Subdiaphragmatic venous stasis and tissular hypoperfusion as sources of metabolic acidosis during passive portal-jugular and caval-jugular bypasses in dogs

Estase venosa subdiafragmática e hipoperfusão tissular como fontes de acidose metabólica durante desvios porta-jugular e cava-jugular passivos em cães

SUBDIAPHRAGMATIC VENOUS STASIS AND TISSULAR HYPOPERFUSION AS SOURCES OF METABOLIC ACIDOSIS DURING PASSIVE PORTAL-JUGULAR AND CAVAL-JUGULAR BYPASSES IN DOGS¹

Antônio Roberto de Barros Coelho²

Álvaro Antônio Bandeira Ferraz²

Renato Dornelas Câmara Neto²

Ayrton Ponce de Souza³

Edmundo Machado Ferraz⁴

Coelho ARB, Ferraz AAB, Câmara Neto RD, Souza AP, Ferraz EM. Subdiaphragmatic venous stasis and tissular hypoperfusion as sources of metabolic acidosis during passive portal-jugular and caval-jugular bypasses in dogs. Acta Cir Bras [serial online] 2000 Apr-Jun;15(2). Available from: URL: http://www.scielo.br/acb.

SUMMARY: Subdiafragmatic venous decompression during anhepatic stage of canine orthotopic liver transplantation attenuates portal and caval blood stasis and minimize hipoperfusion and metabolic acidosis observed with occlusion of portal and caval veins. During two hours, six dogs submitted to portal-jugular and caval-jugular passive shunts, with maintenance of arterial hepatic flow, were evaluated for pH, carbon dioxide tension (PCO₂), base deficit (BD) and oxygen tension (PO₂) in portal, caval and systemic arterial blood, as well as for increments of BD (DBD) in portal and caval blood. With a confidence level of 95%, the results showed that: 1. There were not changes of pH anDBD in portal and systemic arterial blood in the majority of studied times; 2. There was metabolic acidosis in caval blood; 3. The negative increments of BD (DBD) were higher in caval blood than in splancnic venous blood at T₁₀, T₃₀ and T₁₀₅; and, 4. Deoxigenation of portal and caval blood were detected. Acid-base metabolism and oxigenation monitoring of subdiaphramatic venous blood can constitute an effective way to evaluate experimental passive portal-jugular and caval-jugular bypass in dogs.

SUBJECT HEADINGS: Portal vein. Inferior vena cava. Passive venous shunt. Acid-base balance. Liver transplantation. Dogs.

INTRODUCTION

Total hepatectomy without preserving the retrohepatic vena cava, during orthotopic transplantation in dogs implies in the occlusion of both the portal vein and the inferior vena cava. In this species, simultaneous interruption of the flow of those veins leads to death in a period of up to 35 minutes, mainly as a result of hypovolemia and metabolic acidosis¹.

The studies on the techniques of hepatic orthotopic transplantation in mammals have made possible the development of passive and active veno-venous bypasses^{2,8,9,16,20,21,28,29}, aiming at the attenuation of metabolic and hemodynamic disturbances.

Reports on veno-venous bypass assisted anhepatic animals have revealed arterial metabolic acidosis, attributed either to the inadequacy of the venous drainage or to the peripheral arterial hypoperfusion or even to the absence of liver^{1,7,15,17,26,27,31}. A few observations on acid-base alterations in the blood of the subdiaphragmatic venous system submitted to a passive or active venous decompression during the anhepatic phase of the liver transplantation in animals suggest the occurrence of lactic acidosis^3,17. Such acidosis has been attributed to the stasis in the subdiaphragmatic venous drainage system, resulting in an anaerobic metabolism¹⁷.

The lack of studies about simultaneous metabolic alterations in the venous blood of the subdiaphragmatic territories and in the systemic arterial blood has triggered a systematic investigation of data on the acid-base balance in the blood in these sites, in dogs undergoing passive and simultaneous portal-jugular and caval-jugular bypasses.

METHOD

Six mongrel dogs, of both sexes, with an average body weight of 17.8 ± 2.3 kg, whose livers remained vascularized by the hepatic artery, under general anesthesia with sodic Pentobarbital at a dose of 30 mg/kg and controlled breathing (VC = 15 ml/kg, FiO2 = 21%, FR = 16 cpm), underwent passive and simultaneous portal-jugular and caval-jugular bypasses, with Silastic tubes (I.D. = 4,8 mm - E.D. = 7,9 mm or I.D. = 6,4 mm - E.D. = 9,5 mm) (Fig. 1), chosen in accordance with the diameter of the external jugular veins. Before the installation of the bypasses, a 1 mg/kg dose of endovenous heparin was administered. During the experiments, 250 ml of a Ringer Lactate solution was infused.

