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. 1995;3(2):149–168. doi: 10.1007/BF02674919

The pathogenesis of inflammatory disease: Surgical shock and multiple system organ failure

A Parke 1, D V Parke 2,
PMCID: PMC7101736

Abstract

Chronic inflammatory disease, embracing rheumatoid arthritis (RA), inflammatory bowel disease (IBD), hepatitis, asthma, atherosclerosis, multiple system organ failure (MSOF), etc., is mediated by reactive oxygen species (ROS). These ROS originate from activated neutrophils in infections and in immune and autoimmune reactions, from tissue deposits of ferritin, and from futile cycling of cytochrome P450 (CYP) following exposure to persistent chemicals, and may be perpetuated by the actions of complement, cytokines and eicosanoids. Acute inflammation is normally arrested by removal of ROS by tissue glutathione (GSH) and the antioxidant vitamins, A, C and E, all of which are regenerated by NADH and NADPH. Failure of this antioxidant defence system can lead to oxidative stress and to chronic inflammatory disease, including surgical shock and MSOF. The roles of oxidative stress and microcirculatory arrest in promoting MSOF, and of GSH, the antioxidant defence system, and fibronectin in preventing this, are reviewed in the light of recent experimental studies of surgical shock, including fasting, anaesthesia, hepatic ischaemia and reperfusion.

Keywords: chronic inflammatory disease, surgical shock, oxygen radicals, multiple system organ failure, rheumatoid arthritis, glutathione, leucocytes, cytokines, cytochromes P450 and toxic chemicals, eicosanoids, fibronectin and microcirculatory arrest, complement

References

  • 1.Winrow VR, Winyard PG, Morris CJ, Blake DR. Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull. 1993;49:506–22. doi: 10.1093/oxfordjournals.bmb.a072627. [DOI] [PubMed] [Google Scholar]
  • 2.Welbourn CRB, Young Y. Endotoxin, septic shock and acute lung injury: neutrophils, macrophages and inflammatory mediators. Br J Surg. 1992;79:998–1003. doi: 10.1002/bjs.1800791006. [DOI] [PubMed] [Google Scholar]
  • 3.Parke AL, Ioannides C, Lewis DFV, Parke DV. Molecular pathology of drug-disease interactions in chronic autoimmune inflammatory diseases. Inflammopharmacology. 1991;1:3–36. [Google Scholar]
  • 4.Babbs CF. Oxygen radicals in ulcerative colitis. Free Rad Biol Med. 1992;13:169–81. doi: 10.1016/0891-5849(92)90079-V. [DOI] [PubMed] [Google Scholar]
  • 5.Trush MA, Kensler TW. An overview of the relationship between oxidative stress and chemical carcinogenesis. Free Rad Biol Med. 1991;10:201–9. doi: 10.1016/0891-5849(91)90077-G. [DOI] [PubMed] [Google Scholar]
  • 6.Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants and the degenerative diseases of aging. Proc Natl Acad Sci USA. 1993;90:7915–22. doi: 10.1073/pnas.90.17.7915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Witz G. Active oxygen species as factors in multistage carcinogenesis. Proc Soc Exptl Biol Med. 1991;198:675–82. doi: 10.3181/00379727-198-43306. [DOI] [PubMed] [Google Scholar]
  • 8.Piotrowski JJ, Hunter GC, Eskelson CD, Dubick MA, Bernhard VM. Evidence for lipid peroxidation in atherosclerosis. Life Sci. 1990;46:715–21. doi: 10.1016/0024-3205(90)90077-5. [DOI] [PubMed] [Google Scholar]
  • 9.Halliwell B. Free radicals and antioxidants: A personal view. Nutr Rev. 1994;52:253–65. doi: 10.1111/j.1753-4887.1994.tb01453.x. [DOI] [PubMed] [Google Scholar]
  • 10.Elliot RH, Strunin L. Hepatotoxicity of volatile anaesthetics. Br J Anaesth. 1993;70:339–49. doi: 10.1093/bja/70.3.339. [DOI] [PubMed] [Google Scholar]
