Metabolic Effects of Hepatic Replacement in Wilson's Disease
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1 Metablic Effects f Hepatic Replacement in Wilsn's Disease By Carl G. Grth, Reuben S. Dubis, Jacques Crman, Ake Gustafssn, Shunzabur watsuki, Denis O. Rdgersn, Charles G. Halgrimsn, and Thmas E. Starzl WLSON's disease is an inbrn disrder f metablism characterized by prgressive accumulatin f cpper in tissues with subsequent degenerative changes that affect mainly the brain and the liver. Disclratin f the crnea by the metal is bservable n split-lamp examinatin as the Kayser-Fleischer ring. Abnrmal bichemical findings may include elevated albumin-bund serum cpper, increased urinary excretin f cpper, lw level f the cpper-cntaining serum prtein cerulplasmin, and lw ttal serum cpper. The nature f the primary metablic defect remians bscure.1 The frequency and significance f severe hepatic invlvement in Wilsn's disease has becme increasingly apparent in the last years.2,3 Clinically, the hepatic disrder is indistinguishable frm ther frms f chrnic hepatitis. Histlgically, there is "pstnecrtic" cirrhsis with alchlic hyaline bdies f Mallry. Tw teen-age bys with liver cirrhsis due t Wilsn's disease have been treated with rthtpic hepatic transplantatin at ur institutin. Studies f the cpper metablism in these patients has prvided imprtant infrmatin cncerning the rle f the liver in Wilsn's disease. Frm the Departments f Surgery and Pediatrics, University f Clrad Schl f Medicine and Veterans Administratin Hspital, Denver, Clrad. Supprted by research grants frm the Veterans Administratin, by Grants RR and RR frm the General Clinic Research Centers prgram f the Divisin f Research Resurces, Natinal nstitutes f Health, and by USPHS Grants A-AM-08898, AM-07772, and HE by Grune & Strattn, nc. CASE REPORTS Patient N.1: An ll-yr-ld by was admitted fr hepatic transplantatin in July His liver disease dated back t the age f 8 when he was fund t have abnrmal liver-functin tests and a liver bipsy shwed "pstnecrtic" cirrhsis. n April 1969 he develped symptms f hepatic failure. A liver bipsy shwed cirrhsis with Mallry bdies; the findings were interpreted as being cnsistent with Wilsn's disease. There were n neurlgical symptms and n Kayser-Fleischer rings. Tw mnths later the patient was transferred t ur institutin in precma. At this time he had massive ascites and anasarca. The serum bilirubin was 20.6 mg/oo ml, the serum albumin 1.5/ ml, the prthrmbin time 13% f nrmal, and bld ammnia 432 lg nitrgen/l00 ml. A few hurs after arrival the patient develped upper gastrintestinal hemrrhage and became agnal. Shrtly afterward a cadaveric dnr became available and the patient underwent an rthtpic hepatic transplantatin.4 Psttransplantatin immunsuppressin included azathiprine r cyclphsphamide, prednisne, and antilymphcyte glbulin4,5 (Fig. 1). After the peratin there was a clearing f the sensrium and a fall in the bld ammnia level. The serum bilirubin diminished (Fig. 1), and ttal serum prtein and the prthrmbin time nrmalized. Tw early rejectin episdes ccurred. At the time f the secnd, there was an extreme degree f hyperbilirubinemia and alkaline phsphatmia (Fig. 1). Reversal f the rejectin was fllwed by 1 yr f nrmal graft functin but in the succeeding years there has been mderate elevatin f SePT and sme episdes f hyperbilirubinemia (Fig. 1). Presently, 3 yr 2 m after transplantatin, the bilirubin is 2.2 mg/loo ml, alkaline phsphatase is 292 U, and sept is 210 U. Tests fr Australia antigen in serum has cnsistently been negative. The patient is clinically well. N dietary limtatins have been impsed and chelating agents have never been administered except fr tw brief tests. Patient N.2. This by was admitted in March 1971 at the age f 14 yr fr hepatic transplantatin. At 11 yr f age liver disease had been diagnsed when he presented with ascites Transplantatin Prceedings, Vl. V, N.1 (March),
