The site of the Media Sphera Publishers contains materials intended solely for healthcare professionals.
By closing this message, you confirm that you are a certified medical professional or a student of a medical educational institution.

Login
EN
+7 (495) 482-4118
+7 (495) 482-0604
+8 800 250-18-12
  • (toll-free number for subscriptions)
    Mon-Fri from 10 a.m. to 6 p.m.

  • © 1998-2025
+7 (495) 482-43-29
EN
All journals
Journal
Year
Year
Search result: 0

Agapov A.B.

Pavlov Ryazan State Medical University;
Ryazan Regional Clinical Hospital

Kalinin R.E.

Pavlov Ryazan State Medical University

Mzhavanadze N.D.

Pavlov Ryazan State Medical University;
Ryazan City Clinical Emergency Hospital

Povarov V.O.

Pavlov Ryazan State Medical University

Nikiforov A.A.

Pavlov Ryazan State Medical University

Suchkov I.A.

Pavlov Ryazan State Medical University

Platelet apoptosis markers under anticoagulation for COVID-19 infection

Authors:

Agapov A.B., Kalinin R.E., Mzhavanadze N.D., Povarov V.O., Nikiforov A.A., Suchkov I.A.

More about the authors

Journal: Russian Journal of Cardiology and Cardiovascular Surgery. 2024;17(2): 194‑203

DOI: 10.17116/kardio202417021194

Read: 1134 times

Download PDF (RU)
Contact the author
Table of contents

PLATELET APOPTOSIS MARKERS UNDER ANTICOAGULATION FOR COVID-19 INFECTION
PLATELET APOPTOSIS MARKERS UNDER ANTICOAGULATION FOR COVID-19 INFECTION

To cite this article:

Agapov AB, Kalinin RE, Mzhavanadze ND, Povarov VO, Nikiforov AA, Suchkov IA. Platelet apoptosis markers under anticoagulation for COVID-19 infection. Russian Journal of Cardiology and Cardiovascular Surgery. 2024;17(2):194‑203. (In Russ.)
https://doi.org/10.17116/kardio202417021194

ЭндоКард
Подписка 2026 Кардиология и сердечно-сосудистая хирургия (Russian Journal of Cardiology and Cardiovascular Surgery)
 
МСФ на ЯМ
Использование инфографики авторами научных работ
Close metadata
Recommended articles:
Effi­cacy and Safety of the Oral Anti­coagulant DIMO­LEGIN Compared to Enoxaparin Sodium for the Prevention of Venous Thro­mboembolism Following Major Joint Replacement Surgery (hip or knee arthroplasty): A Randomized, Double-Blind, Multicenter Trial. Russian Journal of Cardiology and Cardiovascular Surgery. 2025;(5):577-585
The role of drug Cyto­flavin in the correction of dysautonomia in patients with post-COVID syndrome. S.S. Korsakov Journal of Neurology and Psychiatry. 2024;(11):140-146
Long-term outcomes in patients after hospital treatment for COVID-19 (three-year follow-up data). Russian Journal of Preventive Medi­cine. 2024;(12):114-121
Sele­ctive anosmia for mono­molecular odorants in a cohort of young indi­viduals. Russian Rhinology. 2024;(4):262-268
Posi­tive Predictive Value of the Wells Score in Diagnosis of Deep Vein Thro­mbosis: Resu­lts of Bayesian Analysis. Journal of Venous Diso­rders. 2024;(4):274-282
Inci­dence of diseases of the circulatory system in the working-age popu­lation of the Ural Fede­ral District in 2012—2022. Russian Journal of Preventive Medi­cine. 2025;(1):24-29
Morphogenesis and mole­cular regu­lation of poly­posis rhinosinusitis. Russian Journal of Archive of Pathology. 2025;(1):68-76
Post-COVID syndrome: orga­nizing COVID-19-associated pneumonia. Clinical case. Journal of Respiratory Medi­cine. 2025;(1):65-72
Abstract:

OBJECTIVE

To assess the level of platelet apoptosis markers (phosphatidylserine and calreticulin) under anticoagulation for COVID-19 infection.

