radlooraphics indexterms: crohn’sdisease: lesscommon

Volume 8, Number 2 #{149}March, 1988 #{149}RadioGraphics 259

Radlooraphics Index terms:Gastrointestinal Imaging

GENERAL/MULTiPLE SIThS

Cumulative index terms:IntestInes, diseases

THIS CONTRIBUTED MANUSCRIPTWAS RE\.IEWED BY THE GASTRO-INTESTINAL RADIOLOGY PANEL, ANDACCEPTED FOR PUBLICATION AFTERREVISION ON JULY 31 , 1987.

From the Department ofRadiology, North Shore Univer-sily Hospital, Manhasset, NewYork.

Address reprint requests toBR. Javons, M.D., Departmentof Radiology, North Shore Uni-versily Hospital, 300 CommunityDrive, Manhasset, NY 11030.

Crohn’s disease: Less commonradiographic manifestations

Bruce P. Javors, M.D.

Alan Wecksell, M.D.

Donald Fagelman, M.D.

Crohn’s disease may involve The gasfrointestinal tractfrom The esophagus to the anus. Unless the unusualmanifestations of The disease are kept In mind, manycases are ilkely to be misdiagnosed radlographically.

Introduction

The usual radiographic appearance of Crohn’s disease involvingthe distal small bowel and colon is well known. Less well known,however, are the atypical radiographic manifestations of this disease.This pictorial essay will demonstrate many of the unusual radiographicfindings seen in Crohn’s disease.

Atypical Locations

Although Crohn’s disease may affect the gastrointestinal tract fromthe oropharynx to the anus, radiographic evidence of esophagealinvolvement is unusual. Aphthous ulcers are the classic finding in Crohn’sdisease of the esophagus, but their presence is not pathognomonic,and the finding must be considered in the overall clinical and radio-graphic context before the diagnosis can be established (Figure 1).Aphthous ulcers in the esophagus may be seen in up to 3% of patientswith Crohn’s disease, if double contrast techniques are used (20). As theinvolvement progresses, the size and number of the ulcers increase toproduce a more severe esophagitis. The ulcers may become confluentand, rarely, they may progress to produce a cobblestone mucosa. Fistulasare seen in very advanced cases (15).

Figure 1A double contrast examination of theesophagus reveals scattered aphthousulcers (open arrows) on a backgroundof otherwise normal mucosa.

2A compression spot radiograph from a single contrast uppergastrointestinal examination shows at least Iwo aphthousulcers (arrows) and thickened, nodular gastric folds in theantrum. Slightly limited distensibility is also seen.

Unusual manifestations of Crohn’s disease Javors et al.

260 RadioGraphics #{149}March, 1988 #{149}Volume 8, Number 2

C0

� In the stomach, the presence of aphthous

�a ulcers may suggest the diagnosis of Crohn’s dis-

g ease, but these are virtually indistinguishable� from gastric erosions. Both single contrast (Figure

2) and double contrast radiography (Figure 3)may show this feature. According to Stevensonand Laufer (19), double contrast studies revealaphthous gastric ulcers in 20-30% of patientswith granulomatous ileocolitis. As the gastric in-volvement becomes more severe, it causes nor-rowing and decreasing pliability of the distalstomach, especially the antrum (Figure 4). Thisaccounts for the unique configuration called theram’s horn or “Shofar” sign (3). The scarring maycross the pylorus to involve the adjacent duo-denal bulb creating a tubular appearance sim-ilar to that seen following Billroth I surgery (18).

Javors et al. Unusual manifestations of Crohn’s disease


Figure 3A double contrast spot radiograph ofthe antrum (different patient from Fig-ure 2) shows multiple aphthous ulcerswith very prominent halos of edema.Thickened prepyloric folds with normalpliability are also seen.

Figure 4A single contrast uppergastrointestinal study re-veals severe narrowingof the body and antrumof the stomach with ir-regular, ulceratedmucosal contours. Theduodenal bulb is similarlyinvolved and cannot bedistinguished from thedistal antrum. This con-tinuum of gastroduo-denal involvement pro-duces the “Shofar” sign.

fI

C0

Unusual manifesto lions of Crohn’s disease Javors et al.


Despite the finding of the NationalCooperative Crohn’s Disease Study (5) that theduodenum was abnormal in 20% of all casesand showed the classical features of Crohn’s dis-ease in approximately 10% of all cases, anec-dotal evidence suggests a less frequent rate ofradiographic demonstration. Duodenal involve-ment is usually found in patients with antraldisease, although isolated duodenal Crohn’sdisease may rarely be seen. Aphthous ulcers,seen early in the disease process in theduodenum, may progress to larger ulcers in thebulb or post bulbar duodenum. Differentiation

from peptic disease is often extremely difficult.Eventually, a deformed duodenum with thicknodular folds may be seen (Figure 5). Whenfibrosis and scarring lead to a stricture, it usuallyis not the typical cloverleaf seen as a sequela ofduodenal peptic ulcer disease (15).

