Differences cancer histological type: of carcinoma · lymph node metastasis, direct invasion into surrounding organ, andperitoneal dissemina-tion werehigher. In groupIII, whichshowed

Gut, 1992,33,606-612

Differences in the mode of the extension of gastriccancer classified by histological type: newhistological classification of gastric carcinoma

N Goseki, T Takizawa, M Koike

AbstractBy combining two of the morphologicalcharacteristics of gastric cancer, the degree ofdifferentiation of the glandular tubules and theamount of mucus in the cytoplasm, the histo-logical type of the gastric carcinoma wascategorised into four groups. Group I: tubulardifferentiation - well; mucus in cytoplasm -poor; group II: tubular differentiation - well;mucus in cytoplasm - rich; group III: tubulardifferentiation - poor; mucus in cytoplasm -poor; group IV: tubular differentiation - poor;mucus in cytoplasm - rich. A study of therelation between the types of primary lesionand the mode of extension and recurrence ofgastric carcinoma in 200 autopsy cases wasthen undertaken. In group I, the frequency andextent of haematogenous metastasis such asin the liver was high, while in group IV, that oflymph node metastasis, direct invasion intosurrounding organ, and peritoneal dissemina-tion were higher. In group III, which showedthe intermediate mode of extension in natureto those of group I and IV, although thefrequency and severity of the bone marrowmetastasis was the highest. There weresignificant differences in the modes ofdevelopment and the extent of infiltration in allgroups.

The First Department ofSurgery, School ofMedicine, TokyoMedical and DentalUniversity, JapanN Goseki

The Department ofPathology, TokyoMetropolitan KomagomeHospital, JapanT TakizawaM KoikeCorrespondence to:Dr N Goseki, FirstDepartment of Surgery,School of Medicine, TokyoMedical and DentalUniversity, 1-5-45 Yushima,Bunkyo-ku, Tokyo 113,Japan.Accepted for publication9 September 1991

Although gastric carcinoma is a malignanttumour originating from the same gastricglandular epithelium, its tissue morphologyvaries substantially with the individual patientand the location of the tumour in the area of thestomach - that is, whether in the pyloric, fundic,or cardiac glands. It also varies with the tissueenvironment of the primary and metastasisedlesions in which the tumours grow and develop.As a result, there is a wide variation in themorphological future of gastric carcinoma, andthere are many histological classifications ofgastric carcinoma according to the criteria used.The currently used histological classification ofgastric carcinoma is largely divided into twoforms - that is, classification either by twohistological types or by three histological types.The former classification was first introduced byJarvi et al, who proposed the metaplasticintestinal epithelial origin of gastric carcinoma'(the socalled Lauren's classification).' This led tothe theory of the two histological types, gastricand intestinal type carcinoma (differentiated andundifferentiated types), advocated by Mulligan,3Morson,4 and more recently by Nakamura et al.The latter classification was used in The generalrules for the study of gastric cancer in surgery and

pathology, edited by the Japanese ResearchSociety for Gastric Cancer (Jpn RSGC),6 and it isconsistent with Nagayo's classification by threehistological types.7 The Japanese ResearchSociety for Gastric Cancer divided the socalledcommon type into well differentiated tubularadenocarcinoma (tub,), moderately differenti-ated tubular adenocarcinoma (tub2) and poorlydifferentiated adenocarcinoma (por). Thesewere classified further into papillary adenocar-cinoma (pap), mucinous adenocarcinoma (muc),and signet ring cell carcinoma (sig). In the finalanalysis, it appears that the difficulty of classify-ing tub2 in the three histological type classifica-tion by the two histological types led to thedevelopment of this complex classification by theJpn RSGC.When surgeons treat patients with gastric

cancer, if the former classifications are used, themode of extension after the operation, it is toodifficult to select the suitable form of treatmentbecause the modes of recurrence cannot be reallyidentified before the actual recurrence, thoughthese classifications are simple and useful toevaluate the preoperative extension of cancer,and to select a suitable operation procedure. Onthe other hand, if the latter classifications areused, it is too complicated to understand theextension of the cancer preoperatively.The authors therefore carried out investiga-

tions in order to make a new histologicalclassification to satisfy, even surgeons, for therequirements necessary in the treatment ofpatients with gastric cancer.By using such a combination of the two

histological features of gastric carcinoma, theauthors attempted to classify gastric carcinomainto four groups that include undifferentiatedcarcinoma (ud) as well as the common typeclassified by the Jpn R S G C. If a discussion onthe tissue origin of gastric carcinoma is set aside,this classification is basically a subtype of the twohistological type classification.

