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Malignant gastric ulceration
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A REVIEW OF 26 C A S E S IN W H I C H T H E R E W A S D E L A Y IN T H E D I A G N O S I S BY G. A. S. LLOYD, B.M., B.Ch., D.M.R.D., AND J. L. MORRIS, M.B., B.Ch., D.M.R.D. FROM THE RADIODIAGNOSTI C DEPARTMENT OF THE LONDON HOSPITAL, WHITECHAPEL
INTRODUCTION GASTRIC neoplasms commonly present at barium meal examinations as ulcerative lesions. T h e earliest changes which occur d e m a n d a high standard of radiological technique for their demonstration and the problem of interpretation at this stage may be very difficult, especially with ulcers situated on the lesser curvature, since they have to be differentiated from benign lesions. I n this paper we have selected for investigation a series of neoplastic ulcers in which there was serious delay before a correct diagnosis was reached. T h e majority of these had presented a considerable diagnostic p r o b l e m to the radiologist and all had been examined more than once. I t was thus possible to review the original radiographs and those of later examinations in sequence, together with the radiological reports made at the time. Using this method, our principal objects have been to in~vestigate the earliest changes which occur in these neoplasms and to study their subsequent development ; also to show how far the classical criteria of malignant gastric ulceration are applicable in the early stages, a n d to determine the major causes of diagnostic delay when these have been radiological in origin.
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Examination of the records of the Bernhard Baron Institute of Pathology of the London Hospital revealed a diagnosis of gastric carcinoma in 254 cases from post-gastrectomy specimens in the years I949-53 inclusive. Of these there were 23 cases of carcinomatous ulcer, whose radiographs were available for study, and which fulfilled the following criteria : - - ( i ) T h e r e was evidence of ulceration of the body, cardia, or pyloric antrum, excluding the pre-pyloric area. F o r the purposes of anatomical localization we have used the terminology proposed by Russell, Weintraub, and T e m p l e (i948). (2) T h e r e was a delay of more than two months from the time of the first b a r i u m meal examination to gastrectomy. T h r e e other cases were added to the original 23. One of these was a case of sarcoma of the stomach diagnosed after gastrectomy, and 2 were carcinomata of the stomach, in which the diagnosis was made by a combination of gastroscopy and biopsy, and gastroscopy and peritoneoscopy.
CASE
REPORTS
T e n illustrative case summaries are appended. Brief clinical, gastroscopic, and pathological details are included, but the main attention is focused on the radiograph reports at the time of examination. W h e r e necessary, the anatomical terms in the actual reports have been altered to preserve the uniformity of terminology. A short comment is given after each case. Case I.--C. B. Female. Born 1886. Presented Oct. 28, 1952, and diagnosed clinically as a functional dyspepsia, possibly gastric ulcer. First barium meal, Nov. 14, I95Z, reported an irregularity of the pyloric antrum, possibly due to spasm. No ulcer reported. (Films show flat projection at the incisura angularis and shortening of the lesser curvature, Fig. 192 A.) Attended again May z6, 1953, complaining of diarrhoea and the clinical diagnosis of ' colonic dysfunction ' was made. A second barium meal was not performed until Nov. 18, 1953. This showed a ' saddleback ' ulcer at the incisura angularis, associated with a filling defect, and the diagnosis of carcinoma was made (Fig. 192 B). Gastrectomy was performed Nov. 27, and the specimen showed a carcinomatous ulcer 2 cm. in diameter with rolled edges. C o m m e n t . - - C a r c i n o m a presenting as a flat ulcer with lesser curve shortening.
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Case z . - - H . R. Male. B o r n I893. P r e s e n t e d Nov. i3, x95o, with a t w o - m o n t h history of epigastric pain lasting the whole day, a n d n o t relieved by p o w d e r or food. T h e r e was also anorexia a n d wasting. T h e clinical diagnosis was c a r c i n o m a of t h e stomach. A barium meal at this time, N o v . I4, z95o (Fig. ~93), was reported as
B A Fig. I92.--The original film (A) shows a flat projection at the incisura angularis which eventually became an ulcer within a large filling defect (B).
s h o w i n g a flat projection on the lesser c u r v e of t h e b o d y and diagnosis of chronic gastric ulcer was m a d e . A t a second barium meal on M a y 29, I95I, t h e ulcer was reported as being smaller, signifying healing. (Review of these films s h o w s a flat ulcer with a s u r r o u n d i n g half shadow, almost certainly a filling defect.) S u b s e q u e n t l y the patient i m p r o v e d s y m p t o m a t i c a l l y for eight m o n t h s , a n d t h e r e was an increase in weight of I5 lb., b u t his condition deteriorated in t h e following two m o n t h s . T h e r e was no pain, b u t he felt poorly a n d was pale. N e o p l a s m of t h e s t o m a c h was again s u g g e s t e d clinically. Barium meal at this time s h o w e d an extensive n e o p l a s m of the whole of the lesser curve, and t h e r e was a palpable l u m p . Peritoneoscopy Jan. 9, I952, s h o w e d a gastric m a s s with s e c o n d a r y deposits in the liver. T w o m o n t h s later t h e ulcer perforated a n d t h e patient died. " Comment.--Carcinoma presenting d i a g n o s e d as c h r o n i c g a s t r i c u l c e r .
Fig. I93.--Flat carcinomatous ulcer on the lesser curvature of the body of the stomach.
a s a flat u l c e r ,
mis-
Case 3 . - - F . S. Male. B o r n i898. P r e s e n t e d in F e b r u a r y , I95I, w i t h six m o n t h s ' history of epigastric pain two h o u r s after food, poor appetite, a n d weight loss. Clinical diagnosis d u o d e n a l ulcer, possibly n e o p l a s m . A barium meal, Feb. I5, was reported as n o a b n o r m a l i t y detected. (Films s h o w a very small, flat projection on t h e lesser curve at t h e incisura angularis.) (Fig. I94 A.) Clinically regarded as a d u o d e n a l ulcer a n d treated as such. A second barium meal I3 months later, M a r c h 6,
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1952, reported as showing a fiat ulcer distal to the incisura angularis, with convergent folds and diagnosed as neoplasm. (The films show, in addition, an incisura of the greater curve side of the pyloric antrum.) (Fig. 194 B.) T h e diagnosis was confirmed by gastroscopy and biopsy. Comment.--Carcinoma p r e s e n t i n g as a s m a l l flat ulcer at t h e i n e i s u r a a n g u l a r i s , n o t r e c o g n i z e d at first e x a m i n a t i o n , clinically t r e a t e d as a d u o d e n a l ulcer. T h e final b a r i u m m e a l d e m o n s t r a t e d a typical m a l i g n a n t ulcer.
A
B
Fig. I 9 4 . - - S m a l l plateau ulcer at the incisura angularis (A) which eventually showed features considered characteristic of a malignant ulcer (B).
A
B
Fig. 195.--Carcinomatous ulcer simulating a benign lesion with converging mucosal folds and lesser curve shortening of the type described in the text (A).
B shows the appearance 15 months later immediately prior to gastrectomy.
