Multipotent role of platelets in inflammatory bowel diseases: A clinical approach

World Journal of Gastroenterology

Volumn 20, Issue 12, 2014, Pages 3180-3190

  Voudoukis, Evangelos ^a   Karmiris, Konstantinos ^a   Koutroubakis, Ioannis E ^b  

^a Venizelion General Hospital   (Greece)

^b UNIVERSITY HOSPITAL OF HERAKLION   (Greece)

Author keywords

Anemia; Crohn's disease; Platelets; Throm bocytosis; Ulcerative colitis

Indexed keywords

ABCIXIMAB; ADENOSINE DIPHOSPHATE; AZATHIOPRINE; CD40 LIGAND; CLOPIDOGREL; ENDOTHELIAL CELL GROWTH FACTOR; EPTIFIBATIDE; HISTAMINE; IMMUNOGLOBULIN G; INFLIXIMAB; INTERLEUKIN 6; INTERLEUKIN 8; MERCAPTOPURINE; MESALAZINE; PLATELET DERIVED GROWTH FACTOR; RANTES; THROMBOCYTE FACTOR 4; THROMBOPOIETIN; TIROFIBAN; TRANSFORMING GROWTH FACTOR; TRAPIDIL; VASCULOTROPIN; VON WILLEBRAND FACTOR; ANTITHROMBOCYTIC AGENT;

ARTICLE; BLOOD CLOTTING; CLINICAL PRACTICE; CROHN DISEASE; HUMAN; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; IRON DEFICIENCY ANEMIA; LEUKOCYTE ACTIVATION; PATHOGENESIS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTE STRUCTURE; THROMBOCYTOPOIESIS; THROMBOCYTOSIS; ULCERATIVE COLITIS; BLOOD; COLITIS, ULCERATIVE; COMPLICATION; CYTOLOGY; HEMOSTASIS; INFLAMMATORY BOWEL DISEASES; MEMBRANE MICROPARTICLE; METABOLISM; THROMBOCYTE COUNT;

ANEMIA, IRON-DEFICIENCY; BLOOD COAGULATION; BLOOD PLATELETS; CELL-DERIVED MICROPARTICLES; COLITIS, ULCERATIVE; CROHN DISEASE; HEMOSTASIS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; PLATELET AGGREGATION INHIBITORS; PLATELET COUNT; THROMBOCYTOSIS;

EID: 84896940573     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i12.3180     Document Type: Article

References (113)

1. Danese S, Motte Cd Cde L, Fiocchi C. Platelets in inflammatory bowel disease: clinical, pathogenic, and therapeutic implications. Am J Gastroenterol 2004; 99: 938-945 [PMID: 15128364 DOI: 10.1111/j.1572-0241.2004.04129.x]
2. Yoshida H, Granger DN. Inflammatory bowel disease: a paradigm for the link between coagulation and inflammation. Infamm Bowel Dis 2009; 15: 1245-1255 [PMID: 19253306 DOI: 10.1002/ibd.20896]
3. Fiocchi C. Inflammatory bowel disease: etiology and patho-genesis. Gastroenterology 1998; 115: 182-205 [PMID: 9649475 DOI: 10.1016/S0016-5085(98)70381-6]
4. Baughman RP, Lower EE, Flessa HC, Tollerud DJ. Throm-bocytopenia in the intensive care unit. Chest 1993; 104: 1243-1247 [PMID: 8404200 DOI: 10.1378/chest.104.4.1243]
5. Huang HS, Chang HH. Platelets in inflammation and immune modulations: functions beyond hemostasis. Arch Immunol Ther Exp (Warsz) 2012; 60: 443-451 [PMID: 22940877 DOI: 10.1007/s00005-012-0193-y]
6. Danese S. Nonimmune cells in inflammatory bowel disease: from victim to villain. Trends Immunol 2008; 29: 555-564 [PMID: 18838297 DOI: 10.1016/j.it.2008.07.009]
7. Ripoche J. Blood platelets and inflammation: their relationship with liver and digestive diseases. Clin Res Hepatol Gas-troenterol 2011; 35: 353-357 [PMID: 21482218 DOI: 10.1016/ j.clinre.2011.02.012]
8. Cognasse F, Lafarge S, Chavarin P, Acquart S, Garraud O. Lipopolysaccharide induces sCD40L release through human platelets TLR4, but not TLR2 and TLR9. Intensive Care Med 2007; 33: 382-384 [PMID: 17180393 DOI: 10.1007/ s00134-006-0488-8]
9. Youssefian T, Drouin A, Massé JM, Guichard J, Cramer EM. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcel-lular compartment and is enhanced by platelet activation. Blood 2002; 99: 4021-4029 [PMID: 12010803 DOI: 10.1182/ blood-2001-12-0191]
10. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, Keys EM, Allen-Vercoe E, Devinney R, Doig CJ, Green FH, Kubes P. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463-469 [PMID: 17384648 DOI: 10.1038/nm1565]
11. Ma AC, Kubes P. Platelets, neutrophils, and neutro-phil extracellular traps (NETs) in sepsis. J Thromb Hae-most 2008; 6: 415-420 [PMID: 18088344 DOI: 10.1111/ j.1538-7836.2007.02865.x]
12. Smyth SS, McEver RP, Weyrich AS, Morrell CN, Hoffman MR, Arepally GM, French PA, Dauerman HL, Becker RC. Platelet functions beyond hemostasis. J Thromb Hae-most 2009; 7: 1759-1766 [PMID: 19691483 DOI: 10.1111/ j.1538-7836.2009.03586.x]
13. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252 [PMID: 9521319 DOI: 10.1038/32588]
14. Sprague DL, Elzey BD, Crist SA, Waldschmidt TJ, Jensen RJ, Ratliff TL. Platelet-mediated modulation of adaptive immunity: unique delivery of CD154 signal by platelet-derived membrane vesicles. Blood 2008; 111: 5028-5036 [PMID: 18198347 DOI: 10.1182/blood-2007-06-097410]
15. Morowitz DA, Allen LW, Kirsner JB. Thrombocytosis in chronic inflammatory bowel disease. Ann Intern Med 1968; 68: 1013-1021 [PMID: 5646806 DOI: 10.7326/0003-4819-68-5-1 013]
16. Skoda RC. Thrombocytosis. Hematology Am Soc Hematol Educ Program 2009; 159-167 [PMID: 20008195 DOI: 10.1182/ asheducation-2009.1.159]
17. Schafer AI. Thrombocytosis. N Engl J Med 2004; 350: 1211-1219 [PMID: 15028825 DOI: 10.1056/NEJMra035363]
18. Kaushansky K. Determinants of platelet number and regulation of thrombopoiesis. Hematology Am Soc Hematol Educ Program 2009; 147-152 [PMID: 20008193 DOI: 10.1182/ashe-ducation-2009.1.147]
19. Cerutti A, Custodi P, Mduranti M, Balduini CL. Circulating thrombopoietin in reactive conditions behaves like an acute phase reactant. Clin Lab Haematol 1999; 21: 271-275 [PMID: 10583330 DOI: 10.1046/j.1365-2257.1999.00226.x]
20. Heits F, Stahl M, Ludwig D, Stange EF, Jelkmann W. Elevated serum thrombopoietin and interleukin-6 concentrations in thrombocytosis associated with inflammatory bowel disease. J Interferon Cytokine Res 1999; 19: 757-760 [PMID: 10454346 DOI: 10.1089/107999099313604]
21. Papa A, Danese S, Piccirillo N, Toriani-Terenzi C, Bartolozzi F, Piscaglia AC, Grillo A, Leone G, Gentiloni-Silveri N, Gas-barrini G, Gasbarrini A. Thrombopoietin serum levels in patients with inflammatory bowel disease with and without previous thromboembolic events. Hepatogastroenterology 2003; 50: 132-135 [PMID: 12630008]
22. Harries AD, Fitzsimons E, Fifield R, Dew MJ, Rhoades J. Platelet count: a simple measure of activity in Crohn's disease. Br Med J (Clin Res Ed) 1983; 286: 1476 [PMID: 6405846 DOI: 10.1136/bmj.286.6381.1896]
23. Simanek R, Vormittag R, Ay C, Alguel G, Dunkler D, Schwarzinger I, Steger G, Jaeger U, Zielinski C, Pabinger I. High platelet count associated with venous thromboembo-lism in cancer patients: results from the Vienna Cancer and Thrombosis Study (CATS). J Thromb Haemost 2010; 8: 114-120 [PMID: 19889150 DOI: 10.1111/j.1538-7836.2009.03680.x]
24. Fleshner P, Ippoliti A, Dubinsky M, Ognibene S, Vasiliaus-kas E, Chelly M, Mei L, Papadakis KA, Landers C, Targan S. A prospective multivariate analysis of clinical factors associated with pouchitis after ileal pouch-anal anastomosis. Clin Gastroenterol Hepatol 2007; 5: 952-998; quiz 887 [PMID: 17544871 DOI: 10.1016/j.cgh.2007.03.020]
25. Okon A, Dubinsky M, Vasiliauskas EA, Papadakis KA, Ip-politi A, Targan SR, Fleshner PR. Elevated platelet count before ileal pouch-anal anastomosis for ulcerative colitis is associated with the development of chronic pouchitis. Am Surg 2005; 71: 821-826 [PMID: 16468527]
