Impaired acetaldehyde oxidation in alcoholics*
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1 Impaired aetaldehyde oxidation in aloholis* K R PALMR and W J JNKINSt From the Aademi Department of Mediine, Royal Free Hospital, London Gut, 1982, 23, SUMMARY High blood aetaldehyde levels in aloholis after ethanol ingestion are due to redued aetaldehyde oxidation rather than to an inreased rate of its formation from ethanol. This is assoiated with low hepati aetaldehyde dehydrogenase ativity in aloholi subjets and may represent a speifi abnormality in them. Aetaldehyde, whih is formed during ethanol metabolism in the liver, is extremely toxi. It has been suggested as an important agent in the pathogenesis of aloholi liver disease, 1-3 and as a basis for alohol addition.4 5 After drinking ethanol most aetaldehyde is not only formed in the liver, but is also immediately oxidised there, so that little enters the blood in normal subjets.6 7 In aloholis given infusions of ethanol, however, higher blood levels of aetaldehyde have been reported.7 Both a 'viious yle' theory of aloholi liver injury mediated by aetaldehyde9 and a primary abnormality of aetaldehyde metabolism predisposing to aloholism1 have been suggested to explain this differene, but the reason for it remains unlear, and the original studies have been ritiised beause the methods used to measure aetaldehyde were inadequate.1" More aetaldehyde may leave the liver in the blood if the rate of its formation from ethanoll whih ours during ethanol metabolism.17 It was inreases, or if the liver's apaity to oxidise therefore determined in some of the patients during aetaldehyde falls. In aloholis both mehanisms the ethanol-loading study. are possible, as the rate of ethanol metabolism may be inreased12 13 and the ativity of hepati aetaldehyde dehydrogenase (aetaldehyde dehydro- Methods genase) is redued.14 In the majority of biohemial reations, however, enzyme ativity is not the rate-limiting fator, so that a redution in hepati aetaldehyde dehydrogenase ativity may not neessarily limit aetaldehyde oxidation in the liver, just as alohol dehydrogenase ativity is not ratelimiting for the oxidation of ethanol. 16 In this study both these possible mehanisms were Presented in part to the British Soiety of Gastroenterology Meeting, Bristol t Address for orrespondene: Dr W J Jenkins, Department of Mediine, Royal Free Hospital Shool of Mediine, London, NW3 2G Reeived for publiation 18 January 1982 investigated. Aloholi and ontrol subjets were given ethanol orally, and the onentrations of ethanol and aetaldehyde in the blood were measured at intervals afterwards. In addition, the speifi ativity of aetaldehyde dehydrogenase was assayed in liver biopsies from some of the aloholi patients. As the redued speifi ativity of hepati aetaldehyde dehydrogenase observed in the aloholi patients might be a non-speifi onsequene of liver damage, aetaldehyde dehydrogenase ativity was also assayed in liver biopsies from patients with other forms of liver disease, and in some other ontrol subjets. NAD is an essential ofator for aetaldehyde oxidation in the liver, so that hepati NADH/NAD ratio is another possible influene at this reation. The latate/pyruvate ratio in the blood reflets the dramati hange in hepati NADH/NAD ratio Seventeen male aloholi subjets and nine healthy male ontrol subjets were studied. Their linial and biohemial details are shown in the Table. All the aloholi subjets had regularly onsumed more than 8g ethanol daily for at least two years, and had ontinued to do so until 48 hours before the study. After an overnight fast eah subjet drank lg ethanol/kg body weight as a 1% solution (w/v) in orange juie over 1 minutes. Venous blood samples for the estimation of ethanol and aetaldehyde were taken through an indwelling silionised annula before and for six hours after the ethanol was drunk. Samples were taken every 15 minutes for two hours, and then every 3 minutes. Blood ethanol and 729 Gut: first published as /gut on 1 September Downloaded from on 5 July 218 by guest. Proteted by opyright.