Granulomatous bowel disease may also in-volve the proximal jejunum. Jejunal involvementis reported in approximately 8% of cases (10).

Multifocal segmental involvement of theduodenum and jejunum was seen in one of ourpatients who previously had had small and largebowel resections (Figure o).

Figure 5Two spot radiographs of the descending duodenum reveala very irregular, nodular, narrowed but changeable lumen.An inconstant outpouching along the lateral wall is probablya pseudodiverticulum.

Figure 7 _____A double contrast barium enema shows a markedly distorted proximal trans-verse colon with pseudopolyps and ulcerations. Extending superiorly, is afistula to the air filled distal descending duodenum. The duodenum showsminimally thickened folds, but was otherwise unremarkable, even on anupper gastrointestinal series (not shown).

Unusual Fistulas


Volume 8, Number 2 #{149}March, 1988 #{149}RadloGraphics 263

Figure 6An upper gastrointesfinal series with a watersoluble contrast medium demonstrates multipleareas of duodenal and jejunal narrowing. Themedial wall of the descending duodenum isstiff, and the mucosal folds are effaced. In thetransverse duodenum, thick, irregular folds areseen superiorly. Starting at the ligament of Treifz,multiple smooth areas of narrowing (string signs)with intervening areas of dilatation can beseen.

Enteroenteric, enterocolic and entero-cutaneous fistulas are well known and relativelycommon features of Crohn’s disease. Less oftenseen are duodenocolic, enterovesical or col-ovesical fistulas.

Duodenocolic fistulas may form as a resultof the intimate anatomic relationship of theretroperitoneal descending duodenum and theproximal transverse colon. The root of the trans-verse mesocolon arises at the level of the infra-ampullary portion of the duodenum and is rela-tively short at this level; providing a direct pathwayfor the spread of disease. These fistulas are almostalways the result of transverse colon disease thatsecondarily involves the duodenum (15). Althoughreadily apparent on a barium enema, the fistulaseen in Figure 7 was not demonstrated on anantegrade study in the same time period. Theduodenum, which may show nonspecificchanges in the presence of such a fistula, oftenreturns to a normal appearance following resec-tion of the fistula (11).

U)

a

I

Figure 8A become radiographically detectable.This double contrast barium enema, with reflux into the terminal ileum,reveals a coarse granular mucosa in the terminal ileum and proximaltransverse colon. The appendix shows irregular narrowing. All thesefindings are consistent with Crohn’s disease.



Many tests have been advocated for dem-onstrating suspected enterovesical or colovesicalfistulas. These include examining the urine forpreviously ingested colored materials, cystoscopy,computed tomography and conventionalbarium studies. The Bourne test is probably thesimplest, briefest and least expensive test to per-form �V. In this test, following the rectal adminis-tration of barium, a freshly voided orcatheterized urine sample is obtained and cen-trifuged. The centrifuge tube is then radiog-raphed with a horizontal x-ray beam. The bariumsediment, if present, is revealed as a separatelayer from the supernatant liquid. In this manner,extremely dilute concentrations

of barium may be detected. Althoughevaluated before the widespread use of com-puted tomography, the Bourne test was positivein 9 of 10 cases with proven fistulas. In seven ofthese cases, it was the only positive evidence ofa fistula (V. This compares favorably with resultsobtained using computed tomography as theprimary diagnostic tool (6). In our example, abarium enema revealed evidence of Crohn’sileocolitis, but no fistulous tract or opacificationof the bladder (Figure 8A). A freshly voided urinespecimen, however, revealed traces of bariumin the sediment confirming the clinical suspicionof an enterovesical fistula (Figure 8B).

C

C10Ca

I

Figure 9A single contrast barium enema reveals a long, paracolic, intramural sinustract parallel to the medial (mesenteric) border of the sigmoid colon. Thesinus tract communicates with multiple diverticula. This may be difficult todifferentiate from the sinus tracts seen in diverticulitis.

Abscesses



Another unusual fistula isthe intramural, paracolic orparaenteric sinus tract (Figure9). When seen in the colon,this lesion may be difficult todistinguish from the sinus tractcharacteristic of diverticulitis.

