ADAMTS-13 assays in thrombotic thrombocytopenic purpura

Journal of Thrombosis and Haemostasis

Volumn 8, Issue 4, 2010, Pages 631-640

  Peyvandi, F ^a,b   Palla, R ^a   Lotta, L A ^a   Mackie, I ^b   Scully, M A ^b   Machin, S J ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

ADAMTS 13; Assays; Clinical utility; Standardization

Indexed keywords

AUTOANTIBODY; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ANTIPHOSPHOLIPID SYNDROME; AUTOIMMUNE HEMOLYTIC ANEMIA; CHROMOSOME 9Q; DIFFERENTIAL DIAGNOSIS; DISSEMINATED INTRAVASCULAR CLOTTING; ECLAMPSIA; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRAIT; HELLP SYNDROME; HEMOLYTIC UREMIC SYNDROME; HUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PREECLAMPSIA; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; STANDARDIZATION; THROMBOCYTOPENIA; THROMBOTIC THROMBOCYTOPENIC PURPURA; WESTERN BLOTTING;

ADAM PROTEINS; AUTOANTIBODIES; BIOLOGICAL MARKERS; CLINICAL ENZYME TESTS; DIAGNOSIS, DIFFERENTIAL; HUMANS; IMMUNOASSAY; PREDICTIVE VALUE OF TESTS; PURPURA, THROMBOTIC THROMBOCYTOPENIC; REAGENT KITS, DIAGNOSTIC;

EID: 77952734070     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2010.03761.x     Document Type: Review

References (67)