For those animals, the pH, the dioxide tension (PCO₂), the base deficit (BD) and the oxygen tension (PO₂) were tested in the blood of the portal vein (PV), in the infrahepatic inferior vena cava (IHIVC) and in the right brachial artery (RBA). The values of these parameters were determined after the dissection of both the portal vein and the infrahepatic inferior vena cava (time zero) and at 5, 10, 15, 30, 45, 60, 75, 90, 105, and 120 minutes of the set-up of the portal-jugular and caval-jugular bypasses. The increments of the base deficit (DBD) were also calculated as compared to time zero at 5, 10, 15, 30, 45, 60, 75, 90, 105, and 120 minutes in the portal blood (DBDPV) and in the blood of the infrahepatic inferior vena cava (DBDIHIVC) after putting the veno-venous bypasses into operation.

A comparative analysis was accomplished between the average of the values of pH, PCO2, BD, and PO2 obtained at "time zero" and those determined in the times subsequent to the installation of the portal-jugular and caval-jugular bypasses. A comparative study was also accomplished between the average of the values of DBDPV and DBDIHIVC, after the installation of the scheduled bypasses, in corresponding times.

The statistical treatment consisted of the application of one-tailed Student's "t" test, with correction of the incidental error and with a confidence interval of 95%. The experiments were driven according to the code of ethics of the WHO for biomedical trials in animals^*.

RESULTS

1. Study of the alterations of the acid-base metabolism in the portal vein blood and in the blood of the inferior vena cava

The comparative study showed that the values of pH, PCO2, and BD in the portal blood after the installation of the bypasses, in most of the studied times, did not differ from those obtained at "time zero", except for BD levels determined at 30, 90, and 120 minutes of the portal-jugular bypass (Table 1).

Drops in the values of pH and BD were verified in the blood of the IHIVC, from 10 minutes of the installation of the veno-venous bypasses until the end of the experiments, when compared to the values obtained at "time zero" (Table 2).

The BD increments in the portal vein (DBDPV) were inferior to those verified in the blood of the vena cava (DBDIHIVC) at times T₁₀, T₃₀, and T₁₀₅ (Table 4). A decline in the levels of PO2 was observed in the blood at the PV and at the IHIVC (Tables 1 and 2). The values of PCO2 remained stable during the experiments, except in the level determined in the blood of the inferior vena cava at 120 minutes of the installation of the bypasses (Tables 1 and 2).

2. Study of the alterations of the acid-base metabolism in the systemic arterial blood

Significant differences between values of pH, PCO2 and BD were not observed in the systemic arterial blood, except in the pH values determined at 30 minutes of the installation of the portal-jugular and caval-jugular bypasses and at the levels of BD verified at 45, 60, and 75 minutes of the installation of these bypasses (Table 3). On the other hand, alterations were not verified with the values of PO2 determined in the systemic arterial blood (Table 3).

DISCUSSION

The use of a passive portosystemic extracorporeal bypass associated to the preservation of the retrohepatic inferior vena cava has been reported in human cases of elective orthotopic transplantation of the liver^4,30, moreover in cases in which there is no previous portal systemic circulation or when a heart disease constitutes a prior disturbance³⁰.

Subdiaphragmatic venous decompression accomplished via active veno-venous bypasses, as well as via portal-caval anastomosis associated to the preservation of the retrohepatic vena cava (Piggy-back technique), have been used in patients with a severely acute hepatic necrosis, undergoing a total hepatectomy or a complete devascularization of the liver, with the objective of avoiding the perfusion of necrotic livers^13,23,24,25. Total hepatectomy using a femoral-atrial passive bypass associated to the portosystemic shunt, without preserving the retrohepatic vena cava, has been occasionally practiced in cases of hepatic trauma¹⁸.

In these cases, the decompression of the subdiaphragmatic venous bed aims at allowing a hemodynamic and metabolic stability during the usually long anhepatic period that precedes the availability of organs for transplantation. In humans, preexisting hepatic disease and portal hypertension, as well as more tendencies for bleeding, constitute additional reasons for the occurrence of hemodynamic disturbances, acid-base metabolism inbalance and blood clotting changes³².

