Marked Eosinophilia as the First Manifestation of Sclerosing Cholangitis
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1 CASE REPORT Marked Eosinophilia as the First Manifestation of Sclerosing Cholangitis Katsuhiko Horiuchi 1, Satoru Kakizaki 2, Takashi Kosone 1, Takeshi Ichikawa 2,KenSato 2, Hitoshi Takagi 2, Masatomo Mori 2, Shinji Sakurai 3 and Toshio Fukusato 4 Abstract We encountered a 45-year-old man who presented with marked eosinophilia as the first manifestation of sclerosing cholangitis. He was found to have a liver dysfunction during a regular physical check up and thereafter consulted our hospital. The laboratory data on admission indicated an elevation of AST (96 IU/L), ALT (136 IU/L) and ALP (1,025 IU/L). Furthermore, the leukocyte count was 18,190/mm 3 and he also showed marked eosinophilia (54.5%, 9,914/mm 3 ). There were no atypical findings in the eosinophils. Other diseases causing eosinophilia, including parasite infection, allergic disorders, hypereosinophilic syndromes, drug-induced eosinophilia, malignancies, etc. were all investigated and ruled out. A liver biopsy revealed marked eosinophilic infiltration in the portal area and interlobular bile duct injury. Magnetic resonance cholangiopancreatography (MRCP) demonstrated a slight dilatation of the left intrahepatic bile ducts, but no clear diagnosis could be made at that time. A follow-up liver biopsy and endoscopic retrograde cholangiopancreatography (ERCP) finally revealed a diagnosis of secondary sclerosing cholangitis due to eosinophilic cholangiopathy. According to previous Japanese reports, eosinophilia of more than 5% was reported in 39 of 142 (27.0%) primary sclerosing cholangitis (PSC) patients. Eosinophilic cholangiopathy could cause a condition mimicking PSC and it might be confused as PSC with eosinophilia. The literature contains only about 40 case reports on eosinophilic cholangiopathy, and therefore, to date little attention has been paid to this condition. We should therefore pay attention to this condition when making a differential diagnosis of either PSC or IgG4-related sclerosing cholangitis. Key words: eosinophilic cholangiopathy, eosinophilia, sclerosing cholangitis, liver biopsy (Inter Med 48: , 2009) () Introduction Primary sclerosing cholangitis (PSC) is a rare, chronic cholestatic liver disease characterized by the destruction of the intrahepatic and/or extrahepatic bile ducts through chronic inflammation and fibrosis, thus leading to biliary complications, including bile stasis, and cirrhosis (1, 2). The cause of PSC is unknown, and even though it is thought that the disease may have an autoimmune origin, PSC often responds unfavorably to immunosuppressive therapy (1, 2). Primary sclerosing cholangitis has been thought to be a very rare disease in Japan. However, with more knowledge of the disease, the number of patients diagnosed with PSC recently seems to be increasing (3-7). Furthermore, it has been also revealed that PSC patients in Japan are different from those in foreign countries in various aspects (3-7). Patients with PSC in Japan have two peaks in age distribution, one in their twenties and the other in their fifties and sixties (3). PSC patients in Japan have different characteristics from those in other countries: there is a higher incidence of eosinophilia and positivity for anti-nuclear antibody, less frequent complications with inflammatory bowel diseases, and more frequent complications with chronic pancreatitis (3). Department of Gastroenterology, Kusunoki Hospital, Fujioka, Department of Medicine and Molecular Science, Gunma University Graduate School of Medicine, Maebashi, Department of Tumor Pathology, Gunma University Graduate School of Medicine, Maebashi and Department of Pathology, Teikyo University School of Medicine, Tokyo Received for publication March 2, 2009; Accepted for publication April 29, 2009 Correspondence to Dr. Satoru Kakizaki, kakizaki@showa.gunma-u.ac.jp 1377
