Overlap of IgG4-related Disease and Primary Biliary Cirrhosis Complicated with Autoimmune Thrombocytopenia
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1 CASE REPORT Overlp of IgG4-relted Disese nd Primry Biliry Cirrhosis Complicted with Autoimmune Thromocytopeni Mik Tksumi 1,2, Msyuki Miyt 1, Mshito Kurod 1, Kumiko Tershim 1, Kzumichi Ae 2, Atsushi Tkhshi 2, Hiroko Koyshi 2, Kzuhiro Tzki 3, Hiroshi Wtne 2 nd Hiroms Ohir 2 Astrct A 63-yer-old womn ws referred to Fukushim Red Cross Hospitl with n enlrgement of the left sumndiulr glnd nd sucutneous leeding in the chest nd legs. A diffuse enlrgement of the pncres ws lso detected y dominl computed tomogrphy, nd lortory dt showed severe thromocytopeni. She ws dignosed with IgG4-relted disese (IgG4-RD) complicted with utoimmune thromocytopeni nd ws treted with methylprednisolone, fter which the numer of pltelets fvorly incresed. Further investigtion for liver dysfunction reveled underlying primry iliry cirrhosis (PBC). We herein report rre cse of IgG4-RD overlpping PBC complicted with utoimmune thromocytopeni. Key words: IgG4-relted disese, primry iliry cirrhosis, utoimmune thromocytopeni, prednisolone (Intern Med 55: , 2016) (DOI: /internlmedicine ) Introduction IgG4-relted disese (IgG4-RD) ws first reported in 1993 (1), nd new disese clssifiction ws estlished in Jpn in 2011 (2). It is novel clinicl disese entity chrcterized y n elevted serum IgG4 concentrtion nd tumefction or tissue infiltrtion y IgG4-positive plsm cells (3-6). A certin proportion of ptients formerly dignosed with utoimmune pncretitis (7, 8) or Mikulicz s disese (9, 10) re elieved to hve hd IgG4-RD. Persistent enlrgement of the lcriml nd slivry glnds re chrcteristic of Mikulicz s disese. On the other hnd, primry iliry cirrhosis (PBC) is chronic cholesttic disese with progressive course, chrcterized y the presence of serum nti-mitochondril ntiodies nd histologicl nonsuppurtive destructive cholngitis. PBC is n utoimmune liver disese distinct from IgG4-relted sclerosing cholngitis (IgG4- SC), which is clssified s iliry mnifesttion of IgG4- RD. However, few cses of overlpping PBC nd IgG4- SC hve een reported (11-13). Although utoimmune thromocytopeni is well-defined utoimmune disese, its ssocition with IgG4-RD or PBC is rre. We herein descrie rre cse of overlpping IgG4-RD nd PBC complicted with utoimmune thromocytopeni nd discuss the possile mechnisms underlying the ssocition of these three diseses. Cse Report A 63-yer-old womn ws referred to our deprtment with n enlrgement of the left sumndiulr glnd nd purpur on the chest nd legs in Decemer Her height nd weight were 153 cm nd 56 kg, respectively. The ptient s vitl signs were stle: lood pressure of 135/75 mmhg, hert rte of 73 ets per minute, ody temperture Deprtment of Internl Medicine nd Gstroenterology, Fukushim Red Cross Hospitl, Jpn, Deprtment of Gstroenterology nd Rheumtology, Fukushim Medicl University School of Medicine, Jpn nd Deprtment of Pthology, Fukushim Medicl University School of Medicine, Jpn Received for puliction July 17, 2015; Accepted for puliction August 16, 2015 Correspondence to Dr. Mik Tksumi, pper@fmu.c.jp 1387
2 DOI: /internlmedicine Tle. Lortory Dt t Admission. Peripherl lood WBC 7,400 / RBC 4, / H 14.5 g/d Plt 4,000 / Cogultion PT % PT-INR 0.96 APTT 25.4 sec Infection HBs-Ag (-) HCV-A (-) H.Pylori IgG 28 U/ Blood chemistry T-il 0.9 mg/d AST 35 IU/ A T 36 IU/ H 217 IU/ P 671 IU/ -GTP 457 IU/ P-AMY 27 IU/ BUN 12.3 mg/d Cre 0.62 mg/d N 143 mmol/ K 3.9 mmol/ Cl 105 mmol/ PG 109 mg/d TP 8.8 g/d IgG 1,765 mg/d IgG4 160 mg/d IgA 269 mg/d IgM 378 mg/d C3 159 mg/d C4 20 mg/d CH50 45 U/ ANA( iscrete -Speckled) 640 Anti-P T ntiody Slightly positive Anti-SS-A ntiody negtive Anti-M2 ntiody 214 U/ Figure 1. CT of the sumndiulr glnd. : At dmission: Non-contrst CT reveled enlrgement of the ilterl sumndiulr glnd. : Two weeks fter the eginning of PSL tretment: Contrstenhnced CT reveled decresed swelling of the ilterl sumndiulr glnd. of 36.2 C, nd SpO2 of 100% (room ir). Lortory dt (Tle) showed severe thromocytopeni, with pltelet (PLT) count of 4,000/μL. A cogulofirinolysis test showed no normlities. Her nti-plt ntiody ws slightly positive. The serum levels of γ-glutmyl trnspeptidse (γ-gtp), lkline phosphtse, sprtte minotrnsferse (AST), nd lnine minotrnsferse (ALT) were high. Serum IgG ws elevted t 3,160 mg/dl, nd IgG4 ws elevted t 160 mg/ dl (norml rnge mg/dl). The serum IgM level ws lso elevted t 378 mg/dl (norml rnge mg/dl). The complement level, which included C3, C4, nd CH50, ws not low. No pprent iliry dilttion or structurl normlities of the liver were oserved. However, ntinucler ntiody ws positive t 640 in discrete speckled pttern nd cytoplsmic ntiody ws positive t 80, while nti-ss-a ntiody ws negtive. Helicocter pylori (H. pylori) IgG ws positive t 28 U/mL. Computed tomogrphy (CT) reveled the enlrgement of oth sumndiulr glnds (Fig. 1) nd diffuse enlrgement of the pncres (Fig. 2). The enlrgement of the sumndiulr glnd ws ilterl, lthough only the left side ws plple. No diltion of the ile nd pncretic ducts ws oserved. A differentil count of the one mrrow fluid otined y spirtion ws within norml limits with slight increse of megkryocytes, lthough typicl cells were not detected (Fig. 3). Immunostining for CD138 nd IgG4 did not revel n increse of IgG4-producing plsm cells in the one mrrow (Fig. 3 nd c). From these findings, IgG4-RD nd utoimmune thromocytopeni ws dignosed, lthough tumefction or tissue infiltrtion y IgG4-positive plsm cells 1388
3 DOI: /internlmedicine Figure 2. CT of the pncres. : At dmission: Contrst-enhnced CT reveled diffuse enlrgement of the pncres s shown y rrows. Diltion of oth ile nd pncretic ducts ws not seen. : Two weeks fter the eginning of PSL tretment: Contrst-enhnced CT reveled decrese in diffuse swelling of the pncres. c Figure 3. Pthologicl findings of the one mrrow fluid otined y spirtion. : Hemtoxylin nd Eosin stining (200 ): A differentil count of the one mrrow fluid ws within norml limits with slight increse in the numer of megkryocytes. Atypicl cells were not detected. : Immunostining of CD138 (200 ): The numer of CD138-positive plsm cells ws pproximtely 5%, which remined smll. c: Immunostining of IgG4 (200 ): IgG4-producing plsm cells in the one mrrow were not detected. 1389
4 DOI: /internlmedicine mpsl (mg/dy) ( 10 3 / L) dy Bone mrrow spirtion ALP (IU/L) PLT ( 10 3 / ) PLT 125 Figure 4. The clinicl course of the ptient. 24 PLT ALP PSL 13.Dec 14.Fe Mr My Jul Liver iopsy Sep ALT IgG (mg/dl) ALT (IU/L) 90 could not e estlished due to severe thromocytopeni. Tretment with methylprednisolone (mpsl) semi-pulse (500 mg/ody/dy) ws strted for utoimmune thromocytopeni. Becuse the PLT count ws elevted to more thn /μl within three dys, we tpered mpsl to hlf the dose (Fig. 4). Both totl IgG nd IgG4 were decresed to within norml limits within two months (Fig. 4). Two weeks fter eginning tretment with mpsl, CT showed mrked improvement of diffuse swelling of the ilterl sumndiulr glnd nd pncres (Fig. 1, 2). The ptient lso received H. pylori erdiction 7-dy course of triple therpy of lnsoprzole, moxicillin, nd clrithromycin. Successful erdiction ws ssessed y the ure reth test. Although the serum levels of AST, ALT, lkline phosphtse (ALP), nd γ-gtp decresed temporrily, γ-gtp did not decrese to within norml levels, nd AST nd ALT reelevted six months fter eginning mpsl tretment (Fig. 4). The serum level of nti-mitochondril M2 (nti-m 2) ntiody ws mesured in order to determine cuse relted to liver dysfunction, nd it ws elevted t 214 U/mL (norml rnge, <7 