Experimentally, in the anhepatic condition, hemodynamic stability propitiated by the efficient decompression of the PV and of the IHIVC decreases the pooling of blood in these sites, minimizes venous stasis, attenuates the drop of the blood return to the heart and produces less alterations in the tissular perfusion, possibly contributing to a decline in the production of lactic acid and consequently of the arterial metabolic acidosis^{7,15,19,26,27}. The absence of the liver, by itself, has not been considered as the only reason for such a kind of acidosis^26,27,32. It is more likely that the lactate increase is related to the rate of supply of this ion, determined by the occurrence of an anaerobic metabolism and by the content of organic acids in blood transfusion, as well as for the capacity of the myocardium and kidneys in metabolizing them^6,17,32. Eviscerated animals have been able to metabolize exogenous lactate, an indication that oxidation mechanisms are provided by extrahepatic tissue¹⁰.

As emphasized in previous studies, portal and IHIVC stasis, translated by increases of PP and IHIVCP, occurred in dogs undergoing passive portal-jugular and caval-jugular bypasses⁵. Such stasis could induce a decline in the arterial perfusion pressure in the splanchnic territories and in the inferior vena cava territories, a drop in tissular oxygen, an occurrence of anaerobic metabolism, an increase in the production of lactic acid and the development of metabolic acidosis, as suggested in humans undergoing liver transplantation with an active portal-caval-axillary bypass²². Absence of significant alterations of pH in the splanchnic venous blood, as well as the non-existence of drops of BD in the portal blood, in most of the studied times, were emphasized (Table 1).

After the installation of the caval-jugular bypass, significant drops of pH and BD were verified in the blood of the IHIVC in most of the studied times (Table 2). This way, metabolic acidosis, seemingly more pronounced in the blood of the IVC, could be related to the higher degree of pressure than what has been determined in this venous system, as compared to the one verified in the portal territory⁵. However, comparative studies between the degrees of intensity of metabolic acidosis, represented by the increments of BD (DBD) in the blood of the IVC and of the PV, did not present significant differences in most of the evaluation period (Table 4). The PCO2 study on the portal blood and on the blood of the IVC did not reveal significant alterations (Tables 1 and 2).

Blood pooling in the territories of both the PV and the IVC, inducing a significant drop of the CVP, an indication of a decrease in the blood return to the heart, could determine a decline in the cardiac output (CO), a splanchnic and systemic arterial vasoconstriction, as a compensation mechanism, contributing to the maintenance of the levels of MAP and for subsequent drops of PP and of IHIVCP⁵. Such vasoconstriction could contribute to the tissular hypoperfusion and hypoxia, resulting in an anaerobic metabolism and in the production of lactate^26,27,32. In clinical transplantation, during the anhepatic period, a correlation among de drop of the heart index, which indicates a peripheral hypoperfusion and an increase in serum lactate, has been observed¹¹. Under these circumstances, the absence of the liver and the existence of badly perfused extrahepatic tissue could contribute to a decrease in the oxidation of the ion lactate¹¹. By the way, significant drops in the PO₂ were determined in the blood of both the Portal Vein and the infrahepatic inferior vena cava (Tables 1 and 2). This disturbance could be a result of the drop in the level of tissular oxygen, either because of a decrease in the arterial perfusion pressure or because of the previously mentioned splanchnic and systemic vasoconstriction. A sequence of physiopathological events capable of interfering in the occurrence of metabolic acidosis during the functioning of veno-venous bypasses can be seen on Fig. 2.

It is worth to point out that active and passive decompression processes of both the portal vein and the inferior vena cava lead to drops in both the cardiac output (CO) and in the CVP, followed by a compensatory elevation of the systemic vascular resistance (SVR), by means of the vasoconstriction¹⁴.

The non occurrence of significant alterations in the average of the values of pH and BD in the systemic arterial blood, in most of the studied times, after the installation of the portal-jugular and caval-jugular bypasses (Table 3), is an indication of a moderated arterial metabolic acidosis.

Taking into account the occurrence of a subdiaphragmatic venous stasis and probable tissular hypoperfusion, considered as sources of lactic acid production, the appearance of a moderate metabolic acidosis could have been a result of the development of satisfactory blood flows in the veno-venous bypasses used, and also of the removal and metabolization of ions of lactate generated, made possible by means of hepatic function^6,32, and the perfusion pressure to the liver through the hepatic artery was considered appropriate. In in vitro perfused livers, lactate infusion through the portal vein determined an increase in the intrahepatic pH, which indicates a metabolization of lactate, by the liver⁶.