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Case 4 . - - E . R. Female. Born 1899. First a t t e n d e d t h e L o n d o n Hospital Oct. 3 o, 1948 with history of thirty years' i n d i g e s t i o n a n d acid eructation, a n d pain in the left side for four m o n t h s . Clinical diagnosis of duodenal ulcer. Barium meal at this time, Nov. 25, a large gastric ulcer was reported low d o w n on t h e lesser curve of t h e body of t h e stomach. (Films s h o w a large gastric ulcer with c o n v e r g e n t folds, s h o r t e n i n g of t h e lesser curve a n d an incisura of the greater curve of t h e pyloric a n t r u m , Fig. I95 A.) She h a d no pain for t h e following thirteen m o n t h s , a l t h o u g h her weight d u r i n g this time d r o p p e d b y 5 lb. I n D e c e m b e r , 1949, s h e b e g a n to g e t pain again, a n d at the second barium meal, March i, 195o, t h e report stated that there was lesser curve s h o r t e n i n g a n d excess resting secretion b u t no ulcer was d e m o n s t r a t e d . ( T h e films s h o w t h a t the s h o r t e n i n g h a d increased, and there was m o r e m a r k e d deformity of the pyloric a n t r u m , Fig. 195 B.) T h e r e h a d been a drop of a stone in weight in t h e previous three m o n t h s . G a s t r e c t o m y was p e r f o r m e d on M a r c h 17, a n d a s p e c i m e n s h o w e d a shallow ulcer 7 × 4 cm. in t h e m i d d l e of t h e lesser curve, histologically a carcinoma. Comment.--Carcinoma p r e s e n t i n g as a c o n i c a l ulcer with gross antral deformity, and shortening of t h e l e s s e r c u r v e , d i a g n o s e d as a b e n i g n g a s t r i c u l c e r .
Fig. z96.--Conical malignant ulcer at the incisura angularis with mneosal convergence,
Case 5 . - - G . M. Male. Born 19o6. A t t e n d e d the L o n d o n Hospital in D e c e m b e r , 1952, c o m p l a i n i n g of 6 to 7 weeks' belching and epigastric pain. Clinically t h o u g h t to be a peptic ulcer r a t h e r t h a n a n e o p l a s m . Barium meal at this time, Dec. 3 i, reported a gastric ulcer at t h e incisura angularis, with c o n v e r g e n t folds (Fig. 196). D i a g n o s e d as b e n i g n gastric ulcer. T h e r e was loss of weight d u r i n g the following four m o n t h s , a n d a second barium meal, March io, 1953, reported no change. S u b s e q u e n t l y t h e r e was s o m e i m p r o v e m e n t in the clinical condition a n d a f u r t h e r barium meal, April 21, again reported no change. G a s t r e c t o m y was p e r f o r m e d two weeks later a n d an ulcer 2 cm. in diameter, w i t h shelving edges a n d s u r r o u n d i n g thickening, was found. It was t h o u g h t to be simple macroscopically. Histologically this was a diffuse scirrhous carcinoma.
Comment,--Carcinoma p r e s e n t i n g as a c o n i c a l u l c e r at t h e i n c i s u r a a n g u l a r i s w i t h m u c o s a l c o n v e r g e n c e , d i a g n o s e d as b e n i g n g a s t r i c u l c e r .
Case 6 . - - J . G. Male. Born 1895. First seen at the L o n d o n Hospital Jan. 23, 195o, c o m p l a i n i n g of u p p e r a b d o m i n a l fullness and s h o r t n e s s of b r e a t h for a year. Pain was colicky a n d h e h a d p a s s e d blood per r e c t u m one m o n t h previously. Clinical diagnosis was n e o p l a s m of the colon. B a r i u m e n e m a at this time ' no a b n o r m a l i t y detected '. Seen again July 29, 1952, c o m p l a i n i n g of dyspepsia for two years. Barium meal at this time, Aug. 7, reported as ' n o a b n o r m a l i t y d e t e c t e d ' . (Films s h o w a small flat ulcer on t h e lesser curve of t h e body of t h e stomach, Fig. 197 A.) T h e patient was seen in A u g u s t , 1953, a n d a second barium meal, Sept. i, reported an encastrd defect h i g h on t h e lesser curve, diagnosed as c a r c i n o m a (Fig. 197 B). G a s t r e c t o m y was p e r f o r m e d four weeks later a n d showed an ulcerated i n t r a l u m i n a l carcinoma j u s t below t h e cardia. Histologically this was a well-differentiated carcinoma. Comment.--Carcinoma at first examination.
p r e s e n t i n g as a flat u l c e r o n t h e l e s s e r c u r v e o f t h e b o d y , n o t r e c o g n i z e d
Case 7 . - - M . P. Female. Born 1894. A t t e n d e d Aug. i, 1947, c o m p l a i n i n g of epigastric pain for eighteen m o n t h s . Barium meal, Oct. 8, reported a conical gastric ulcer on t h e lesser curve of t h e b o d y (Fig. 198). T h e barium meal was repeated two months later, Dec. 1. A gastric ulcer with c o n v e r g e n t folds was repoiTted. T h e appearances were considered to be ' odd '. (Films s h o w an irregular r e c t a n g u l a r ulcer ; the incisura on the greater curve was still present.) _//.third barium meal, Feb. 1948, was reported as s h o w i n g a gastric ulcer. (Films s h o w little change f r o m t h e previous b a r i u m meal.) D u r i n g t h e following three and a half years, no b a r i u m meals were performed, b u t the patient was gastroscoped on f o u r occasions. At first the lesion
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was t h o u g h t to be p o s s i b l y neoplastic, b u t a diagnosis of a b e n i g n lesion was later made, as the ulcer appeared to be healing. It was never reported as healed. A fourth barium meal, July 6, I95I, s h o w e d gross irregularity a n d d e f o r m i t y of the greater curve of t h e lower part of t h e body, a n d d e f o r m i t y of the lesser curve at t h e site of previous ulceration. G a s t r e c t o m y was p e r f o r m e d six weeks later. S p e c i m e n showed a large ulcerated m a s s
A
B
Fig. i97.--Small plateau ulcer (A) which became a plateau ulcer within a shallow filling defect (nicheenplateau encastrde)(g). astride t h e greater curve, histologically an anaplastic carcinoma. b e n i g n ulcer.
Pathological diagnosis was c a r c i n o m a in a
Comment.--Carcinoma p r e s e n t i n g as a c o n i c a l u l c e r w i t h g r e a t e r c u r v e i n c i s u r a , d i a g n o s e d as s i m p l e g a s t r i c u l c e r . The ulcer did not heal for nearly four years.
Case 8 . - - H . S. Male. B o r n I89o. First attended t h e L o n d o n Hospital in i 9 3 8 - - n o notes are available. D o u b t f u l d u o d e n a l ulcer, diagnosed at b a r i u m meal. A t t e n d e d again Feb. 5, I947, with a ten-year history of periodic epigastric pain one h o u r after food, lately associated with acid reflux. Barium meal, Feb. i I , gastric ulcer reported on the lesser curve of t h e u p p e r t h i r d of t h e body of t h e stomach. (Films show a conical ulcer crater, Fig. 199 A.) Barium meal was repeated July zz. T h e ulcer was reported as being still present, b u t shallower. A third barium meal, Nov. 4, was reporte:l as ' n o a b n o r m a l i t y d e t e c t e d ' . (Films are rather poor, b u t s h o w w h a t appears to be a conical ulcer on the lesser curve of the body.) A fourth barium meal, Dec. 5, I949, reported a h i g h gastric ulcer, larger t h a n previously, p r o b a b l y benign. ( T h e films show a large ulcer e n c r o a c h i n g u p o n the l u m e n of t h e stomach, Fig. I99 B.) O n C h r i s t m a s D a y of t h a t year, he was feeling as well as at any t i m e in the past eighteen m o n t h s , b u t after d i n n e r h a d a severe h~ematemesis. H e was a d m i t t e d a n d a g a s t r e c t o m y was p e r f o r m e d , Jan. 6, 195o. S p e c i m e n s h o w e d a 3 cm. diameter ulcer on t h e lesser curve of the b o d y of t h e stomach, histologically a carcinoma. Comment.--Carcinoma presenting H ~ e m a t e m e s i s l e d to g a s t r e c t o m y .
as a c o n i c a l u l c e r o n l e s s e r c u r v e , d i a g n o s e d
as s i m p l e .
