Eosinophilia and thrombophilia in churg strauss syndrome: A clinical and pathogenetic overview

Clinical and Applied Thrombosis/Hemostasis

Volumn 16, Issue 6, 2010, Pages 628-636

  Ames, Paul R J ^a   Margaglione, Maurizio ^b   MacKie, Sara ^c   Delgado Alves, José ^d  

^a AIREDALE GENERAL HOSPITAL   (United Kingdom)

^b UNIVERSITY OF FOGGIA   (Italy)

^c CHAPEL ALLERTON HOSPITAL   (United Kingdom)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

clinical thrombophilia; hypercoagulability; venous thromboembolism

Indexed keywords

ANTICOAGULANT AGENT; ANTITHROMBOCYTIC AGENT; AZATHIOPRINE; BLOOD CLOTTING FACTOR 12; CHARCOT LEYDEN CRYSTAL PROTEIN; CYCLOPHOSPHAMIDE; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL PEROXIDASE; INTERCELLULAR ADHESION MOLECULE 1; MAJOR BASIC PROTEIN; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; MYELOBLASTIN; NEUTROPHIL CYTOPLASMIC ANTIBODY; PROTEIN; PROTEIN C; STEROID; THROMBIN; THROMBOCYTE ACTIVATING FACTOR; THROMBOPLASTIN; UNCLASSIFIED DRUG;

ACUTE CORONARY SYNDROME; ANGINA PECTORIS; ANTIBODY BLOOD LEVEL; ANTICOAGULATION; ARTERY OCCLUSION; ARTICLE; BLOOD CLOTTING; BRAIN ISCHEMIA; BUDD CHIARI SYNDROME; CHURG STRAUSS SYNDROME; EMBASE; ENDOTHELIUM CELL; EOSINOPHIL; EOSINOPHILIA; HUMAN; HYPEREOSINOPHILIC SYNDROME; INFERIOR CAVA VEIN OBSTRUCTION; LUNG EMBOLISM; LUNG INFARCTION; MEDLINE; PATHOGENESIS; PRIORITY JOURNAL; SYSTEMATIC REVIEW; THROMBOCYTE ACTIVATION; THROMBOPHILIA; VASOSPASM; VEIN OCCLUSION; VENOUS THROMBOEMBOLISM;

ADOLESCENT; ADULT; AGED; CHURG-STRAUSS SYNDROME; EOSINOPHILIA; FEMALE; HUMANS; MALE; MIDDLE AGED; THROMBOPHILIA; THROMBOSIS; YOUNG ADULT;

EID: 78650334234     PISSN: 10760296     EISSN: None     Source Type: Journal    
DOI: 10.1177/1076029609348647     Document Type: Article

References (114)