On the other hand, the absence of significant alterations in the levels of PO₂ and of PCO₂ verified in the systemic arterial blood (Table 3), the animals being under controlled breathing with room air, indicates stability of lung ventilation and oxygenation, in the course of the experiments.

In short, the development of a moderate metabolic acidosis in the portal blood, in the blood of the inferior vena cava and in the systemic arterial blood, was attributed to the satisfactory performance of the procedure of the subdiaphragmatic venous decompression studied and the presence of a hepatic function made possible by the liver vascularized by the hepatic artery.

The study of both the acid-base metabolism data and oxygenation data in the subdiaphragmatic venous blood can constitute an effective way to evaluate the passive portal-jugular and caval-jugular bypass efficiency, used in orthotopic liver transplantation in dogs.

CONCLUSIONS

In the present study, results obtained with the use of passive portal-jugular and caval-jugular bypasses in dogs, practiced in an independent and simultaneous way, allow us to conclude, with a 5% error probability, that: 1. Significant alterations of pH and BD were neither verified in the splanchnic venous blood nor in the systemic arterial in most of the studied times; 2. Metabolic acidosis was found in the blood of the IHIVC; 3. The negative increments of BD (DBD) were more significant in the blood of the IHIVC than in the blood of the PV, at times T₁₀, T₃₀, and T₁₀₅; and, 4. Deoxygenation was observed in the splanchnic venous blood and in the blood of the IHIVC.

REFERENCES

1. Arullani A, Gargiulo A, Baroni B, Sanpietro G, Casciani C, Cortesini R. Trapianto di fegato: studio fisiopatologico della fase epatopriva. Il Policlinico 1968;75:319-31.

2. Birtch, A G , Moore, F D. Experience in liver transplantation. Transplant Rev 1969;2:90-128.

3. Boeckl O, Hell E, Zimmermann G, Fitzga H, Jecel P, Gibitz H J. Blutgasanalytische untersuchungen während homologer lebertransplantationen am hausschwein. Z Ges Exp Med 1971;156:67-72.

4. Calne R Y, Williams R. Liver transplantation in man. I. Observations on technique and organization in five cases. Brit Med J 1968;4:535-40.

5. Coelho ARB, Ferraz AAB, Câmara Neto RD, Souza AP, Ferraz EM. Desvios porta-jugular e cava-jugular passivos: investigação de pressões sangüíneas. Acta Cir Bras 1999;14:35-42.

6. Cohen R D, Iles R A, Barnett D, Howell M E O, Strunin J. The effect of changes in lactate uptake on the intracellular pH of the perfused rat liver. Clin Sci 1971;41:159-70.

7. Cucchiara G, Minio Paluello F , Gargiulo A, Boffo V, Elti di Rodeano G. Il trapianto ortotopico di fegato sperimentale: fisiopatologia. Policlinico (Chir.) 1968;75:63-92.

8. Cutropia JC , Coratolo F, Spinetta A, Keil J, Ribas A, Assini L, Delle Donne G, Bianchi M, Guinazu A, Verdaguer J A. Transplante hepático ortotópico experimental. Rev Esp Enf Ap Digest 1972;38:553-70.

9. Denmark SW, Shaw Jr BW, Starzl TE, Griffith BP. Veno-venous bypass without systemic anticoagulation in canine and human liver transplantation. Surg Forum 1983;34:380-2.

10. Drury DR, Wick AN, Morita TN. Metabolism of lactic acid in extrahepatic tissues. Am J Physiol 1955;180:345-9.

11. Fath JJ, Ascher NL, Konstantinides BS, Bloomer J, Sharp H, Najarian JS. Metabolism during hepatic transplantation: indicators of allograft function. Surgery 1984;96:664-74.

12. Howard-Jones N. A CIOMS ethical code for animal experimentation. WHO Chronicle 1985;39:51-6.

13. Husberg BS, Goldstein, RM, Klintmalm GB, Gonwa T, Ramsay M, Cofer J, Solomon H, Watemberg I. A totally failling liver may be more harmful than no liver at all: three cases of total hepatic devascularization in preparation for emergency liver transplantation. Transplant Proc 1991;23:1533-35.

