Ross Golden, M.D.

Early detectionof cancerof thestomach may mean detection of a smallcancer,orofcancerbeforeithasspreadbeyondthewallsofthestomach,orofcancer before it has produced symptoms. Small cancers may already havemetastasized before the disease is recognized and removed.

Two direct objective methods of detection of cancer of the stomach areroentgenography and gastroscopy. It isunfortunate that these two methods areoften regarded as rivals rather than ascomplementary methods, each of whichhas its particular advantages and limitations.

Carcinoma of the stomach can bedetected by roentgen-ray methods onlywhen it has produced a recognizablemodification of the form or of themovements of the stomach. First theabnormality must be demonstrated andthen it must be recognized as the res.lltof cancer. This depends upon two factors: (1) the location of the growth inthe stomach, and (2) the gross growthcharacteristics,notthemicroscopicappearance of the cells, of the neoplasm.

Location of the Growthin the Stomach

A study of the roentgenograms of315 proved cases of carcinoma of thestomach seen at the Presbyterian Hospital in New York showed that approximately 75 per cent arose in the antrum,20 per cent in the body or media, and5 per cent in the fundus. The fundusmay be defined as that portion of thestomach lying roughly above the levelof the cardiac orifice, the body or media as that portion between the cardiacorifice and the incisura angularis, andthe antrum as the portion that turns tothe right and extends to the pylorus.

Dr. A. Purdy Stout made a similar

mE@Ez@I:@iII@1Figure 1. The location of 120 car

cinomas in 120 resected stomachs(Stout's diagram).

study of 120 resected cancers of thestomach. His diagram is reproduced inFig. 1. It is obvious that the distributionof these cancers is similar to that described in the preceding paragraph.

It is apparent from these two studiesthat the great majority of carcinomasarise in the lower half of the stor@iach.This is the motor portion, accessible topalpation and pressure under the fluoroscope, where abnormalities of formand disorders of movement can be mosteasily demonstrated. Carcinomas of thefundus in general are much more difficult to detect; and they present technical problems beyond the scope of thisdiscussion.

Gross Growth CharacteristicsCarcinoma of the stomach arises in

the mucous membrane but grows indifferent ways in different individuals.Classification of these growths according to the microscopic appearance ofthe cells is useless from the standpointof understanding the effect of the neoplasm on the stomach wall. Further

From the Department of Radiology of the Col.lege of Physicians & Surgeons of Columnbia Uni.versity and the Radiological Service of the Presby.terian Hospital, New York, New York.

Figures 1, 2, 6A, and 7 are reproduced fromnGolden: Diagnostic Roentgenology, Volumime 1,The Williams and Wilkins Company, Baltimore.

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Early Detection of Carcinoma of theStomach

The PENETRATINGtypeapparentlyextends through all layers of the stomach wall to the serosa early in its development. It destroys and replaces themuscle. It invariably ulcerates. Thistype was found in 32 per cent of the342 cases. Because of the ulceration,the lesion is easy to detect but it may bedifficult to differentiate the excavationin the penerating carcinoma from someof the benign peptic ulcers. This aspectof the problem cannot be discussedhere (Fig. 3).The SUPERFICIALSPREADINGtypeex

tends along the wall in the mucosa andsubmucosa and in some cases is limitedto the mucous membrane. It may produce tiny nodular elevations on thesurface (Fig. 4). It may ulcerate. Thisis the type of carcinoma found in themucous membrane adjacent to themargin of some gastric craters thathave the structural characteristics ofbenign peptic ulcers. The new growthmay completely encircle the crater butusually involves only a portion of itscircumference. The carcinoma adjacent to the benign crater may itself ul

@erateproducing a double or a lobulated crater shadow (Fib. 5). In itslater stages the malignant cells pass tothe scerosa through the musculariswithout destroying or replacing themuscle cells. In one instance (Fig. 6)the mucosa of the entire stomach wasreplaced by carcinoma, with malignant

Figure 2. B, The photograph of thespecimen shows a mass projecting fromthe mucosa into the lumen of the stomach.