1. Sadler JE. Von Willebrand factor, ADAMTS-13, and thrombotic thrombocytopenic purpura. Blood 2008, 112:11-8.
2. Tsai HM, Lian EC. Antibodies to von Willebrand factor cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med 1998, 339:1585-9.
3. Furlan M, Robles R, Galbusera M, Remuzzi G, Kyrle PA, Brenner B, Krause M, Scharrer I, Aumann V, Mittler U, Solenthaler M, Lämmle B. von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura and the hemolytic-uremic syndrome. N Engl J Med 1998, 339:1578-84.
4. Gerritsen HE, Turecek PL, Schwarz HP, Lämmle B, Furlan M. Assay of von Willebrand factor (vWF)-cleaving protease based on decreased collagen binding affinity of degraded vWF: a tool for the diagnosis of thrombotic thrombocytopenic purpura (TTP). Thromb Haemost 1999, 82:1386-9.
5. Rick ME, Moll S, Taylor MA, Krizek DM, White GC, Aronson DL. Clinical use of a rapid collagen binding assay for von Willebrand factor cleaving protease in patients with thrombotic thrombocytopenic purpura. Thromb Haemost 2002, 88:598-604.
6. Knovich MA, Lawson HL, Burke MH, McCoy TP, Owen J. Rapid quantitative assay of ADAMTS13 activity on an automated coagulation analyzer: clinical applications and comparison with immunoblot method. Am J Hematol 2008, 83:654-6.
7. Bohm M, Vigh T, Scharrer I. Evaluation and clinical application of a new method for measuring activity of von Willebrand factor-cleaving metalloprotease (ADAMTS13). Ann Hematol 2002, 81:430-5.
8. Kostousov V, Fehr J, Bombeli T. Novel, semi-automated, 60-min-assay to determine von Willebrand factor cleaving activity of ADAMTS-13. Thromb Res 2006, 118:723-31.
9. Obert B, Tout H, Veyradier A, Fressinaud E, Meyer D, Girma JP. Estimation of the von Willebrand factor-cleaving protease in plasma using monoclonal antibodies to vWF. Thromb Haemost 1999, 82:1382-5.
10. Knovich MA, Craver K, Matulis MD, Lawson H, Owen J. Simplified assay for VWF cleaving protease (ADAMTS13) activity and inhibitor in plasma. Am J Hematol 2004, 76:286-90.
11. Whitelock JL, Nolasco L, Bernardo A, Moake J, Dong JF, Cruz MA. ADAMTS-13 activity in plasma is rapidly measured by a new ELISA method that uses recombinant VWF-A2 domain as substrate. J Thromb Haemost 2004, 2:485-91.
12. Cruz MA, Whitelock J, Dong JF. Evaluation of ADAMTS-13 activity in plasma using recombinant von Willebrand Factor A2 domain polypeptide as substrate. Thromb Haemost 2003, 90:1204-9.
13. Wu JJ, Fujikawa K, Lian EC, McMullen BA, Kulman JD, Chung DW. A rapid enzyme-linked assay for ADAMTS-13. J Thromb Haemost 2006, 4:129-36.
14. Zhou W, Tsai HM. An enzyme immunoassay of ADAMTS13 distinguishes patients with thrombotic thrombocytopenic purpura from normal individuals and carriers of ADAMTS13 mutations. Thromb Haemost 2004, 91:806-11.
15. Kokame K, Nobe Y, Kokubo Y, Okayama A, Miyata T. FRETS-VWF73, a first fluorogenic substrate for ADAMTS13 assay. Br J Haematol 2005, 129:93-100.
16. Kremer Hovinga JA, Mottini M, Lämmle B. Measurement of ADAMTS-13 activity in plasma by the FRETS-VWF73 assay: comparison with other assay methods. J Thromb Haemost 2006, 4:1146-8.
17. Kokame K, Matsumoto M, Fujimura Y, Miyata T. VWF73, a region from D1596 to R1668 of von Willebrand factor, provides a minimal substrate for ADAMTS-13. Blood 2003, 103:607-12.
18. Ai J, Smith P, Wang S, Zhang P, Zheng XL. The proximal carboxyl terminal domains of ADAMTS13 determine substrate specificity and are all required for cleavage of von Willebrand factor. J Biol Chem 2005, 280:29428-34.
19. Kato S, Matsumoto M, Matsuyama T, Isonishi A, Hiura H, Fujimura Y. Novel monoclonal antibody-based enzyme immunoassay for determining plasma levels of ADAMTS13 activity. Transfusion 2006, 46:1444-52.
20. Jin M, Casper TC, Cataland SR, Kennedy MS, Lin S, Li YJ, Wu HM. Relationship between ADAMTS13 activity in clinical remission and the risk of TTP relapse. Br J Haematol 2008, 141:651-8.
