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Clinical significance of measuring ADAMTS-13, its inhibitor and von Willebrand factor in obstetric and gynecological practice

https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.203

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Abstract

ADAMTS-13 is a crucial metalloproteinase involved in liberating fragments of von Willebrand factor (vWF) into the plasma as well as regulating its activity by cleaving "ultra-large" multimers into smaller and less active counterparts. Many pathological conditions, including those emerged during pregnancy are characterized by increased level of vWF and decreased ADAMTS-13 activity. In this regard, it is necessary to monitor the levels of vWF and ADAMTS-13 activity to prevent thrombotic thrombocytopenic purpura (Moschcowitz disease) as one of the most severe forms of thrombotic microangiopathy.

 

About the Authors

K. N. Grigoreva
Sechenov University
Russian Federation

Kristina N. Grigoreva - MD, Medical Resident, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.



V. O. Bitsadze
Sechenov University
Russian Federation

Viktoria O. Bitsadze - MD, Dr Sci Med, Professor of RAS, Professor, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.
Scopus Author ID: 6506003478
Researcher ID: F-8409-2017



J. Kh. Khizroeva
Sechenov University
Russian Federation

Jamilya Kh. Khizroeva - MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.
Scopus Author ID: 57194547147
Researcher ID: F-8384-2017



M. V. Tretyakova
«Medical Center» LLC
Russian Federation

Maria V. Tretyakova - MD, PhD, Obstetrician-Gynecologist, Department of Gynecology, «Medical Center» LLC.
15/1 Timura Frunze Str., Moscow 119021.



D. A. Ponomarev
Maternity Hospital № 4, Branch of Vinogradov City Clinical Hospital, Moscow Healthcare Department
Russian Federation

Dmitry A. Ponomarev - Head of Maternity Hospital № 4, Branch of Vinogradov City Clinical Hospital, Moscow Healthcare Department.
3 Novatorov Str., Moscow 119421.



K. Yu. Tsvetnova
Maternity Hospital № 4, Branch of Vinogradov City Clinical Hospital, Moscow Healthcare Department
Russian Federation

Ksenia Yu. Tsvetnova - Head of the Department of Anesthesiology and Reanimation № 2, Hospital № 4, Branch of Vinogradov City Clinical Hospital, Moscow Healthcare Department.
3 Novatorov Str., Moscow 119421.



D. A. Doronicheva
Sechenov University
Russian Federation

Dariya A. Doronicheva - 6th year student, Faculty of Pediatrics, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.



A. R. Mamaeva
Sechenov University
Russian Federation

Amina R. Mamaeva - 3th year student, Sklifosovsky Institute of Clinical Medicine, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.



K. V. Mekhedova
Sechenov University
Russian Federation

Ksenia V. Mekhedova - Postgraduate Student, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.



G. Rizzo
Sechenov University; Tor Vergata University of Rome
Russian Federation

Giuseppe Rizzo - MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University; Professor, Director, Division of Maternal and Fetal Medicine, Ospedale Cristo Re, University of Rome Tor Vergata.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991; Rome.
Scopus Author ID: 7102724281
Researcher ID: G-8234-2018



J.-C. Gris
Sechenov University; University of Montpellier
Russian Federation

Jean-Christophe Gris - MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University; University of Montpellier.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991; Paris.
Researcher ID: AAA-2923-2019



I. Elalamy
Sechenov University; Medicine Sorbonne University; 2 Hospital Tenon
Russian Federation

Ismail Elalamy - MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University; Professor, Medicine Sorbonne University; Director of Hematology Department of Thrombosis Center, Hospital Tenon.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991; 12 Rue de l'Ecole de Medecine, 75006 Paris; 4 Rue de la Chine, 75020 Paris.
Scopus Author ID: 7003652413
Researcher ID: AAC-9695-2019



A. D. Makatsariya
Sechenov University
Russian Federation

Alexander D. Makatsariya - MD, Dr Sci Med, Academician of RAS, Professor, Head of the Department of Obstetrics and Gynecology, Filatov Clinical Institute of Children's Health, Sechenov University.
2 bldg. 4, Bolshaya Pirogovskaya Str., Moscow 119991.
Scopus Author ID: 6602363216
Researcher ID: M-5660-2016



References

1. Moschcowitz E. Hyaline thrombosis of the terminal arterioles and capillaries: a hitherto undescribed disease. Proc NY Pathol Soc. 1924;24:21-4.

