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1 pissn eissn imri 2015;19: Pncretic Arteriovenous Mlformtion s n Unusul Cuse of Chronic Gstrointestinl Bleeding in Ptient with Erly Gstric Cncer: Multimodlity Imging Spectrum with Pthologic Correltion Cse Report Received: Septemer 23, 2015 Revised: Octoer 23, 2015 Accepted: Octoer 26, 2015 Correspondence to: Jeong Eun Lee, M.D. Deprtment of Rdiology, Chungnm Ntionl University Hospitl, 282 Munhw-ro, Junggu, Dejeon , Kore. Tel Fx Emil: leeje290@gmil.com; ns80@cnuh.co.kr Borhm Lee 1, Jeong Eun Lee 1, June Sik Cho 1, Kyung Sook Shin 1, Sun Kyoung You 1, Kwng Sik Cheon 2, In Sng Song 2, Kyung Hee Kim 3 1 Deprtment of Rdiology, Chungnm Ntionl University Hospitl, Chungnm Ntionl University School of Medicine, Dejeon, Kore 2 Deprtment of Surgery, Chungnm Ntionl University Hospitl, Chungnm Ntionl University School of Medicine, Dejeon, Kore 3 Deprtment of Pthology, Chungnm Ntionl University Hospitl, Chungnm Ntionl University School of Medicine, Dejeon, Kore Arteriovenous mlformtion (AVM) of the pncres is extremely rre, lthough it my e incresingly dignosed due to the widespred use of cross-sectionl imging of the domen. Erly dignosis of this disese is importnt to prevent dely of tretment nd resulting ftl complictions. We report rre cse of pncretic AVM in 48-yer-old mn who presented with severe chronic nemi nd erly gstric cncer, which mde dignosis chllenging. Imging findings, including ultrsound, computed tomogrphy, nd mgnetic resonnce imging, re shown, s well s the pthologic fetures. Keywords: Arteriovenous mlformtions; Pncres; Pncreticoduodenectomy; Mgnetic resonnce imging; Tomogrphy; X-Ry Computed; Ultrsound This is n Open Access rticle distriuted under the terms of the Cretive Commons Attriution Non-Commercil License ( y-nc/3.0/) which permits unrestricted non-commercil use, distriution, nd reproduction in ny medium, provided the originl work is properly cited. Copyright 2015 Koren Society of Mgnetic Resonnce in Medicine (KSMRM) INTRODUCTION Anemi is one of the most common cuses of dizziness. Most chronic nemi is ssocited with gstrointestinl leeding, such s peptic ulcers or cncer of vrious orgns (1). Pncretic rteriovenous mlformtion (AVM) is rre cuse of gstrointestinl leeding (2). They re usully symptomtic ut my present with dominl pin, portl hypertension in the sence of heptopthy, or gstrointestinl leeding. Although pncretic AVM is rre, it should e considered in ptients with nemi of unknown origin or those who filed therpy for more common cuses of nemi. Even though previous studies hve reported the imging findings of pncretic AVM including ultrsound, computed tomogrphy, nd mgnetic resonnce imging, most 241
2 Arteriovenous Mlformtion of the Pncres Borhm Lee, et l. reports include only single or limited numer of imging modlities. We report cse of pncretic AVM in ptient with erly gstric cncer (EGC) nd severe chronic nemi, which ws successfully mnged with pylorus-preserving pncreticoduodenectomy (PPPD) which mde pthologic correltion possile. Concomitnt EGC mde the dignosis of AVM chllenging. Multimodlity rdiologic findings, emphsizing mgnetic resonnce imging (MRI), nd the pthologic correltion re presented. CASE REPORT A 47-yer-old mn ws referred to our hospitl to determine the cuse of his dizziness. He ws dignosed with n iron deficiency nemi of unknown origin 2 yers prior to dmission t our hospitl. His hemogloin level decresed to 6.2 g/dl. Cogultion profile ws within the norml rnge, with the interntionl normlized rtio (INR) of 1.01, ctivted prtil thromoplstin time of 24.4 s, nd pltelets of /µl. Other lortory dt were grossly norml, prt from elevted levels of totl mylse of 279 U/L, lipse of 724 IU/L, nd totl iliruin of 2.00 mg/dl. The ptient tested negtive for heptitis B nd C viruses. Upper gstrointestinl (UGI) endoscopy showed n pproximtely 0.5 cm flt, depressed lesion in the lesser curvture of the ntrum of the stomch tht ws confirmed s n denocrcinom using n endoscopic iopsy. He underwent contrst-enhnced multidetector computed Tle 1. MR Imging Sequence nd Prmeters Sequence TR/TE (msec) FA Section thickness (mm) Mtrix size FOV (cm) Breth-hold multishot T2WI / x x 360 Breth-hold single-shot hevily T2WI / x x 360 Nvigtor-triggered hevily T2WI, thin section / x x 350 DWI ( = 800) / x