2 830 GROTH ET AL. 80 CERULOPLASMN 60 (mg 1 mil g TOTAL SERUM COPPER gg ("g/oo m) URNE COPPER EXCRETON ("9/ 24 hotjr) 500 SGPT (LU.) gg 0 ALKALNE PHOSPHATASE gg (.u.) 50 til BLRUBN (mg/loo mil AZATHOPRNE liliiii OR CYCLOPHOSPHAMDE = (mg/day) PREDNSONE liliiii (mg/day) ORTHOTOPC HEPATC TRANSPLANTATON ! ---- N, p., Ab,G L t,, r , : DAYS MONTHS '-- Fig. 1. The curse in the first patient. and a serum bilirubin f 9.5 mg/oo m!. n the next year there was an imprvement but at 13 yr he had tw episdes f hematemesis. At this time there was mderate neurlgical invlvement with tremr and athettic mvements. Split-lamp examinatin revealed Kayser-Fleischer rings. An pen liver bipsy shwed pstnecrtic cirrhsis. The finding f an elevated cpper cntent in the liver specimen as well as typical abnrmalities in the serum and urine cpper established the diagnsis f Wilsn's disease. A lw-cpper diet was instituted and chelating therapy was attempted initially with D-penicillamine and later with triethylene tetramine dihydrchlride. n spite f increased cupriuresis the patient's neurlgical status deterirated and he became severely crippled with chrea and dysarthria. At the time f transplantatin the serum bilirubin was 2.9 mg/oo m!, serum albumin was 2.9 g/oo ml, and prthrmbin time 44% f nrmal. Pstperative immunsuppressin was as in the first patient except that cyclphsnhamide was given instead f azathiprine during the first 9 rna (Fig. 2). After 1 m f nrmal graft functin there was a sudden rise in the serum bilirubin (maximum 9.6 mg/oo ml), the alkaline phsphatase (maximum 952 U), and the SGPT (maximum U) (Fig. 2). The cncurrent develpment f Australia antigenemia suggested serum hepatitis. Over the next few mnths liver functin became nrmal (Fig. 2). Presently, 17 rna after transplantatin, serum bilirubin is 0.64 mg/oo ml, alkaline phsphatase is 94 U, and SGPT 30 U, all within nrmal limits f ur labratry. After transplantatin the chelating therapy was nt resumed and the dietary limitatin in cpper intake was ablished. During the first 12 rna pstperative the patient's neurlgical status was intermittently imprved but in intervening perids chrea and dysarthria was prminent. On the mst recent neurlgical evaluatin 17 m after peratin a definite imprvement was nted, althugh the symptms had nt cleared cmpletely. Repeated examinatins f the crneas shwed unchanged Kayser-Fleischer rings during the first
3 '----'--'----'-- WLSON'S DSEASE 831 CERULOPLASMN mg/looml) TOTAL SERUM COPPER l"g/oo mil URNE COPPER EXCRETON )Jg/24 hur) SGPT ( U) ALKALNE PHOSPHATASE U BLRUBN mg/loo mil CYCLOPHOSPHAMDE = OR AZATHOPRNE = mg/dayl PREDNSONE _ mg/dayl ORTHOTOPC HEPATC TRANSPLANTATON O-H tt-==-::==::.:.::: lg 20 Lt====t r- r-,, DAYS / 6 B MONTHS Fig. 2. The curse in the secnd patient. 12 m f pstperative fllw-up. At 17 m, hwever, a distinct decrease in clratin was nted. STUDES OF THE COPPER METABOLSM Liver Cpper: The diseased native livers bth had an abnrmally high cpper cntent. The cpper cncentratin in the remved liver f the first patient was 216 pg/g wet weight (nrmal < 20,ug). n the secnd patient a bipsy specimen btained 12 m befre transplantatin cntained 329 Pg cpper/g wet weight. After therapy with chelating agents the remved liver cntained 184 p.gl g wet weight. Bipsy specimens f the hepatic hmgraft btained in the first patient at 6, 17, and 28 m after transplantatin cntained 15, 13, and 17 /Lg f cpper/g wet weight. Histpathlgically, these tissues had minr abnrmalities as previusly reprted.6 n the secnd patient the liver cpper cncentratin was 48, 30, and 45 p.g in bipsy specimens btained after 12, 13, and 17 m, respectively. Histpathlgically, these liver specimens were nrmal. Urinary Cpper Excretin: The first patient had nrmal urinary cpper excretin when studied at anther hspital several mnths befre transplantatin. n cntrast, the secnd patient had an elevated cpper excretin f 340 'g 24 hr (nrmal < 30 'g) befre institutin f chelating therapy. At the time f transplantatin when chelating agent had been given fr 1 yr 540 'g was excreted in 24 h. During the first several mnths after the hepatic replacement, the urinary cpper excretin increased t high levels in the first patient and it remained elevated in the secnd patient. After apprximately 5 m a decrease tward nrmal was nted in bth patients (Figs. 1 and 2). n the last year the first patient has ccasinally excreated increased amunts f cpper (maximum 225 'g/24 hr) (Fig. 2). A 3-day curse f D-penicillamine (1.5 g/day) given t the first patient at 7 and again at 35 m after transplantatin increased the cpper excretin t 974 and 770 /Lg/24 hr, respectively, A similar test in the secnd patient at 12 m psttransplantatin resulted in an excretin f 646 p.g, as cmpared with 1412 'g/24 hr 1 yr befre the peratin.
