European Journal of Internal Medicine
Volume 20, Issue 8 , Pages 739-743 , December 2009

Lessons from acute pancreatitis-induced thrombotic thrombocytopenic purpura

  • Jecko Thachil

      Affiliations

    • Corresponding Author InformationTel.: +44 151 706 4322; fax: +44 151 706 5810.

Received 8 June 2009 ,Revised 9 September 2009 ,Accepted 10 September 2009.

References 

  1. George JN. Clinical practice. Thrombotic thrombocytopenic purpura. N Engl J Med. 2006;354:1927–1935
  2. Vesely SK, George JN, Lammle B, Studt JD, Alberio L, El-Harake MA, et al. ADAMTS13 activity in thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: relation to presenting features and clinical outcomes in a prospective cohort of 142 patients. Blood. 2003;102:60–68
  3. Sadler JE. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood. 2008;112:11–18
  4. Swisher KK, Doan JT, Vesely SK, Kwaan HC, Kim B, Lämmle B, et al. Pancreatitis preceding acute episodes of thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: report of five patients with a systematic review of published reports. Haematologica. 2007;92:936–943
  5. McDonald V, Laffan M, Benjamin S, Bevan D, Machin S, Scully MA. Thrombotic thrombocytopenic purpura precipitated by acute pancreatitis: a report of seven cases from a regional UK TTP registry. Br J Haematol. 2009;144:430–433
  6. Piton G, Navellou JC, Morati P, Patry C, Carbonnel F, Capellier G. Thrombotic thrombocytopenic purpura associated with severe acute pancreatitis in a context of decreased ADAMTS-13 activity: a case report. Eur J Gastroenterol Hepatol. 2008;20:1226–1230
  7. Banno F, Kokame K, Okuda T, Honda S, Miyata S, Kato H, et al. Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura. Blood. 2006;107:3161–3166
  8. Moore JC, Hayward CP, Warkentin TE, Kelton JG. Decreased von Willebrand factor protease activity associated with thrombocytopenic disorders. Blood. 2001;98:1842–1846
  9. Mannucci PM, Canciani MT, Forza I, Lussana F, Lattuada A, Rossi E. Changes in health and disease of the metalloprotease that cleaves von Willebrand factor. Blood. 2001;98:2730–2735
  10. Ono T, Mimuro J, Madoiwa S, Soejima K, Kashiwakura Y, Ishiwata A, et al. Severe secondary deficiency of von Willebrand factor-cleaving protease (ADAMTS13) in patients with sepsis-induced disseminated intravascular coagulation: its correlation with development of renal failure. Blood. 2006;107:528–534
  11. Bernardo A, Ball C, Nolasco L, Moake JF, Dong J. Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand factor multimers under flow. Blood. 2004;104:100–106
  12. Kusterer K, Poschmann T, Friedemann A, Enghofer M, Zendler S, Usadel KH. Arterial constriction, ischemia reperfusion, and leukocyte adherence in acute pancreatitis. Am J Physiol. 1993;265:G165–G171
  13. Mayer J, Rau B, Gansauge F, Beger HG. Inflammatory mediators in human acute pancreatitis: clinical and pathophysiological implications. Gut. 2000;47:546–552
  14. Mannucci PM, Capoferri C, Canciani MT. Plasma levels of von Willebrand factor regulate ADAMTS-13, its major cleaving protease. Br J Haematol. 2004;126:213–218
  15. Mannucci PM, Parolari A, Canciani MT, Alemanni F, Camera M. Opposite changes of ADAMTS-13 and von Willebrand factor after cardiac surgery. J Thromb Haemost. 2005;3:397–399
  16. Sanchez-Luceros A, Farias CE, Amaral MM, Kempfer AC, Votta R, Marchese C, et al. von Willebrand factor-cleaving protease (ADAMTS13) activity in normal non-pregnant women, pregnant and post-delivery women. Thromb Haemost. 2004;92:1320–1326
  17. Galbusera M, Noris M, Rossi C, Orisio S, Caprioli J, Ruggeri ZM, et al. Increased fragmentation of von Willebrand factor, due to abnormal cleavage of the subunit, parallels disease activity in recurrent hemolytic uremic syndrome and thrombotic thrombocytopenic purpura and discloses predisposition in families. The Italian Registry of Familial and Recurrent HUS/TTP. Blood. 1999;94:610–620