2 73 Palmer and Jenkins Table Clinial and biohemial data ofsubjets in enthanol-loading study Mean + SD Histology Number Age (yr) AST (lull) Albumin (gll) GGT (IUll) MCV (fl) Controls 9 33( 5) 15( 5) 46(4) 38( 15) 85( 4) Fattyliver 9 49( 9) 33(12) 46(4) 155( 5) 99( 5) Aloholi hepatitis 5 46 ( 8) 57(24) 46(4) 198( 8) 16(14) Aloholi irrhosis 3 58(1) 7(5) 37(2) 485 (146) 99 ( 8) Normal range aetaldehyde were assayed simultaneously by the head-spae gas hromatography method of Brien and Loomis.18 This method gives similar results to the more omplex semiarbazide method of Stowell.19 It prevents the non-enzymati formation of aetaldehyde from ethanol in blood, and gives an 84% reovery of 22 gmolal aetaldehyde (final onentration) added to blood. The rates of ethanol oxidation,2 and the mean blood aetaldehyde onentrations were alulated in ontrol and aloholi subjets, and the differenes between the two groups were analysed using the Wiloxon rank test. Blood latate and pyruvate onentrations were assayed by standard methods21 22 in 1 of the aloholi patients before, and 6 and 9 minutes after the ethanol was drunk. HPATIC ACTALDHYD DHYDROGNAS ACTIVITY The speifi ativity of aetaldehyde dehydrogenase was measured in liver biopsies from 1 of the patients who took part in the ethanol-loading study, and in 2 other patients with aloholi liver disease. It was also assayed in eight patients with other forms of liver disease, and in 1 subjets undergoing diagnosti liver biopsy to exlude liver disease, but who had normal serum liver funtion tests at the time, and whose biopsies were subsequently shown to be histologially normal. Aetaldehyde dehydrogenase ativity in the liver biopsies was assayed by a gas hromatographi method.23 It involves repeated measurement of aetaldehyde in the head-spae gas above an inubation mixture ontained within a sealed vial. This method gives values for the speifi ativity of hepati aetaldehyde dehydrogenase similar to those obtained by a standard spetrophotometri assay, 14 if the same onentration of aetaldehyde is used.23 In this study a low onentration of aetaldehyde (23,mol/l) was used to inrease the preision of the assay. Consequently the speifi ativities of hepati aetaldehyde dehydrogenase are lower than those previously reported.14 Protein has been shown previously to be a satisfatory referene for the speifi ativity aloholi liver disease.24 Lowry method.25 Results of hepati enzymes in It was measured by the Figure 1 shows the blood ethanol and aetaldehyde onentrations measured at intervals after the ethanol was drunk in the ontrol and aloholi groups. Although the peak values of blood ethanol were slightly higher in the aloholi subjets, the mean rate of ethanol oxidation (132±28 (SD) mg/h/kg) did not differ signifiantly from that in ontrol subjets (13±3 mg/h/kg). In ontrast, blood aetaldehyde onentrations were signifiantly higher in the aloholi group than in the ontrol group at all time points exept 12 minutes. The mean blood aetaldehyde onentrations over the six hour period after ethanol loading were 17.8±6 (SD),umol/l in the aloholi subjets and 9.2 LU o m o Time after ethanol (Min) I u Fig. 1 Blood ethanol and aetaldehyde onentrations (mean ± SM) in aloholi (n=177) and ontrol nine subjets. (1 mmol/l ethanol = 4.6mg%). Z U -o.: 2.2 U CD Uj Gut: first published as /gut on 1 September Downloaded from on 5 July 218 by guest. Proteted by opyright.
3 Impaired aetaldehyde oxidation in aloholis 1.±4,umol/l in the ontrols (p<.1). The mean blood aetaldehyde onentration after drinking ethanol did not vary signifiantly with age in either ontrol or aloholi subjets, and in the aloholi group it did not orrelate with either abnormal serum liver funtion tests or the histologial severity of the liver damage. In the aloholi patients, however, the speifi ativity of hepati aetaldehyde dehydrogenase was signifiantly lower (p<1) than in both normal subjets of a similar age (mean 46.3±11 (SD) years), and patients with other forms of liver disease (mean age 52-5±6 years) (Fig. 2). There was also a signifiant inverse relationship (p<5) between the speifi ativity of aetaldehyde dehydrogenase in the liver biopsies from the aloholi patients and the mean onentration of aetaldehyde in their blood after drinking ethanol (Fig. 3). There was a similar inverse relationship between the mean blood latate/pyruvate ratio 6 and 9 minutes after ethanol and the mean blood aetaldehyde onentrations (Fig. 4). Disussion This study onfirms that reently drinking aloholis have higher onentrations of aetaldehyde in C. -.5 :6 *a = ) CD JUCD 'V IS U A. v. a:. v Steatosis Hep. Cir. ALCOHOL- CONTROL ALCOHOLIC LIVR DIS. ULIVRD S Fig. 2 Hepati aetaldehyde dehydrogenase ativities in biopsies from aloholi, ontrol, and alohol-unrelated liver disease subjets with mean ± SMfor eah group. (The alohol-unrelated liver disease group omprised hroni ative hepatitis (two subjets), ryptogeni irrhosis (two), intrahepati holestasis (two), drug reations (one), and primary biliary irrhosis (one) ). a I a, g.c a, U9i 9 l l r = -.68 p <.5 range () ( 6 Ald-DH Ativity (nmoles aetaidehyde oxidised/minlmg protein) Fig. 3 Relationship between mean blood aetaldehyde onentration and hepati aetaldehyde dehydrogenase ativity in 1 aloholi subjets.. X :p IT C Q U UC 8 m. n r= -.87 p<o.l O Mean blood latate: Pyruvate ratio 619 mins after ethanol Fig. 4 Relationship between mean blood aetaldehyde onentration and mean blood latatelpyruvate ratio after ethanol in 1 aloholi subjets.. ---n 731 Gut: first published as /gut on 1 September Downloaded from on 5 July 218 by guest. Proteted by opyright.