26. Lian L, Fazio VW, Lavery IC, Hammel J, Remzi FH, Shen B. Evaluation of association between precolectomy thrombocy-tosis and the occurrence of inflammatory pouch disorders. Dis Colon Rectum 2009; 52: 1912-1918 [PMID: 19966641 DOI: 10.1007/DCR.0b013e3181b300f4]
27. Collins CE, Rampton DS. Platelet dysfunction: a new dimension in inflammatory bowel disease. Gut 1995; 36: 5-8 [PMID: 7890235 DOI: 10.1136/gut.36.1.5]
28. Turhan O, Coban E, Inan D, Yalcin AN. Increased mean platelet volume in chronic hepatitis B patients with inactive disease. Med Sci Monit 2010; 16: CR202-CR205 [PMID: 20357720]
29. Kisacik B, Tufan A, Kalyoncu U, Karadag O, Akdogan A, Ozturk MA, Kiraz S, Ertenli I, Calguneri M. Mean platelet volume (MPV) as an inflammatory marker in an- kylosing spondylitis and rheumatoid arthritis. Joint Bone Spine 2008; 75: 291-294 [PMID: 18403245 DOI: 10.1016/ j.jbspin.2007.06.016]
30. Balcik ÖS, Bilen S, Ulusoy EK, Akdeniz D, Uysal S, Ikizek M, Ak F, Kosar A. Thrombopoietin and mean platelet volume in patients with ischemic stroke. Clin Appl Thromb Hemost 2013; 19: 92-95 [PMID: 22327824 DOI: 10.1177/1076029611434528]
31. Albayrak Y, Albayrak A, Albayrak F, Yildirim R, Aylu B, Uyanik A, Kabalar E, Güzel IC. Mean platelet volume: a new predictor in confirming acute appendicitis diagnosis. Clin Appl Thromb Hemost 2011; 17: 362-366 [PMID: 20460349 DOI: 10.1177/1076029610364520]
32. Coban E, Ozdogan M, Yazicioglu G, Akcit F. The mean platelet volume in patients with obesity. Int J Clin Pract 2005; 59: 981-982 [PMID: 16033624 DOI: 10.1111/ j.1742-1241.2005.00500.x]
33. Varol E, Ozaydin M. Decreased mean platelet volume in patients with amylodiosis. Clin Appl Thromb Hemost 2013; 19: 578 [PMID: 23288868 DOI: 10.1177/1076029612459677]
34. Sahin A, Sahin M, Yüksel H, Türkcü FM, Cinar Y, Cingü AK, Ari S, Caça I. The mean platelet volume in patients with retinal vein occlusion. J Ophthalmol 2013; 2013: 236371 [PMID: 23781328 DOI: 10.1155/2013/236371]
35. Aliosmanoglu I, Gul M, Oguz A, Basol O, Uslukaya O, Keles C. Can mean platelet volume be a new risk factor in portal venous thrombosis? Clin Appl Thromb Hemost 2013; 19: 433-436 [PMID: 23162018 DOI: 10.1177/1076029612464903]
36. Khode V, Sindhur J, Kanbur D, Ruikar K, Nallulwar S. Mean platelet volume and other platelet volume indices in patients with stable coronary artery disease and acute myocardial infarction: A case control study. J Cardiovasc Dis Res 2012; 3: 272-275 [PMID: 23233769 DOI: 10.4103/0975-3583.102694]
37. Kilinçalp S, Ekiz F, Başar O, Ayte MR, Coban S, Yilmaz B, Altinbaş A, Başar N, Aktaş B, Tuna Y, Erbiş H, Uçar E, Erarslan E, Yüksel O. Mean platelet volume could be pos sible biomarker in early diagnosis and monitoring of gastric cancer. Platelets 2013; Epub ahead of print [PMID: 23537073 DOI: 10.3109/09537104.2013.783689]
38. Wang RT, Li JY, Cao ZG, Li Y. Mean platelet volume is decreased during an acute exacerbation of chronic obstructive pulmonary disease. Respirology 2013; 18: 1244-1248 [PMID: 23786593 DOI: 10.1111/resp.12143]
39. Järemo P, Sandberg-Gertzen H. Platelet density and size in inflammatory bowel disease. Thromb Haemost 1996; 75: 560-561 [PMID: 8743178]
40. Kapsoritakis AN, Koukourakis MI, Sfridaki A, Potamianos SP, Kosmadaki MG, Koutroubakis IE, Kouroumalis EA. Mean platelet volume: a useful marker of inflammatory bowel disease activity. Am J Gastroenterol 2001; 96: 776-781 [PMID: 11280550 DOI: 10.1111/j.1572-0241.2001.03621.x]