  18. Federici AB, Berkowitz SD, Lattuada A, Mannucci PM. Degradation of von Willebrand factor in patients with acquired clinical conditions in which there is heightened proteolysis. Blood. 1993;81:720–725
  19. Radomski MW, Palmer RM, Moncada S. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet. 1987;2:1057–1058
  20. Rother RP, Bell L, Hillmen P, Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA. 2005;293:1653–1662
  21. Cappellini MD. Coagulation in the pathophysiology of hemolytic anemias. Hematology Am Soc Hematol Educ Prog. 2007;74–78
  22. Huang KT, Han TH, Hyduke DR, Vaughn MW, Van Herle H, Hein TW, et al. Proc Natl Acad Sci U S A. 2001;98:11771–11776
  23. Olson JS, Foley EW, Rogge C, Tsai AL, Doyle MP, Lemon DD. NO scavenging and the hypertensive effect of hemoglobin-based blood substitutes. Free Radic Biol Med. 2004;36:685–697
  24. Schnog JJ, Jager EH, van der Dijs FP, Duits AJ, Moshage H, Muskiet FD, et al. Evidence for a metabolic shift of arginine metabolism in sickle cell disease. Ann Hematol. 2004;83:371–375
  25. Olsen SB, Tang DB, Jackson MR, Gomez ER, Ayala B, Alving BM. Enhancement of platelet deposition by cross-linked Hb in a rat carotid endarterectomy model. Circulation. 1996;93:327–332
  26. Studt JD, Hovinga JA, Antoine G, Hermann M, Rieger M, Scheiflinger F, et al. Fatal congenital thrombotic thrombocytopenic purpura with apparent ADAMTS13 inhibitor: in vitro inhibition of ADAMTS13 activity by hemoglobin. Blood. 2005;105:542–544
  27. Shao J, Miyata T, Yamada K, Hanafusa N, Wada T, Gordon KL, et al. Protective role of nitric oxide in a model of thrombotic microangiopathy in rats. J Am Soc Nephrol. 2001;12:2088–2097
  28. Jimenez JJ, Jy W, Mauro LM, Horstman LL, Ahn YS. Elevated endothelial microparticles in thrombotic thrombocytopenic purpura: findings from brain and renal microvascular cell culture and patients with active disease. Br J Haematol. 2001;112:81–90
  29. Wang JM, Wang Y, Huang JY, Yang Z, Chen L, Wang LC, et al. C-Reactive protein-induced endothelial microparticle generation in HUVECs is related to BH4-dependent NO formation. J Vasc Res. 2007;44:241–248
  30. Ang AD, Adhikari S, Ng SW, Bhatia M. Expression of nitric oxide synthase isoforms and nitric oxide production in acute pancreatitis and associated lung injury. Pancreatology. 2009;9:150–159
  31. Werner J, Fernández-del Castillo C, Rivera JA, Kollias N, Lewandrowski KB, Rattner DW. On the protective mechanism of nitric oxide in acute pancreatitis. Gut. 1998;43:401–407
  32. DiMagno MJ, Williams JA, Hao Y, Ernst SA, Owyang C. Endothelial nitric oxide synthase is protective in the initiation of caerulein-induced acute pancreatitis in mice. Am J Physiol: Gastrointest Liver Physiol. 2004;287:G80–G87
  33. Sugiyama Y, Kato S, Mitsufuji S, Okanoue T, Takeuchi K. Pathogenic role of endothelial nitric oxide synthase (eNOS/NOSIII) in cerulein- induced rat acute pancreatitis. Dig Dis Sci. 2006;51:1396–1403
  34. Goodwin BL, Pendleton LC, Levy MM, Solomonson LP, Eichler DC. Tumor necrosis factor-alpha reduces argininosuccinate synthase expression and nitric oxide production in aortic endothelial cells. Am J Physiol, Heart Circ Physiol. 2007;293:H1115–H1121
  35. Orshal JM, Khalil RA. Reduced endothelial NO-cGMP-mediated vascular relaxation and hypertension in IL-6-infused pregnant rats. Hypertension. 2004;43:434–444
  36. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358:1129–1136
  37. Aird WC. Vascular bed-specific thrombosis. J Thromb Haemost. 2007;5:283–291(Suppl)
