus at endoscopy; (b) the horizontal level of the angle of His shown by barium meal examination; (c) the proximal end of the longitudinal folds of the greater curve of the stomach shown at endoscopy or barium meal study; or (d) the level of the macroscopic caliber change of the resected esophagus and stomach. It is important to note that the squamocolumnar junction (SCJ) does not always coincide with the EGJ.
Clinically, the tumor location is often expressed as cardia, fundus, body, incisura, and antrum.
Cross-sectional parts of the stomach
Carcinoma in the remnant stomach
The primary lesion at the previous gastrectomy: benign (B), malignant (M), or unknown (X).
The time interval elapsed between the previous gastrectomy and the current diagnosis, in years (unknown: X).
Tumor location in the remnant stomach: anastomotic site (A), gastric suture line (S), other gastric site (O), or total remnant stomach (T). Extension into the esophagus (E), duodenum (D), or jejunum (J) is recorded.
Type 0 (superficial)
Typical of T1 tumors.
Type 1 (mass)
Polypoid tumors, sharply demarcated from the surrounding mucosa.
Type 2 (ulcerative)
Ulcerated tumors with raised margins surrounded by a thickened gastric wall with clear margins.
Type 3 (infiltrative ulcerative)
Ulcerated tumors with raised margins, surrounded by a thickened gastric wall without clear margins.
Type 4 (diffuse infiltrative)
Tumors without marked ulceration or raised margins, the gastric wall is thickened and indurated and the margin is unclear.
Type 5 (unclassifiable)
Tumors that cannot be classified into any of the above types.
Subclassification of Type 0 (Fig. 4, modified from the Japanese Endoscopy Society Classification of 1962)
Subclassification of Type 0
Type 0-I (protruding)a
Type 0-II (superficial)
Tumors with or without minimal elevation or depression relative to the surrounding mucosa.
Type 0-IIa (superficial elevated)a
Slightly elevated tumors.
Type 0-IIb (superficial flat)
Tumors without elevation or depression.
Type 0-IIc (superficial depressed)
Slightly depressed tumors.
Type 0-III (excavated)
Tumors with deep depression.
Description of macroscopic type
The macroscopic tumor type should be recorded in both the clinical and pathological classifications.
Histological classification (Table 4)
Histological classification of gastric tumors
Benign epithelial tumor
Malignant epithelial tumor
Papillary adenocarcinoma (pap)
Tubular adenocarcinoma (tub)
Moderately differentiated (tub2)
Poorly differentiated adenocarcinoma (por)
Solid type (por1)
Non-solid type (por2)
Signet-ring cell carcinoma (sig)
Mucinous adenocarcinoma (muc)
Carcinoma with lymphoid stroma
Squamous cell carcinoma
Gastrointestinal stromal tumor (GIST)
Smooth muscle tumor
Miscellaneous non-epithelial tumors
MALT (mucosa-associated lymphoid tissue) lymphoma
Mantle cell lymphoma
Diffuse large B-cell lymphoma
Other B-cell lymphomas
Fundic gland polyp
Heterotopic submucosal gland
Inflammatory fibroid polyp (IFP)
Familial polyposis coli, Peutz–Jeghers syndrome, juvenile polyposis, Cowden’s disease
Depth of tumor invasion (T)
Depth of tumor unknown
No evidence of primary tumor
- Tumor confined to the mucosa (M) or submucosa (SM)
Tumor confined to the mucosa (M)
Tumor confined to the submucosa (SM)1
Tumor invades the muscularis propria (MP)
Tumor invades the subserosa (SS)
Cancer stromal volume, infiltrative pattern, and capillary invasion
Cancer stromal volume (to be recorded for T1b or deeper tumors)
Medullary type (med): Scanty stroma
Scirrhous type (sci): Abundant stroma
Intermediate type (int): The quantity of stroma is intermediate between the two above types.
Tumor infiltrative (INF) pattern into the surrounding tissues (to be recorded in T1b or deeper tumors; Fig. 5)
Tumor displays expanding growth with a distinct border from the surrounding tissue
Tumor shows an intermediate pattern between INFa and INFc
Tumor displays infiltrative growth with no distinct border with the surrounding tissue.
- 220.127.116.11.1Lymphatic invasion (ly)
ly0: No lymphatic invasion
ly1: Minimal lymphatic invasion
ly2: Moderate lymphatic invasion
ly3: Marked lymphatic invasion
- 18.104.22.168.2Venous invasion (v)
v0: No venous invasion
v1: Minimal venous invasion
v2: Moderate venous invasion
v3: Marked venous invasion
Lymph node metastasis
Anatomical definitions of lymph node stations
Right paracardial LNs, including those along the first branch of the ascending limb of the left gastric artery.