MATERIAL AND METHODS

A prospective study included 370 patients. They were divided into 3 groups depending on anticoagulation: group 1 (n=190) — low molecular weight heparin (LMWH); group 2 (n=123) — unfractionated heparin (UFH); group 3 (n=57) — direct oral anticoagulants (DOACs). We assessed clinical and anamnestic data, laboratory parameters, specific markers of apoptosis (phosphatidylserine and calreticulin). To identify cases of VTECs, Doppler ultrasound of lower limb veins was performed.

RESULTS

At the end of anticoagulation, serum calreticulin and phosphatidylserine were higher only in patients taking LMWH (group 1). C-reactive protein decreased in all groups (p=0.135), but serum ferritin and procalcitonin were lower in patients taking LMWH (group 1). The lowest serum fibrinogen was observed in patients taking LMWH. Patients receiving UFH were characterized by higher incidence of isolated pulmonary embolism without deep vein thrombosis (11.4% of cases), DVT and PE with a source in the lower extremities (6.5% and 6.5% of cases, respectively) compared to patients taking LMWH (1.6%, 1.1%, and 0.5% of cases, respectively).

CONCLUSION

Increased apoptosis markers (phosphatidylserine and calreticulin) were found in patients receiving VTEC prophylaxis with low molecular weight heparin. Baseline serum phosphatidylserine >62.75 pg/ml reduces the risk of VTEC by 1.033 times (1.005—1.062, p=0.02). Decrease in pro-inflammatory markers (CRP, ferritin) and coagulation markers (D-dimer and fibrinogen) was more significant in patients receiving LMWH.

Keywords:

phosphatidylserine
calreticulin
apoptosis
venous thromboembolic complications
new coronavirus infection

Authors:

Agapov A.B.

Pavlov Ryazan State Medical University;
Ryazan Regional Clinical Hospital

Kalinin R.E.

Pavlov Ryazan State Medical University

Mzhavanadze N.D.

Pavlov Ryazan State Medical University;
Ryazan City Clinical Emergency Hospital

Povarov V.O.

Pavlov Ryazan State Medical University

Nikiforov A.A.

Pavlov Ryazan State Medical University

Suchkov I.A.

Pavlov Ryazan State Medical University

Received:

13.09.2023

Accepted:

15.01.2024

Close metadata

References:

