HEPATIC ANGIOGRAPHY IN ULCERATIVE COLITIS AND CROHN S DISEASE

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1 Am 7 Roentgenol 126: , 2976 HEPATIC ANGIOGRAPHY IN ULCERATIVE COLITIS AND CROHN S DISEASE ABSTRACT: LEIF EKELUND, ANDER5 LUNDERQUIST,1 HANS DENCKER,2 AND MANS AKERMAN Liver angiography was performed in 13 patients with Crohn s disease and three with ulcerative colitis. Of these patients, 13 underwent liver biopsy, and findings were correlated with results of angiography and biochemical tests. Twelve liver biopsies were abnormal, primarily showing fatty infiltration and reactive hepatitis. Thirteen angiographies were abnormal, with widened and tortuous liver arteries being the most common finding. Liver function tests were within normal limits for all but three of the i6 patients, thus correlating poorly with findings of the other tests. These data show that angiography is useful in detecting hepatic abnormality, but evaluation with liver biopsy is necessary to determine the nature of the lesion. Recently a number of reports concerning hepatobiliary disease associated with ulcerative colitis and Crohn s disease have been published [i-6]. Fatty changes, pericholangitis, hepatic granulomata, amyloidosis, increased fibrosis, and cirrhosis are the most frequently reported lesions. A thorough survey of the hepatic changes in Crohn s disease and ulcerative colitis is given by Perrett et al. [., 5]. However, to our knowledge no reports on angiographic findings have been published. When patients with Crohn s disease and ulcerative colitis were referred for angiographic evaluation of the extent of the inflammatory lesions, we therefore thought it worthwhile to extend the study to the liver. MATERIALS AND METHODS Three patients with ulcerative colitis and 13 with Crohn s disease were examined. Six were males and io were females; ages ranged from i6 to 57 years. The diagnosis was verified in all cases by histological examination. The extent and site of the lesions in the 13 patients with Crohn s disease are given in table. For the three patients with ulcerative colitis, radiological evidence indicated involvement of the entire colon. In another four patients with supplemental arterial supply to the liver from the superior mesenteric artery, this accessory artery was also catheterized. A radiopaque catheter (ID/OD = 1.4/2.2 mm) was used in all examinations, and the contrast medium (Isopaque Coronar, Nyco, Norway) was injected at a rate of mi/sec, depending on the size of the catheterized artery. In evaluating the angiograms, attention was paid to size of liver and spleen, caliber of common hepatic and splenic artery as well as intrahepatic branches, tortuosity of intrahepatic arteries, density of hepatogram, visualization of veins, and eventual signs of portal hypertension. A liver biopsy was performed in 13 of the patients. Five patients had a large needle histological biopsy and the other eight a fine needle aspiration biopsy for cytologic analysis. Hepatic Angiograp/zy RESULTS The angiographic findings are summarized in table 2. All 13 patients with Crohn s disease had some type of angiographic abnormality. Five had liver enlargement and one had decreased liver size, while three patients had enlarged spleens. In eight patients the diameter of the common hepatic artery was larger than or equal to that of Selective angiography of the celiac axis was performed in all patients, followed by catheterization of the common hepatic artery in four. hepatic flow, and six of these patients the splenic artery, indicating an increased also Department of Diagnostic Radiology, University of Lund, Lund, Sweden. 2 Department of Surgery, University of Lund, Lund, Sweden. 3 Department of Pathology, University of Lund, Lund, Sweden. 952