2. Moschcowitz E. An acute febrile pleiochromic anemia with hyaline thrombosis of the terminal arterioles and capillaries: an undescribed disease. Am J Med. 1952;13(5):567-9. https://doi.org/10.1016/0002-9343(52)90022-3.

3. SoRelle R. Clopidogrel-associated thrombotic thrombocytopenic purpura identified. Circulation. 2000;101(18):Е9036-7. https://doi.org/10.1161/01.cir.101.18.e9036.

4. Schulman I., Pierce M., Lukens A., Currimbhoy Z. Studies on thrombopoiesis. I. A factor in normal human plasma required for platelet production; chronic thrombocytopenia due to its deficiency. Blood. 1960;16:943-57.

5. Upshaw J.D. Congenital deficiency of a factor in normal plasma that reverses microangiopathic hemolysis and thrombocytopenia. N Engl J Med. 1978;298(24):1350-2. https://doi.org/10.1056/NEJM197806152982407.

6. Rennard S., Abe S. Decreased cold-insoluble globulin in congenital thrombocytopenia (Upshaw-Schulman syndrome). N Engl J Med. 1979;300(7):368. https://doi.org/10.1056/NEJM197902153000718.

7. Kinoshita S., Yoshioka A., Park Y.D. et al. Upshaw-Schulman syndrome revisited: a concept ofcongenital thrombotic thrombocytopenic purpura. Int J Hematol. 2001;74(1):101-8. https://doi.org/10.1007/BF02982558.

8. Amorosi E., Ultmann J. Thrombotic thrombocytopenic purpura: report of 16 cases and review of the literature. Medicine. 1966;45(2):139-60. https://doi.org/10.1097/00005792-196603000-00003.

9. Bell W.R., Braine H.G., Ness P.M., Kickler T.S. Improved survival in thrombotic thrombocytopenic purpura hemolytic uremic syndrome. Clinical experience in 108 patients. N Engl J Med. 1991;325(6):398-403. https://doi.org/10.1056/NEJM199108083250605.

10. Tsai H.M., Lian E.C. 1998. Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med. 1998;339:1585-94. https://doi.org/10.1056/NEJM199811263392203.

11. Rock G.A., Shumak K.H., Buskard N.A. et al. Comparison of plasma exchange with plasma infusion in the treatment of thrombotic thrombocytopenic purpura. Canadian Apheresis Study Group. N Engl J Med. 1991;325(6):393-7. https://doi.org/10.1056/NEJM199108083250604.

12. Moake J.L., Rudy C.K., Troll J.H. et al. Unusually large plasma factor VIII:von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura. N Engl J Med. 1982;(23)307:1432-5. https://doi.org/10.1056/NEJM198212023072306.

13. Furlan M., Robles R., Solenthaler M. et al. Deficient activity of von Willebrand factor-cleaving protease in chronic relapsing thrombotic thrombocytopenic purpura. Blood. 1997;89(9):3097-103.

14. Tsai H.M. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood. 1996;87(10):4235-44.

15. Furlan M., Robles R., Solenthaler M., Lammle B. Acquired deficiency of von Willebrand factor-cleaving protease in a patient with thrombotic thrombocytopenic purpura. Blood. 1998;91(8):2839-46.

16. Furlan M., Robles R., Lammle B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood. 1996;87(10):4223-34.

17. Fujikawa K., Suzuki H., McMullen B., Chung D. Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family. Blood. 2001;98(6):1662-6. https://doi.org/10.1182/blood.v98.6.1662.

18. Gerritsen H.E., Robles R., Lammle B., Furlan M. Partial amino acid sequence of purified von Willebrand factor-cleaving protease. Blood. 2001;98(6):1654-61. https://doi.org/10.1182/blood.v98.6.1654.

19. Zheng X., Chung D., Takayama T.K. et al. Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J Biol Chem. 2001;276(44):41059-63. https://doi.org/10.1074/jbc.C100515200.

20. Plaimauer B., Zimmermann K., Volkel D. et al. Cloning, expression, and functional characterization of the von Willebrand factor-cleaving protease (ADAMTS13). Blood. 2002;100(10):3626-32. https://doi.org/10.1182/blood-2002-05-1397.

