Overview of Diagnostic Criteria for Autoimmune Pancreatitis
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1 2007 년도대한췌담도학회추계학술대회 Session II: Comparison of Diagnostic Criteria for AIP: Japan, USA & Korea Overview of Diagnostic Criteria for Autoimmune Pancreatitis Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Korea Ji Kon Ryu, M.D. Introduction 1n 1995, Yoshida et al. 1 summarized the clinical features of several patients with unusual chronic pancreatitis showing diffuse irregular narrowing of main pancreatic duct and proposed the concept of autoimmune pancreatitis (AIP). Thereafter, many cases of AIP have been reported in Western countries as well as Japan. In Korea, 1 st case of AIP was reported in and AIP is increasingly being reported. 3 The increments probably seems to be due to the growing awareness of the disease entity rather than a rise of the true incidence. According to the multicenter nationwide study in Korea, AIP was 2.0% among 814 patients with chronic pancreatitis. 4 For the past four decades, various morphologic descriptions have been proposed to characterize this disease: nonalcoholic duct-destructive chronic pancreatitis, lymphoplasmacytic sclerosing pancreatitis with cholangitis, chronic sclerosing pancreatitis, pseudotumorous pancreatitis, and duct-narrowing chronic pancreatitis. Recently, the term autoimmune pancreatitis has become widely accepted, although it is apparent that AIP is a heterogeneous disease. Although, Japan Pancreas Society proposed the diagnostic criteria for the first time in 2002, 5 the diagnosis of AIP is still challenging. Recently, several other diagnostic criteria were proposed as followings: revised proposal of JPS criteria 2006, 6 HISORt criteria by Mayo Clinic, 7 Kim s criteria, 8 Massachusetts General Hospital criteria. 9 So, the new diagnostic criteria which lead to less inter-observer variation and provide a strong base for the research with worldwide consensus are necessary. Historical Background of AIP In 1961, pancreatitis associated with hypergammaglobulinemia was first reported and autoimmunity was suggested as a pathogenetic mechanism. 10 Since then, there were several worldwide case reports about unusual chronic pancreatitis with extrapancreatic manifestations suggesting the possibility of AIP However, they did not have the concept of AIP and various terminology were used such as lymphoplasmacytic sclerosing pancreatitis with cholangitis, chronic sclerosing pancreatitis in Sjogren's syndrome, pseudotumor of the pancreas associated with retroperitoneal fibrosis with a dramatic response to corticosteroid therapy. After all, Yoshida et al. summarized the clinical features of several patients with unusual chronic pancreatitis showing diffuse irregular narrowing of main pancreatic duct and proposed the concept of AIP in 1995, for the first time. 1 In 1997, Ito T also reported three cases of AIP with effective steroid therapy, 14 and Irie H described CT and MR imaging characteristics in patients with AIP as diffuse pancreatic enlargement and capsule like rim in Since then, some European authors also reported 105
2 년도대한췌담도학회추계학술대회 the several cases with unusual chronic pancreatitis as a non-alcoholic duct destructive chronic pancreatitis and accepted the concept of AIP In 2000, Okazaki K studied the association of autoantibody and AIP in 17 patients and reported that more than one autoantibody such as antinuclear Ab, antilactoferrin Ab, anti-carbonic anhydrase II Ab was observed in all patients. 19 His study suggested that an autoimmune mechanism against carbonic anhydrase-ii or lactoferrin might be involved in AIP. In 2001, Japanese researchers have carefully studied the changes in immunoglobulin levels in AIP patients. They found a distinctive rise in serum IgG4 levels and an elevation of IgG4 containing immune complexes in the vast majority of patients with AIP. 20 Finally, based on the radiological, serological and pathological features of these patients, Japan Pancreas Society proposed the diagnostic criteria for the first time in In 2001, Whitcomb DC proposed new TIGAR-O classification system based on the etiologic risk factors associated with chronic pancreatitis and TIGAR-O system included AIP as a distinct entity of chronic pancreatitis. 