@..

Figure 2. The fungating type of carcinoma of the stomach. A, A large filling defect is shown on the greatercurvature of the antrum.

more, the characteristics of the cellsmay vary in different parts of thegrowth. On the other hand the mannerin which the growth involves the wall isof great importance. The gross growthcharacteristics form the basis of Stout'sclassification of carcinoma of the stomach (Golden and Stout):

(1) fungating; (2) penetrating; (3)spreading—(a) superficial type, (b)linitis plastica type; (4) advanced, unclassifiable.

FUNGATING growths were present in

26 per cent of 342 cases seen in theDepartment of Surgical Pathology atthePresbyterianHospitalbetween1937and 1949. This type forms a massprojecting into the lumen. It may reacha large size before it penetrates intothe submucosa, and it metastasizes late.Itmay or may notulcerate.Becauseof itsmass the fungatinggrowthisrelatively easy to detect (Fig. 2).

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cells lying among the muscle bundlesof the hypertrophied muscularis; thisstomach expelled barium rapidly butthe contractions were unlike flexibleperistaltic waves. In other instances aslight stiffening or flattening of the wallwas present at the site of involvementof a relatively small area with no extension into the muscularis itself. Thereason for this phenomenon is notclear.

SUPERFICIAL SPREADING carcinoma

comprised 11 per cent of the 342 cases,of which approximately four fifthswere associated with ulceration, eitherwith a peptic ulcer or with an excavation in the cancer itself. The abnormality is more easily detected if an excavation in the carcinoma is present.As a result of follow-up observationson some of the early cases, Stout believes the prognosis is better in this typeof cancer than the average of all cancers of the stomach.

The LINITIS PLASTICAtype of spreading carcinoma extends along the wallin the submucosa, the muscle coat, andthe subserosa. It does not destroy themucosa until very late in the disease(Fig.7). Itisoftenassociatedwith

Figure 3. The penetrating type ofcarcinoma of the stomach. A, Theroentgenogram discloses evidence of alarge flat ulcer on the lesser curvature.

.@..,-f, , . I.&‘:@ @. :@

Figure3.B,A low-powerphotomicrographof themarginof thecratershowsnormal muscle cells on the left. On the right, adjacent to the crater, the muscle isreplaced by carcinoma.

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Figure 4. The superficial spreadingtype of cancer of the stomach. A, Theroentgen - ray examination disclosesmarked antral spasm, interpreted asantral gastritis. Gastroscopy disclosedsmall carcinomatous nodules on theanterior wall of the antrum where aboutten months previously an area ofatrophic mucosa with superficial erosions had been seen.

Figure 4. B, The resected specimenshowed an area of carcinomatous infiltration about 6x9 cm. along the lessercurvature and extending on to bothanterior and posterior walls, outlinedby arrows. (The pylorus is on the left;the lesser curvature, on the right.) Inits center were small nodules about 3to 5 mm. in diameter with slightly depressed areas of ulceration. The involved area of mucosa was immovableover the muscle. Microscopic examina[ion showed that the carcinoma involved only the mucosa and had not extended into the submucosa.

with the group of carcinomas that aretoo far advanced to be classified withcertainty under these headings. Thisgroup comprised 25 per cent of 342cases.

high stiff mucosal folds, closely resembling those associated with gastritis—¿�insome cases both on roentgen-rayand gastroscopic examination (Fig. 8).In most cases the malignant cells stimulate the growth of fibrous tissue,which may vary from very slight to extreme. The linitis plastica type of carcinoma was found in 6 per cent of the342 cases.

Stout concludes his classification

Figure 4. C, A low-power photomicrograph shows carcinomatous nodules on theleft with atrophic mucosa on the right.

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methods because of the mass that produces a filling defect in the bariumshadow.Itmay be stimulatedby anymassthatprojectsintothelumenfromthe stomach wall, for example a smallleiomyoma, a polyp, or a localizedmass of so-called giant mucosal folds.If the fungating carcinoma has ulcerated, it is not likely to be confusedwith another growth.