21. Zheng X., Nishio K., Majerus E.M. et al. 2003. Cleavage of von Willebrand factor requires the spacer domain of the metalloprotease ADAMTS13. J Biol Chem. 2003;278(32):30136-41. https://doi.org/10.1074/jbc.M305331200.

22. Plautz W.E., Raval J.S., Dyer M.R. et al. ADAMTS13: origins, applications and prospects. Transfusion. 2018;58(10):2453-62. https://doi.org/10.1111/trf.14804.

23. South K., Luken B.M., Crawley J.T. et al. Conformational activation of ADAMTS13. Proc Natl Acad Sci U S A. 2014;111(52):18578-83. https://doi.org/10.1073/pnas.1411979112.

24. South K., Freitas M.O., Lane D.A. A model for the conformational activation of the structurally quiescent metalloprotease ADAMTS13 by von Willebrand factor. J Biol Chem. 2017;292(14):5760-9. https://doi.org/10.1074/jbc.M117.776732.

25. Sadler J.E. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem. 1998;67:395-424. https://doi.org/10.1146/annurev.biochem.67.1.395.

26. Roth G.J., Titani K., Hoyer L.W. et al. Localization of binding sites within human von Willebrand factor for monomeric type III collagen. Biochemistry. 1986;25(26):8357-61. https://doi.org/10.1021/bi00374a004.

27. Tsai H.-M. Shear stress and von Willebrand factor in health and disease. Semin Thromb Hemost. 2003;29(5):479-88. https://doi.org/10.1055/s-2003-44556.

28. Sadler J.E. Von Willebrand factor, ADAMTS-13, and thrombotic thrombocytopenic purpura. Blood. 2008;112(1):11-8. https://doi.org/10.1182/blood-2008-02-078170.

29. Hobbs W.E., Moore E.E., Penkala R.A. et al. Cocaine and specific cocaine metabolites induce von Willebrand factor release from endothelial cells in a tissue-specific manner. Arterioscler Thromb Vasc Biol. 2013;33(6):1230-7. https://doi.org/10.1161/ATVBAHA.113.301436.

30. de Groot R., Bardhan A., Ramroop N. et al. Essential role of the disintegrin-like domain in ADAMTS13 function. Blood. 20098;113(22):5609-16. https://doi.org/10.1182/blood-2008-11-187914.

31. de Groot R., Lane D.A., Crawley J.T. The role of the ADAMTS13 cysteine-rich domain in VWF binding and proteolysis. Blood. 2015;125(12):1968-7. https://doi.org/10.1182/blood-2014-08-594556.

32. Schaller M., Studt J.D., Voorberg J., Kremer Hovinga J.A. Acquired thrombotic thrombocytopenic purpura. Development of an autoimmune response. Hamostaseologie. 2013;33(2):121-30. https://doi.org/10.5482/HAMO-12-12-0023.

33. Molvarec A., Rigo J., Boze T. et al. Increased plasma von Willebrand factor antigen levels but normal von Willebrand factor cleaving protease (ADAMTS13) activity in preeclampsia. Thromb Haemost. 2009;101(2):305-11.

34. Sanchez-Luceros A., Meschengieser S.S., Marchese C. et al. Factor VIII and von Willebrand factor changes during normal pregnancy and puerperium. Blood Coagul Fibrinolysis. 2003;14(7):647-5. https://doi.org/10.1097/00001721-200310000-00005.

35. Aref S., Goda H. Increased VWF antigen levels and decreased ADAMTS13 activity in preeclampsia. Hematology. 2013;18(4):237-41. https://doi.org/10.1179/1607845412Y.0000000070.

36. Stepanian A., Cohen-Moatti M., Sanglier T. et al. Von Willebrand factor and ADAMTS13: a candidate couple for preeclampsia pathophysiology. Arterioscler Thromb Vasc Biol. 2011;31(7):1703-9. https://doi.org/10.1161/ATVBAHA.111.223610.

37. Laurence J. Atypical hemolytic uremic syndrome (aHUS): making the diagnosis. Clin Adv Hematol Oncol. 2012;10(10 Suppl 17):1-12.

38. Levi M., van der Poll T. Coagulation and sepsis. Thromb Res. 2017;149:38-44. https://doi.org/10.1016/j.thromres.2016.11.007.

39. Schwameis M., Schorgenhofer C., Assinger A. et al. VWF excess and ADAMTS13 deficiency: a unifying pathomechanism linking inflammation to thrombosis in DIC, malaria, and TTP. Thromb Haemost. 2015;113(3):708-18. https://doi.org/10.1160/TH14-09-0731.

