Skip to main content
Log in

Cholelithiasis in Taiwan

Gallstone characteristics, surgical incidence, bile lipid composition, and role of β-glucuronidase

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

Abstract

The nature and occurrence of gallstones in Taiwan and their etiologic factors might not be the same as in Western countries and warranted a systematic investigation. Gallbladder biles and gallstones were obtained at surgery from 100 and 74 patients, respectively. Common duct bile and stones were either drained through an indwelling common duct T-tube or aspirated through a nasobiliary catheter in 108 patients. Gallstones were analyzed for bilirubin, cholesterol, bile acid, calcium, and residue, and biles for bile acid, cholesterol, phospholipid, bilirubin, and β-glucuronidase. There were four major kinds of gallstones in Taiwan: cholesterol/mixed stones, high-residue black formed pigment stones, low-residue brown formed pigment stones, and muddy pigment stones. The surgical incidence of all types of stones increased steadily during the past four decades. During the past 15 years the relative frequencies for mixed, formed pigment, and muddy pigment stones had been roughly 40, 40, and 20%, respectively, with a further increase in the mixed stones and a decrease in the muddy pigment stones in recent years. Improvement of nutritional status and living standards might contribute to such changes. Cholesterol content in the common duct and gallbladder biles was higher in the mixed stone group than in other groups. Bacterial β-glucuronidase activity was detected in 53% of patients with muddy pigment stones. Endogenous β-glucuronidase activity and concentration were also highest in this group, intermediate in the formed pigment and mixed stone group, and lowest in the control. We concluded that hypercholesterobilia was responsible for increasing incidence of mixed stones during the past two decades, while both bacterial and human β-glucuronidase might contribute to pigment cholelithiasis.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Nakayama F, Soloway RD, Nakama T, Miyazaki K, Ichimiya H, Sheen PC, Ker CG, Ong GB, Choi TK, Boey F, Foong WC, Tan EC, Tung KH, Lee CN: Hepatolithiasis in East Asia—retrospective study. Dig Dis Sci 31:21–26, 1986

    PubMed  Google Scholar 

  2. Ker CG, Huang TJ, Sheen PC: Intrahepatic stones: 1. Etiological study. J Formosan Med Assoc 80:698–711, 1981

    Google Scholar 

  3. Hsu SC, Ho KJ, Chen JS, Chen YR: Biliary composition and excretion in Chinese and its relationship to cholethiasis. II. Epidemiological and pathological studies. J Formosan Med Assoc 78:670–687, 1979

    Google Scholar 

  4. Su CH, Lui WY, Peng FK: Relative prevalence of gallstone diseases in Taiwan: A nationwide cooperative study. Dig Dis Sci 37:764–768, 1992

    PubMed  Google Scholar 

  5. Ker CG, Lee KT, Sheen PC, Wei TC, Wu CW, Lui WY, Peng FK, Lin FY, Ho LC, Wang YH: A study of 1211 patients with intrahepatic stones in Taiwan. Asian J Surg 13:102–105, 1990

    Google Scholar 

  6. Chen JS, Ho KJ, Hsu SC: Biliary composition and excretion in Chinese and its relationship to cholelithiasis. I. Gross appearance and chemical composition of gallstones. J Formosan Med Assoc 78:661–669, 1979

    Google Scholar 

  7. Ho KJ, Hsu SC, Chen JS: Biliary composition and excretion in Chinese and its relationship to cholelithiasis: III. Gallbladder bile composition and its lithogenicity. J Formosan Med Assoc 78:735–748, 1979

    Google Scholar 

  8. Malloy HT, Evelyn KA: The determination of bilirubin with a photoelectric colorimeter. J Biol Chem 119:418–490, 1937

    Google Scholar 

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

    PubMed  Google Scholar 

  10. Allain CC, Poon LS, Chan CSG: Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475, 1974

    PubMed  Google Scholar 

  11. Hitachi Scientific Instrument Technical Data: AA No. 32: Concentration area for creating calibration curve in graphite furnace polarized Zeeman atomic absorption analytic method (optical temperature control method), p 3

  12. Goodwin JF, Thibert R, McCann D, Boyle AJ: Estimation of serum phospholipid and total phosphorous using chloric acid. Anal Chem 30:1097–1099, 1958

    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. Ho YC, Ho KJ: Human β-glucuronidase: Measurement of its activity in the gallbladder bile devoid of intrinsic interference. Dig Dis Sci 33:435–442, 1988

    PubMed  Google Scholar 

  15. Ho YC, Ho KJ: Differential quantitation of urinary β-glucuronidase of human and bacterial origin. J Urol 134:1227–1234, 1985

    PubMed  Google Scholar 

  16. Ho KJ: Development and optimization of an enzyme-linked immunosorbent assay employing two murine monoclonal antibodies for absolute quantitation of human β-glucuronidase. Biotech Applied Biochem 16:1–10, 1992