2 The incidence of eosinophilia in PSC patients in other countries is rare and tends to be around 5% (8). In contrast, in Japan the incidence of eosinophilia is reported to be 27% of PSC patients (3). Primary sclerosing cholangitis with marked eosinophilia, such as that observed in the present case have also been described as case reports (9-11). However, the pathoetiological significance of eosinophils in PSC remains to be elucidated. Eosinophilic cholangiopathy is one of the causes of sclerosing cholangitis (12-16). However, the literature contains only about 40 case reports on eosinophilic cholangiopathy (15-17), and therefore, to date little attention has been paid to this condition. Miura et al (18) recently reported eosinophilic cholangiopathy presenting with secondary sclerosing cholangitis (SSC) mimicking our case. Sclerosing cholangitis from eosinophilic cholangiopathy is sometimes difficult to differentiate from PSC because PSC patients in Japan have a higher incidence of eosinophilia (3). The establishment of the concept of IgG4-related sclerosing cholangitis accompanying autoimmune pancreatitis has provided a solution for the question of the different clinical characteristics of PSC between Western countries and Japan, except for the higher incidence of eosinophilia in Japan (19, 20). A precise study of cases with eosinophilic cholangitis and PSC with eosinophilia may therefore bring new insight into the pathoetiology of PSC in Japan. We encountered a case of secondary sclerosing cholangitis complicated with marked eosinophilia as the first manifestation and herein report our findings. Case Report A 45-year-old man was pointed out to have a liver dysfunction during a physical check up and thereafter consulted Kusunoki Hospital. The laboratory data on admission indicated elevated levels of aspartate aminotransferase (AST), 96 IU/L (normal range, IU/L), alanine aminotransferase (ALT) 136 IU/L (5-40 IU/L) and alkaline phosphatase (ALP) 1,025 IU/L ( IU/L). Furthermore, the leukocyte count was 18,190/mm 3 and thus showed marked eosinophilia (54.5%, 9,914/mm 3 ). Other laboratory tests showed an erythrocyte count of /mm 3 (normal: /mm 3 ), hemoglobin 15.8 g/dl ( g/dl), platelet count /mm 3 ( /mm 3 ), serum albumin 4.5 g/dl ( g/dl), total bilirubin (T-Bil) 0.7 mg/ml ( mg/ml), amylase 112 IU/L ( IU/L), gamma-glutamyltransferase 406 IU/L (<70 IU/L), blood urea nitrogen (BUN) 15.5 mg/dl ( mg/dl), and creatinine (Cr) 0.7 mg/dl ( mg/dl). Hepatitis B surface antigen and hepatitis C virus antibody were negative. Anti-nuclear antibody (ANA) and anti-mitochondrial antibody (AMA) were negative. Immunoglobulin G (IgG) was 1,400 mg/dl, immunoglobulin M (IgM) was 82 mg/dl, immunoglobulin E (IgE) was 13 IU/mL, IgG4 was 7.58 mg/ dl. Bone marrow aspiration showed an increase of morphologically normal eosinophils. There were no atypical findings in the eosinophils. Other diseases causing eosinophilia including parasite infection, allergic disorders, hypereosinophilic syndromes, drug-induced eosinophilia, malignancies, etc. were all ruled out. The patient did not receive any supplements or alternative medicines. Abdominal computed tomography (CT) revealed gall bladder wall swelling and a slight dilatation of the intrahepatic bile ducts (Fig. 1AB) and chest CT showed no abnormality. Magnetic resonance cholangiopancreatography (MRCP, Fig. 1C) demonstrated a slight dilatation of left intrahepatic bile ducts and strictures of the hilar hepatic bile ducts, but no clear diagnosis could be made at that time. Colonoscopy revealed no abnormal findings such as inflammatory bowel disease (IBD). A liver biopsy revealed marked eosinoplilic infiltration in the portal area and interlobular bile duct injury (Fig. 2). Intralobular necrosis was rare and no granulomas were observed. Figure 3 showed the clinical course of this patient. Although a definitive diagnosis could not be