  • 11.Evans PH. Free radicals in brain metabolism and pathology. Br Med Bull. 1993;49:577–87. doi: 10.1093/oxfordjournals.bmb.a072632. [DOI] [PubMed] [Google Scholar]
  • 12.Baruchel S, Wainberg MA. The role of oxidative stress in disease progression in individuals infected by the human immunodeficiency virus. J Leuk Biol. 1992;52:111–14. doi: 10.1002/jlb.52.1.111. [DOI] [PubMed] [Google Scholar]
  • 13.Marshall JC, Cristou NV, Meakins JL. The gastrointestinal tract. The undrained absess of multiple organ failure. Ann Surg. 1993;218:111–19. doi: 10.1097/00000658-199308000-00001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Fry DE. Multiple system organ failure. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 3–14. [Google Scholar]
  • 15.McLean JS, Byrick RJ. ARDS and sepsis — definitions and new therapy. Can J Anaesth. 1993;40:585–90. doi: 10.1007/BF03009692. [DOI] [PubMed] [Google Scholar]
  • 16.Babior BM. Oxygen dependent microbial killing by phagocytes. N Engl J Med. 1978;298:659–68. doi: 10.1056/NEJM197803232981205. [DOI] [PubMed] [Google Scholar]
  • 17.Clevenger FW, Fry DE. Complement. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 167–77. [Google Scholar]
  • 18.Reines HD, Cook JA. Prostaglandins. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 123–41. [Google Scholar]
  • 19.Liu PT, Ioannides C, Symons AM, Parke DV. Role of tissue glutathione in prevention of surgical trauma. Xenobiotica. 1993;23:899–911. doi: 10.3109/00498259309059417. [DOI] [PubMed] [Google Scholar]
  • 20.Liu PT, Symons AM, Howarth JA, Boulter PS, Parke DV. Studies in surgical trauma: oxidative stress in ischaemia-reperfusion of rat liver. Clin Sci. 1994;86:453–60. doi: 10.1042/cs0860453. [DOI] [PubMed] [Google Scholar]
  • 21.Parke DV, Ioannides C. The effects of nutrition on chemical toxicity. Drug Metab Rev. 1994;26:739–65. doi: 10.3109/03602539408998325. [DOI] [PubMed] [Google Scholar]
  • 22.Sussman MS, Schiller HJ, Buchman TG, Bulkley GB. Oxygen free radicals. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 143–65. [Google Scholar]
  • 23.Bagchi M, Hassoun EA, Bagchi D, Stohs SJ. Production of reactive oxygen species by peritoneal macrophages and hepatic mitochondria and microsomes from endrin-treated rats. Free Rad Biol Med. 1993;14:149–55. doi: 10.1016/0891-5849(93)90005-F. [DOI] [PubMed] [Google Scholar]
  • 24.Kukielka E, Cederbaum AI. DNA strand cleavage as a sensitive assay for the production of hydroxyl radicals: role of cytochrome P4502E1 in the increased activity after ethanol treatment. Biochem J. 1994;302:773–9. doi: 10.1042/bj3020773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Parke DV. The cytochromes P450 and mechanisms of chemical carcinogenesis. Environ Health Persp. 1994;102:852–3. doi: 10.2307/3432116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Myers SI, Hernandez R. Role of oxygen-derived free radicals on rat splanchnic eicosanoid production during acute haemorrhage. Prostaglandins. 1992;44:25–36. doi: 10.1016/0090-6980(92)90104-2. [DOI] [PubMed] [Google Scholar]
  • 27.Parke DV. The importance of diet and nutrition in the detoxication of chemicals. In: Parke DV, Ioannides C, Walker R, editors. Food nutrition and chemical toxicity. London: Smith-Gordon; 1993. pp. 1–15. [Google Scholar]
  • 28.Palozza P, Krinsky NI. β-Carotene and α-tocopherol are synergistic antioxidants. Arch Biochem Biophys. 1992;297:184–7. doi: 10.1016/0003-9861(92)90658-J. [DOI] [PubMed] [Google Scholar]