1. Masi AT, Hunder GG, Lie JT, et al. The American College of Rheumatology 1990 criteria for the classification of Churg-Strauss syndrome. Arthritis Rheum. 1990 ; 33 (8). 1094-1100.
2. Churg J., Strauss L. Allergic granulomatosis, allergic angiitis and periarteritis nodosa. Am J Pathol. 1951 ; 27 (2). 277-301.
3. Lanham JG, Elkon KB, Pusey CD, Hughes GR Systemic vasculitis with asthma and eosinophilia: a clinical approach to the Churg-Strauss syndrome. Medicine (Baltimore). 1984 ; 63 (2). 65-81.
4. Jennette JC, Flak RJ, Andrassy K., et al. Nomenclature of systemic vasculitides. Proposal of an international consensus conference. Arthritis Rheum. 1994 ; 37 (2). 187-192.
5. Engfeldt B., Zetterstrom R. Disseminated eosinophilic collagen disease; a clinical and pathological study of a clinical entity related to Löffler's syndromes. Acta Med Scand. 1956 ; 153 (5). 337-353.
6. Pierce LE, Hosseinian AH, Constantine AB Disseminated eosinophilic collagen disease. Blood. 1967 ; 29 (4). 540-549.
7. Bousser J. Eosinophilie et leucemie. Sang. 1957 ; 28 (6). 553.
8. Ishii T., Koide O., Hosoda Y., Takahashi R. Hypereosinophilic multiple thrombosis. A proposal of a new designation of disseminated eosinophilic ''collagen disease''. Angiology. 1977 ; 28 (6). 361-375.
9. Ames PRJ, Froes L., Lupoli S., et al. Thrombosis in Churg-Strauss syndrome. Beyond vasculitis ? Br J Rheumatology. 1996 ; 35 (11). 1181-1183.
10. Chumbley LC, Harrison EG Jr, DeRemee RA Allergic granulomatosis and angiitis (Churg-Strauss syndrome). Report and analysis of 30 cases. Mayo Clin Proc. 1977 ; 52 (8). 477-484.
11. Morgan JM, Raposo L., Gibson DG Cardiac involvement in Churg-Strauss syndrome shown by echocardiography. Br Heart J. 1989 ; 62 (6). 462-466.
12. Gaskin G., Clutterbuck EJ, Pusey CD Renal disease in the Churg-Strauss syndrome. Diagnosis, management and outcome. Contrib Nephrol. 1991 ; 94: 58-65.
13. Abu-Shakra M., Smythe H., Lewtas J., Badley E., Weber D., Keystone E. Outcome of polyarteritis nodosa and Churg-Strauss syndrome. An analysis of twenty-five patients. Arthritis Rheum. 1994 ; 37 (12). 1798-1803.
14. Sehgal M., Swanson JW, De Remee TV Neurological manifestations of Churg Strauss syndrome. Mayo Clin Proc. 1995 ; 70 (4). 337-341.
15. Guillevin L., Cohen P., Gayraud M., Lhote F., Jarrousse B., Casassus P. Churg-Strauss syndrome. Clinical study and long-term follow-up of 96 patients. Medicine (Baltimore). 1999 ; 78 (1). 26-37.
16. Kang DW, Jeong IK, Kim HJ, et al. Neurologic Manifestations of Churg-Strauss syndrome. J Korean Neurol Assoc. 1999 ; 17 (6). 836-840.
17. Solans R., Bosch JA, Perez-Bocanegra C., et al. Churg-Strauss syndrome: outcome and long term follow up of 32 patients. Rheumatol. 2001 ; 40 (7). 763-771.
18. Della Rossa A., Baldini C., Tavoni A., et al. Churg-Strauss syndrome: clinical and serological features of 19 patients from a single Italian centre. Rheumatology. 2002 ; 41 (11). 1286-1294.
19. Hattori N., Mori K., Misu K., Koike H., Ichimura M., Sobue G. Mortality and morbidity in peripheral neuropathy associated Churg-Strauss syndrome and microscopic polyangiitis. J Rheumatol. 2002 ; 29 (7). 1408-1414.
20. Keogh KA Churg-Strauss syndrome: clinical presentations, antineutrophil cytoplasmic antibodies and leukotriene receptor antagonists. Am J Med. 2003 ; 115 (4). 284-290.
21. Garcia G., Achouh L., Cobarzan D., Fichet D., Humbert M. Severe venous thromboembolic disease in Churg-Strauss syndrome. Allergy. 2005 ; 60 (3). 409-410.
22. Lane SE, Watts RA, Shepstone L., Scott DG Primary systemic vasculitis: clinical features and mortality. QJM. 2005 ; 98 (2). 97-111.
