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Oxidative stress in rodent closed duodenal loop pancreatitis

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Summary

Conclusions

Production of excited oxygen species is earlier in the liver than in the pancreas and could contribute to damage in a reflux model. Treatment with SOD could attenuate 59% light emission in pancreas, but did not modify serum enzyme levels or pancreatic edema, resulting as an insufficient isolated therapy. Unexpectedly, it was found an increased plasma antioxidant capacity that was related to total bilirubin levels, and declined at late stages probably denoting other circulating antioxidant consumption.

Background

Oxidative stress has been shown to play a role in different models of acute pancreatitis, although it has not been studied in the severe necrohemorrhagic model produced by closed duodenal loop pancreatitis.

Methods

We studied Sprague Dawley female rats in two groups: a closed duodenal loop pancreatitis group and a control, sham-operated group. In order to evidence the oxygen excited species production,in situ spontaneous chemiluminescence from living and naturally perfused pancreas and liver was measured at 0, 0.5, 1.5, 3, 6, 12, and 24 h after the duodenal ligature. Blood pancreatic amylase and aminotransferases levels were determined as expression of tissue damage in pancreas and liver. At the same time, plasma antioxidant capacity was measured by the peroxyl radical trapping capability of plasma samples compared to that of Trolox (synthetic analog of vitamin E), and results are expressed as Trolox equivalence. Bovine superoxide dismutase (SOD) was administered to attenuate oxygen free radicals activity at the beginning of the peroxidation chain and also as a therapeutic tool.

Results

The experimental procedure induced a severe pancreatitis, as evidenced by pancreatic enzymes that rose markedly in the early hours of disease and remained heightened throughout the experiment. The results show early light emission from the liver at 3 h and peak levels at 12 h, whereas in the pancreas, luminescence increased at 6 h and doubled later at 12 h, both returning to control levels at 24 h.

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References

  1. Schölmerich J. Special Topic: Pancreatitis.Hepato-Gastroenterol 1993; 40: 514–516.

    Google Scholar 

  2. Gough DB, Boyle B, Joyce WP, Delaney CP, McGeeney KE, Gorey TE, Fitzpatrick JM. Free radical inhibition and serial chemiluminescence in evolving experimental pancreatitis.Br J Surg 1990; 77: 1256–1259.

    Article  PubMed  CAS  Google Scholar 

  3. Dabrowski A, Gabryelewicz A. Oxidative stress-An early phenomenon characteristic of acute experimental pancreatitis.Int J Pancreatol 1986; 1: 237–248.

    Google Scholar 

  4. Schoenberg MH, Büchler M, Schädlich H, Younes M, Bültmann B, Beger HG. Involvement of oxygen radicals and phospholipase A2 in acute pancreatitis of the rat.Klin Wochenschr 1989; 67: 166–170.

    Article  PubMed  CAS  Google Scholar 

  5. Rutledge PL, Saluja AK, Powers RE, Steer ML. Role of oxygen-derived free radicals in diet-induced hemorrhagic pancreatitis in mice.Gastroenterology 1987; 93: 41–47.

    PubMed  CAS  Google Scholar 

  6. Sanfey H, Bulkey GB, Cameron JL. The role of oxygen-derived free radicals in the pathogenesis of acute pancreatitis.Ann Surg 1984; 200: 405–413.

    Article  PubMed  CAS  Google Scholar 

  7. Anderson RJL, Jeffrey IJM, Kay PM, Braganza JM. Peroxidised linoleic acid and experimental pancreatitis.Int J Pancreatol 1986; 1: 237–248.

    PubMed  CAS  Google Scholar 

  8. Braganza JM, Wickens DG, Cawood P, Dormandy TL. Lipid peroxidation (free-radical-oxidation) products in bile from patients with pancreatic disease.Lancet 1983; ii: 375–379.

    Article  Google Scholar 

  9. Guyan PM, Uden S, Braganza JM. Heightened free radical activity in pancreatitis.Free Radical Biol & Med 1990; 8: 347–359.

