Elevated Levels of Procoagulant Microvesicles and Tissue-Factor Bearing Microvesicles in Malaria Patients

References

• World Health Organization. World malaria report 2021; 2021. Available from: https://www.who.int/publications/i/item/9789240040496. Accessed March 31, 2023.
   Google Scholar
• Vos T, Lim SS, Abbafati C, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the global burden of disease study 2019. Lancet. 2020;396(10258):1204–1222. doi:10.1016/S0140-6736(20)30925-9
   PubMed Web of Science ®Google Scholar
• Ghosh K, Shetty S. Blood coagulation in falciparum malaria--a review. Parasitol Res. 2008;102(4):571–576. doi:10.1007/s00436-007-0832-0
   PubMed Web of Science ®Google Scholar
• Turner GD, Ly VC, Nguyen TH, et al. Systemic endothelial activation occurs in both mild and severe malaria. Correlating dermal microvascular endothelial cell phenotype and soluble cell adhesion molecules with disease severity. Am J Pathol. 1998;152(6):1477–1487.
   PubMed Web of Science ®Google Scholar
• Moxon CA, Alhamdi Y, Storm J, et al. Parasite histones are toxic to brain endothelium and link blood barrier breakdown and thrombosis in cerebral malaria. Blood Adv. 2020;4(13):2851–2864. doi:10.1182/bloodadvances.2019001258
   PubMed Web of Science ®Google Scholar
• Piccin A, Murphy WG, Smith OP. Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 2007;21(3):157–171. doi:10.1016/j.blre.2006.09.001
   PubMed Web of Science ®Google Scholar
• Shill DD, Lansford KA, Hempel HK, Call JA, Murrow JR, Jenkins NT. Effect of exercise intensity on circulating microparticles in men and women. Exp Physiol. 2018;103(5):693–700. doi:10.1113/EP086644
   PubMed Web of Science ®Google Scholar
• Aharon A, Brenner B. Microparticles and pregnancy complications. Thromb Res. 2011;127(Suppl):S67–71. doi:10.1016/S0049-3848(11)70019-6
   PubMed Web of Science ®Google Scholar
• Burton JO, Hamali HA, Singh R, et al. Elevated levels of procoagulant plasma microvesicles in dialysis patients. PLoS One. 2013;8(8):e72663. doi:10.1371/journal.pone.0072663
   PubMed Web of Science ®Google Scholar
• Hamali H, Elhussein O, Jamil A, Hussain S, Alshraim M, Alshehri A. Elevated levels of pro‑coagulant microvesicles in children in‑steady state sickle cell disease. J Appl Hematol. 2015;6:115–118. doi:10.4103/1658-5127.165650
   Google Scholar
• Shet AS, Aras O, Gupta K, et al. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood. 2003;102(7):2678–2683. doi:10.1182/blood-2003-03-0693
   PubMed Web of Science ®Google Scholar
• Nantakomol D, Dondorp AM, Krudsood S, et al. Circulating red cell-derived microparticles in human malaria. J Infect Dis. 2011;203(5):700–706. doi:10.1093/infdis/jiq104
   PubMed Web of Science ®Google Scholar
• Combes V, Taylor TE, Juhan-Vague I, et al. Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma. JAMA. 2004;291(21):2542–2544. doi:10.1001/jama.291.21.2542-b
   PubMed Web of Science ®Google Scholar
• Campos FMF, Franklin BS, Teixeira-Carvalho A, et al. Augmented plasma microparticles during acute Plasmodium vivax infection. Malar J. 2010;9(1):327. doi:10.1186/1475-2875-9-327
   PubMedGoogle Scholar
• Pankoui Mfonkeu JB, Gouado I, Fotso Kuaté H, et al. Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. PLoS One. 2010;5(10):e13415. doi:10.1371/journal.pone.0013415
   PubMed Web of Science ®Google Scholar
• Sahu U, Sahoo PK, Kar SK, Mohapatra BN, Ranjit M. Association of TNF level with production of circulating cellular microparticles during clinical manifestation of human cerebral malaria. Hum Immunol. 2013;74(6):713–721. doi:10.1016/j.humimm.2013.02.006
   PubMed Web of Science ®Google Scholar
• Faille D, Combes V, Mitchell AJ, et al. Platelet microparticles: a new player in malaria parasite cytoadherence to human brain endothelium. FASEB J. 2009;23(10):3449–3458. doi:10.1096/fj.09-135822