NEW HISTOLOGICAL CLASSIFICATION OF GASTRICCARCINOMAA combination of the two histological features ofgastric carcinoma - namely, (1) tubular differen-tiation (good or poor), and (2) mucus in thecytoplasm (rich or poor), was used as the indexfor the histological classification of gastriccarcinoma. In other words, on the basis of(1) whether or not the differentiation of themalignant cells leads to a tubular formation, and(2) the functional status of cellular mucus pro-ductivity, gastric carcinoma was classified intothe following four groups:

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Differences in the mode ofthe extension ofgastric cancer classified by histological type: new histological classification ofgastric carcinoma

Tubulardifferentiation

Well

Poor

Mucus in

Poor Rich cytoplasm

(El: Mucus)

Group I: Tubular differentiation: wellMucus in the cytoplasm: poor

Group II: Tubular differentiation: wellMucus in the cytoplasm: rich

Group III: Tubular differentiation: poor

Mucus in the cytoplasm: poor

Group IV: Tubular differentiation: poor

Mucus in the cytoplasm: richFigure 1 is a schematic illustration of the above

histological classification. The degree of tubulardifferentiation is shown on the ordinate and theamount of mucus in the cytoplasm on theabscissa. The amount of mucus in the cytoplasmwas determined by the intensity of staining and

the localisation of mucus in the cytoplasm, aswell as by microscopically observing the histo-logical materials prepared by alcian blue PASdouble staining. As a result, tub2 in the histo-logical classification by the Jpn RSGC was

mostly classified as group I, provided that mucusvacuoles were not present in the cytoplasm, andas group IV, provided that mucus vacuoles were

present in the cytoplasm (Fig 2a, b, c, d).The relationship between the new histological

classification of gastric carcinoma and that of theJpn RSGC is illustrated in Figure 3. Most of papand part of tub, and tub2 were classified as groupI, while most of muc was classified as group II.

Both por and ud were classified as group III,while part of sign, muc and tub2 was classified as

group IV.Using this method, the author assessed the

characteristics of the mode of development ofgastric carcinoma in various histological typesand the results are reported in this paper.

Methods

MATERIALSThe new histological classification of gastriccarcinoma described above was applied to theprimary and metastasised lesions of 200 patientswith gastric carcinoma (144 after gastrectomy

Figure 2: (a) According to the histological classification ofgastric carcinoma by the Japanese Research Societyfor Gastric Cancer of the carcinomatous lesion

(arrow) is classified as moderately differentiated tubular adenocarcinoma (tub,) (alcian blue-PAS double staining). (b) In high magnification, the carcinomatous

lesion showed with arrow in Figure (a) the PAS and/or alcian blue positive deposit cannot be defined in the cytoplasm, so the authors classified this fiture as groupI: The tubular differentiation is well and the mucus in the cytoplasm is poor (alcian blue-P'AS staining). (c) According to the histological classification of gastriccarclnoma by the3Japanese Research Society for Gastric Carcinoma, this histologicalfeature ofcarcinomatous lesion (arrow) is also classified as moderatelvdifferentiated tubular adenocarcinoma (tub,) (alcian-blue double staining). (d) In high magnification of the carcinomatous lesion shozwed zwith arrozw in (c) thePAS and/or alcian blue positive mucus is apparentlv visible in the cytoplasm, so the authors classified this feature as group IV: the tubular differentiation is poorand the mucus in the cvtoplasm is rich (alcian blue-PAS double staining).

Figure 1: Schematicillustration of the fourhistological types ofgastniccarcinoma classified by thetwo morphologicalcharacteristics of thecarcinomatous tissue, lhedegree ofdifferentiation ofthe glandular tubules and theamount of intracellularmucus.

