diagnostics Review The Diagnosis of Autoimmune Pancreatitis Using Endoscopic Ultrasonography Atsushi Kanno 1,* , Eriko Ikeda 1, Kozue Ando 1, Hiroki Nagai 1, Tetsuro Miwata 1, Yuki Kawasaki 1, Yamato Tada 1, Kensuke Yokoyama 1, Norikatsu Numao 1, Jun Ushio 1, Kiichi Tamada 1, Alan Kawarai Lefor 2 and Hironori Yamamoto 1 1 Department of Medicine, Division of Gastroenterology, Jichi Medical University, Shimotsuke 329-0498, Japan; r1403ie@jichi.ac.jp (E.I.); kozue_ando@jichi.ac.jp (K.A.); m05069hn@jichi.ac.jp (H.N.); tetsurou_miwata@yahoo.ac.jp (T.M.); kawasakiyuki1219@gmail.com (Y.K.); tadayamatoday@gmail.com (Y.T.); r0760ky@jichi.ac.jp (K.Y.); numawo@jichi.ac.jp (N.N.); j.ushio@jichi.ac.jp (J.U.); tamadaki@jichi.ac.jp (K.T.); yamamoto@jichi.ac.jp (H.Y.) 2 Department of Surgery, Jichi Medical University, Shimotsuke 329-0498, Japan; alefor@jichi.ac.jp * Correspondence: atsushih@jichi.ac.jp; Tel.: +81-285-58-7348; Fax: 81-285-44-8297 Received: 29 October 2020; Accepted: 20 November 2020; Published: 25 November 2020 Abstract: Autoimmune pancreatitis (AIP) is characterized by enlargement of the pancreas and irregular narrowing of the main pancreatic duct. It is often associated with IgG4-related sclerosing cholangitis (IgG4-SC), in which the bile duct narrows. Although characteristic irregular narrowing of the pancreatic duct caused by endoscopic retrograde cholangiopancreatography is noted in AIP, it is difficult to differentiate between localized AIP and pancreatic carcinoma based on imaging of the pancreatic duct. While stenosis of the bile duct in IgG4-SC is characterized by longer-length stenosis than in cholangiocarcinoma, differentiation based on bile duct imaging alone is challenging. Endoscopic ultrasound (EUS) can characterize hypoechoic enlargement of the pancreas or bile duct wall thickening in AIP and IgG4-SC, and diagnosis using elastography and contrast-enhanced EUS are being evaluated. The utility of EUS-guided fine needle aspiration for the histological diagnosis of AIP has been reported and is expected to improve diagnostic performance for AIP. Findings in the bile duct wall from endoscopic retrograde cholangiopancreatography followed by intraductal ultrasonography are useful in differentiating IgG4-SC from cholangiocarcinoma. Diagnoses based on endoscopic ultrasonography play a central role in the diagnosis of AIP. Keywords: autoimmune pancreatitis (AIP); endoscopic ultrasound (EUS); EUS-guided fine needle aspiration (EUS-FNA); EUS-guided fine needle biopsy (EUS-FNB); International Consensus Diagnostic Criteria (ICDC) 1. Introduction The concept of autoimmune pancreatitis (AIP) was first proposed by Yoshida et al. in 1995 [1]. Subsequently, there were reports about the diagnosis and treatment of AIP. Many patients with AIP present with other organ involvement, such as sclerosing cholangitis and sialadenitis, and AIP is considered a pancreatic lesion of systemic IgG4-related disease (IgG4-RD) [2]. Diagnostic criteria have been reported from various countries. The diagnostic criteria in Japan were released in 2002 [3] and subsequently revised three times [4,5]. The International Consensus Diagnostic Criteria (ICDC) for AIP [6] were published in 2011 based on the Honolulu consensus [7]. Due to the process by which the current diagnostic criteria were developed, the importance of endoscopic ultrasound (EUS) in the diagnosis of AIP needs to be clarified. This review shows the role and progress of EUS in the diagnosis of AIP. Diagnostics 2020, 10, 1005; doi:10.3390/diagnostics10121005 www.mdpi.com/journal/diagnostics Diagnostics 2020, 10, x 2 of 13 Diagnostics 2020, 10, 1005 2 of 13 2. Diagnostic Criteria for AIP 2. Diagnostic Criteria for AIP In 2009, a joint meeting between the American Pancreatic Association and the Japan Pancreas SocietyIn 2009,(JPS) was a joint held meeting in Honolulu between to discuss the American about the Pancreatic concept Association of AIP [7]. This and meeting the Japan resulted Pancreas in Societythe release (JPS) of wasthe Honolulu held in Honolulu consensus, to discusswhich emphas about theized concept the histological of AIP [7 findings]. This meeting in types resulted 1 and 2 inAIP the showing release oflymphoplasmacytic the Honolulu consensus, sclerosing which pancre emphasizedatitis and the idiopathic histological duct-centric findings in chronic types 1 andpancreatitis/granulocytic 2 AIP showing lymphoplasmacytic epithelia lesions, sclerosing respectively pancreatitis [7]. Based and on idiopathicthe Honolulu duct-centric consensus, chronic ICDC pancreatitisfor AIP [6] /granulocyticwere published epithelia after lesions,further respectivelydiscussion at [7 ].an Based international on the Honolulu joint meeting consensus, between ICDC the for AIPInternational [6] were Pancreas published Society after furtherand