Skip to main content
SpringerLink
Log in

Gallstone formation and gallbladder bile composition after colectomy in dogs

  • Pancreatic And Biliary Disorders
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

A high prevalence of gallstones has been described in patients following colectomy. The aim of this study was to examine whether lithogenicity is attributed to colectomy. In the present study, changes in gallbladder bile composition and the mechanism of gallstone formation after colectomy were examined in dogs. Ten mongrel dogs underwent restorative proctocolectomy. Seven dogs which received sham operations served as controls. Over a 12-week postoperative period, samples of gallbladder bile, formed gallstones and serum were collected and analyzed. In 7 of the 10 (70%) colectomized dogs, gallstones were found in the gallbladder, while the control dogs had no stones. Macroscopically the gallstones were similar to black pigment stones observed in humans. Chemical analysis and Fourier transform-infrared spectroscopy examination revealed that the stones were composed mainly of sodium bilirubinate and proteins, with minor amounts of calcium salts and cholesterol. Significant increases in biliary pH and concentrations of ionized calcium and unconjugated bilirubin were observed in the gallbladder bile of the colectomy group compared with that of the control group. The total bile acid and total bilirubin concentrations were significantly decreased in the colectomy group. Cholesterol crystal nucleation did not occur. The inhibitory effect of gallbladder bile on calcium carbonate precipitation in anin vitro assay system was preserved even after colectomy. In conclusion, proctocolectomy increases the concentration of unconjugated bilirubin in gallbladder bile and induces pigment gallstones which are composed mainly of sodium bilirubinate and proteins since calcium ions and cholesterol are stabilized in dogs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Mair WJS, Hill GL, Goligher JC: Cholelithiasis: A metabolic consequence of ileostomy. Gut 15:830, 1974

    Google Scholar 

  2. Hill GL, Mair WJS, Goligher JC: Gallstones after ileostomy and ileal resection. Gut 16:932–936, 1975

    PubMed  Google Scholar 

  3. Jones MR, Gregory D, Evans KT, Rhodes: The prevalence of gallbladder disease in patients with ileostomy. J Clin Radiol 27:561–562, 1976

    Google Scholar 

  4. Kurchin A, Ray JE, Bluth EI, Merritt CRB, Gathright Jr. JB, Pehrsson BF, Ferrari BT: Cholelithiasis in ileostomy patients. Dis Colon Rectum 27:585–588, 1984

    PubMed  Google Scholar 

  5. Heaton KW, Read AE: Gall stones in patients with disorders of the terminal ileum and disturbed bile salt metabolism. Br Med J 30:494–496, 1969

    Google Scholar 

  6. Baker AL, Kaplan MM, Norton RA, Patterson JF: Gallstones in inflammatory bowel disease. Am J Dig Dis 19:109–112, 1974

    PubMed  Google Scholar 

  7. Mibu R, Itoh H, Nakayama F: Effect of total colectomy and mucosal proctectomy on intestinal absorptive capacity in dogs. Dis Colon Rectum 30:47–51, 1987

    PubMed  Google Scholar 

  8. Michaelsson M: Bilirubin determination in serum and urine. Scand J Clin Lab Invest 56(Suppl):40–50, 1961

    Google Scholar 

  9. Spivak W, Carey MC: Reverse-phase h.p.l.c. separation, quantification and preparation of bilirubin and its conjugates from native bile. Biochem J 225:787–805, 1985

    PubMed  Google Scholar 

  10. Talalay P: Enzymatic analysis of steroid hormones. Methods Biochem Anal 8:119–143, 1960

    PubMed  Google Scholar 

  11. Bartlett GR: Phosphorus assay in column chromatography. J Biol Chem 234:466–468, 1959

    PubMed  Google Scholar 

  12. Chijiiwa K, Nakayama F: Simultaneous microanalysis of bile acids and cholesterol in bile by glass capillary column gas chromatography. J Chromatogr 431:17–25, 1988

    PubMed  Google Scholar 

  13. Carey MC: Critical tables for calculating the cholesterol saturation of native bile. J Lipid Res 19:945–955, 1978

    PubMed  Google Scholar 

  14. Harvey PRC, Upadhya GA, Toth JL, Strasberg SM: Fluorometric assay of protein in native human bile. Clin Chim Acta 183:147–154, 1989

    PubMed  Google Scholar 

  15. Holan KR, Holzbach RT, Hermann RE, Cooperman AM, Claffey WJ: Nucleation time: A key factor in the pathogenesis of cholesterol gallstone disease. Gastroenterology 77:611–617, 1979

    PubMed  Google Scholar 

  16. Trotman BW, Soloway RD: Pigment gallstone disease: Summary of the National Institutes of Health-International workshop. Hepatology 2:879–884, 1982

    PubMed  Google Scholar 

  17. Dawes LG, Moore EW, Rege RV, Shimizu S, Ostrow JD: Canine bile contains anticrystallization factors that inhibit precipitation of calcium carbonate. Hepatology 14:701–706, 1991

    PubMed  Google Scholar 

  18. Wheeler AP, George JW, Evans CA: Control of calcium carbonate nucleation and crystal growth by soluble matrix of oyster shell. Science 212:1397–1398, 1981

    Google Scholar 

  19. Sciarretta G, Ligabue A, Garuti G, Pieromaldi S, Verri A, Giacobazzi G, Malaguti P: Inhibition activity of gallbladder bile on calcium carbonate crystallizationin vitro. Scand J Gastroenterol 19:626–630, 1984

