Clin. Radiol. (1977) 28, 617-624

T H E D I S T R I B U T I O N OF G A S T R I C U L C E R S : D O U B L E C O N T R A S T B A R I U M M E A L AND E N D O S C O P Y F I N D I N G S

GILES STEVENSON

From the Department of Radiology, Freedom Fields Hospital, Plymouth

One thousand consecutive double contrast barium meals and 424 consecutive upper gastrointestinal endoscopic examinations have been reviewed. 70 gastric ulcers were found radiologically in 56 patients and 82 gastric ulcers endoscopically in 70 patients. 55% of radiological and 53.6% of endoscopic ulcers were located in the mid or upper body of the stomach. This distribution is contrary to previous radiological findings with the traditional barium meal. Age did not seem to be a major factor. The double contrast meal and in particular the left anterior oblique view with the head elevated, display en face the lesser curve of the upper body around the cardia where many benign ulcers and carcinomas arise.

INTRODUCTION

In discussing the urgent investigation of the upper gastrointestinal haemorrhage, Palmer has written: 'The cardia, too often considered in the past a desert by roentgen opinion, is known to be the Needing segment in at least half of city hospital bleeders' (Palmer, 1974). In 1971, a Veteran's Administration Co-operative Study of 638 patients with benign gastric ulcer diagnosed radiologically was published, and in this series 70.5% of ulcers occurred within 7.2 cm of the pylorus (Sun et al., 1971). The author has been surprised by the frequency with which endos- copy reveals high lesser curve ulcers in patients with barium negative dyspepsia, sometimes invisible with a forward viewing instrument but clearly shown with a side viewing gastroscope. In order to resolve these conflicting findings a review of the location of gastric ulcers in a series of 1000 consecutive double contrast barium meals and 424 consecutive upper gastro- intestinal endoscopic examinations has been carried out.

METHODS AND MATERIALS

The patients were all examined by the author between January 1974 and September 1975. Patients were referred for examination from general practi- tioners and hospital colleagues and included both in and out patients. Ages were from 10 to 94 years (under the age of 10 double contrast technique was not used). Most examinations were performed using an under couch tube with a 2.0 mm focal spot, although for a few patients a 1.2 mm focal spot tube was available. Intravenous Hyoscine Butyl Bromide (Bus-

Present address: The Department of Radiology, McMaster University Medical Centre, 1200 Main Street West, Hamilton, Ontario, Canada.

copan) 20 mg, or Glucagon 0.2 mg was used routinely. Barosperse was used initially, but Baritop 200 ml for the majority of examinations. Additional gas was produced by an effervescent powder, and an anti-foam solution was added to the barium. A standard set of radiographs was obtained, although with some variation according to the individual problems that arose.

The endoscopes used included the ACMI F8 and Olympus paediatric GIFP end viewing instruments, the side viewing Olympus GFB2 gastroscope and JFB2 duodenoscope. 27% of patients were examined with more than one instrument, the second being passed whenever the first had failed to exclude a lesion, obtain a good view, or was inadequate for satisfac'tory biopsies.

RESULTS

Radiology - Seventy gastric ulcers were found in 56 patients. Ulcer scars and carcinomas were ex- clude& 52 of these ulcers in 47 patients were confirmed endoscopically and were benign on biopsy. The distribution of these ulcers within the stomach is shown in Figs. 1 and 2. Over half the ulcers lie in the mid or upper body of the stomach, mostly on the lesser curve or the posterior wall. There is a relative absence of ulcers on the anterior wall, probably partly due to inadequate technique, although it is known endoscopically that ulcers do occur much more frequently on the posterior than the anterior wall. Apart from the 56 patients mentioned above, it is known that superficial linear gastric ulcers were missed radiologically and seen endoscopically in a further four patients and are, therefore, represented in this paper only in the endoscopic series. In 2 of these, the linear ulcer was visible retrospectively on

618 CLINICAL R A D I O L O G Y

Fig. 1. - Diagram illustrating the position of 70 gastric ulcers found on double contrast barium meal in 56 patients. The diagram represents a stomach opened from the pylorus to cardia along the junction of posterior wall and greater curve; mucosal surface uppermost with the greater curve at the top of the diagram and the posterior wall at the bottom. Vertical lines divide the proximal and distal antrum, angulus, lower mid and upper body and fundus.