21 There was a 1 st topic discussion session about controversies in clinical pancreatology (Autoimmune Pancreatitis: dose It Exist?) at the American Pancreatic Association meeting November 14, The Japanese, Italian and American doctors presented their experiences about AIP and discussed about the points of consensus and differences. Okazaki K presented the diagnostic criteria of AIP which was proposed by the Japan Pancreas society and Cavallini G talked about the Italian criteria. However, American doctors presented the clinicopathologic features of idiopathic tumefactive chronic pancreatitis. They concluded that the entity of AIP may be an important emerging clinical syndrome and patients presenting with painless obstructive jaundice with markers of autoimmunity, may deserve a short course of corticosteroid before surgical resection. They also expected the agreement of the pathology of AIP and simplification of terminology. Before the proposal of AIP, histopathologic features of chronic pancreatitis usually encountered in practice did not provide information about its etiology. However, in 2003, several American retrospective pathologic studies reported unusual characteristic chronic pancreatitis diagnosed after surgical resection which was clearly different from usual chronic pancreatitis and obstructive pancreatitis The titles were 1) Idiopathic tumefactive chronic pancreatitis: clinical profile, histology, and natural history after resection, 2) Lymphoplasmacytic sclerosing pancreatitis: inflammatory mimic of pancreatic carcinoma, 3) Pancreaticoduodenectomy (Whipple resections) in patients without malignancy: are they all chronic pancreatitis?, 4) Idiopathic chronic pancreatitis with periductal lymphoplasmacytic infiltration. Especially, Mayo Clinic collected retrospectively surgical pathology database underwent pancreatic resection for suspicion of pancreatic cancer owing to a mass and/or obstructive jaundice and on histology were diagnosed to have chronic pancreatitis. 22 They defined such patients as having tumefactive chronic pancreatitis in which three distinct histologic patterns were identified such as typical CP, lymphoplasmacytic sclerosing pancreatitis (LPSP), and idiopathic duct-centric CP (IDCP). Because LPSP had diffuse fibrosis with lymphoplasmacytic infiltration and obliterative phlebitis, they agreed that LPSP was pathologically similar to AIP. However, they only suggested the possibility of AIP and did not use the terminology of AIP. In 2003, European pathologists described the pathological, clinical, and immunological features of AIP based on the 54 patients that were accumulated in Germany, Belgium, and Italy. 26 However, they did
3 Ji Kon Ryu:Overview of Diagnostic Criteria for Autoimmune Pancreatitis 107 not propose the diagnostic criteria of AIP. In 2003, close relationship between autoimmune pancreatitis and multifocal fibrosclerosis was reported by Japanese. 27 They suggested that AIP may not be a simple pancreatitis but one lesion of systemic disease of multifocal fibrosclerosis including sclerosing cholangitis, retroperotoneal fibrosis and Riedel's thyroiditis, fibrotic pseudotumour of the orbit and fibrosis of the salivary glands. In 2006, the concept of IgG4 related autoimmune disease was first proposed by Kamisawa T et al, who showed a number of IgG4 antibody stained plasma cells in number of organs in human body. 28 Kamisawa T insisted that the elevation of serum IgG4 levels and infiltration of abundant IgG4 positive plasma cells into various organs were rather specific to AIP patients. Recently, in 2007, Bjornsson E reviewed the literature about steroid response unusual cholangitis on new emerging clinical entity and suggested that this condition of steroid responsive biliary strictures be named IgG4 associated cholangitis which seemed to have a better prognosis than primary sclerosing cholangitis and were often, but not always, associated with AIP. 29 Many Kinds of Diagnostic Criteria for AIP Because AIP can mimic pancreatic cancer both clinically and radiographically, and because it is responsive to steroid therapy, the goal is to make a diagnosis preoperatively to avoid unnecessary surgery. The overall impact of a missed diagnosis of AIP is not trivial. In one large series, 11 (2.5%) of 442 Whipple resections were for AIP; all were thought to be malignant preoperatively. 