41. Yüksel O, Helvaci K, Başar O, Köklü S, Caner S, Helvaci N, Abayli E, Altiparmak E. An overlooked indicator of disease activity in ulcerative colitis: mean platelet volume. Platelets 2009; 20: 277-281 [PMID: 19459134 DOI: 10.1080/0953710090 2856781]
42. Mustafa Güçlü, Hakan Sakalli, Tolga Yakar. Mean Platelet Volume may be Reflects the Disease Activity of Ulcerative Colitis. Eur J Gen Med 2010; 7: 259-263
43. Liu S, Ren J, Han G, Wang G, Gu G, Xia Q, Li J. Mean platelet volume: a controversial marker of disease activity in Crohn's disease. Eur J Med Res 2012; 17: 27 [PMID: 23058104 DOI: 10.1186/2047-783X-17-27]
44. Kayahan H, Akarsu M, Ozcan MA, Demir S, Ates H, Unsal B, Akpinar H. Reticulated platelet levels in patients with ul-cerative colitis. Int J Colorectal Dis 2007; 22: 1429-1435 [PMID: 17549498 DOI: 10.1007/s00384-007-0330-y]
45. Öztürk ZA, Dag MS, Kuyumcu ME, Cam H, Yesil Y, Yilmaz N, Aydinli M, Kadayifci A, Kepekci Y. Could platelet indices be new biomarkers for inflammatory bowel diseases? Eur Rev Med Pharmacol Sci 2013; 17: 334-341 [PMID: 23426536]
46. Voudoukis E, Karmiris K, Oustamanolakis P, Theodo-ropoulou A, Sfiridaki A, Paspatis GA, Koutroubakis IE. Association between thrombocytosis and iron deficiency anemia in inflammatory bowel disease. Eur J Gastroenterol Hepatol 2013; 25: 1212-1216 [PMID: 23839158 DOI: 10.1097/ MEG.0b013e328363e354]
47. Gasche C. Anemia in IBD: the overlooked villain. Inflamm Bowel Dis 2000; 6: 142-150; discussion 151 [PMID: 10833075 DOI: 10.1002/ibd.3780060214]
48. Gomollón F, Gisbert JP. Anemia and inflammatory bowel diseases. World J Gastroenterol 2009; 15: 4659-4665 [PMID: 19787829 DOI: 10.3748/wjg.15.4659]
49. Oustamanolakis P, Koutroubakis IE, Messaritakis I, Kefalo-giannis G, Niniraki M, Kouroumalis EA. Measurement of re-ticulocyte and red blood cell indices in the evaluation of anemia in inflammatory bowel disease. J Crohns Colitis 2011; 5: 295-300 [PMID: 21683299 DOI: 10.1016/j.crohns.2011.02.002]
50. Dan K. Thrombocytosis in iron deficiency anemia. Intern Med 2005; 44: 1025-1026 [PMID: 16293910 DOI: 10.2169/in-ternalmedicine.44.1025]
51. Choi SI, Simone JV, Jackson CW. Megakaryocytopoiesis in experimental iron deficiency anemia. Blood 1974; 43: 111-120 [PMID: 4809091]
52. Lordier L, Jalil A, Aurade F, Larbret F, Larghero J, Debili N, Vainchenker W, Chang Y. Megakaryocyte endomitosis is a failure of late cytokinesis related to defects in the contractile ring and Rho/Rock signaling. Blood 2008; 112: 3164-3174 [PMID: 18684864 DOI: 10.1182/blood-2008-03-144956]
53. Choi SI, Simone JV. Platelet production in experimental iron deficiency anemia. Blood 1973; 42: 219-228 [PMID: 4793111]
54. Bilic E, Bilic E. Amino acid sequence homology of thrombo-poietin and erythropoietin may explain thrombocytosis in children with iron deficiency anemia. J Pediatr Hematol Oncol 2003; 25: 675-676 [PMID: 12902931 DOI: 10.1097/00043426-20 0308000-00023]
55. Kulnigg-Dabsch S, Evstatiev R, Dejaco C, Gasche C. Effect of iron therapy on platelet counts in patients with inflammatory bowel disease-associated anemia. PLoS One 2012; 7: e34520 [PMID: 22506024 DOI: 10.1371/journal.pone.0034520]
56. Kulnigg-Dabsch S, Schmid W, Howaldt S, Stein J, Mickisch O, Waldhör T, Evstatiev R, Kamali H, Volf I, Gasche C. Iron deficiency generates secondary thrombocytosis and platelet activation in IBD: the randomized, controlled thromboVIT trial. Infamm Bowel Dis 2013; 19: 1609-1616 [PMID: 23644823 DOI: 10.1097/MIB.0b013e318281f4db]
