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The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1970 Feb;49(2):232–242. doi: 10.1172/JCI106232

Effects of controlled interruption of the enterohepatic circulation of bile salts by biliary diversion and by ileal resection on bile salt secretion, synthesis, and pool size in the rhesus monkey

R Hermon Dowling 1,2, Eberhard Mack 1,2, Donald M Small 1,2
PMCID: PMC322465  PMID: 4983661

Abstract

The effects of controlled interruption of the enterohepatic circulation (EHC) of bile salts by biliary diversion on bile volume, bile salt secretion and synthesis rates, bile salt pool size, and the relationship to fecal fat excretion were studied in 16 rhesus monkeys.

Bile from a chronic bile fistula was returned to the intestine through an electronic stream-splitter which, by diverting different percentages of bile to a collecting system, provided graded and controlled interruption of the EHC.

The increase in hepatic bile salt synthesis in response to interruption of the EHC was limited and reached a maximum rate at 20% interruption of the EHC. Up to this level of biliary diversion, the increased hepatic synthesis compensated for bile salt loss so that bile salt secretion and pool size were maintained at normal levels. With diversion of 33% or more, there was no further increase in hepatic bile salt synthesis to compensate for external loss, and as a result there was diminished bile salt secretion, a reduction in bile salt pool size, and steatorrhea was observed.