Left paracardial LNs including those along the esophagocardiac branch of the left subphrenic artery
Lesser curvature LNs along the branches of the left gastric artery
Lesser curvature LNs along the 2nd branch and distal part of the right gastric artery
Left greater curvature LNs along the short gastric arteries (perigastric area)
Left greater curvature LNs along the left gastroepiploic artery (perigastric area)
Rt. greater curvature LNs along the 2nd branch and distal part of the right gastroepiploic artery
Suprapyloric LNs along the 1st branch and proximal part of the right gastric artery
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
LNs along the trunk of left gastric artery between its root and the origin of its ascending branch
Anterosuperior LNs along the common hepatic artery
Posterior LNs along the common hepatic artery
Celiac artery LNs
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
Proximal splenic artery LNs from its origin to halfway between its origin and the pancreatic tail end
Distal splenic artery LNs from halfway between its origin and the pancreatic tail end to the end of the pancreatic tail
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
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
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
LNs on the posterior surface of the pancreatic head cranial to the duodenal papilla
LNs along the superior mesenteric vein
LNs along the middle colic vessels
Paraaortic LNs in the diaphragmatic aortic hiatus
Paraaortic LNs between the upper margin of the origin of the celiac artery and the lower border of the left renal vein
Paraaortic LNs between the lower border of the left renal vein and the upper border of the origin of the inferior mesenteric artery
Paraaortic LNs between the upper border of the origin of the inferior mesenteric artery and the aortic bifurcation
LNs on the anterior surface of the pancreatic head beneath the pancreatic sheath
LNs along the inferior border of the pancreatic body
Infradiaphragmatic LNs predominantly along the subphrenic artery
Paraesophageal LNs in the diaphragmatic esophageal hiatus
Paraesophageal LNs in the lower thorax
Supradiaphragmatic LNs separate from the esophagus
Posterior mediastinal LNs separate from the esophagus and the esophageal hiatus
Recording of lymph node metastasis
For surgical resection specimens, the total number of lymph nodes and the number of involved lymph nodes at each nodal station are recorded. When a tumor nodule without histological evidence of lymph node structure is found in the lymphatic drainage area of the primary tumor, it is recorded as extranodal metastasis and counted as a metastatic lymph node in the pN determination.
Lymph node metastasis (N)
NX: Regional lymph nodes cannot be assessed
N0: No regional lymph node metastasis
N1: Metastasis in 1–2 regional lymph nodes
N2: Metastasis in 3–6 regional lymph nodes
N3: Metastasis in 7 or more regional lymph nodes
N3a: Metastasis in 7–15 regional lymph nodes
N3b: Metastasis in 16 or more regional lymph nodes
Although it is not a prerequisite, the examination of 16 or more regional lymph nodes is recommended for N status determination.
Metastatic ratio of lymph nodes
The metastatic ratio is the ratio of metastatic nodes to the total number of dissected nodes and is recorded for each nodal station for all regional lymph nodes.
Metastasis to sites other than regional lymph nodes (distant metastasis) is M1 disease. In addition, peritoneal metastasis, peritoneal lavage cytology, and hepatic metastasis may be described by the conventional symbols P, CY, and H, respectively (see below). Positive peritoneal lavage cytology is recorded as cy+ by the International Union Against Cancer (UICC)/TNM system.
Presence or absence and sites of distant metastasis (M)
MX: Distant metastasis status unknown
M0: No distant metastasis
M1: Distant metastasis
Sites of metastasis are recorded using the following notation: LYM (lymph nodes), SKI (skin), PUL (lung), MAR (bone marrow), OSS (bone), PLE (pleura), BRA (brain), MEN (meninx), ADR (adrenal), OTH (others)5
Peritoneal metastasis (P)
PX: Peritoneal metastasis is unknown
P0: No peritoneal metastasis
P1: Peritoneal metastasis.
Peritoneal lavage cytology (CY)
CYX: Peritoneal cytology not performed
CY0: Peritoneal cytology negative for carcinoma cells
CY1: Peritoneal cytology positive for carcinoma cells
A macroscopically curative resection with CY1 is R1.
Hepatic metastasis (H)
HX: Hepatic metastasis is unknown
H0: No hepatic metastasis
H1: Hepatic metastasis.
Evaluation after surgical or endoscopic resection
Surgical specimen resection margin
Proximal margin (PM)
Involvement of the proximal margin cannot be assessed
No involvement of the proximal margin
Involvement of the proximal margin.