24 For the first time, the Japanese published diagnostic criteria in 2002 based on their clinical experience (Fig. 1) The criteria contained three components: pancreatic imaging, laboratory data, and histopathologic findings. At the American Pancreatic Association meeting November 14, 2002, Italian doctor, Giorgio Cavallini presented their own criteria which consisted of histology and cytology, the association with other autoimmune disease, response to steroid therapy. 5 In 2005, Spain group published their own diagnostic criteria using scoring system. The criteria included clinical manifestation, morphologic parameters, laboratory parameters (serum IgG and ANA) and definite diagnosis was made only with histopathology. 30 A total joint score of 0 or 1 was considered probably not AIP, 2 as possible AIP, and 3 as probable AIP. In 2006, four diagnostic criteria were published in Korea, Japan and U.S.A. In Korea, Kim MH proposed Kim's criteria based on his experience of 28 patients with AIP at single center. 8 Kim s criteria included pancreatic imaging, laboratory findings, histopathologic findings and response to steroid. He had designed a system where patients are stratified by evidence strength for AIP into definite, probable and possible. He emphasized Fig. 1. Diagnostic criteria of 2002 autoimmune pancreatitis by Japan Pancreas Society.
4 년도대한췌담도학회추계학술대회 that a diagnostic trial of steroid can be initiated even though serologic markers or pathologic findings do not fulfill the Japanese criteria, providing that pancreatic image are typical to AIP. In Japan, clinical diagnostic criteria of AIP were published as a revised proposal by the research Fig. 2. Clinical diagnostic criteria of autoimmune pancreatitis (2006 Revised Proposal) by Japan Pancreas Society. Fig. 3. Diagnostic criteria of autoimmune pancreatitis (HISORt criteria) by Mayo Clinic.
5 Ji Kon Ryu:Overview of Diagnostic Criteria for Autoimmune Pancreatitis 109 committee of intractable disease of the pancreas supported by the Japan Pancreas Society (Fig. 2). 6 They focused on how to distinguish it from pancreatic or biliary cancer. The criteria contained three components as same as previous Japan criteria and some minor modification were done. The Japanese criteria are based on the minimum consensus features of AIP in order to avoid the misdiagnosis of malignancy as far as possible, but not to pick up suspicious cases of AIP. The HISORt criteria were proposed by the Mayo Clinic based on the 29 patients who met histologic criteria for AIP at single center (Fig. 3). 7 The criteria included 5 categories: histology, imaging, serology, other organ involvement and response to steroid therapy. According to HISORt criteria, AIP can be diagnosed by three groups of diagnostic criteria: group A with typical histology and IgG4 immunostaining, group B with typical imaging and serology, group C with unexplained pancreatic disease with serology and response to steroid. The authors pointed out that the Japanese criteria for AIP focus heavily on characteristic pancreatic imaging and therefore lack sensitivity to diagnose the wide spectrum of manifestations of AIP. They insisted that HISORt criteria reflected the current understanding of AIP as a systemic steroid-responsive disorder characterized by tissue infiltration with IgG4-positive cells and clearly identify a wider. Another new diagnostic criteria were proposed by Brugge WR at Massachusetts General Hospital (MGH) (Fig. 4). 9 They defined AIP as a type of chronic pancreatitis characterized by an autoimmune inflammatory process in which prominent lymphocyte infiltration with associated fibrosis of the pancreas causes organ dysfunction. The MGH criteria were modified from those of the Japan Pancreas Society and minor modifications were done to elevate diagnostic sensitivity. They also suggested the diagnostic and treatment algorithm for AIP according to their diagnostic criteria. Recently, Japanese authors examined the imaging findings of 37 AIP cases and also examined misdiagnosed cases of AIP to determine their reasons for Fig. 4. Diagnostic criteria of autoimmune pancreatitis by MGH.