The effects of interruption of the EHC by the streamsplitter were compared with those produced by resection of the distal one-third or two-thirds of small bowel. While ileal resection appreciably reduced bile salt secretion, the EHC was by no means abolished. Bile salt reabsorption from the residual intestine was greater after one-third than after two-thirds small bowel resection. These observations suggest that jejunal reabsorption of bile salts occurs and may well contribute to the normal EHC.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aach R. D., Peterson M. L., Ternberg J. L. A modified T tube for quantitative collection of bile. J Lab Clin Med. 1968 Sep;72(3):517–520. [PubMed] [Google Scholar]
  2. Admirand W. H., Small D. M. The physicochemical basis of cholesterol gallstone formation in man. J Clin Invest. 1968 May;47(5):1043–1052. doi: 10.1172/JCI105794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Austad W. I., Lack L., Tyor M. P. Importance of bile acids and of an intact distal small intestine for fat absorption. Gastroenterology. 1967 Apr;52(4):638–646. [PubMed] [Google Scholar]
  4. BORGSTROM B. On the mechanism of the intestinal fat absorption. V. The effect of bile diversion on fat absorption in the rat. Acta Physiol Scand. 1953;28(2-3):279–286. doi: 10.1111/j.1748-1716.1953.tb00981.x. [DOI] [PubMed] [Google Scholar]
  5. BOWERS M. A., LUND P. K., MATHIES J. C. A RAPID, RELIABLE PROCEDURE FOR THE DETERMINATION OF TOTAL FECAL LIPIDS, WITH OBSERVATIONS ON THE COMPOSITION OF THE LIPIDS EXCRETED BY HUMAN SUBJECTS IN NORMAL AND PATHOLOGICAL STATES. Clin Chim Acta. 1964 Apr;9:344–347. doi: 10.1016/0009-8981(64)90024-5. [DOI] [PubMed] [Google Scholar]
  6. Beher W. T., Beher M. E., Rao B. Bile acid and cholesterol metabolism in the mouse as affected by cholestyramine. Proc Soc Exp Biol Med. 1966 Jul;122(3):881–884. doi: 10.3181/00379727-122-31278. [DOI] [PubMed] [Google Scholar]
  7. DANIELSSON H., ENEROTH P., HELLSTROM K., LINDSTEDT S., SJOVALL J. On the turnover and excretory products of cholic and chenodeoxycholic acid in man. J Biol Chem. 1963 Jul;238:2299–2304. [PubMed] [Google Scholar]
  8. Dietschy J. M. Mechanisms for the intestinal absorption of bile acids. J Lipid Res. 1968 May;9(3):297–309. [PubMed] [Google Scholar]
  9. Dietschy J. M., Salomon H. S., Siperstein M. D. Bile acid metabolism. I. Studies on the mechanisms of intestinal transport. J Clin Invest. 1966 Jun;45(6):832–846. doi: 10.1172/JCI105399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dowling R. H., Mack E., Picott J., Berger J., Small D. M. Experimental model for the study of the enterohepatic circulation of bile in rhesus monkeys. J Lab Clin Med. 1968 Jul;72(1):169–176. [PubMed] [Google Scholar]
  11. EKDAHL P. H., SJOVALL J. On the conjugation and formation of bile acids in the human liver. I. On the excretion of bile acids by patients with postoperative choledochostomy drainage; bile acids and steroids 61. Acta Chir Scand. 1958 May 10;114(6):439–452. [PubMed] [Google Scholar]
  12. ENCRANTZ J. C., SJOVALL J. On the bile acids in duodenal contents of infants and children. Bile acids and steroids 72. Clin Chim Acta. 1959 Nov;4:793–799. doi: 10.1016/0009-8981(59)90030-0. [DOI] [PubMed] [Google Scholar]
  13. ERIKSSON S. Biliary excretion of bile acids and cholesterol in bile fistula rats; bile acids and steroids. Proc Soc Exp Biol Med. 1957 Mar;94(3):578–582. doi: 10.3181/00379727-94-23018. [DOI] [PubMed] [Google Scholar]
  14. Eneroth P., Gordon B., Ryhage R., Sjövall J. Identification of mono- and dihydroxy bile acids in human feces by gas-liquid chromatography and mass spectrometry. J Lipid Res. 1966 Jul;7(4):511–523. [PubMed] [Google Scholar]
  15. Eneroth P., Gordon B., Sjövall J. Characterization of trisubstituted cholanoic acids in human feces. J Lipid Res. 1966 Jul;7(4):524–530. [PubMed] [Google Scholar]
  16. GRUNDY S. M., AHRENS E. H., Jr, MIETTINEN T. A. QUANTITATIVE ISOLATION AND GAS--LIQUID CHROMATOGRAPHIC ANALYSIS OF TOTAL FECAL BILE ACIDS. J Lipid Res. 1965 Jul;6:397–410. [PubMed] [Google Scholar]
  17. HASLEWOOD G. A. THE BIOLOGICAL SIGNIFICANCE OF CHEMICAL DIFFERENCES IN BILE SALTS. Biol Rev Camb Philos Soc. 1964 Nov;39:537–574. doi: 10.1111/j.1469-185x.1964.tb01170.x. [DOI] [PubMed] [Google Scholar]
