The autodigestion hypothesis for shock and multi-organ failure

Annals of Biomedical Engineering

Volumn 42, Issue 2, 2014, Pages 405-414

  Schmid Schönbein, Geert W ^a   Chang, Marisol ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Epithelium; Inflammation; Mucin; Pancreatic digestive enzymes; Sepsis; Trypsin; Unbound free fatty acids

Indexed keywords

PATHOLOGY;

DIGESTIVE ENZYMES; EPITHELIUM; FREE FATTY ACID; INFLAMMATION; MUCIN; SEPSIS; TRYPSIN;

ENZYMES;

INTERLEUKIN 1; MUCIN; PANCREAS ENZYME; TRYPSIN; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC REACTION; AUTODIGESTION; BLEEDING; BLOOD VOLUME; CAUSE OF DEATH; CELL ADHESION; CHRONIC INFLAMMATION; CONFERENCE PAPER; CYTOKINE RELEASE; CYTOTOXICITY; DIGESTION; ENZYME ACTIVITY; FOOD INTAKE; HEMORRHAGIC SHOCK; HUMAN; INFECTION; INJURY; INTENSIVE CARE UNIT; INTESTINE MOTILITY; LEUKOCYTE ACTIVATION; MEAN ARTERIAL PRESSURE; MEMBRANE TRANSPORT; MULTIPLE ORGAN FAILURE; PRIORITY JOURNAL; SHOCK; SURVIVAL RATE; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TEMPERATURE; WEIGHT GAIN;

ANIMALS; HUMANS; INFLAMMATION MEDIATORS; INTESTINAL MUCOSA; MULTIPLE ORGAN FAILURE; PANCREAS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84899464541     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-013-0891-6     Document Type: Conference Paper

References (59)

