Surgical Resection for Hepatocellular Carcinoma with Cardiac Cirrhosis after the Fontan Procedure
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1 CASE REPORT Surgil Resetion for Heptoellulr Crinom with Crdi Cirrhosis fter the ontn Proedure Yoshitk Tkum, Yuji ukd, Shot Iwdou, Hirokzu iytke, Shuji Uemtsu, Ryoihi Okmoto, Disuke Sto 2, Hiroyoshi tsukw 2, Shigehiro Shiozki 2, shiro Kmd 3, Toshiki orito 4 nd Ysuyuki Arki Astrt A 29-yer-old womn who underwent the ontn proedure t 0 yers of ge hd n inidentl finding of liver msses on dominl ultrsonogrphy. Susequent gdolinium ethoxyenzyl diethylenetrimine penteti id mgneti resonne imging showed 5 mm hypervsulr mss with wshout in the heptoiliry phse in liver segment 4 (S4), nd n 8 mm hypervsulr mss without wshout in the heptoiliry phse in liver segment 2 (S2). The S2 liver mss ws pthologilly dignosed to e regenertive nodule y n ultrsound-guided needle iopsy, nd the S4 liver mss ws pthologilly dignosed s poorly differentited heptoellulr rinom fter prtil heptetomy. Key words: heptoellulr rinom (HCC), ontn, rdi irrhosis, surgil resetion (Intern ed 55: , 206) (DOI: 0.269/internlmediine ) Introdution The ontn proedure is used to seprte the systemi nd pulmonry irultions in ptients with vrious forms of funtionlly univentriulr herts. In the ontn irultion, systemi venous return is sent to the pulmonry rteries without pssge through ventrile. The ontn proedure n result in vrious lte omplitions, inluding entrl venous hypertension, diminished oxygen delivery, redued rdi output, venous thromosis, nd rrhythmi (, 2). These omplitions used y entrl venous hypertension led to prenhyml injury, firosis, nd irrhosis of the liver (2, 3). Crdi irrhosis is serious lte omplition of ongenitl hert disese nd n use heptoellulr rinom (HCC) (4, 5). However, the prevlene nd risk ftors of irrhoti hnges nd HCCs hve not een lerly identified. urthermore, non-invsive dignosti tools for hepti firosis nd the mngement of HCC in ptients fter undergoing the ontn proedure hve not yet een lerly estlished. We herein report se of HCC with rdi irrhosis treted with surgil resetion. Cse Report A 29-yer-old womn with history of univentriulr hert hd undergone ontn opertion 0 yers of ge. She lso hd situs inversus. She ws followed-up t the deprtment of peditri rdiology in our hospitl, nd regulrly underwent lood exmintions without lphfetoprotein (AP) t 2- or 3-month intervls. The results showed tht the trnsminse level ws within the norml rnge. On routine follow-up dy, she experiened slight dominl disomfort nd reeived dominl ultrsonogrphy (US). She hd n inidentl finding of liver msses nd ws referred to our deprtment. B-mode onventionl US showed 5 mm hypoehoi mss in liver segment 4 (S4) (ig. ), nd n 8 mm hyperehoi mss in liver segment 2 (S2) (ig. 2). urthermore, the liver prenhym hd orsened pperne onsistent with irrhosis, nd sites nd splenomegly were Deprtment of Internl ediine, Hiroshim City Hospitl, Jpn, Deprtment of Surgery, Hiroshim City Hospitl, Jpn, Deprtment of Peditri Crdiology, Hiroshim City Hospitl, Jpn nd Deprtment of Pthology, Hiroshim City Hospitl, Jpn Reeived for pulition Novemer 20, 205; Aepted for pulition Jnury 7, 206 Correspondene to Dr. Yoshitk Tkum, tkum@enjoy.ne.jp 3265
