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REVIEW

Pathogenesis and Therapy of Coagulation Disorders in Severe Acute Pancreatitis

ORCID Icon, , , , &
Pages 57-67 | Received 09 Sep 2022, Accepted 12 Nov 2022, Published online: 06 Jan 2023

References

  • Petrov MS, Yadav D. Global epidemiology and holistic prevention of pancreatitis. Nat Rev Gastroenterol Hepatol. 2019;16(3):175–184. doi:10.1038/s41575-018-0087-5
  • Iannuzzi JP, King JA, Leong JH, et al. Global incidence of acute pancreatitis is increasing over time: a systematic review and meta-analysis. Gastroenterology. 2022;162(1):122–134. doi:10.1053/j.gastro.2021.09.043
  • Padureanu V, Florescu D, Pădureanu R, et al. Role of antioxidants and oxidative stress in the evolution of acute pancreatitis (review). Exp Ther Med. 2022;23(3):197. doi:10.3892/etm.2022.11120
  • Cuthbertson CM, Christophi C. Disturbances of the microcirculation in acute pancreatitis. Br J Surg. 2006;93(5):518–530. doi:10.1002/bjs.5316
  • Foitzik T, Eibl G, Hotz B, et al. Persistent multiple organ microcirculatory disorders in severe acute pancreatitis: experimental findings and clinical implications. Dig Dis Sci. 2002;47(1):130–138. doi:10.1023/A:1013284008219
  • Liu C, Zhou X, Ling L, et al. Prediction of mortality and organ failure based on coagulation and fibrinolysis markers in patients with acute pancreatitis: a retrospective study. Medicine. 2019;98(21):e15648. doi:10.1097/MD.0000000000015648
  • Yang N, Hao J, Zhang D, Antithrombin III. D-dimer levels as indicators of disease severity in patients with hyperlipidaemic or biliary acute pancreatitis. J Int Med Res. 2017;45(1):147–158. doi:10.1177/0300060516677929
  • Ding L, Deng F, Yu C, et al. Portosplenomesenteric vein thrombosis in patients with early-stage severe acute pancreatitis. World J Gastroenterol. 2018;24(35):4054–4060. doi:10.3748/wjg.v24.i35.4054
  • Lu XS, Fu Q, Jie-Qin L, et al. Low molecular weight heparin in the treatment of severe acute pancreatitis: a multiple centre prospective clinical study. Asian J Surg. 2009;32(2):89–94. doi:10.1016/S1015-9584(09)60017-8
  • Yano T, Taniguchi M, Shirasaka T, et al. Effectiveness of soluble recombinant human thrombomodulin in patients with severe acute pancreatitis complicated by disseminated intravascular coagulation. Turk J Anaesthesiol Reanim. 2019;47(4):320–326. doi:10.5152/TJAR.2019.42709
  • Eguchi T, Tsuji Y, Yamashita H, et al. Efficacy of recombinant human soluble thrombomodulin in preventing walled-off necrosis in severe acute pancreatitis patients. Pancreatology. 2015;15(5):485–490. doi:10.1016/j.pan.2015.08.002
  • Hollemans RA, Hallensleben NDL, Mager DJ, et al. Pancreatic exocrine insufficiency following acute pancreatitis: systematic review and study level meta-analysis. Pancreatology. 2018;18(3):253–262. doi:10.1016/j.pan.2018.02.009
  • Zhu R, Wei S, Wu C, et al. Utility of clot formation and lysis assay to monitor global coagulation state of patients with severe acute pancreatitis. Dig Dis Sci. 2012;57(5):1399–1403. doi:10.1007/s10620-012-2034-6
  • Maduzia D, Ceranowicz P, Cieszkowski J, et al. Administration of warfarin accelerates the recovery in ischemia/reperfusion-induced acute pancreatitis. J Physiol Pharmacol. 2020;71(3). doi:10.26402/jpp.2020.3.13.