Case 9 . - - E . E. Male. B o r n I884. First attended Jan. 7, *943 -with glycosuria a n d treated as a diabetic. A t t e n d e d s u b s e q u e n t l y in I947 a n d gave a history of attacks o f epigastric p a i n half an h o u r after food in I933,
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and further attacks in 1942. He was well in between the attacks and up until June, 1947, when the pain recurred. Barium meal, Nov. I i, I947, reported a medium-sized flat gastric ulcer just above the incisura angularis. (Films show a fiat ulcer on the lesser curve of the body.) Barium meal was repeated, April 9, 1948. An ulcer was shown only in the prone position, and reported to be healing. A third barium meal, Sept. 14, reported a small niche which was tender. (Fihns show a small niche a short way above the incisura angularis, apparently higher than the previous ulcer.) Attended during 1948 and I949 (' sometimes all right, sometimes all wrong '), but was not radiographed again until June 28, 195o. Report stated that an ulcer was still present, and larger than previously. (Films show a flat ulcer at the incisura angularis.) Further radiological examination on July 26 showed a flat ulcer just beyond the incisura angularis, with mucosal convergence towards it and shortening of the lesser curve. At gastroscopy the following month, a diagnosis of carcinoma was made and ' t w i n ulcers' were reported. Gastrectomy was performed Sept. 6. T h e specimen showed an ulcer 3 × I'8 cm. with slightly raised edge, shelving in some areas--vertical in others. Histologically, three pieces were reported as showing carcinoma with extensive peptic ulceration, and one piece as stomach showing chronic peptic ulcer, but no growth. Comment.--This was a case of a c a r c i n o m a t o u s ulcer, associated w i t h a p r o x i m a l b e n i g n ulcer. T h e o r i g i n a l ulcer r e p o r t e d was p r o b a b l y neoplastic. O n o n e of t h e l a t e r b a r i u m meals, a m o r e p r o x i m a l u l c e r was d e m o n s t r a t e d , w h i c h was p r o b a b l y t h e s i m p l e ulcer, t h e o r i g i n a l m a l i g n a n t lesion n o t b e i n g s h o w n o n t h a t occasion.
Case Io.--E. W. Female. Born 1892. First attended the London Hospital Oct. 18, 1952, complaining of many years' epigastric fullness 1½-2 hours after food, associated with belchFig. i98.--SmaU conical crater later proved to be ing--powders being reasonably effective. Diagnosed as malignant, carcinoma of the stomach, but there was passage of blood per rectum, and the colon was first investigated to exclude neoplasm here. Following sigmoidoscopy, a 4-cm. diameter carcinomatous ulcer at the pelvi-rectal junction was excised on Nov. 12. One m o n t h later the patient complained of pain after food, not relieved by powders and associated with nausea and vomiting. Gastroscopy, Dec. 23, suggested that there was a simple gastric ulcer. A barium meal, Dec. 24, reported a flat gastric ulcer at the incisura angularis with a suggestion of mucosal convergence--probably simple ulcer. T h e barium meal was repeated Feb. 4, 1953. T h e report stated that the flat gastric ulcer was a little smaller. There was still convergence of the folds, and it was thought to be a simple ulcer. (Review of the films shows a flat ulcer with an irregular margin and folds running to the rim of the ulcer.) Partial gastrectomy was performed on Feb. 18, 1953, and a specimen showed a typical carcinomatous ulcer infiltrating all coats of the stomach. Comment.--Carcinoma p r e s e n t i n g as a flat u l c e r at t h e i n c i s u r a angularis, d i a g n o s e d as s i m p l e , b e c a u s e of t h e p r e s e n c e of c o n v e r g i n g m u c o s a l folds.
DISCUSSION T h e n e o p l a s t i c ulcers w e r e classifiable i n t o two g r o u p s d e p e n d i n g u p o n t h e s h a p e of t h e lesion o n t h e r a d i o g r a p h s . T h e first g r o u p (~5 cases) s h o w e d a flat, shallow, a n d in s o m e cases s a u c e r - l i k e p r o j e c t i o n f r o m t h e lesser c u r v a t u r e b l e n d i n g s m o o t h l y w i t h t h e s t o m a c h o u t l i n e . (Cases I, 2, 3, 6, a n d io.) T h e s e c o n d g r o u p (8 cases) s h o w e d a n u l c e r usually conical in shape, p r o j e c t i n g f u r t h e r f r o m t h e s t o m a c h o u t l i n e t h a n t h e flat variety, t h e c r a t e r b e i n g m u c h g r e a t e r in d e p t h t h a n in t r a n s v e r s e d i a m e t e r . (Cases 4, 5, 7, a n d 8.) T h i s g r o u p gave a l o n g e r h i s t o r y t h a n t h e first, a n d t h e average delay f r o m t h e first b a r i u m m e a l to g a s t r e c t o m y was n e a r l y twice as long, b e i n g 20 m o n t h s
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as compared with i i months. From analysis of this series, it appears that the radiological problem is also different in the two varieties. In the first group the main difficulty is to demonstrate the lesion in the early stages, and of the 13 cases which showed evidence of ulceration on the original films, 9 were not recognized at first examination. In the second variety, the problem was entirely
A Fig. I 9 9 . - - S m a l l conical crater (A).
B B shows the malignant ulcer a m o n t h before gastrectomy.
Fig. 2 o o . - - L e s s e r curve shortening due to an ulcer (measuring i o × 5 cm.) in a scirrhous carcinoma which was not demonstrated radiologically.
one of interpretation, and 6 out of the 8 cases were originally diagnosed as benign. This diagnosis was changed subsequently to one of malignancy in 2 cases when a filling defect was demonstrated in association with the ulcer, but in the remaining 4 cases no radiological diagnosis of malignancy was ever made. Examination of radiographs of these revealed no features which could distinguish them from benign lesions, and an exact diagnosis was not possible on the appearance of the ulcer crater. T h e very long history and repeated radiographic examinations in this group (e.g., Cases 7 and 8) suggest that some of them could be instances of malignant change in a benign ulcer, and two were diagnosed as such by the pathologist. It is of interest that these were the only two cases in the whole series which diminished in size whilst under surveillance. I5
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The problem of interpretation in the flat variety was not so difficult. Some of this group presented characteristic features of malignancy fairly early in their evolution. This type of ulcer corresponds to that described by Gutmann, Bertrand, and Peristiany (i939) as ' Niche en Plateau ' or ' Niche en Plateau Encastr4e '. There is a flat shallow ulcer crater with an irregular serrated margin and a surrounding meniscus. The base of the crater may be slightly irregular and it is often possible to demonstrate converging mucosal folds advancing either as far as the edge of the crater or just short of it. The ulcer may, or may not, be intraluminal and depending on this it may be designated ' en plateau ' or ' en plateau encastr4e '. We do not consider that too sharp a distinction can be drawn between these two types, since the plateau ulcer may become an embedded ulcer (niche en plateau encastr4e) by simple evolution of the lesion depending upon the emergence of a shallow filling defect in association with the crater. Good compression films are usually essential to display all the features of this type of lesion, and well penetrated films are often necessary especially in areas inaccessible to compression. Fig. i94 B is the best example in this series. Thus the evidence from this series suggests that malignant lesions of this t y p e may present either as small projecting ulcers, usually conical in shape, which closely simulate a benign lesion, or as small flat ulcers which are often difficult to demonstrate but which may present characteristic features of malignant ulceration fairly early in their evolution. I n both types, the ulcer at its earliest will show only as a projection from the line of the lesser curvature, but as the lesion progresses it becomes an ulcer within a filling defect. Ulceration of both types at or about the incisura angularis often produced lesser curve shortening, recognized by failure to demonstrate a normal incisura. The resultant deformity of the stomach was the only abnormality demonstrated pre-operatively in two cases. In this type of shortening, the duodenal cap and pylorus tend to assume a horizontal position, and the cap is not approximated to the lesser curve of the body of the stomach. The incisura angularis is obliterated and there is usualtv an incisura of the great curve side of the pyloric antrum. T h e appearances are similar to a type of deformity described bv Ilinds and Kemp Harper (195a), ~hich they ascribe to contraction of part of the gastro-hepatic o m e n t u m ; Figs, i95 A, B, and 200 are examples. Although this appearance is not always associated with malignancy, our experience in this series has shown that its incidence is sufficiently high to warrant the consideration of malignancy and to suggest ti~e desirability of gastroscopy in an endeavour to exclude neoplasm. T h e ulcer may be very difficult to show as the stomach deformity often makes the area of ulceration inaccessible to compression, especially when a full amount of barium is used. W h e n an ulcer crater is not demonstrated, the common error is to attribute the deformity to a healed or healing benign ulcer. Meuwissen (I955) describes a typical instance of this. However, by use of a small quantity of barium, it should always be possible to display the crater, and we believe that all cases of unexplained lesser curve shortening of this type should be examined by this method. An important observation was the finding of benign ulceration in association with, but discrete from, a malignant neoplasm of the stomach (e.g., Case 9). Three instances of this association were demonstrated. In two the neoplasm was a carcinoma, and in the other it was diagnosed histologically as a lymphosarcoma. In each instance the benign gastric ulcer was located proximal to the site of the neoplasm on the lesser curve. It it obvious that this type of case can be a major diagnostic pitfall, if the association is not borne in mind, and it led to error in diagnosis in all three cases, the proximal benign ulcer being recognized and the neoplasm overlooked. T h e series was reviewed to assess the value of the classical radiological criteria of malignant gastric ulceration when applied to the early lesion. The earliest films of all the twenty-one cases which showed undoubted evidence of ulceration on their original radiographs were examined for the following features : 2. Presence of an intraluminal meniscus.