made, ursodeoxycholic acid (UDCA) was administered because of the patient s liver dysfunction and elevated biliary enzyme levels. As a result, the serum aminotransferase levels transiently decreased and eosinophilia improved to the normal range. However, the aminotransferase levels thereafter increased again, while the eosinophils were slightly increased to 10.8% (696/mm 3 ). A second liver biopsy (Fig. 4) showed decreased eosinophil infiltration in comparison to the findings of the first liver biopsy. Therefore, the infiltrated cells changed to lymphocytes. Bile duct injury and marked fibrosis around the bile ducts were observed, and the number of interlobular bile ducts was decreased. Endoscopic retrograde cholangiopancreatography (ERCP) revealed sclerosing, narrowing and diffuse obstruction compatible with sclerosing cholangitis (Fig. 5). We therefore finally diagnosed this case as secondary sclerosing cholangitis complicated with eosinophilic cholangiopathy. Additional medication with bezafibrate in combination with UDCA eventually normalized the aminotransferase levels (Fig. 3). A follow-up liver biopsy also showed decreased eosinophilic infiltration, a decreased number of interlobular bile ducts and marked fibrosis (Fig. 6). Discussion We herein describe a case of sclerosing cholangitis complicated with marked eosinophilia as the first manifestation. Sclerosing cholangitis is classified into two entities: PSC and SSC (13, 21). Secondary sclerosing cholangitis is morphologically similar to PSC but it originates from a known pathological process. It includes IgG4-related autoimmune pancreatitis, eosinophilic cholangitis, intraductal stone disease, surgical or blunt abdominal trauma, and intra-arterial chemotherapy, etc. (13, 21). Eosinophilic cholangiopathy is one of the causes of sclerosing cholangitis (12-16). However, the literature contains only about 40 case reports on eosinophilic cholangiopathy (15-17), and therefore, little at- 1378
3 Figure1. Abdominalcomputedtomography(CT)andmagneticresonancecholangiopancreatog raphy(mrcp)findings.a,bctrevealedgalbladderwalswelingandslightdilatationofintra hepaticbileducts.c MRCPdemonstratedaslightdilatationofleftintrahepaticbileductsand stricturesofthehilarhepaticbileducts,butnocleardiagnosiscouldbemadeatthattime. Figure2. Histopathologicalfindingsofthefirstliverbiopsyspecimen.A liverbiopsyrevealed markedeosinophilicinfiltrationintheportalareaandinterlobularbileductinjury.intralobular necrosiswasrareandnogranulomaswereobserved.a)azan-malorystaining.b,c)hematoxylin andeosinstaining. 1379
4 Figure3. Clinicalcourseofthepatient.Theadministrationofursodeoxycholicacid(UDCA) transientlyloweredtheserum aminotransferaselevelsandnormalizedtheeosinophilia.however, theaminotransferaselevelsthereafterbecameelevatedagain.additionalmedicationwithbezafi bratetoudcanormalizedtheaminotransferaselevels. Figure4. Thehistopathologicalfindingsofthesecondliverbiopsyspecimen.A liverbiopsy showeddecreasedeosinophilinfiltrationincomparisonwiththefirstliverbiopsy.theinfiltrating celswerelymphocytes.bileductinjuryandmarkedfibrosisaroundthebileductswereobserved. Interlobularbileductsweredecreased.A)Azan-Malorystaining.B,C)HematoxylinandEosin staining. tention has been paid to this condition. It is characterized by dense transmural eosinophilic infiltration of the biliary tract. Miura et al (18) recently reported eosinophilic cholangiopathy presenting with SSC mimicking the present case. In their case, marked eosinophilic infiltration was seen in the gallbladder wall but not in the liver biopsy specimen mimicking our second and third liver biopsy findings. Their case resembles our case in the CT findings with gall-bladder wall 1380