  • Dumnicka P, Kuśnierz-Cabala B, Sporek M, et al. Serum concentrations of angiopoietin-2 and soluble fms-like tyrosine kinase 1 (sFlt-1) Are Associated with coagulopathy among patients with acute pancreatitis. Int J Mol Sci. 2017;18(4):753. doi:10.3390/ijms18040753
  • Saluja A, Dudeja V, Dawra R, et al. Early intra-acinar events in pathogenesis of pancreatitis. Gastroenterology. 2019;156(7):1979–1993. doi:10.1053/j.gastro.2019.01.268
  • Lee PJ, Papachristou GI. New insights into acute pancreatitis. Nat Rev Gastroenterol Hepatol. 2019;16(8):479–496. doi:10.1038/s41575-019-0158-2
  • Macey MG, Wolf SI, Wheeler-Jones CPD, et al. Expression of blood coagulation factors on monocytes after exposure to TNF-treated endothelium in a novel whole blood model of arterial flow. J Immunol Methods. 2009;350(1–2):133–141. doi:10.1016/j.jim.2009.08.007
  • Pereda J, Sabater L, Aparisi L, et al. Interaction between cytokines and oxidative stress in acute pancreatitis. Curr Med Chem. 2006;13(23):2775–2787. doi:10.2174/092986706778522011
  • Grignani G, Maiolo A. Cytokines and hemostasis. Haematologica. 2000;85(9):967–972.
  • Dugina TN, Kiseleva EV, Chistov IV, et al. Receptors of the PAR family as a link between blood coagulation and inflammation. Biochemistry. 2002;67(1):65–74. doi:10.1023/A:1013952114485
  • Lisman T, Porte RJ. Activation and regulation of hemostasis in acute liver failure and acute pancreatitis. Semin Thromb Hemost. 2010;36(4):437–443. doi:10.1055/s-0030-1254052
  • Schmaier AH. Transferrin: a blood coagulation modifier. Cell Res. 2020;30(2):101–102. doi:10.1038/s41422-020-0275-z
  • Radenkovic D, Bajec D, Ivancevic N, et al. D-dimer in acute pancreatitis a new approach for an early assessment of organ failure. Pancreas. 2009;38(6):655–660. doi:10.1097/MPA.0b013e3181a66860
  • Andersson E, Axelsson J, Eckerwall G, Ansari D, Andersson R. Tissue factor in predicted severe acute pancreatitis. World J Gastroenterol. 2010;16(48):6128–6134. doi:10.3748/wjg.v16.i48.6128
  • Jackson SP, Darbousset R, Schoenwaelder SM. Thromboinflammation: challenges of therapeutically targeting coagulation and other host defense mechanisms. Blood. 2019;133(9):906–918. doi:10.1182/blood-2018-11-882993
  • Eibl G, Buhr HJ, Foitzik T. Therapy of microcirculatory disorders in severe acute pancreatitis: what mediators should we block? Intensive Care Med. 2002;28(2):139–146. doi:10.1007/s00134-001-1194-1
  • Yuan HQ, Hao Y-M, Ren Z, et al. Tissue factor pathway inhibitor in atherosclerosis. Clin Chim Acta. 2019;491:97–102. doi:10.1016/j.cca.2019.01.024
  • Mast AE. Tissue factor pathway inhibitor: multiple anticoagulant activities for a single protein. Arterioscler Thromb Vasc Biol. 2016;36(1):9–14. doi:10.1161/ATVBAHA.115.305996
  • Sungurlu S, Kuppy J, Balk RA. Role of antithrombin III and tissue factor pathway in the pathogenesis of sepsis. Crit Care Clin. 2020;36(2):255–265. doi:10.1016/j.ccc.2019.12.002
  • Lindstrom OK, Tukiainen EM, Kylänpää M-L, et al. Thrombin generation in vitro and in vivo, and disturbed tissue factor regulation in patients with acute pancreatitis. Pancreatology. 2011;11(6):557–566. doi:10.1159/000333481
  • Yasuda T, Ueda T, Kamei K, et al. Plasma tissue factor pathway inhibitor levels in patients with acute pancreatitis. J Gastroenterol. 2009;44(10):1071–1079. doi:10.1007/s00535-009-0096-9
  • Zelaya H, Rothmeier AS, Ruf W. Tissue factor at the crossroad of coagulation and cell signaling. J Thromb Haemost. 2018;16(10):1941–1952. doi:10.1111/jth.14246
  • Pendurthi UR, Rao LVM. Endothelial cell protein C receptor-dependent signaling. Curr Opin Hematol. 2018;25(3):219–226. doi:10.1097/MOH.0000000000000416
  • Dinarvand P, Moser KA. Protein C deficiency. Arch Pathol Lab Med. 2019;143(10):1281–1285. doi:10.5858/arpa.2017-0403-RS