14. Ishine N, Tanaka N, Yagi T, Oishi M, Ishikawa T, Orita K. Postreperfusion syndrome in swine liver transplantation: comparation between orthotopic liver transplantation and total hepatectomy with portocaval shunt using aortic graft. Transplant Proc 1996;28:1756-58.

15. Jakab F, Závodszky Z, Sugár I, Záborszky A, Ráth Z, Metzger P, Ughy T. Changes in pH and acid-base equilibrium during experimental liver transplantation by active and passive veno-venous bypass. Acta Chir Hung 1988;29:107-16.

16. Kaupp HA, Starzl TE. The use of an external bypass during total hepatectomy. Surgery 1960;48:330-3.

17. Lie Von TS, Albrecht F. Die diagnostische Bedeutung der metabolischen Azidose für die ischämische Schädigung eines Lebertransplantates. Zentralbl für Chir 1971;96:272-85.

18. Lin PJ, Jeng LB, Chen RJ, Kao CL, Chu JL, Chang CH. Femoro-atrial bypass using Gott shunt in liver transplatation following severe hepatic trauma. Int Surg 1993;78:295-7.

19. Mann FC. Studies in the physiology of the liver. I. Technic and general effects of removal. Am J Med Sci 1921;161:37-42.

20. Moore FD, Smith LL, Burnap TK, Dallenbach FD, Dammin GJ, Gruber UF, Shoemaker WC, Steenburg RW, Ball MR, Belko JS. One-stage homotransplantation of the liver following total hepatectomy in dogs. Transplant Bull 1959;6:103-7.

21. Moore FD, Wheeler HB, Demissianos HV, Smith LL, Balankura O, Abel K, Greenberg JB, Dammin GJ. Experimental whole-organ transplantation of the liver and of the spleen. Ann Surg 1960;152:374-87.

22. Paulsen AW, Whitten CW, Ramsay MAE, Klintmalm GB. Considerations for anesthetic management during veno-venous bypass in adult hepatic transplantation. Anesth Analg 1989;68:489-96.

23. Ringe B, Lübbe N, Kuse E, Frei U, Pichlmayr R. Management of emergencies before and after liver transplantation by early total hepatectomy. Transplant Proc 1993;25:1090.

24. Ringe B, Lübbe N, Kuse E, Frei U, Pichlmayr R. Total hepatectomy and liver transplantation as two-stage procedure. Ann Surg 1993;218:3-9.

25. Ringe B, Pichlmayr R, Lübbe N, Bornscheuer A, Kuse E. Total hepatectomy as a temporary approach to acute hepatic or primary graft failure. Transplant Proc 1988;20:552-7.

26. Serrou B, Coburg AJ, Abouna GM, Aldrete JA. Hemodynamic and metabolic stability after total hepatectomy in the dog. Int Surg 1971;55:235-42.

27. Serrou B, Michel H, Coburg A, Abouna GM, Karcenty L, Solassol CL, Romieu Cl. Hépatectomie totale chez le chien: étude appliquée à la transplantation du foie. Lyon Chir 1971;67:385-8.

28. Starzl TE, Kaupp Jr H, Brock DR, Lazarus RE, Johnson RV. Reconstructive problems in canine liver homotransplantation with special reference to the postoperative role of hepatic venous flow. Surg Gynecol Obstet 1960;111:733-43.

29. Starzl TE, Putnam CW. Experience in hepatic transplantation. Philadelphia: W.B. Saunders; 1969.

30. Stieber AC. One surgeon’s experience with the piggyback versus the standard technique in orthotopic liver transplantation: is one better than the other? Hepatogastroenterol 1995;42:403-5.

31. TØnnesen K. Experimental liver failure: a comparison between hepatectomy and hepatic devascularization in the pig. Acta Chir Scand 1977;143:271-77.

32. Thompson JF, Bell R, Bookallil MJ, Sheil AGR. Effects of total hepatectomy: studies in a porcine model. Aust NZ J Surg 1994;64:560-4.

Coelho ARB, Ferraz AAB, Câmara Neto RD, Souza AP, Ferraz EM. Estase venosa subdiafragmática e hipoperfusão tissular como fontes de acidose metabólica durante desvios porta-jugular e cava-jugular passivos em cães. Acta Cir Bras [serial online] 2000 Apr-Jun;15(2). Available from: URL: http://www.scielo.br/acb.