4 732 Palmer and Jenkins venous blood after drinking ethanol than normal subjets. This differene does not result from an inreased rate of aetaldehyde prodution from ethanol in the aloholis, as the rates of ethanol oxidation were similar in the aloholi and ontrol groups (Fig. 1). The higher blood levels in the aloholis are probably due to redued oxidation of aetaldehyde in the liver, where the majority of aetaldehyde formed from ethanol is normally metabolised. The hepati ativity of aetaldehyde dehydrogenase has previously been shown to be redued in aloholis,' and numerous animal experiments have suggested that its ativity in the liver is rate-limitin for hepati oxidation of aetaldehyde.2 29 Hepati aetaldehyde dehydrogenase ativity is probably rate-limiting for the oxidation of aetaldehyde in human liver too, as there was a signifiant inverse relationship between the mean venous blood aetaldehyde onentration after ethanol and the aetaldehyde dehydrogenase ativity assayed in liver biopsies from our aloholi patients (Fig. 3). In ontrast, the inverse relationship between the mean venous blood aetaldehyde onentration and the blood latate/pyruvate ratio after ethanol administration (Fig. 4) indiates that the hepati redox state does not regulate aetaldehyde metabolism in the liver, as a positive orrelation would be expeted if it did. Similar results have been obtained in animal studies.27 3 Whether the redution in hepati aetaldehyde dehydrogenase ativity in aloholis represents a primary abnormality, or is seondary to liver damage remains unknown. The lak of an assoiation between redued hepati aetaldehyde dehydrogenase ativity and either abnormalities of serum liver funtion tests, or histologial severity of the liver lesion in the aloholis (Fig. 2), and the finding of almost normal levels of ativity in other forms of liver disease, however, lead us to suggest that redued hepati aetaldehyde dehydrogenase ativity may represent a primary abnormality at least in some aloholis. Suh a primary redution in hepati aetaldehyde dehydrogenase ativity may go some way in explaining the inheritane of impaired aetaldehyde metabolism previously reported in the healthy non-aloholi sons of aloholi fathers. 1 We wish to thank Professor Dame Sheila Sherlok for permission to study patients under her are. The Medial Counil for Aloholism supported this study and KRP was supported by the British Soiety of Gastroenterology and the Wellome Trust. Referenes 1 Lieber CS. Alohol, protein metabolism and liver injury. Gastroenterology 198; 79: Cederbaum AI, Lieber CS, Rubin. The effet of aetaldehyde on mitohondrial funtion. Arh Biohem Biophys 1974; 161: Cederbaum AI, Lieber CS, Rubin. ffet of aetaldehyde on fatty aid oxidation and ketogenesis by hepati mitohondria. Arh Biohem Biophys 1975; 169: Myers RD. Tetrahydroisoquinolines in the brain: the basis of an animal model of addition. Aloholism. Clin xp Res 1978; 2: Davies V, Walsh MJ. Alohol, amines and alkaloids: possible biohemial basis for alohol addition. Siene 197; 167: riksson CJP, Peahey J. Lak of differene in blood aetaldehyde of aloholis and ontrols after ethanol ingestion. Pharmaol Biohem Behav 198; 13: Lindros KO, Stowell A, Pikkarainen P, Salaspuro M. levated blood aetaldehyde in aloholis with aelerated ethanol elimination. Pharmaol Biohem Behav 198; 13: Korsten MA, Matsuzaki S, Feinman L, Lieber CS. High blood aetaldehyde levels after ethanol administration. Differene between aloholis and non-aloholi