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Goseki, Takizawa, Koike

Figure 3: Relationship ofthenew histologicalclassification ofgastnrccarcinoma with that oftheJ7apanese Research Societyfor Gastric Cancer.

and 56 without gastrectomy) autopsied withinsix hours after death at the Department ofPathology, Tokyo Metropolitan KomagomeHospital over the 15 year period from 1975 to1989. Both the primary and metastatic lesionswere observed grossly in detail for the purpose ofassessing the metastasis and the extent of thecancer. Specimens of the primary and metastaticlesions were prepared for histological analysis bymeans of haematoxylin and eosin staining andalcian blue PAS double staining, followed by amicroscopic examination. The histological typeswere determined based on the predominantmorphological findings of a primary lesion. Thiswas done semiquantitatively, using sectionsin which the tumour was well represented andin which there was agreement between theobservers.

In the analysis of 56 cases without gastrec-tomy, the predominant histological type wasassessed as above for primaly gastric cancer butusing those areas showing no autolytic changes.Of the various organs to which gastric cancer

metastasised, the following five areas of meta-stasis were mainly analysed to find the incidenceand severity of metastasis according to the histo-logical type: (1) haematogenous liver metastasis,(2) lymph node metastasis, (3) direct invasion,(4) peritoneal dissemination, and (5) metastasisto the bone marrow. The severity of metastasiswas evaluated according to the following threegrades:

LYMPH NODE METASTASIS

SevereMetastases have spread to the distant lymphnodes such as the Virchow, auxiliary and/oringuinal lymph nodes, including other super-ficial lymph nodes outside the abdominal andthoracic cavities.

ModerateMetastases have spread to the regional lymphnodes in the abdominal cavity, lymph nodessurrounding the aorta, and those in the thoraciccavity.

Slight to noneMetastases are confined to the regional lymphnodes in the abdominal cavity and have notextended to the lymph nodes surrounding theaorta. (Clinically, lymph node metastases aresurgically resectable.)

DIRECT INVASIONStrictly speaking, to differentiate between directinvasion and peritoneal dissemination is imposs-ible in many cases (particularly those in groupIV). This section deals with the cases where thedirect and continuous invasion of the primarylesion was obvious.

SevereThe intestinal and/or biliary tracts are totallyobstructed by a direct tumour invasion (all of thepatients are considered to have developedclinical symptoms of intestinal obstruction and/or obstructive jaundice).

ModerateA direct invasion to other organs is evident, butmarked clinical symptoms of intestinal andbiliary obstruction are unlikely to have beenmanifested.

HAEMATOGENOUS LIVER METASTASIS

SevereThe metastases have grown practically all overthe lobes and seem to have been followed byhepatic insufficiency (H3 according to the classi-fication by the Jpn RSGC. Nearly all the hepatictissues have been replaced by cancerous tissue.)

Slight to noneThere is almost notumour invasion.

gross evidence of a direct

Tubulardifferentiation

ModerateGross metastatic lesions are visible, but areunlikely to have caused an impairment of thehepatic function (HI2 according to the classifica-tion by the Jpn RSGC).

Well

Poor

Slight to noneThere is no gross evidence of metastasis. Ifpresent, it is detected by a histological examina-tion (Ho or ho and h, according to the classifica-tion by the Jpn RSGC).

80 cases(40-0%)

40 cases(20.0%)

Poor

7 cases(3.5%)

73 cases(36-5%)

&.I Mucus in|Rich ' cytoplasm

Figure 4: Patient numbers in each ofthe histological types ofprimary lesion in 200 autopsy cases classified by the newhistological classification.

A

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PERITONEAL DISSEMINATION

SevereAs a result of severe dissemination, the visceraland parietal peritoneum form a mass coveredwith a thick plaster like fibrous cancer tissue.

ModerateGross peritoneal dissemination is visible, but ithas not diffused all over the intestinal wall andthe peritoneum. Although disseminated meta-static nodes are present, no clinical symptoms ofintestinal and biliary stenosis are unlikely to havebeen manifested.