  • Lindstrom O, Kylanpaa L, Mentula P, et al. Upregulated but insufficient generation of activated protein C is associated with development of multiorgan failure in severe acute pancreatitis. Crit Care. 2006;10(1):R16. doi:10.1186/cc3966
  • Chen Y, Ke L, Meng L, et al. Endothelial markers are associated with pancreatic necrosis and overall prognosis in acute pancreatitis: a preliminary cohort study. Pancreatology. 2017;17(1):45–50. doi:10.1016/j.pan.2016.12.005
  • Esmon CT. Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost. 2006;32(Suppl 1):49–60. doi:10.1055/s-2006-939554
  • Villegas-Mendez A, Montes R, Ambrose LR, et al. Proteolysis of the endothelial cell protein C receptor by neutrophil proteinase 3. J Thromb Haemost. 2007;5(5):980–988. doi:10.1111/j.1538-7836.2007.02480.x
  • Song D, Ye X, Xu H, et al. Activation of endothelial intrinsic NF-{kappa}B pathway impairs protein C anticoagulation mechanism and promotes coagulation in endotoxemic mice. Blood. 2009;114(12):2521–2529. doi:10.1182/blood-2009-02-205914
  • Dargaud Y, Scoazec JY, Wielders SJH, et al. Characterization of an autosomal dominant bleeding disorder caused by a thrombomodulin mutation. Blood. 2015;125(9):1497–1501. doi:10.1182/blood-2014-10-604553
  • Kyhala L, Lindström O, Kylänpää L, et al. Activated protein C retards recovery from coagulopathy in severe acute pancreatitis. Scand J Clin Lab Invest. 2016;76(1):10–16. doi:10.3109/00365513.2015.1084041
  • Yamanel L, Mas M, Comert B, et al. The effect of activated protein C on experimental acute necrotizing pancreatitis. Crit Care. 2005;9(3):R184–90. doi:10.1186/cc3485
  • Schlommer C, Brandtner A, Bachler M. Antithrombin and its role in host defense and inflammation. Int J Mol Sci. 2021;22:8. doi:10.3390/ijms22084283
  • Fidan S, Erkut M, Cosar A, et al. Higher thrombin-antithrombin III complex levels may indicate severe acute pancreatitis. Dig Dis. 2018;36(3):244–251. doi:10.1159/000485613
  • Wang D, Tian M, Cui G, et al. Antithrombin deficiency and decreased protein C activity in a young man with venous thromboembolism: a case report. Front Med. 2018;12(3):319–323. doi:10.1007/s11684-017-0553-4
  • Iba T, Saitoh D. Efficacy of antithrombin in preclinical and clinical applications for sepsis-associated disseminated intravascular coagulation. J Intensive Care. 2014;2(1):66. doi:10.1186/s40560-014-0051-6
  • Nakahara K, Okuse C, Adachi S, et al. Use of antithrombin and thrombomodulin in the management of disseminated intravascular coagulation in patients with acute cholangitis. Gut Liver. 2013;7(3):363–370. doi:10.5009/gnl.2013.7.3.363
  • Kienast J, Juers M, Wiedermann CJ, et al. Treatment effects of high-dose antithrombin without concomitant heparin in patients with severe sepsis with or without disseminated intravascular coagulation. J Thromb Haemost. 2006;4(1):90–97. doi:10.1111/j.1538-7836.2005.01697.x
  • Madoiwa S. Recent advances in disseminated intravascular coagulation: endothelial cells and fibrinolysis in sepsis-induced DIC. J Intensive Care. 2015;3:8. doi:10.1186/s40560-015-0075-6
  • Urano T, Suzuki Y, Iwaki T, Sano H, Honkura N, Castellino FJ. Recognition of plasminogen activator inhibitor type 1 as the primary regulator of fibrinolysis. Curr Drug Targets. 2019;20(16):1695–1701. doi:10.2174/1389450120666190715102510
  • Nakajima T, Ueda T, Takeyama Y, et al. Protective effects of vascular endothelial growth factor on intestinal epithelial apoptosis and bacterial translocation in experimental severe acute pancreatitis. Pancreas. 2007;34(4):410–416. doi:10.1097/mpa.0b013e3180335c64
  • Kaji H. Adipose tissue-derived plasminogen activator inhibitor-1 function and regulation. Compr Physiol. 2016;6(4):1873–1896.