5 Figure5. Endoscopicretrogradecholangiopancreatography(ERCP)findings.ERCP revealed sclerosing,narrowinganddifuseobstructioncompatiblewithsclerosingcholangitis. Figure6. Thehistopathologicalfindingsofthethird liverbiopsyspecimen.a liverbiopsy showeddecreasedeosinophilinfiltration,anddecreasedinterlobularbileducts.markedfibrosis wasobserved.a)azan-malorystaining.b,c)hematoxylinandeosinstaining. swelling. They diagnosed it to be SSC caused by eosinophilic cholangiopathy based on different criteria from PSC with eosinophilia. Although our case did not undergo any histological analyses of the gall bladder, our case may be classified according to these criteria. Eosinophilic cholangiopathy might sometimes be confused with PSC associated with eosinophilia. Confirmation thus depends on further investigations. The pathogenesis of eosinophilia in PSC or SSC is still unknown. However, previous reports showing eosinophilic infiltration in the liver of the patients with PSC (9-11) and primary biliary cirrhosis (PBC) (22) may explain a relationship to the pathology of these diseases. Foong et al (23) reported a patient with eosinophil-induced chronic active hepatitis in the idiopathic hypereosinophilic syndrome, suggesting that hepatocytes are the target of damage caused by the release of a cationic eosinophil granule protein, such as major basic protein (MBP). Furthermore, activated eosinophils were reported to produce not only MBP but also various cytokines including transforming growth factor beta (24). These cytokines may lead to inflammation and fibrotic changes in the wall of the bile ducts. Eosinophils also play an important role in the fibrotic conditions of different etiopathologies, including endomyocardial fibrosis, 1381
6 scleroderma and scleroderma like-conditions, idiopathic pulmonary and retroperitoneal fibrosis, asbestos-induced lung fibrosis, wound repair, and tissue remodeling (25, 26). Uchida et al (27) reported that four of 7 PSC patients had unclassified or eosinophilic colitis. These relationships between PSC and eosinophilic colitis may explain the role of eosinophils in the pathogenesis of PSC or SSC. Although not a study of PSC, Terasaki et al (22) described that eosinophilic infiltration of the portal tracts may play a role in immunological injuries of the interlobular bile ducts in primary biliary cirrhosis (PBC). A considerable number of eosinophils were found in the portal tracts in 51 of 176 patients with PBC (29%), whereas this finding occurred in only 2 of 50 (4%) specimens from patients with viral chronic active hepatitis (22). The present patient underwent sequential liver biopsies. At the first biopsy, marked eosinophil infiltration was observed. However, the infiltrating cells were lymphocytes at the follow-up biopsy. Watanabe et al (10) reported a case of PSC with marked eosinophilic infiltration in the liver. In their case, a marked infiltration of eosinophils in the portal area was only observed at the onset of the disease and it was not observed at a follow-up biopsy performed 11 years after onset (10). It therefore would appear that the eosinophilia and the eosinophilic infiltration in the liver observed at the onset of the disease can be explained in terms of the relationship to the pathology of PSC or SSC. In conclusion, we herein described a case of sclerosing cholangitis complicated with marked eosinophilia as the first manifestation. Eosinophilic cholangiopathy could cause a condition mimicking PSC and it might be confused as PSC with eosinophilia. To date there are only about 40 case reports on eosinophilic cholangiopathy, and therefore, little attention has been paid to this condition. We should therefore play close attention to this condition when making a differential diagnosis of either PSC, or IgG4-related sclerosing cholangitis. Although confirmation requires further investigation, the new entitity of SSC with eosinophilic cholangiopathy may bring new insight into the pathoetiology of sclerosing cholangitis. References 1. Tischendorf JJ, Hecker H, Krüger M, Manns MP, Meier PN. Characterization, outcome, and prognosis in 273 patients with primary sclerosing cholangitis: A