40. Bockmeyer C.L., Claus R.A., Budde U et al. Inflammation-associated ADAMTS-13 deficiency promotes formation of ultra-large von Willebrand factor. Haematologica. 2008;93(1):137-40. https://doi.org/10.3324/haematol.11677.

41. Turner N.A., Moake J. Assembly and activation of alternative complement components on endothelial cell-anchored ultra-large von Willebrand factor links complement and hemostasis thrombosis. PLoS One. 2013;8(3):e59372. https://doi.org/10.1371/journal.pone.0059372.

42. Xu J., Zhang X., Pelayo R. et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318-21. https://doi.org/10.1038/nm.2053.

43. Kim J.E., Lee N., Gu J.-Y. et al. Circulating levels of DNA-histone complex and dsDN are independent prognostic factors of disseminated intravascular coagulation. Thromb Res. 2015;135(6):1064-9. https://doi.org/10.1016/j.thromres.2015.03.014.

44. Fuchs T.A., Kremer Hovinga J.A., Schatzberg D. et al. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood. 2012;120(6):1157-64. https://doi.org/10.1182/blood-2012-02-412197.

45. Ono T., Mimuro J., Madoiwa S. et al. Severe secondary deficiency of von Willebrand factor-cleaving protease (ADAMTS-13) in patients with sepsis-induced disseminated intravascular coagulation: its correlation with development of renal failure. Blood. 2006;107(2):528-34. https://doi.org/10.1182/blood-2005-03-1087.

46. Crawley J.T., Lam J.K., Rance J.B. et al. Proteolytic inactivation of ADAMTS-13 by thrombin and plasmin. Blood. 2005;105(3)1085-93. https://doi.org/10.1182/blood-2004-03-1101.

47. Bernardo A., Ball C., Nolasco L. et al. Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand factor multimers under flow. Blood. 2004;104(1):100-6. https://doi.org/10.1182/blood-2004-01-0107.

48. Bonnefoy A., Daenens K., Feys H.B. et al. Thrombospondin-1 controls vascular platelet recruitment and thrombus adherence in mice by protecting (sub)endothelial VWF from cleavage by ADAMTS-13. Blood. 2006;10(3):955-64. https://doi.org/10.1182/blood-2004-12-4856.

49. Schwameis M., Schorgenhofer C., Assinger A. et al. VWF excess and ADAMTS13 deficiency: a unifying pathomechanism linking inflammation to thrombosis in DIC, malaria, and TTP. Thromb Haemost. 2015;113(4):708-18. https://doi.org/10.1160/TH14-09-0731.

50. Habe K., Wada H., Ito-Habe N. et al. Plasma ADAMTS-13, von Willebrand factor (VWF) and VWF propeptide profiles in patients with DIC and related diseases. Thromb Res. 2012;129(5):598-602. https://doi.org/10.1016/j.thromres.2011.10.011.

51. Kremer Hovinga J.A., Zeerleder S., Kessler P. et al. ADAMTS-13, von Willebrand factor and related parameters in severe sepsis and septic shock. J Thromb Haemost. 2007;5(11):2284-90. https://doi.org/10.1111/j.1538-7836.2007.02743.x.

52. Peigne V., Azoulay E., Coquet I. et al. The prognostic value of ADAMTS-13 (a disintegrin and metalloprotease with thrombospondin type 1 repeats, member 13) deficiency in septic shock patients involves interleukin-6 and is not dependent on disseminated intravascular coagulation. Crit Care. 2013;17(6):R273. https://doi.org/10.1186/cc13115.

53. Thachil J., Tang N., Gando S. et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost. 2020;18(5):1023-6. https://doi.org/10.1111/jth.14810.

54. McGonagle D., O'Donnell J.S., Sharif K. et al. Immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia. Lancet Rheumatol. 2020;2(7):e437-45. https://doi.org/10.1016/S2665-9913(20)30121-1.

55. Driggin E., Madhavan M.V., Bikdeli B. et al. Cardiovascular considerations for patients, health care workers, and health systems during the coronavirus disease 2019 (COVID-19) pandemic. J Am Coll Cardiol. 2020;75(18):2352-71. https://doi.org/10.1016/j.jacc.2020.03.031.

