J Clin Ultrasound 7:425-431. December 1979

REAL-TIME ULTRASOUND EXAMINATION IN THE DIAGNOSIS OF GASTROINTESTINAL TUMORS W. Schwerk, M.D., B. Braun, M.D., and H. Dombrowski, M.D.

Inflammatory and neoplastic infiltrations of the intestinal wall lead in advanced stages to a tumorous thickening that can be visualized by ultrasound as t h e so-called cockade sign. The possibilities and limitations of ultrasound diagnosis of gastrointestinal tumors are presented. Over a period of 2 years, 73 tumors were diagnosed, 39 primarily by means of ultrasound with the real-time technique; 15 tumors were curatively resected at the time of primary ultrasound diagnosis. Indexing Words: Ultrasound Gastrointestinal tumors

Ultrasound has continually been gaining in importance as a morphological investigative imaging technique in the diagnosis of abdominal diseases. Since the gastrointestinal tract cannot be visualized sonographically in its continuity, and since interpretation of the scans is often difficult, only a few publications have appeared concerning investigations of tumorous processes of the intestine (1 -8). Our study was undertaken to evaluate the possibilities and limitations of ultrasound imaging of gastrointestinal tumors. METHOD AND TECHNIQUE

In most cases we carried out ultrasound investigation by means of real-time scanning technique: the image on the screen was built up automatically by using a water-path system (Vidoson) with rotating transducers (2.5 MHz) and a parabolic reflector (parallel-scan equipment). Image frequency was 15-30kec. By the use of this dynamic procedure it is possible to visualize movements of the organs that are caused by palpation or respiration, pulsation of the large vessels, or peristalsis in the distal part of the stomach. The examinations are performed on the fasting patient without any special preparation. Overlying intestinal gas interferes with ultrasound scanning, and therefore it may be necessary to repeat the examination after administration of drugs (e.g., From the Department of Medicine, University of Marburg, and Second Department of Medicine, University of Mainz, West Germany. Manuscript received May 16,1979; revised manuscript accepted July 13, 1979. For reprints contact W. Schwerk. M.D., Med.-Universitatsklinik, Mannkopffstrasse 1, D-3550, Marburg, West Germany. 01979 by John Wiley & Sons, Inc. 0091-2751/79/060425-07$01.00

polysiloxan) to degas the bowel. Thus it seems sensible to perform sonography as the first diagnostic measure, because air insufflation during endoscopy and a n intestinal barium meal hampers the transmission of sound. The region of interest is investigated in parallel longitudinal and transverse scans with the patient in the supine position. It is possible to palpate the structures and prove their compressibility as depicted on the screen with direct ultrasound guidance. The echographic findings may be documented with a Polaroid camera. PATIENTS AND RESULTS

Over a 2-year period we have performed sonograms visualizing gastrointestinal tumors in 73 patients; in 39 of these the diagnosis was made primarily by means of ultrasound and was confirmed by further investigations (Table I). During the same period we suspected spaceoccupying lesions of intestinal loops from the sonograms of 14 patients, the lesions being mainly in the descending colon and pylorus area; in all of these, repeat ultrasound studies or further diagnostic measures failed to demonstrate tumoral growth. Most patients were examined for abdominal masses or symptoms suggesting malignancy. In 3 cases the gastrointestinal tumors were detected unexpectedly during ultrasound abdominal screening: 2 patients had symptoms indicating gallstones; 1 patient was presented for control of a n enlarged spleen. Only 1 of 10 gastric carcinomas, but 13 of 20 large-bowel neoplasms, primarily visualized by ultrasound, were found to be resectable at operation. The small-bowel tumors in our series showed advanced stages of Crohn’s disease and Hodgkin’s disease with rigid thickening of the bowel wall. 425

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TABLE I Localization, Curative Surgical Treatment, and Pathological Findings in 39 Patients with Gastrointestinal Tumors, Primarily Visualized by Means of Ultrasound TUMOR LOCALIZATION Stomach Cardiaicorpus Corpusiantrum

PRIMARILY WSUAUZED BY ULTRASOUND

CURATIVE PATHOLOGICAL RESECTION flNDlNGS

0 2

Small intestine

(0)

Large intestine Ascending colon

a

Transverse colon

6

Descending colon Sigmoidlrectum

4

n

0

10 Carcinoma 1 Malignant lymphoma 1 Ulcer

2 Crohn's disease 20 Carcinoma 1 Hodgkin's lymphoma 3 Periappendicular abscess 1 Abscessing diverticulitis

20

The smallest neoplasm, primarily diagnosed by means of sonography, was a n adenocarcinoma of the ascending colon. It had expanded to 5 cm, with thickening of the intestinal wall to about 1.5 cm. DISCUSSION

Normal intestinal loops are not discriminated in their continuity by means of sonography because of the limited effective acoustic resolution capability of diagnostic ultrasound. Only the stronger (muscular) wall of the pars pylorica ventriculi can be imaged regularly. The ultrasound appearance of a cross-sectional scan through the pylorus/ antrum area is a small targetlike formation caudal to the margin of the liver, with varying shape dependent on peristaltic movements. The sonographic features of the intestinal wall with a

FIGURE 1. Longitudinal scans through the upper abdomen along the aorta (A). The arrows demonstrate cross sections of the antrum adjacent t o the caudal margin of the liver (L). Left: normal, Right: infiltrated antrum wall (cockade); carcinoma of the antrum. ED: abdominal wall.