21. Tripodi A, Peyvandi F, Chantarangkul V, Palla R, Afrasiabi A, Canciani MT, Chung DW, Ferrari S, Fujimura Y, Karimi M, Kokame K, Kremer Hovinga JA, Lämmle B, de Meyer SF, Plaimauer B, Vanhoorelbeke K, Varadi K, Mannucci PM. Second international collaborative study evaluating performance characteristics of methods measuring the von Willebrand factor cleaving protease (ADAMTS-13). J Thromb Haemost 2008, 6:1534-41.
22. Studt JD, Hovinga JA, Antoine G, Hermann M, Rieger M, Scheiflinger F, Lämmle B. Fatal congenital thrombotic thrombocytopenic purpura with apparent ADAMTS13 inhibitor: in vitro inhibition of ADAMTS13 activity by hemoglobin. Blood 2005, 105:542-4.
23. Meyer SC, Sulzer I, Lämmle B, Kremer Hovinga JA. Hyperbilirubinemia interferes with ADAMTS-13 activity measurement by FRETS-VWF73 assay: diagnostic relevance in patients suffering from acute thrombotic microangiopathies. J Thromb Haemost 2007, 5:866-7.
24. Eckmann CM, De Laaf RT, van Keulen JM, van Mourik JA, De Laat B. Bilirubin oxidase as a solution for the interference of hyperbilirubinemia with ADAMTS-13 activity measurement by FRETS-VWF73 assay. J Thromb Haemost 2007, 5:1330-1.
25. Raife TJ, Cao W, Atkinson BS, Bedell B, Montgomery RR, Lentz SR, Johnson GF, Zheng XL. Leukocyte proteases cleave von Willebrand factor at or near the ADAMTS13 cleavage site. Blood 2009, 114:1666-74.
26. Lam JK, Chion CK, Zanardelli S, Lane DA, Crawley JT. Further characterization of ADAMTS-13 inactivation by thrombin. J Thromb Haemost 2007, 5:1010-8.
27. Dong JF, Moake JL, Nolasco L, Bernardo A, Arceneaux W, Shrimpton CN, Schade AJ, McIntire LV, Fujikawa K, Lopez JA. ADAMTS-13 rapidly cleaves newly secreted ultralarge vonWillebrand factor multimers on the endothelial surface under flowing conditions. Blood 2002, 100:4033-9.
28. Shenkman B, Inbal A, Tamarin I, Lubetsky A, Savion N, Varon D. Diagnosis of thrombotic thrombocytopenic purpura based on modulation by patient plasma of normal platelet adhesion under flow condition. Br J Haematol 2003, 120:597-604.
29. Tripodi A, Chantarangkul V, Böhm M, Budde U, Dong JF, Friedman KD, Galbusera M, Girma JP, Moake J, Rick ME, Studt JD, Turecek PL, Mannucci PM. Measurement of von Willebrand factor cleaving protease (ADAMTS-13): results of an international collaborative study involving 11 methods testing the same set of coded plasmas. J Thromb Haemost 2004, 2:1601-9.
30. Feys HB, Liu F, Dong N, Pareyn I, Vauterin S, Vandeputte N, Noppe W, Ruan C, Deckmyn H, Vanhoorelbeke K. ADAMTS-13 plasma level determination uncovers antigen absence in acquired thrombotic thrombocytopenic purpura and ethnic differences. J Thromb Haemost 2006, 4:955-62.
31. Rieger M, Ferrari S, Kremer Hovinga JA, Konetschny C, Herzog A, Koller L, Weber A, Remuzzi G, Dockal M, Plaimauer B, Scheiflinger F. Relation between ADAMTS13 activity and ADAMTS13 antigen levels in healthy donors and patients with thrombotic microangiopathies (TMA). Thromb Haemost 2006, 95:212-20.
32. Ishizashi H, Yagi H, Matsumoto M, Soejima K, Nakagaki T, Fujimura Y. Quantitative Western blot analysis of plasma ADAMTS13 antigen in patients with Upshaw-Schulman syndrome. Thromb Res 2007, 120:381-6.
33. Scheiflinger F, Knobl P, Trattner B, Plaimauer B, Mohr G, Dockal M, Dorner F, Rieger M. Nonneutralizing IgM and IgG antibodies to vonWillebrand factor-cleaving protease (ADAMTS-13) in a patient with thrombotic thrombocytopenic purpura. Blood 2003, 102:3241-3.
34. Peyvandi F, Lavoretano S, Palla R, Feys HB, Vanhoorelbeke K, Battaglioli T, Valsecchi C, Canciani MT, Fabris F, Zver S, Réti M, Mikovic D, Karimi M, Giuffrida G, Laurenti L, Mannucci PM. ADAMTS13 and anti-ADAMTS13 antibodies as markers for recurrence of acquired thrombotic thrombocytopenic purpura during remission. Haematologica 2008, 93:232-9.
35. Rieger M, Mannucci PM, Kremer Hovinga JA, Herzog A, Gerstenbauer G, Konetschny C, Zimmermann K, Scharrer I, Peyvandi F, Galbusera M, Remuzzi G, Böhm M, Plaimauer B, Lämmle B, Scheiflinger F. ADAMTS13 autoantibodies in patients with thrombotic microangiopathies and other immunomediated diseases. Blood 2005, 106:1262-7.