  18. HOLASEK A. Uber den Ursprung des Kotfettes. II. Versuche an Ratten mit Gallengangverschluss. Hoppe Seylers Z Physiol Chem. 1954;298(3-5):219–223. [PubMed] [Google Scholar]
  19. Hardison W. G., Rosenberg I. H. Bile-salt deficiency in the steatorrhea following resection of the ileum and proximal colon. N Engl J Med. 1967 Aug 17;277(7):337–342. doi: 10.1056/NEJM196708172770704. [DOI] [PubMed] [Google Scholar]
  20. Heaton K. W., Austad W. I., Lack L., Tyor M. P. Enterohepatic circulation of C14-labeled bile salts in disorders of the distal small bowel. Gastroenterology. 1968 Jul;55(1):5–16. [PubMed] [Google Scholar]
  21. Hofmann A. F., Small D. M. Detergent properties of bile salts: correlation with physiological function. Annu Rev Med. 1967;18:333–376. doi: 10.1146/annurev.me.18.020167.002001. [DOI] [PubMed] [Google Scholar]
  22. Josephson B., Rydin A. The resorption of the bile acids from the intestines. Biochem J. 1936 Dec;30(12):2224–2228. doi: 10.1042/bj0302224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. KAY R. E., ENTENMAN C. Stimulation of taurocholic acid synthesis and biliary excretion of lipids. Am J Physiol. 1961 Apr;200:855–859. doi: 10.1152/ajplegacy.1961.200.4.855. [DOI] [PubMed] [Google Scholar]
  24. LACK L., WEINER I. M. INTESTINAL ABSORPTION OF BILE SALTS AND SOME BIOLOGICAL IMPLICATIONS. Fed Proc. 1963 Nov-Dec;22:1334–1338. [PubMed] [Google Scholar]
  25. LIGHT H. G., WITMER C., VARS H. M. Interruption of the enterohepatic cirucaltion and its effect on rat bile. Am J Physiol. 1959 Dec;197:1330–1332. doi: 10.1152/ajplegacy.1959.197.6.1330. [DOI] [PubMed] [Google Scholar]
  26. McLeod G. M., Wiggins H. S. Bile-salts in small intestinal contents after ileal resection and in other malabsorption syndromes. Lancet. 1968 Apr 27;1(7548):873–876. doi: 10.1016/s0140-6736(68)90235-3. [DOI] [PubMed] [Google Scholar]
  27. Meihoff W. E., Kern F., Jr Bile salt malabsorption in regional ileitis, ileal resection and mannitol-induced diarrhea. J Clin Invest. 1968 Feb;47(2):261–267. doi: 10.1172/JCI105722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NORMAN A., SJOVALL J. On the transformation and enterohepatic circulation of cholic acid in the rat: bile acids and steroids 68. J Biol Chem. 1958 Oct;233(4):872–885. [PubMed] [Google Scholar]
  29. PLAYOUST M. R., LACK L., WEINER I. M. EFFECT OF INTESTINAL RESECTION ON BILE SALT ABSORPTION IN DOGS. Am J Physiol. 1965 Feb;208:363–369. doi: 10.1152/ajplegacy.1965.208.2.363. [DOI] [PubMed] [Google Scholar]
  30. SJOVALL J., AKESSON I. Intestinal absorption of taurocholic acid in the rat. Bile acids and steroids, 26. Acta Physiol Scand. 1955 Oct 27;34(2-3):273–278. doi: 10.1111/j.1748-1716.1955.tb01246.x. [DOI] [PubMed] [Google Scholar]
  31. SULLIVAN M. F. BILE SALT ABSORPTION IN THE IRRADIATED RAT. Am J Physiol. 1965 Jul;209:158–164. doi: 10.1152/ajplegacy.1965.209.1.158. [DOI] [PubMed] [Google Scholar]
  32. Samuel P., Saypoi G. M., Meilman E., Mosbach E. H., Chafizadeh M. Absorption of bile acids from the large bowel in man. J Clin Invest. 1968 Sep;47(9):2070–2078. doi: 10.1172/JCI105892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Small D. M. Gallstones. N Engl J Med. 1968 Sep 12;279(11):588–593. doi: 10.1056/NEJM196809122791106. [DOI] [PubMed] [Google Scholar]
  34. Stanley M. M., Nemchausky B. Fecal C-14-bile acid excretion in normal subjects and patients with steroid-wasting syndromes secondary to ileal dysfunction. J Lab Clin Med. 1967 Oct;70(4):627–639. [PubMed] [Google Scholar]
  35. TALALAY P. Enzymic analysis of steroid hormones. Methods Biochem Anal. 1960;8:119–143. doi: 10.1002/9780470110249.ch3. [DOI] [PubMed] [Google Scholar]
  36. THOMPSON J. C., VARS H. M. Biliary excretion of cholic acid and cholesterol in hyper-, hypo-, and euthyroid rats. Proc Soc Exp Biol Med. 1953 Jun;83(2):246–248. doi: 10.3181/00379727-83-20320. [DOI] [PubMed] [Google Scholar]
  37. Van Deest B. W., Fordtran J. S., Morawski S. G., Wilson J. D. Bile salt and micellar fat concentration in proximal small bowel contents of ileectomy patients. J Clin Invest. 1968 Jun;47(6):1314–1324. doi: 10.1172/JCI105823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. WIGGINS H. S., WOOTTON I. D. Studies in the bile acids. 3. The conjugated bile salts of certain primates. Biochem J. 1958 Oct;70(2):349–352. doi: 10.1042/bj0700349. [DOI] [PMC free article] [PubMed] [Google Scholar]

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