1. Altshuler, A. E., M. J. Morgan, S. Chien, and G. W. Schmid-Schönbein. Proteolytic activity attenuates the response of endothelial cells to fluid shear stress. Cell. Mol. Bioeng. 5:82-91, 2012.
2. Altshuler, A. E., A. H. Penn, J. A. Yang, G. R. Kim, and G. W. Schmid-Schönbein. Protease activity increases in plasma, peritoneal fluid, and vital organs after hemorrhagic shock in rats. PLoS ONE 7:e32672, 2012.
3. Arndt, H., C. W. Smith, and D. N. Granger. Leukocyteendothelial cell adhesion in spontaneously hypertensive and normotensive rats. Hypertension 21:667-673, 1993.
4. Bacsy, E., Z. Nagy, and M. Papp. Intra-acinar lipolysis, an early sign of intravital pancreatic autodigestion. Acta Med. Acad. Sci. Hung 27:331-335, 1970.
5. Barroso-Aranda, J., and G. W. Schmid-Schonbein. Transformation of neutrophils as indicator of irreversibility in hemorrhagic shock. Am. J. Physiol. 257:H846-H852, 1989.
6. Barroso-Aranda, J., B. W. Zweifach, J. C. Mathison, and G. W. Schmid-Schönbein. Neutrophil activation, tumor necrosis factor, and survival after endotoxic and hemorrhagic shock. J. Cardiovasc. Pharmacol. 25(Suppl 2):S23-S29, 1995.
7. Chang, M. Mucin Disruption and Transport of Digestive Enzymes in Early Stages of Intestinal Ischemia. Ph. D. Thesis, University of California San Diego, 2012.
8. Chang, M., T. Alsaigh, E. B. Kistler, and G. W. Schmid-Schönbein. Breakdown of mucin as barrier to digestive enzymes in the ischemic rat small intestine. PLoS ONE 7:e40087, 2012.
9. Chang, M., E. B. Kistler, and G. W. Schmid-Schönbein. Disruption of the mucosal barrier during gut ischemia allows entry of digestive enzymes into the intestinal wall. Shock 37:297-305, 2012.
10. Chen, A. Y., F. A. DeLano, S. R. Valdez, J. N. Ha, H. Y. Shin, and G. W. Schmid-Schönbein. Receptor cleavage reduces the fluid shear response in neutrophils of the spontaneously hypertensive rat. Am. J. Physiol. Cell Physiol. 299:C1441-C1449, 2010.
11. Chen, A. Y., J. N. Ha, F. A. Delano, and G. W. Schmid-Schonbein. Receptor cleavage and P-selectin-dependent reduction of leukocyte adhesion in the spontaneously hypertensive rat. J. Leukoc. Biol. 299:C1441-C1449, 2012.
12. Deitch, E. A., H. P. Shi, Q. Lu, E. Feketeova, and D. Z. Xu. Serine proteases are involved in the pathogenesis of trauma-hemorrhagic shock-induced gut and lung injury. Shock 19:452-456, 2003.
13. Del Sorbo, L., and A. S. Slutsky. Acute respiratory distress syndrome and multiple organ failure. Curr. Opin. Crit. Care 17:1-6, 2011.
14. Delano, F. A., D. B. Hoyt and G. W. Schmid-Schonbein. Pancreatic digestive enzyme blockade in the intestine increases survival after experimental shock. Sci. Transl. Med. 5:169ra11, 2013.
15. DeLano, F. A., and G. W. Schmid-Schönbein. Proteinase activity and receptor cleavage: mechanism for insulin resistance in the spontaneously hypertensive rat. Hypertension 52:415-423, 2008.
16. Dinarello, C. A. Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 112:321S-329S, 1997.
17. Doucet, J. J., D. B. Hoyt, R. Coimbra, G. W. Schmid-Schonbein, W. G. Junger, L. W. Paul, W. H. Loomis, and T. E. Hugli. Inhibition of enteral enzymes by enteroclysis with nafamostat mesilate reduces neutrophil activation and transfusion requirements after hemorrhagic shock. J. Trauma 56:501-510, 2004; discussion 510-511.
18. Fitzal, F., F. A. Delano, C. Young, H. S. Rosario, W. G. Junger, and G. W. Schmid-Schonbein. Pancreatic enzymes sustain systemic inflammation after an initial endotoxin challenge. Surgery 134:446-456, 2003.
19. Fitzal, F., F. A. DeLano, C. Young, H. S. Rosario, and G. W. Schmid-Schonbein. Pancreatic protease inhibition during shock attenuates cell activation and peripheral inflammation. J. Vasc. Res. 39:320-329, 2002.
20. Fitzal, F., F. A. DeLano, C. Young, and G. W. Schmid-Schonbein. Improvement in early symptoms of shock by delayed intestinal protease inhibition. Arch. Surg. 139:1008-1016, 2004.