56. Rotzinger D.C., Beigelman-Aubry C., von Garnier C., Qanadli S.D. Pulmonary embolism in patients with COVID-19: time to change the paradigm of computed tomography. Thromb Res. 2020;190:58-9. https://doi.org/10.1016/j.thromres.2020.04.011.

57. Wang J., Hajizadeh N., Moore E.E. et al. Tissue plasminogen activator (tPA) treatment for COVID-19 associated acute respiratory distress syndrome (ARDS): a case series. J Thromb Haemost. 2020;18(7):1752-5. https://doi.org/10.1111/jth.14828.

58. Wang T, Chen R., Liu C., et al. Attention should be paid to venous thromboembolism prophylaxis in the management of COVID-19. Lancet Haematol. 2020;7(5):e362-3. https://doi.org/10.1016/S2352-3026(20)30109-5.

59. Tang N., Bai H., Chen X. et al. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost. 2020;18(5):1094-9. https://doi.org/10.1111/jth.14817.

60. Danzi G.B., Loffi M., Galeazzi G., Gherbesi E. Acute pulmonary embolism and COVID-19 pneumonia: a random association? Eur Heart J. 2020;41(19):1858. https://doi.org/10.1093/eurheartj/ehaa254.

61. Nguyen T.C., Liu A., Liu L. et al. Acquired ADAMTS-13 deficiency in pediatric patients with severe sepsis. Haematologica. 2007;92(1):121-4. https://doi.org/10.3324/haematol.10262.

62. Morici N., Bottiroli M., Fumagalli R. et al. Role of von Willebrand factor and ADAMTS-13 in the pathogenesis of thrombi in SARS-CoV-2 infection: time to rethink. Thromb Haemost. 2020;120(9):1339-42. https://doi.org/10.1055/s-0040-1713400.

63. Tiscia G.L., Favuzzi G., De Laurenzo A. et al. Reduction of ADAMTS13 levels predicts mortality in SARS-CoV-2 patients. TH Open. 2020;4(3):e203-6. https://doi.org/10.1055/s-0040-1716379.

64. Bazzan M., Montaruli B., Sciascia S. et al. Low ADAMTS 13 plasma levels are predictors of mortality in COVID-19 patients. Intern Emerg Med. 2020;15(5):861-3. https://doi.org/10.1007/s11739-11020-02394-11730.

65. Iba T., Levi M., Levy J.H. Sepsis-induced coagulopathy and disseminated intravascular coagulation. Semin Thromb Hemost. 2020;46(1):89-95. https://doi.org/10.1055/s-0039-1694995.

66. Schonrich G., Raftery M.J., Samstag Y. Devilishly radical NETwork in COVID-19: oxidative stress, neutrophil extracellular traps (NETs), and T cell suppression. Adv Biol Regul. 2020;77:100741. https://doi.org/10.1016/j.jbior.2020.100741.

67. Zuo Y., Yalavarthi S., Shi H. et al. Neutrophil extracellular traps (NETs) as markers of disease severity in COVID-19. medRxiv. 2020 Apr 14;2020.04.09.20059626. https://doi.org/10.1101/2020.04.09.20059626.Preprint.

68. He Y., Yang F.-Y., Sun E.-W. Neutrophil extracellular traps in autoimmune diseases. Chin Med J (Engl). 2018;131(13):1513-9. https://doi.org/10.4103/0366-6999.235122.

69. Cao W., Krishnaswamy S., Camire R.M. et al. Factor VIII accelerates proteolytic cleavage of von Willebrand factor by ADAMTS-13. Proc Natl Acad Sci U S A. 2008;105(21):7416-21. https://doi.org/10.1073/pnas.0801735105.

70. Gavriilaki E., Chrysanthopoulou A., Sakellari I. et al. Linking complement activation, coagulation, and neutrophils in transplant-associated thrombotic microangiopathy. Thromb Haemost. 2019;119(9):1433-40. https://doi.org/10.1055/s-0039-1692721.

71. Rutten B., Maseri A., Cianflone D. et al. Plasma levels of active Von Willebrand factor are increased in patients with first ST-segment elevation myocardial infarction: a multicenter and multiethnic study. Eur Heart J Acute Cardiovasc Care. 2015;4(1):64-74. https://doi.org/10.1177/2048872614534388.