The penetrating carcinoma is easilydetected because of its excavation. Theproblem is to differentiate it from abenign gastric ulcer. This growth replaces muscle and stiffens the wall overthe involved area.

Superficial spreading carcinoma extending along the wall and replacingthe mucosa sometimes produces smallnodular elevations on the surface and,at least in many cases, obliterates penstalsis over the involved area in spite ofthe fact that the muscle has not beendestroyed. It often causes a localizedsegmental spasm of the muscularismanifested by an incisura. Small nodules on the mucosa may also be produced by gastritis.

Figure 5. C, The gross specimen disclosed a deep crater with the usualcharacteristics of a peptic ulcer base.Around part of its circumference wassuperficial spreading carcinoma whichhad ulcerated. This shallow ulcerationin the carcinoma produced two of thecontours of the crater shadow shownin B. (Lesser curvature on right.)

Figure 5. Superficial spreading carcinoma with a peptic ulcer. A, Theroentgenogram of the barium-distended stomach discloses a crater shadow on the lesser curvature (arrow).Other projections disclosed a doublecontour of the apex of the crater.

It is quite obvious that the problemof detection of the carcinoma by roentgen-ray methods is different in thesegroups.

Growth Characteristics and theRoentgenographic Examination

The fungating carcinoma is theeasiest of all to detect by roentgen-ray

LFigure5.B,A supinespot-filmwith

the ulcer en face discloses a trilobedappearance.

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b.,.@ Jj

I

Figure 6. Advanced superficialspreading carcinoma. A, Three roentgenograms reproduced here show (1)absence of mucosal folds and (2)strong deep contractions that expel thebarium rapidly.

be intramural rather than extendingthrough the wall. The mucosal foldsradiate toward but usually stop shortof the crater. Some benign peptic ulcersare shallow and do not penetratethrough the wall, and for this reasonunfortunately the differential diagnosiscannot be made with absolute certaintyin some instances.Ulcerationmayoccur in superficial spreading carcinoma arising in the mucosa adjacentto a benign crater. This may produce abibbed or trilobed crater.

A differential diagnosis between apenetrating ulcer and an ulceratingsuperficial spreading carcinoma cannotbe made with certainly. Under somecircumstances a trial of medical treatment is advisable on the theory thatthe benign ulcer will reduce in size during a period of two to three weeks. Unfortunately, the excavation in some carcinomas will fill in to a certain extentwith carcinoma tissue when the digestive power of the gastric juice is reduced. However, the two types of ulcerrespond differently. The benign craterisusuallyreducedtoonehalfitsprevi

This is the type of carcinoma sometimes found adjacent to an excavationthat has the pathological characteristics of a benign peptic ulcer. The typical benign ulcer extends through allcoats of the stomach and has its baseon or beyond the serosa. The depth ofthe benign crater is usually relativelygreat as compared to its diameter. Itsmargins are often undermined. Themucosal folds radiating toward it oftenappear to extend into the crater shadowbecause the mucosa overhangs the excavation in the muscle.

The excavation in the penetrating orsuperficial spreading carcinoma is shallow with sloping saucer-like margins,without undermining, and appears to

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Figure 6. B, Photograph of the grossspecimen shows thickening of the wallof the stomach from one end to theother. The wall measured 1.5 cm. nearthe pylorus and 0.5 cm. at the fundus.The mucosa was replacedthroughoutby carcinoma.

ous size or less in three weeks; it diminishesintransversediameteraswellasin depth. The crater in the carcinomareduces somewhat in depth but changesvery slightly in transverse diameter.Failure of a crater to behave properly

Figure 6. C, A low-power photomicrograph shows the preserved hypertrophiedmuscleatthebottomof thesection. The muscle was hypertrophiedandwas widerthantheentirewallofanormal stomach. The mass of tissueabove the muscle was carcinoma whichhad replaced the mucosa and filled thesubmucosa. Malignant cells had infiltrated through the muscle bundles totheserosa.