the films. The greatest diff icul ty was exper ienced in the distal an t rum where th ickened folds were diff icult to interpret . In 2 pat ients , erosions are known to have been missed in the distal antrum; in one case 3 erosions were present on th ickened antral folds and in the other , a single erosion approx imate ly 3 m m in diameter. No ulcer in the distal an t rum over 5 m m in size was missed radiologically, as far as is known, but there was over-diagnosis o f small ulcers in this part o f the s tomach. Several pat ients were en- doscoped for suspected small antral ulcers which were no t in fact present , and in 3 cases small mal ignant ulcers were suspected due to the trapping of bar ium be tween th ickened antral folds, producing an ap- parent int ra luminal ulcer even on compress ion (Figs. 2 and 3). On endoscopy the th ickened folds were conf i rmed but there was no ulcer or neoplasm. One persistent depression on the poster ior wall o f the mid body due to a healed previously penet ra t ing ulcer was mis-diagnosed as a shallow active ulcer, and in several further pat ients minor scars or deformit ies were suspected o f being small ulcers. These diagnoses were disproved on endoscopy and biopsy. Such errors have occurred less f requen t ly as famil iar i ty has been gained wi th the technique, but the distal an t rum remains a d i f f icul t area wi th a t endency to over diagnosis. A conf iden t negative diagnosis is almost always correct wi th the double contras t technique.

Fig. 2. - Supine right anterior oblique projection showing a puddle of barium between thickened folds in the antrum. Thickened folds confirmed at endoscopy but no ulcer.

Fig. 3. - Erect compression view of lesser curve of distal antrum showing thickened folds and a lesser curve pre-pyloric irregular puddle of barium, suggesting an intraluminal ulcer. At endoscopy thickened folds were confirmed but no ulcer. Normal biopsies.

THE DISTRIBUTION OF GASTRIC ULCERS 619

Fig. 4. - Endoscopic distribution of 82 gastric ulcers in 70 patients. Diagram prepared as for Fig. 1, showing slightly more ulcers on the anterior wall, but still relatively few compared with the lesser curve and posterior wall.

E n d o s c o p y - In the 424 patients examined endoscopically, 82 benign ulcers were seen in 70 patients. All were benign on mult iple biopsy and no case of carcinoma has yet developed. Ulcer scars and malignant ulcers were excluded. Fig. 4 shows the distribution of these 82 ulcers, illustrating the number found in each segment of the stomach. The distribution of the 51 ulcers which were included in the radiological series is shown separately. 53.6% of the ulcers were in the mid or upper body of the stomach.

Gastric ulcers have been divided into three types (Johnson 1965). Type 1 (57%) occur on the lesser curve proximal to or on the incisura, associated with a normal pyloric canal and duodenum and with low or normal gastric acid sec re t ion :An excess of blood group A is found in these patients. Type 2 (22%) occur in the same site as Type 1, but are associated with active duodenal ulceration or deformity of the pyloric canal. These patients are acid hypersecretors and an excess of blood group O is found as in duodenal ulcer patients. Type 3 (22%) are pre-pyloric - distal to the incisura. They behave as duodenal ulcers and are associated with hypersecretion of gastric acid and excess of blood group O. An excess of duodenal ulceration in a populat ion is, therefore, likely to be associated with an increased proport ion of gastric ulcers occurring in the distal part o f the stomach, and conversely a populat ion or hospital group with a low incidence of duodenal ulceration may have a high proport ion of gastric ulcers occurring

in the upper body. Johnson's classification is impor- tant for radiologists, since a report of ulceration, scarring or deformity in the duodenum or pylorus in a gastric ulcer pat ient may influence the surgical t reatment .

