Clin. Radiol. (1977) 28,457-463 THE RADIOLOGICAL FEATURES OF GASTRIC LYMPHOMA J. T. J. PRIVETT,* E. RHYS DAVIES and J. ROYLANCE Department o f Radiodiagnosis, Bristol Health District (Teaching) Primary gastric lymphoma accounts for 2.5% of all malignant gastric neoplasms. The clinical, macroscopic, and radiological appearances frequently resemble those of other gastric lesions, notably carcinoma. However, the prognosis of lymphoma is much better and accurate diagnosis is therefore important. The prognosis of secondary gastric lymphoma is less good but its accurate recognition is still important. Conventional radiology is a key investigation and the radiological appearances have been reviewed in 18 patients with a histological diagnosis of lymphoma. 5 of these were already known to have lymphoma elsewhere. The radiological appearances were similar whether or not there was lymphoma elsewhere. There is no single accurate pattern of recognition but the following features occurred often enough to be useful pointers: (a) Distensible stomach in the presence of a mass. (b) Mucosal hypertrophy in the presence of a mass. (c) Mucosal hypertrophy associated with large gastric ulcer or multiple gastric ulcers. (d) Contiguous spread of abnormality into the duodenal cap. (e) Duodenal ulceration associated with gastric mass. (f) The youth of the patient. The reported incidence of primary lymphoma of the stomach is 2.5% of all malignant gastric neoplasms (Welborn et al., 1965). Similarly about 2.5% of lymphomas present with a primary lesion in the stomach (Bush and Ash, 1969). Its very rarity leads to difficulty in recognition and at laparotomy it may resemble an inoperable carcinoma (Salmela, 1968). However, the prognosis oflymphomas is much better than that of carcinoma (Jenkinson et al., 1954, Jordan et al, 1955) even when regional lymph nodes are involved (Friedman, 1959), and the treatment of choice is resection followed by radiotherapy (Friedman, 1959). Therefore accurate pre-operative diagnosis is important. Secondary lymphoma of the stomach occurs more often than the primary form (McNeer and Berg, 1959) but is still uncommon, and occurs in up to 3.5% of patients known to have lymphoma (Rosenberg et al, 1961: Block, 1967). The prognosis is not as good as in the primary form (Snoddy, 1952), but early recognition of gastric involvement is still important so that appropriate local treatment can be undertaken (Burnett and Herbert, 1956). The diagnosis of both forms of the disease has proved difficult from clinical features (Sherrick et al., 1965) and from radiol0gical studies (Jenkinson et al., 1954; Jordan et al., 1955). The most optimistic estimate of a 50% success rate was obtained after combined clinical, radiological and gastroscopic examination (Palmer, 1950). Radiological studies remain the most important investigation (Ochsner and Ochsner, 1955), but have proved disappointing. 18 consecutive cases of proven lymphoma of the stomach have been reviewed to seek a reliable pattern of recognition. THE PATIENTS
The 18 patients had been referred to the Radiotherapy Centre of the Royal Infirmary, Bristol. A histological diagnosis was obtained in all cases, from either a biopsy or a resected specimen (Table I). 14 patients were male and 4 were female. Their ages ranged from 16 - 77 years (mean 54 years). 5 patients were known to have lymphoma elsewhere, *Present address: Coventry& Warwickshire Hospital.
tonsil (2), sphenoid (1), humerus (1) and retroperitoneal nodes (1). 8 of the 13 patients whose disease was confined to the stomach were treated with surgery alone, and 5 by surgery and radiotherapy. 3 of the 5 with generalised disease had local radiotherapy to the abdomen and 1 of these had simple suturing of a perforated gastric ulcer. 1 of the remaining 2 patients had local radiotherapy to the skull base and chemotheraphy, and the other died before treatment was started.
