Abstract
Dimensional alteration of hepatic microvessels was demonstrated during reperfusion after normothermic hepatic ischemia. Using a specially designed cover glass, it was possible to relocate selected sites of observation and microvessels repeatedly throughout the whole reperfusion time. Twenty minutes of hepatic ischemia resulted in a decrease of sinusoidal diameter (mean±SEM; 10.0±0.3 μm at baseline, 8.2±0.2 μm after ischemia) and diameter of postsinusoidal venules (26.4±1.2 at baseline, 23.0±1.0 after ischemia). In the control group (no ischemia induced) no changes of these parameters were observed. Thus, the reduction of hepatic microvascular cross section was present during the early phase of reperfusion. Hepatic dysfunction was characterized by increased serum activity of liver enzymes and reduction of bile flow in the ischemia-exposed animals. It has been suggested that postischemic dimensional microvascular changes are involved in postischemic liver dysfunction.
Similar content being viewed by others
References
Vollmar B, Glasz J, Post S, Menger MD (1996) Role of microcirculatory derangements in manifestation of portal triad cross-clamping-induced hepatic reperfusion injury. J Surg Res 60:49–54
Menger MD, Müller MJ, Friedl HP, Trentz O, Messmer K (1992) Ischemia-reperfusion injury of the liver: role of neutrophils and xanthine oxidase. In: Faist E, Meakins J, Schildberg FW (eds) Host defence dysfunction in trauma. Shock and Sepsis. Springer, Berlin Heidelberg New York, pp 499–503
Menger MD, Vollmar B, Glasz J, Post S, Messmer K (1993) Microcirculatory manifestations of hepatic ischemia/reperfusion injury. In: Messmer K, Menger MD (eds) Liver microcirculation and hepatobiliary function. Prog Appl Microvasc 19:106–124
Rappaport AM, Borowy ZJ, Lougheed WM, Lotto WN (1954) Subdivision of hexagonal liver lobules into a structural and functional unit. Anat Rec 119:11–33
Rappaport AM (1958) The structural and functional unit in the human liver (liver acinus). Anat Rec 130:673–689
Wisse E, Zanger RD, Jacobs R, McCuskey RS (1983) Scanning electron microscope observations on the structure of portal veins, sinusoids and central veins in rat liver. Scanning Electron Microsc 3:1441–1452
Lim SP, Andrews FJ, Christophi C, O’Brien PE (1994) Microvascular changes in liver after ischemia-reperfusion injury. Protection with misoprostol. Dig Dis Sci 39: 1683–1690
Motta P (1975) A scanning electron microscopic study of the rat liver sinusoid: endothelial and Kupffer cells. Cell Tissue Res 164:371–385
Gundersen Y, Corso CO, Leiderer R, Dörger M, Lilleaasen P, Aasen AA, Messmer K (1997) Use of selective and nonselective nitric oxide synthase inhibitors in rat endotoxemia: effects on hepatic morphology and function. Shock 8:368–372
Bauer M, Marzi I, Ziegenfuß T, Seeck G, Bühren V, Larsen R (1993) Comparative effects of crystalloid and small volume hypertonic hyperoncotic fluid resuscitation on hepatic microcirculation after hemorrhagic shock. Circ Shock 40:187–193
Zhang JX, Pegoli W, Clemens MG (1994) Endothelin-1 induces direct constriction of hepatic sinusoids. Am J Physiol 266:G624–G632
Okumura S, Takei Y, Kawano S, Nagano K, Masuda E, Goto M, Tsuji S, Michida T, Chen S-S, Kashiwagi T, Fusamoto H, Kamada T, Sato N (1994) Vasoactive effect of endothelin-1 on rat liver in vivo. Hepatology 19:155–161
Zhang JX, Bauer M, Clemens MG (1995) Vessel- and target cell-specific actions of en-dothelin-1 and endothelin-3 in rat liver. Am J Physiol 269:G269–G277
Bauer M, Paquette NC, Zhang JX, Bauer I, Pannen BHJ, Kleeberger SR, Clemens MG (1995) Chronic ethanol consumption increases hepatic sinusoidal contractile response to endothelin-1 in the Rat. Hepatology 22:1565–1576
Goto M, Takei Y, Kawano S, Nagano K, Tsuji S, Masuda E, Nishimura Y, Okumura S, Kashiwagi T, Fusamoto H, Kamada T (1994) Endothelin-1 is involved in the pathogenesis of ischemia/reperfusion liver injury by hepatic microcirculatory disturbances. Hepatology 19:675–681