  38. Mentula P, Kylänpää ML, Kemppainen E, Eklund KK, Orpana A, Puolakkainen P, et al. Serum levels of mast cell tryptase, vascular endothelial growth factor and basic fibroblast growth factor in patients with acute pancreatitis. Pancreas. 2003;27:e29–e33
  39. Ueda T, Takeyama Y, Yasuda T, Matsumura N, Sawa H, Nakajima T, et al. Vascular endothelial growth factor increases in serum and protects against the organ injuries in severe acute pancreatitis. J Surg Res. 2006;134:223–230
  40. Amar S, Wu KJ, Tan WW. Sorafenib-induced pancreatitis. Mayo Clin Proc. 2007;82:521
  41. Li M, Srinivas S. Acute pancreatitis associated with sorafenib. South Med J. 2007;100:909–911
  42. Hartwig W, Klafs M, Kirschfink M, Hackert T, Schneider L, Gebhard MM, et al. Interaction of complement and leukocytes in severe acute pancreatitis: potential for therapeutic intervention. Am J Physiol: Gastrointest Liver Physiol. 2006;291:G844–G850
  43. Büchler M, Malfertheiner P, Schoetensack C, Uhl W, Beger HG. Sensitivity of antiproteases, complement factors and C-reactive protein in detecting pancreatic necrosis. Results of a prospective clinical study. Int J Pancreatol. 1986;1(3–4):227–235
  44. Garvey MB, Freedman J. Complement in thrombotic thrombocytopenic purpura. Am J Hematol. 1983;15:397–398
  45. Ruiz-Torres MP, Casiraghi F, Galbusera M, Macconi D, Gastoldi S, Todeschini M, et al. Complement activation: the missing link between ADAMTS-13 deficiency and microvascular thrombosis of thrombotic microangiopathies. Thromb Haemost. 2005;93:443–452
  46. Wada H, Ohiwa M, Kaneko T, Tamaki S, Tanigawa M, Shirakawa S, et al. Plasma thrombomodulin as a marker of vascular disorders in thrombotic thrombocytopenic purpura and disseminated intravascular coagulation. Am J Hematol. 1992;39:20–24
  47. Vianelli N, Catani L, Gugliotta L, Nocentini F, Baravelli S, Lancellotti G, et al. Increased P-selectin plasma levels in patients with thrombotic thrombocytopenic purpura. Haematologica. 1996;81:3–7
  48. Mantke R, Pross M, Kunz D, Ebert M, Kahl S, Peters B, et al. Soluble thrombomodulin plasma levels are an early indication of a lethal course in human acute pancreatitis. Surgery. 2002;131:424–432
  49. Lu XL, Cai JT, Lu XG, Si JM, Qian KD. Plasma level of thrombomodulin is an early indication of pancreatic necrosis in patients with acute pancreatitis. Intern Med. 2007;46:441–445
  50. Hackert T, Sperber R, Hartwig W, Fritz S, Schneider L, Gebhard MM, et al. P-selectin inhibition reduces severity of acute experimental pancreatitis. Pancreatology. 2009;9:369–374
  51. Olsen H. Thrombotic thrombocytopenic purpura as a cause of pancreatitis. Report of a case and review of the literature. Am J Dig Dis. 1973;18:238–246
  52. Cuthbertson CM, Christophi C. Disturbances of the microcirculation in acute pancreatitis. Br J Surg. 2006;93:518–530
  53. Druml W, Laggner AN, Lenz K, Grimm G, Schneeweiss B. Pancreatitis in acute hemolysis. Ann Hematol. 1991;63:39–41
  54. Ahmed S, Siddiqui AK, Siddiqui RK, Kimpo M, Russo L, Mattana J. Acute pancreatitis during sickle cell vaso-occlusive painful crisis. Am J Hematol. 2003;73:190–193
  55. Morioka C, Uemura M, Matsuyama T, Matsumoto M, Kato S, Ishikawa M, et al. Plasma ADAMTS13 activity parallels the APACHE II score, reflecting an early prognostic indicator for patients with severe acute pancreatitis. Scand J Gastroenterol. 2008;43:1387–1396
  56. Chauhan AK, Kisucka J, Brill A, Walsh MT, Scheiflinger F, Wagner DD. ADAMTS13: a new link between thrombosis and inflammation. J Exp Med. 2008;205:2065–2074

PII: S0953-6205(09)00185-X

doi: 10.1016/j.ejim.2009.09.008

European Journal of Internal Medicine
Volume 20, Issue 8 , Pages 739-743 , December 2009

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