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Enterohepatic Circulation of Bile Acids After Cholecystectomy

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Enterohepatic Circulation of Bile Acids After Cholecystectomy Gut: first published as 10.1136/gut.19.7.640 on 1 July 1978. Downloaded from Gut, 1978, 19, 640-649 Enterohepatic circulation of bile acids after cholecystectomy E. RODA1, RITA ALDINI, G. MAZZELLA, A. RODA, CLAUDIA SAMA, D. FESTI, AND L. BARBARA From the Department of Gastroenterology and Institute of Chemistry, University of Bologna, Italy SUMMARY Bile acid metabolism was investigated in 10 patients after cholecystectomy, 10 gallstone patients, and 10 control subjects. Diurnal variations of serum levels of cholic and chenodeoxy- cholic acid conjugates were not abolished by cholecystectomy. Cholic acid pool size was significantly reduced in cholecystectomised patients and the fractional turnover rate and the rate of intestinal degradation of bile acid showed a significant increase. In cholecystectomised patients fasting bile was supersaturated in cholesterol, though less than in gallstone patients, but, in both, feeding resulted in improvement of cholesterol solubility in bile. These data suggest that after cholecystectomy the small intestine alone acts as a pump in regulating the dynamics of the enterohepatic circulation of bile acids and that the improvement of cholesterol solubility in bile is due to a more rapid circulation of the bile acid pool in fasting cholecystectomised patients. The production of bile supersaturated in cholesterol tubes in the common duct, Soloway and Schoenfield is the major determinant for the formation of (1975) reported an increased output of bile acid and http://gut.bmj.com/ cholesterol gallstones in man (Admirand and Small, decreased cholesterol saturation of bile in response to 1968; Swell et al., 1971; Grundy et al., 1972; meals compared with fasting, while others Redinger and Small, 1972; Grundy et al., 1974). (Malagelada et al., 1973) reported no increase in the The low incidence of choledocholithiasis in output of bile acid in cholecystectomised patients in cholecystectomised patients suggests that the gall- response to cholecystokinin-pancreozymin (CCK- bladder plays an important role in the formation of PZ) infusion. Recently, studies on diurnal variations cholesterol gallstones. of biliary lipids following cholecystectomy (Kimball on September 27, 2021 by guest. Protected copyright. Some authors (Sarles et al., 1970; Shaffer et al., et al., 1976) showed that postprandial bile was less 1972; Simmons et al., 1972) have reported that saturated with cholesterol than fasting bile. cholecystectomy improves the solubility of choles- The purpose of this study was to determine the terol in bile, although others (Nilsson and effect of cholecystectomy on bile lipid composition Schersten, 1969; Small and Rapo, 1970; Almond and secretion rates, diurnal serum levels of bile et al., 1973) have found no modification in bile acids, pool size, and intestinal metabolism in order composition after cholecystectomy. to detect whether the gallbladder plays an important As far as bile lipid secretion rates are concerned, role in gallstone formation. Schersten et al. (1974) concluded that hepatic bile can be supersaturated in cholesterol at relatively Methods high bile acid secretion rates in cholecystectomised patients and that the gallbladder is not essential for EXPERIMENTAL PROCEDURE continuous production of lithogenic bile. Adler et al. (1974) found no difference in biliary lipid composi- Bile acid metabolism tion and hepatic secretion rates before and after Diurnal variations of serum levels of cholic acid cholecystectomy. (CCA) and chenodeoxycholic acid (CCDCA) In cholecystectomised patients with indwelling T conjugates Ten 10 'Address for reprint requests: E. Roda, Cattedra di Gastro- control subjects, cholesterol gallstone and 10 enterologia, Policlinico S. Orsola, Via Massarenti n. 9, cholecystectomised (one year previously) patients Bologna, Italy. were studied. Received for publication 25 January 1978 Conventional liver function tests did not reveal 640 Gut: first published as 10.1136/gut.19.7.640 on 1 July 1978. Downloaded from Enterohepatic circulation of bile acids after cholecystectomy ,6AI liver dysfunction in any of these patients. All to maintain the integrity ofthe enterohepatic circula- patients and control subjects received three solid tion of bile acids. meals of 300, 800, and 600 calories respectively at Liquid meals of respectively 300, 800, and 600 8.15 a.m., 12.15 p.m., and 5.15 p.m. Blood samples calories were infused at 8 am., 12 noon and 6 pm. were collected at 30 minute intervals over a 12-14 A second nasoduodenal tube was then positioned, hour period. for the infusion of 51CrCla (5,uCi) as a marker for Serum CCA and CCDCA levels were measured in the complete recovery of bile;- 1 ml of each bile each sample by a specific radioimmunoassay (RIA), sample, 1:10 diluted with isopropanol, was stored according to Simmonds (Simmonds et al., 1973) and kept at 4° C until bile lipid analysis and 51CrC13 modified by us (Roda et al., 1976a; Roda et