23. Oh MJ, Lee JY, Kwon NH, Choi DC Churg-Strauss syndrome: the clinical features and long-term follow-up of 17 patients. J Korean Med Sci. 2006 ; 21 (2). 265-271.
24. Pelà G., Tirabassi G., Pattoneri P., Pavone L., Garini G., Bruschi G. Cardiac involvement in the Churg-Strauss syndrome. Am J Cardiol. 2006 ; 97 (10). 1519-1524.
25. Chen YX, Yu HJ, Zhang W., et al. Analyzing fatal cases of chinese patients with primary antineutrophil cytoplasmic antibodies-associated renal vasculitis: a 10 year retrospective study. Kidney Blood Press Res. 2008 ; 31 (5). 343-349.
26. Allenbach Y., Seror R., Pagnoux C., et al. High frequency of venous thromboembolic events in Churg-Strauss syndrome, Wegener's granulomatosis and microscopic polyangiitis but not polyarteritis nodosa: a systematic retrospective study on 1130 patients. Ann Rheum Dis. 2009 ; 68 (4). 564-567.
27. Dinç A., Soy M., Pay S., Simsek I., Erdem H., Sobaci G. A case of Churg-Strauss syndrome presenting with cortical blindness. Clin Rheumatol. 2000 ; 19 (4). 318-320.
28. Kok J., Bosseray A., Brion JP, Micoud M., Besson G. Chorea in a child with Churg-Strauss syndrome. Stroke. 1993 ; 24 (8). 1263-1264.
29. Sonneville R., Lagrange M., Guidoux C., et al. The association of cardiac involvement and ischemic stroke in Churg Strauss syndrome. Rev Neurol (Paris). 2006 ; 162 (2). 229-232.
30. Teresa Sartori M., Briani C., Munari M., Amistà P., Pagnan A., Zampieri P. Cerebral venous thrombosis as a rare onset of Churg-Strauss syndrome. Thromb Haemost. 2006 ; 96 (1). 90-92.
31. Ikemoto Y., Kohdera U., Uraoka M., Teraguchi M., Okamura A., Kobayashi Y. Pulmonary infarction and deep venous thrombosis in a 13-year-old boy with Churg-Strauss syndrome. Pediatr Int. 2001 ; 43 (4). 441-443.
32. Sieminska A., Damps-Konstanska I., Kuziemski K., et al. Fatal course of Churg-Strauss disease. Adv Palliat Med. 2007 ; 32 (6). 115-117.
33. Damps-Konstaska I., Siemiska A., Górska L., et al. Case report of Churg-Strauss syndrome-signs and symptoms suggesting disseminated neoplastic disease. Adv Palliat Med. 2008 ; 33 (4). 171-174.
34. Alberts AR, Lasonde R., Ackeman KR, Chartash EK, Susin M., Furie RA Reversible monocular blindness complicating Churg-Strauss syndrome. J Rheumatol. 1994 ; 21 (2). 363-365.
35. Omoto A., Kawahito Y., Muraguchi N., et al. A case report of Churg-Strauss syndrome combined with various vessel diseases. Jpn J Clin Immunol. 2004 ; 27 (6). 420-426.
36. Komarov VT, Olenikov VE, Devina OV, Nikishina AIu, Khichina NS Clinical variants of Churg-Strauss eosinophilic vasculitis. Klin Med (Mosk). 2007 ; 85 (6). 63-66.
37. Campbell CD, Marshall DA A case of Budd-Chiari syndrome presenting in a lady with newly diagnosed Churg-Strauss syndrome. Rheumatology. 2007 ; 46 (5). 890.
38. Abdulwahab A., Almoallim H., Khan N. Isolated eosinophilic mesenteric vasculitis with extensive thrombosis and splenic infarction in a 13-year-old boy. Clin Rheumatol. 2007 ; 26 (2). 254-257.
39. Mizia-Stec K., Gasior Z., Duawa J., et al. Churg-Strauss syndrome and congenital factor Leiden thrombophilia as non-typical causes of intracardiac thrombosis. Heart Vessels. 2006 ; 21 (4). 263-266.
40. León-Ruíz L., Jiménez-Alonso J., Hidalgo-Tenorio C., et al. Churg-Strauss syndrome complicated by endomyocardial fibrosis and intraventricular thrombus. Importance of the echocardiography for the diagnosis of asymptomatic phases of potentially severe cardiac complications. Lupus. 2002 ; 11 (11). 765-767.
41. Schwab J., Schwab M., Manger K., Manger B., Wünsch PH, Gottwik M. Churg-Strauss syndrome with right ventricular tumor. Dtsch Med Wochenschr. 1998 ; 123 (16). 487-492.