Slight to noneThere is no gross evidence of peritoneal dissemi-nation. If present, it is detected by a histologicalexamination.

I Tubular 1differentiation

8801Well cases

Poor 1i

Rich

METASTASIS TO THE BONE MARROW

SevereNumerous gross metastatic lesions are seen,replacing nearly all of the bone marrow.

ModerateGross metastatic lesions are limited to severalareas of the bone marrow.

Slight to noneThere is no gross evidence of metastatic lesions.If present, they are detected by a histologicalexamination.

OTHER METASTASISAlthough metastatic lesions in other organs,including the lung, ovary, etc, were alsoexamined histologically, the results are omittedfrom this paper.

Results

00

Severe

: Moderate

Slight none I

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* * ** ** ** *

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invasion * OOe O@ O@O@O Oh OOOQO O OOOOOO

ooooooOooooooooooooo

.....oOOoOoooooooooPeritoneal * *9 *0 *B * * * * * * * * * * *dissemination oooooooooooooooooooo

OOOOOOOOOOOOOOOOOOOO

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(* = Post gastrectomy case)Figure 5: Mode ofdevelopment and recurrence in 80 autopsy cases, histologically classified in

group I: the tubular differentiation is well and the mucus in the cytoplasm is poor.

DIFFERENCES OF THE MODE OF SPREADING OFGASTRIC CARCINOMA CONCERNED WITH THEHISTOLOGICAL TYPESAccording to the new histological classificationof gastric carcinoma, of the 200 autopsy cases, 80(40.0%) were classified as group I, seven (3.5%)as group II, 40 (20.0%) as group III, and 73(36.5%) as group IV (Fig 4). The mode ofdevelopment of gastric carcinoma in the histo-logical groups is analysed below.

GROUP I (Fig 5)Of the 80 cases in group I, 42 (52.5%) hadundergone a gastrectomy (indicated by anasterisk (*) in the Figure), while the remaining38 (47.5) had not undergone a gastrectomy.

Liver metastasisModerate to severe haematogenous liver meta-stases were observed in 56 cases (70.0%), ofwhich 30 (37.5%) had severe metastases.

Lymph node metastasisBecause the subjects were all autopsy cases, theincidence of severe lymph node metastases wasnaturally high. Moderate to severe metastaseswere observed in 52 cases (65.0%), of which 28(35.0%) had severe metastases. In 28 (35.0%),lymph node metastasis was found to some extentor not detected. Upon a gross examination, it wasfound that the metastatic nodes in this groupwere larger and more configurated than thoseobserved in the other groups.

Direct invasionModerate to severe direct invasion was observedin 50 cases (62.5%), of which 22 (27 5%) had asevere invasion. Direct invasion was found tosome extent or not detected in remaining 30(37.5%).

Livermetastasis

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Goseki, Takizawa, Koike

Peritoneal disseminationIn 54 (67 5%), dissemination was found to someextent or not detected. Moderate to severeperitoneal dissemination was observed in only 26cases (32.5%), of which 10 (12-5%) had severedissemination.

Metastasis to the bone marrowModerate to severe bone marrow metastaseswere observed in six cases (7.5%), of which four(5.0%) had severe metastases. In remaining 74(92.5%) bone marrow metastasis was found tosome extent or not detected.

GROUP IIAs only seven cases (3.5%) were classified asgroup II, these were not analysed in the presentstudy. As soon as enough cases are found,however, the findings will be analysed.

GROUP III (Fig 6)Forty cases (20 0%) were classified as group III,of which 20 (50%) had undergone a gastrectomyand remaining 20 (50%) had not.

F :Severe

* Moderate

O Slight- none

* * *

00 000 0*00

I000000000000000

Lymph node WWWWWW0WW W W * * * *metastasis *-

***** *********Direct

invasion * * * * * *Oh 0 0 0 0 -4 0 0 0 0 -000 00 00 0

-~~~~~~~~~~*Peritoneal Q 0

dissemination * * * * * *00 0O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0O

Metastasis ID g -g g Oto

bone marrow 0 0 0 0 0 00 O O O O O O O O 0

(* = Post gastrectomy case)Figure 6: Mode ofdevelopment and recurrence in 14 autopsy cases, histologically classified ingroup III: the tubular differentiation is poor and the mucus in the cytoplasm is also poor.