   PubMed Web of Science ®Google Scholar
• Francischetti IMB, Seydel KB, Monteiro RQ, et al. Plasmodium falciparum-infected erythrocytes induce tissue factor expression in endothelial cells and support the assembly of multimolecular coagulation complexes. J Thromb Haemost. 2007;5(1):155–165. doi:10.1111/j.1538-7836.2006.02232.x
   PubMed Web of Science ®Google Scholar
• Hamali HA, Saboor M, Dobie G, et al. Procoagulant microvesicles in COVID-19 patients: possible modulators of inflammation and prothrombotic tendency. Infect Drug Resist. 2022;15:2359–2368. doi:10.2147/IDR.S355395
   PubMed Web of Science ®Google Scholar
• Hamali HA, Mobarki AA, Akhter MS, et al. Elevated levels of procoagulant microvesicles in patients with dengue fever. Future Virol. 2020;15(10):701–706. doi:10.2217/fvl-2020-0202
   Web of Science ®Google Scholar
• Nieuwland R, Berckmans RJ, McGregor S, et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood. 2000;95(3):930–935. doi:10.1182/blood.V95.3.930.003k46_930_935
   PubMed Web of Science ®Google Scholar
• Morel O, Toti F, Hugel B, et al. Procoagulant microparticles: disrupting the vascular homeostasis equation? Arterioscler Thromb Vasc Biol. 2006;26(12):2594–2604. doi:10.1161/01.ATV.0000246775.14471.26
   PubMed Web of Science ®Google Scholar
• Abid Hussein MN, Böing AN, Sturk A, Hau CM, Nieuwland R. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost. 2007;98(5):1096–1107. doi:10.1160/TH05-04-0231
   PubMed Web of Science ®Google Scholar
• Bidot L, Jy W, Bidot CJ, et al. Microparticle-mediated thrombin generation assay: increased activity in patients with recurrent thrombosis. J Thromb Haemost. 2008;6(6):913–919. doi:10.1111/j.1538-7836.2008.02963.x
   PubMed Web of Science ®Google Scholar
• Zwaal RFA, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci. 2005;62(9):971–988. doi:10.1007/s00018-005-4527-3
   PubMed Web of Science ®Google Scholar
• Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost. 2001;85(4):639–646. doi:10.1055/s-0037-1615646
   PubMed Web of Science ®Google Scholar
• Mackman N, Tilley RE, Key NS. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol. 2007;27(8):1687–1693. doi:10.1161/ATVBAHA.107.141911
   PubMed Web of Science ®Google Scholar
• Giesen PLA, Rauch U, Bohrmann B, et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A. 1999;96(5):2311–2315. doi:10.1073/pnas.96.5.2311
   PubMed Web of Science ®Google Scholar
• GASTAT. Riyadh: General Authority for Statistics. Kingdom of Saudi Arabia: Census; 2010.
   Google Scholar
• World Health Organization. Microscopy for the Detection, Identification and Quantification of Malaria Parasites on Stained Thick and Thin Blood Films in Research Settings. Geneva, Switzerland: World Health Organization; 2015.
   Google Scholar
• Fransisca L, Kusnanto JH, Satoto TBT, et al. Comparison of rapid diagnostic test Plasmotec Malaria-3, microscopy, and quantitative real-time PCR for diagnoses of plasmodium falciparum and plasmodium vivax infections in mimika regency, Papua, Indonesia. Malar J. 2015;14:103. doi:10.1186/s12936-015-0615-5
   PubMed Web of Science ®Google Scholar
• Guervilly C, Bonifay A, Burtey S, et al. Dissemination of extreme levels of extracellular vesicles: tissue factor activity in patients with severe COVID-19. Blood Adv. 2021;5(3):628–634. doi:10.1182/bloodadvances.2020003308
   PubMed Web of Science ®Google Scholar
• Combes V, Coltel N, Alibert M, et al. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol. 2005;166(1):295–302. doi:10.1016/S0002-9440(10)62253-5
   PubMed Web of Science ®Google Scholar
• Combes V, Coltel N, Faille D, Wassmer SC, Grau GE. Cerebral malaria: role of microparticles and platelets in alterations of the blood-brain barrier. Int J Parasitol. 2006;36(5):541–546. doi:10.1016/j.ijpara.2006.02.005
   PubMed Web of Science ®Google Scholar