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Table 1 - Histological Diagnosis
Primary Secondary Total
Reticulum Cell Sarcoma
7
2
9
Giant Follicular Lymphoma
1
1
2
Lymphosarcoma
2
-
2
Itodgkin's Lymphoma
1
-
1
Malignant Lymphoma
2
2
4
13
5
18
TOTAL:
CLINICAL FEATURES The majority presented within one year of onset of symptoms, and were divided into two groups. (a) Patients not k n o w n to have lymphoma previously (13 cases). In 12 patients the mode of presentation was similar with upper abdominal pain, anorexia, nausea and weight loss. 1 patient presented with melaena after anticoagulation for pulmonary embolus and was found to have had symptoms of dyspepsia for 5 years. (b) Patients already k n o w n to have lymphoma elsewhere (5 cases). Two patients had upper abdominal pain, anorexia, nausea and weight loss a similar syndrome to 12 cases in group (a). Attention was drawn to the intestinal tract in the other three patients because of jaundice and an abdominal mass (1), diarrhoea (1) and acute abdominal pain due to perforated peptic ulcer (1). Three patients had gastroscopy. A malignant ulcer was shown in two of these, but there were no specific features to suggest lymphoma. In the third patient, biopsy confirmed reticulum cell sarcoma.
effacement of adjacent mucosal folds (Fig. 4a). This patient also had trefoil deformity of the duodenal cap (Fig. 4b). The third case had a lesser curvature filling defect with mucosal effacement and central ulceration. A repeat examination after 3 years showed that the ulcer had healed leaving a rigid segment of stomach (Figs. 5a, b). 2. Thickening o f the Mucosal Folds (6 cases). The rugae were enlarged and tortuous or even polypoidal (Fig. 6) although they became more effaced as the stomach distended. (A) In two cases the abnormality involved the whole stomach and extended into the duodenum. (B) In four cases the fundus was spared. Two of these had gastric ulcer and duodenal cap deformity. 3. Local Pyloric Rigidity (4 cases). In all these cases the pyloric antrum was narrowed and rigid, with destruction of the mucosal pattern, giving a ragged outline. In two of these cases the abnormality extended into the duodenal bulb (Fig. 7). All the patients had had a chest X-ray at the time of the barium meal. None showed mediastinal or parenchymal involvement. Subsequently one patient
RADIOLOGICAL APPEARANCES The appearances on barium meal were not uniform and were grouped as follows: 1. Loealised Masses (7 cases) (A) Four had smooth lobulated filling defects at the fundus, with sharp re-entrant angles (Figs. 1, 2b). The adjacent mucosal pattern was normal. As the fundus was filled with barium it distended readily, so that the mass became less obvious. In 2 patients repeat examinations over 5 years showed slow increases in the size of these lesions without changes in their character (Fig. 2). (B) Three patients had pre-pyloric filling defects with sharp re-entrant angles (Fig. 3). 2 of these cases had proximal gastric ulcers, and in one of them the ulcer contained filling defects and there was
Fig. 1 - A.S. Male. There are multiple filling defects in the fundus of the stomach.
THE RADIOLOGICAL
FEATURES
OF GASTRIC
LYMPHOMA
Fig. 2 - W.G. Female. (a) 14.12.66. There is a small filling defect at t h e j u n c t i o n o f s t o m a c h and oesophagus. (b) 21.12.71. There are m a n y lobulated filling defects over the whole fundus.
Fig. 3 - W.P. Male. The pylorus and a n t r u m are d e f o r m e d and rigid. 28
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Fig. 4 - R.P. Male. (a) There is a lesser curve gastric ulcer with a fluid level. There are several filling defects in and r o u n d the gastric ulcer. (b) In addition to the gastric ulcer there is a trefoil d e f o r m i t y o f the duodenal cap,
developed multiple lung lesions and a lesion in the right femur. Only one patient had a lymphogram, and this showed extensive para-aortic involvement by lymphoma.
gastric lymphoma involves the submucosal nerve plexus of the stomach early in the course of the disease so that the patient often presents with pain before there are radiologically demonstrable gastric abnormalities (Azzopardi and Menzies, 1960). The converse syndrome with extensive radiological abnormality and relative freedom from symptoms is one that is well recognised (Ngan and James, 1973) but it did not occur in the present series. The endoscopic appearances were not distinctive in the only 3 patients examined but the biopsy was positive in one of these. Endoscopy and biopsy have not fulfilled their promise (Palmer, 1950) and the barium meal is still the diagnostic keystone. Repeated examinations may be needed because of early onset of pain and the slow growth of the lesion (Fig. 2); and knowledge of previous normal examination is sometimes helpful.