single center study. Am J Gastroenterol 102: , LaRusso NF, Shneider BL, Black D, et al. Primary sclerosing cholangitis: summary of a workshop. Hepatology 44: , Takikawa H. Recent status of primary sclerosing cholangitis in Japan. J Hepatobiliary Pancreat Surg 6: , Takikawa H, Manabe T. Primary sclerosing cholangitis in Japan analysis of 192 cases. J Gastroenterol 32: , Tanaka A, Takamori Y, Toda G, Ohnishi S, Takikawa H. Outcome and prognostic factors of 391 Japanese patients with primary sclerosing cholangitis. Liver Int 28: , Takikawa H. Characteristics of primary sclerosing cholangitis in Japan. Hepatol Res 37: S470-S473, Takikawa H, Takamori Y, Tanaka A, Kurihara H, Nakanuma Y. Analysis of 388 cases of primary sclerosing cholangitis in Japan; Presence of a subgroup without pancreatic involvement in older patients. Hepatol Res 29: , Wiesner RH, Porayko MK, LaRusso NF, Ludwig J. Primary sclerosing cholangitis. In: Diseases of the Liver, seventh edn. Schiff L, Schiff ER, Eds. Lippincott, Philadelphia, 1993: Shimomura I, Takase Y, Matsumoto S, et al. Primary sclerosing cholangitis associated with increased peripheral eosinophils and serum IgE. J Gastroenterol 31: , Watanabe H, Ohira H, Kuroda M, et al. Primary sclerosing cholangitis with marked eosinophilic infiltration in the liver. J Gastroenterol 30: , Grauer L, Padilla VM 3rd, Bouza L, Barkin JS. Eosinophilic sclerosing cholangitis associated with hypereosinophilic syndrome. Am J Gastroenterol 88: , Butler TW, Feintuch TA, Caine WP Jr. Eosinophilic cholangitis, lymphadenopathy, and peripheral eosinophilia: a case report. Am J Gastroenterol 80: , Abdalian R, Heathcote EJ. Sclerosing cholangitis: a focus on secondary causes. Hepatology 44: , Rosengart TK, Rotterdam H, Ranson JH. Eosinophilic cholangitis: a self-limited cause of extrahepatic biliary obstruction. Am J Gastroenterol 85: , Matsumoto N, Yokoyama K, Nakai K, et al. A case of eosinophilic cholangitis: imaging findings of contrast-enhanced ultrasonography, cholangioscopy, and intraductal ultrasonography. World J Gastroenterol 13: , Duseja A, Nada R, Dhiman RK, et al. Eosinophilic cholangiopathy--a case report. Dig Dis Sci 50: , Vauthey JN, Loyer E, Chokshi P, Lahoti S. Case 57: eosinophilic cholangiopathy. Radiology 227: , Miura F, Asano T, Amano H, et al. Resected case of eosinophilic cholangiopathy presenting with secondary sclerosing cholangitis. World J Gastroenterol 15: , Kamisawa T, Egawa N, Tsuruta K, Okamoto A, Funata N. Primary sclerosing cholangitis may be overestimated in Japan. J Gastroenterol 40: , Nishino T, Oyama H, Hashimoto E, et al. Clinicopathological differentiation between sclerosing cholangitis with autoimmune pancreatitis and primary sclerosing cholangitis. J Gastroenterol 42: , Gossard AA, Angulo P, Lindor KD. Secondary sclerosing cholangitis: a comparison to primary sclerosing cholangitis. Am J Gastroenterol 100: , Terasaki S, Nakanuma Y, Yamazaki M, Unoura M. Eosinophilic infiltration of the liver in primary biliary cirrhosis: a morphological study. Hepatology 17: , Foong A, Scholes JV, Gleich GJ, Kephart GM, Holt PR. Eosinophil-induced chronic active hepatitis in the idiopathic hypereosinophilic syndrome. Hepatology 13: , Wong DT, Elovic A, Matossian K, et al. Eosinophils from patients with blood eosinophilia express transforming growth factor beta 1. Blood 78: , Noguchi H, Kephart GM, Colby TV, Gleich GJ. Tissue eosinophilia and eosinophil degranulation in syndromes associated with fibrosis. Am J Pathol 140: , Levi-Schaffer F, Garbuzenko E, Rubin A, et al. Human eosinophils regulate human lung- and skin-derived fibroblast properties in vitro: a role for transforming growth factor beta (TGF-beta). Proc Natl Acad Sci USA 96: , Uchida N, Ezaki T, Fukuma H, et al. Concomitant colitis associated with primary sclerosing cholangitis. J Gastroenterol 38: , The Japanese Society of Internal Medicine
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