  • Chapin JC, Hajjar KA. Fibrinolysis and the control of blood coagulation. Blood Rev. 2015;29(1):17–24. doi:10.1016/j.blre.2014.09.003
  • Fender AC, Rauch B, Geisler T, et al. Protease-activated receptor PAR-4: an inducible switch between thrombosis and vascular inflammation? Thromb Haemost. 2017;117(11):2013–2025. doi:10.1160/TH17-03-0219
  • Lordan R, Tsoupras A, Zabetakis I, et al. Forty years since the structural elucidation of platelet-activating factor (paf): historical, current, and future research perspectives. Molecules. 2019;24:23. doi:10.3390/molecules24234414
  • Zinellu A, Mangoni AA, Review S. and meta-analysis of the effect of statins on circulating E-selectin, L-selectin, and P-Selectin. Biomedicines. 2021;9:11. doi:10.3390/biomedicines9111707
  • Zhang X, Zhu M, Jiang XL, et al. P-selectin glycoprotein ligand 1 deficiency prevents development of acute pancreatitis by attenuating leukocyte infiltration. World J Gastroenterol. 2020;26(41):6361–6377. doi:10.3748/wjg.v26.i41.6361
  • Rossaint J, Zarbock A. Platelets in leucocyte recruitment and function. Cardiovasc Res. 2015;107(3):386–395. doi:10.1093/cvr/cvv048
  • Zwicker JI, Trenor CC, Furie BC, et al. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol. 2011;31(4):728–733. doi:10.1161/ATVBAHA.109.200964
  • Tsaroucha AK, Schizas D, Vailas MG, et al. E and P selectins as potential markers in the assessment of the severity of acute pancreatitis. Pancreas. 2018;47(4):406–411. doi:10.1097/MPA.0000000000001009
  • Setiadi H, Yago T, Liu Z, et al. Endothelial signaling by neutrophil-released oncostatin M enhances P-selectin-dependent inflammation and thrombosis. Blood Adv. 2019;3(2):168–183. doi:10.1182/bloodadvances.2018026294
  • Hartman H, Abdulla A, Awla D, et al. P-selectin mediates neutrophil rolling and recruitment in acute pancreatitis. Br J Surg. 2012;99(2):246–255. doi:10.1002/bjs.7775
  • Jin H, Gebska MA, Blokhin IO, et al. Endothelial PPAR-gamma protects against vascular thrombosis by downregulating P-selectin expression. Arterioscler Thromb Vasc Biol. 2015;35(4):838–844. doi:10.1161/ATVBAHA.115.305378
  • Hackert T, Sperber R, Hartwig W, et al. P-selectin inhibition reduces severity of acute experimental pancreatitis. Pancreatology. 2009;9(4):369–374. doi:10.1159/000212098
  • Carestia A, Kaufman T, Rivadeneyra L, et al. Mediators and molecular pathways involved in the regulation of neutrophil extracellular trap formation mediated by activated platelets. J Leukoc Biol. 2016;99(1):153–162. doi:10.1189/jlb.3A0415-161R
  • Darbousset R, Thomas GM, Mezouar S, et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood. 2012;120(10):2133–2143. doi:10.1182/blood-2012-06-437772
  • Carminita E, Crescence L, Panicot-Dubois L, Dubois C. Role of neutrophils and NETs in animal models of thrombosis. Int J Mol Sci. 2022;23:3.