Distal margin (DM)
Involvement of the distal margin cannot be assessed
No involvement of the distal margin
Involvement of the distal margin.
Resection margin of the endoscopic resection specimen
Horizontal margin (HM)
Involvement of the horizontal margin cannot be assessed
No involvement of the horizontal margin
Involvement of the horizontal margin.
Vertical margin (VM)
Involvement of the vertical margin cannot be assessed
No involvement of the vertical margin
Involvement of the vertical margin.
Residual tumor (R)
Presence of residual tumor cannot be assessed
No residual tumor
Microscopic residual tumor (positive resection margin or CY1)
Macroscopic residual tumor.
Tumor evaluation after preoperative treatment
Description of tumor classification after preoperative treatment
Tumor classification after preoperative chemotherapy or chemoradiotherapy is designated by the prefix ‘y’. The clinical classification following preoperative treatment is designated ycTNM and the pathological classification ypTNM. The ycTNM and ypTNM classification describes the extent of tumor actually present at the time of that examination; it is not an estimate of the extent of tumor prior to preoperative therapy. Only viable tumor cells are taken into account when calculating ypTNM. Signs of tumor regression, including scars, areas of fibrosis, granulation tissue, or mucin lakes are not taken into consideration.
For example: A large adenocarcinoma with computed tomography (CT) evidence of serosal irregularity and lymph node metastasis was classified as cT4aN1M0. Preoperative chemotherapy achieved significant tumor regression, with the tumor being undetectable by endoscopy and CT (ycT0N0M0). Gastrectomy was performed and histological examination revealed viable carcinoma cells in the muscularis propria and in two regional lymph nodes; granulation tissue with mucin lakes was present in five other lymph nodes (ypT2N1M0).
Histological evaluation criteria of tumor response after preoperative therapy (Fig. 8)
- Grade 0 (no effect)
No evidence of effect
- Grade 1 (slight effect)
- Grade 1a (very slight effect)
Viable tumor cells occupy more than 2/3 of the tumorous area
- Grade 1b (slight effect)
Viable tumor cells remain in more than 1/3 but less than 2/3 of the tumorous area
- Grade 2 (considerable effect)
Viable tumor cells remain in less than 1/3 of the tumorous area
- Grade 3 (complete response)
No viable tumor cells remain. It is recommended that the finding is confirmed on additional sectioning.
Response evaluation of chemotherapy and radiotherapy
Tumor response to chemotherapy and/or radiotherapy is assessed using the Response Evaluation Criteria in Solid Tumors (RECIST) version 1.1 .
The Japanese Gastric Cancer Association (JGCA) developed an original method to evaluate the response of the primary gastric lesion to chemotherapy or radiotherapy , but it was not widely used, mainly because of technical difficulties. In the RECIST, primary gastric tumors are regarded as non-target lesions and endoscopic diagnosis is not recommended as an objective evaluation. However, the response of the primary tumor is clinically important and the JGCA methods may provide useful information in future neoadjuvant trials. The results of response evaluation of the primary tumor made by the following methods can be recorded and used as information that is additional to the RECIST results in some trial settings.
JGCA response evaluation of primary tumor
Tumor response, morphological changes, and efficacy are evaluated by double-contrast barium meal study and/or endoscopic examination of the following three types of primary lesions.
Measurable lesions (a-lesions)
Reduction rate = (longest diameter before therapy − longest diameter after therapy)/longest diameter before therapy.
Evaluable but not measurable lesions (b-lesions)
Describe changes in protruded lesions as follows:
Progression, no change, regression, flattening, or disappearance
- (ii)Describe changes in excavated lesions as follows:
Raised margin: progression, no change, regression, flattening, or disappearance
Crater: progression, no change, regression, flattening, or disappearance.
Diffusely infiltrating lesions (c-lesions) 
In diffusely infiltrating tumors (type 4), treatment response may be evaluated by expansion of the gastric lumen. In principle, the squares of the lesion shown with standing barium X-ray examination are compared before and after therapy, at the same position with the same volume of barium, and the enlargement rate is calculated.
Enlargement rate = (product calculated before therapy) − (product calculated after therapy)/(product calculated before therapy) × 100%
Definition of response in primary lesion
Complete response (CR)
Disappearance of all tumor lesions and no diagnosis of carcinoma. Biopsy specimens are negative for carcinoma.
- Partial response (PR)
a-lesions: At least a 30% decrease in total size
b-lesions: Remarkable regression and flattening of a tumor on X-ray/endoscopic examinations, which roughly corresponds to at least a 50% decrease in tumor size.
c-lesions: At least 50% enlargement of the gastric lumen in the area of the lesions by X-ray examination.