6 년도대한췌담도학회추계학술대회 misdiagnosis. 31 Only 7 patients had typical AIP findings and six patients were misdiagnosed with pancreatic cancer and 2 with bile-duct cancer. Seven cases were surgically treated. They pointed out that Japanese criteria are too narrow and do not capture the broad spectrum of presentation. They suggest that AIP presents a variety of imaging findings and the most important diagnostic factor is clinician awareness of the concept of AIP and the diverse nature of imaging findings. Can a tissue biopsy be the gold standard for the diagnosis of AIP? Theoretically, the answer is yes, because there are histopathologic features of AIP that are distinct from other forms of chronic pancreatitis. The histology of AIP, termed lymphoplasmacytic sclerosing pancreatitis, is characterized by a lymphoplasmacytic infiltrate around small-sized ducts, swirling fibrosis centered around ducts and veins (storiform fibrosis), and obliterative phlebitis wherein the infiltrate surrounds pancreatic venules while sparing arterioles. AIP is a heterogeneous disease, however, and the diagnostic features can be missed on a single core biopsy. Interestingly, in the study by Chari ST et al, 7 7 (44%) of 16 core biopsies showed the characteristic features of AIP, including periductal lymphoplasmacytic inflammation with fibrosis and obliterative phlebitis. In a separate report by the same institution, the diagnosis of AIP can not be made in patients undergoing EUS with fine-needle aspiration (nine patients) because of the lack of tissue Korean Criteria for Autoimmune Pancreatitis Definite Diagnosis: Criterion I with anyone of Criterion II to IV Criterion I. Imaging (Both required) 1. Imaging (CT or MRI) of pancreatic parenchyma; Diffusely/segmentally/focally enlarged gland, occasionally with mass and/or hypoattenuation rim 2. Imaging (ERCP or MRCP) of pancreaticobiliary ducts; Diffuse/segmental/focal pancreatic ductal narrowing, often with the stenosis of bile duct Criterion II. Serology (One required) 1. Elevated level of serum IgG or IgG4 2. Detected autoantibodies Criterion III. Histopathology of pancreatic / extrapancreatic lesions (One required) 1. Lymphoplasmacytic infiltration & fibrosis, often with obliterative phlebitis 2. Presence of abundant (>10 cells/hpf) IgG4-positive plasma cells Criterion IV. Response to steroids 1. Resolution/marked improvement of pancreatic/ extrapancreatic lesion with steroid therapy Probable Diagnosis: Criterion V or VI Criterion V. Unexplained pancreatic disease but only with characteristic pancreatic histology Criterion VI. (Both required) 1. Other organ involvement and/or serologic abnormalities* 2. Various atypical pancreatic imaging suggesting chronic pancreatitis with negative workup for known etiologies * The confirmation of other organ involvement detected on imaging findings (One required). i) The histology of other organ shows changes of full spectrum of lymphoplasmacytic sclerosing pancreatitis (LPSP). ii) The histology of other organ shows abundant IgG4-positive cell infiltration on immunostaining. iii) The elevated serum IgG/IgG4 level in combination with marked improvement/resolution of the organ lesion after steroid therapy. Fig. 5. Korean Diagnostic Criteria of Autoimmune Pancreatitis by Korean Society of Pancreatobiliary Diseases.