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z. Position of the ulcer crater with respect to the stomach lumen, i.e., whether the crater was intraluminal or extraluminal. 3. Irregularity of shape of the ulcer. 4. Size of the ulcer crater. An intraluminal meniscus was the sign most often present and was noted in 8 cases, all of which were flat or plateau ulcers. There is no doubt that in this variety of early malignant lesion it is a most important sign and probably could have been demonstrated in more cases had better compression films been obtained. However, in the conical ulcers it was never present on the original films and appears at a comparatively late stage in their development. It is therefore only of limited value in establishing a diagnosis in the early lesion, and its absence gives no assurance that an ulcer is benign. Only 5 ulcers could be considered intraluminal in position on the earliest radiographs and in only 6 cases was there any irregularity of the crater outline. As for the size of the crater, it was found that in only 3 cases was the diameter greater than z½ cm., this being the measurement above which an ulcer should be considered suspicious of malignancy ; see Text-Book of X-ray Diagnosis by Shanks, Kerley, and Twining (I95o), Obviously measurement of the size of the crater is of little value in the early lesion when it is bound to be small, and this criterion could not be considered strictly applicable to the series. Initially 12 of the 21 cases showed none of the features listed above, and whilst the validity of these signs is unquestioned in the later stages of malignant ulceration, it is concluded that they are of very limited help in the diagnosis when the ulcers are small and at an early stage in their development. As indicated the only sign which can be regarded as important is the intraluminal meniscus since it may accompany the small plateau ulcer. A variety of factors contributed to the delay in the diagnosis of these cases. The method of their selection necessarily included all possible causes of diagnostic delay, whether clinical, radiological or otherwise. Consideration of all these is beyond the scope of the present investigation, however, and we have concerned ourselves only with the main radiological causes apparent in the series. These ~\ere 5 in number, and can bc summarized as follows : I. Failure to detect the earl)" flat malignant ulcer. As atreadv mentioned, the main radiologica[ difficulty h~ the plateau ulcer was to demonstrate the lesion in its early stages. These ulcers, ~hela small, are easitv mistaken for a normal peristaltic wave, or rugal fold. (~'ee Fig. *94 A.) Nevertheless, a greater awareness of the significance of such an appearance, and the not too ready acceptance of a simple explanation for its presence, should lead to the early discovery of more of these lesions. 2. Difficulty in differentiating the conical shaped malignant ulcer from a benign lesion. We have already shown that the early conical shaped malignant ulcers are often impossible to distinguish from a benign ulcer on their appearances alone. A tentative diagnosis is only possible by consideration of the behaviour of the lesion under medical treatment and some delay in the radiological diagnosis can therefore hardly be avoided. 3 . Failure to recognize the characteristic features of malignant ulceration, i.e., ' niche en plateau encastr4e ' 4. Failure to detect a malignant lesion when associated with a proximal benign ulcer. 5. The repeated assumption on the film reports of this series, that an ulcer was benign because of the presence of converging mucosal folds to the crater. This sign is often quoted as evidence of benign ulceration, and in a recent publication Kirsh (I955) has re-emphasized its value. I n the present series, however, it was possible to demonstrate converging rugae in over a third of the cases and often the ulcer was reported as benign because of this. In some cases (Fig. i94 g) the folds stopped short of the ulcer margin, presumably due to a surrounding zone of infiltration, but in others (Fig. *95 A) they reached to the edge of the crater
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without interruption and it was these cases which were labelled benign. The sign can therefore be very misleading and should not be relied upon to differentiate the benign and the malignant ulcer. We wish to thank Dr. M. H. Jupe, the Director of the Radiodiagnostic Department of the London Hospital, for permission to publish these cases and for his most helpful advice on the preparation of the paper. We also gratefully acknowledge the help given to us by Dr. R. S. Murray and Dr. Charles Maclean, and we are indebted to Professor Dorothy Russell for allowing us access to the records of the Bernhard Baron Institute of Pathology. REFERENCE S GUTMANN, R. A., BERTRAND, I., and PERISTIANY, T. J. (I939), Le Cancer de L'estomac au Debut. Paris : Doin. HINDS, S. J., and KEMPHARPER,R. A. (I95e), ]?rlt. 7. Radiol., 25, 297. KIRSH, ISRAELE. (t955), Radiology, 64, 357MEUWlSSEN,T. J. J. H. (I955), X - r a y Atlas and Manual of G~.sophagus, Stomach and Duodenum. Amsterdam : Elsevier. RUSSELL,W. A., WEINTRAUB,S., and TEMPLE,H. (I948), Radiology, 5I, 79o. SHANKS, S. C., KEKLEY, P., and TWINING,E. W. (I950), A Text-book of X - r a y Diagnosis, 3, 145.
lrmoriam LORD HORDER OF ASHFORD, G.C.V.O., M.D., D.C.L., F.R.C.P. LONG and eloquent tributes have been paid to Lord Horder in both the lay and medical press. We cannot effectively add to these, but merely show our respect and appreciation for all he did for Radiology. Lord Horder was an Honorary Fellow of the Faculty of Radiologists. He often took part in our early discussions and meetings and he supported our activities until his death. His knowledge of cancer, his interest in ' follow-up ', and his association with the British Empire Cancer Campaign perhaps brought him closer to Radiotherapy than to Radiodiagnosis, but we shall all miss him. We shall miss his criticism, his advice, his help, and his ready support in our development as a specialty.
THOMAS DIGBY WHEELER, M.A., M.D., F.F.R., F.A.C.R., F.R.C.P. (C.), F.I.C.S. DR. DIGBY WHEELERdied September 20, 1955, at the age of 63. He received his medical training at the University of Manitoba and on graduation enlisted in the Canadian Army Medical Corps, serving overseas in the first world war with the rank of Captain. Returning to Canada, he practised at Winnipeg, Manitoba, and taught anatomy in the University of Manitoba. In I932 he began the practice of radiology and held appointments in Radiology at several Winnipeg hospitals. He was appointed Professor of Radiology at the University of Manitoba, and on retirement was made Professor Emeritus. Dr. Wheeler was a past President of the Canadian Association of Radiologists and of the Manitoba Medical Society. During the second world war he was consultant in radiology to the Canadian Armed Forces in Military District No. io. His interests were wide and his aid and counsel were sought by governmental, civic, and medical bodies. For the past two years he was President of the Winnipeg Symphony Orchestra, on the Board of which he had served since i948.