Liver metastasisModerate to severe haematogenous liver meta-stases were observed in 20 cases (50.0%), ofwhich four (10-0%) had severe metastases. Livermetastasis was found to some extent or notdetected in the remaining 20 (50.0%).

Lymph node metastasisModerate to severe metastases were observed in32 cases (80.0%), ofwhich 14 (35.0%) had severemetastases. In the remaining eight (20.0%)lymph node metastasis was found to some extentor not detected.

Direct invasionModerate to severe direct invasion was observedin 32 cases (80.0%), of which 20 (50.0%) had asevere invasion. A direct invasion was found tosome extent or not detected in eight (20.0%).

Peritoneal disseminationModerate to severe peritoneal dissemination wasobserved in 20 cases (50.0%), of which 18(38.9%) had severe dissemination. Peritonealdissemination was found to some extent or notdetected at all in the remaining 20 (50.0%).

Metastasis to the bone marrowModerate to severe bone marrow metastaseswere observed in 19 cases (47 5%), of which 12(30.0%) had severe metastases. In the remaining21 (52.5%) bone marrow metastasis was found tosome extent or not detected.

GROUP iv (Fig 7)Seventy three cases (36.5%) were classified asgroup IV, of which 53 (72 6%) had undergone agastrectomy and 20 (27.4%) had not.

Liver metastasisModerate haematogenous liver metastases wereobserved in 10 cases (13-7%), but no cases ofsevere metastases were observed. In the remain-ing 63 (86 3%) liver metastasis was found tosome extent or not detected.

Lymph node metastasisModerate to severe metastases were observed in64 cases (87 7%), ofwhich 50 (68 5%) had severemetastases. Only in the remaining nine (12.3%)lymph node metastasis was found to some extentor not detected.As compared with group I, the metastatic

nodes in this group were small and confluent,accompanied by peritoneal dissemination.

Direct invasionModerate to severe direct invasion was observedin 70 cases (90 3%), of which 58 (79 4%) had a

severe invasion. In the remaining three (4. 1%), a

direct invasion was found to some extent or notdetected.

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Peritoneal disseminationModerate to severe peritoneal dissemination wasobserved in 68 cases (93 1%), of which 63(86.3%) had severe dissemination. In theremaining five (6.9%), peritoneal disseminationwas found to some extent or not detected.

Metastasis to the bone marrowBone marrow metastasis was found to someextent or not detected in 55 (75 3%). Moderate tosevere bone marrow metastases were observed in18 cases (24 7%), ofwhich 14 (19-2%) had severemetastases.

[ : Severe

*: Moderate

O Slight- none

Tubulardifferentataion

Well -K-__,- 73 cases

Poor _ L [Poor Mucus in

Poor Rich cytoplasm

I**************ooooo..........O 0000400000000000* * ** ** *** * * * * * * * ** * *00000000000000000000

00000000000000000000

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Lymph nodemetastasis *eee--**O ooo-

** ******CO 00 0 4 o o o o o 0.0 0 0

********* **** *** **

Direct **inason********************invasion *******------- o

**********ooo****. * * * ** * * * * * * * * *

Peritoneal *----@@@@@@@@@@dissemination

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*w OR OR *0 *0 OR Oh *0 Oh00* *0*0 *0******************

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(* = Post gastrectomy case)Figure 7: Mode ofdevelopment and recurrence in 73 autopsy cases, histologically classified ingroup IV: the tubular differentiation is poor and the mucus in the cytoplasm is rich. Acombination oftwo morphologicalfeatures, the degree oftubular differentiation and the contentofmucus in the cytoplasm, was used to classify the histological types ofgastric carcinoma intofour groups. The mode ofdevelopment and recurrence in autopsy cases was assessed according tothe histological types ofprimary lesion. As a result, the characteristic mode ofdevelopment andrecurrence could be observed in thefour histological groups. Furthermore, there were statisticallysignificant differences in the incidence and severity ofthe metastases among the groups.