42. van Ledden-Klok MJ, Fiselier TJ, Draaisma JM A boy with Churg-Strauss syndrome and thrombosis associated with eosinophilia. Ned Tijdschr Geneeskd. 2006 ; 150 (16). 913-917.
43. Meireles N., Ferreira ME, Castro JS, et al. Churg-Strauss syndrome, femoral venous aneurysms and pulmonary thromboembolism. Rev Port Cir Cardiotorac Vasc. 2003 ; 10 (3). 147-151.
44. Wagner AD, Meyer GP, Rihl M., et al. Acute coronary syndrome associated with Churg-Strauss syndrome. Vasc Health Risk Manag. 2007 ; 3 (5). 775-779.
45. Suzuki N., Arai Y., Miyamoto Y., Isokane N., Fukushima N., Sano Y. Acute myocardial injury and repeated angina pectoris-like attacks in a young patient with Churg-Strauss syndrome. Jpn J Thoracic Dis. 1991 ; 29 (12). 1630-1637.
46. Kozak M., Gill EA, Green LS The Churg-Strauss syndrome. A case report with angiographically documented coronary involvement and a review of the literature. Chest. 1995 ; 107 (2). 578-580.
47. Kubota T., Yamaguchi J., Higashitani M., et al. Survivor of cardiogenic shock following acute myocardial infarction with Churg-Strauss syndrome: first angiographic documention of coronary recanalization of infarct-related arteries: a case report. J Cardiol. 2004 ; 44 (4). 153-159.
48. Kawai T., Mokuo Y., Nagamoto A., et al. A case of Churg-Strauss syndrome presented with bilateral ureteral stenosis and myocardial infarction. Arerugi. 2002 ; 51 (6). 489-492.
49. Buhaescu I., Williams A., Yood R. Rare manifestations of Churg- Strauss syndrome: coronary artery vasospasm, temporal artery vasculitis and reversible monocular blindness-a case report. Clin Rheumatol. 2009 ; 28 (2). 231-233.
50. Lau EW, Carruthers DM, Prasad N. Churg-Strauss syndrome as an unusual cause of spontaneous a-traumatic intra-pericardial thrombosis. Eur J Echocardiogr. 2004 ; 5 (1). 65-67.
51. Weinstein JM, Chui H., Lane S., Corbett J., Towfighi J. Churg-Strauss syndrome (allergic granulomatous angiitis). Neuroophthalmologic manifestations. Arch Ophtalm. 1983 ; 101 (8). 1217-1220.
52. Dagi LR, Currie J. Branch retinal artery occlusion in the Churg-Strauss syndrome. J Clin Neuroophthalmol. 1985 ; 5 (4). 229-237.
53. Granata M., Ammendolea C., Trudu R., Spimpolo N., Martelletti P. Thrombosis of the retinal artery in a patient with Churg-Strauss syndrome. Clin Exp Rheumatol. 2001 ; 19 (2). 234.
54. Udono T., Abe T., Sato H., Tamai M. Bilateral central retinal artery occlusion in Churg-Strauss syndrome. Am J Ophtalmol. 2003 ; 136 (6). 1181-1183.
55. Skrapari I., Kagkelari E., Charitatos E., Pantelidaki C., Gounaris T., Sioula E. Acute painless monocular visual loss due to central retinal artery occlusion in a patient with Churg-Strauss vasculitis. Clin Rheumatol. 2008 ; 27 (1). 125-127.
56. Türkçüolu P., Isik A., Deniz N., Turgut B., Kan EK Central retinal artery occlusion in an ANCA negative Churg-Strauss syndrome patient. Int Ophtalmol. 2007 ; 27 (6). 369-371.
57. Koenig M., Maillard N., Lévy M., N'Guyen F., Cathébras P. Monocular blindness as the first symptom of Churg-Strauss syndrome. Presse Med. 2008 ; 32 (2 pt 1). 235-238.
58. Hoffman PM, Godfrey T., Stawell RJ A case of Churg-Strauss syndrome with visual loss following central retinal artery occlusion. Lupus. 2005 ; 14 (2). 174-175.
59. Bastiaensen LAK, Kienstra G., van Boven W., et al. Churg-Strauss syndrome (allergic granulomatous angiitis) as a cause of central retinal artery occlusion. Neuro Ophtalmology. 1993 ; 13: 227-229.
60. Sutcliffe N., Morris V., Gomperts B., et al. Relationship between the development of blindness in Churg-Strauss syndrome and antimyeloperoxidase antibodies. Brit J Rheumatol. 1997 ; 36 (2). 273-275.