2 Intern ed 55: , 206 DOI: 0.269/internlmediine d e f igure. Ultrsonogrphy findings (rrows). B-mode onventionl ultrsonogrphy showed 5 mm hypoehoi mss in liver segment 4 (S4) (), the liver prenhym hd orsened pperne onsistent with irrhosis, nd sites nd splenomegly were oserved (, ).CEUS using Sonzoid showed homogeneously enhned mss in the rteril dominnt phse (d), hypoehoi mss reltive to the djent liver prenhym during the portl dominnt phse (e), nd ontrst defet with ler order in the postvsulr phse (f). oserved (ig. nd ). We next performed ontrst-enhned US (CEUS) using olus injetion of 0.05 ml/kg Sonzoid (perfluoroutne; Diihi-Snkyo, Tokyo, Jpn). The mss lesion in S4 ws homogeneously enhned in the rteril dominnt phse (from 0 to 30 seonds) (ig. d). The lesion eme progressively hypoehoi reltive to the djent liver prenhym during the portl dominnt phse (from 30 to 20 seonds) (ig. e), nd provided ontrst defet with ler order in the postvsulr phse (0 minutes lter) (ig. f). The mss lesion in S2 ws homogeneously enhned in the rteril dominnt phse (ig. 2). The lesion eme isoehoi mss reltive to the djent liver prenhym during the portl dominnt phse (ig. 2) nd provided no defets in the postvsulr phse (0 minutes lter) (ig. 2d). We susequently performed mgneti resonne imging (RI) with onventionl T-nd T2-weighted imging (WI) efore nd fter ontrst medi dministrtion, inluding diffusion imging. The ontrst medi used ws heptoytespeifi Primovist [gdolinium ethoxyenzyl diethylenetrimine penteti id (Gd-EOB-DTPA); Byer Shering Phrm, Berlin, Germny]. There ws rdiogrphi evidene of liver irrhosis with portl hypertension, inluding nodulr surfe, orse texture, sites, nd splenomegly on RI (ig. 3 nd ). This imging reveled mss lesion in S4 with modertely low intensity in T-WI (ig. 3) nd modertely high intensity in T2-WI (ig. 3d). In diffusion imging, the lesion showed modertely high intensity (ig. 3e). In the postontrst phses, the lesion reveled homogeneous enhnement in the rteril phse t 20 seonds (ig. 3 nd f), nd wshout in the portl phse t 70 seonds nd interstitil phse t 80 seonds. At 20 minutes (heptoiliry phse) fter the ontrst uptke the lesion showed wshout (ig. 3g). Aording to these findings, finl dignosis of HCC ws mde. In ddition, RI imging reveled mss lesion in S2 with modertely high intensity in T-WI (ig. 4) nd modertely low intensity in T2-WI (ig. 4). In diffusion imging, the lesion showed modertely low intensity (ig. 4d). In the postontrst phses, the lesion reveled homogeneous enhnement in the rteril phse (ig. 4 nd e), n isoenhnement reltive to the djent liver prenhym in the portl nd interstitil phses, nd high intensity in the heptoiliry phse (ig. 4f). The lortory dt re given in Tle. Her liver fun- 3266
3 Intern ed 55: , 206 DOI: 0.269/internlmediine d igure 2. B-mode onventionl ultrsonogrphy showed n 8 mm hyperehoi mss in liver segment 2 (S2) (); nd CEUS showed homogeneously enhned mss in the rteril dominnt phse (), isoehoi mss reltive to the djent liver prenhym during the portl dominnt phse (), nd no defets in the postvsulr phse (d). d e f g igure 3. There ws rdiogrphi evidene of liver irrhosis with portl hypertension, inluding nodulr surfe, orse texture, sites, nd splenomegly on RI (, ). Gd-EOB-DTPA RI showed 5 mm S4 mss with modertely low intensity in T-WI (), modertely high intensity in T2-WI (d), modertely high intensity in diffusion (e), homogeneous rteril enhnement (, f), nd omplete wshout in the heptoiliry phse (g). 3267