Figure 7. Linitis plastica type of carcinoma. A, The roentgenogram showsevidence of stiffening of the middlethirdofthestomachwithlargemucosalfolds along the greater curvature. Normal peristaltic waves were seen in thelower part of the antrum.

under treatment can be taken as evidence in favor of malignant disease.

The linitis plastica type of carcinomais the most subtle, difficult, and dangerous of all. Because it infiltrates toand along the subserosa, it metastasizesrelatively early through the lymphaticsand spreads over the peritoneum. Because the muscle is not destroyed, thewallisnotstiffeneduntilverylateand,even when the growth is extensive, apparently normal peristaltic waves passalong the stomach wall. In some casesthemucosalfoldsmay be obliteratedbut more frequently they are elevatedin a manner simulatingtheeffectofgastritis polyposa. In such cases gastroscopy discloseslargefoldsof apparently intact mucosa.

The amount of fibrous tissue associated with the linitis plastica tumorcells in the wall varies greatly in different individuals. In one case prac

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V

Figure 7. B, Pressure films along the greater curvature show star-shaped shadowsproduced by barium caught between thickened mucosal folds which resemble cratershadows.

tically no fibrosis was present but thetumor cells spread through the wall intypical linitis-plastica fashion. In welladvanced cases the mucosal folds arelarge and stiff, and pressure films mayshow the creases between the foldsradiating from a point that resembles acrater shadow but that is not an ulcer.

Figure7.C, The resectedstomachwas opened along the greater curvature where thick mucosal folds can beseen.The carcinomahad infiltratedunder the mucosa without destroyingitandwasresponsibleforthethickenedfolds. The malignant cells infiltrated tothe serosa without destroying themuscle and had produced a moderateamount of fibrosis. Dr. Stout describedthis as the smallest linitis-plastica typeof carcinoma he had encountered uptothattime.

It is my impression that, when fibrosisis marked, the inner surface of thestomach is more likely to be abnormally smooth and to resemble the rarecases of atrophic gastritis with veryfew mucosal folds. Its lesser curvaturemargin may show fine irregularities.The more the fibrosis, the more thestomach becomes diminished in sizewith reduced expansibility or distensibility when a barium preparation isswallowed or when air is introducedfor gastroscopy. It must be emphasizedthat this description of this disease isinadequate. This type, even when welladvanced, is the most difficult of allcarcinomas of the stomach to detectand to differentiate from inflammatorychanges. I have yet to see a case survive as long as five years after resection.

The unclassifiable advanced growthsare, in the great majority of cases,demonstrated by roentgen-ray methodswith relative ease and need no furtherdiscussion here.

SummaryThe detection of carcinoma of the

stomach by roentgen-ray methods, andto a certain extent by gastroscopy, depends upon two basic physical factors:

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(1)thelocationofthegrowthinthestomach, and (2) the gross growthcharacteristics of the tumor, i.e., thephysical manner in which the tumor involves the stomach wall. Stout's classi

fication is based on this second factorand is the foundation for an understanding of the clinical evolution of thisdisease and of the difficulties encountered in attempting to detect it.

Figure 8. Linitis plastica type of carcinoma of the stomach. Three roentgenograms (A,B,C) are reproducedhere to show (1) the remarkable flexibility of the wall manifested by deepperistaltic waves that expelled bariumrapidly, and (2) the great thickeningof the mucosal folds. Pressure films disclosed the appearance shown in Fig.7, B. The gastroscopist interpretedthe thickened folds of intact mucosaas evidence of gastritis. At operationextensiveinoperablecarcinomawasfound. A biopsy of the wall, which didnot go clear through to the mucosa,disclosed carcinoma cells infiltratingthrough the muscle without destroyingit and growing along the subserosa.Very little fibrosis was present. Thepreservation of the muscle and the absence of fibrous tissue explain the ability of the stomach to produce deepperistalsis.

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