36. Palla R, Valsecchi C, Bajetta MT, Canciani MT, Lavoretano S, Mannucci PM, Peyvandi F. Determination of anti-ADAMTS13 autoantibodies in thrombotic trombocitopenic purpura (TTP) patients: comparison of two different methods. J Thromb Haemost 2007, 5(Suppl. 2):PT-303.
37. Sanmarco M, Bardin N, Blank M, Pascal V, Christine Alessi M, Dignat-George F, Shoenfeld Y, Harlé JR. Heterogeneity of anti-beta2-glycoprotein I antibodies. A factor of variability in test results. Thromb Haemost 2005, 93:80-7.
38. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw JD, Ginsburg D, Tsai HM. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 2001, 413:488-94.
39. Lotta LA, Garagiola I, Palla R, Cairo A, Peyvandi F. ADAMTS13 mutations and polymorphisms in congenital thrombotic thrombocytopenic purpura. Hum Mutat 2009, http://dx.doi.org/10.1002/humu.21143, DOI:
40. Kokame K, Matsumoto M, Soejima K, Yagi H, Ishizashi H, Funato M, Tamai H, Konno M, Kamide K, Kawano Y, Miyata T, Fujimura Y. Mutations and common polymorphisms in ADAMTS13 gene responsible for von Willebrand factorcleaving protease activity. Proc Natl Acad Sci USA 2002, 99:11902-7.
41. Plaimauer B, Fuhrmann J, Mohr G, Wernhart W, Bruno K, Ferrari S, Konetschny C, Antoine G, Rieger M, Scheiflinger F. Modulation of ADAMTS13 secretion and specific activity by a combination of common amino acid polymorphisms and a missense mutation. Blood 2006, 107:118-25.
42. Lotta LA, Garagiola I, Cairo A, Klaassen R, Metin A, Gurgey A, Peyvandi F. Genotype-phenotype correlation in congenital ADAMTS13 deficient patients. Blood (ASH annual meeting abstracts) 2008, 112:273.
43. Meyer SC, Shengyu J, Wenjing C, Zheng XL, Lammle B, Kremer Hovinga JA. Characterization of five homozygous mutations in hereditary thrombotic thrombocytopenic purpura - Towards a phenotype-genotype correlation. Blood (ASH annual meeting abstracts) 2008, 112:274.
44. Fujimura Y, Matsumoto M, Kokame K, Isonishi A, Soejima K, Akiyama N, Tomiyama J, Natori K, Kuranishi Y, Imamura Y, Inoue N, Higasa S, Seike M, Kozuka T, Hara M, Wada H, Murata M, Ikeda Y, Miyata T, George JN. Pregnancy-induced thrombocytopenia and TTP, and the risk of fetal death, in Upshaw-Schulman syndrome: a series of 15 pregnancies in 9 genotyped patients. Br J Haematol 2009, 60:1325-32.
45. Veyradier A, Obert B, Houllier A, Meyer D, Girma JP. Specific von Willebrand factor-cleaving protease in thrombotic microangiopathies: a study of 111 cases. Blood 2001, 98:1765-72.
46. Vesely SK, George JN, Lämmle B, Studt JD, Alberio L, El-Harake MA, Raskob GE. ADAMTS-13 activity in thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: relation to presenting features and clinical outcomes in a prospective cohort of 142 patients. Blood 2003, 102:60-8.
47. Kremer Hovinga JA, Studt JD, Alberio L, Lämmle B. von Willebrand factor-cleaving protease (ADAMTS-13) activity determination in the diagnosis of thrombotic microangiopathies: the Swiss experience. Semin Hematol 2004, 41:75-82.
48. Matsumoto M, Yagi H, Ishizashi H, Wada H, Fujimura Y. The Japanese experience with thrombotic thrombocytopenic purpura-hemolytic uremic syndrome. Semin Hematol 2004, 41:68-74.
49. Peyvandi F, Ferrari S, Lavoretano S, Canciani MT, Mannucci PM. von Willebrand factor cleaving protease (ADAMTS-13) and ADAMTS-13 neutralizing autoantibodies in 100 patients with thrombotic thrombocytopenic purpura. Br J Haematol 2004, 127:433-9.
50. Zheng XL, Kaufman RM, Goodnough LT, Sadler JE. Effect of plasma exchange on plasma ADAMTS-13 metalloprotease activity, inhibitor level, and clinical outcome in patients with idiopathic and nonidiopathic thrombotic thrombocytopenic purpura. Blood 2004, 103:4043-9.
51. Scully M, Yarranton H, Liesner R, Cavenagh J, Hunt B, Benjamin S, Bevan D, Mackie I, Machin S. Regional UK TTP Registry: correlation with laboratory ADAMTS 13 analysis and clinical features. Br J Haematol 2008, 142:819-26.