72. Maino A., Siegrink B., Lotta L.A. et al. Plasma ADAMTS-13 levels and the risk of myocardial infarction: an individual patient data meta-analysis. J Thromb Haemost. 2015;13(8):1396-404. https://doi.org/10.1111/jth.13032.

73. Horii M., Uemura S., Uemura M., M. Matsumoto et al. Acute myocardial infarction as a systemic prothrombotic condition evidenced by increased von Willebrand factor protein over ADAMTS13 activity in coronary and systemic circulation. Heart Vessels. 2008;23(5):301-7. https://doi.org/10.1007/s00380-008-1053-x.

74. Anderson H.M., Siegerink B., Luken B.M. et al. High VWF, low ADAMTS13, and oral contraceptives increase the risk of ischemic stroke and myocardial infarction in young women. Blood. 2012;119(6):1555-60. https://doi.org/10.1182/blood-2011-09-380618.

75. Zhao B.Q., Chauhan A.K., Canault M., et al. von Willebrand factorcleaving protease ADAMTS13 reduces ischemic brain injury in experimental stroke. Blood. 2009;114(15):3329-34. https://doi.org/10.1182/blood-2009-03-213264.

76. Fujioka M., Hayakawa K., Mishima K. et al. ADAMTS13 gene deletion aggravates ischemic brain damage: a possible neuroprotective role of ADAMTS13 by ameliorating postischemic hypoperfusion. Blood. 2010;115(8):1650-3. https://doi.org/10.1182/blood-2009-06-230110.

77. Doi M., Matsui H., Takeda H., et al. ADAMTS13 safeguards the myocardium in a mouse model of acute myocardial infarction. Thromb Haemost. 2012;108(6):1236-8. https://doi.org/10.1160/TH12-09-0674.

78. Akyol O., Akyol S., Chen C.-H. et al. Update on ADAMTS13 and VWF in cardiovascular and hematological disorders. Clin Chim Acta. 2016;463:109-18. https://doi.org/10.1016/j.cca.2016.10.017.

79. Lambers M., Goldenberg N.A., Kenet G. et al. Role of reduced ADAMTS13 in arterial ischemic stroke: a pediatric cohort study. Ann Neurol. 2013;73(1):58-64. https://doi.org/10.1002/ana.23735.

80. Sonneveld M., de Maat M.P.M, Leebeek F.W.G. Von Willebrand factor and ADAMTS13 in arterial thrombosis: a systemic review and meta-analysis. Blood Rev. 2014;28(4):167-78. https://doi.org/10.1016/j.blre.2014.04.003.

81. Folsom A.R., Rosamond W.D., Shahar E. et al. Prospective study of markers of hemostatic function with risk of ischemic stroke. The Atherosclerosis Risk in Communities (ARIC) Study Investigators. Circulation. 1999;100(7):736-42. https://doi.org/10.1161/01.cir.100.7.736.

82. Tzoulaki I., Murray G.M., Lee A.J. et al. Relative value of inflammatory, hemostatic, and rheological factors for incident myocardial infarction and stroke: the Edinburgh Artery Study. Circulation. 2007;115(16):2119-27. https://doi.org/10.1161/CIRCULATIONAHA.106.635029.

83. Gottesman R.F., Cummiskey C., Chambless L. et al. Hemostatic factors and subclinical brain infarction in a community-based sample: the ARIC study. Cerebrovasc Dis. 2009;28(6):589-94. https://doi.org/10.1159/000247603.

84. Knuiman M.W., Folsom A.R., Chambless L.E. et al. Association of hemostatic variables with MRI-detected cerebral abnormalities: the atherosclerosis risk in communities study. Neuroepidemiology. 2001;20(2):96-104. https://doi.org/10.1159/000054767.

85. Kozuka K., Kohriyama T., Nomura E. et al. Endothelial markers and adhesion molecules in acute ischemic stroke - sequential change and differences in stroke subtype. Atherosclerosis. 2002;161(1):161-8. https://doi.org/10.1016/s0021-9150(01)00635-9.

86. Hanson E., Jood K., Karlsson S. et al. Plasma levels of von Willebrand factor in the etiologic subtypes of ischemic stroke. J Thromb Haemost. 2011;9(2):275-81. https://doi.org/10.1111/j.1538-7836.2010.04134.x.

87. Jansson J.H., Nilsson T.K., Johnson O. von Willebrand factor, tissue plasminogen activator, and dehydroepiandrosterone sulphate predict cardiovascular death in a 10 year follow up survivors of acute myocardial infarction. Heart. 1998;80(4):334-7. https://doi.org/10.1136/hrt.80.4.334.