U/mL). Serologic mrkers for heptitis B nd C viruses were negtive. Mgnetic resonnce cholngiopncretogrphy reveled neither strictures of the lower common ile duct nor segmentl stricture. Becuse underlying PBC ws suspected t this time, liver iopsy ws Nov performed. The liver specimen showed infiltrtion of lymphocytes in the portl re ut did not revel ny ovious ile duct destruction y lymphocytes. IgG4-positive plsm cells were not oserved in this specimen. Erly-phse chronic nonsuppurtive destructive cholngitis (CNSDC) ws suggested (Fig. 5). Liver dysfunction ws improved y the dministrtion of ursodeoxycholic cid fter the liver iopsy. Discussion IgG4-RD nd utoimmune thromocytopeni (ITP) were initilly dignosed in this cse. However, PBC ws susequently suspected fter the dministrtion of mpsl therpy. Although liver iopsy did not revel ny ovious ile duct destruction due to CNSDC, PBC could e dignosed y n elevted serum nti-m2 ntiody level, which hs high sensitivity nd specificity for the dignosis of PBC (14, 15). Elevtion of serum IgM lso suggested the existence of PBC. Mgnetic resonnce cholngiopncretogrphy ws performed, ut the presence of IgG4-SC ws not determined. IgG4-SC generlly revels segmentl strictures, long strictures with prestenotic dilttion, nd strictures of the lower common ile duct. Biliry strictures in IgG4-SC typiclly respond to steroids, nd complete resolution of the strictures nd/or normliztion of liver tests hs een oserved in pproximtely two-thirds of ptients, wheres improvement ws seen in the remining one-third (16). It ws difficult to rule out the presence of IgG4-SC in our cse treted y mpsl. An underlying common pthogenesis my exist in these three diseses. First, regrding the common pthogenesis of PBC nd IgG4-RD, Shimod et l. (17) reported the role of Toll-like receptors nd nturl killer (NK) cells in PBC ptients. Toll-like receptor 4 lignd (TLR4-L)-stimulted NK cells destroy utologous iliry epithelil cells in the presence of interferon (IFN)-α synthesized y TLR 3 lignd (TLR3-L)-stimulted monocytes. According to Shimod et l., IFN-α production y heptic monocytes ws significntly incresed in ptients with PBC. The cytotoxic ctivity of heptic NK cells ws lso incresed compred to controls. However, this only occurred when the NK cells were prepred following ligtion of oth TLR3-L- nd TLR4-Lstimulted liver mononucler cells. On the other hnd, Wtne et l. (18) reported tht ctivtion of TLR nd nucleotide-inding oligomeriztion domin-like receptors enhnced IgG4 responses in utoimmune pncretitis. Stimultion with TLR3 nd TLR4 lignds enhnces IgG4 production y peripherl lood mononucler cells in IgG4-RD ptients. These consequences suggest common pthogenesis in IgG4-RD nd PBC through norml innte immune responses ginst microil ntigens. Next, we exmined the pthogenesis of PBC nd utoimmune thromocytopeni. Pnzer et l. (19) reported tht utontiodies eluted from ptient with PBC nd utoimmune thromocytopeni, precipitte glycoprotein II/III of 1390
5 DOI: /internlmedicine Figure 5. Pthologicl findings of the liver otined y needle iopsy. : Hemtoxylin nd Eosin stining (200 ). : Elstic-Msson stining (200 ). A liver specimen showed infiltrtion of lymphocytes in the portl re, ut no ovious ile duct destruction y lymphocytes ws found. There ws slight deformtion of the ile duct. Tken together, erly phse chronic nonsuppurtive destructive cholngitis (CNSDC) could not e ruled out. utologous nd llogeneic PLT nd ind to n epitope of the rt 70-kD mitochondril protein M2. Furthermore, n in silico nlysis of pulished peptide sequences of the mitochondril protein nd glycoprotein II/III showed prtil mino cid sequence homology, suggesting the possiility of common ntiody-inding site. From these findings, PBCrelted utontiodies might cross-rect with PLT surfce utontigens in ITP (20). A common underlying pthogenesis of IgG4-RD nd utoimmune thromocytopeni ws considered. However, the role of the IgG4 ntiody response in the immunopthogenesis of IgG4-RD is poorly understood. Moreover, serum IgG4 levels fluctute long with the stte of IgG4-RD. A few cses hve een reported regrding the ssocition etween IgG4-RD, especilly with utoimmune pncretitis, nd utoimmune thromocytopeni (21-24). In the present cse, no significnt increse in the numer of IgG4-positive cells or decrese in megkryocytes in the one mrrow ws oserved. This suggests tht the cuse of thromocytopeni ws not decrese in megkryocytes in reltion to the prolifertion of IgG4-positive cells in the one mrrow, ut the presence of nti-plt ntiody. Ptients with ITP hve nti- PLT utontiodies tht re most frequently directed ginst PLT glycoproteins II/III or I/IX/V. Chn et l. (25) reported tht the most common suclss of nti-ii/iii ntiodies in ITP ptients ws IgG1. Murse et l. (22) reported n IgG suclss of PLT ntiody to e potentilly IgG4. While this suggested role of IgG4 s n nti-plt ntiody in IgG4-RD ptients, this finding is controversil ecuse IgG4-RD is rrely complicted with thromocytopeni. H. pylori infection could lso contriute to IgG4-RD nd ITP. The peptide showed homology with n mino cid sequence etween H. pylori α-cronic nhydrse (α-ca) nd humn CA type II nd etween H. pylori plsminogeninding protein nd humn uiquitin-protein ligse E3 component n-recognin 2, n enzyme highly expressed in cinr cells of the pncres (26, 27). It hs een suggested tht this moleculr mimicry cn led to immunologicl crossrectivity. Furthermore, CgA ntigen of H. pylori my induce nti-gpii/iii ntiody production y moleculr mimicry mechnism (28), suggested contriution to ITP. Although there is moleculr mimicry etween the urese et ntigen of H. pylori nd E2 suunit of the pyruvte dehydrogense complex of the mjor mitochondril utoepitope, this homology does not led to immunologicl crossrectivity (29, 30). In summry, it could e inferred tht serum nti-m2 ntiody from PBC or IgG4 from IgG4-RD recognized PLT s n ntigen, susequently inducing severe thromocytopeni in our ptient. In ddition, IgG4 production my e enhnced y PBC. H. pylori infection could lso contriute to IgG4-RD nd ITP. We herein experienced rre cse of overlpping IgG4-RD nd PBC complicted with utoimmune thromocytopeni. A comintion of these three diseses suggests tht common immunogenetic fctors might e involved in the development of IgG4-RD, PBC, nd utoimmune thromocytopeni. The uthors stte tht they hve no Conflict of Interest (COI). References 1. Suzuki S, Kid S, Ohir Y, et l. A cse of Sjögren s syndrome ccompnied y lymphdenopthy nd IgG4 hypergmmgloulinemi. Ryumchi 33: , Umehr H, Okzki K, Mski Y, et l. Comprehensive dignostic criteri for IgG4-relted disese (IgG4-RD), Mod Rheumtol 22: 21-30, Okzki K, Umehr H. Are clssifiction criteri for IgG4-RD now possile? The concept of IgG4-relted disese nd proposl of comprehensive dignostic criteri in Jpn. Int J Rheumtol 1391
6 DOI: /internlmedicine : , Umehr H. A new clinicl entity: IgG4-relted disese (IgG4- RD) discovered in the 21st century. Intern Med 51: , Umehr H, Okzki K, Mski Y, et l. A novel clinicl entity, IgG4-relted disese (IgG4RD): generl concept nd detils. Mod Rheumtol 22: 1-14, Umehr H, Sto T, Nkmur T, Tnk M. IgG4-relted disese - new clinicl entity estlished y ll Jpn IgG4 tem in 21st century. Arerugi 62: , Hmno H, Kw S, Horiuchi A, et l. High serum IgG4 concentrtions in ptients with sclerosing pncretitis. N Engl J Med 344: , Yoshid K, Toki F, Tkeuchi T, Wtne S, Shirtori K, Hyshi N. Chronic pncretitis cused y n utoimmune normlity. Proposl of the concept of utoimmune pncretitis. Dig Dis Sci 40: , Ymmoto M, Ohr M, Suzuki C, et l. Elevted IgG4 concentrtions in serum of ptients with Mikulicz s disese. Scnd J Rheumtol 33: , Ymmoto M, Tkhshi H, Nishiro Y, et l. Mikulicz s disese nd systemic IgG4-relted plsmcytic syndrome (SIPS). Nihon Rinsho Meneki Gkki Zsshi (Jpn J Clin Immunol) 31: 1-8, 2008 (in Jpnese, Astrct in English). 