    Google Scholar 

  17. Duncan DB: Multiple range and multiple F tests. Biometrics 11:1–42, 1955

    Google Scholar 

  18. Bernhoff RA, Pellegrini CA, Motson RW, Way LW: Composition and morphologic and clinical features of common duct stones. Am J Surg 148:77–85, 1984

    PubMed  Google Scholar 

  19. Malet PF, Dabezies MA, Huang G, Long WB, Gadacz TR, Soloway RD: Quantitative infrared spectroscopy of common bile duct gallstones. Gastroenterology 94:1217–1221, 1988

    PubMed  Google Scholar 

  20. Wosiewitz U, Schroebler S: On the chemistry of “black” pigment stones from the gallbladder. Clin Chim Acta 89:1–12, 1978

    PubMed  Google Scholar 

  21. Black BE, Carr SH, Ohkubo H, Ostrow JD: Equilibrium swelling of pigment gallstones: Evidence of network polymer structure. Biopolymers 21:601–610, 1982

    PubMed  Google Scholar 

  22. Ohkubo H, Ostrow JD, Carr SH, Rege RV: Polymer networks in pigment and cholesterol gallstones assessed by equilibrium swelling and infrared spectroscopy. Gastroenterology 87:805–814, 1984

    PubMed  Google Scholar 

  23. Rege RV, Webster CC, Ostrow JD, Carr SH, Ohkubo H: Validation of infrared spectroscopy for assessment of vinyl polymers of bile-pigment gallstones. Biochem J 224:871–876, 1984

    PubMed  Google Scholar 

  24. Friedman GD, Kannel WB, Dawler TR: The epidemiology of gallbladder disease: Observation in the Framingham study. J Chron Dis 19:273–292, 1966

    PubMed  Google Scholar 

  25. Trotman BW, Ostrow JD, Soloway RD: Pigment vs cholesterol cholelithiasis: Comparison of stone and bile composition. Am J Dig Dis 19:585–590, 1974

    PubMed  Google Scholar 

  26. Trotman BW, Soloway RD: Pigment vs cholesterol cholelithiasis: Clinical and epidemiological aspects. Am J Dig Dis 20:735–740, 1975

    PubMed  Google Scholar 

  27. Holzback RT, Marsh M, Olszewski M, Holan K: Cholesterol solubility in bile: Evidence that supersaturated bile is frequent in healthy man. J Clin Invest 52:1467–1479, 1973

    PubMed  Google Scholar 

  28. Oviedo MA, Ho KJ, Taylor CB, Dorsey JM: Biliary phospholipids and cholesterol in different ethnic groups. Surg Forum 20:390–391, 1969

    PubMed  Google Scholar 

  29. Nakayama F, van der Linden W: Bile compositions: Sweden vs Japan. Its possible significance in the difference in gallstone incidence. Am J Surg 122:8–12, 1971

    PubMed  Google Scholar 

  30. Trotman BW, Soloway RD: Pigment gallstone disease: summary of the National Institutes of Health International Workshop. Hepatology 2:879–884, 1982

    PubMed  Google Scholar 

  31. Nagase M, Tanimura H, Setoyama M, Hikasa Y: Present features of gallstones in Japan: A collective review of 2,144 cases. Am J Surg 135:788–790, 1978

    PubMed  Google Scholar 

  32. Maki T: Pathogenesis of calcium bilirubinate gallstones: Role ofE. coli, β-glucuronidase and coagulation by inorganic ions, polyelectrolytes, and agitation. Ann Surg 164:90–100, 1966

    PubMed  Google Scholar 

  33. Stewart L, Smith AL, Pellegrini CA: Pigment gallstones form as a composite of bacterial microcolonies and pigment solids. Ann Surg 206:242–250, 1987

    PubMed  Google Scholar 

  34. Kaufman HS, Magnuson TH, Lillemoe KD: The role of bacteria in gallbladder and common duct stone formation. Ann Surg 209:584–592, 1989

    PubMed  Google Scholar 

  35. Cetta F: Bile infection documented as initial event in the pathogenesis of brown pigment biliary stones. Hepatology 6:482–489, 1986

    PubMed  Google Scholar 

  36. Skar V, Saxerholt H: High performance liquid chromatography of bilirubin conjugates in bile: Effect of β-glucuronidase on the bile pigments. Scand J Gastroenterol 24:657–665, 1989

    PubMed  Google Scholar 

  37. Cetta F: The role of bacteria in pigment gallstone disease. Ann Surg 213:315–326, 1991

    PubMed  Google Scholar 

  38. Cahalane MJ, Neubrand MW, Carey MC: Physical-chemical pathogenesis of pigment gallstones. Semin Liver Dis 8:317–328, 1988