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A REVIEW OF 26 C A S E S IN W H I C H T H E R E W A S D E L A Y IN T H E D I A G N O S I S BY G. A. S. LLOYD, B.M., B.Ch., D.M.R.D., AND J. L. MORRIS, M.B., B.Ch., D.M.R.D. FROM THE RADIODIAGNOSTI C DEPARTMENT OF THE LONDON HOSPITAL, WHITECHAPEL
INTRODUCTION GASTRIC neoplasms commonly present at barium meal examinations as ulcerative lesions. T h e earliest changes which occur d e m a n d a high standard of radiological technique for their demonstration and the problem of interpretation at this stage may be very difficult, especially with ulcers situated on the lesser curvature, since they have to be differentiated from benign lesions. I n this paper we have selected for investigation a series of neoplastic ulcers in which there was serious delay before a correct diagnosis was reached. T h e majority of these had presented a considerable diagnostic p r o b l e m to the radiologist and all had been examined more than once. I t was thus possible to review the original radiographs and those of later examinations in sequence, together with the radiological reports made at the time. Using this method, our principal objects have been to in~vestigate the earliest changes which occur in these neoplasms and to study their subsequent development ; also to show how far the classical criteria of malignant gastric ulceration are applicable in the early stages, a n d to determine the major causes of diagnostic delay when these have been radiological in origin.
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Examination of the records of the Bernhard Baron Institute of Pathology of the London Hospital revealed a diagnosis of gastric carcinoma in 254 cases from post-gastrectomy specimens in the years I949-53 inclusive. Of these there were 23 cases of carcinomatous ulcer, whose radiographs were available for study, and which fulfilled the following criteria : - - ( i ) T h e r e was evidence of ulceration of the body, cardia, or pyloric antrum, excluding the pre-pyloric area. F o r the purposes of anatomical localization we have used the terminology proposed by Russell, Weintraub, and T e m p l e (i948). (2) T h e r e was a delay of more than two months from the time of the first b a r i u m meal examination to gastrectomy. T h r e e other cases were added to the original 23. One of these was a case of sarcoma of the stomach diagnosed after gastrectomy, and 2 were carcinomata of the stomach, in which the diagnosis was made by a combination of gastroscopy and biopsy, and gastroscopy and peritoneoscopy.
CASE
REPORTS
T e n illustrative case summaries are appended. Brief clinical, gastroscopic, and pathological details are included, but the main attention is focused on the radiograph reports at the time of examination. W h e r e necessary, the anatomical terms in the actual reports have been altered to preserve the uniformity of terminology. A short comment is given after each case. Case I.--C. B. Female. Born 1886. Presented Oct. 28, 1952, and diagnosed clinically as a functional dyspepsia, possibly gastric ulcer. First barium meal, Nov. 14, I95Z, reported an irregularity of the pyloric antrum, possibly due to spasm. No ulcer reported. (Films show flat projection at the incisura angularis and shortening of the lesser curvature, Fig. 192 A.) Attended again May z6, 1953, complaining of diarrhoea and the clinical diagnosis of ' colonic dysfunction ' was made. A second barium meal was not performed until Nov. 18, 1953. This showed a ' saddleback ' ulcer at the incisura angularis, associated with a filling defect, and the diagnosis of carcinoma was made (Fig. 192 B). Gastrectomy was performed Nov. 27, and the specimen showed a carcinomatous ulcer 2 cm. in diameter with rolled edges. C o m m e n t . - - C a r c i n o m a presenting as a flat ulcer with lesser curve shortening.
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Case z . - - H . R. Male. B o r n I893. P r e s e n t e d Nov. i3, x95o, with a t w o - m o n t h history of epigastric pain lasting the whole day, a n d n o t relieved by p o w d e r or food. T h e r e was also anorexia a n d wasting. T h e clinical diagnosis was c a r c i n o m a of t h e stomach. A barium meal at this time, N o v . I4, z95o (Fig. ~93), was reported as
B A Fig. I92.--The original film (A) shows a flat projection at the incisura angularis which eventually became an ulcer within a large filling defect (B).
s h o w i n g a flat projection on the lesser c u r v e of t h e b o d y and diagnosis of chronic gastric ulcer was m a d e . A t a second barium meal on M a y 29, I95I, t h e ulcer was reported as being smaller, signifying healing. (Review of these films s h o w s a flat ulcer with a s u r r o u n d i n g half shadow, almost certainly a filling defect.) S u b s e q u e n t l y the patient i m p r o v e d s y m p t o m a t i c a l l y for eight m o n t h s , a n d t h e r e was an increase in weight of I5 lb., b u t his condition deteriorated in t h e following two m o n t h s . T h e r e was no pain, b u t he felt poorly a n d was pale. N e o p l a s m of t h e s t o m a c h was again s u g g e s t e d clinically. Barium meal at this time s h o w e d an extensive n e o p l a s m of the whole of the lesser curve, and t h e r e was a palpable l u m p . Peritoneoscopy Jan. 9, I952, s h o w e d a gastric m a s s with s e c o n d a r y deposits in the liver. T w o m o n t h s later t h e ulcer perforated a n d t h e patient died. " Comment.--Carcinoma presenting d i a g n o s e d as c h r o n i c g a s t r i c u l c e r .
Fig. I93.--Flat carcinomatous ulcer on the lesser curvature of the body of the stomach.
a s a flat u l c e r ,
mis-
Case 3 . - - F . S. Male. B o r n i898. P r e s e n t e d in F e b r u a r y , I95I, w i t h six m o n t h s ' history of epigastric pain two h o u r s after food, poor appetite, a n d weight loss. Clinical diagnosis d u o d e n a l ulcer, possibly n e o p l a s m . A barium meal, Feb. I5, was reported as n o a b n o r m a l i t y detected. (Films s h o w a very small, flat projection on t h e lesser curve at t h e incisura angularis.) (Fig. I94 A.) Clinically regarded as a d u o d e n a l ulcer a n d treated as such. A second barium meal I3 months later, M a r c h 6,
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1952, reported as showing a fiat ulcer distal to the incisura angularis, with convergent folds and diagnosed as neoplasm. (The films show, in addition, an incisura of the greater curve side of the pyloric antrum.) (Fig. 194 B.) T h e diagnosis was confirmed by gastroscopy and biopsy. Comment.--Carcinoma p r e s e n t i n g as a s m a l l flat ulcer at t h e i n e i s u r a a n g u l a r i s , n o t r e c o g n i z e d at first e x a m i n a t i o n , clinically t r e a t e d as a d u o d e n a l ulcer. T h e final b a r i u m m e a l d e m o n s t r a t e d a typical m a l i g n a n t ulcer.
A
B
Fig. I 9 4 . - - S m a l l plateau ulcer at the incisura angularis (A) which eventually showed features considered characteristic of a malignant ulcer (B).
A
B
Fig. 195.--Carcinomatous ulcer simulating a benign lesion with converging mucosal folds and lesser curve shortening of the type described in the text (A).
B shows the appearance 15 months later immediately prior to gastrectomy.