DISCUSSION
The stomach may be involved by any of the varieties of lymphoma (Madding and Waiters, 1940; Naqvi et aL, 1969), lymphosarcoma being the most common and Hodgkin's disease the least common of the primary gastric lesions (Table 1; Bush and Ash, 1969). All are very rare in children (Rosenberg et al., 1961) and it is exceptional to be able to predict the histological type from the radiographic features (Highman and Key, 1962). The clinical syndrome was similar in the great majority of the present series but not distinctive enough to eliminate other causes. Characteristically
DIAGNOSTIC PROBLEMS
Even when the barium examination is obviously abnormal, the abnormality is not always recognisable as lymphoma, and the greatest difficulty is in distinguishing between lymphoma and carcinoma. There are several useful discriminatory features. (a) Distensibility of the Stomach Wall. Because lymphoma frequently spreads extensively through the submucosa before involving other layers of the gastric wall, the stomach remains distensible, although it contains one or more polypoidal masses, and this
THE RAD1OLOGICAL
FEATURES
OF GASTRIC LYMPHOMA
461
Fig. 5 - G.B.L. Male. (a) 31.10.67. There is a lesser curve gastric ulcer with radiating folds o f thickened mucosa. (b) 16.10.70. The ulcer has healed b u t the prepyloric region o f the s t o m a c h is rigid and indistensible.
Fig. 6 - C.P. Male. There is extensive m u c o s a l fold thickening - polypoidal at t h e fundus. Fig. 7 - F.M. Female. The a n t r u m pylorus and duodenal cap are d e f o r m e d and rigid.
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feature strongly favours lymphoma. In the present series it occurred most often at the fundus. (b) Mucosal Pattern. The mucosa over a lymphoma mass is frequently intact and the mucosal pattern elsewhere is either normal or even hypertrophied. These features contrast sharply with gastric atrophy that is such a well-recognised association o f gastric carcinoma. (c) Duodenal Abnormalities - Extension of lesion. Histological examination shows that carcinoma of the stomach has spread to the duodenum in at least 30% of cases (Paramanandhan, 1967), but it is very rare to be able to demonstrate this spread radiologically. Spread of lymphoma to the duodenum is relatively commoner and when it is detectable radiologically it is a useful sign, particularly when there is rigidity of the pyloric antrum. Ulceration. Two of the present series had apparently simple duodenal ulcers. This association occurs in less than 1% o f gastric carcinoma (Bateson, 1972), and favours lymphoma. (d) Age of Patient. Occasionally the age of the patient carries some weight in that the span of lymphoma is wider than that of carcinoma. For example one of our patients was aged 16 years, and carcinoma is extremely rare at this age. (e) Evidence of Lymphoma elsewhere. In a patient already known to have lymphoma, gastric involvement is likely to be identified correctly, but failure to show lymphoma elsewhere is unhelpful in primary gastric lymphoma. The main diagnostic difficulty is in distinguishing lymphoma from carcinoma, but other diagnostic problems may arise, and the most important of these is the evaluation o f gastric ulceration. (a) Single Penetrating Ulcer. Gastric ulceration was commoner than expected in this small series and is important because it can distract attention from the co-existent lymphoma, particularly if the ulcer is some distance from the mass. Furthermore the ulcer may heal with conservative treatment, which emphasises the importance of searching carefully for filling defects. The association of gastric ulcer with hypertrophied mucosal folds may raise the possibility of Menetriere's disease, but ulcers are uncommon in this condition and usually they are less than 1 cm across (Reese et al., 1962). In one of the present series filling defects in the ulcer were an important indication of malignant disease. (b) Multiple Ulcers. Multiple gastric ulcers are very uncommon in association with any malignant gastric disease. The proportion of gastric lymph0ma associated with multiple ulcers is much higher than that of carcinoma, but this is balanced by the overall greater incidence of carcinoma (Sherrick et al., 1965).
RADIOLOGY
Rarely, multiple small ulcers surrounded by a raised mucosal edge present a 'target' appearance said to be characteristic of reticulum cell sarcoma (Highman and Key, 1962), though it did not occur in the present series. Rarer causes o f multiple gastric ulcers include cor pulmonale, stress, and tuberculosis (Highrnan and Key, 1962). (c) Ulcerating Mass. Usually, this is a late feature, and the ulcers are superficial and more than 4 cm across (Sherrick et al., 1965). When the ulceration occurs early in the disease, it may be difficult to recognise unless the discriminatory features already described are sought.