• Mooberry MJ, Bradford R, Hobl EL, Lin FC, Jilma B, Key NS. Procoagulant microparticles promote coagulation in a factor XI-dependent manner in human endotoxemia. J Thromb Haemost. 2016;14(5):1031–1042. doi:10.1111/jth.13285
   PubMed Web of Science ®Google Scholar
• Sinauridze EI, Kireev DA, Popenko NY, et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost. 2007;97(3):425–434. doi:10.1160/TH06-06-0313
   PubMed Web of Science ®Google Scholar
• Wolberg AS, Monroe DM, Roberts HR, Hoffman MR. Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and -independent mechanisms. Blood Coagul Fibrinolysis an Int J Haemost Thromb. 1999;10(4):201–210. doi:10.1097/00001721-199906000-00007
   PubMed Web of Science ®Google Scholar
• Hron G, Kollars M, Binder BR, Eichinger S, Kyrle PA. Identification of patients at low risk for recurrent venous thromboembolism by measuring thrombin generation. JAMA. 2006;296(4):397–402. doi:10.1001/jama.296.4.397
   PubMed Web of Science ®Google Scholar
• Hrachovinová I, Cambien B, Hafezi-Moghadam A, et al. Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nat Med. 2003;9(8):1020–1025. doi:10.1038/nm899
   PubMed Web of Science ®Google Scholar
• Szotowski B, Antoniak S, Poller W, Schultheiss HP, Rauch U. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res. 2005;96(12):1233–1239. doi:10.1161/01.RES.0000171805.24799.fa
   PubMed Web of Science ®Google Scholar
• Rosell A, Havervall S, von Meijenfeldt F, et al. Patients with COVID-19 have elevated levels of circulating extracellular vesicle tissue factor activity that is associated with severity and mortality-brief report. Arterioscler Thromb Vasc Biol. 2021;41(2):878–882. doi:10.1161/ATVBAHA.120.315547
   PubMed Web of Science ®Google Scholar
• Østerud B, Bjørklid E. The tissue factor pathway in disseminated intravascular coagulation. Semin Thromb Hemost. 2001;27(6):605–617. doi:10.1055/s-2001-18866
   PubMed Web of Science ®Google Scholar
• Abbate R, Cioni G, Ricci I, Miranda M, Gori AM. Thrombosis and acute coronary syndrome. Thromb Res. 2012;129(3):235–240. doi:10.1016/j.thromres.2011.12.026
   PubMed Web of Science ®Google Scholar
• Moxon CA, Chisala NV, Mzikamanda R, et al. Laboratory evidence of disseminated intravascular coagulation is associated with a fatal outcome in children with cerebral malaria despite an absence of clinically evident thrombosis or bleeding. J Thromb Haemost. 2015;13(9):1653–1664. doi:10.1111/jth.13060
   PubMed Web of Science ®Google Scholar
• Liechti ME, Zumsteg V, Hatz CFR, Herren T. Plasmodium falciparum cerebral malaria complicated by disseminated intravascular coagulation and symmetrical peripheral gangrene: case report and review. Eur J Clin Microbiol Infect Dis off Publ Eur Soc Clin Microbiol. 2003;22(9):551–554. doi:10.1007/s10096-003-0984-5
   PubMed Web of Science ®Google Scholar
• Nielsen MH, Beck-Nielsen H, Andersen MN, Handberg A. A flow cytometric method for characterization of circulating cell-derived microparticles in plasma. J Extracell Vesicles. 2014;3(1):20795. doi:10.3402/jev.v3.20795
   PubMedGoogle Scholar
• Herring JM, McMichael MA, Smith SA. Microparticles in health and disease. J Vet Intern Med. 2013;27(5):1020–1033. doi:10.1111/jvim.12128
   PubMed Web of Science ®Google Scholar
• Asare R, Opoku-Okrah C, Danquah KO, et al. Assessment of platelet indices and platelet activation markers in children with Plasmodium falciparum malaria. Malar J. 2020;19(1):143. doi:10.1186/s12936-020-03218-4
   PubMedGoogle Scholar
• Moulin F, Lesage F, Legros A-H, et al. Thrombocytopenia and Plasmodium falciparum malaria in children with different exposures. Arch Dis Child. 2003;88(6):540LP–541. doi:10.1136/adc.88.6.540
   Web of Science ®Google Scholar
• Hamali HA. The mighty role of platelets in immunity, inflammation, cancer and angiogenesis. Majmaah J Heal Sci. 2020;8(1):65–81. doi:10.5455/mjhs.2020.01.008