2 HEPATIC ANGIOGRAPHY IN COLITIS AND CROHN S DISEASE 953 TABLE i EXTENT ANDS1TE OF LESIONS IN PATIENTS WITH CROHN S DISEASE Site No. Patients Terminal ileum and caecum 5 Terminal ileum 3 Multiple small intestinal lesions 3 Extensive colonic involvement 2 had widened intrahepatic arteries. Seven patients had increased tortuosity of intrahepatic arteries, while five had nonhomogeneous hepatograms (fig. i). In i 2 cases the portal and splenic veins appeared normal; in one case these veins were widened. Retrograde flow in the gastroduodenal artery was demonstrated in one case in which widening of the hepatic artery was also present. Stenosis of the celiac artery was found in one case. Of the patients with ulcerative colitis, one had a normal hepatic angiogram, except for a slight stenosis of the common hepatic artery which could be due to spasm. The second had normal liver size but enlargement of the spleen. Intrahepatic arteries were tortuous and the hepatogram was nonhomogeneous. The hepatic vein was visualized in spite of injection into the ANGIOGRAPHIC TABLE 2 FINDINGS Finding No. Patients Widening of common hepatic artery. 9 Increased tortuosity of intrahepatic arteries 9 Nonhomogenous hepatogram 7 Widening of intrahepatic arteries... 7 Hepatomegaly 6 Splenomegaly 5 Visualization of hepatic veins 3 Retrograde flow in gastroduodenal artery Portal hypertension with collateral circulation N0TE.-13 patients have Crohn s disease and three have ulcerative colitis. i i FIG. i.-selective common hepatic angiography in 33-year-old woman with Crohn s disease. A, Arterial phase; B, parenchymal phase. Intrahepatic arteries wide and tortuous; nonhomogeneous hepatogram.

3 954 EKELUND ET AL. Fic. 2.-Angiography in 32-year-Old woman with ulcerative colitis since childhood. A, Superior mesenteric angiography showing supplementary artery to enlarged right liver lobe; wide and tortuous intrahepatic arteries. B, Celiac angiography, venous phase. Note splenomegaly with collateral circulation over inferior mesenteric vein indicating portal hypertension. celiac artery in this case. The third patient was a 32-year-old woman who had colitis since she was seven. She developed carcinoma of the transverse colon, and colectomy was performed. At operation portal hypertension was diagnosed, and subsequent angiography demonstrated enlargement of the liver and spleen, widened and tortuous intrahepatic arteries, and signs of portal hypertension (fig. 2). Liver Function Tests Liver function studies including serum bilirubin, bromsuiftalein retention test (BSP), serum alkaline phosphatase, lactic dehydrogenase (LDH), and serum glutamic oxalacetic transaminase (SGOT) were within normal limits in 13 of the i6 patients. In the other three (two with ulcerative colitis and one with Crohn s disease), all liver function tests were abnormal: serum bilirubin, mg/i00 ml; BSP, 20-30%; serum alkaline phosphatase, U; LDH, U; and SGOT, U. Liver Biopsy Of the 13 patients who underwent liver biopsy, only one showed a normal liver. In six cases reactive hepatitis with a more or less pronounced fatty infiltration was noted. Five patients had reactive hepatitis without fatty infiltration, and one patient with ulcerative colitis had cirrhosis. Cholangitis or granulomata were not found. In 10 of 12 patients whose liver biopsies were abnormal, angiography also showed pathological changes (table 3). In one case the biopsy was normal, but angiography showed pathological changes. DISCUSSION Eade and Cooke [2] found inflammatory changes of the liver in about 70% of the patients with ulcerative colitis. According to these authors, cirrhosis develops in 2%- 3% of cases. Mistilis [3] performed 82 aspiration liver biopsies in 49 patients with ulcerative colitis and found pericholangitis to be the most common change, followed by