4 832 Serum Cerulplasmin and Cpper: n the first patient, preperative serum cerulplasmin was within nrmal range except fr ne sample in which it was diminished t 15 mg/loo ml (nrmal mg/loo ml). Serum cpper was nrmal in ne specimen btained at a previus admissin t anther hspital. n the send patient serum cerulplasmin was almst absent with cncentratins f mg/loo ml, and ttal serum cpper cncentratin was lw at tg/loo ml (nrmal tg). After hepatic transplantatin serum cerulplasmins and ttal serum cppers have been nrmal r slightly abve nrmal during the 3 yr 2 m f fllw-up in the first patient (Fig. 1). n the secnd patient, these measures rse within the first weeks after transplantatin t reach nrmal levels. The levels have been subsequently within r abve nrmal range (Fig. 2). DSCUSSON The early wrk-up f the first patient had revealed pstnecrtic cirrhsis with Mallry bdies suggesting Wilsn's disease, but the lack f neurlgic impairment and the absence f Kayser-Fleischer rings as well as the nrmal serum cerulplasmin and cpper made the diagnsis equivcal. As a cnsequence, chelating therapy was never instituted in spite f the prgressive deteriratin in liver functin. When the patient presented at ur institutin his cnditin was n lnger amenable t medical treatment and hepatic transplantatin was carried ut.6 The secnd patient had all the classical clinical and bichemical manifestatins f Wilsn's disease. Cnsequently, lw-cpper diet and therapy with chelating drugs had been tried fr mre than 1 yr. During this time the liver cpper decreased smewhat but there was n evidence f crllary imprvement in hepatic functin. Furthermre, the patient's chrea and dysarthria prgressed t a stage where he was severely crippled. When hepatic transplantatin was carried ut it was hped that the prvisin f a nrmal liver wuld imprve the cpper metablism with cnsequent ameliratin GROTH ET AL. f the extrahepatic manifestatins f the disease. Several findings indicate that the handling f cpper was indeed favrably affected by the hepatic replacement. There was n accumulatin f the metal in the new liver f the first patient. n the secnd patient, the serum cerulplasmin and cpper nrmalized shrtly after transplantatin and bipsy specimens f the graft have shwn nly a slightly elevated cpper cncentratin. The initial high urinary excretin f cpper is cnsistent with clearing f tissue cpper stres, althugh bth patients had cncurrent hepatic dysfunctin with chlestasis which might interfere with biliary excretin f cpper and cause a cmpensatry capriuresis. When later in the curse D-penicillamine was administered ver 3 days, bth patients shwed a cpper excretin nly slightly exceeding that seen in nrmal persns. Finally, the fact that the neurlgic symptms have abated and that the Kayser-Fleischer rings have becme less prminent in the secnd patient indicates that the extrahepatic manifestatins are being favrably affected by the hepatic transplantatin. The present findings are cnsistent with the hypthesis that the metablic defect in Wilsn's disease is liver based. Hpefully, the future curse f these tw patients will prvide grunds fr a definite cnclusin cncerning the rle f the liver in the pathgenesis f the disease. SUMMARY Tw bys with Wilsn's disease had liver replacement 3 and 11/2 yr ag fr terminal hepatic failure and mderate cirrhsis plus severe neurlgic invlvement, respectively. Bth patients had a high liver cpper value but nly the secnd by had lw cerulplasma and ttal serum cpper and increased urinary cpper excretin. Bipsy specimen f the grafts have shwn cpper
5 WLSON'S DSEASE levels that are nrmal r nly slightly elevated. The serum and urine findings in the secnd patient have nrmalized, his neurlgic symptms have abated, and the Kay- 833 ser-fleischer rings have becme less prminent. The findings are cnsistent with the hypthesis that the metablic defect in Wilsn's disease is liver based. 1. Bearn, A. G.: n Stanbury, J. B., Wyngaarden, J. B., and Fredricksn" D. 5. (Eds.): New Yrk, McGraw-Hill, 1972, pp Slvis, T. L., Dubis, R. 5., Rdgersn, D.O., and Silverman, A.: J. Pediatr. 78 :578, Sternlieb,., and Scheinberg, 1. H.: Ann. ntern. Med. 76 :59, Starz!, T. E., and Putnam, C. W.: Experience in Hepatic Transplantatin. Philadelphia, Saunders, REFERENCES 5. Starzl, T. E., Putnam, C. W., Halgrimsn, C. G., Schrter, G. T., Martineau, G., Launis, B., Crman, J. L., Penn, 1., Bth, A. S., Jr., Grth, C. G., and Prter, K. A.: Surg. Gynecl. Obstet. 133 :981, Dubis, R. S., Giles, G., Rdgersn, D.O., Lilly, J., Martineau, G., Halgrimsn, C. G., Schrter, G., Starzl, T. E., Sternlieb, 1., and cheinberg, 1. H.: Lancet 1:505, 1971.
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