Chun K, Zhang J, Biewer J, Ferguson D, Clemens MG (1994) Microcirculatory failure determines lethal hepatocyte injury in ischemic/reperfused rat livers. Shock 1:3–9
Kondo T, Okamoto S, Todoroki T, Hirano T, Schildberg FW, Messmer K (1998) Application of a novel method for subsequent evaluation of sinusoids and postsinusoidal venules after ischemia-reperfusion injury of rat liver. Eur Surg Res 30:252–258
Rappaport AM (1973) The microcirculatory hepatic unit. Microvasc Res 6:212–228
Grisham JW, Nopanitaya W, Compagno J (1976) Scanning electron microscopy of the liver: a review of methods and results. Prog Liver Dis 5:1–23
Prado R, Watson BD, Kuluz J, Dietrich WD (1992) Endothelium-derived nitric oxide synthase inhibition. Stroke 23:1118–1124
Ngai AC, Winn HR (1995) Modulation of cerebral arteriolar diameter by intraluminal flow and pressure. Circ Res 77:832–840
Wit Cd, Bismarck P, Pohl U (1993) Mediator role of prostaglandins in acetylcholine-induced vasodilation and control of resting vascular diameter in the hamster cremaster microcirculation in vivo. J Vasc Res 30:272–278
Saito Y, Eraslan A, Hester RL (1994) Role of EDRFs in the control of arteriolar diameter during increased metabolism of striated muscle. Am J Physiol 267: H195–H200
Lefroy DC, Crake T, Uren NG, Davies GJ, Maseri A (1993) Effect of inhibition of nitric oxide synthesis on epicardial coronary artery caliber and coronary blood flow in humans. Circulation 88:43–54
Jaeschke H, Schini VB, Farhood A (1992) Role of nitric oxide in the oxidant stress during ischemia/reperfusion injury of the liver. Life Sci 50:1797–1804
Kobayashi H, Nonami T, Kurokawa T, Takeuchi Y, Harada A, Nakao A, Takagi H (1995) Role of endogenous nitric oxide in ischemia-reperfusion injury in rat liver. J Surg Res 59:772–779
Langle F, Roth E, Steininger R, Winkler S, Mühlbacher F (1995) Arginase release following liver reperfusion. Evidence of hemodynamic action of arginase infusions. Transplantation 59:1542–1549
Wang Y, Mathews WR, Guido DM, Farhood A, Jaeschke H (1995) Inhibition of nitric oxide synthesis aggravates reperfusion injury after hepatic ischemia and endotoxemia. Shock 4:282–288
Ma TT, Ischiropoulos H, Brass CA (1995) Endotoxin-stimulated nitric oxide production increases injury and reduces rat liver chemiluminescence during reperfusion. Gastroenterology 108:463–469
Liu P, Yin K, Yue G, Wong PY (1995) Role of nitric oxide in hepatic ischemia-reperfusion with endotoxemia. J Inflamm 46:144–154
Peralta C, Closa D, Hotter G, Gelpí E, Prats N, Roselló CJ (1996) Liver ischemic pre-conditioning is mediated by the inhibitory action of nitric oxide on endothelin. Biochem Biophys Res Commun 229:264–270
Shiraishi M, Kusano T, Aihara T, Ikeda Y, Koyama Y, Muto Y (1996) Protection against hepatic ischemia/reperfusion injury by exogenous L-arginine. Transplant Proc 28:1887–1888
Saito A, Matsuno N, Kozaki K, Sakurai E, Takeuchi H, Uchiyama M, Kozaki M (1996) Changes in plasma nitrite/nitrate level after orthotopic liver transplantation in pigs. Transplant Proc 28:1761–1762
Koeppel TA, Thies JC, Schemmer P, Trauner M, Gebhard M-M, Otto G, Post S (1997) Inhibition of nitric oxide synthesis in ischemia/reperfusion of the rat liver is followed by impairment of hepatic microvascular blood flow. J Hepatol 27:163–169
Spiegel HU, Scommotau S, Uhlmann D, Giersch B (1996) Effect of the endothelin receptor antagonist bosentan on postischemic liver microcirculation. Zentralbl Chir 121:788–793
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kondo, T., Todoroki, T., Hirano, T. et al. Impact of ischemia-reperfusion injury on dimensional changes of hepatic microvessels. Res. Exp. Med. 198, 63–72 (1998). https://doi.org/10.1007/s004330050090
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s004330050090