FIGURE 2. A: Radiography made elsewhere: pyloric stenosis due t o a suspected tumor of the head of the pancreas. E: Sagittal scan (left) and axial scan (right) through the antrum (arrows); cone-shaped thickened antrum wall due t o antrum carcinoma. X: intraluminal gas with distal sound shadow (S).

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low-level echo pattern and a highly echogenic center (gas-containing content) (Fig. 1) have been termed the “intestinal cockade” ( I ) . In particular, a circular inflammatory or neoplastic thickening of intestinal loops can be demonstrated sonographically as a characteristic ringlike structure with a wall of low echogenicity and an echo-rich lumen.

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Kremer and associates demonstrated “cockade signs” in two-thirds of a total of 40 patients with known wall-infiltrating gastrointestinal tumors (2). In 1 case they detected a double carcinoma of the colon, primarily by means of ultrasound (3). The ultrasound demonstration of a thickened intestinal loop is not, of course, a specific morphological sign of malignancy. Inflammatory proliferations, as in Crohn’s disease, ileocecal tuberculosis, periappendicular tumor, extensive ulceration or hyperplastic coarse giant folds in Menetrier’s disease, and edema of the intestinal wall in thrombosis of the mesenteric veins, can

FIGURE 4. Longitudinal scan along the aorta (A). The arrows at the caudal margin of the liver (Ll demonstrate an eccentrically thickened antruin wall ventral to the cross-sectioned pancreas (P) and the vena mesenterica superior (V); carcinoma of the antruni.

FIGURE 3. Carcinoma of the descending colon with stenosis. Arrows point to longitudinal and transverse scans through the concentric tumorous gut wall infiltratiori.

FIGURE 5. False positive intestinal cockade caused by overlapping stool-filled loop of the leh colon. R: rib with distal sound shadow (S).

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FIGURE 6. Poorly echogenic mesenteric metastases (M) due to carcinoma of the colon.

also show a thickened gut wall in the ultrasound image (2,4,5). Thus we were generally not able to discriminate specific acoustic contours and structural echo patterns of inflammatory infiltrated intestinal loops as in Crohn’s disease versus neoplastic infiltrations. Although demonstration of intestinal cockade generally indicates advanced inflammatory or tumoral growth, it does not necessarily mean inoperability in the case of neoplasms. In fact, 13 of the 20 colonic carcinomas in our group were treated curatively by surgery a t the time of primary ultrasound diagnosis. On the other hand, all but one of the stomach tumors, primarily diagnosed by ultrasound in our group, revealed advanced incurable malignant lesions. However, one must consider the smaller number of cases, in particular since up to 55 percent of stomach carcinomas subjected to surgery are found to be incurable at the time of operation (9).Thus in the group of known stomach tumors that were subjected to sonographic search for metastases, we were able to demonstrate echographic patterns of circular thickening or eccentric infiltration of the stomach wall due to a n operable tumoral growth (Fig. 4). This applies especially to the antrum, which is particularly accessible to ultrasound investigation. Because of the limited effective resolution capability of the ultrasound imaging technique, one cannot expect a sonographic contribution toward the desired diagnosis of early stages of gas-

