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Hepatocyte ultrastructure in rats with portacaval shunt

A morphometric study of acinar zones

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Abstract

The principal reported morphological consequence of portacaval shunt in the rat is liver atrophy. The present study was designed to investigate ultrastructural changes in hepatocytes using electron microscopy morphometry. Two weeks following portacaval shunt, rat livers were fixed by perfusion and hepatocyte organelles from the two opposite zones of the acinus (zones 1 and 3) were quantified. Liver weight/body weight decreased by 50%, hepatocyte-specific volume decreased by 30% (28% in zone 1 and 35% in zone 3). Estimated sinusoidal space increased, and estimated number of hepatocytes decreased by 50%. Hepatocytes had a normal ultrastructure except for mitochondria. Smooth endoplasmic reticulum-specific surface area was reduced by 65% (zone 3), and rough endoplasmic reticulum surface density was increased in zone 1 only. Mitochondriaspecific volume was unchanged but decreased inner and outer membrane-specific surface area in zone 3 suggests in this zone a change in their conformation and possibly their number. Golgi-rich area surface density increased but not significantly. Hepatocyte loss and atrophy and rearrangement of organelles represent a new ultrastructural steady state following portacaval shunt that may help explain the new functional steady state.

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References

  1. Starlz TE, Putnam CW, Chase HP, Porter KA: Portacaval shunt in hyperlipoproteinemia. Lancet 1:940–944, 1973

    PubMed  Google Scholar 

  2. Starlz TE, Chase HP, Putnam CW, Nora JJ: Follow-up of patient with portacaval shunt for the treatment of hyperlipidemia. Lancet 2:714–715, 1974

    PubMed  Google Scholar 

  3. Madras PN: Portacaval shunt for familial heterozygous hypercholesterolemia. Surg Gynecol Obstet 152:187–190, 1981

    PubMed  Google Scholar 

  4. Starlz TE, Putnam CW, Porter KA, Halgrimson CG, Corman J, Brown BI, Gotlin RW, Rodgerson DO, Greene HL: Portal diversion for the treatment of glycogen storage disease in humans. Ann Surg 178:525–539, 1973

    PubMed  Google Scholar 

  5. Corbeel L, Hue L, Lederer B, De Barsy T, Van Den Berghe G, Devlieger H, Jaeken J, Bracke P, Eeckels R: Clinical and biochemical findings before and after portacaval shunt in girl with type Ib glycogen storage disease. Pediatr Res 15:58–61, 1981

    PubMed  Google Scholar 

  6. Bützow GH, Ossenberg FW, Becker K, Schudt C, Gaertner U: Effect of portacaval anastomosis on hepatic HMG-CoA-reductase activity in normal rats. FEBS Lett 75:101–104, 1977.

    PubMed  Google Scholar 

  7. Bützow GH, Dammann HG, Czok G: Effect of portacaval shunt on biliary cholesterol and bile salt secretion in normal rats. Eur J Clin Invest 8:411–414, 1978

    PubMed  Google Scholar 

  8. Balasubramaniam S, Press CM, Mitropoulos KA, Magide AA, Myant NB: Effect of portacaval anastomosis on the activities of hepatic enzymes related to cholesterol and bile acid metabolism in rats. Biochim Biophys Acta 441:308–315, 1976

    PubMed  Google Scholar 

  9. Magide AA, Press CM, Myant CB, Mitropoulos KA, Balasubramanian S: The effect of portacaval anastomosis on plasma lipoprotein metabolism in rats. Biochim Biophys Acta 441:302–307, 1976

    PubMed  Google Scholar 

  10. Nestruck AC, Lussier-Cacan S, Bergseth M, Bidalier M, Davignon J, Marcel YL: The effect of portacaval shunt on plasma lipids and lipoproteins in swine. Biochim Biophys Acta 488:43–54, 1977

    PubMed  Google Scholar 

  11. Prioa A, McNamara DJ, Edwards DG, Ahrens EH: Cholesterol homeostasis in the rat with a portacaval anastomosis. Proc Natl Acad Sci USA 76:4654–4657, 1979

    PubMed  Google Scholar 

  12. Nestruck AC, Bergseth M, Bidalier M, Davignon J, Marcel YL: Lipid and lipoprotein secretion following portacaval shunt in swine. Atherosclerosis 29:355–362, 1978

    PubMed  Google Scholar 

  13. Rossouw JE, Labadarios D, Vinjk AI, de Villiers AS: Liver glycogen after portacaval shunt in rats. Metabolism 27:1067–1073, 1978

    PubMed  Google Scholar 

  14. Assal J, Livrat R, Stauffecher W, Renold AE: Metabolic consequences of portacaval shunting in the rat; effects on glucose tolerance and serum immunoreactive insulin response. Metabolism 20:850–858, 1971

    PubMed  Google Scholar 

  15. Sarna GS, Cunningham VJ, Tucker S, Cremer JE: The turnover of plasma glucose and free fatty acidsin vivo after portacaval anastomosis and chronic underfeeding in the rat. Clin Sci 60:87–93, 1981