61. Chen SD, Lochhead J., Satchi K., Patel CK, Frith P. Bilateral retinal venous occlusion and unilateral cystoid macular edema in Churg-Strauss syndrome treated with intravitreal triamcinolone. Retina. 2005 ; 25 (5). 655-657.
62. Rosenthal G., Schneck M., Lifshitz T. Branch retinal vein occlusion in Churg-Strauss syndrome. Clin Exp Ophthalmol. 2002 ; 30 (5). 381-382.
63. Hamann S., Johansen S. Combined central retinal artery and vein occlusion in Churg-Strauss syndrome: case report. Acta Ophthalmol Scand. 2006 ; 84 (5). 703-706.
64. De Salvo G., Li Calzi C., Anastasi M., Lodato G. Branch retinal vein occlusion followed by central retinal artery occlusion in Churg-Strauss syndrome: unusual ocular manifestations in allergic granulomatous angiitis. Eur J Ophthalmol. 2009 ; 19 (2). 314-317.
65. Popken-Harris P., McGrogan M., Loegering DA, et al. Expression, purification and characterisation of the recombinant proform of eosinophil granule major basic protein. J Immunol. 1995 ; 155 (3). 1472-1480.
66. Moosbauer C., Morgenstern E., Cuvelier SL, et al. Eosinophils are a major intravascular location for tissue factor storage and exposure. Blood. 2007 ; 109 (3). 995-1002.
67. Popken-Harris P., Checkel J., Loegering D., et al. Regulation and processing of a precursor form of eosinophil granule major basic protein (ProMBP) in differentiating eosinophils. Blood. 1998 ; 92 (2). 623-631.
68. Young JD, Peterson CG, Venge P., Cohn ZA Mechanism of membrane damage mediated by human eosinophil cationic protein. Nature. 1986 ; 321 (6070). 613-616.
69. Kleine TJ, Gleich GJ, Lewis SA Eosinophil major basic protein increases membrane permeability in mammalian urinary bladder epithelium. Am J Physiol Cell Physiol. 1998 ; 275 (1 pt 1). 93-103.
70. Ten RM, Pease LR, McKean DJ, Bell MP, Gleich GJ Molecular cloning of the human eosinophil peroxidase. Evidence for the existence of a peroxidase multigene family. J Exp Med. 1989 ; 169 (5). 1757-1769.
71. Thomas EL, Bozeman PM, Jefferson MM, King CC Oxidation of bromide by the human leukocyte enzymes myeloperoxidase and eosinophil peroxidase. Formation of bromamines. J Biol Chem. 1995 ; 270 (7). 2906-2913.
72. Bussolino F., Silvagno F., Garbarino G., et al. Human endothelial cells are targets for platelet activating factor (PAF). Activation of alpha and beta protein kinase C isozymes in endothelial cells stimulated by PAF. J Biol Chem. 1994 ; 269 (4). 2877-2886.
73. Marzano AV, Tedeschi A., Fanoni D., et al. Activation of blood coagulation in bullous pemphigoid: role of eosinophils, and local and systemic implications. Br J Dermatol. 2009 ; 160 (2). 266-272.
74. Sovershaev MA, Lind KF, Devold H., et al. No evidence for the presence of tissue factor in high-purity preparations of immunologically isolated eosinophils. J Thromb Haemost. 2008 ; 6 (10). 1742-1749.
75. Glich CJ, Frigs E., Loegering DA, Wassom DL, Steinmuller D. Cytotoxic properties of the eosinophil major basic protein. J Immunol. 1979 ; 123 (6). 2925-2927.
76. Venge P., Dahl R., Hilgren R. Enhancement of factor XII dependent reactions by eosinophil cationic protein. Thromb Res. 1979 ; 14 (4-5). 641-649.
77. Ratnoff OD, Gleich GJ, Shurin SB, Kazura J., Everson B., Embury P. Inhibition of the activation of hageman factor (factor XII) by eosinophils and eosinophilic constituents. Am J Hematol. 1993 ; 42 (1). 138-145.
78. Levi M., Hack CE, de Boer JP, Brandjes DP, Büller HR, ten Cate JW Reduction of contact activation related fibrinolytic activity in Factor XII deficient patients. Further evidence for the role of the contact system on fibrinolysis in vivo. J Clin Invest. 1991 ; 88 (4). 1155-1160.