88. Andrew M., Paes B., Milner R. et al. Development of the human coagulation system in the full-term infant. Blood. 1987;70(1):165-72.

89. Andrew M., Vegh P., Johnston M. et al. Maturation of the hemostatic system during childhood. Blood. 1992;80(8):1998-2005.

90. Andrew M., Paes B., Milner R. et al. Development of the human coagulation system in the healthy premature infant. Blood. 1988;72(5):1651-7.

91. Ehrenforth S., Junker R., Koch H.G. et al. Multicentre evaluation of combined prothrombotic defects associated with thrombophilia in childhood. Childhood Thrombophilia Study Group. Eur J Pediatr. 1999;158(Suppl 3):S97-104. https://doi.org/10.1007/pl00014359.

92. Thomas K.B., Sutor A.H., Altinkaya N. et al. von Willebrand factor-collagen binding activity is increased in newborns and infants. Acta Paediatr. 1995;84(6):697-9. https://doi.org/10.1111/j.1651-2227.1995.tb13733.x.

93. Hellstrom-Westas L., Ley D., Berg A.C. et al. VWF-cleaving protease (ADAMTS13) in premature infants. Acta Paediatr. 2005;94(2):205-10. https://doi.org/10.1111/j.1651-2227.2005.tb01892.x.

94. Feys H.B., Canciani M.T., Peyvandi F. et al. ADAMTS13 activity to antigen ratio in physiological and pathological conditions associated with an increased risk of thrombosis. Br J Haematol. 2007;138(4):534-40. https://doi.org/10.1111/j.1365-2141.2007.06688.x.

95. Kavakli K., Canciani M.T., Mannucci P.M. Plasma levels of the von Willebrand factor-cleaving protease in physiological and pathological conditions in children. Pediatr Hematol Oncol. 2002;19(7):467-73. https://doi.org/10.1080/08880010290097288.

96. Mannucci P.M., Canciani M.T., Forza I. et al. Changes in health and disease of the metalloprotease that cleaves von Willebrand factor. Blood. 2001;98(9):2730-5. https://doi.org/10.1182/blood.v98.9.2730.

97. Schmugge M., Dunn M.S., Amankwah K.S. et al. The activity of the von Willebrand factor cleaving protease ADAMTS-13 in newborn infants. J Thromb Haemost. 2004;2:228-33. https://doi.org/10.1046/j.1538-7933.2003.00575.x.

98. Tsai H.M., Sarode R., Downes K.A. Ultralarge von Willebrand factor multimers and normal ADAMTS13 activity in the umbilical cord blood. Thromb Res. 2002;108(2-3):121-5. https://doi.org/10.1016/s0049-3848(02)00396-1.

99. Reiter R.A., Varadi K., Turecek P.L. et al. Changes in ADAMTS13 (vonWillebrand-factor-cleaving protease) activity after induced release of von Willebrand factor during acute systemic inflammation. Thromb Haemost. 2005;93(3):554-8. https://doi.org/10.1160/TH04-08-0467.

100. Levitan N., Dowlati A., Remick S.C. et al. Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine (Baltimore). 1999;78:285-91. https://doi.org/10.1097/00005792-199909000-00001.

101. Pabinger I, Thaler J, Ay C. Biomarkers for prediction of venous thromboembolism in cancer. Blood. 2013;122(12):2011-8. https://doi.org/10.1182/blood-2013-04-460147.

102. Koo B.H., Oh D., Chung S.Y. et al. Deficiency of von Willebrand factorcleaving protease activity in the plasma of malignant patients. Thromb Res. 2002;105(6):471-6. https://doi.org/10.1016/S0049-3848(02)00053-1.

103. Wang W.S., Lin J.K., Lin T.C. et al. Plasma von Willebrand factor level as a prognostic indicator of patients with metastatic colorectal carcinoma. World J Gastroenterol. 2005;11(14):2166-70. https://doi.org/10.3748/wjg.v11.i14.2166.

104. Nossent A.Y., VAN Marion V., VAN Tilburg N.H. et al. von Willebrand factor and its propeptide: the influence of secretion and clearance on protein levels and the risk of venous thrombosis. J Thromb Haemost. 2006;4(12):2556-62. https://doi.org/10.1111/j.1538-7836.2006.02273.x.