subjets. N nglj Med 1975; 292: Hasumura Y, Teshe R, Lieber CS. Aetaldehyde oxidation by hepati mitohondria: derease after hroni ethanol onsumption. Siene 1975; 189: Shukitt MA, Rayses V. thanol ingestion: differene in blood aetaldehyde onentration in relatives of aloholis and ontrols. Siene 1979; 23: riksson CJP. Problems and pitfalls in aetaldehyde determination. Aloholism. Clin xp Res 198; 4: Ugarte G, Pereda T, Pino M, Iturriaga H. Influene of alohol intake, length of abstinane and meprobamate on the rate of ethanol metabolism in man. Q J Stud Al 1972; 33: Kater RMH, Carulli N, Iber FL. Differenes in the rate of ethanol metabolism in reently drinking aloholi and non-drinking subjets. Am J Clin Nutr 1969; 22: Jenkins WJ, Peters TJ. Seletively redued hepati aetaldehyde dehydrogenase in aloholis. Lanet 198; 2: Meijer AJ, Van Woekom GM, Williamson JR, Tager JM. Rate limiting fators in the oxidation of ethanol by isolated rat liver ells. Biohem J 1975; 15: Li TK. nzymology of human alohol metabolism. Adv nzymol 1977; 45: Salaspuro MP, Lindros KO, Pikkarainen PH. ffet of 4 methyl pyrazole on ethanol elimination rate in aloholis with adequate or inadequate nutrition and in non-aloholi ontrols. Metabolism Clin xp 1978; 27: Brien JF, Loomis CW. Gas liquid hromatographi determination of ethanol and aetaldehyde in blood. Clin Chim Ata 1978; 87: Stowell AR. An improved method for the determina- Gut: first published as /gut on 1 September Downloaded from on 5 July 218 by guest. Proteted by opyright.
5 Impaired aetaldehyde oxidation in aloholis 733 tion of aetaldehyde in human blood with minimal ethanol interferene. Clin Chim Ata 1979; 98: Kalant H. Absorption, diffusion, distribution and elimination of ethanol: effets of biologial membranes. In: Kissen B, Begleiter H, eds. The biology of aloholism vol 1. Biohemistry. London: Plenun Press, 1971: Gutman I, Wahlefeld AW. L- (+) -Latate. Determination with latate dehydrogenase and NAD. In: Bergmeyer HU, ed. Methods of enzymi analysis vol 2. New York and London: Aademi Press 1977: Czok RW, Lampreht W. In: Bergmeyer HU, ed. Methods of enzymi analysis vol 2. New York and London: Aademi Press: Palmer KR, Jenkins WJ. An improved method for the determination of aldehyde dehydrogenase in human liver biopsies using gas hromatography. Clin Chim Ata 1981; 155: Jenkins WJ, Peters TJ. Mitohondrial enzyme ativities in liver biopsies from patients with aloholi liver disease. Gut 1978; 19: Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193: Shepperd JR, Albershiem P, MClearn G. Aldehyde dehydrogenase and ethanol preferene in mie. J Biol Chem 197; 245: riksson CJP. thanol and aetaldehyde metabolism in rat strains genetially seleted for their ethanol preferene. Biohem Pharmaol 1973; 22: Koivula T, Kiovusalo M, Lindros K. Liver aldehyde dehydrogenase ativities in rat strains genetially seleted for their ethanol preferene. Biohem Pharmaol 1975; 24: Petersen DR, Collins AC, Dietrih RA. Role of liver ytosoli aldehyde dehydrogenase isoenzyme in ontrol of blood aetaldehyde onentrations. J Pharmaol xp Ther 1977; 21: Lindros KO. Regulatory fators in hepati aetaldehyde metabolism during ethanol oxidation. In: Lindros KO, riksson CJP, eds. The role of aetaldehyde in the ations of ethanol. Helsinki: Finnish Foundation of Alohol Studies, 1957: Gut: first published as /gut on 1 September Downloaded from on 5 July 218 by guest. Proteted by opyright.
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