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Case 4 . - - E . R. Female. Born 1899. First a t t e n d e d t h e L o n d o n Hospital Oct. 3 o, 1948 with history of thirty years' i n d i g e s t i o n a n d acid eructation, a n d pain in the left side for four m o n t h s . Clinical diagnosis of duodenal ulcer. Barium meal at this time, Nov. 25, a large gastric ulcer was reported low d o w n on t h e lesser curve of t h e body of t h e stomach. (Films s h o w a large gastric ulcer with c o n v e r g e n t folds, s h o r t e n i n g of t h e lesser curve a n d an incisura of the greater curve of t h e pyloric a n t r u m , Fig. I95 A.) She h a d no pain for t h e following thirteen m o n t h s , a l t h o u g h her weight d u r i n g this time d r o p p e d b y 5 lb. I n D e c e m b e r , 1949, s h e b e g a n to g e t pain again, a n d at the second barium meal, March i, 195o, t h e report stated that there was lesser curve s h o r t e n i n g a n d excess resting secretion b u t no ulcer was d e m o n s t r a t e d . ( T h e films s h o w t h a t the s h o r t e n i n g h a d increased, and there was m o r e m a r k e d deformity of the pyloric a n t r u m , Fig. 195 B.) T h e r e h a d been a drop of a stone in weight in t h e previous three m o n t h s . G a s t r e c t o m y was p e r f o r m e d on M a r c h 17, a n d a s p e c i m e n s h o w e d a shallow ulcer 7 × 4 cm. in t h e m i d d l e of t h e lesser curve, histologically a carcinoma. Comment.--Carcinoma p r e s e n t i n g as a c o n i c a l ulcer with gross antral deformity, and shortening of t h e l e s s e r c u r v e , d i a g n o s e d as a b e n i g n g a s t r i c u l c e r .
Fig. z96.--Conical malignant ulcer at the incisura angularis with mneosal convergence,
Case 5 . - - G . M. Male. Born 19o6. A t t e n d e d the L o n d o n Hospital in D e c e m b e r , 1952, c o m p l a i n i n g of 6 to 7 weeks' belching and epigastric pain. Clinically t h o u g h t to be a peptic ulcer r a t h e r t h a n a n e o p l a s m . Barium meal at this time, Dec. 3 i, reported a gastric ulcer at t h e incisura angularis, with c o n v e r g e n t folds (Fig. 196). D i a g n o s e d as b e n i g n gastric ulcer. T h e r e was loss of weight d u r i n g the following four m o n t h s , a n d a second barium meal, March io, 1953, reported no change. S u b s e q u e n t l y t h e r e was s o m e i m p r o v e m e n t in the clinical condition a n d a f u r t h e r barium meal, April 21, again reported no change. G a s t r e c t o m y was p e r f o r m e d two weeks later a n d an ulcer 2 cm. in diameter, w i t h shelving edges a n d s u r r o u n d i n g thickening, was found. It was t h o u g h t to be simple macroscopically. Histologically this was a diffuse scirrhous carcinoma.
Comment,--Carcinoma p r e s e n t i n g as a c o n i c a l u l c e r at t h e i n c i s u r a a n g u l a r i s w i t h m u c o s a l c o n v e r g e n c e , d i a g n o s e d as b e n i g n g a s t r i c u l c e r .
Case 6 . - - J . G. Male. Born 1895. First seen at the L o n d o n Hospital Jan. 23, 195o, c o m p l a i n i n g of u p p e r a b d o m i n a l fullness and s h o r t n e s s of b r e a t h for a year. Pain was colicky a n d h e h a d p a s s e d blood per r e c t u m one m o n t h previously. Clinical diagnosis was n e o p l a s m of the colon. B a r i u m e n e m a at this time ' no a b n o r m a l i t y detected '. Seen again July 29, 1952, c o m p l a i n i n g of dyspepsia for two years. Barium meal at this time, Aug. 7, reported as ' n o a b n o r m a l i t y d e t e c t e d ' . (Films s h o w a small flat ulcer on t h e lesser curve of t h e body of t h e stomach, Fig. 197 A.) T h e patient was seen in A u g u s t , 1953, a n d a second barium meal, Sept. i, reported an encastrd defect h i g h on t h e lesser curve, diagnosed as c a r c i n o m a (Fig. 197 B). G a s t r e c t o m y was p e r f o r m e d four weeks later a n d showed an ulcerated i n t r a l u m i n a l carcinoma j u s t below t h e cardia. Histologically this was a well-differentiated carcinoma. Comment.--Carcinoma at first examination.
p r e s e n t i n g as a flat u l c e r o n t h e l e s s e r c u r v e o f t h e b o d y , n o t r e c o g n i z e d
Case 7 . - - M . P. Female. Born 1894. A t t e n d e d Aug. i, 1947, c o m p l a i n i n g of epigastric pain for eighteen m o n t h s . Barium meal, Oct. 8, reported a conical gastric ulcer on t h e lesser curve of t h e b o d y (Fig. 198). T h e barium meal was repeated two months later, Dec. 1. A gastric ulcer with c o n v e r g e n t folds was repoiTted. T h e appearances were considered to be ' odd '. (Films s h o w an irregular r e c t a n g u l a r ulcer ; the incisura on the greater curve was still present.) _//.third barium meal, Feb. 1948, was reported as s h o w i n g a gastric ulcer. (Films s h o w little change f r o m t h e previous b a r i u m meal.) D u r i n g t h e following three and a half years, no b a r i u m meals were performed, b u t the patient was gastroscoped on f o u r occasions. At first the lesion
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was t h o u g h t to be p o s s i b l y neoplastic, b u t a diagnosis of a b e n i g n lesion was later made, as the ulcer appeared to be healing. It was never reported as healed. A fourth barium meal, July 6, I95I, s h o w e d gross irregularity a n d d e f o r m i t y of the greater curve of t h e lower part of t h e body, a n d d e f o r m i t y of the lesser curve at t h e site of previous ulceration. G a s t r e c t o m y was p e r f o r m e d six weeks later. S p e c i m e n showed a large ulcerated m a s s
A
B
Fig. i97.--Small plateau ulcer (A) which became a plateau ulcer within a shallow filling defect (nicheenplateau encastrde)(g). astride t h e greater curve, histologically an anaplastic carcinoma. b e n i g n ulcer.
Pathological diagnosis was c a r c i n o m a in a
Comment.--Carcinoma p r e s e n t i n g as a c o n i c a l u l c e r w i t h g r e a t e r c u r v e i n c i s u r a , d i a g n o s e d as s i m p l e g a s t r i c u l c e r . The ulcer did not heal for nearly four years.
Case 8 . - - H . S. Male. B o r n I89o. First attended t h e L o n d o n Hospital in i 9 3 8 - - n o notes are available. D o u b t f u l d u o d e n a l ulcer, diagnosed at b a r i u m meal. A t t e n d e d again Feb. 5, I947, with a ten-year history of periodic epigastric pain one h o u r after food, lately associated with acid reflux. Barium meal, Feb. i I , gastric ulcer reported on the lesser curve of t h e u p p e r t h i r d of t h e body of t h e stomach. (Films show a conical ulcer crater, Fig. 199 A.) Barium meal was repeated July zz. T h e ulcer was reported as being still present, b u t shallower. A third barium meal, Nov. 4, was reporte:l as ' n o a b n o r m a l i t y d e t e c t e d ' . (Films are rather poor, b u t s h o w w h a t appears to be a conical ulcer on the lesser curve of the body.) A fourth barium meal, Dec. 5, I949, reported a h i g h gastric ulcer, larger t h a n previously, p r o b a b l y benign. ( T h e films show a large ulcer e n c r o a c h i n g u p o n the l u m e n of t h e stomach, Fig. I99 B.) O n C h r i s t m a s D a y of t h a t year, he was feeling as well as at any t i m e in the past eighteen m o n t h s , b u t after d i n n e r h a d a severe h~ematemesis. H e was a d m i t t e d a n d a g a s t r e c t o m y was p e r f o r m e d , Jan. 6, 195o. S p e c i m e n s h o w e d a 3 cm. diameter ulcer on t h e lesser curve of the b o d y of t h e stomach, histologically a carcinoma. Comment.--Carcinoma presenting H ~ e m a t e m e s i s l e d to g a s t r e c t o m y .
as a c o n i c a l u l c e r o n l e s s e r c u r v e , d i a g n o s e d
as s i m p l e .