  1. Kalinin RE, Suchkov IA, Agapov AB, et al. Analysis of risk factors for venous thromboembolic complications and different variants of anticoagulant therapy in patients with novel coronavirus infection. Rossijskij mediko-biologicheskij vestnik im. akad. I.P. Pavlova. 2023;31(2):243-250. (In Russ.). https://doi.org/10.17816/PAVLOVJ110956
  2. Klok FA, Kruip MJ, van der Meer NJ, Arbous MS, Gommers DA, Kant KM. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145-147.  https://doi.org/10.1016/j.thromres.2020.04.013
  3. Vertkin AL, Avdeev SN, Roitman EV, et al. Treatment of COVID-19 from the perspective of endotheliopathy correction and prevention of thrombotic complications. The agreed position of the experts. Profilakticheskaya meditsina. 2021;24(4):45-51. (In Russ.). https://doi.org/10.17116/profmed20212404145
  4. Borodina IA, Selezneva IA, Borisova OV, et al. Blood groups and secretory state in COVID-19. Nauka molodykh (Eruditio Juvenium). 2021;9(4):589-596. (In Russ.). https://doi.org/10.23888/HMJ202194589-596
  5. Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054-1062.
  6. Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420-422.  https://doi.org/10.1016/S2213-2600(20)30076-X
  7. Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation. Blood, J Am Soc Hematol. 2020;135(23): 2033-2040.
  8. Lind SE. Phosphatidylserine is an overlooked mediator of COVID-19 thromboinflammation. Heliyon. 2021;7(1):e06033. https://doi.org/10.1016/j.heliyon.2021.e06033
  9. Cosemans JM, Van Kruchten R, Olieslagers S, et al. Potentiating role of Gas6 and Tyro3, Axl and Mer (TAM) receptors in human and murine platelet activation and thrombus stabilization. J Thromb Haemost. 2010;8(8):1797-808.  https://doi.org/10.1111/j.1538-7836.2010.03935.x
  10. Rezende SM, Simmonds RE, Lane DA. Coagulation, inflammation, and apoptosis: different roles for protein S and the protein S-C4b binding protein complex. Blood. 2004;103(4):1192-1201. https://doi.org/10.1182/blood-2003-05-1551
  11. Kimani SG, Geng K, Kasikara C, Kumar S, Sriram G, Wu Y, Birge RB. Contribution of Defective PS Recognition and Efferocytosis to Chronic Inflammation and Autoimmunity. Front Immunol. 2014;5:566.  https://doi.org/10.3389/fimmu.2014.00566
  12. Yasen A, Herrera R, Rosbe K, Lien K, Tugizov SM. HIV internalization into oral and genital epithelial cells by endocytosis and macropinocytosis leads to viral sequestration in the vesicles. Virology. 2018;515:92-107.  https://doi.org/10.1016/j.virol.2017.12.012
  13. Yang X, Cheng X, Tang Y et al. Bacterial Endotoxin Activates the Coagulation Cascade through Gasdermin D-Dependent Phosphatidylserine Exposure. Immunity. 2019;51(6):983-996.e6.  https://doi.org/10.1016/j.immuni.2019.11.005
  14. Meertens L, Carnec X, Lecoin MP, Ramdasi R, Guivel-Benhassine F, Lew E, Lemke G, Schwartz O, Amara A. The TIM and TAM families of phosphatidylserine receptors mediate dengue virus entry. Cell Host Microbe. 2012;12(4):544-557.  https://doi.org/10.1016/j.chom.2012.08.009
  15. Shibata T, Makino A, Ogata R, Nakamura S, Ito T, Nagata K, Terauchi Y, Oishi T, Fujieda M, Takahashi Y, Ato M. Respiratory syncytial virus infection exacerbates pneumococcal pneumonia via Gas6/Axl-mediated macrophage polarization. J Clin Invest. 2020;130(6):3021-3037. https://doi.org/10.1172/JCI125505
  16. Wang L, Bi Y, Yu M, et al. Phosphatidylserine-exposing blood cells and microparticles induce procoagulant activity in non-valvular atrial fibrillation. Int J Cardiol. 2018;258:138-143.  https://doi.org/10.1016/j.ijcard.2018.01.116
  17. Dai E, Stewart M, Ritchie B, et al. Calreticulin, a potential vascular regulatory protein, reduces intimal hyperplasia after arterial injury. Arterioscler Thromb Vasc Biol. 1997;17(11):2359-2368. https://doi.org/10.1161/01.atv.17.11.2359
  18. Zimmerman KA, Xing D, Pallero MA, et al. Calreticulin Regulates Neointima Formation and Collagen Deposition following Carotid Artery Ligation. J Vasc Res. 2015;52(5):306-320.  https://doi.org/10.1159/000443884
  19. Fischer CR, Mikami M, Minematsu H et al. Calreticulin inhibits inflammation-induced osteoclastogenesis and bone resorption. J Orthop Res. 2017;35(12):2658-2666. https://doi.org/10.1002/jor.23587