RESUMO: A descompressão venosa subdiafragmática durante a fase anhepática do transplante ortotópico de fígado em cães atenua a estase de sangue nas veias Porta e Cava Inferior e minimiza a hipoperfusão tissular e a acidose metabólica observadas na oclusão dessas veias. Durante duas horas, seis cães submetidos a desvios porta-jugular e cava-jugular passivos, com permanência do fluxo arterial hepático, foram avaliados através de pH, PCO₂, DB e PO₂ no sangue portal, da Veia Cava Inferior e arterial sistêmico, bem como por incrementos de DB (DDB) no sangue portal e da Veia Cava Inferior. Os resultados obtidos permitem concluir com uma confiança de 95% que: 1. Não foram constatadas alterações de pH e DB no sangue portal e arterial sistêmico na maioria dos tempos estudados; 2. Houve acidose metabólica no sangue da VCIIH; 3. Os incrementos negativos da DB (DDB) foram mais intensos no sangue da VCIIH do que no sangue da VP, em T₁₀, T₃₀ e T₁₀₅; e, 4. Ocorreu desoxigenação no sangue portal e da VCIIH. O acompanhamento do equilíbrio ácido-básico e da oxigenação no sangue venoso subdiafragmático pode constituir uma maneira efetiva de avaliar os desvios porta-jugular e cava-jugular passivos em cães.

DESCRITORES: Veia porta. Veia cava inferior. Desvio venoso passivo. Equilíbrio ácido-básico. Transplante de fígado. Cães.

Endereço para correspondência:

Edmundo Machado Ferraz

Rua Dom Sebastião Leme, 171/2501

Recife - PE

52011-160

Tel./Fax: [phone]

e-mail: [e-mail]