The abscesses most often associated withCrohn’s disease are interloop or mesenteric inlocation. Although separation of small bowelloops on conventional contrast examinations ismost commonly the result of fibrofatly proliferationof the mesentery, it may be evidence of anabscess, and computed tomography can differ-entiate fibrofatty proliferation from abscess for-motion (7). Fluid collections with or without

associated extraluminal air can be detectedreadily by CT. Two of the more unusual locations,in our experience, were the anterior abdominalwall and the psoas muscles. In the first case, CTscans revealed an abnormally thickened loopof bowel leading to an anterior abdominal wallabscess (Figure 10). Although this patient hadknown Crohn’s disease, no external sign of thisabscess was recognized clinically.

Figure 10This CT section through the pelvis revealsan abnormal small bowel loop with athickened wall adjacentto the paste-nor aspect of the anterior abdominalwall. Within the abdominal wall at thissite, is an air and fluid collection rep-resenting an abscess. The attenuationof the mesenteric fat in the area isincreased, representing inflammatorychange.

Figure IIAA pelvic CT section demonstrates multiple circumscribed lucencies repre-senting fluid collections in the right psoas muscle and a large fluid collec-tion in the left psoas muscle. These findings are evidence of bilateral psoasabscesses.

..�

Unusual manifesto lions of Crohn’s disease Javors et al.


U)

In the second patient,� back pain was the most signif-

icant clinical feature. The CTexamination revealed bilateral

P5005 abscesses (Figure hA).A subsequent barium enemademonstrated the changes ofCrohn’s disease in both theileocecal region and the sig-moid colon, accounting forthe bilateral involvement (Fig-ure IIB).

Figure IIBA double contrast barium enema onthe same patient reveals distortedmucosal folds and compression of themedial wall of the cecum by an ex-trinsic mass. The sigmoid colon showsmultiple areas of narrowing withmucosal irregularity and some ulcera-tions. Spot radiographs of these sites(not shown) demonstrated many smallsinus tracts.



Secondary Ch#{228}flg6sin Adjacent Bowel

Inflammatory changes in one segment ofthe gastrointestinal tract secondary to the pres-ence of inflammatory disease in an adjacentbowel loop may be seen. These changes maybe produced either by an adjacent extrinsic in-flammatory mass (phlegmon or abscess) or byfistulization from adjacent, diseased bowel. Ineither case, the secondary changes arenonspecific but readily differentiated fromCrohn’s disease. Following resection of the dis-eased bowel, these nonspecific changes re-solve, and the affected areas return to a normalappearance (IV.

In one patient, the greater curvature of thestomach was abnormal (Figure 12A). Computedtomography revealed involvement of the trans-verse colon by Crohn’s colitis that had spreadvia the gastrocolic ligament to involve thestomach (Figure 12B). In a second patient, an aircontrast barium enema revealed abnormalitiesinvolving the ileocecal valve and the medialwall of the ascending colon (Figure 13A). A smallbowel series showed multiple fistulas to this re-gion (Figure 13B).

Figure 12AThis double contrast spotfilm of the antrum showsa flattened greater cur-vature. Prominent foldswithout evidence of amass or ulceration arenoted. The overlyingmucosal pattern is normal.

Figure 12BThis CT section demonstrates irregularthickening of the wall of the transversecolon with narrowing of the lumen.Inflammatory changes are noted inthe pericolonic fat. More superior sec-tions revealed these inflammatorychanges, which arose in the colon, toextend to the greater curvature of thestomach.

Figure I3AA spot radiograph from a double contrast bariumenema reveals abnormal thickening of thesuperior lip of the ileocecal valve. This thickeningextends superiorly along the medial wall of theproximal ascending colon. The overlying mucosais intact.

Figure I3BThis spot radiograph from a small bowel followthrough examination shows an abnormal terminalileum with nodularily. deep ulcerations and multi-pie ileocolic fistulas involving the abnormal seg-ment of the ascending colon seen in Figure 13A

Unusual manifestations of Crohn’s disease Javors et al


U)0a)CC

.CC)

CVC

Tumors and Pseudotumors

The incidence of malignant neoplasms ofthe bowel in patients with Crohn’s disease isgreater than in the general population. A preva-lence of 0.5% has been reported (14). Smallbowel tumors are usually found distally, parallelingthe distribution of Crohn’s disease and differingfrom the usual more proximal involvement seenin the general population (4). Most commonlyaffected are those loops of diseased bowel that

have been bypassed in diversionary surgery (9)and those involved in fistulas (4). Colonic neo-plasms may also be encountered. This risk is notas great as in the case of ulcerative pancolitis,however (4). In one of our patients with a previ-ous ileotransverse colostomy (without smallbowel or colon resection), a carcinoma of thebypassed loop was found (Figures 14A and 14B).