JPS discussionheld in Fukuoka, at an internationalJapan in July joint 2010. meeting In the ICDC, between AIP the is Internationaldiagnosed based Pancreas on the Society presence/absence and JPS held in of Fukuoka, a combination Japan in of July five 2010. findings: In the ICDC,(i) pancreatic AIP is diagnosed imaging basedfindings on (parenchyma the presence /absence(P) and ofpancreatic a combination duct (D)) of five, (ii) findings: serologic(i) findings pancreatic (S), imaging(iii) other findings organ (parenchymainvolvement (O), (P) and(iv) histological pancreatic duct findings (D)), (H), (ii) serologicand (v) response findings to (S), steroid (iii) other therapy organ (Rt). involvement The ICDC (O),enables (iv) the histological diagnosis findings of AIP (H),using and global (v) response diagnostic to steroid criteria. therapy However, (Rt). the The ICDC ICDC were enables overly the diagnosiscomplicated of for AIP general using globalclinicians diagnostic to diagnose criteria. patien However,ts with AIP the and ICDC Type were 2 AIP overly is extremely complicated rare for in generalJapan. Therefore, clinicians the to diagnose JPS developed patients Clinical with AIP Diagno andstic Type Criteria 2 AIP isfor extremely AIP 2011 rare [5] (JPS in Japan. 2011) Therefore, based on the JPSICDC. developed Later, these Clinical criteria Diagnostic were further Criteria revised for AIP as 2011the Clinical [5] (JPS Diagnostic 2011) based Criteria on the for ICDC. AIP Later, 2018 these(JPS 2018) criteria [8]. wereCurrently, further the revised diagnosis as the of AIP Clinical by EUS Diagnostic plays an Criteria important for AIProle 2018in the (JPS ICDC 2018) of JPS [8]. Currently,2018. the diagnosis of AIP by EUS plays an important role in the ICDC of JPS 2018. 3. The Role of Endoscopy in the Diagnosis of AIP 3.1. Endoscopic Retrograde Cholangiopancreatography While this review focuses on EUS, endoscopicendoscopic retrograde cholangiopancreatography (ERCP) will be brieflybriefly described because ERCPERCP is also an essential modality for the diagnosis of AIP and is an essential procedure for intraductal ultrasonographyultrasonography (IDUS). Pancreatic enlargement with diffuse diffuse irregular narrowing of the main pancreatic duct (MPD) is a typical imaging findingfinding in patients with AIP [[1].1]. NarrowingNarrowing of of the the MPD MPD is is defined defined as aas finding a finding where where smaller smaller than than normal normal pancreatic pancreatic ducts dilateducts anddilate present and present with irregular with irregular margins margins (Figure1 )[(Figure9]. ERCP 1) [9]. is essentialERCP is foressential diagnosing for diagnosing irregular narrowing irregular ofnarrowing the MPD. of Levelthe MPD. 1 narrowing Level 1 narrowing of the MPD of wasthe MPD defined was as defined at least as one-third at least one-third of the total of length the total of thelength pancreatic of the pancreatic duct without duct a without dilatation a dilatation of pancreatic of pancreatic body and body tail in and the tail ICDC in the [6]. ICDC The ICDC [6]. The [6] andICDC JPS2011 [6] and [5 JPS2011] mention [5] narrowing mention narrowing of the MPD of in the ERCP MPD as in a conditionERCP as fora condition the definitive for the diagnosis definitive of localizeddiagnosis AIP.of localized However, AIP. diff erentiatingHowever, differentiating stenosis of the MPDstenosis due of to the pancreatic MPD due cancer to pancreatic from narrowing cancer offrom the narrowing MPD in localized of the MPD AIP isin extremelylocalized AIP diffi cult.is extremely difficult. Figure 1. Endoscopic retrograde pancreat pancreatographyography revealed diffuse diffuse irre irregulargular narrowing of the main pancreatic duct (arrowhead) andand stenosisstenosis ofof thethe lowerlower bilebile ductduct (arrow).(arrow). Diagnostics 2020, 10, 1005 3 of 13 There are numerous reports of ERCP findings observed in AIP and pancreatic cancer [9–11]. Although the narrowing of at least one-third of the entire length of the MPD has been shown to be an important characteristic of pancreatic duct images in AIP, there have been reports of the sensitivity, specificity, and interobserver agreement of diagnosis of AIP using ERCP as being low [11]. In addition, it is important to make a comprehensive diagnosis along with other findings because there is a risk of post-ERCP pancreatitis. AIP is sometimes complicated by IgG4-related sclerosing cholangitis (IgG4-SC) [12,13]. However, IgG4-SC is difficult to differentiate from primary sclerosing cholangitis and malignant tumors [14,15]. Most patients with primary sclerosing cholangitis have progressive disease and many develop stenosis in both the intrahepatic and extrahepatic bile ducts, leading to liver cirrhosis.
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