    PubMed  Google Scholar 

  16. Vassanelli P, Chiesara E: Microsomal drug-metabolizing enzymes activity and induction in the rat liver after portacaval shunt. Arch Int Pharmacodyn Ther 196:158–161, 1972

    PubMed  Google Scholar 

  17. Okolincsanyi L, Vassanelli P, Scremin S, Stella GD: Modifications of the biliary excretion of bilirubin glucuronide in rats with portacaval shunt: The role of UDP-glucuronyl transferase. Biomedicine 19:253–256, 1973

    PubMed  Google Scholar 

  18. Hirner A, Roots I, Gundelach J, Hildebrandt AG, Karavias T, Häring R: Change in liver function after portacaval shunt and arterialization as determined by the14C-aminopyrine breath test in rat and man. Eur Surg Res 12 (suppl 1):4, 1980

    Google Scholar 

  19. Bircher J: The rat with portacaval shunt: An animal model with chronic hepatic failure. Pharmacol Ther 5:219–222, 1979

    Google Scholar 

  20. Lauterburg BH, Sautter U, Presig R, Bircher J: Hepatic functional deterioration following portacaval shunt in the rat. Effects on sulfobromophtalein transport maximum, indocyanine green clearance and galactose elimination capacity. Gastroenterology 71:221–227, 1976

    PubMed  Google Scholar 

  21. Fisher ER, Fisher B: Ultrastructural hepatic changes following partial hepatectomy and portacaval shunt in the rat. Lab Invest 12:929–942, 1975

    Google Scholar 

  22. Oudea P, Bismuth HP: L'anastomose porto-cave expérimentale chez le rat normal. Etude des lésions hépatiques par la microscopie électronique. Pathol Biol 13:288–296, 1965

    PubMed  Google Scholar 

  23. Mallet-Guy P, Feroldi J, Mallet-Guy Y, de Roissard JP, Herez G: Les lésions hépatiques de l'anastomose porto-cave termino-latérale. Lyon Chir 67:181–192, 1971

    PubMed  Google Scholar 

  24. Marks C, Markey C, Dyer R, Vaupel MR: An electron microscopic study of the effects of portacaval shunts on the ultrastructure of the rat liver after partial hepatectomy. Am J Surg 129:156–162, 1975

    PubMed  Google Scholar 

  25. Putnam CW, Porter KA, Starzl TE: Hepatic encephalopathy and light and electron micrographic changes of the baboon liver after portal diversion. Ann Surg 184:155–161, 1976

    PubMed  Google Scholar 

  26. Bioulac P, Dubuisson L, Saric J, Balabaud C: Etude ultrastructurale des différentes zones de l'acinus hépatique de rat après anastomose porto-cave. CR Soc Biol 173:60–67, 1979

    Google Scholar 

  27. Rubin E, Gevirtz NR, Cohan P, Fusayoshi T, Jacobson JH: Liver cell damage produced by portacaval shunts. Proc Soc Exp Biol Med 118:235–237, 1965

    PubMed  Google Scholar 

  28. Terlunen E, Altenahr E, Becker K, Ossenberg FW: Liver atrophy following portacaval shunt in normal rats. A morphometric study. Res Exp Med 170:133–142, 1977

    Google Scholar 

  29. Dubuisson L, Saric J, Balabaud C, Bioulac P: Liver ultrastructure of the rat with portacaval shunt. A stereological study. Gastroenterology 79:1105, 1980

    Google Scholar 

  30. Gumucio JJ, Miller DL: Functional implications of liver atrophy and portacaval shunt. Gastroenterology 80:393–403, 1981

    PubMed  Google Scholar 

  31. Lee S, Chandler JG, Broelsch C, Flamant YM, Orloff MJ: Portal systemic anastomosis in the rat. J Surg Res 17:53–73, 1974

    PubMed  Google Scholar 

  32. Miller DL, Harasin JM, Gumucio JJ: Bromobenzene induced zonal necrosis in the hepatic acinus. Exp Mol Pathol 29:358–370, 1978

    PubMed  Google Scholar 

  33. Weibel ER, Bolender RP: Stereological techniques for electron microscopy morphometry.In Principles and Techniques for Electron Microscopy. MA Hayatt (eds). New York, Van Nostrand Reinhold, 1973, pp 237–295

    Google Scholar 

  34. Weibel ER, Kistler GS, Scherle WF: Practical stereological methods for morphometric cytology. J Cell Biol 38:23–28, 1966

    Google Scholar 

  35. Weibel ER, Staubli W, Gnagi HR: Correlated morphometric and biochemical studies on the liver cell. 1 morphometric model, stereological methods and normal morphometric data for rat liver. J Cell Biol 42:68–91, 1969

    PubMed  Google Scholar 

  36. Schmucker DL, Jones AL, Mills ES: Morphometric analysis of the ultrastructural changes in the liver of aging rats. J Gerontol 29:506–513, 1974