Javors et al Unusual manifestations of Crohn’s disease


Figure 14AThis upright radiograph from a double contrastbarium enema reveals an ileotransverse colas-tomy. There was no history of a prior colonicresection. There was obstruction to the flow ofbarium in the short segment of visualized smallbowel.

Figure I4BA spot radiograph of the obstructed, bypassedileum shows irregular abrupt tapering of thebowel with an overhanging edge consistentwith a carcinoma.

30aa3a..D

aI30a

0E

V

3

a.

C

C

0E3

Figure I5BA spot radiograph ofthe ascending colon reveals thatthe ‘apple-core” is composed of innumerable small, inflammatory and postinflammatory polyps rather than of an annular ulcerated mass.



Postinflammatory polyps (previously calledpseudopolyps) secondary to prolonged andintense mucosal regeneration may be seen invarying sizes and configurations (16). They havebeen reported to occur in up to 15% of cases ofgranulomatous colitis (2). Rare reports of the

Figure ISAThis double contrast barium enema reve-als an annular, constricting, “apple core”type of lesion of the ascending colon.

giant overgrowth of these polyps, sometimesleading to obstruction, can be found (13). In oneof our patients, a large, bulky mass of polypssimulated an apple core lesion of the ascendingcolon (Figure 15A). Close inspection revealed thetrue polypoid nature of this lesion (Figure 15B).

-S

C

30aa

3

I;


Volume 8, Number 2 #{149}March, 1988 #{149}RadloGraphics 271

In another patient, a large, intraluminal, ulcerated mass was seenin the rectum associated with abnormal rectal mucosa (Figure 16). Clin-ically, this was thought to be a rectal carcinoma. Subsequent surgeryrevealed it to be a penetrating ulcer and inflammatory mass second-ary to Crohn’s disease affecting the entire rectum.

Figure 16A frontal view from a barium enema shows alarge intraluminal mass arising from the rightlateral wall of the rectum. A large central ulcer-ation is noted within it. The entire rectal vault isnarrowed and the mucosal contour is very ir-regular. Surgical exploration revealed a deepulcer with a large inflammatory mass.

I

‘1

,�



Obstruction and Dilatation

The transmural nature of the inflammationand associated fibrosis may lead to obstructionin Crohn’s disease. Rarely intussusception is seen(Figure 17). Intussusception in Crohn’s disease isusually seen in the postoperative period (12). In-tussusceptions usually are jejunojejunal in typeand are secondary to chronic dilatation relatedto long standing obstruction. In our case, a moredistal ileocolonic intussusception was seen.There was no history of previous surgery and noleading mass was identified.

Enterolith formation depends on stasis, usuallyproximal to an obstruction or in a diverticulumor pseudodiverticulum. Because both true and

false diverticula may be found in Crohn’s dis-ease, these patients are at risk for enteric stoneformation. In one patient, stone formation re-suIted from the presence of multiple sites offocal narrowing (Figures 18A and B).

Asymmetric dilatation may occur on theantimesenteric border of the small bowel sec-ondary to fibrosis on the mesenteric border withresulting loss of pliability (17) (Figure 19). Thisasymmetric involvement can be seen in approx-imately 25% of the cases of small bowel disease.In one third of these (8% of the total), asymmetricdilatation leads to sacculation of the antimesen-teric border (10).

Figure 17A coned down view from a singlecontrast barium enema shows arounded mass in the ascending colonwith just a hint of a “coiled spring” ap-pearance. This represented the leadpoint of an ileocolic intussusception.A small bowel examination (notshown) revealed evidence of Crohn’sdisease with thickening of the bowelwall but no mass.

This upright abdominal radiograph shows an ovoid soft A small bowel series reveals the smooth ovoid defect totissue density within a dilated loop of small bowel in the be within a dilated ileal loop. It is completely outlined byright lower quadrant. barium and has no apparent point of attachment. This

represents a totally intraluminal mass consistent with anenterolith. Adjacent areas of ileitis can be seen.


Volume 8, Number 2 #{149}March, 1988 ‘ RadioGraphics 273

Figure 19This small bowel examination shows a giant sacculationwith a relatively short base, representing a pseudodiver-ticulum ofthe ileum. Strictures and a “cobblestone” mucosasecondary to Crohn’s disease are seen immediately proxi-mal and distal to the pseudodiverficulum. The sacculationis along the antimesenteric border opposite the less dis-tensible and more fibrotic mesenteric margin. (Courtesyof D. Faegenburg, M.D., Mineola, NY)

0

Ia03a3

a.