x 370 CE-T1WI 3.2/ x x 360 Breth-hold multishot 2D MRCP 1800/ x x 330 2D = two dimensionl; CE-T1WI = contrst enhnced-t1 weighted imging; DWI = diffusion weighted imging; FA = flip ngle; FOV = field of view; MRCP = mgnetic resonnce cholngiopncretogrphy; T2WI = T2 weighted imging; TE = echo time; TR = repetition time * CE-T1WI ws cquired fter the dministrtion of Gdoxette disodium (Primovist, Gd-EOB-DTPA, Byer Schering Phrm, Berlin, Germny) t dose of 0.1 mmol/kg nd n injection rte of 1 ml/sec. Fig. 1. Pncretic rteriovenous mlformtion in 41-yer-old mn, CT findings. () Axil scn, during the rteril phse, shows n irregulrly tngled hypervsculr lesion in the pncretic hed. () In the delyed phse, the lesion is difficult to define ecuse of isodense enhncement reltive to norml pncretic prenchym. 242
3 tomogrphy (Senstion 64; Siemens Helthcre, Erlngen, Germny) of the domen t tht time. The CT scn otined during the rteril phse reveled n irregulr shped hypervsculr lesion of cm in the pncretic hed without evidence of vsculr or djcent orgn invsion. In the portl venous phse, this lesion ws slightly more enhnced reltive to the norml pncretic prenchym. It ws difficult to define ecuse of isodense enhncement c d Fig. 2. Pncretic rteriovenous mlformtion in 41-yerold mn, MRI findings. (, ) T2-weighted imging shows the chrcteristic clustered tuulr signl void (rrows). (c-e) Axil scn during the rteril phse of dynmic T1-weighted imging shows n irregulrly tngled hypervsculr lesion in the pncretic hed (c) nd erly enhncement of the dilted portl vein (d) nd pncreticoduodenl vein (rrow) tht drined into the dilted portl vein (e). e 243
4 Arteriovenous Mlformtion of the Pncres Borhm Lee, et l. during the delyed phse (Fig. 1). For further evlution, he underwent MRI of the domen using 3.0-Tesl (T) MRI system (Achiev; Philips Medicl System, Bothell, WA, USA) using the prmeters presented in Tle 1. On T2-weighted imges, clustered tuulr structures nd dilted pncreticoduodenl vein demonstrting chrcteristic signl void, indicting the presence of rpid lood flow. This lesion did not show mss effect or diltion of the min pncretic duct. After n intrvenous injection of prmgnetic contrst gent, the enhncement oserved ws similr to tht of the ort. Dynmic T1- weighted imging during the rteril phse showed erly filling of the proximl portions of the superior mesenteric vein nd superior nd inferior pncreticoduodenl veins tht drined into the dilted portl vein (Fig. 2). For further hemodynmic evlution, noninvsive Doppler ultrsonogrphy (iu22 unit; Philips Medicl System, Bothell, WA, USA) ws performed. Color Doppler ultrsonogrphy showed mosic pncretic color flow pttern with dilttion of the heptic portl vein nd pncreticoduodenl vein. On spectrl Doppler ultrsonogrphy, we found rteril wveforms with incresed velocity showing pulstile pttern, indicting the drining role of the portl vein (Fig. 3). These clinicl nd rdiologic findings led to the dignosis of EGC nd pncretic AVM. The clinicin thought tht his chronic nemi hd risen from EGC ecuse cncer is one of the most common cuses of chronic gstrointestinl leeding. He susequently underwent endoscopic sumucosl dissection (ESD). After tretment of EGC, we expected tht his symptoms, nd lortory profile relted to nemi, would improve. However, lortory findings (including hemogloin levels) did not normlize. Immeditely fter ESD, the ptient s hemogloin level ws 8.6 g/dl, ut 9 Fig. 3. Pncretic rteriovenous mlformtion in 41-yerold mn, US findings. () A gry-scle ultrsonogrm demonstrtes n ill-mrginted nechoic lesion (rrows) round the hed of the pncres. () On color Doppler ultrsonogrm shows mosic color flow pttern with lrge mount of color signls round the pncres. (c) Spectrl Doppler ultrsonogrm of the min portl vein revels pulstile pttern, suggesting the drining role of the portl vein. c 244