4 Intern ed 55: , 206 DOI: 0.269/internlmediine e d f igure 4. Gd-EOB-DTPA RI showed n 8 mm S2 mss with modertely high intensity in TWI (), modertely low intensity in T2-WI (), modertely low intensity in diffusion (d), homogeneous rteril enhnement (, e), nd high intensity in the heptoiliry phse (f). Tle. Results of Blood Tests. Hemtology WBC RBC H Ht PLT Blood iohemistry Serology TP 7.7 g/dl HBsAg Al 4.9 g/dl HBsA ChE 66 IU/L HBA T.Bil.0 mg/dl HCV-A D.Bil 0.5 mg/dl ANA AST 23 IU/L AA-2 ALT 3 IU/L IgG,267 mg/dl Cogultion test LDH 226 IU/L IgA 233 mg/dl PT% 33. % ALP 63 IU/L Ig 23 mg/dl PT-INR.68 DŽ-GTP 47 IU/L AP 7. ng/ml ZTT 8.5 KU AP-L % TTT 4.6 KU CEA 0.4 ng/ml BUN 9mg/dL CA ng/ml Cr 0.79mg/dL CRP 0.00 mg/dl hyluroni id 53 ng/ml type IV ollgen7s 8.5 ng/ml ICG-R5 9.9% WBC: white lood ells, RBC: red lood ells, H: hemogloin, Ht: hemtorit, PLT: pltelets, PT: prothromin time, INR: interntionl normlized rtio, TP: totl protein, Al: lumin, ChE: holinesterse, T.Bil: totl iliruin, D.Bil: diret iliruin, AST: sprtte minotrnsferse, ALT: lnine minotrnsferse, LDH: ltte dehydrogense, ALP: lkline phosphtse, Ȗ-GTP: Ȗ-glutmyltrnspeptidse, ZTT: zin sulfte turidity test, TTT: thymol turidity test, BUN: lood ure nitrogen, Cr: retinine, CRP: C-retive protein, ICG-R: indoynine green retention, HBsAg: heptitis B surfe ntigen, HBsA: heptitis B surfe ntiody, HBA: heptitis B ore ntiody, HCV: heptitis C virus ntiody, ANA: ntinuler ntiodies, AA-2: nti-mitohondril 2 ntiody, AP: lph-fetoprotein, AP-L3: Lens ulinris gglutinin-retive frtion of AP, CEA: rinoemryoni ntigen, CA: rohydrte ntigen /ǍL /ǍL 9.5 g/dl 32.7% /ǍL tion ws well preserved with the Child-Pugh lssifition A, nd her interntionl normlized rtio ws low (the ptient ws on wrfrin for tril rrhythmi). Other l findings inluded high AP level [norml less thn 40 nn- ogrms/milliliter (ng/ml)], high Lens ulinris gglutininretive frtion of AP (AP-L3) (norml less thn 0%), low pltelet ount (norml greter thn 50,000/miroliter), high hyluroni id (norml less thn 50 ng/ml), nd high 3268
5 Intern ed 55: , 206 DOI: 0.269/internlmediine igure 5. A histologil speimen ws otined y n ultrsound-guided needle iopsy of the S2 lesion. irosopi histologil findings reveled ridging firosis in the liver setion. The prenhyml ells did not disply ellulr or struturl typi [Hemtoxylin nd Eosin stining (), nd silver impregntion () with low-power field]. The liver mss in S2 ws pthologilly dignosed s regenertive nodule. type IV ollgen 7S (norml less thn 6.0 ng/ml). An ehordiogrm demonstrted norml ventriulr funtion nd no ostrution in the ontn iruit. The ptient hd no other signifint medil prolems nd no other risk ftors for irrhosis, s she expressed negtivity for virl nd utoimmune mrkers, no loholi onsumption, no heptotoxi drugs (suh s miodrone), nd no metoli ftors suh s dietes mellitus, oesity (her ody mss index ws 7.7), or ftty liver in US. ollowing the reversl of her wrfrin therpy, n ultrsound-guided needle iopsy of the S2 lesion ws performed. Histologil findings reveled tht ridging firosis in the liver setion, nd the prenhyml ells did not disply ellulr or struturl typi (ig. 5). The liver mss in S2 ws pthologilly dignosed to e regenertive nodule. The ptient underwent urtive opertion, involving prtil heptetomy of S4 in the liver. rosopilly, setions of the speimen reveled yellowish-white enpsulted solid tumor mesuring 5 mm in size (ig. 6). The growth pttern of the liver tumor showed expnsive growth with extrpsulr invsions (ig. 6). The tumor ells hd n inresed nuler/ytoplsmi rtio, polymorphi, nd hromtin-rih nulei, nd the pthologil dignosis ws poorly differentited HCC (ig. 6). The nonnerous re of the reseted speimen reveled tht ridging firosis ws oserved without ft deposition, nd the ptient ws dignosed with liver irrhosis (ig. 7). irosis ws oserved in oth the portl nd periellulr res, the sinusoidl struture ws mintined, ut no signifint inflmmtion