It is known that gastric ulcers almost always arise in a pyloric type of mucosa or in the zone of transition between pyloric and body gland mucosa (Morson, 1975), and there is pseudo-pyloric meta- plasia and gastritis distal to the ulcer. The gastritis and pseudo-pyloric metaplasia are not caused by the gastric ulcer but precede it, and do not regress when the ulcer is healed (Gear, 1971). The stimulus, possibly reflux of bile or pancreatic juice (Delaney, 1972) may produce a stepwise proximal spread of chronic gastritis and pyloric metaplasia. Gastric ul- ceration may occur at any stage, provided there is still some gastric acid secretion (Lennard Jones, 1960). Thus histological enlargement of the 'ant rum' pre- cedes gastric ulceration of the body, but probably does not necessarily always produce a gastric ulcer, and it may occur at any age. Atrophic gastritis is more common in old age (Andrews et aL, 1967). Amberg has described the geriatric ulcer as being one that lies high on the lesser curve (Amberg etal . , 1966), but high lesser curve ulcers also occur in the young. It may be that the elderly develop larger ulcers due to delay in seeking diagnosis and treatment, while the young patient with a high gastric ulcer may have presented earlier and been treated medically for barium negative dyspepsia. Our own figures do not show any noticeable effect of age on the posit ion o f gastric ulcers (Table 1), however, very large ulcers in the body were seen more often in elderly patients. Thus it may not be so much the site that is the hall mark o f the geriatric gastric ulcer as the size that it is liable to attain before presenting for diagnosis.

Table 1 - Effect of age of patient on posit ion of gastric ulcer. An ulcer in the distal antrum scored 1, in the proximal antrum 2, and so on to 6 in the upper body. The total ulcer score in each decade was then divided by the number of ulcers to produce the figures in the third column. Proximal gastric ulcers do not appear to be more common with increasing age.

Number o f Score for mean Decade ulcers ulcer location

3rd 8 4.7 4th 4 5.0 5th 5 4.0 6th 12 4.0 7th 16 4.2 8th 20 4.3 9th 5 4.0

620 CLINICAL RADIOLOGY

DISCUSSION

In 1971 there was published a Veteran's Administrat ion Co-operative Study o f 638 patients who completed t reatment for benign gastric ul- ceration, and the distribution of ulcers in this series was given (Sun e t al., 1971). Routine conventional barium meals were employed, although many ulcers were confirmed by gastroscopy. 70.5% of ulcers occurred within 7.2 cm of the pylorus and 84.9% within 9 cm. Measurement from a series of conven- tional barium meal radiographs indicates that the angulus is approximately 5 cm from the pylorus and the cardia 12 -15 cm, depending on the patient 's position, with 13 cm an average figure. From this it is possible to represent the Veteran's Administrat ion Survey distribution graphically and compare it with the figures from our 56 patients (Fig. 6). The difference is striking. If 7.2 cm is taken as the junction between lower and mid body Of the stomach, then in Plymouth only 45% of ulcers occur in this distal segment radiologically. Our endoscopy findings are very similar to the double contrast radiology with 46 .4% of the endoscopic ulcers occur- ring in the distal segment. Fig. 7 shows on the same graph the double contrast radiology, endoscopy and conventional radiological findings.

There are two possible causes ~,for the different distribution between the Veteran's Administration series and the present s tudy.

• 1. Dissimilarity of pat ient groups 2. Failure of the tradit ional barium meal to detect

ulcers in the upper body around the cardia. 1. Dissimilarity of groups - An endoscopic survey

of 88 patients in Chicago with multiple and single benign gastric ulcers, examined with a side viewing gastrocamera demonstrated 59 ulcers in the antrum, 44 at the angulus and only 28 in the body of the stomach (Winans et al., 1972). This distribution is not very dissimilar from the Veteran's Administrat ion Radiological Study. Of the 88 patients, no ulcer had been found in 34 by radiology, and in those with single gastric ulcers endoscopically, radiology had failed to demonstrate the lesion in 51.5% when the ulcer was under 1 cm in diameter and 29% when it was over 1 cm. The location of the ulcers that had been missed was not given. The distribution from this Chicago study gives l imited support to the Veteran's Administrat ion Radiological Survey but is against the experience in upper gastrointestinal bleeding en- doscopically as quoted by Palmer. A further series from the United States showing the distribution with double contrast radiology and with modern en- doscopic instruments would be interesting.

I ~ E51 ,E82

30%

Distal ProxY. Angulus Lower Mid Upper Antrum Antrum body body body

30%

20%

10%

. ~ ~ DCBM 70

~ V A 638

Distal Prox'. AnguJus Lower Mid Upper Antrum Antrum body body body

30% 20%

10%

~ EB2

~ ~-DCBM 70

~ V A 638

Q Distal Prox.' Angulus Lower Mid Upper Antrum Antrum body body body

Fig. 5. - Endoscopic distribution of gastric ulcers. The 51 ulcers also occurring in the radiological series are shown separately from the total figure of 82.