79. Rodeghiero F., Castaman G., Ruggeri M., Cazzavillan M., Ferracin G., Dini E. Fibrinolytic studies in 13 unrelated families with factor XII deficiency. Haematologica. 1991 ; 76 (1). 28-32.
80. Girolami A., Randi ML, Gavasso S., et al. The occasional venous thromboses seen in patients with severe (homozygous) FXII deficiency are probably due to associated risk factors: a study of prevalence in 21 patients and review of the literature. J Thromb Thrombolysis. 2004 ; 17 (2). 139-143.
81. Fredens K., Dahl R., Venge P. In vitro studies of the interaction between heparin and eosinophil cationic protein. Allergy. 1991 ; 46 (1). 27-29.
82. Slungaard A., Vercellotti GM, Tran T., Gleich GJ, Key NS Eosinophil cationic granule proteins impair thrombomodulin function. A potential mechanism for thromboembolism in hypereosinophilic heart disease. J Clin Invest. 1993 ; 91 (4). 1721-1730.
83. Mukai HY, Ninomiya H., Ohtani K., Nagasawa T., Abe T. Major basic protein binding to thrombomodulin potentially contributes to the thrombosis in patients with eosinophilia. Br J Haematol. 1995 ; 90 (4). 892-899.
84. Vazquez JJ, Fernandez Pavon A., Arnalich F., et al. Coagulation abnormalities in patients with eosinophilia. Postgrad Med J. 1987 ; 63 (745). 943-945.
85. Lippi G., Montagnana M., Salvagno GL, Franchini M., Targher G., Guidi GC Eosinophilia and first-line coagulation testing. J Thromb Thrombolysis. 2009 ; 28 (1). 90-93.
86. Mayet WJ, Csernok E., Szymkowiak C., Gross WL, Meyer zum Büschenfelde KH Human endothelial cells express proteinase 3, the target antigen of anticytoplasmic antibodies in Wegener's granulomatosis. Blood. 1993 ; 82 (4). 1221-1229.
87. De Bandt M., Meyer O., Dacosta L., Elbim C., Pasquier C. Anti-proteinase-3 (PR3) antibodies (C-ANCA) recognize various targets on the human umbilical vein endothelial cell (HUVEC) membrane. Clin Exp Immunol. 1999 ; 115 (2). 362-368.
88. Molet S., Gosset P., Vanhee D., et al. Modulation of cell adhesion molecules on human endothelial cells by eosinophil-derived mediators. J Leukoc Biol. 1998 ; 63 (3). 351-358.
89. Costa JJ, Matossian K., Resnick MB, et al. Human eosinophils can express the cytokines tumor necrosis factor-alpha and macrophage inflammatory protein-1 alpha. Clin Invest. 1993 ; 91 (6). 2673-2684.
90. Wang JG, Mahmud SA, Thompson JA, Geng JG, Key NS, Slungaard A. The principal eosinophil peroxidase product, HOSCN, is a uniquely potent phagocyte oxidant inducer of endothelial cell tissue factor activity: a potential mechanism for thrombosis in eosinophilic inflammatory states. Blood. 2006 ; 107 (2). 558-565.
91. Rucinski B., Niewiarowski S., Strzyzewski M., Holt JC, Mayo KH Human platelet 4 and its C-terminal peptides: heparin binding and clearance from the circulation. Thromb Haemost. 1990 ; 63 (3). 493-498.
92. Slungaard A., Vercellotti GM, Walker G., et al. Tumour necrosis factor alpha/cachectin stimulates eosinophil oxidant production and toxicity towards human endothelium. J Exp Med. 1990 ; 171 (6). 2025-2041.
93. Kroegel C., Matthys H. Platelet-activating factor-induced human eosinophil activation. Generation and release of cyclooxygenase metabolites in human blood eosinophils from asthmatics. Immunology. 1993 ; 78 (2). 279-285.
94. Seguchi M., Nakajima S. Induction of ICAM-1 expression on the eosinophilic leukemia cell line-3 (EoL-3) by platelet-activating factor and platelet factor 4. Ann Allergy Asthma Immunol. 1995 ; 74 (3). 255-257.