  • 29.Yoshioka A, Miyachi Y, Imamura S, Niwa Y. Anti-oxidant effects of retinoids on inflammatory skin diseases. Arch Dermatol Res. 1986;278:177–83. doi: 10.1007/BF00412920. [DOI] [PubMed] [Google Scholar]
  • 30.Trenam CW, Winyard PG, Morris CJ, Blake DR. Iron-promoted oxidative damage in rheumatic diseases. In: Lauffer VB, editor. Iron and human disease. Boca Raton: CRC Press; 1992. pp. 395–417. [Google Scholar]
  • 31.Vallance P, Moncada S. Nitric oxide — from mediator to medicines. J R Coll Phys (Lond) 1994;28:209–19. [PMC free article] [PubMed] [Google Scholar]
  • 32.Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: Physiology, pathophysiology and pharmacology. Pharmac Rev. 1991;43:109–42. [PubMed] [Google Scholar]
  • 33.Adams DH. Leucocyte adhesion molecules and alcoholic liver disease. Alcohol Alcoholism. 1994;29:249–60. [PubMed] [Google Scholar]
  • 34.McGiff JC. Cytochrome P450 metabolism of arachidonic acid. Ann Rev Pharmac Toxicol. 1991;31:339–69. doi: 10.1146/annurev.pa.31.040191.002011. [DOI] [PubMed] [Google Scholar]
  • 35.Schirmer WJ, Fry DE. Microcirculatory arrest. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 73–85. [Google Scholar]
  • 36.Pellicane JV, De Maria EJ, Abd-Elfattah A, Reines HD, Vannice JL, Carson KW. Interleukin-1 receptor antagonist improves survival and preserves organ adenosine-5′-triphosphate after haemorrhagic shock. Surgery. 1993;114:278–84. [PubMed] [Google Scholar]
  • 37.Kracht M, Shiroo M, Marshall CJ, Hsuan JJ, Saklatvala J. Interleukin-1 activates a novel protein kinase that phosphorylates the epidermal-growth-factor receptor peptide T669. Biochem J. 1994;302:897–905. doi: 10.1042/bj3020897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Ala Y, Palluy O, Favero J, Bonne C, Modat G, Dornand J. Hypoxia/reoxygenation stimulates endothelial cells to promote interleukin-1 and interleukin-6 production. Effects of free radical scavengers. Agents Actions. 1992;37:134–9. doi: 10.1007/BF01987902. [DOI] [PubMed] [Google Scholar]
  • 39.Graeve L, Baumann M, Heinrich PC. Interleukin-6 in autoimmune diseases. Clin Invest. 1993;71:664–71. doi: 10.1007/BF00184499. [DOI] [PubMed] [Google Scholar]
  • 40.Hall GM, Desborough JP. Interleukin-6 and the metabolic response to surgery. Br J Anaesth. 1992;69:337–8. doi: 10.1093/bja/69.4.337-a. [DOI] [PubMed] [Google Scholar]
  • 41.Edwards MJ, Miller FN, Sims DE, Abney DL, Schuschke DA, Corey TS. Interleukin-2 acutely induces platelet and neutrophil-endothelial adherence and macromolecular leakage. Cancer Res. 1992;52:3425–31. [PubMed] [Google Scholar]
  • 42.Kurokohchi K, Matsuo Y, Yoneyama H, Nishioka M, Ichikawa Y. Interleukin 2 induction of cytochrome P450-linked monooxygenase systems of rat liver microsomes. Biochem Pharmacol. 1993;45:585–92. doi: 10.1016/0006-2952(93)90131-F. [DOI] [PubMed] [Google Scholar]
  • 43.Kay AB. T cells, cytokines and asthma. J R Coll Phys (Lond) 1994;28:325–31. [PMC free article] [PubMed] [Google Scholar]
  • 44.Rainsford KD. Diet, eicosanoids and chemical toxicity. In: Parke DV, Ioannides C, Walker R, editors. Food, nutrition and chemical toxicity. London: Smith-Gordon; 1993. pp. 171–80. [Google Scholar]
  • 45.Gonzalez FJ, Nebert DW. Evolution of the P450 gene superfamily. Trends Genet. 1990;6:182–6. doi: 10.1016/0168-9525(90)90174-5. [DOI] [PubMed] [Google Scholar]
  • 46.Parke DV, Ioannides C, Lewis DFV. The role of cytochromes P450 in the detoxication and activation of drugs and other chemicals. Can J Physiol Pharmacol. 1991;69:537–49. doi: 10.1139/y91-081. [DOI] [PubMed] [Google Scholar]