5 months fter ESD, it hd reduced to 4.5 g/dl. On follow-up UGI endoscopy, intermittent leeding ws suspected sed on petechil lesion nd ple mucos in the second portion of the duodenum without n ctive leeding focus. We concluded tht the cuse of duodenl leeding ws pncretic AVM locted in the hed of the pncres. At the sme time, there were no clinicl signs of portl hypertension which ws good indiction of erly surgicl removl nd good prognosis. Although trnsctheter rteril emoliztion with n-utyl-2-cynocrylte could e nother tretment option, surgicl resection of the ffected orgn ws recommended s the only curtive tretment in ptient with good indictions (3). After sufficient discussion etween the ptient, clinicins, nd rdiologists, the ptient underwent PPPD, nd the surgicl findings included ulky pncretic hed with multiple collterls. Despite mssive intropertive leeding, the pncretic mss ws successfully removed. Multiple honeycom-like dilted spces were found in the pncretic hed nd the uncinte process in the surgicl specimen (Fig. 4). Histopthologic exmintion of the resected pncres showed irregulrly dilted ngiodysplstic vessels, composed of thick-wlled rtery nd thin-wlled vein connections with irregulr dupliction (Fig. 4). Finlly, the smple ws pthologiclly confirmed s pncretic AVM. The ptient recovered uneventfully. Immeditely fter PPPD, the ptient s hemogloin level reched 8.1 g/dl nd grdully improved during follow-up. The ptient hs een well for 1 yer since the opertion, nd his hemogloin level normlized t 13.2 g/dl without complictions. Fig. 4. Pncretic rteriovenous mlformtion in 41-yerold mn, gross nd microscopic findings. () A cut section of the pncres shows multiple honeycom-like dilted spces. (, c) Histopthologic exmintion of the resected pncres revels irregulrly dilted ngiodysplstic vessels in the pncres ( 40, H&E stining) () nd thick-wlled rtery nd thin-wlled vein connections with irregulr dupliction (rrows) ( 100, elstin stining) (c). c 245
6 Arteriovenous Mlformtion of the Pncres Borhm Lee, et l. DISCUSSION Pncretic AVM is very rre. According to Meyer et l. (4), the most common site of AVM is the cecum nd right colon (78%), followed y the jejunum (10.5%), wheres only 0.9% of ll AVMs re found in the pncres (4). The cuse of pncretic AVM is thought to e congenitl in 90% of cses, nd 10% to 30% of pncretic AVM re ssocited with Osler-Weer-Rendu disese (3). Severl cses of cquired pncretic AVM occurred ecuse of pncretitis, trum, nd tumors. As our ptient hd no history of pncretitis or liver cirrhosis, the pncretic AVM ws thought to e congenitl. The most common presenttion of pncretic AVM is gstrointestinl leeding. Ptients with pncretic AVM cn lso present with dominl pin, cused y the shunting of lood wy from the mesenteric circultion through the AVM. Jundice, secondry to hemoili, is possile, ut rre, clinicl mnifesttion of AVM. According to prior report (5), gstrointestinl leeding cn e cused y duodenl ulcer or duodenitis leeding ssocited with the pncretic AVM, direct leeding from the pncretic AVM to the pncretic duct or ile duct, or leeding from esophgel or gstric vrices ssocited with portl hypertension. Among these cuses, duodenl ulcer or duodenitis ppered to hve risen from regionl ischemi cused y the disesed mucos (6). In our cse, the ptient complined only of dizziness without ny dominl pin or jundice, nd there ws no direct evidence of gstrointestinl leeding, such s melen or hemtochezi, preopertively. However, chronic leeding might hve occurred, considering the low hemogloin level. Concomitnt EGC contriuted to the delyed dignosis of the exct cuse of the chronic nemi, even though it ws smll lesion, ecuse cncer is one of the most common cuses of nemi. Although there ws no direct evidence of mssive gstrointestinl leeding, chronic occult lood loss might hve occurred from petechil lesion in the second portion of the duodenum ssocited with pncretic AVM, considering improvement of his lortory profile fter PPPD. Pncretic AVM is dignosed using CT, MRI, color Doppler ultrsonogrphy, nd ngiogrphy. Contrst-enhnced dynmic CT shows multiple, pronounced enhncements of smll hypervsculr spots in the lesion. Bsed on these CT findings, hypervsculr pncretic cncer cnnot e ruled out in the differentil dignosis, especilly for inexperienced rdiologists. In such cse, chrcteristic signl void on T1- nd T2-weighted imging could provide the dignostic clue for pncretic AVM. This signl void is chrcteristic of rpid lood flow (7). After enhncement, erly contrst filling of the enlrged portl venous system ws seen in the rteril phse. In ddition, demonstrtion of enhncement of the lesion, commensurte with the ort, on contrst enhnced multiphsic imging is helpful in dignosing pncretic AVM (2). On the other hnd, color Doppler ultrsonogrphy