11. Nitoh I, Nkzw T, Hyshi K, et l. A cse of IgG4-relted sclerosing cholngitis overlpped with primry iliry cirrhosis. Intern Med 51: , Tkemoto R, Miyke Y, Hrd K, et l. Overlp of IgG4-relted sclerosing cholngitis nd primry iliry cirrhosis. Intern Med 53: , Wiegnd J, Neid M, Kiser T, et l. Coexistence of utoimmune pncretitis nd primry iliry cirrhosis in Cucsin ptient - rre cuse of cholestsis. Z Gstroenterol 44: , Bssendine MF, Collins JD, Stephenson J, Sunders P, Jmes OF. Pltelet ssocited immunogloulins in primry iliry cirrhosis: cuse of thromocytopeni? Gut 26: , Berg PA, Klein R, Lindenorn-Fotinos J, Kloppel W. ATPsessocited ntigen (M2): mrker ntigen for serologicl dignosis of primry iliry cirrhosis. Lncet 2: , Ghzle A, Chri ST, Zhng L, et l. Immunogloulin G4- ssocited cholngitis: clinicl profile nd response to therpy. Gstroenterology 134: , Shimod S, Hrd K, Niiro H, et l. Interction etween Toll-like receptors nd nturl killer cells in the destruction of ile ducts in primry iliry cirrhosis. Heptology 53: , Wtne T, Ymshit K, Fujikw S, et l. Involvement of ctivtion of toll-like receptors nd nucleotide-inding oligomeriztion domin-like receptors in enhnced IgG4 responses in utoimmune pncretitis. Arthritis Rheum 64: , Pnzer S, Penner E, Nelson PJ, Prochzk E, Bend H, Surugger PN. Identifiction of the pltelet glycoprotein II/III complex s trget ntigen in primry iliry cirrhosis-ssocited utoimmune thromocytopeni. Evidence tht pltelet-rective utontiodies cn lso ind to the mitochondril ntigen M2. J Autoimmun 3: , Toshikuni N, Ymto R, Koshi H, et l. Assocition of primry iliry cirrhosis with idiopthic thromocytopenic purpur. World J Gstroenterol 14: , Fukushim H, Ktou E, Ngym K, Shirchi A, St M. A cse of utoimmune pncretitis complicted with immune thromocytopeni. Jpn J Gstroenterol 103: , 2006 (in Jpnese, Astrct in English). 22. Murse K, Mtsung T, Hyshi T, et l. Successful tretment of utoimmune pncretitis complicted with utoimmune thromocytopeni nd interstitil pneumoni y prednisolone. Intern Med 47: , Nkmur A, Funtomi H, Ktgiri A, et l. A cse of utoimmune pncretitis complicted with immune thromocytopeni during mintennce therpy with prednisolone. Dig Dis Sci 48: , Seko S, Tniguchi T, Nishikw H, et l. A cse of utoimmune pncretitis ssocited with immune thromocytopeni. Nihon Shokki Nishikyo Gkki Zsshi (Gstroenterol Endosc) 42: , 2000 (in Jpnese, Astrct in English). 25. Chn H, Moore JC, Finch CN, Wrkentin TE, Kelton JG. The IgG suclsses of pltelet-ssocited utontiodies directed ginst pltelet glycoproteins II/III in ptients with idiopthic thromocytopenic purpur. Br J Hemtol 122: , Frulloni L, Lunrdi C, Simone R, et l. Identifiction of novel ntiody ssocited with utoimmune pncretitis. N Engl J Med 361: , Buljic M, Pnic N, Lohr JM. Helicocter pylori nd pncretic diseses. World J Gstrointest Pthophysiol 5: , Cheng YS, Kung LP, Zhung CL, Jing JD, Shi M. Effects of cytotoxin-ssocited gene A (CgA) positive Helicocter pylori infection on nti-pltelet glycoprotein ntiody producing B cells in ptients with primry idiopthic thromocytopenic purpur (ITP). Pk J Med Sci 31: , Bogdnos DP, Bum H, Gunsr F, et l. Extensive homology etween the mjor immunodominnt mitochondril ntigen in primry iliry cirrhosis nd Helicocter pylori does not led to immunologicl cross-rectivity. Scnd J Gstroenterol 39: , Durzzo M, Rosin F, Premoli A, et l. Lck of ssocition etween seroprevlence of Helicocter pylori infection nd primry iliry cirrhosis. World J Gstroenterol 10: , The Jpnese Society of Internl Medicine
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