  • 47.Ioannides C, Parke DV. The cytochrome P4501 gene family of microsomal haemoproteins and their role in the metabolic activation of chemicals. Drug Metab Rev. 1990;22:1–86. doi: 10.3109/03602539008991444. [DOI] [PubMed] [Google Scholar]
  • 48.Manns MP, Griffin KJ, Quattorchi LC, et al. Identification of cytochrome P4501 A2 as a human autoantigen. Arch Biochem Biophys. 1990;280:229–32. doi: 10.1016/0003-9861(90)90541-6. [DOI] [PubMed] [Google Scholar]
  • 49.Kushimoto K, Nagasawa K, Udea A, et al. Liver abnormalities and liver membrane autoantibodies in systemic lupus erythematosus. Ann Rheum Dis. 1989;48:946–52. doi: 10.1136/ard.48.11.946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Neuberger J, Williams R. Immune mechanisms in tienilic acid associated hepatotoxicity. Gut. 1989;30:515–19. doi: 10.1136/gut.30.4.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.De Leve LD, Kaplowitz N. Glutathione metabolism and its role in hepatotoxicity. Pharmac Ther. 1991;52:287–305. doi: 10.1016/0163-7258(91)90029-L. [DOI] [PubMed] [Google Scholar]
  • 52.Robinson MK, Rodrick ML, Jacobs DO, et al. Glutathione depletion in rats impairs T-cell and macrophage immune function. Arch Surg. 1993;128:29–35. doi: 10.1001/archsurg.1993.01420130033006. [DOI] [PubMed] [Google Scholar]
  • 53.Esposito F, Agosti V, Morrone G, et al. Inhibition of the differentiation of human myeloid cell lines by redox changes through glutathione depletion. Biochem J. 1994;301:649–53. doi: 10.1042/bj3010649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Kilbourne EM, Rigau-Perez JG, Heath CWJ. Clinical epidemiology of toxic oil syndrome: manifestations of a new illness. N Engl J Med. 1983;309:1408–14. doi: 10.1056/NEJM198312083092302. [DOI] [PubMed] [Google Scholar]
  • 55.Posada de la Paz M, Philen RM, Borda IA. Manufacturing processes at two French rapeseed oil companies: possible relationship to toxic oil syndrome in Spain. Food Chem Toxicol. 1991;29:797–803. doi: 10.1016/0278-6915(91)90105-G. [DOI] [PubMed] [Google Scholar]
  • 56.Kilbourne E, Bernet JTJ, Posada de la Paz M. Chemical correlates of pathogenicity of oils related to the toxic oil syndrome epidemic in Spain. Am J Epidemiol. 1988;127:1210–27. doi: 10.1093/oxfordjournals.aje.a114914. [DOI] [PubMed] [Google Scholar]
  • 57.Tabuenca JM. Toxic-allergic syndrome caused by the ingestion of rapeseed oil denatured with aniline. Lancet. 1981;2:567–8. doi: 10.1016/s0140-6736(81)90949-1. [DOI] [PubMed] [Google Scholar]
  • 58.Pestana A, Munoz E. Anilides and the Spanish toxic oil syndrome. Nature. 1982;298:608–608. doi: 10.1038/298608a0. [DOI] [PubMed] [Google Scholar]
  • 59.Maneta-Peyret L, Picard J-P, Bezian J-H, Cassagne C. Fatty acids rendered immunogenic. Immunol Lett. 1992;31:227–31. doi: 10.1016/0165-2478(92)90118-8. [DOI] [PubMed] [Google Scholar]
  • 60.Kaufman LD, Seidman RJ. L-Tryptophan-associated eosinophilia-myalgia syndrome: perspective of a new illness. Rheum Dis Clin N Am. 1991;17:427–41. [PubMed] [Google Scholar]
  • 61.Katz JD, Wakem CJ, Parke AL. L-Tryptophan associated eosinophilia myalgia syndrome. J Rheumatol. 1990;17:1559–61. [PubMed] [Google Scholar]
  • 62.Mayeno AN, Lin F, Foote CS. Characterisation of ‘peak E’ a novel amino acid with the eosinophilia-myalgia syndrome. Science. 1990;250:1707–8. doi: 10.1126/science.2270484. [DOI] [PubMed] [Google Scholar]
  • 63.Dröge W. Cysteine and glutathione deficiency in AIDS patients: a rationale for treatment withN-acetylcysteine. Pharmacology. 1983;46:61–5. doi: 10.1159/000139029. [DOI] [PubMed] [Google Scholar]