  • Nakazawa D, Desai J, Steiger S, et al. Activated platelets induce MLKL-driven neutrophil necroptosis and release of neutrophil extracellular traps in venous thrombosis. Cell Death Discov. 2018;4:6. doi:10.1038/s41420-018-0073-2
  • Zucoloto AZ, Jenne CN. Platelet-neutrophil interplay: insights into neutrophil extracellular trap (NET)-driven coagulation in infection. Front Cardiovasc Med. 2019;6:85. doi:10.3389/fcvm.2019.00085
  • Merza M, Hartman H, Rahman M, et al. Neutrophil extracellular traps induce trypsin activation, inflammation, and tissue damage in mice with severe acute pancreatitis. Gastroenterology. 2015;149(7):1920–1931 e8. doi:10.1053/j.gastro.2015.08.026
  • Madhi R, Rahman M, Taha D, et al. Platelet IP6K1 Regulates Neutrophil Extracellular Trap-Microparticle Complex Formation in Acute Pancreatitis. JCI Insight. 2019. doi:10.1172/jci.insight.129270
  • Hu J, Kang H, Chen H, et al. Targeting neutrophil extracellular traps in severe acute pancreatitis treatment. Therap Adv Gastroenterol. 2020;13:1756284820974913. doi:10.1177/1756284820974913
  • Dzik S. Complement and coagulation: cross talk through time. Transfus Med Rev. 2019;33(4):199–206. doi:10.1016/j.tmrv.2019.08.004
  • Conway EM. Complement-coagulation connections. Blood Coagul Fibrinolysis. 2018;29(3):243–251. doi:10.1097/MBC.0000000000000720
  • Zhang L, Qiao Z, Feng H, et al. The early predictive role of complement C3 and C4 in patients with acute pancreatitis. J Clin Lab Anal. 2020;34(5):e23205. doi:10.1002/jcla.23205
  • Bettac L, Denk S, Seufferlein T, et al. Complement in pancreatic disease-perpetrator or savior? Front Immunol. 2017;8:15. doi:10.3389/fimmu.2017.00015
  • Del Conde I, Cruz MA, Zhang H, et al. Platelet activation leads to activation and propagation of the complement system. J Exp Med. 2005;201(6):871–879. doi:10.1084/jem.20041497
  • Linders J, Madhi R, Mörgelin M, King BC, Blom AM, Rahman M. Complement component 3 is required for tissue damage, neutrophil infiltration, and ensuring NET formation in acute pancreatitis. Eur Surg Res. 2021;2021:1–14.
  • Madhi R, Rahman M, Taha D, et al. Targeting peptidylarginine deiminase reduces neutrophil extracellular trap formation and tissue injury in severe acute pancreatitis. J Cell Physiol. 2019;234(7):11850–11860. doi:10.1002/jcp.27874
  • Murthy P, Singhi AD, Ross MA, et al. Enhanced neutrophil extracellular trap formation in acute pancreatitis contributes to disease severity and is reduced by chloroquine. Front Immunol. 2019;10:28. doi:10.3389/fimmu.2019.00028
  • Easler J, Muddana V, Furlan A, et al. Portosplenomesenteric venous thrombosis in patients with acute pancreatitis is associated with pancreatic necrosis and usually has a benign course. Clin Gastroenterol Hepatol. 2014;12(5):854–862. doi:10.1016/j.cgh.2013.09.068
  • Lin L, Zhao L, Gao N, et al. From multi-target anticoagulants to DOACs, and intrinsic coagulation factor inhibitors. Blood Rev. 2020;39:100615. doi:10.1016/j.blre.2019.100615
  • Maduzia D, Ceranowicz P, Cieszkowski J, et al. Pretreatment with warfarin attenuates the development of ischemia/reperfusion-induced acute pancreatitis in rats. Molecules. 2020;25:11. doi:10.3390/molecules25112493
  • Kong Y, Yin J, Cheng D, et al. Antithrombin III attenuates AKI following acute severe pancreatitis. Shock. 2018;49(5):572–579. doi:10.1097/SHK.0000000000000946
  • Tozlu M, Kayar Y, Ince AT, et al. Low molecular weight heparin treatment of acute moderate and severe pancreatitis: a randomized, controlled, open-label study. Turk J Gastroenterol. 2019;30(1):81–87. doi:10.5152/tjg.2018.18583
  • Lu XS, Qiu F, Li Y-X, et al. Effect of lower-molecular weight heparin in the prevention of pancreatic encephalopathy in the patient with severe acute pancreatitis. Pancreas. 2010;39(4):516–519. doi:10.1097/MPA.0b013e3181c3c954
  • Patil B, Meena LN, Sharma DC, et al. Impact of low-molecular-weight heparin in the treatment of moderately severe and severe acute pancreatitis; a randomized, single blind, Phase 3 control trial. Int J Surg. 2022;101:106621. doi:10.1016/j.ijsu.2022.106621