ws oserved (ig. 7 nd ). After dishrge from the hospitl, the ptient ws followed-up t 3-month intervls. At the -yer follow-up, her AP level ws 2.7 ng/ml, AP-L3 ws less thn 0.5%, nd the tumor mrkers remined norml. urthermore, US nd RI showed no evidene of HCC reurrene. Disussion In the present se, there were no known etiologil ftors suh s heptitis virl infetion, loholi liver disese, utoimmune liver diseses, utoimmune heptitis, primry iliry irrhosis, metoli liver diseses [suh s nonloholi stetoheptitis (NASH)], or medition with heptotoxi drugs (suh s miodrone). oreover, signifint hepti inflmmtion or ft deposition ws not seen s result of proesses suh s heptitis virl infetion or NASH. On histology in the present se, hepti sinusoidl firosis extending from entriloulr res towrd the portl trt without inflmmtion were oserved. Shwrz et l. disussed tht hepti firosis fter the ontn proedure ws mixed disese tht ffets oth the portl nd entriloulr res in liver iopsy nd utopsy speimens (6, 7). Sinusoidl firosis is elieved to result from n inrese in entrl venous pressure trnsmitted to hepti ells tht surround the entrl veins, euse the extent of irrhosis is strongly orrelted with elevted hepti venous pressures nd low rdi index in ptients fter undergoing the ontn proedure (8). After ontn pllition, signifint liver disese n result in entrl venous ongestion nd hypoxi resulting from low rdi output, however, little is known regrding firogeni mehnisms independent of the inflmmtion-medited pthwy in ongestive liver disese (CLD). In CLD, mehnotrnsdution ssoited with strething nd ompression of hepti stellte ells my e potent induer of hepti firosis (9, 0). Using newly hrterized murine CLD model, sinusoidl thromosis nd mehnil strething of djent hepti stellte ells used y sinusoidl dilttion ws shown to indue the relese of fironetin y hepti stellte ells, nd oth firin nd strething stimulted fironetin firil ssemly through β-integrin nd tin-dependent mehnism (). In ddition, hepti omplitions fter the ontn proe- 3269
6 Intern ed 55: , 206 DOI: 0.269/internlmediine igure 6. A mrosopi pperne of the reseted S4 speimen reveled yellowish-white enpsulted solid tumor mesuring 5 mm in size (). irosopilly, the growth pttern of the S4 liver tumor showed expnsive growth with extrpsulr invsions [, Hemtoxylin nd Eosin (H&E) stining with low-power field]. Tumor ells hd n inresed nuler/ytoplsmi rtio, polymorphi, nd hromtin-rih nulei, nd the pthologil dignosis ws poorly differentited HCC (, H&E stining with high-power field). dure re ssoited with the durtion of follow-up (8, 2). Progression to irrhosis my even e oserved within 0 yers fter the initil ontn proedure (3). In 34 ptients with medin follow-up of.5 yers fter the ontn proedure, 30% experiened norml trnsminses, 6% norml γ-gtp, 32% norml iliruin, nd 58% ogulopthy (4). As ompred to durtion of 0-5 yers, the odds rtio of hepti omplitions ws 4.4 for post-ontn durtion of -5 yers nd 9.0 for durtion of 6-20 yers, respetively (2). Liver irrhosis is potentil prerequisite for HCC, however, the prevlene nd progression of irrhoti hnges in the ontn popultion hve not een lerly identified. Noninvsive dignosti tools for hepti firosis re needed, euse liver iopsy, the golden stndrd for dignosing liver irrhosis, is diffiult to perform in ontn ptients due to prophylti ntiogultion. Similr to the present se, rdiologil ssessment of liver firosis using vrious methods suh s US, CT, or RI my e useful. There re severl reports of HCC in ptients with CLD following the ontn proedure. As shown in Tle 