  • 64.Haverkos HW, Kopstein AN, Wilson H, Drotman P. Nitrite inhalants: history, epidemiology, and possible links to AIDS. Envir Health Persp. 1994;102:858–61. doi: 10.2307/3432118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Newell GR, Adams SC, Mansell PWA, Hersh EM. Toxicity, immunosuppressive effects and carcinogenic potential of volatile nitrites: possible relationship to Karposi’s syndrome. Pharmacotherapy. 1984;4:284–91. doi: 10.1002/j.1875-9114.1984.tb03376.x. [DOI] [PubMed] [Google Scholar]
  • 66.Meloche BA, O’Brien PJ. S-Nitrosylglutathione-mediated hepatocyte toxicity. Xenobiotica. 1993;23:863–71. doi: 10.3109/00498259309059414. [DOI] [PubMed] [Google Scholar]
  • 67.Buettner GR. The pecking order of free radicals and antioxidants: Lipid peroxidation, α-tocopherol, and ascorbate. Arch Biochem Biophys. 1993;300:535–43. doi: 10.1006/abbi.1993.1074. [DOI] [PubMed] [Google Scholar]
  • 68.Chow CK. Vitamin E and oxidative stress. Free Rad Biol Med. 1991;11:215–32. doi: 10.1016/0891-5849(91)90174-2. [DOI] [PubMed] [Google Scholar]
  • 69.Munday R, Winterbourn CC. Reduced glutathione in combination with superoxide dismutase as an important biological antioxidant defence mechanism. Biochem Pharmacol. 1989;38:4349–52. doi: 10.1016/0006-2952(89)90641-2. [DOI] [PubMed] [Google Scholar]
  • 70.Diplock AT. Low dietary selenium and its relationship to human disease. In: Parke DV, Ioannides C, Walker R, editors. Food, nutrition and chemical toxicity. London: Smith-Gordon; 1993. pp. 395–402. [Google Scholar]
  • 71.Saba TM, Fortune JB, Wallace JR. Microaggregation hypothesis of multiple system organ failure. In: Fry DE, editor. Multiple system organ failure. St Louis: Mosby Year Book; 1992. pp. 25–41. [Google Scholar]
  • 72.Preece NE, Hall DE, Howarth JA, King LJ, Parke DV. Effects of acute and sub-chronic administration of iron nitrilotriacetate in the rat. Toxicology. 1989;59:37–58. doi: 10.1016/0300-483X(89)90155-8. [DOI] [PubMed] [Google Scholar]
  • 73.Liu PT, Symons AM, Parke DV. Autoxidative injury with loss of cytochrome P-450 following acute exposure of rats to fasting and ether anaesthesia. Xenobiotica. 1991;21:205–15. doi: 10.3109/00498259109039462. [DOI] [PubMed] [Google Scholar]
  • 74.Liu PT, Symons AM, Parke DV. The effects of fasting and ether anaesthesia on hepatic and renal function in surgical trauma. In: Parke DV, Ioannides C, Walker R, editors. Food, nutrition and chemical toxicity. London: Smith-Gordon; 1993. pp. 385–94. [Google Scholar]
  • 75.Liu PT, Ioannides C, Shavilla J, Symons AM, Parke DV. Effects of ether anaesthesia and fasting on various cytochromes P450 of rat liver and kidney. Biochem Pharmacol. 1993;45:871–7. doi: 10.1016/0006-2952(93)90171-R. [DOI] [PubMed] [Google Scholar]
  • 76.Liu PT, Kentish PA, Symons AM, Parke DV. The effects of ether anaesthesia on oxidative stress in rats - dose response. Toxicology. 1993;80:37–49. doi: 10.1016/0300-483X(93)90075-4. [DOI] [PubMed] [Google Scholar]
  • 77.Babcock WW, editor. Principles and practice of surgery. Philadelphia: Lea and Febiger; 1994. pp. 5–55. [Google Scholar]
  • 78.Bourne W. Anaesthetics and liver function. Am J Surg. 1936;34:486–92. doi: 10.1016/S0002-9610(36)90671-2. [DOI] [Google Scholar]
  • 79.Lewis DFV, Ioannides C, Parke DV. Molecular orbital studies of oxygen activation and mechanisms of cytochrome P450-mediated oxidative metabolism of xenobiotics. Chem Biol Interact. 1989;70:263–80. doi: 10.1016/0009-2797(89)90049-5. [DOI] [PubMed] [Google Scholar]

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