Data do recebimento: 20/03/2000

Data da revisão: 12/04/2000

Data da aprovação: 05/05/2000

• 2. Birtch, A G , Moore, F D. Experience in liver transplantation. Transplant Rev 1969;2:90-128.
• 3. Boeckl O, Hell E, Zimmermann G, Fitzga H, Jecel P, Gibitz H J. Blutgasanalytische untersuchungen während homologer lebertransplantationen am hausschwein. Z Ges Exp Med 1971;156:67-72.
• 4. Calne R Y, Williams R. Liver transplantation in man. I. Observations on technique and organization in five cases. Brit Med J 1968;4:535-40.
• 5. Coelho ARB, Ferraz AAB, Câmara Neto RD, Souza AP, Ferraz EM. Desvios porta-jugular e cava-jugular passivos: investigaçăo de pressőes sangüíneas. Acta Cir Bras 1999;14:35-42.
• 6. Cohen R D, Iles R A, Barnett D, Howell M E O, Strunin J. The effect of changes in lactate uptake on the intracellular pH of the perfused rat liver. Clin Sci 1971;41:159-70.
• 9. Denmark SW, Shaw Jr BW, Starzl TE, Griffith BP. Veno-venous bypass without systemic anticoagulation in canine and human liver transplantation. Surg Forum 1983;34:380-2.
• 10. Drury DR, Wick AN, Morita TN. Metabolism of lactic acid in extrahepatic tissues. Am J Physiol 1955;180:345-9.
• 11. Fath JJ, Ascher NL, Konstantinides BS, Bloomer J, Sharp H, Najarian JS. Metabolism during hepatic transplantation: indicators of allograft function. Surgery 1984;96:664-74.
• 12. Howard-Jones N. A CIOMS ethical code for animal experimentation. WHO Chronicle 1985;39:51-6.
• 13. Husberg BS, Goldstein, RM, Klintmalm GB, Gonwa T, Ramsay M, Cofer J, Solomon H, Watemberg I. A totally failling liver may be more harmful than no liver at all: three cases of total hepatic devascularization in preparation for emergency liver transplantation. Transplant Proc 1991;23:1533-35.
• 14. Ishine N, Tanaka N, Yagi T, Oishi M, Ishikawa T, Orita K. Postreperfusion syndrome in swine liver transplantation: comparation between orthotopic liver transplantation and total hepatectomy with portocaval shunt using aortic graft. Transplant Proc 1996;28:1756-58.
• 15. Jakab F, Závodszky Z, Sugár I, Záborszky A, Ráth Z, Metzger P, Ughy T. Changes in pH and acid-base equilibrium during experimental liver transplantation by active and passive veno-venous bypass. Acta Chir Hung 1988;29:107-16.
• 16. Kaupp HA, Starzl TE. The use of an external bypass during total hepatectomy. Surgery 1960;48:330-3.
• 17. Lie Von TS, Albrecht F. Die diagnostische Bedeutung der metabolischen Azidose für die ischämische Schädigung eines Lebertransplantates. Zentralbl für Chir 1971;96:272-85.
• 18. Lin PJ, Jeng LB, Chen RJ, Kao CL, Chu JL, Chang CH. Femoro-atrial bypass using Gott shunt in liver transplatation following severe hepatic trauma. Int Surg 1993;78:295-7.
• 19. Mann FC. Studies in the physiology of the liver. I. Technic and general effects of removal. Am J Med Sci 1921;161:37-42.
• 20. Moore FD, Smith LL, Burnap TK, Dallenbach FD, Dammin GJ, Gruber UF, Shoemaker WC, Steenburg RW, Ball MR, Belko JS. One-stage homotransplantation of the liver following total hepatectomy in dogs. Transplant Bull 1959;6:103-7.
• 21. Moore FD, Wheeler HB, Demissianos HV, Smith LL, Balankura O, Abel K, Greenberg JB, Dammin GJ. Experimental whole-organ transplantation of the liver and of the spleen. Ann Surg 1960;152:374-87.
• 22. Paulsen AW, Whitten CW, Ramsay MAE,  Klintmalm GB. Considerations for anesthetic management during veno-venous bypass in adult hepatic transplantation. Anesth Analg 1989;68:489-96.
• 23. Ringe B, Lübbe N, Kuse E, Frei U, Pichlmayr R. Management of emergencies before and after liver transplantation by early total hepatectomy. Transplant Proc 1993;25:1090.
• 24. Ringe B, Lübbe N, Kuse E, Frei U, Pichlmayr R. Total hepatectomy and liver transplantation as two-stage procedure. Ann Surg 1993;218:3-9.
• 25. Ringe B, Pichlmayr R, Lübbe N, Bornscheuer A, Kuse E. Total hepatectomy as a temporary approach to acute hepatic or primary graft failure. Transplant Proc 1988;20:552-7.
• 26. Serrou B, Coburg AJ, Abouna GM, Aldrete JA. Hemodynamic and metabolic stability after total hepatectomy in the dog. Int Surg 1971;55:235-42.
• 27. Serrou B, Michel H, Coburg A, Abouna GM, Karcenty L, Solassol CL, Romieu Cl. Hépatectomie totale chez le chien: étude appliquée ŕ la transplantation du foie. Lyon Chir 1971;67:385-8.
• 28. Starzl TE, Kaupp Jr H, Brock DR, Lazarus RE, Johnson RV. Reconstructive problems in canine liver homotransplantation with special reference to the postoperative role of hepatic venous flow. Surg Gynecol Obstet 1960;111:733-43.
• 29. Starzl TE, Putnam CW. Experience in hepatic transplantation. Philadelphia: W.B. Saunders; 1969.
• 30. Stieber AC. One surgeons experience with the piggyback versus the standard technique in orthotopic liver transplantation: is one better than the other? Hepatogastroenterol 1995;42:403-5.
• 31. TŘnnesen K. Experimental liver failure: a comparison between hepatectomy and hepatic devascularization in the pig. Acta Chir Scand 1977;143:271-77.
• 32. Thompson JF, Bell R, Bookallil MJ, Sheil AGR. Effects of total hepatectomy: studies in a porcine model. Aust NZ J Surg 1994;64:560-4.

1-

From the Nucleus of Experimental Surgery, Department of Surgery - Federal University of Pernambuco. Supported by grant from FACEPE (APQ - 0476-4.01/93).

2-

Associated Professor of Abdominal Surgery, Department of Surgery - Federal University of Pernambuco, Doctor in Medicine.

3-

Professor of Post-graduation Courses, Federal University of Pernambuco, Doctor in Medicine.

4-

Head Professor of Abdominal Surgery, Department of Surgery - Federal University of Pernambuco, Doctor in Medicine.

*

Howard-Jones N. A CIOMS ethical code for animal experimentation. WHO Chronicle, 1985 ; 39: 51-6

¹².

Publication Dates

• Publication in this collection
  08 June 2000
• Date of issue
  June 2000

History

• Accepted
  05 May 2000
• Reviewed
  12 Apr 2000
• Received
  20 Mar 2000