57. Kadikoylu G, Yavasoglu I, Bolaman Z, Senturk T. Platelet parameters in women with iron deficiency anemia. J Natl Med Assoc 2006; 98: 398-402 [PMID: 16573304]
58. Kuku I, Kaya E, Yologlu S, Gokdeniz R, Baydin A. Platelet counts in adults with iron deficiency anemia. Platelets 2009; 20: 401-405 [PMID: 19658005 DOI: 10.1080/095371009031373 06]
59. Collins CE, Cahill MR, Newland AC, Rampton DS. Platelets circulate in an activated state in inflammatory bowel disease. Gastroenterology 1994; 106: 840-845 [PMID: 8143990]
60. Collins CE, Rampton DS, Rogers J, Williams NS. Platelet aggregation and neutrophil sequestration in the mesenteric circulation in inflammatory bowel disease. Eur J Gastroenterol Hepatol 1997; 9: 1213-1217 [PMID: 9471028]
61. Senzel L, Gnatenko DV, Bahou WF. The platelet proteome. Curr Opin Hematol 2009; 16: 329-333 [PMID: 19550320 DOI: 10.1097/MOH.0b013e32832e9dc6]
62. Danese S, de la Motte C, Sturm A, Vogel JD, West GA, Strong SA, Katz JA, Fiocchi C. Platelets trigger a CD40-dependent inflammatory response in the microvasculature of inflammatory bowel disease patients. Gastroenterol-ogy 2003; 124: 1249-1264 [PMID: 12730866 DOI: 10.1016/ S0016-5085(03)00289-0]
63. Magro F, Araujo F, Pereira P, Meireles E, Diniz-Ribeiro M, Velosom FT. Soluble selectins, sICAM, sVCAM, and angio-genic proteins in different activity groups of patients with inflammatory bowel disease. Dig Dis Sci 2004; 49: 1265-1274 [PMID: 15387356 DOI: 10.1023/B:DDAS.0000037822.55717.31]
64. Celi A, Pellegrini G, Lorenzet R, De Blasi A, Ready N, Furie BC, Furie B. P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci USA 1994; 91: 8767-8771 [PMID: 7522321 DOI: 10.1073/pnas.91.19.8767]
65. Scaldaferri F, Lancellotti S, Pizzoferrato M, De Cristofaro R. Haemostatic system in inflammatory bowel diseases: new players in gut inflammation. World J Gastroenterol 2011; 17: 594-608 [PMID: 21350708 DOI: 10.3748/wjg.v17.i5.594]
66. Russo S, Bussolati B, Deambrosis I, Mariano F, Camussi G. Platelet-activating factor mediates CD40-dependent angio-genesis and endothelial-smooth muscle cell interaction. J Immunol 2003; 171: 5489-5497 [PMID: 14607955]
67. Danese S, Katz JA, Saibeni S, Papa A, Gasbarrini A, Vecchi M, Fiocchi C. Activated platelets are the source of elevated levels of soluble CD40 ligand in the circulation of infamma-tory bowel disease patients. Gut 2003; 52: 1435-1441 [PMID: 12970136 DOI: 10.1136/gut.52.10.1435]
68. Anand SX, Viles-Gonzalez JF, Badimon JJ, Cavusoglu E, Marmur JD. Membrane-associated CD40L and sCD40L in atherothrombotic disease. Thromb Haemost 2003; 90: 377-384 [PMID: 12958605]
69. Koutroubakis IE, Theodoropoulou A, Xidakis C, Sfiridaki A, Notas G, Kolios G, Kouroumalis EA. Association between enhanced soluble CD40 ligand and prothrombotic state in inflammatory bowel disease. Eur J Gastroenterol Hepatol 2004; 16: 1147-1152 [PMID: 015489574 DOI: 10.1097/00042737-2004 11000-00011]
70. Prasad KS, Andre P, Yan Y, Phillips DR. The platelet CD40L/GP IIb-IIIa axis in atherothrombotic disease. Curr Opin Hematol 2003; 10: 356-361 [PMID: 12913790 DOI: 10.109 7/00062752-200309000-00006]
71. Danese S, Scaldaferri F, Vetrano S, Stefanelli T, Graziani C, Repici A, Ricci R, Straface G, Sgambato A, Malesci A, Fiocchi C, Rutella S. Critical role of the CD40 CD40-ligand pathway in regulating mucosal inflammation-driven angiogenesis in inflammatory bowel disease. Gut 2007; 56: 1248-1256 [PMID: 17317789 DOI: 10.1136/gut.2006.111989]