    Article  CAS  Google Scholar 

  10. Peralta JG, Reides C, Pargament G, Carreras MC, Llesuy S, Poderoso JJ. Estress oxidativo en la pancreatitis aguda por reflujo duodenal.Medicina(BsAs) 1993; 53: 123–124.

    Google Scholar 

  11. Boveris A, Cadenas E, Reiter R, Filipowsky M, Nakase Y, Chance B. Organ chemiluminescence: Noninvasive assay for oxidative radical reactions.Proc Natl Acad Sci USA 1980; 77: 347–351.

    Article  PubMed  CAS  Google Scholar 

  12. Nevalainen TJ, Seppa A. Acute pancreatitis caused by closed duodenal loop in the rat.Scand J Gastroenterol 1975, 10: 521–527.

    PubMed  CAS  Google Scholar 

  13. Pfeffer RB, Stasior O, Hilton JW. The clinical picture of the sequential development of acute hemorrhagic pancreatitis in the dog.Surg Forum 1957; 8: 248–51.

    PubMed  CAS  Google Scholar 

  14. Adler G, Kern HF, Scheele GA. Experimental models and concepts in acute pancreatitis, inThe Exocrine Pancreas: Biology, Pathobiology, and Diseases, Go VLW, Gardner JD, Brooks FP, Lebenthal E, Di Magno EP, Scheele GA, eds., Raven, New York 1986; pp. 407–421.

    Google Scholar 

  15. Wayner DDM, Burton GW, Ingold KU, Locke SJ. Quantitative measurement of the total peroxyl radical-trapping antioxidant capability of human blood plasma by controlled lipid peroxidation.FEBS Lett 1985; 187: 33–37.

    Article  PubMed  CAS  Google Scholar 

  16. Lissi E, Pascual C, Del Castillo MD. Luminol luminescence induced by 2,2′-AZO-bis(2-Amidinopropane)thermolysis.Free Radical Res Commun 1992; 17: 299–311.

    Article  CAS  Google Scholar 

  17. Markert M, Andrews PC, Babior BM. Measurement of O2-production by human neutrophils. The preparation and assay of NADPH oxidase-containing particle from human neutrophils.Methods Enzymol 1984; 105: 358–361.

    Article  PubMed  CAS  Google Scholar 

  18. Peterson BT, Brooks JA, Zack AG. Use of microwave oven for determination of postmortem water volume of lungs.J Appl Physiol 1982; 52: 1661–1663.

    PubMed  CAS  Google Scholar 

  19. Peralta J, Llesuy S, Evelson P, Carreras MC, Gonzalez Flecha B, Poderoso JJ. Oxidative stress in skeletal muscle during sepsis in rats.Circ Shock 1993; 39: 153–159.

    PubMed  CAS  Google Scholar 

  20. Llesuy S, Evelson P, Gonzalez Flecha B, Peralta J, Carreras MC, Poderoso JJ, Boveris A. Oxidative stress in muscle and liver of rats with septic syndrome.Free Radical Med & Biol 1994; 16: 445–451.

    Article  CAS  Google Scholar 

  21. Turrens JF, Giulivi C, Pinus CR, Lavagno C, Boveris A. Spontaneous lung chemiluminescence upon paraquat administration.Free Radical Med & Biol 1988; 5: 319–323.

    Article  CAS  Google Scholar 

  22. Peralta J, Barnard M, Turrens JF. Characteristics of neutrophil influx in rat lungs following fecal peritonitis.Inflammation 1993; 17: 263–271.

    Article  PubMed  CAS  Google Scholar 

  23. Boveris A, Llesuy S, Fraga CG. Increased liver chemiluminescence in tumor bearing mice.Free Radical Med & Biol 1985; 1: 131–138.

    Article  CAS  Google Scholar 

  24. Roldan EJ, Pinus CR, Turrens JF, Boveris A. Chemiluminescence of ischaemic and reperfused intestine in vivo.Gut 1989; 30: 184–187.