   Google Scholar
• Coltel N, Combes V, Wassmer SC, Chimini G, Grau GE. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 2006;8(8):2305–2316. doi:10.1016/j.micinf.2006.04.006
   PubMed Web of Science ®Google Scholar
• Chimalizeni Y, Kawaza K, Taylor T, Molyneux M. The platelet count in cerebral malaria, is it useful to the clinician? Am J Trop Med Hyg. 2010;83(1):48–50. doi:10.4269/ajtmh.2010.09-0614
   PubMed Web of Science ®Google Scholar
• Brejt JA, Golightly LM. Severe malaria: update on pathophysiology and treatment. Curr Opin Infect Dis. 2019;32(5):413–418. doi:10.1097/QCO.0000000000000584
   PubMed Web of Science ®Google Scholar
• Trappenburg MC, van Schilfgaarde M, Marchetti M, et al. Elevated procoagulant microparticles expressing endothelial and platelet markers in essential thrombocythemia. Haematologica. 2009;94(7):911–918. doi:10.3324/haematol.13774
   PubMed Web of Science ®Google Scholar
• Erdman LK, Finney CAM, Liles WC, Kain KC. Inflammatory pathways in malaria infection: tLRs share the stage with other components of innate immunity. Mol Biochem Parasitol. 2008;162(2):105–111. doi:10.1016/j.molbiopara.2008.08.006
   PubMed Web of Science ®Google Scholar
• Ardoin SP, Shanahan JC, Pisetsky DS. The role of microparticles in inflammation and thrombosis. Scand J Immunol. 2007;66(2–3):159–165. doi:10.1111/j.1365-3083.2007.01984.x
   PubMed Web of Science ®Google Scholar
• Verhamme P, Hoylaerts MF. Hemostasis and inflammation: two of a kind? Thromb J. 2009;7:15. doi:10.1186/1477-9560-7-15
   PubMedGoogle Scholar
• Egorina EM, Sovershaev MA, Hansen J-B. The role of tissue factor in systemic inflammatory response syndrome. Blood Coagul Fibrinolysis an Int J Haemost Thromb. 2011;22(6):451–456. doi:10.1097/MBC.0b013e328346ef3f
   PubMed Web of Science ®Google Scholar
• Crews FT, Zou J, Coleman LGJ. Extracellular microvesicles promote microglia-mediated pro-inflammatory responses to ethanol. J Neurosci Res. 2021;99(8):1940–1956. doi:10.1002/jnr.24813
   PubMed Web of Science ®Google Scholar
• Mantel P-Y, Hoang AN, Goldowitz I, et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe. 2013;13(5):521–534. doi:10.1016/j.chom.2013.04.009
   PubMed Web of Science ®Google Scholar
• Butenas S. Tissue factor structure and function. Scientifica. 2012;2012:964862. doi:10.6064/2012/964862
   PubMedGoogle Scholar
• Couper KN, Barnes T, Hafalla JCR, et al. Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PLoS Pathog. 2010;6(1):e1000744. doi:10.1371/journal.ppat.1000744
   PubMed Web of Science ®Google Scholar
• Morel O, Toti F, Hugel B, Freyssinet J-M. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11(3):156–164. doi:10.1097/01.moh.0000131441.10020.87
   PubMed Web of Science ®Google Scholar
• Pluskota E, Woody NM, Szpak D, et al. Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood. 2008;112(6):2327–2335. doi:10.1182/blood-2007-12-127183
   PubMed Web of Science ®Google Scholar
• Del Conde I, Shrimpton CN, Thiagarajan P, López JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood. 2005;106(5):1604–1611. doi:10.1182/blood-2004-03-1095
   PubMed Web of Science ®Google Scholar
• Trelka DP, Schneider TG, Reeder JC, Taraschi TF. Evidence for vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol. 2000;106(1):131–145. doi:10.1016/s0166-6851(99)00207-8
   PubMed Web of Science ®Google Scholar
• Kimbi HK, Sumbele IUN, Nweboh M, et al. Malaria and haematologic parameters of pupils at different altitudes along the slope of Mount Cameroon: a cross-sectional study. Malar J. 2013;12(1):193. doi:10.1186/1475-2875-12-193
   PubMedGoogle Scholar
• Francischetti IMB, Seydel KB, Monteiro RQ. Blood coagulation, inflammation, and malaria. Microcirculation. 2008;15(2):81–107. doi:10.1080/10739680701451516
   PubMed Web of Science ®Google Scholar