72. Cognasse F, Hamzeh-Cognasse H, Lafarge S, Chavarin P, Cogné M, Richard Y, Garraud O. Human platelets can activate peripheral blood B cells and increase production of immunoglobulins. Exp Hematol 2007; 35: 1376-1387 [PMID: 17656005 DOI: 10.1016/j.exphem.2007.05.021]
73. Borcherding F, Nitschke M, Hundorfean G, Rupp J, von Smolinski D, Bieber K, van Kooten C, Lehnert H, Fellermann K, Büning J. The CD40-CD40L pathway contributes to the proinflammatory function of intestinal epithelial cells in in-fammatory bowel disease. Am J Pathol 2010; 176: 1816-1827 [PMID: 20133813 DOI: 10.2353/ajpath.2010.090461]
74. Vowinkel T, Anthoni C, Wood KC, Stokes KY, Russell J, Gray L, Bharwani S, Senninger N, Alexander JS, Krieglstein CF, Grisham MB, Granger DN. CD40-CD40 ligand mediates the recruitment of leukocytes and platelets in the inflamed murine colon. Gastroenterology 2007; 132: 955-965 [PMID: 17324402 DOI: 10.1053/j.gastro.2006.12.027]
75. Dhillon AP, Anthony A, Sim R, Wakefeld AJ, Sankey EA, Hudson M, Allison MC, Pounder RE. Mucosal capillary thrombi in rectal biopsies. Histopathology 1992; 21: 127-133 [PMID: 1505929 DOI: 10.1111/j.1365-2559.1992.tb00360.x]
76. Miehsler W, Reinisch W, Valic E, Osterode W, Tillinger W, Feichtenschlager T, Grisar J, Machold K, Scholz S, Vogelsang H, Novacek G. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut 2004; 53: 542-548 [PMID: 15016749 DOI: 10.1136/ gut.2003.025411]
77. Koutroumpakis EI, Tsiolakidou G, Koutroubakis IE. Risk of venous thromboembolism in patients with inflammatory bowel disease. Semin Thromb Hemost 2013; 39: 461-468 [PMID: 23629820 DOI: 10.1055/s-0033-1343886]
78. Talbot RW, Heppell J, Dozois RR, Beart RW. Vascular complications of inflammatory bowel disease. Mayo Clin Proc 1986; 61: 140-145 [PMID: 3080643 DOI: 10.1016/ S0025-6196(12)65200-8]
79. Jackson LM, O'Gorman PJ, O'Connell J, Cronin CC, Cotter KP, Shanahan F. Thrombosis in inflammatory bowel disease: clinical setting, procoagulant profile and factor V Leiden. QJM 1997; 90: 183-188 [PMID: 9093595 DOI: 10.1093/ qjmed/90.3.183]
80. Irving PM, Macey MG, Shah U, Webb L, Langmead L, Rampton DS. Formation of platelet-leukocyte aggregates in inflammatory bowel disease. Infamm Bowel Dis 2004; 10: 361-372 [PMID: 15475744 DOI: 10.1097/00054725-200407000-00007]
81. Irving PM, Macey MG, Feakins RM, Knowles CH, Frye JN, Liyanage SH, Dorudi S, Williams NS, Rampton DS. Platelet-leucocyte aggregates form in the mesenteric vascu-lature in patients with ulcerative colitis. Eur J Gastroenterol Hepatol 2008; 20: 283-289 [PMID: 18334871 DOI: 10.1097/ MEG.0b013e3282f246c2]
82. Irving PM, Pasi KJ, Rampton DS. Thrombosis and infamma-tory bowel disease. Clin Gastroenterol Hepatol 2005; 3: 617-628 [PMID: 16206491 DOI: 10.1016/S1542-3565(05)00154-0]
83. Peters MJ, Dixon G, Kotowicz KT, Hatch DJ, Heyderman RS, Klein NJ. Circulating platelet-neutrophil complexes represent a subpopulation of activated neutrophils primed for adhesion, phagocytosis and intracellular killing. Br J Haematol 1999; 106: 391-399 [PMID: 10460597 DOI: 10.1046/ j.1365-2141.1999.01553.x]
84. Michelson AD, Barnard MR, Krueger LA, Valeri CR, Fur-man MI. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001; 104: 1533-1537 [PMID: 11571248 DOI: 10.1161/hc3801.095588]
85. Nieuwland R, Sturk A. Why do cells release vesicles? Thromb Res 2010; 125 Suppl 1: S49-S51 [PMID: 20149923 DOI: 10.1016/j.thromres.2010.01.037]
86. Montoro-García S, Shantsila E, Marín F, Blann A, Lip GY. Circulating microparticles: new insights into the biochemical basis of microparticle release and activity. Basic Res Cardiol 2011; 106: 911-923 [PMID: 21691898 DOI: 10.1007/ s00395-011-0198-4]
87. Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS, Weinblatt ME, Massarotti EM, Remold-O'Donnell E, Farn-dale RW, Ware J, Lee DM. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327: 580-583 [PMID: 20110505 DOI: 10.1126/sci-ence.1181928]
88. Horstman LL, Ahn YS. Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol 1999; 30: 111-142 [PMID: 10439058 DOI: 10.1016/S1040-8428(98)00044-4]
89. Flaumenhaft R, Dilks JR, Richardson J, Alden E, Patel-Hett SR, Battinelli E, Klement GL, Sola-Visner M, Italiano JE. Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 2009; 113: 1112-1121 [PMID: 18802008 DOI: 10.1182/ blood-2008-06-163832]
90. Oyabu C, Morinobu A, Sugiyama D, Saegusa J, Tanaka S, Morinobu S, Tsuji G, Kasagi S, Kawano S, Kumagai S. Plasma platelet-derived microparticles in patients with connective tissue diseases. J Rheumatol 2011; 38: 680-684 [PMID: 21239749 DOI: 10.3899/jrheum.100780]
91. Tamagawa-Mineoka R, Katoh N, Kishimoto S. Platelet activation in patients with psoriasis: increased plasma levels of platelet-derived microparticles and soluble P-selectin. J Am Acad Dermatol 2010; 62: 621-626 [PMID: 19962788 DOI: 10.1016/j.jaad.2009.06.053]
92. Sellam J, Proulle V, Jüngel A, Ittah M, Miceli Richard C, Gottenberg JE, Toti F, Benessiano J, Gay S, Freyssinet JM, Mariette X. Increased levels of circulating microparticles in primary Sjögren's syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity. Arthritis Res Ther 2009; 11: R156 [PMID: 19832990 DOI: 10.1186/ar2833]
93. Nomura S, Uehata S, Saito S, Osumi K, Ozeki Y, Kimura Y. Enzyme immunoassay detection of platelet-derived microparticles and RANTES in acute coronary syndrome. Thromb Haemost 2003; 89: 506-512 [PMID: 12624635]
94. Inami N, Nomura S, Kikuchi H, Kajiura T, Yamada K, Na-kamori H, Takahashi N, Tsuda N, Hikosaka M, Masaki M, Iwasaka T. P-selectin and platelet-derived microparticles associated with monocyte activation markers in patients with pulmonary embolism. Clin Appl Thromb Hemost 2003; 9: 309-316 [PMID: 14653440 DOI: 10.1177/107602960300900406]
95. Nomura S, Imamura A, Okuno M, Kamiyama Y, Fujimura Y, Ikeda Y, Fukuhara S. Platelet-derived microparticles in patients with arteriosclerosis obliterans: enhancement of high shear-induced microparticle generation by cytokines. Thromb Res 2000; 98: 257-268 [PMID: 10822072 DOI: 10.1016/ S0049-3848(00)00186-9]
96. Nadaud S, Poirier O, Girerd B, Blanc C, Montani D, Eyries M, Imbert-Bismut F, Pacheco A, Vigne J, Tregouet DA, Humbert M, Soubrier F. Small platelet microparticle levels are increased in pulmonary arterial hypertension. Eur J Clin Invest 2013; 43: 64-71 [PMID: 23176388 DOI: 10.1111/eci.12018]
97. Taube J, McWilliam N, Luddington R, Byrne CD, Baglin T. Activated protein C resistance: effect of platelet activation, platelet-derived microparticles, and atherogenic lipopro-teins. Blood 1999; 93: 3792-3797 [PMID: 10339485]
98. Nomura S, Okamae F, Abe M, Hosokawa M, Yamaoka M, Ohtani T, Onishi S, Matsuzaki T, Teraoka A, Ishida T, Fuku-hara S. Platelets expressing P-selectin and platelet-derived microparticles in stored platelet concentrates bind to PSGL-1 on filtrated leukocytes. Clin Appl Thromb Hemost 2000; 6: 213-221 [PMID: 11030527 DOI: 10.1177/107602960000600406]
99. Andoh A, Tsujikawa T, Hata K, Araki Y, Kitoh K, Sasaki M, Yoshida T, Fujiyama Y. Elevated circulating platelet-derived microparticles in patients with active inflammatory bowel disease. Am J Gastroenterol 2005; 100: 2042-2048 [PMID: 16128950 DOI: 10.1111/j.1572-0241.2005.50381.x]