    PubMed  Google Scholar 

  20. Knyrim K, Vakil N: Bile from patients with gallstones is defective in an anti-nucleating factor for calcium carbonate. Gastroenterology 96:A614, 1989

    Google Scholar 

  21. Yamashita N, Yanagisawa J, Nakayama F: Composition of intrahepatic calculi. Dig Dis Sci 33:449–453, 1988

    PubMed  Google Scholar 

  22. Harvey PRC, McLeod RS, Cohen Z, Strasberg SM: Effects of colectomy on bile composition, cholesterol crystal formation, and gallstones in patients with ulcerative colitis. Ann Surg 214:396–402, 1991

    PubMed  Google Scholar 

  23. Makino I, Chijiiwa K, Higashijima H, Nakahara S, Kishinaka M, Kuroki S, Mibu R: Rapid cholesterol nucleation time and cholesterol gall stone formation after subtotal or total colectomy in humans. Gut 35:1760–1764, 1994

    PubMed  Google Scholar 

  24. Kestell MF, Sekijima J, Lee SP, Park HZ, Long M, Kaler EW: A calcium-binding protein in bile and gallstones. Hepatology 16:1315–1321, 1992

    PubMed  Google Scholar 

  25. Moore EW: The role of calcium in the pathogenesis of gallstones: Ca++ electrode studies of model bile salt solutions and other biologic systems. Hepatology 4:228S-243S, 1984

    PubMed  Google Scholar 

  26. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN: Bilirubin is an antioxidant of possible physiological importance. Science 235:1043, 1987

    PubMed  Google Scholar 

  27. Fevery J, Verwilghen R, Tan TG, DeGroote J: Glucuronidation of bilirubin and the occurrence of pigment gallstones with chronic haemolytic disease. Eur J Clin Invest 10:219–226, 1980

    PubMed  Google Scholar 

  28. Williamson BWA, Percy-Robb IW: Contribution of biliary lipids to calcium binding in bile. Gastroenterology 78:696–702, 1980

    PubMed  Google Scholar 

  29. Scharschmidt BF, Schmid R: The micellar sink. J Clin Invest 62:1122–1131, 1978

    PubMed  Google Scholar 

  30. Wosiewitz U, Schroebler: Solubilization of unconjugated bilirubin by bile salts. Experimentia 35:717–718, 1979

    Google Scholar 

  31. Natori H, Utsunomiya J, Yamamura T, Benno Y, Uchida K: Fecal and stomal bile acid composition after ileostomy or ileoanal anastomosis in patients with chronic ulcerative colitis and adenomatosis coli. Gastroenterology 102:1278–1288, 1992

    PubMed  Google Scholar 

  32. Bickerstaff KI, Moossa AR: Effects of resection or bypass of the distal ileum on the lithogenecity of bile. Am J Surg 145:34–40, 1983

    PubMed  Google Scholar 

  33. Coyle JJ, Hoyt DB, Sedaghat A: Relationship of intestinal bypass operations and cholelithiasis. Surg Forum 21:139–141, 1980

    Google Scholar 

  34. Matushiro T, Suzuki N, Sato T, Maki T: Effects of diet on glucaric acid concentration in bile and the formation of calcium bilirubinate stones. Gastroenterology 72:630–633, 1977

    PubMed  Google Scholar 

  35. Englert E Jr, Harman CG, Freston JW, Straight RC, Wales EE: Studies on the pathogenesis of diet-induced dog gallstones. Am J Dig Dis 22:305–314, 1977

    PubMed  Google Scholar 

  36. Pemberton JH, Kelly KA, Beart RW, Dozois RR, Wolff BG, Ilstrup DM: Ileal pouch-anal anastomosis for chronic ulcerative colitis. Ann Surg 206:504–513, 1987

    PubMed  Google Scholar 

  37. Kelly RE, Abedin MZ, Fonkalsrud EW, Cates JA, Saunders-Kirkwood K, Masuda H, Huang E-J, Dhiman JK, Roslyn JJ: Early and long-term effects of colectomy and endorectal pull-through on bile acid profile. Ann Surg 217:321–328, 1993

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Gastroenterology, The University of Texas Medical Branch at Galveston, Texas, USA

    Hirokazu Noshiro MD, Masayuki Hotokezaka MD, Hidetaka Higashijima MD, Takuya Iwamoto MD, Shosaku Nakahara MD, Ryuichi Mibu MD, Roger D. Soloway MD &  Kazuo Chijiiwa MD, PhD (FACS)

  2. Department of Surgery I, Kyushu University, Faculty of Medicine, 3-1-1 Maidashi, Higashi-ku, 812-82, Fukuoka, Japan

    Hirokazu Noshiro MD, Masayuki Hotokezaka MD, Hidetaka Higashijima MD, Takuya Iwamoto MD, Shosaku Nakahara MD, Ryuichi Mibu MD, Roger D. Soloway MD &  Kazuo Chijiiwa MD, PhD (FACS)

Authors
  1. Hirokazu Noshiro MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayuki Hotokezaka MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hidetaka Higashijima MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takuya Iwamoto MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shosaku Nakahara MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ryuichi Mibu MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Roger D. Soloway MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kazuo Chijiiwa MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Noshiro, H., Hotokezaka, M., Higashijima, H. et al. Gallstone formation and gallbladder bile composition after colectomy in dogs. Digest Dis Sci 41, 2423–2432 (1996). https://doi.org/10.1007/BF02100138

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02100138

Key words

Search

Navigation