Case 9 . - - E . E. Male. B o r n I884. First attended Jan. 7, *943 -with glycosuria a n d treated as a diabetic. A t t e n d e d s u b s e q u e n t l y in I947 a n d gave a history of attacks o f epigastric p a i n half an h o u r after food in I933,
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and further attacks in 1942. He was well in between the attacks and up until June, 1947, when the pain recurred. Barium meal, Nov. I i, I947, reported a medium-sized flat gastric ulcer just above the incisura angularis. (Films show a fiat ulcer on the lesser curve of the body.) Barium meal was repeated, April 9, 1948. An ulcer was shown only in the prone position, and reported to be healing. A third barium meal, Sept. 14, reported a small niche which was tender. (Fihns show a small niche a short way above the incisura angularis, apparently higher than the previous ulcer.) Attended during 1948 and I949 (' sometimes all right, sometimes all wrong '), but was not radiographed again until June 28, 195o. Report stated that an ulcer was still present, and larger than previously. (Films show a flat ulcer at the incisura angularis.) Further radiological examination on July 26 showed a flat ulcer just beyond the incisura angularis, with mucosal convergence towards it and shortening of the lesser curve. At gastroscopy the following month, a diagnosis of carcinoma was made and ' t w i n ulcers' were reported. Gastrectomy was performed Sept. 6. T h e specimen showed an ulcer 3 × I'8 cm. with slightly raised edge, shelving in some areas--vertical in others. Histologically, three pieces were reported as showing carcinoma with extensive peptic ulceration, and one piece as stomach showing chronic peptic ulcer, but no growth. Comment.--This was a case of a c a r c i n o m a t o u s ulcer, associated w i t h a p r o x i m a l b e n i g n ulcer. T h e o r i g i n a l ulcer r e p o r t e d was p r o b a b l y neoplastic. O n o n e of t h e l a t e r b a r i u m meals, a m o r e p r o x i m a l u l c e r was d e m o n s t r a t e d , w h i c h was p r o b a b l y t h e s i m p l e ulcer, t h e o r i g i n a l m a l i g n a n t lesion n o t b e i n g s h o w n o n t h a t occasion.
Case Io.--E. W. Female. Born 1892. First attended the London Hospital Oct. 18, 1952, complaining of many years' epigastric fullness 1½-2 hours after food, associated with belchFig. i98.--SmaU conical crater later proved to be ing--powders being reasonably effective. Diagnosed as malignant, carcinoma of the stomach, but there was passage of blood per rectum, and the colon was first investigated to exclude neoplasm here. Following sigmoidoscopy, a 4-cm. diameter carcinomatous ulcer at the pelvi-rectal junction was excised on Nov. 12. One m o n t h later the patient complained of pain after food, not relieved by powders and associated with nausea and vomiting. Gastroscopy, Dec. 23, suggested that there was a simple gastric ulcer. A barium meal, Dec. 24, reported a flat gastric ulcer at the incisura angularis with a suggestion of mucosal convergence--probably simple ulcer. T h e barium meal was repeated Feb. 4, 1953. T h e report stated that the flat gastric ulcer was a little smaller. There was still convergence of the folds, and it was thought to be a simple ulcer. (Review of the films shows a flat ulcer with an irregular margin and folds running to the rim of the ulcer.) Partial gastrectomy was performed on Feb. 18, 1953, and a specimen showed a typical carcinomatous ulcer infiltrating all coats of the stomach. Comment.--Carcinoma p r e s e n t i n g as a flat u l c e r at t h e i n c i s u r a angularis, d i a g n o s e d as s i m p l e , b e c a u s e of t h e p r e s e n c e of c o n v e r g i n g m u c o s a l folds.
DISCUSSION T h e n e o p l a s t i c ulcers w e r e classifiable i n t o two g r o u p s d e p e n d i n g u p o n t h e s h a p e of t h e lesion o n t h e r a d i o g r a p h s . T h e first g r o u p (~5 cases) s h o w e d a flat, shallow, a n d in s o m e cases s a u c e r - l i k e p r o j e c t i o n f r o m t h e lesser c u r v a t u r e b l e n d i n g s m o o t h l y w i t h t h e s t o m a c h o u t l i n e . (Cases I, 2, 3, 6, a n d io.) T h e s e c o n d g r o u p (8 cases) s h o w e d a n u l c e r usually conical in shape, p r o j e c t i n g f u r t h e r f r o m t h e s t o m a c h o u t l i n e t h a n t h e flat variety, t h e c r a t e r b e i n g m u c h g r e a t e r in d e p t h t h a n in t r a n s v e r s e d i a m e t e r . (Cases 4, 5, 7, a n d 8.) T h i s g r o u p gave a l o n g e r h i s t o r y t h a n t h e first, a n d t h e average delay f r o m t h e first b a r i u m m e a l to g a s t r e c t o m y was n e a r l y twice as long, b e i n g 20 m o n t h s
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as compared with i i months. From analysis of this series, it appears that the radiological problem is also different in the two varieties. In the first group the main difficulty is to demonstrate the lesion in the early stages, and of the 13 cases which showed evidence of ulceration on the original films, 9 were not recognized at first examination. In the second variety, the problem was entirely
A Fig. I 9 9 . - - S m a l l conical crater (A).
B B shows the malignant ulcer a m o n t h before gastrectomy.
Fig. 2 o o . - - L e s s e r curve shortening due to an ulcer (measuring i o × 5 cm.) in a scirrhous carcinoma which was not demonstrated radiologically.
one of interpretation, and 6 out of the 8 cases were originally diagnosed as benign. This diagnosis was changed subsequently to one of malignancy in 2 cases when a filling defect was demonstrated in association with the ulcer, but in the remaining 4 cases no radiological diagnosis of malignancy was ever made. Examination of radiographs of these revealed no features which could distinguish them from benign lesions, and an exact diagnosis was not possible on the appearance of the ulcer crater. T h e very long history and repeated radiographic examinations in this group (e.g., Cases 7 and 8) suggest that some of them could be instances of malignant change in a benign ulcer, and two were diagnosed as such by the pathologist. It is of interest that these were the only two cases in the whole series which diminished in size whilst under surveillance. I5
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The problem of interpretation in the flat variety was not so difficult. Some of this group presented characteristic features of malignancy fairly early in their evolution. This type of ulcer corresponds to that described by Gutmann, Bertrand, and Peristiany (i939) as ' Niche en Plateau ' or ' Niche en Plateau Encastr4e '. There is a flat shallow ulcer crater with an irregular serrated margin and a surrounding meniscus. The base of the crater may be slightly irregular and it is often possible to demonstrate converging mucosal folds advancing either as far as the edge of the crater or just short of it. The ulcer may, or may not, be intraluminal and depending on this it may be designated ' en plateau ' or ' en plateau encastr4e '. We do not consider that too sharp a distinction can be drawn between these two types, since the plateau ulcer may become an embedded ulcer (niche en plateau encastr4e) by simple evolution of the lesion depending upon the emergence of a shallow filling defect in association with the crater. Good compression films are usually essential to display all the features of this type of lesion, and well penetrated films are often necessary especially in areas inaccessible to compression. Fig. i94 B is the best example in this series. Thus the evidence from this series suggests that malignant lesions of this t y p e may present either as small projecting ulcers, usually conical in shape, which closely simulate a benign lesion, or as small flat ulcers which are often difficult to demonstrate but which may present characteristic features of malignant ulceration fairly early in their evolution. I n both types, the ulcer at its earliest will show only as a projection from the line of the lesser curvature, but as the lesion progresses it becomes an ulcer within a filling defect. Ulceration of both types at or about the incisura angularis often produced lesser curve shortening, recognized by failure to demonstrate a normal incisura. The resultant deformity of the stomach was the only abnormality demonstrated pre-operatively in two cases. In this type of shortening, the duodenal cap and pylorus tend to assume a horizontal position, and the cap is not approximated to the lesser curve of the body of the stomach. The incisura angularis is obliterated and there is usualtv an incisura of the great curve side of the pyloric antrum. T h e appearances are similar to a type of deformity described bv Ilinds and Kemp Harper (195a), ~hich they ascribe to contraction of part of the gastro-hepatic o m e n t u m ; Figs, i95 A, B, and 200 are examples. Although this appearance is not always associated with malignancy, our experience in this series has shown that its incidence is sufficiently high to warrant the consideration of malignancy and to suggest ti~e desirability of gastroscopy in an endeavour to exclude neoplasm. T h e ulcer may be very difficult to show as the stomach deformity often makes the area of ulceration inaccessible to compression, especially when a full amount of barium is used. W h e n an ulcer crater is not demonstrated, the common error is to attribute the deformity to a healed or healing benign ulcer. Meuwissen (I955) describes a typical instance of this. However, by use of a small quantity of barium, it should always be possible to display the crater, and we believe that all cases of unexplained lesser curve shortening of this type should be examined by this method. An important observation was the finding of benign ulceration in association with, but discrete from, a malignant neoplasm of the stomach (e.g., Case 9). Three instances of this association were demonstrated. In two the neoplasm was a carcinoma, and in the other it was diagnosed histologically as a lymphosarcoma. In each instance the benign gastric ulcer was located proximal to the site of the neoplasm on the lesser curve. It it obvious that this type of case can be a major diagnostic pitfall, if the association is not borne in mind, and it led to error in diagnosis in all three cases, the proximal benign ulcer being recognized and the neoplasm overlooked. T h e series was reviewed to assess the value of the classical radiological criteria of malignant gastric ulceration when applied to the early lesion. The earliest films of all the twenty-one cases which showed undoubted evidence of ulceration on their original radiographs were examined for the following features : 2. Presence of an intraluminal meniscus.