    PubMed  Google Scholar 

  39. Fevery J, Leroy P, Van de Vijver M, Heirwegh KPM: Structures of bilirubin conjugates synthesizedin vitro from bilirubin and uridine diphosphate glucuronic acid, uridine diphosphate glucose or uridine diphosphate xylose by preparation from rat liver. Biochem J 129:635–644, 1972

    PubMed  Google Scholar 

  40. Spivak W, Carey MC: Reverse-phase H.P.L.C. separation, quantification and preparation of bilirubin and its conjugation from native bile. Biochem J 225:787–805, 1985

    PubMed  Google Scholar 

  41. Nakano T, Tabata M, Nakayama F: Unconjugated bilirubin in hepatic bile with brown pigment gallstones and cholangitis. Dig Dis Sci 33:1116–1120, 1988

    PubMed  Google Scholar 

  42. Allen B, Bernhoft R, Blanckaert N, Svanvik J, Filly R, Gooding G, Way L: Sludge is calcium bilirubinate associated with bile statis. Am J Surg 141:51–56, 1981

    PubMed  Google Scholar 

  43. Lee SP: Pathogenesis of biliary sludge. Hepatology 12:200S-205S, 1990

    PubMed  Google Scholar 

  44. Magnuson TH, Lillemoe KD, Scheeres DE, Pitt HA: Altered bile composition during cholesterol gallstone formation: Cause or effect? J Surg Res 48:584–589, 1990

    PubMed  Google Scholar 

  45. Ostrow JD, Celic L: Bilirubin chemistry, ionization and solubilization by bile salts. Hepatology 4:38S-45S, 1984

    PubMed  Google Scholar 

  46. Ostrow JD, Celic L, Mukerjee P: Molecular and micellar association in the pH-dependent stable and metastable dissolution of unconjugated bilirubin by bile salts. J Lipid Res 29:335–348, 1988

    PubMed  Google Scholar 

  47. Rege RV, Webster CC, Ostrow JD: Interactions of unconjugated bilirubin with bile salts. J Lipid Res 29:1289–1296, 1988

    PubMed  Google Scholar 

  48. McDonagh AF, Lightner DA Phototherapy and the photobiology of bilirubin. Semin Liver Dis 8:272–283, 1988

    PubMed  Google Scholar 

  49. Falk H, Müller N, Ratzenhofer M, Winsauer K: The structure of photobilirubin. Monatsh Chem 113:1421–1432, 1982

    Google Scholar 

  50. Spivak W, DiVenuto D, Yuey W: Non-enzymic hydrolysis of bilirubin mono- and diglucuronide to unconjugated bilirubin in model and native bile systems. Biochem J 242:323–329, 1987

    PubMed  Google Scholar 

  51. Shinya F, Toshima T, Takahashi W, Suzuki N: Effects of pH on the deconjugation of conjugated bilirubin in human bile. Tohoku J Exp Med 147:281–293, 1985

    PubMed  Google Scholar 

  52. LeSage GD, Robertson WE, Baumgart MA: Bile acid-dependent vesicular transport of lysosomal enzymes into bile in the rat. Gastroenterology 105:889–900, 1993

    PubMed  Google Scholar 

  53. Ballantyne B, Wood WG: Biochemical and histochemical observations on β-glucuronidase in the mammalian gallbladder. Am J Dig Dis 13:551–557, 1968

    PubMed  Google Scholar 

  54. Wosiewitz U, Althoff J, Langhans P: β-Glucuronidase activity in human cholesterol and pigment stone bile. Z Gastroenterol 17:301–309, 1979

    PubMed  Google Scholar 

  55. Ho KJ: Human β-glucuronidase: Studies on the effects of pH and bile acids in regard to its role in the pathogenesis of cholelithiasis. Biochim Biophys Acta 827:197–206, 1985

    PubMed  Google Scholar 

  56. Ho KJ, Hsu SC, Chen JS, Ho LHC: Human biliary β-glucuronidase: Correlation of its activity with deconjugation of bilirubin in the bile. Eur J Clin Invest 16:361–367, 1986

    PubMed  Google Scholar 

  57. Womack NA, Zeppa R, Irvin GL III: The anatomy of gallstones. Ann Surg 157:670–686, 1963

    PubMed  Google Scholar 

  58. Malet PF, Williamson CE, Trotman BW, Soloway RD: Composition of pigmented centers of cholesterol gallstones. Hepatology 6:477–481, 1986

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported in part by Research Grant 820412B002-342 from the National Science Council, Executive Yuen, Republic of China and Medical Research Fund from Department of Veterans Affairs, USA.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ho, KJ., Lin, XZ., Yu, SC. et al. Cholelithiasis in Taiwan. Digest Dis Sci 40, 1963–1973 (1995). https://doi.org/10.1007/BF02208665

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02208665

Key Words

Navigation