7 Ji Kon Ryu:Overview of Diagnostic Criteria for Autoimmune Pancreatitis 111 architecture. 32 EUS guided pancreatic aspiration is preferred to percutaneous core biopsy because the low risk of complication and cancer seeding risk if the pancreatic mass is malignant. In most clinical situation, it is not common to use the histological criteria to diagnose AIP unless surgical biopsy. In Korea, new Korean diagnostic criteria are established by the Korean Society of Pancreatobiliary Diseases and based on the Kim s criteria including response to steroid therapy to improved the diagnostic sensitivity and specificity (Fig. 5). Korean criteria considered the variety of imaging findings of AIP and low yield of histologic acquisition. The Korean criteria will be published sooner or later. Conclusions AIP is a benign, IgG4-related, fibroinflammatory form of chronic pancreatitis that can mimic pancreatic ductal adenocarcinoma both clinically and radiologically. Clinically, AIP most commonly presents as obstructive jaundice associated with a biliary stricture and tends to respond to steroid therapy. Radiologically, AIP can appear as a focal lesion or mass, or can diffusely involve the pancreas with associated focal or diffuse narrowing of the pancreatic duct. Histopathologically, the hallmark features of AIP are a periductal lymphoplasmacytic infiltrate; obliterative phlebitis; and abundant IgG4-positive plasma cells. These features are used as diagnostic criteria in AIP. Making a diagnosis of AIP can be challenging but is important to prevent unnecessary surgery. Diagnostic criteria have been proposed that incorporate histologic, radiologic, serologic, and clinical information, including the presence of other associated diseases and response to steroid therapy. Because the distinction between AIP and pancreatic cancer is difficult to make in many cases, every attempt needs to be made to exclude the possibility of malignancy, even if it results in a pancreatic resection for benign disease in some patients. As more data are gathered on AIP across the world, the diagnostic criteria will be shifted. REFERENCES 1. Yoshida K, Toki F, Takeuchi T, Watanabe S, Shiratori K, Hayashi N: Chronic pancreatitis caused by an autoimmune abnormality. Proposal of the concept of autoimmune pancreatitis. Dig Dis Sci 1995; 40: Kim JY, Chang HS, Kim MH, et al: A case of autoimmune chronic pancreatitis improved with oral steroid therapy. Korean J Gastroenterol 2002; 39: Kim KP, Kim MH, Lee YJ, et al: Clinical characteristics of 17 cases of autoimmune chronic pancreatitis. Korean J Gastroenterol 2004; 43: Ryu JK, Lee JK, Kim YT, et al: Clinical features of chronic pancreatitis in Korea: a multicenter nationwide study. Digestion 2005; 72: Pearson RK, Longnecker DS, Chari ST, Smyrk TC, Okazaki K, Frulloni L, Cavallini G. Controversies in clinical pancreatology: autoimmune pancreatitis: does it exist? Pancreas 2003; 27: Okazaki K, Kawa S, Kamisawa T, et al: Clinical diagnostic criteria of autoimmune pancreatitis: revised proposal. J Gastroenterol 2006; 41: Chari ST, Smyrk TC, Levy MJ, et al: Diagnosis of autoimmune pancreatitis: the Mayo Clinic experience. Clin Gastroenterol Hepatol 2006; 4: Kim KP, Kim MH, Kim JC, Lee SS, Seo DW, Lee SK: Diagnostic criteria of autoimmune chronic pancreatitis revisited. World J Gastroenterol 2006; 12: Finkelberg DL, Sahani D, Deshpande V, Brugge WR: Autoimmune pancreatitis. N Engl J Med 2006; 355: Sarles H, Sarles JC, Muratoren R, Guien C: Chronic inflammatory sclerosis of the pancreas--an autonomous pancreatic disease? Am J Dig Dis 1961; 6: Kawaguchi K, Koike M, Tsuruta K, Okamoto A, Tabata I, Fujita N: Lymphoplasmacytic sclerosing pancreatitis with cholangitis: a variant of primary sclerosing cholangitis extensively involving pancreas. Hum Pathol 1991; 22:
8 년도대한췌담도학회추계학술대회 12. Sood S, Fossard DP, Shorrock K: Chronic sclerosing pancreatitis in Sjogren's syndrome: a case report. Pancreas 1995; 10: Chutaputti A, Burrell MI, Boyer JL: Pseudotumor of the pancreas associated with retroperitoneal fibrosis: a dramatic response to corticosteroid therapy. Am J Gastroenterol 1995; 90: Ito T, Nakano I, Koyanagi S, Miyahara T, Migita Y, Ogoshi K, Sakai H, Matsunaga S, Yasuda O, Sumii T, Nawata H: Autoimmune pancreatitis as a new clinical entity. Three cases of autoimmune pancreatitis with effective steroid therapy. Dig Dis Sci 1997; 42: Irie H, Honda H, Baba S, Kuroiwa T, Yoshimitsu K, Tajima T, Jimi M, Sumii T, Masuda K: Autoimmune pancreatitis: CT and MR characteristics. AJR Am J Roentgenol 1998; 170: Ectors N, Maillet B, Aerts R, et al: Non-alcoholic duct destructive chronic pancreatitis. Gut 1997; 41: Van Hoe L, Gryspeerdt S, Ectors N: Non-alcoholic duct-destructive chronic pancreatitis: imaging findings. Am J Roentgenol 1998; 170: Eerens I, Vanbeckevoort D, Vansteenbergen W, et al: Autoimmune pancreatitis associated with primary sclerosing cholangitis: MR imaging findings. Eur Radiol 2001; 11: Okazaki K, Uchida K, Ohana M, Nakase H, Uose S, Inai M, Matsushima Y, Katamura K, Ohmori K, Chiba T: Autoimmune-related pancreatitis is associated with autoantibodies and a Th1/Th2-type cellular immune response. Gastroenterology 2000; 118: Hamano H, Kawa S, Horiuchi A, et al: High serum IgG4 concentrations in patients with sclerosing pancreatitis. N Engl J Med 2001; 344: Etemad B, WhitcombDC: Chronic pancreatitis: diagnosis, classification and new genetic developments. Gastroenterology 2001; 120: Yadav D, Notahara K, Smyrk TC, et al: Idiopathic tumefactive chronic pancreatitis: clinical profile, histology, and natural history after resection. Clin Gastroenterol Hepatol 2003; 1: Weber SM, Cubukcu-Dimopulo O, Palesty JA, et al: Lymphoplasmacytic sclerosing pancreatitis: inflammatory mimic of pancreatic carcinoma. J Gastrointest Surg 2003; 7: Abraham SC, Wilentz RE, Yeo CJ, et al: Pancreaticoduodenectomy (Whipple resections) in patients without malignancy: are they all 'chronic pancreatitis'? Am J Surg Pathol 2003; 27: Notohara K, Burgart L J, Yadav D, et al: Idiopathic chronic pancreatitis with periductal lymphoplasmacytic infiltration: clinicopathologic features of 35 cases. Am J Surg Pathol 2003; 27: Kloppel G, Luttges J, Lohr M, et al: Autoimmune pancreatitis: pathological, clinical, and immunological features. Pancreas 2003; 27: Kamisawa T, Funata N, Hayashi Y, et al: Close relationship between autoimmune pancreatitis and multifocal fibrosclerosis. Gut 2003; 52: Kamisawa T and Okamoto A: Autoimmune pancreatitis: proposal of IgG4-related sclerosing disease. J Gastroenterol 2006; 41: Bjornsson E, Chari ST, Smyrk TC, Lindor K: Immunoglobulin G4 associated cholangitis: description of an emerging clinical entity based on review of the literature. Hepatology 2007; 45: Aparisi L, Farre A, Gomez-Cambronero, et al: Antibodies to carbonic anhydrase and IgG4 levels in idiopathic chronic pancreatitis: relevance for diagnosis of autoimmune pancreatitis. Gut 2005; 54: Nakazawa T, Ohara H, Sano H, Ando T, Imai H, Takada H, Hayashi K, Kitajima Y, Joh T: Difficulty in diagnosing autoimmune pancreatitis by imaging findings. Gastrointest Endosc 2007; 65: Levy MJ, Wiersema MJ, Chari ST: Chronic pancreatitis: focal pancreatitis or cancer? Is there a role for FNA/biopsy? Autoimmune pancreatitis. Endoscopy 2006; 38(Suppl 1): S30-35.
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