I

Summary



C

:� Toxic megacolon is esti-

� mated to occur approximately.� four times more commonly in

a ulcerative colitis than in Crohn’s� colitis (8). Toxic megacolon� occurred as the first manifes-

tatlon of Crohn’s disease in 11of 12 patients in one series,however (21) (Figure 20).

Figure 20A supine abdominal radiographshows a dilated large bowel withprominent haustrations in the ascend-ing and transverse portions of thecolon. These findings, in the appropri-ate clinical setting, are consistent withtoxic megacolon.

Unusual manifestations of common diseases are still relatively com-mon events. Crohn’s disease may involve the entire gastrointestinal tractfrom the pharynx to the anus. Although the classic findings of ileocolicdisease are well known, the changes described above are less com-monly encountered. They may be subject to misdiagnosis unless theprotean manifestations of Crohn’s disease are kept in mind.



References

1. Amendola MA Agha FP, Dent TL, Amendola Be, ShineziKK. Detection of occult colovesical fistula by the BounneTest. MR 1984; 142:715-717.

2. Bernstein JR. Ghahremani GG. Paige ML. Rosenberg JL.Localized giant pseudopolyposis of the colon in ulcera-tive and granulomatous colitis. Gastrointest Radiol 1978;3:431-435.

3. Farman J, Faegenburg D. Dallemand D. Chen CK.

Crohn’s disease of the stomach: the “ram’s horn’ sign.Am J Roentgenol Radium Then NucI Med 1975; 123:242-251.

4. Feczko PJ. Malignancy complicating inflammatorybowel disease. Radiol Clin North Am 1987; 25:157-174.

5. Goldberg HI. Caruther SB Jr. Nelson JA Singleton JW.Radiographic findings of the National CooperativeCrohn’s Disease Study. Gastroenterology 1979; 77:925-937.

6. Goldman SM, Fishman EK Gatewood 0MB, Jones B,Siegelman 55. CT in the diagnosis of enterovesical fis-tulae. AiR 1985; 144:1229-1233.

7. Gone PM. Cross-sectional imaging of inflammatorybowel disease. Radiol Clin North Am 1987; 25:115-131.

8. Greenstein AJ, Sachar D, Gibas A et al. Outcome of toxicdilatation in ulcerative colitis and Cnohn’s colitis. J OlinGastroenterol 1985; 7:137-143.

9. Greenstein AJ, Sachar D, Pucillo A et al. Cancer inCrohn’s disease after diversionary surgery: A report ofseven carcinomas occurring in excluded bowel. Am JSurg 1978; 135:86-90.

10. Herlinger H. The small bowel enema and the diagnosisof Crohn’s disease. Radiol Clin North Am 1982; 20:721-742.

11. Henlingen H, O’Riordan D. Saul 5, Levine M. Nonspecificinvolvement of bowel adjoining Crohn disease. Radiology1986; 159:47-51.

12. Hertz I, Train J. Keller R, Slate G, Greenstein A. Adult post-operative enteroenteric intussusception in Cnohn’s dis-ease. Gastrointest Radiol 1982; 7:131-134.

13. Jones B. Abbruzzese AA Obstructing giant pseudopolypsin granulomatous colitis. Gastrointest Radiol 1978; 3:437-

438.14. Korelilz BI. Carcinoma of the intestinal tract in Crohn’s

disease: Results of a survey conducted by the NationalFoundation for Ileitis and Colitis. Am J Gastroenterol 1983;78:44-46.

15. Levine MS. Crohn’s disease of the upper gastrointestinaltract. Radiol Clin North Am 1987; 25:79-91.

16. Lichtenstein JE. Radiologic-pathologic correlation of in-flammatory bowel disease. Radiol Clin North Am 1987;25:3-24.

17. Meyers MA The small bowel: Normal and pathologicanatomy. In: Meyers MA Dynamic radiology of the ab-domen. 2d ed. New York: Springer. 1982; 277-280.

18. Nelson SW. Some interesting and unusual manifestationsof Crohn’s disease (“regional entenitis”) of the stomach,duodenum and small intestine. Am J Roentgenol RadiumThen NucI Med 1969; 107:86-101.

19. Stevenson GW, Laufer I. Duodenum. In: Laufer I, ed. Doublecontrast gastrointestinal radiology, 2d ed. New York:Springer. 1982; 356-357.

20. Tishlen JMA Helman CA. Crohn’s disease of theesophagus. J Can Assoc Radiol 1984; 35:28-30.

21. Whorwell PJ, lsaacson P. Toxic dilatation of colon inCrohn’s disease. Lancet 1981; 2:1334-1336.

radlooraphics indexterms: crohn’sdisease: lesscommon

Documents