COMPARISON BY MODE OF DEVELOPMENT AMONGTHE HISTOLOGICAL GROUPS AND THE STATISTICALANALYSIS OF THE CHARACTERISTICSThe mode of development of gastric carcinoma,as determined by the incidence and severity ofvarious types of metastasis, were comparedamong the histological groups. The results wereanalysed statistically using the Kruskal-WallisH-test in an attempt to clarify the characteristicsof the mode of development in the histologicalgroups and to assess the significance of the newhistological classification. There were 97 patientsin groups I, III, and IV. The seven patients ingroup II were excluded from the analysis in thepresent study because of the limited number.The results of the analysis are shown accordingto the type of metastasis.

Liver metastasisThe H-test analysis indicated significantdifferences in the incidence and severity ofliver metastasis among the three histologicalgroups (p<OOl). The groups in the order ofthe highest incidence and severity were I, III, andIv.

Lymph node metastasisThere were also significant differences in theincidence and severity of lymph node metastasisamong the histological groups (p<005). Asautopsy patients usually have highly advancedcancer (terminal cancer), the incidence oflymph node metastasis was naturally high. Thegroups in the order of the highest incidence andseverity of lymph node metastasis were IV, III,and I.

Direct invasionThere were also significant differences in theincidence and severity of direct invasion amongthe histological groups (p<OO1). The groups inthe order of the highest incidence and severitywere IV, III, and I.

Peritoneal disseminationThere were significant differences in the incid-ence and severity of peritoneal disseminationamong the histological groups (p<O0Ol). Thegroups in the order of the highest incidence andseverity were IV, III, and I.

Metastasis to the bone marrowThere were significant differences in the incid-ence and severity of bone marrow metastasisamong the histological groups (p<0-01). Thegroups in the order of the highest incidence andseverity were III, IV, and I.The statistical significance of the differences

among the histological groups was furtheranalysed using Wilcoxon's two sample test (ttest). There were significant differences betweengroup I and III (p<O0O1) and group I and IV(p<005). No significant difference wasobserved, however, between groups III and IV(p<O- 10).

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Discussion

HISTOLOGICAL CLASSIFICATION OF GASTRICCARCINOMA ACCORDING TO THE TUBULARDIFFERENTIATION AND MUCUS PRODUCTIONHistologically, the criteria for the histologicalclassification of tumours has been based on themorphological characteristics of (1) the organwhere carcinoma originated and (2) the histo-genesis, or (3) the degree and the characteristicsof the atypical cells.The histological classification of gastric

carcinoma such as Lauren's classification andNakamura's classification in Japan is based onthe findings of the proposed histogenesis. On theother hand, the classification by the Jpn RSGC orOhta (Ohta's classification8) uses the degree andfeatures of the atypical cells.The histological classification examined in this

paper uses a combination of the two character-istics of gastric cancer, the structural feature oftubular differentiation, and the functional statusofmucus production.The use of tubular differentiation as an index

of the structure of cancer tissue is unlikely toraise any questions. The use of the mucuscontent in the cytoplasm as an index of thefunctional characteristic of gastric cancer cells,however, may be debatable. Because signet ringcell carcinoma proliferates in a disorganisedfashion and does not form glandular tubules, theformed mucus cannot be drained, this causesmucus to accumulate in the cytoplasm. Accord-ing to Nagayo, an electron microscopic study ofsignet ring cells appearing small and containing arelatively limited amounts of mucus as seenunder a light-microscopic examination (type Iaccording to his classification) revealed mucussecretion, the presence ofabundant organelles inthe cells, and well developed microvilli on thesurface of the cells.7

It is therefore too short sighted to merelyconclude that the accumulation of mucus insignet ring cell adenocarcinoma is attributableto the absence of tubular differentiation thathampers the drainage of the mucus. For thisreason, we chose the amount of mucus in thecytoplasm as an index of the functional status ofgastric cancer and used it in combination withthe structural characteristic of tubular differen-tiation for the histological classification of gastriccarcinoma. This method must be assessedfurther in a greater number of patients.