al., recovery determination. The remainder was stored 1977a), as described below. at - 20°C. Bile acid composition, pool size, and kinetics ANALYTICAL PROCEDURE Bile acid pool size and kinetics were measured in all subjects. Radioimmunoassay ofbile acids Carboxyl-14C-cholic acid (10,Ci) was admini- [3(H)G] glycocholic acid (5 Ci/mmol) and [3(H)G] stered intravenously to each patient at 7.30 a.m., in glycochenodeoxycholic acid (5 Ci/mmol) (NEN fasting conditions, immediately before breakfast. Corp., Boston, Mass., USA) were used as tracers. Duodenal drainage was performed under fluoro- The unlabelled glyco-conjugated bile acids were scopic control following infusion of CCK-PZ (75 Ivy coupled to bovine serum albumin by the carbodi- dog units/70 kg body weight) (Karolinska, Sweeden) imide method (Simmonds et al., 1973). 10, 24, 48, and 72 hours after administration of the Antisera were obtained by weekly immunisation isotope. of New Zealand rabbits with 200 ,ug antigen, over a Three millilitres of duodenal bile was collected; 1 three month period. ml of each sample was diluted 1:10 (v/v) in isopro- Antisera, thus produced, were diluted 1/700 and panol for the estimation of bile acid pool size, daily 1/800 respectively for CCA and CCDCA assay, synthesis and turnover rate. The remainder of the giving 40% bound, when 0'5 pmol/ml of labelled sample was stored at -20° C. antigen were used in each tube. http://gut.bmj.com/ Each antiserum was found to be highly specific for Labelled cholyl-glycine breath test each glyco- and tauro-conjugated bile acid, showing Cholyl-1-14C glycine (5,uCi) was administered to the minimal cross-reaction with the free antigen and no same patients, to evaluate intestinal deconjugation of cross-reaction with the other bile acids in serum. bile acids and faecal excretion of 14C labelled bile Studies on cross-reaction together with parallelism acid, by means of the breath test, described by and recovery studies to assess the reproducibility, Hepner (Hepner, 1975) and modified by us (Roda et precision, accuracy, and applicability of the CCA al., 1977b) as described below. and CCDCA radioimmunoassay have already been on September 27, 2021 by guest. Protected copyright. reported (Roda et al., 1977a). Bile lipid composition and secretion Bile lipid composition and saturation index were Bile acid composition, pool size, synthesis, and determined on the fasting bile samples collected. turnover rate Biliary lipid output was investigated in three Pool size, synthesis, and turnover rate of bile acids controls, three gallstone and three cholecystecto- were assessed by the isotope dilution technique mised patients. A three lumen balloon occludable according to Lindstedt (1957). tube was passed in fasting conditions under fluoro- Carboxyl-14C-cholic acid (S.A. = 59.5 mCi/ scopic control through the nose, so that the aspira- mmol), purchased from the Radiochemical Centre tion site was situated in the second part of the (Amersham, England) was more than 98 % pure by duodenum, the infusion site distally, 25 cm below the thin-layer-chromatography. ligament of Treitz, while the balloon, positioned The specific activity of cholic acid was determined under the aspiration site, permitted the complete on each bile sample and the natural logarithm was collection of the bile. plotted against time to permit the calculationofpool The draining limb of the tube was connected to a size, synthesis, and turnover rate. stream splitter, which diverted 5% of the bile into The criteria for the validity of the isotope dilution graduated tubes. procedure in the determination of the cholic acid The remainder was reinfused into the tube, pool have been discussed by Lindstedt (1957) and through a separate infusion lumen and entered the others (Vlahcevic et al., 1970). jejunum 25 cm below the ligament of Treitz, in order The pool size ofchenodeoxycholic acid and deoxy- Gut: first published as 10.1136/gut.19.7.640 on 1 July 1978. Downloaded from 642 E. Roda, Rita Aldini, G. Mazzella, A. Roda, Claudia Sama, D. Festi, and L. Barbara cholic acid was calculated from the cholic acid pool vapours and scraped into scintillation vials. size and from bile acid composition in bile assessed Two millilitres of ethanol/acetic acid (10/1; v/v) by gas-liquid chromatography, as described below. mixture and 15 ml of Unisolve were added to each vial. The radioactivity was counted after dark Gas-liquid chromatography equilibration at 4°C, in an Isocap 300 beta-counter An aliquot (4 ml) of each diluted bile sample (1:10 (Nuclear Chicago). v/v with isopropanol) was transferred into a Nickel bomb and dried under nitrogen stream. Eight Bile acid intestinal deconjugation millilitres of 2N NaOH in 50% methanol solution 1-14C glycocholic acid (S.A. = 51-7 mCi/mmol) (The were added to each sample and alkaline hydrolysis Radiochemical Centre, Amersham, England) (5 ,Ci) carried out at 120°C for four hours. The solution was administered to the fasting patients and 14CO2 was then transferred to a large extraction tube, breath was collected, according to Hepner (1975), at acidified at pH 1 with a few drops of 5N HCI.
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