    PubMed  Google Scholar 

  37. Loud AV, Barany WC, Pack BA: Quantitative evaluation of cytoplasmic structures in electron micrographs. Lab Invest 14:966–1008, 1965

    Google Scholar 

  38. Pector JC, Ossenberg FW, Peignou M, Benhamou JP: The effect of portacaval transposition on hepatic cytochrome P450 in the rat. Biomedicine 23:160–162, 1975

    PubMed  Google Scholar 

  39. Pector JC, Verbeustel S, Lambilliotte JP: Effect of portal arterialization on hepatic cytochrome P450 in rats with portacaval shunt. Digestion 12:144–151, 1975

    PubMed  Google Scholar 

  40. Ossemberg FW, Pointard L, Benhamou JP: Effect of portacaval shunt on hepatic cytochrome P450 in rats. Rev Eur Etude Clin Biol 17:791–793, 1972

    Google Scholar 

  41. Coyle JJ, Schwartz MZ, Marubbio AT, Varco RL, Buchwald H: The effect of portacaval shunt on plasma lipids and tissue cholesterol synthesis in the dog. Surgery 80:54–60, 1976

    PubMed  Google Scholar 

  42. Jones AL, Schmucker DL: Current concept of liver structure as related to function. Gastroenterology 73:833–851, 1977

    PubMed  Google Scholar 

  43. Jones AL, Schmucker DL, Mooney JS, Ockner RK, Adler RD: Alterations in hepatic pericanalicular cytoplasm during enhanced bile secretory activity. Lab Invest 40:512–517, 1979

    PubMed  Google Scholar 

  44. Boyer JL, Itabashi M, Hruban Z: Formation of pericanalicular vacuoles during sodium dehydrocholate choleresis—a mechanism for bile acid transport.In The Liver, Third International Gstaad Symposium, R Preisig, J Bircher (eds). Aulendorf Editio Cantor, 1978, pp 163–178

  45. Herz R, Paumgartner G, Preisig R: Bile salt metabolism and bile formation in the rat with a portacaval shunt. Eur J Clin Invest 4:223–228, 1974

    PubMed  Google Scholar 

  46. Bioulac P, Dubuisson L, Saric J, Despuyoos L, Bedin C, Magne F, Balabaud C: Chronic biliary drainage corrects liver atrophy induced by portacaval shunt in the rat. Gastroenterology 80:1023–1030, 1981

    PubMed  Google Scholar 

  47. Boyd GS, Lawson ME: The effect of portacaval transposition on hepatic cholesterol-hydroxylase activity in the rat. FEBS Lett 64:435–439, 1976

    PubMed  Google Scholar 

  48. Jones AL, Schmucker DL, Mooney JS, Adler RD, Ockner RK: Quantitative analysis of hepatic ultrastructure in rats during enhanced bile secretion. Anat Rec 192:272–287, 1978

    Google Scholar 

  49. Fowler BA, Woods JS, Schiller CM: Studies of hepatic mitochondrial structure and function. Morphometric and biochemical evaluation ofin vivo perturbation by arsenate. Lab Invest 41:313–320, 1979

    PubMed  Google Scholar 

  50. Fisher LG: Portosystemic encephalopathy.In Liver and Biliary Disease Pathophysiology, Diagnosis, Management. KG Alberty, S Karran, GH Millward-Sadler (eds). London, Saunders Company Ltd, 1979, pp 973–1001

    Google Scholar 

  51. Fisher B, Fisher ER, Lee S: Experimental evaluation of liver atrophy and portacaval shunt. Surg Gynecol Obstet 125:1253–1258, 1967

    PubMed  Google Scholar 

  52. Fisher B, Russ C, Updegraff H, Fisher ER: Effect of increased hepatic blood flow upon liver regeneration. Arch Surg 69:263–272, 1954

    Google Scholar 

  53. Starzl TE, Porter KA, Francavilla JA, Benichou J, Putnam CW: A hundred years of the hepatotrophic controversy.In Hepatotrophic Factors (Ciba Foundation 55). R Porter, J Whelan (eds). Amsterdam, Elsevier, 1978, pp 115–151

    Google Scholar 

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Authors and Affiliations

  1. Centre de Microscopie Electronique, Universite de Bordeaux II, 33076, Bordeaux Cedex, France

    Liliane Dubuisson,  Paulette Bioulac, Jean Saric & Charles Balabaud

  2. Laboratoire des Interactions Cellulaires, Universite de Bordeaux II, 33076, Bordeaux Cedex, France

    Liliane Dubuisson,  Paulette Bioulac, Jean Saric & Charles Balabaud

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  1. Liliane Dubuisson
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  2. Paulette Bioulac
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  3. Jean Saric
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  4. Charles Balabaud
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Dubuisson, L., Bioulac, P., Saric, J. et al. Hepatocyte ultrastructure in rats with portacaval shunt. Digest Dis Sci 27, 1003–1010 (1982). https://doi.org/10.1007/BF01391746

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  • DOI: https://doi.org/10.1007/BF01391746

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