Fig. 6. - Comparison of distribution of gastric ulcers found by double contrast barium meal and by conventional barium meal (see text).

Fig. 7. - Conventional radiology, double contrast radiology and endoscopy. Conventional radiology appears to demon- strate more ulcers in the distal part of the stomach and fewer proximally.

T H E D I S T R I B U T I O N O F G A S T R I C U L C E R S 621

Fig. 8. - Supine view. Gastric ulcer obscured by the fundal puddle of barium.

Fig. 9. - Same pat ient as Fig. 8 Left posterior oblique, posit ion revealing an irregular 3 cm diameter radiolucency just below the cardia. Endoscopy showed chronic benign gastric ulcer.

Fig. 10. - Supine double contrast film. Polyp greater curve of lower body. Carcinoma h idden in fundal bar ium puddle.

Fig. 11. - Supine hor izontal beam film of same pat ient as Fig. 10 showing how much of the body of the s tomach is obscured by the funda l puddle in the usual supine film.

622 CLINICAL R A D I O L O G Y

Fig. 12. - Same patient as Figs. 10 & 11. Left anterior oblique view with 45 ° elevation of the head of the table. Lobulated Bormann I carcinoma (4 X 3 cm X 1 cm) on the lesser curve of the upper body.

Fig. 13. - Left anterior oblique view with head of the table elevated 45 °. 1.5 cm diameter benign ulcer, posterior to and just below the cardia with radiating mucosal folds reaching to the edge of the ulcer. Benign on biopsy.

Fig. 14. - Left anterior oblique view with head of table raised 45 °. 1.5 cm diameter ulcer, smooth in outline just below the cardia. Abnormal mucosal pattern surrounding the ulcer (arrows indicate margin) with interruption of mucosal folds (black dots), indicating the lesion to be a carcinoma.

2. Possible fai lure o f c o n v e n t i o n a l rad io logy. - I f the 70% o f gastric ulcers f o u n d w i t h i n 7 cm o f the pylorus in the V e t e r a n ' s A d m i n i s t r a t i o n Survey repre- sents on ly 45% of the i r t rue to ta l , as suggested b y the figures in our p resen t s tudy , t h e n the i r t rue to ta l would have been o f the o rder o f 982 ulcers . It m a y be w o n d e r e d w h e t h e r i t is l ikely t ha t so m a n y ulcers could have been missed in the u p p e r par t of the s t omach by exper i enced radiologists pe r fo rming conven t iona l ba r ium meals . C o n s i d e r a t i o n of th is mus t inc lude w h e t h e r the films d e m o n s t r a t e the

l e s i o n and w h e t h e r the lesion is recognised b y the

Fig. 15. - 5 mm diameter benign gastric ulcer on posterior wall of body of the stomach. Sharply defined anterior wall mucosal folds are seen running vertically. These are crossed by at least three less well defined posterior wall folds running horizontally to a small superficial gastric ulcer.

THE D I S T R I B U T I O N OF G A S T R I C ULCERS 623

Fig. 16. - Two small benign gastric ulcers about 3 cm apart just below the cardia. Radiating mucosal folds.

Fig_ 17. - Large anterior wall duodenal ulcer with sentinel fold running to the ulcer from the antrum.

Fig. 18. Sentinel fold in the antrum running to the pylorus. Slight deformity of base of duodenal cap. Only scarring at endoscopy.

Radiologist. Even large ulcers may be present on the lesser curve of the upper body and be completely hidden by the fundal pool of barium in the supine view. It may not be generally appreciated that in this projection only the lower body and inferior part of the mid body on the lesser curve are seen clear of the fundal puddle if a large quanti ty of barium is given. There is sometimes only one projection from a conventional series of films in which such ulcers are shown. The film taken with the patient prone in the left posterior oblique position, to demonstrate the duodenal cap, pylorus and lower body of the stomach also includes a fundus and cardia outlined by air. The high lesser curve in this projection is filled with air and not with barium and a gastric ulcer here often shows as a ring or irregular outline of barium surround- ing an area of increased lucency representing the ulcer crater (Figs. 8 and 9). Carcinomas o f the lesser curve just below the cardia may be equally difficult to demonstrate due to the fundal puddle of barium hiding the lesion (Figs. ! 0 - 1 2 ) . Moderate size ulcers adjacent to the cardia will be visible with care, whether or not additional air is used, but are much easier to characterise as benign (Fig. 13) or malignant (Fig. 14) by a double contrast method in which the pat tern of the surrounding mucosa is displayed (Ichikawa, 1974). The view which demonstrates this part of the