2, reent Pued serh identified 2 ses of HCCs mong pulished reports. The pulitions desried the use of surgil resetion, trnstheter rteril hemoemoliztion, rdioemoliztion, lol ltion, or sorfeni therpy (5-22). In previous reports, two ptients were treted with surgil resetion (20, 2). or erly stge HCC, surgil resetion provides urtive tretment with long-time survivl, however, heptetomy is rrely performed following the ontn proedure euse it is diffiult to detet erly stge HCCs. Although the present ptient did not reeive periodi surveillne for HCC, suh s US nd AP, it is fortunte tht erly stge HCC ws inidentlly deteted. HCC deteted fter the onset of symptoms hs poor prognosis (5-yer survivl rte of 0-0%). In ontrst, erly stge HCCs deteted y surveillne n e ured with oth surgil resetion nd liver trnsplnttion (5-yer disese-free survivl rte >50%) (23). Thus, surveillne for HCC my e neessry in ptients with CLD who undergo the ontn proedure euse irrhosis is high-risk ftor for HCC. However, the sreening intervl for liver disese fter the ontn proedure hs not yet een estlished. Surveillne is sed on n ultrsound exmintion, nd the reommended sreening intervl is 6 months ording to the Amerin Assoition for the Study of Liver Diseses (AASLD) prtie guidelines on the mn- 3270
7 Intern ed 55: , 206 DOI: 0.269/internlmediine igure 7. The non-nerous re of the reseted speimen reveled ridging firosis without ft deposition, nd the ptient ws dignosed with liver irrhosis [silver impregntion ()]. irosis ws oserved in oth the portl nd periellulr res, the sinusoidl struture ws mintined, nd signifint inflmmtion ws not seen [silver impregntion (, ) with high-power field]. Tle 2. Reported Cses of Heptoellulr Crinom fter ontn Proedure. Referene No. of ses Age(y) Sex AP (ng/ml) Size (mm) Tretment Outome Systemi hemo , Sorfeni TACE Our se Rdioemoliztion TACE Lol ltion Sorfeni Surgil resetion Surgil resetion TAE Surgil resetion : femle, : mle, : not desried, TACE: trnsrteril hemoemoliztion, TAE: trnsrteril emoliztion gement of HCC (24). In ddition, the AP level in the present se ws high. In Jpn (25), ll ptients with high-risk risk ftors for HCC re dvised to undergo periodi surveillne with US nd lortory work ups, inluding AP nd protein indued y vitmin K sene or ntgonists-ii (PIVKA-II), every 6 months. However, similr to the present se, PIVKA-II is not useful in most ptients fter the ontn proedure euse prophylti ntipltelet with ntiogultion therpies, suh s wrfrin dministrtion, re neessry to prevent thromoemoli events, whih re one of the mjor uses of moridity nd mortlity (26). ollowing the ontn proedure, ptients fe risk of HCC nd require lifelong follow-up with not only peditri rdiologist, ut lso heptologist experiened in the re of ptients with liver irrhosis. We herein desried ptient with HCC who ws le to sfely undergo liver resetion following the ontn proedure under preserved rdi nd hepti funtion. The uthors stte tht they hve no Conflit of Interest (COI). 327
8 Intern ed 55: , 206 DOI: 0.269/internlmediine Referenes. Kendll TJ, Stedmn B, Hking N, et l. Hepti firosis nd irrhosis in the ontn irultion: detiled morphologil study. J Clin Pthol 6: , Wnless IR, Liu JJ, Butny J. Role of thromosis in the pthogenesis of ongestive hepti firosis (rdi irrhosis). Heptology 2: , Kulitz R, Luhmer I, Bergmnn, Rodek B, Husdorf G. Sequele fter modified ontn opertion: postopertive hemodynmi dt nd orgn funtion. Hert 78: 54-59, Wrnes CA, Willims RG, Bshore T, et l. ACC/AHA 2008 guidelines for the mngement of dults with ongenitl hert disese: report of the Amerin College of Crdiology/Amerin Hert Assoition Tsk ore on Prtie Guidelines (Writing Committee to Develop Guidelines on the ngement of Adults With Congenitl Hert Disese). Developed in Collortion With the Amerin Soiety of Ehordiogrphy, Hert Rhythm Soiety, Interntionl Soiety for Adult Congenitl Hert Disese, Soiety for Crdiovsulr Angiogrphy nd Interventions, nd Soiety of Thori Surgeons. J Am Coll Crdiol 52: e43-e263, Asrni SK, Asrni NS, reese DK, et l. Congenitl hert disese nd the liver. Heptology 56: 60-69, Shwrtz C, Sullivn L, Cohen S, et l. Hepti pthology my develop efore the ontn opertion in hildren with funtionl single ventrile: n utopsy study. J Thor Crdiovs Surg 43: , Shwrtz C, Sullivn L, Gltz AC, et l. Portl nd sinusoidl firosis re ommon on liver iopsy fter ontn surgery. Peditr Crdiol 34: 35-42, Kiesewetter CH, Sheron N, Vettukttill JJ, et l. Hepti hnges in the filing ontn irultion. Hert 93: , Rokey DC. Current nd future nti-firoti therpies for hroni liver disese. Clin Liver Dis 2: , xi, Goto T, ikmi KI, iur K, et l. ehnil streth indues mtrix metlloproteinse prodution in humn hepti stellte ells. Pthophysiology : 53-58, Simonetto DA, Yng HY, Yin, et l. Chroni pssive venous ongestion drives hepti firogenesis vi sinusoidl thromosis nd mehnil fores. Heptology 6: , Bek JS, Be EJ, Ko JS, et l. Lte hepti omplitions fter ontn opertion; non-invsive mrkers of hepti firosis nd risk ftors. Hert 96: , Pike NA, Evngelist LS, Doering LV, Konik-Griffin D, Lewis AB, Child JS. Clinil profile of the dolesent/dult ontn survivor. Congenit Hert Dis 6: 9-7, Cmposilvn S, ilnesi O, Stellin G, Pettenzzo A, Znn L, D Antig L. Liver nd rdi funtion in the long term fter ontn opertion. Ann Thor Surg 86: 77-82, Ghferi AA, Huthins G. Progression of liver pthology in ptients undergoing the ontn proedure: Chroni pssive ongestion, rdi irrhosis, hepti denom, nd heptoellulr rinom. J Thor Crdiovs Surg 29: , Sli T, Dorkhom S, O Reilly E, Ludwig E, Gnsukh B, Aou-Alf GK. Heptoellulr rinom in two ptients with rdi irrhosis. Eur J Gstroenterol Heptol 22: , Asrni SK, Wrnes CA, Kmth PS. Heptoellulr rinom fter the ontn proedure. N Engl J ed 368: , Elder RW, Prekh S, Book W. ore on heptoellulr rinom fter the ontn proedure. N Engl J ed 369: 490, Rjoriy N, Clift P, Thorne S, Hirshfield G, erguson JW. A liver mss post-ontn opertion. QJ 07: , Weyker PD, Allen-John We C, Emond JC, Brentjens TE, Johnston TA. Anestheti implitions of extended right heptetomy in ptient with fontn physiology. A A Cse Rep 2: 99-0, Kwon S, Sovel L, Yeh, et l. Surgil mngement of heptoellulr rinom fter ontn proedure. J Gstrointest Onol 6: E55-E60, Ymd K, Shinmoto H, Kwmur Y, et l. Trnsrteril emoliztion for peditri heptoellulr rinom with rdi irrhosis. Peditr Int 57: , Llovet J, Burroughs A, Bruix J. Heptoellulr rinom. Lnet 362: , Bruix J, Shermn ; Amerin Assoition for the Study of Liver D. ngement of heptoellulr rinom: n updte. Heptology 53: , Kudo, Izumi N, Kokudo N, et l. ngement of heptoellulr rinom in Jpn: Consensus-Bsed Clinil Prtie Guidelines proposed y the Jpn Soiety of Heptology (JSH) 200 updted version. Dig Dis 29: , ongle P, Krl TR. Thromoemoli prolems fter the ontn opertion. Semin Thor Crdiovs Surg Peditr Crd Surg Annu 5: 36-47, The Internl ediine is n Open Aess rtile distriuted under the Cretive Commons Attriution-NonCommeril-NoDerivtives 4.0 Interntionl Liense. To view the detils of this liense, plese visit ( y-n-nd/4.0/). 206 The Jpnese Soiety of Internl ediine
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