shows delineted hypervsculr, hypoechoic mss with mosic color flow pttern t the site of the mlformtion tht is helpful in evluting hemodynmic chnges. One of the most importnt findings on spectrl Doppler ultrsound is pulstile wve form with high flow velocity of drining portl vein system (8). Angiogrphy plys n importnt role in confirmtory exmintion, s well s plnning tretment (7). The ngiogrphic findings include dilted nd tortuous feeding rteries, rcemose intrtumorl vsculr network, followed y trnsient vid pncretic stin, erly venous filling into the portl vein, nd erly wsh-out of the pncretic stin (9). However, these findings re lso oserved in other conditions such s pncretitis or hypervsculr neoplsms (10). We did not perform ngiogrphy on our ptient ecuse we plnned surgicl resection, nd the ptient did not wnt to undergo n invsive ngiogrphic study. Mngement of pncretic AVM my involve surgicl nd conservtive therpy, such s rteril emoliztion, irrdition, or portovenous shunts. Nishiym et l. (3) recommended totl surgicl resection of the ffected orgn s the only curtive tretment. If the lesion is surgiclly removed t n erly stge, prior to the ptient developing portl hypertension, the ptient hs good prognosis. Although surgicl resection is the tretment of choice, it hs limited role in treting ptients with lrge, complicted pncretic AVM, s they hve high risk of mssive intropertive leeding (8). Fortuntely, our ptient ws n pproprite surgicl cndidte, nd susequently underwent surgicl resection. He recovered uneventfully nd hs not experienced gstrointestinl leeding since the surgery. Although severl previous reports offer estlished imging findings of pncretic AVM, unlike our cse, these reports provide single or limited imging modlities. Becuse our ptient underwent MRI, CT, nd noninvsive Doppler ultrsonogrphy for evlution, we were le to correlte severl findings of the lesion etween multimodlities nd mde comprehensive conclusion efore surgicl tretment. It is very importnt for inexperienced rdiologists 246
7 to rememer tht pncretic AVM is esily differentited from hypervsculr mss on CT imges when using signl void on T2-weighted MR imge. Furthermore, we cn correlte these vrious findings of multimodlities directly with pthology fter PPPD. Becuse most ptients with pncretic AVM re treted with rteril emoliztion using n-utyl-2-cynocrylte, rther thn PPPD, our report is meningful nd presents rre cse of multimodlity imging spectrum with pthologic correltion. In summry, lthough pncretic AVM is rre disese, it should e included in the differentil dignosis s cuse of chronic nemi of unknown origin, or for therpeutic filure for more common cuses of nemi. Fmilirity with imging findings of pncretic AVM on CT, MRI, nd ultrsonogrphy, s shown in this cse, will id in the erly dignosis in uncertin cses. In ddition, signl void on MRI is dignostic clue in cses of pncretic hypervsculr lesions. REFERENCES 1. Rockey DC. Occult gstrointestinl leeding. N Engl J Med 1999;341: Hnsen W, Mximin S, Shriki JE, Bhrgv P. Multimodlity imging of pncretic rteriovenous mlformtion. Curr Prol Dign Rdiol 2015;44: Nishiym R, Kwnishi Y, Mitsuhshi H, et l. Mngement of pncretic rteriovenous mlformtion. J Heptoiliry Pncret Surg 2000;7: Meyer CT, Troncle FJ, Gllowy S, Shehn DG. Arteriovenous mlformtions of the owel: n nlysis of 22 cses nd review of the literture. Medicine (Bltimore) 1981;60: Aid K, Nkmur H, Kihr Y, Ae S, Okmoto K, Otsuki M. Duodenl ulcer nd pncretitis ssocited with pncretic rteriovenous mlformtion. Eur J Gstroenterol Heptol 2002;14: Koito K, Nmieno T, Ngkw T, et l. Congenitl rteriovenous mlformtion of the pncres: its dignostic fetures on imges. Pncres 2001;22: Mkhoul F, Kur P, Johnston TD, Jeon H, Gedly R, Rnjn D. Arteriovenous mlformtion of the pncres: cse report nd review of literture. Int J Angiol 2008;17: Yoon JH, Hn SS, Ch SS, Lee SJ. Color Doppler ultrsonogrphy of pncretic rteriovenous mlformtion. J Ultrsound Med 2005;24: Wlter JF, Chung VP, Bookstein JJ, Reuter SR, Cho KJ, Pulmno CM. Angiogrphy of mssive hemorrhge secondry to pncretic diseses. Rdiology 1977;124: Chng S, Lim HK, Lee WJ, Choi D, Jng KT. Arteriovenous mlformtion of the pncres in ptient with gstrointestinl leeding: helicl CT findings. Adom Imging 2004;29:
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