21. Hanson, P. J., A. P. Moran, and K. Butler. Paracellular permeability is increased by basal lipopolysaccharide in a primary culture of colonic epithelial cells; an effect prevented by an activator of Toll-like receptor-2. Innate Immun. 17:269-282, 2011.
22. Herold, S., K. Mayer, and J. Lohmeyer. Acute lung injury: how macrophages orchestrate resolution of inflammation and tissue repair. Front. Immunol. 2:65, 2011.
23. Ishimaru, K., H. Mitsuoka, N. Unno, K. Inuzuka, S. Nakamura, and G. W. Schmid-Schonbein. Pancreatic proteases and inflammatory mediators in peritoneal fluid during splanchnic arterial occlusion and reperfusion. Shock 22:467-471, 2004.
24. Kim, H. D., D. J. Malinoski, B. Borazjani, M. S. Patel, J. Chen, J. Slone, X. M. Nguyen, E. Steward, G. W. Schmid-Schonbein, and D. B. Hoyt. Inhibition of intraluminal pancreatic enzymes with nafamostat mesilate improves clinical outcomes after hemorrhagic shock in swine. J. Trauma 68:1078-1083, 2010.
25. Kistler, E. B., T. Alsaigh, M. Chang, and G. W. Schmid-Schonbein. Impaired small-bowel barrier integrity in the presence of lumenal pancreatic digestive enzymes leads to circulatory shock. Shock 38:262-267, 2012.
26. Kistler, E. B., T. E. Hugli, and G. W. Schmid-Schönbein. The pancreas as a source of cardiovascular cell activating factors. Microcirculation 7:183-192, 2000.
27. Kistler, E. B., A. M. Lefer, T. E. Hugli, and G. W. Schmid-Schonbein. Plasma activation during splanchnic arterial occlusion shock. Shock 14:30-34, 2000.
28. Koenig, W., M. Sund, M. Frohlich, H. G. Fischer, H. Lowel, A. Doring, W. L. Hutchinson, and M. B. Pepys. C-Reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation 99:237-242, 1999.
29. Kollias, G., E. Douni, G. Kassiotis, and D. Kontoyiannis. The function of tumour necrosis factor and receptors in models of multi-organ inflammation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann. Rheum. Dis. 58(Suppl 1):132-139, 1999.
30. Lee, Y. T., J. Wei, Y. C. Chuang, C. Y. Chang, I. C. Chen, C. F. Weng, and G. W. Schmid-Schönbein. Successful treatment with continuous enteral protease inhibitor in a patient with severe septic shock. Transpl. Proc. 44:817-819, 2012.
31. Lefer, A. M., and Y. Barenholz. Pancreatic hydrolases and the formation of a myocardial depressant factor in shock. Am. J. Physiol. 223:1103-1109, 1972.
32. Lefkowitz, R. B., G. W. Schmid-Schönbein, and M. J. Heller. Whole blood assay for elastase, chymotrypsin, matrix metalloproteinase-2, and matrix metalloproteinase-9 activity. Anal. Chem. 82:8251-8258, 2010.
33. Li, L., and J. L. Messina. Acute insulin resistance following injury. Trends Endocrinol. Metab. 20:429-435, 2009.
34. Libby, P. Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr. Rev. 65:S140-S146, 2007.
35. Lichtenberger, L. M. The hydrophobic barrier properties of gastrointestinal mucus. Annu. Rev. Physiol. 57:565-583, 1995.
36. Marti-Carvajal, A., G. Salanti, and A. F. Cardona. Human recombinant activated protein C for severe sepsis. Cochrane Database Syst. Rev. CD004388, 2008.
37. Matthews, J. B., J. A. Smith, K. J. Tally, M. J. Menconi, H. Nguyen, and M. P. Fink. Chemical hypoxia increases junctional permeability and activates electrogenic ion transport in human intestinal epithelial monolayers. Surgery 116:150-157, 1994; discussion 157-158.
38. Mitsuoka, H., E. B. Kistler, and G. W. Schmid-Schonbein. Generation of in vivo activating factors in the ischemic intestine by pancreatic enzymes. Proc. Natl. Acad. Sci. U. S. A. 97:1772-1777, 2000.
39. Mitsuoka, H., E. B. Kistler, and G. W. Schmid-Schonbein. Protease inhibition in the intestinal lumen: attenuation of systemic inflammation and early indicators of multiple organ failure in shock. Shock 17:205-209, 2002.