  20. Kuwabara K, Pinsky DJ, Schmidt AM et al. Calreticulin, an antithrombotic agent which binds to vitamin K-dependent coagulation factors, stimulates endothelial nitric oxide production, and limits thrombosis in canine coronary arteries. J Biol Chem. 1995;270(14):8179-8187. https://doi.org/10.1074/jbc.270.14.8179
  21. Kuwabara K, Pinsky DJ, Schmidt AM et al. Calreticulin, an antithrombotic agent which binds to vitamin K-dependent coagulation factors, stimulates endothelial nitric oxide production, and limits thrombosis in canine coronary arteries. J Biol Chem. 1995;270(14):8179-8187. https://doi.org/10.1074/jbc.270.14.8179
  22. Interim guidelines for prevention, diagnosis and treatment of novel coronavirus infection (COVID-19). Version 11 (07.05.2021). Moscow: Ministerstvo zdravoohraneniya Rossijskoj Federacii; 2021. (In Russ.).
  23. Interim guidelines for prevention, diagnosis and treatment of novel coronavirus infection (COVID-19). Version 12 (21.09.2021). M.: Ministerstvo zdravookhraneniya Rossijskoj Federatsii; 2021. (In Russ.).
  24. Interim guidelines for prevention, diagnosis and treatment of novel coronavirus infection (COVID-19). Version 13 (14.10.2021). M.: Ministerstvo zdravoohraneniya Rossijskoj Federacii; 2021. (In Russ.).
  25. Interim guidelines for prevention, diagnosis and treatment of novel coronavirus infection (COVID-19). Version 14 (27.12.2021). Moscow: Ministerstvo zdravoohraneniya Rossijskoj Federacii; 2021. (In Russ.).
  26. Malas MB, Naazie IN, Elsayed N, Mathlouthi A, Marmor R, Clary B. Thromboembolism Risk of COVID-19 Is High and Associated with a Higher Risk of Mortality: A Systematic Review and Meta-Analysis. EClinicalMedicine. 2020;29:100639. https://doi.org/10.1016/j.eclinm.2020.100639
  27. Leytin V, Allen DJ, Mykhaylov S, Lyubimov E, Freedman J. Thrombin-triggered platelet apoptosis. J Thromb Haemost. 2006;4(12):2656-2663. https://doi.org/10.1111/j.1538-7836.2006.02200.x
  28. Lin KH, Chang HC, Lu WJ, Jayakumar T, Chou HC, Fong TH, Hsiao G, Sheu JR. Comparison of the relative activities of inducing platelet apoptosis stimulated by various platelet-activating agents. Platelets. 2009;20(8):575-581.  https://doi.org/10.3109/09537100903315704
  29. Pereira J, Soto M, Palomo I, Ocqueteau M, Coetzee LM, Astudillo S, Aranda E, Mezzano D. Platelet aging in vivo is associated with activation of apoptotic pathways: studies in a model of suppressed thrombopoiesis in dogs. Thromb Haemost. 2002;87(5): 905-909. 
  30. Kalinin RE, Suchkov IA, Agapov AB. Effectiveness of various options of anticoagulant therapy for the treatment of deep vein thrombosis of the lower extremities in routine clinical practice. Flebologiya. 2017;11(1):21-27. (In Russ.). https://doi.org/10.17116/flebo201711121-27
  31. Tovar AM, Teixeira LA, Rembold SM, et al. Bovine and porcine heparins: different drugs with similar effects on human haemodialysis. BMC Res Notes. 2013;6:230.  https://doi.org/10.1186/1756-0500-6-230
Contact the author
Email
Message
The publishing house "Media Sphere" does not provide treatment services, does not give recommendations on contacting medical institutions and specific specialists, on the prescription of medicines and dietary supplements.

Email Confirmation

An email was sent to test@gmail.com with a confirmation link. Follow the link from the letter to complete the registration on the site.

Email Confirmation

Contact us
If you have any questions, complaints or suggestions, please use this feedback form.
Email
Message
The publishing house "Media Sphere" does not provide treatment services, does not give recommendations on contacting medical institutions and specific specialists, on the prescription of medicines and dietary supplements.
Submit Application

You can become an author of one of our magazines, send a request and we will consider it in during the day.

Name
Phone
E-mail
Message
Login
Registration
E-mail
Password
Forgot Password?

Log in to the site using your account in one of the services

Password recovery
E-mail
Login
Register

We use cооkies to improve the performance of the site. By staying on our site, you agree to the terms of use of cооkies. To view our Privacy and Cookie Policy, please. click here.