stomach is an essential part of the double contrast examination and is obtained with the patient in the left anterior oblique position, or sometimes lying completely on his right side with the head of the table raised 45 ° . The error of reporting small ulcers as ulcer scars can often be avoided if the mucosa is adequately distended (Fig. 15) and very small super- ficial ulcers require the double contrast technique for their detection (Fig. 16). Guide lines (Scott Harden, 1975) or mucosal folds radiating to a gastric ulcer are helpful pointers, but in the antrum they may be found pointing to a duodenal ulcer (Fig. 17), corres- ponding to t h e s e n t i n e l fold that is a useful endoscopic marker of duodenal ulceration on the other side of the pylorus. The fold may however persist, and sometimes be found on endoscopy to lead only to a small scar in the base of the cap (Fig. 18).

CONCLUSION

In a personal series of patients seen in Plymouth in 1974 and 1975, the majori ty of gastric ulcers were located in the mid or upper body of the stomach, 55% on double contrast radiography and 53.6% endoscopically. This finding does not appear to be age related. This distribution is at variance with

624 CLINICAL R A D I O L O G Y

previous reports and before accepting that in- adequacies o f convent ional radiology are responsible, i t is necessary to wai t for fur ther in fo rmat ion on the distr ibut ion of gastric ulcers in the Uni ted States on double contrast bar ium meals and with mode rn endoscopes. Small ulcers are mos t easily demon- strated en face, and in the upper b o d y of the s tomach this requires the lef t anterior obl ique view wi th elevation of t he head of the table, together w i th adequate dis tent ion and coat ing o f gastric mucosa.

Acknowledgements. - It is a pleasure to thank Dr Homer Smith for permission to show Figs. 8 and 9.

REFERENCES

Amberg, J. R. & Zboralske F. F. (1966) Gastric ulcers after 70. American Journal of Roentgenology, 96,393-399.

Andrews, G. R., Haneman, B., Arnold, B. J., Booth, J. C., & Taylor, K. (1967). Atrophic gastritis in the aged. Austra- lasian Annals of Medicine, 16, 230--235.

Delaney, J. P., Cheng, J. W. B., Butler, B. A., & Ritchie, W. P.

(1970). Gastric ulcer and regurgitation gastritis. Gut, 1970. 11, 715-719.

Gear, M. W. L., Truelove, S. C. & Whitehead, R. (1971). Gastric ulcer and gastritis, Gut, 12, 639-645.

Ichikawa, H. (1973). Differential diagnosis between benign and malignant ulcers of the stomach. Clinics in Gastro- enterology, 2, 329-343.

Johnson, H. D. (1965). Gastric ulcer. Classification, blood group, characteristics, secretion patterns and patho- genesis. Annals of Surgery, 162, 996-1002.

Lennard Jones, J. E. (1960). Factors in the pathogenesis of peptic ulcer. Postgraduate Medicine Journal 36,722-732.

Morson, B. C. and Dawson, I. M. P. (1972). Gastro.intestinal pathology. Blackwell Scientific Publications. Ch. 11, 114.

Palmer, E. D. (1974). Gastro-intestinal panendoscopy. Ed L. Berry. Ch. 31,489-498.

Scott Harden, W. G. (1975). Emergency radiology in acute upper gastro-intestinal haemor~hage. Topics in Gastro- enterology, Ed. Truelove S. C. and Goodman M. J. Blackwell Scientific Publications. Ch. 3, pp. 23-35.

Sun, D. C. H. and Stempien, S. J. (1971). Site and size of (gastric) ulcer as determinants of outcome. Gastro- enterology, 61,576-584.

Winans, C. S., Yoshii, Y. and Koboayashi, S. (1972). Endoscopic diagnosis of multiple benign gastric ulcers. Gastro-intestinal Endoscopy, 19, 63-66.