40. Mitsuoka, H., and G. W. Schmid-Schönbein. Mechanisms for blockade of in vivo activator production in the ischemic intestine and multi-organ failure. Shock 14:522-527, 2000.
41. Nagai, H., H. Henrich, P. H. Wunsch, W. Fischbach, and J. Mossner. Role of pancreatic enzymes and their substrates in autodigestion of the pancreas. In vitro studies with isolated rat pancreatic acini. Gastroenterology 96:838-847, 1989.
42. Penn, A. H., A. E. Altshuler, J. W. Small, S. F. Taylor, K. R. Dobkins, and G. W. Schmid-Schönbein. Digested formula but not digested fresh human milk causes death of intestinal cells in vitro: implications for necrotizing enterocolitis. Pediatr. Res. 72:560-567, 2012.
43. Penn, A. H., T. E. Hugli, and G. W. Schmid-Schonbein. Pancreatic enzymes generate cytotoxic mediators in the intestine. Shock 27:296-304, 2007.
44. Penn, A. H., and G. W. Schmid-Schönbein. The intestine as source of cytotoxic mediators in shock: free fatty acids and degradation of lipid-binding proteins. Am. J. Physiol. Heart Circ. Physiol. 294:H1779-H1792, 2008.
45. Raman, K., M. Chong, G. G. Akhtar-Danesh, M. D'Mello, R. Hasso, S. Ross, F. Xu, and G. Pare. Genetic markers of inflammation and their role in cardiovascular disease. Can. J. Cardiol. 29:67-74, 2013.
46. Redd, M. J., L. Cooper, W. Wood, B. Stramer, and P. Martin. Wound healing and inflammation: embryos reveal the way to perfect repair. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359:777-784, 2004.
47. Richter, M. D. Protease activity in mesenteric lymph following splanchnic arterial occlusion. UC San Diego, M. S. Thesis, 2012.
48. Rivers, E., B. Nguyen, S. Havstad, J. Ressler, A. Muzzin, B. Knoblich, E. Peterson, and M. Tomlanovich. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N. Engl. J. Med. 345:1368-1377, 2001.
49. Rodrigues, S. F., E. D. Tran, Z. B. Fortes, and G. W. Schmid-Schonbein. Matrix metalloproteinases cleave the beta2-adrenergic receptor in spontaneously hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 299:H25-H35, 2010.
50. Schmid-Schonbein, G. W. Analysis of inflammation. Annu. Rev. Biomed. Eng. 8:93-131, 2006.
51. Tonelli, M., F. Sacks, M. Pfeffer, G. S. Jhangri, and G. Curhan. Biomarkers of inflammation and progression of chronic kidney disease. Kidney Int. 68:237-245, 2005.
52. Tong, S., H. J. Neboori, E. D. Tran, and G. W. Schmid-Schonbein. Constitutive expression and enzymatic cleavage of ICAM-1 in the spontaneously hypertensive rat. J. Vasc. Res. 48:386-396, 2011.
53. Tran, E. D., F. A. DeLano, and G. W. Schmid-Schonbein. Enhanced matrix metalloproteinase activity in the spontaneously hypertensive rat: VEGFR-2 cleavage, endothelial apoptosis, and capillary rarefaction. J. Vasc. Res. 47:423-431, 2010.
54. Tran, E. D., M. Yang, A. Chen, F. A. Delano, W. L. Murfee, and G. W. Schmid-Schönbein. Matrix metalloproteinase activity causes VEGFR-2 cleavage and microvascular rarefaction in rat mesentery. Microcirculation 18:228-237, 2011.
55. Valdez, S. R. Serotonin 5HT-1A Receptor Density in the Brain of the Spontaneously Hypertensive Rats. San Diego, MS: Univ. Calif, 2010.
56. Waldo, S. W., H. S. Rosario, A. H. Penn, and G. W. Schmid-Schonbein. Pancreatic digestive enzymes are potent generators of mediators for leukocyte activation and mortality. Shock 20:138-143, 2003.
57. Weidenbusch, M., and H. J. Anders. Tissue microenvironments define and get reinforced by macrophage phenotypes in homeostasis or during inflammation, repair and fibrosis. J. Innate Immun. 4:463-477, 2012.
58. Westergaard, H., and J. M. Dietschy. Delineation of the dimensions and permeability characteristics of the two major diffusion barriers to passive mucosal uptake in the rabbit intestine. J. Clin. Invest. 54:718-732, 1974.
59. Zweifach, B. W. Hemorrhagic shock in germ-free rats. Ann. N. Y. Acad. Sci. 78:315-319, 1959.