trointestinal tumors. In agreement with other authors (2,4), we were also not able to detect known extensive tumors by means of ultrasound in some patients, in particular in the stomach cardia and rectosigmoid region. Overlying intestinal gas or varying echo patterns in a region can prevent demonstration of a tumor. On the other hand, sonographic assessment and exploration of the rectosigmoid region can usually be simplified by means of a filled urinary bladder, which as a n “acoustic window” can improve transmission of sound and permit display of adjacent structures. Analysis of 14 sonographically false positive intestinal cockades revealed, among other findings, that thin fluid levels in the stomach can simulate eccentric dorsal thickening of the wall in the supine patient under transverse or axial scanning guidance. Fecal formations, especially in the descending colon (Fig. 5), were also causes of false interpretation of acoustic scans. Furthermore, a spastic thickening of the bowel wall was found to be responsible for causing intestinal cockade signs (2). Variability in the findings a t a recheck examination is a common characteristic of these pitfalls whereby the varying forms and positions of these structures can be directly checked by palpation under ultrasound guidance. Since the normal intestine cannot be visualized by ultrasound, correct organ-topographic localization of sonographically imaged infiltrations of the bowel wall is not always possible. Thus, as a result of topographic superimposition on the screen, we falsely localized a tumor of the transverse colon as a tumor of the descending segment. In complementation to radiologic and endoscopic findings, the thickness of tumorous intestinal processes can be directly measured and followed up by ultrasound. Abscess formations, as in Crohn’s disease, appendicitis, or mesenteric (Fig. 6) and organic metastases, can under optimal conditions and accurate examination be demonstrated in the same investigation procedure. Without doubt the diagnosis of gastrointestinal tumors is still the fundamental task of radiologic and endoscopic bioptic techniques, particularly in the early stages when they are still confined to the mucosa and submucosa. Because of the uncharacteristic symptoms of advanced neoplasms on the one hand and the growing use of sonography as a screening investigation a t the beginning of diagnostic measures on the other, knowledge of the sonographic features of these tumors is of importance to the investigator in order to make use of further diagnostic methods more precisely and economically. JOURNAL OF CLINICAL ULTRASOUND

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CONCLUSIONS

Sonography is indicated as the first diagnostic measure in cases of palpable abdominal masses for noninvasively diagnosing the consistency and organic involvement. Ultrasound examination is not suitable for diagnosis of early stages of gastrointestinal tumors confined to the mucosa and submucosa nor for definite exclusion of advanced stages. Advanced inflammatory or neoplastic infiltration of the intestinal wall (intestinal cockade) can be visualized by ultrasound. Intestinal cockade is not a specific morphological sign of malignancy, does not necessarily indicate incurable tumor growth, and needs to be clarified at all events. Mesenteric and liver metastases of gastrointestinal tumors may be demonstrated in the same investigation procedure within the ultrasound resolution capability. @

~~

FIGURE 7. A: Air-barium double-contrast enema demonstrates loss of the haustral pattern and a stiff colonic wall with burrowing ulceration and cobblestoning; extensive granulomatous colitis. 6: Longitudinal scan (1) along the aorta (A); axial scans through the transverse colon (2) and the upper (4) and lower (3) parts of the descending colon. Shown here is the marked thickening of the involved bowel wall (arrows). Ps: psoas sheath.

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FIGURE 9. A: Regional enteritis (Crohn's disease) of the terminal ileum with stenoses and thickening of the adjacent mesentery. B: Axial scan through the poorly echogenic rigid bowel segment; thickening of the bowel wall and involved mesentery (arrows). X: echo-rich lumen of the intestinal loop.

REFERENCES

FIGURE 8. A: Coarse folds and rigidity of the whole stomach as in a wall-infiltrating scirrhous neoplasm. B: Arrows point to crosssectional (above) and axial (below) scans through the distinctly thickened echo-free stomach wall with narrowed echo-rich gascontaining lumen (X). S: sound shadow. Advanced malignant lyrnphoma of the stomach.

1. 1,utz H, Rettenmaier G : Sonographic pattern of tumors of the stomach and the intestine, in Proceedings of the Second World Congress on Ultrasonics in Medicine. Amsterdam, Excerpts Medics, 1973, p 277. 2. K~~~~~ H, ~~,l~~~ E, &hier] w, et al: ultrasonic diagnosis in infiltrative gastrointestinal diseases. Dtsch Med Wochenschr 103:965, 1978. 3. Kremer H, Kellner E, Zollner N: Primary ultrasonic detection of a double carcinoma of the colon. Radiology 124:481, 1977.

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4. Lutz H, Petzoldt R: Ultrasonic patterns of space occupying lesions of the stomach and the intestine. Ultrasound Med Biol 2:129, 1976. 5. Schwerk W, Braun B: The use of ultrasound in the diagnosis of gastrointestinal tumors. Z Gastroenterol 16:431, 1978. 6. Frank P, Menges V, Klein M: Ultrasound diagnosis of mural infiltration of the intestinal tract. Fortschr Geb Roentgenstr Nuklearmed 129:90, 1978.

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7. Walls W: The evaluation of malignant gastric neoplasms by ultrasonic B-scanning. Radiology 118: 159, 1976. 8. Peterson LR, Cooperberg PL: Ultrasound demonstration of lesions of the gastrointestinal tract. Gastrointest Radio1 3:303, 1978. 9. Bogach A, e t al: The stomach and duodenum, in Bogach A (ed): Gastroenterology. New York, McGraw-Hill, 1973.

Real-time ultrasound examination in the diagnosis of gastrointestinal tumors.

J Clin Ultrasound 7:425-431. December 1979 REAL-TIME ULTRASOUND EXAMINATION IN THE DIAGNOSIS OF GASTROINTESTINAL TUMORS W. Schwerk, M.D., B. Braun, M...
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