95. Tezono K., Sarker KP, Kikuchi H., Nasu M., Kitajima I., Maruyama I. Bioactivity of the vascular endothelial growth factor trapped in fibrin clots: production of IL-6 and IL-8 in monocytes by fibrin clots. Haemostasis. 2001 ; 31 (2). 71-79.
96. Sablé-Fourtassou R., Cohen P., Mahr A., et al. Antineutrophil cytoplasmic antibodies and the Churg-Strauss syndrome. Ann Intern Med. 2005 ; 143 (9). 632-638.
97. Sinico RA, Di Toma L., Maggiore U., et al. Prevalence and clinical significance of antineutrophil cytoplasmic antibodies in Churg-Strauss syndrome. Arthritis Rheum. 2005 ; 52 (9). 2926-2935.
98. Stassen PM, Derks RPH, Kallenberg CGM, Stegeman CA Venous thromboembolism in ANCA-associated vasculitis-incidence and risk factors. Rheumatology. 2008 ; 47 (4). 530-535.
99. Engelmann B., Luther T., Müller I. Intravascular tissue factor pathway: a model for rapid initiation of coagulation within the blood vessel. Thromb Haemost. 2003 ; 89 (1). 3-8.
100. Chen KR, Su WP, Pittelkow MR, Conn DL, George T., Leiferman KM Eosinophilic vasculitis in connective tissue disease. J Am Acad Dermatol. 1996 ; 35 (2 pt 1). 173-182.
101. Yamamoto H., Ninomiya H., Yoshimatsu K., et al. Serum levels of major basic protein in patients with or without eosinophilia: measurement by enzyme-linked immunosorbent assay. Br J Haematol. 1994 ; 86 (3). 490-495.
102. Wassom DL, Loegering DA, Solley GO, et al. Elevated serum levels of the eosinophil granule major basic protein in patients with eosinophilia. J Clin Invest. 1981 ; 67 (3). 651-661.
103. Schmitt WH, Csernok E., Kobayashi S., Klinkenborg A., Rein-hold-Keller E., Gross WL Churg-Strauss syndrome: serum markers of lymphocyte activation and endothelial damage. Arthritis Rheum. 1998 ; 41 (3). 445-452.
104. Mitsuyama H., Matsuyama W., Iwakawa J., et al. Increased serum vascular endothelial growth factor level in Churg-Strauss syndrome. Chest. 2006 ; 129 (2). 407-411.
105. Ogbogu P., Rosing DR, Horne MK III. Cardiovascular manifestations of hypereosinophilic syndromes. Immunol Allergy Clin North Am. 2007 ; 27 (3). 457-475.
106. Spry CJ, Davies J., Tay PC, Olsen EG, Oakley CM, Goodwin JF Clinical features of 15 patients with hypereosinophilic syndrome. Q J Med. 1983 ; 52 (205). 1-22.
107. Ames PRJ, Aloj G., Gentile F. Eosinophilia and thrombosis in parasitic diseases: a brief overview. Clin Appl Thromb Haemost. In press.
108. Ames PRJ, Aye WW Pleural mesothelioma and venous thrombosis: the eosinophilia link. Thromb J. 2008 ; 6: 3-5.
109. Williams E., Smart SC, Go RS Catastrophic thromboembolism in a patient with acute lymphoblastic leukaemia and hypereosinophilia. Haematologica. 2004 ; 89 (4). 15.
110. Iriuchishima H., Ogawa Y., Hoshino T., et al. Chronic eosinophilic leukemia with symptoms resembling Budd-Chiari syndrome due to liver infiltration. Rinsho Ketsueki. 2007 ; 48 (6). 505-509.
111. Ames PRJ. Recurrent abdominal thrombosis despite heparin thromboprophylaxis in a patient with transient eosinophilia. Clin Appl Thromb Hemost. In press.
112. Phillip R., Luqmani R. Mortality in systemic vasculitis: a systematic review. Clin Exp Rheumatol. 2008 ; 26 (5 suppl 51). S94 - S104.
113. Takahashi T., Kikuchi A., Kuroda H., Fujihara K., Itoyama Y. Remarkable effect of anticoagulation therapy in Churg-Strauss syndrome-associated neuropathy: a case report. Eur J Neurol. 2006 ; 13 (7). e12.
114. Vignoli A., Marchetti M., Balducci D., Barbui T., Falanga A. Differential effect of the low-molecular-weight heparin, dalteparin, and unfractionated heparin on microvascular endothelial cell haemostatic properties. Haematologica. 2006 ; 91 (2). 207-214.