CONCLUSION There is no single clinical or radiological pattern by which gastric lymphoma can be recognised. However, there are certain signs and associations which must alert the radiologist to the possibility o f its presence. This suspicion should be conveyed to the clinician so that he can seek histological confirmation, either at gastroscopy or laparotomy. In this way palliative procedures for supposedly inoperable gastric carcinoma will be avoided.
REFERENCES Azzopardi J. G. & Menzies T. (1960). Primary Malignant Lymphoma of the Alimentary Tract. British Journal of Surgery, 47, 358-366. Bateson E. M. (1972). Cancer of the Stomach and Duodenal Ulcer: Report of Two Cases with discussion of the Significance of this Rare Association. Clinical Radiology, 23, 208-212. Block C. (1967). Roentgen features of Hodgkin's disease of. the stomach. American Journal of Roentgenology, 99, 175-181. Burnett H. W. & Herbert E. A. (1956). The role of irradiation in the treatment of primary malignant lymphoma of the stomach. Radiology, 67, 723-728. Bush R. A. & Ash C. L. (1969). Primary lymphomas of the gastro-intestinal tract. Radiology, 92, 1349-1352. Friedman A. I. (1959). Primary lymphosarcoma of the stomach. American Journal of Medicine, 26, 783-796. Highman Z. A. & Key J. J. (1962). Multiple ulceration of the stomach in reticulum cell sarcoma. British Journal of Radiology, 35, 614-618. Jenkinson E. L., Epperson K. D. & Pfisterer W. H. (1954). Primary lympliosarcoma of the stomach. American Journal of Roentgenology, 72, 34-44. Jordan G. L., Bolton B. F., Heard J. G. & Waldron G. W. (1955). Sarcomas of the stomach. Surgery~ Gynaecology and Obstetrics, 100, 453-457. McNeer G. & Berg J. W. (1959). The clinical behaviour and management of primary malignant lymphoma of the stomach. Surgery, 46, 829-840. Madding G. F. & Waiters W. (1940). Lymphosarcoma of the stomach. Archives of Surgery, 40, 120-134. Naqvi M. S., Burrows L., Kark A. E. (1969). Lymphoma of
THE R A D I O L O G I C A L F E A T U R E S OF G A S T R I C L Y M P H O M A the gastro-intestinal tract: Prognostic guides based on 162 cases. Annals of Surgery, 170, 2 2 1 - 2 3 1 . Ngan H. & James K. W. (1973). Clinical radiology of the lymphomas. Butterworth, p. 117. Ochsner S. & Ochsner A. (1955). Sarcoma of the stomach, analysis of 17 cases. Annals of Surgery, 142, 804-809. Palmer E. D. (1950). The sarcomas of the stomach: A review with reference to gross pathology and gastroscopic manifestation. American Journal of Digestive Diseases, 17, 186-195. Paramanandhan T. (1967). The duodenal spread of gastric carcinoma. British Journal of Surgery, 54, 169-174. Reese D. F., Hodgson J. R., & Docherty M. B. (1962). Giant hypertrophy of the gastric mucosa (Menetriere's disease): A correlation of the roentgenographic, pathologic and
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clinical findings. American Journal of Roentgenology, 88, 619-626. Rosenberg S. A., Diamond H. D., Jaslowitz B. & Craver L. F. (1961). Lymphosarcoma: A review of 1269 cases, Medicine, Baltimore, 440, 3 1 - 8 4 . Satmela H. (1968). Lymphosarcoma of the stomach. Acta Chirurgica Scandinavica, 134, 567-576. Sherrick D. W., Hodgson J. R. & Docherty M. B. (1965). The roentgenolic diagnosis of primary gastric lymphoma. Radiology, 84, 9 2 5 - 9 3 2 . Snoddy W. T. (1952). Primary lymphosarcoma of the stomach. Gastroenterology, 20, 537-553. Welborn J. K., Ponka J. L. & Rebuck J. W. (1965). Lymphoma of the stomach. Archives of Surgery, 90, 480-487.