MODE OF DEVELOPMENT OF GASTRIC CARCINOMAACCORDING TO THE HISTOLOGICAL TYPETo date, a number of studies have been con-ducted on the mode of development of gastriccarcinoma in autopsy cases.9-'4 Basically, theresults of the present study are not entirely

different from those of other studies. Neverthe-less, there has been gradual progress in variousmethods of treatment in cancer therapy and, as aresult, the clinical course of gastric carcinoma upto the time of death - that is, the mode ofdevelopment and recurrence has changed in asubtle way.

Furthermore, it is apparent from the results ofthe statistical analysis of the current study, thatthe classification of primary lesions by the newhistological classification of gastric carcinoma isuseful in predicting the conditions of the meta-stases observed during an autopsy. This meansthat the method in question has a high rate ofpredictability for the mode of development andrecurrence of gastric carcinoma if applied tothe classification of the histological features ofa stomach biopsy and resected specimens.Furthermore, the use of the new histologicalclassification seems to be helpful in determiningthe site of examination, the necessary precau-tions, and the guidelines for treatment duringthe follow up period. Thus far, the authors havenot compared this classification with other classi-fication methods, but a comparative study will beconducted in the future.

The authors are deeply grateful to Takanori Mochizuki, MD,former Director of the Department of Pathology, Tokyo Metro-politan Komagome Hospital, for his guidance in conducting thepresent study and to Tadashige Murakami, MD ex-Professor ofthe First Department of Surgery, School of Medicine, TokyoMedical and Dental University, for his words ofencouragement inthis study.

1 Jarvi 0, Lauren P. On the role of heterotopias of the intestinalepithelium in the pathogenesis of gastric cancer. Acta PatholMicrobiol Scand 1951; 29: 26-44.

2 Lauren P. The two histological main types of gastriccarcinoma. Acta Pathol Microbiol Scand 1965; 64: 31-49.

3 Mulligan RM, Rember RR. Histogenesis and the biologicalbehavior of gastric carcinoma. Arch Pathol 1954; 58: 1-25.

4 Morson BC. Carcinoma arising from areas of intestinal meta-plasia in the gastric mucosa. BrJ Cancer 1955; 9: 377-85.

5 Nakamura K, Sugano H, Takagi K, Kumakura K.Histogenesis of carcinoma of the stomach with specialreference to 50 primary microcarcinomas: light-/Electron-microscopic and statistical studies. Jpn J Cancer Clin 1969;15: 627-47.

6 Japanese Research Society For Gastric Cancer. The Generarulesfor the study ofgastric cancer in surgery andpathology. 11thed. Tokyo: Kanehara Publishing, 1985.

7 Nagayo T. Igan Soshikihassei ni kansuru Soshikigakuteki,Jikkenteki Kenkyu. Transactiones Societatis Pathologicaejaponicae 1976; 65: 3-25.

8 Ohta K. Igan no Hassei. Transactiones Societis PathologicaeJaponicae 1965; 53: 1-16.

9 Imai T. The growth of human carcinoma - a morphologicalanalysis. Fukuoka Ishi 1954; 45: 45-102.

10 Furuno H. Pathological anatomical studies on the matastasis ofthe stomach carcinoma. Igaku Kenkyu S 32; 27: 1496-151.

11 Araki T. A patho-morphological study on the distribution ofthe metastasis of gastric carcinoma - especially the clinico-pathological consideration for the cases of gastric carcinomanot identifiable clinically. Transactiones Societatis Patho-logicaeJaponicae 1959; 48: 757-98.

12 Tanaka T. Pathological studies on the lesion of gastric cancerand the distribution of its metastases - a comparative studybetween gastrectomied and non-gastrectomied cases. ShowaIgakukai-shi 1963; 23: 362-87.

13 Soejima K. The recurrence of gastric cancer - a review of 21cases examined at autopsy. Fukuoka Igaku-zasshi 1%3; 55:410-30.

14 Ishii T, Ikegami N, Hosoda Y, Koide 0, Kaneko M. Thebiological behavior of gastric cancer. J Pathol 1981; 134: 97-115.



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Differences cancer histological type: of carcinoma · lymph node metastasis, direct invasion into surrounding organ, andperitoneal dissemina-tion werehigher. In groupIII, whichshowed