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z. Position of the ulcer crater with respect to the stomach lumen, i.e., whether the crater was intraluminal or extraluminal. 3. Irregularity of shape of the ulcer. 4. Size of the ulcer crater. An intraluminal meniscus was the sign most often present and was noted in 8 cases, all of which were flat or plateau ulcers. There is no doubt that in this variety of early malignant lesion it is a most important sign and probably could have been demonstrated in more cases had better compression films been obtained. However, in the conical ulcers it was never present on the original films and appears at a comparatively late stage in their development. It is therefore only of limited value in establishing a diagnosis in the early lesion, and its absence gives no assurance that an ulcer is benign. Only 5 ulcers could be considered intraluminal in position on the earliest radiographs and in only 6 cases was there any irregularity of the crater outline. As for the size of the crater, it was found that in only 3 cases was the diameter greater than z½ cm., this being the measurement above which an ulcer should be considered suspicious of malignancy ; see Text-Book of X-ray Diagnosis by Shanks, Kerley, and Twining (I95o), Obviously measurement of the size of the crater is of little value in the early lesion when it is bound to be small, and this criterion could not be considered strictly applicable to the series. Initially 12 of the 21 cases showed none of the features listed above, and whilst the validity of these signs is unquestioned in the later stages of malignant ulceration, it is concluded that they are of very limited help in the diagnosis when the ulcers are small and at an early stage in their development. As indicated the only sign which can be regarded as important is the intraluminal meniscus since it may accompany the small plateau ulcer. A variety of factors contributed to the delay in the diagnosis of these cases. The method of their selection necessarily included all possible causes of diagnostic delay, whether clinical, radiological or otherwise. Consideration of all these is beyond the scope of the present investigation, however, and we have concerned ourselves only with the main radiological causes apparent in the series. These ~\ere 5 in number, and can bc summarized as follows : I. Failure to detect the earl)" flat malignant ulcer. As atreadv mentioned, the main radiologica[ difficulty h~ the plateau ulcer was to demonstrate the lesion in its early stages. These ulcers, ~hela small, are easitv mistaken for a normal peristaltic wave, or rugal fold. (~'ee Fig. *94 A.) Nevertheless, a greater awareness of the significance of such an appearance, and the not too ready acceptance of a simple explanation for its presence, should lead to the early discovery of more of these lesions. 2. Difficulty in differentiating the conical shaped malignant ulcer from a benign lesion. We have already shown that the early conical shaped malignant ulcers are often impossible to distinguish from a benign ulcer on their appearances alone. A tentative diagnosis is only possible by consideration of the behaviour of the lesion under medical treatment and some delay in the radiological diagnosis can therefore hardly be avoided. 3 . Failure to recognize the characteristic features of malignant ulceration, i.e., ' niche en plateau encastr4e ' 4. Failure to detect a malignant lesion when associated with a proximal benign ulcer. 5. The repeated assumption on the film reports of this series, that an ulcer was benign because of the presence of converging mucosal folds to the crater. This sign is often quoted as evidence of benign ulceration, and in a recent publication Kirsh (I955) has re-emphasized its value. I n the present series, however, it was possible to demonstrate converging rugae in over a third of the cases and often the ulcer was reported as benign because of this. In some cases (Fig. i94 g) the folds stopped short of the ulcer margin, presumably due to a surrounding zone of infiltration, but in others (Fig. *95 A) they reached to the edge of the crater
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without interruption and it was these cases which were labelled benign. The sign can therefore be very misleading and should not be relied upon to differentiate the benign and the malignant ulcer. We wish to thank Dr. M. H. Jupe, the Director of the Radiodiagnostic Department of the London Hospital, for permission to publish these cases and for his most helpful advice on the preparation of the paper. We also gratefully acknowledge the help given to us by Dr. R. S. Murray and Dr. Charles Maclean, and we are indebted to Professor Dorothy Russell for allowing us access to the records of the Bernhard Baron Institute of Pathology. REFERENCE S GUTMANN, R. A., BERTRAND, I., and PERISTIANY, T. J. (I939), Le Cancer de L'estomac au Debut. Paris : Doin. HINDS, S. J., and KEMPHARPER,R. A. (I95e), ]?rlt. 7. Radiol., 25, 297. KIRSH, ISRAELE. (t955), Radiology, 64, 357MEUWlSSEN,T. J. J. H. (I955), X - r a y Atlas and Manual of G~.sophagus, Stomach and Duodenum. Amsterdam : Elsevier. RUSSELL,W. A., WEINTRAUB,S., and TEMPLE,H. (I948), Radiology, 5I, 79o. SHANKS, S. C., KEKLEY, P., and TWINING,E. W. (I950), A Text-book of X - r a y Diagnosis, 3, 145.
lrmoriam LORD HORDER OF ASHFORD, G.C.V.O., M.D., D.C.L., F.R.C.P. LONG and eloquent tributes have been paid to Lord Horder in both the lay and medical press. We cannot effectively add to these, but merely show our respect and appreciation for all he did for Radiology. Lord Horder was an Honorary Fellow of the Faculty of Radiologists. He often took part in our early discussions and meetings and he supported our activities until his death. His knowledge of cancer, his interest in ' follow-up ', and his association with the British Empire Cancer Campaign perhaps brought him closer to Radiotherapy than to Radiodiagnosis, but we shall all miss him. We shall miss his criticism, his advice, his help, and his ready support in our development as a specialty.
THOMAS DIGBY WHEELER, M.A., M.D., F.F.R., F.A.C.R., F.R.C.P. (C.), F.I.C.S. DR. DIGBY WHEELERdied September 20, 1955, at the age of 63. He received his medical training at the University of Manitoba and on graduation enlisted in the Canadian Army Medical Corps, serving overseas in the first world war with the rank of Captain. Returning to Canada, he practised at Winnipeg, Manitoba, and taught anatomy in the University of Manitoba. In I932 he began the practice of radiology and held appointments in Radiology at several Winnipeg hospitals. He was appointed Professor of Radiology at the University of Manitoba, and on retirement was made Professor Emeritus. Dr. Wheeler was a past President of the Canadian Association of Radiologists and of the Manitoba Medical Society. During the second world war he was consultant in radiology to the Canadian Armed Forces in Military District No. io. His interests were wide and his aid and counsel were sought by governmental, civic, and medical bodies. For the past two years he was President of the Winnipeg Symphony Orchestra, on the Board of which he had served since i948.