52. Francis KK, Kalyanam N, Terrell DR, Vesely SK, George JN. Disseminated malignancy misdiagnosed as thrombotic thrombocytopenic purpura: a report of 10 patients and a systematic review of published cases. Oncologist 2007, 12:11-9.
53. Coppo P, Wolf M, Veyradier A, Bussel A, Malot S, Millot GA, Daubin C, Bordessoule D, Pène F, Mira JP, Heshmati F, Maury E, Guidet B, Boulanger E, Galicier L, Parquet N, Vernant JP, Rondeau E, Azoulay E, Schlemmer B. Prognostic value of inhibitory anti-ADAMTS-13 antibodies in adult-acquired thrombotic thrombocytopenic purpura. Br J Haematol 2006, 132:66-74.
54. Tsai H-M, Li A, Rock G. Inhibitors of von Willebrand Factor cleaving protease in thrombotic thrombocytopenic purpura. Clin Lab 2001, 47:387-92.
55. Ferrari S, Scheiflinger F, Rieger M, Mudde G, Wolf M, Coppo P, Girma JP, Azoulay E, Brun-Buisson C, Fakhouri F, Mira JP, Oksenhendler E, Poullin P, Rondeau E, Schleinitz N, Schlemmer B, Teboul JL, Vanhille P, Vernant JP, Meyer D. Prognostic value of anti-ADAMTS 13 antibody features (Ig isotype, titer, and inhibitory effect) in a cohort of 35 adult French patients undergoing a first episode of thrombotic microangiopathy with undetectable ADAMTS 13 activity. Blood 2007, 109:2815-22.
56. Raife T, Atkinson B, Montgomery R, Vesely S, Friedman K. Severe deficiency of VWF-cleaving protease (ADAMTS-13) activity defines a distinct population of thrombotic microangiopathy patients. Transfusion 2004, 44:146-50.
57. Ferrari S, Mudde GC, Rieger M, Veyradier A, Kremer Hovinga JA, Scheiflinger F. IgG subclass distribution of anti-ADAMTS13 antibodies in patients with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost 2009, 7:1703-10.
58. Wyllie BF, Garg AX, Macnab J, Rock GA, Clark WF. Thrombotic thrombocytopenic purpura/haemolytic uraemic syndrome: a new index predicting response to plasma exchange. Br J Haematol 2006, 132:204-9.
59. Patton JF, Manning KR, Case D, Owen J. Serum lactate dehydrogenase and platelet count predict survival in thrombotic thrombocytopenic purpura. Am J Hematol 1994, 47:94-9.
60. Hghes C, McEwan JR, Longair I, Hughes S, Cohen H, Machin S, Scully M. Cardiac involvement in acute thrombotic thrombocytopenic purpura: association with troponin T and IgG antibodies to ADAMTS 13. J Thromb Haemost 2009, 7:529-36.
61. Remuzzi G, Galbusera M, Noris M, Canciani MT, Daina E, Bresin E, Contaretti S, Caprioli J, Gamba S, Ruggenenti P, Perico N, Mannucci PM. von Willebrand factor cleaving protease (ADAMTS13) is deficient in recurrent and familial thrombotic thrombocytopenic purpura and hemolytic uremic syndrome. Blood 2002, 100:778-85.
62. Ono T, Mimuro J, Madoiwa S, Soejima K, Kashiwakura Y, Ishiwata A, Takano K, Ohmori T, Sakata Y. 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, 107:528-34.
63. Nguyen TC, Carcillo JA. Bench-to-bedside review: thrombocytopenia-associated multiple organ failure--a newly appreciated syndrome in the critically ill. Crit Care 2006, 10:235.
64. Lattuada A, Rossi E, Calzarossa C, Candolfi R, Mannucci PM. Mild to moderate reduction of a von Willebrand factor cleaving protease (ADAMTS-13) in pregnant women with HELLP microangiopathic syndrome. Haematologica 2003, 88:1029-34.
65. Mannucci PM, Vanoli M, Forza I, Canciani MT, Scorza R. Von Willebrand factor cleaving protease (ADAMTS-13) in 123 patients with connective tissue diseases (systemic lupus erythematosus and systemic sclerosis). Haematologica 2003, 88:914-8.
66. Scully M, Cohen H, Cavenagh J, Benjamin S, Starke R, Killick S, Mackie I, Machin SJ. Remission in acute refractory and relapsing thrombotic thrombocytopenic purpura following rituximab is associated with a reduction in IgG antibodies to ADAMTS-13. Br J Haematol 2007, 136:451-61.
67. Studt JD, Böhm M, Budde U, Girma JP, Varadi K, Lämmle B. Measurement of von Willebrand factor-cleaving protease (ADAMTS-13) activity in plasma: a multicenter comparison of different assay methods. J Thromb Haemost 2003, 1:1882-7.