    Article  PubMed  CAS  Google Scholar 

  25. Murphy ME, Sies H. Visible-range low level chemiluminescence in biological systems, inMethods in Enzymology, Packer L, Glazer AN, eds., Academic, New York, 1990, p. 595.

    Google Scholar 

  26. Barnard ML, Gurdian D, Diep D, Ladd M, Turrens JF. Protein and aminoacid oxidation is associated with increased chemiluminescence.Arch Biochem Biophys 1993; 300: 651–656.

    Article  PubMed  CAS  Google Scholar 

  27. Sarr MG, Bulkey GB, Cameron JL. The role of leukocytes in the production of oxygen-derived free radicals in acute experimental pancreatitis.Surgery 1987; 101: 292–296.

    PubMed  CAS  Google Scholar 

  28. Sokol R, Devereaux M, Khandwala RA. Effect of dietary lipid and vitamin E on mitochondrial lipid peroxidation and hepatic injury in the bile duct-ligated rat.J Lipid Res 1991; 32: 1349–1357.

    PubMed  CAS  Google Scholar 

  29. Dahm LJ, Hewett JA, Roth RA. Bile and bile salts potentiate superoxide anion release from activated rat peritoneal neutrophils.Toxicol Appl Pharmacol 1988; 95: 82–92.

    Article  PubMed  CAS  Google Scholar 

  30. Turrens JF. The potential of antioxidant enzymes as pharmacological agents in vivo.Xenobiotica 1991; 21: 1033–1040.

    Article  PubMed  CAS  Google Scholar 

  31. Rao SS, Watt IA, Donaldson LA, Crocket A, Joffe SN. A serial histologic study of the development and progression of acute pancreatitis in the rat.Am J Pathol 1981; 103: 39–46.

    PubMed  CAS  Google Scholar 

  32. Dickson AP, Foulis AK, Imrie CW. Histology and bacteriology of closed duodenal loop models of experimental acute pancreatitis in the rat.Digestion 1986; 34: 15–21.

    PubMed  CAS  Google Scholar 

  33. Carreras MC, Catz SD, Pargament G, Del Bosco CG, Poderoso JJ. Decreased production of nitric oxide by human neutrophils during septic multiple organ dysfunction syndrome—comparison with endotoxin and cytokine effects on normal cells.Inflammation 1994; 18: 151–161.

    Article  PubMed  CAS  Google Scholar 

  34. Sakaguchi S, Kanda N, Hsu C, Sakaguchi O. Lipid peroxide formation and membrane damage in endotoxemia poisoned mice.Microbiol Immunol 1981; 25: 229–244.

    PubMed  CAS  Google Scholar 

  35. Miller NJ, Rice Evans C, Davies MJ, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates.Clin Sci 1993; 84: 407–412.

    PubMed  CAS  Google Scholar 

  36. Cao GH, Alessio HM, Cutler RG. Oxygen radical absorbance capacity assay for antioxidants.Free Radical Biol & Med 1993; 14: 303–311.

    Article  CAS  Google Scholar 

  37. Frei B, Stocker R, Ames BN. Antioxidant defenses and lipid peroxidation in human blood plasma.Proc Natl Acad Sci USA 1988; 85: 9748–9752.

    Article  PubMed  CAS  Google Scholar 

  38. Stocker R, Yamamoto Y, Mc Donagh AF, Glazer A, Ames B. Bilirubin is an antioxidant of possible physiological importance.Science 1987; 235: 1043–1046.

    Article  PubMed  CAS  Google Scholar 

  39. Richard C, Lemmonier F, Thibault M, Couturier M, Auzepy P. Vitamin E deficiency and lipoperoxidation during adult respiratory distress syndrome.Crit Care Med 1990; 18: 4–9.

    Article  PubMed  CAS  Google Scholar 

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Peralta, J., Reides, C., García, S. et al. Oxidative stress in rodent closed duodenal loop pancreatitis. Int J Pancreatol 19, 61–69 (1996). https://doi.org/10.1007/BF02788377

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