105. Koster T., Blann A.D., Briet E. et al. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep vein thrombosis. Lancet. 1995;345(8943):152-5. https://doi.org/10.1016/s0140-6736(95)90166-3.

106. Lancellotti S., Basso M., Veca V. et al. Presence of portal vein thrombosis in liver cirrhosis is strongly associated with low levels of ADAMTS-13: a pilot study. Intern Emerg Med. 2016;11(7):959-67. https://doi.org/10.1007/s11739-016-1467-x.

107. Mazetto B.M., Orsi F.L., Barnabe A. et al. Increased ADAMTS13 activity in patients with venous thromboembolism. Thromb Res. 2012;130(6):889-93. https://doi.org/10.1016/j.thromres.2012.09.009.

108. Franchini M., Montagnana M., Targher G., Lippi G. Reduced von Willebrand factor-cleaving protease levels in secondary thrombotic microangiopathies and other diseases. Semin Thromb Hemost. 2007;33(8):787-77. https://doi.org/10.1055/s-2007-1000365.

109. Lotta L.A., Tuana G., Yu J. et al. Next generation sequencing study finds an excess of rare, coding single nucleotide variants of ADAMTS13 in patients with deep vein thrombosis. J Thromb Haemost. 2013;11(7):1228-39. https://doi.org/10.1111/jth.12291.

110. Bittar L.F., de Paula E.V., Mello T.B. et al. Polymorphisms and mutations in vWF and ADAMTS13 genes and their correlation with plasma levels of FVIII and vWF in patients with deep venous thrombosis. Clin Appl Thromb Hemost. 2011;17(5):514-8. https://doi.org/10.1177/1076029610375815.

111. Dean S.A., Mathis B., Litzky L.A., Hood I.C. Sudden death by occult metastatic carcinoma. J Forensic Sci. 2015;60(6):1637-9. https://doi.org/10.1111/1556-4029.12837.

112. Abe H., Hino R., Fukayama M. Platelet-derived growth factor-A and vascular endothelial growth factor-C contribute to the development of pulmonary tumor thrombotic microangiopathy in gastric cancer. Virchows Arch. 2013;462(5):523-31. https://doi.org/10.1007/s00428-013-1403-7.

113. Hotta M., Ishida M., Kojima F. et al. Pulmonary tumor thrombotic microangiopathy caused by lung adenocarcinoma: case report with review of theliterature. Oncol Lett. 2011;2(3):435-7. https://doi.org/10.3892/ol.2011.270.

114. Zwicker J.I., Liebman H.A., Neuberg D. et al. Tumor-derived tissue factorbearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res. 2009;15(22):6830-40. https://doi.org/10.1158/1078-0432.CCR-09-0371.

115. Grange S., Coppo P.; Centre de reference des microangiopathies thrombotiques (CNR-MAT). Thrombotic microangiopathies and antineoplastic agents. Nephrol Ther. 2017;13(Suppl 1):S109-13. https://doi.org/10.1016/j.nephro.2017.01.016.

116. Izzedine H., Escudier B., Lhomme C. et al. Kidney disease associated with anti-vascular endothelial growth factor (VEGF): an 8-year observational study at a single center. Medicine (Baltimore). 2014;93(24):333-9. https://doi.org/10.1097/MD.0000000000000207.

117. Griffin P.T., Jaglal M. Metastatic prostate cancer mimicking thrombotic thrombocytopenic pupura. Blood. 2015;125(8):1349. https://doi.org/10.1182/blood-2014-11-608828.

118. Al-Nouri Z.L., Reese J.A., Terrell D.R. et al. Drug-induced thrombotic microangiopathy: a systematic review of published reports. Blood. 2015;125(4):616-8. https://doi.org/10.1182/blood-2014-11-611335.


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Grigoreva K.N., Bitsadze V.O., Khizroeva J.Kh., Tretyakova M.V., Ponomarev D.A., Tsvetnova K.Yu., Doronicheva D.A., Mamaeva A.R., Mekhedova K.V., Rizzo G., Gris Zh., Elalamy I., Makatsariya A.D. Clinical significance of measuring ADAMTS-13, its inhibitor and von Willebrand factor in obstetric and gynecological practice. Obstetrics, Gynecology and Reproduction. 2021;15(1):93-106. (In Russ.) https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.203

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