4 HEPATIC ANGIOGRAPHY IN COLITIS AND CROHN S DISEASE 55 TABLE 3 CORRELATION BETWEEN HEPATIC ANGIOGRAPHY, LiVER Biopsy, AND LIVER FuNcrIoN TESTS No. LIVER FUNC- ANGIOGRAPHY Bsosv TION TESTS PATIENTS N.D I I I I I 1* I I... I 1* I.... I I I I... I N0TE.-+ = pathological; - = normal; N.D.= not done. S Only splenomegaly, otherwise normal. active chronic hepatitis. Severe fatty liver degeneration was uncommon during life but was the most common postmortem finding. Thorpe et al. [6] described four cases of primary sclerosing cholangitis associated with ulcerative colitis. Similar changes associated with Crohn s disease have been reported as well. Thus Eade et a!. [ i] found abnormalities in i8 of2o operative biopsies (90%), with 75% showing more than minor changes. Cirrhosis, amyloidosis, and multiple hepatic granulomata were also found. Perrett Ct a!. [] studied clinical, hematological, biochemical, bacteriological, histological, and immunological data of 100 patients with Crohn s disease. Of 3 patients who underwent liver biopsy, 9 had pathological specimens, with fatty change and pericholangitis being the most common findings. The liver changes referred to above can explain the angiographic findings in our patients. All 13 patients with Crohn s disease and two of three with ulcerative colitis had angiographic abnormali ties. I ncreased blood flow with dilated arteries is a common finding in inflammatory lesions. Widening of the common hepatic artery (ratio of the diameters of the common hepatic artery and the splenic artery I [8]) as well as intrahepatic branches, indicating increased blood flow to the liver, may also be present in cases of malignant tumors of the liver [8]. Increased tortuosity of intrahepatic arteries was also a fairly common finding in our material (nine of i6 cases), but the pathologic significance may be uncertain, at least in older age groups [8]. However, i I of our patients were under the age of 40. Nonhomogeneous hepatograms (seen in seven of our patients) may indicate a scattered distribution of liver changes, which is also reported in histological examinations [2]. This may explain why liver biopsy can fail to demonstrate abnormality. In this study, however, angiographic abnormalities were found at about the same frequency as pathological changes at biopsy. Angiography may thus suggest hepatic abnormality, but further evaluation with liver biopsy is necessary to determine the nature of the lesion. Regarding the efficiency of laboratory tests, Dyer and Dawson [] found that i 6 of 62 patients (26%) with Crohn s disease had elevated serum level of alkaline phosphatase and 22 of38 patients (8%) showed impaired excretion of BSP. Eade et al. [, ] found a poor correlation between biochemical and histological findings in their patients with Crohn s disease, which is in accordance with our results. In our material only three of 16 patients had abnormal liver function tests. The genesis of the hepatic changes seen in connection with ulcerative colitis and Crohn s disease is unclear. Portal bacteremia has been found in 24% of patients with ulcerative colitis at the time of colectomy [7], and this may be a triggering factor. One point of theoretical interest is the reported release of bradykinin from inflammatory tissue [io, i i]. This might explain the widening of the hepatic artery and its branches, since bradykinin is known to be a potent vasodilator. REFERENCES I. Eade MN, Cooke WT, Williams JA: Liver disease in Crohn s disease. Scand 7 Gastroenterol 6: , Eade MN, Cook WT: Hepatobiliary disease associated with ulcerative colitis. Postgrad Med 53: , 1973

5 956 EKELUND ET AL. 3. Mistilis SP: Pericholangitis and ulcerative colitis. Ann Intern Med 63:1-I 6, Perrett AD, Higgins G, Johnston HH, Massarella GR, Truelove SC, Wright R: The liver in Crohn s disease. Q 7 Med ig8 : , Perrett AD, Higgins G, Johnston HH, Massarella GR, Truelove SC, Wright R: The liver in ulcerative colitis. Q7Med 158: , Thorpe MEC, Scheuer PJ, Sherlock 5: Primary sclerosering cholangitis in the biliary tract, and ulcerative colitis. Gut 8 : , Eade MN, Cooke WT, Brooke BN: Liver disease in Crohn s disease. A study of 21 consecutive patients having colectomy. Ann Intern Med 74: , Lunderquist A: Arterial segmental supply of the liver. An angiographic study. Acta Radiol[Suppl] (Stockh) 272 :36, 70, Dyer NH, Dawson AM: The incidence and significance of liver dysfunction in Crohn s disease. Digestion 5: , Haverback BJ: Vasoactive substances and the gastrointestinal tract. Gastroenterolog,y , 1967 II. Lewis GP: Bradykinin. Nature 192 : , 1961

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