100. Chamouard P, Desprez D, Hugel B, Kunzelmann C, Gidon-Jeangirard C, Lessard M, Baumann R, Freyssinet JM, Grune-baum L. Circulating cell-derived microparticles in Crohn's disease. Dig Dis Sci 2005; 50: 574-580 [PMID: 15810645 DOI: 10.1007/s10620-005-2477-0]
101. Palkovits J, Novacek G, Kollars M, Hron G, Osterode W, Quehenberger P, Kyrle PA, Vogelsang H, Reinisch W, Papay P, Weltermann A. Tissue factor exposing microparticles in inflammatory bowel disease. J Crohns Colitis 2013; 7: 222-229 [PMID: 22705067 DOI: 10.1016/j.crohns.2012.05.016]
102. Davì G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med 2007; 357: 2482-2494 [PMID: 18077812 DOI: 10.1056/NEJMra071014]
103. Storey RF, Husted S, Harrington RA, Heptinstall S, Wil-cox RG, Peters G, Wickens M, Emanuelsson H, Gurbel P, Grande P, Cannon CP. Inhibition of platelet aggregation by AZD6140, a reversible oral P2Y12 receptor antagonist, compared with clopidogrel in patients with acute coronary syndromes. J Am Coll Cardiol 2007; 50: 1852-1856 [PMID: 17980251 DOI: 10.1016/j.jacc.2007.07.058]
104. Storey RF, Judge HM, Wilcox RG, Heptinstall S. Inhibition of ADP-induced P-selectin expression and platelet-leukocyte conjugate formation by clopidogrel and the P2Y12 receptor antagonist AR-C69931MX but not aspirin. Thromb Haemost 2002; 88: 488-494 [PMID: 12353080]
105. Storey RF, Wilcox RG, Heptinstall S. Comparison of the pharmacodynamic effects of the platelet ADP receptor antagonists clopidogrel and AR-C69931MX in patients with ischaemic heart disease. Platelets 2002; 13: 407-413 [PMID: 12487788 DOI: 10.1080/0953710021000024402]
106. Patel SH, Rachchh MA, Jadav PD. Evaluation of anti-inflam-matory effect of anti-platelet agent-clopidogrel in experimentally induced inflammatory bowel disease. Indian J Pharmacol 2012; 44: 744-748 [PMID: 23248405 DOI: 10.4103/0253-7613]
107. Carty E, MacEy M, Rampton DS. Inhibition of platelet activation by 5-aminosalicylic acid in inflammatory bowel disease. Aliment Pharmacol Ther 2000; 14: 1169-1179 [PMID: 10971234 DOI: 10.1046/j.1365-2036.2000.00824.x]
108. Tan VP, Chung A, Yan BP, Gibson PR. Venous and arterial disease in inflammatory bowel disease. J Gastroenterol Hepatol 2013; 28: 1095-1113 [PMID: 23662785 DOI: 10.1111/jgh.12260]
109. Thomas G, Skrinska VA, Lucas FV. The influence of glu-tathione and other thiols on human platelet aggregation. Thromb Res 1986; 44: 859-866 [PMID: 3099423 DOI: 10.1016/0 049-3848(86)90031-9]
110. Nannizzi-Alaimo L, Alves VL, Phillips DR. Inhibitory effects of glycoprotein IIb/IIIa antagonists and aspirin on the release of soluble CD40 ligand during platelet stimulation. Circulation 2003; 107: 1123-1128 [PMID: 12615789 DOI: 10.1161/01.CIR.0000053559.46158.AD]
111. Danese S, Sans M, Scaldaferri F, Sgambato A, Rutella S, Cit-tadini A, Piqué JM, Panes J, Katz JA, Gasbarrini A, Fiocchi C. TNF-alpha blockade down-regulates the CD40/CD40L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infiximab in Crohn's disease. J Immunol 2006; 176: 2617-2624 [PMID: 16456024]
112. André P, Prasad KS, Denis CV, He M, Papalia JM, Hynes RO, Phillips DR, Wagner DD. CD40L stabilizes arterial thrombi by a beta3 integrin--dependent mechanism. Nat Med 2002; 8: 247-252 [PMID: 11875495 DOI: 10.1038/nm0302-247]
113. Mori M, Salter JW, Vowinkel T, Krieglstein CF, Stokes KY, Granger DN. Molecular determinants of the prothrombo-genic phenotype assumed by inflamed colonic venules. Am J Physiol Gastrointest Liver Physiol 2005; 288: G920-G926 [PMID: 15550557 DOI: 10.1152/ajpgi.00371.2004]