Stable disease (SD)
Changes in tumor size or shape are less than PR, but are not progressive disease (PD).
Progressive disease (PD)
Increase in tumor size and/or worsening of the shape (20% or more increase in a-lesions), or new intragastric lesions.
Handling of the resected specimen
Description of findings
The whole resected stomach is macroscopically observed.
The representative sections of the whole resected stomach including the carcinoma are microscopically examined.
Preparation of the resected stomach
Fixation of the resected stomach
After dissection of the lymph nodes from the specimen, the stomach is placed on a flat board with the mucosal side up, pinned at the edges with stainless steel pins, and fixed in a 10% buffered formalin solution. A relatively short fixation time (48 h) is recommended for additional immunohistochemical or genetic examinations in the future.
Sectioning of the stomach
Sectioning of lymph nodes
Each dissected lymph node should be studied individually. The plane of largest dimension of the node including the hilus should be sectioned.
Handling of endoscopically resected specimens
A single resection procedure performed for a single lesion is defined as “en-bloc resection”, and multiple resection procedures for a single lesion are defined as “piecemeal resection”.
Fixation, inspection, and sectioning
The size and number of specimens
Macroscopic type of the tumor
The size of the tumor (longest and shortest diameters)
- Histological type of the tumor
Different histological types seen in a tumor are recorded according to their quantitative predominance
- Depth of tumor invasion (pT1a, pT1b1, pT1b2 or M, SM1, SM2)
Depth is determined and recorded only when the vertical margin is negative for cancer invasion.
When submucosal invasion is present, the actual measured length (in microns) from the lower border of the muscularis mucosae should also be recorded. If the muscularis mucosae is obscure due to ulcerative changes, the length should be measured on the virtual line based on the adjacent normal layer.
When the vertical margin is involved, the possibility of deeper invasion should be described.
- Intratumoral ulcerative findings
UL(−): Ulcer or ulcer scar is absent
UL(+): Ulcer or ulcer scar is present.
- Capillary invasion
ly(−): Lymphatic invasion is absent
ly(+): Lymphatic invasion is present
v(−): Venous invasion is absent
v(+): Venous invasion is present.
- Horizontal margin involvement
HMX: Horizontal margin involvement is unknown
HM0: Horizontal margin is not involved (The length of the margin should be recorded)
HM1: Horizontal margin is involved (The number of positive sections should be recorded).
- Vertical margin involvement
VMX: Vertical margin involvement is unknown
VM0: Vertical margin is not involved
VM1: Vertical margin is involved.
Histological diagnosis of gastric biopsy (“Group Classification”)
This classification is applied only to endoscopic biopsy materials. Materials obtained by polypectomy, endoscopic resection, or surgery are not included. The “Group Classification” is applied only to epithelial tissue. In principle, the diagnosis is written first, followed by the Group Classification.
- Group X
Inappropriate material for which histological diagnosis cannot be made
- Group 1
Normal tissue or non-neoplastic lesion
- Group 2
Material for which diagnosis of neoplastic or non-neoplastic lesion is difficultIn such a case, the pathologist should describe the lesion as “indefinite for neoplasia” and add the following reasons for clinicians:
Atypical cells exist, but diagnosis of neoplasia based on cellular atypia is difficult because of the small volume.
Atypical cells exist, but diagnosis of neoplastic or non-neoplastic lesion is difficult due to remarkable erosion and/or inflammation.
Atypical cells exist, but diagnosis of neoplastic or non-neoplastic lesion is difficult due to tissue damage.
- Group 3
- Group 4
Neoplastic lesion that is suspected to be carcinoma
- Group 5
The histological subtype of carcinoma should be recorded.
SM may be subclassified as SM1 or T1b1 (tumor invasion is within 0.5 mm of the muscularis mucosae) or SM2 or T1b2 (tumor invasion is 0.5 mm or more deep into the muscularis mucosae).
Tumor extending into the greater or lesser omentum without visceral peritoneal perforation is classified as T3.
Invaded adjacent structures should be recorded. The adjacent structures of the stomach are the liver, pancreas, transverse colon, spleen, diaphragm, abdominal wall, adrenal gland, kidney, small intestine, and retroperitoneum. Serosal invasion with involvement of the greater and lesser omentum is classified as T4a, not T4b. Invasion of the transverse mesocolon is not T4b unless it extends to the colic vessels or penetrates the posterior surface of the mesocolon.
In endoscopically resected specimens, capillary invasion is recorded as ly (−) or ly (+), and v (−) or v (+).
Other sites include retroperitoneal carcinomatosis and the ovaries (Krukenberg).