Maternal malaria induces a procoagulant and antifibrinolytic state that is embryotoxic but responsive to anticoagulant therapy

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Avery, John W ^a   Smith, Geoffrey M ^a   Owino, Simon O ^a,b   Sarr, Demba ^a   Nagy, Tamas ^a   Mwalimu, Stephen ^a,b   Matthias, James ^a   Kelly, Lauren F ^a   Poovassery, Jayakumar S ^a   Middii, Joab D ^a,b   Abramowsky, Carlos ^c   Moore, Julie M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRIN; LOW MOLECULAR WEIGHT HEPARIN;

ABORTION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICOAGULANT THERAPY; ARTICLE; BIRTH WEIGHT; BLOOD ANALYSIS; BLOOD CLOTTING DISORDER; CONTROLLED STUDY; EMBRYONIC HEMORRHAGE; EMBRYONIC NECROSIS; EMBRYOPATHY; EMBRYOTOXICITY; FEMALE; FIBRINOLYSIS; GESTATION PERIOD; HUMAN; HUMAN TISSUE; INFLAMMATION; MAJOR CLINICAL STUDY; MALARIA; MATERNAL DISEASE; MONOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PLASMODIUM CHABAUDI INFECTION; PREGNANCY OUTCOME; PRIMIGRAVIDA; SOLUTIO PLACENTAE; TREATMENT RESPONSE; ANIMAL; BLOOD; BLOOD CLOTTING; HEMOSTASIS; PARASITOLOGY; PREGNANCY; PREGNANCY COMPLICATION; THROMBOPHILIA; TREATMENT OUTCOME; VASCULARIZATION;

ANIMALIA; MUS; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM;

ANIMALS; BIRTH WEIGHT; BLOOD COAGULATION; FEMALE; FIBRINOLYSIS; HEMOSTASIS; HEPARIN, LOW-MOLECULAR-WEIGHT; HUMANS; MALARIA; MICE; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; THROMBOPHILIA; TREATMENT OUTCOME;

EID: 84863012464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031090     Document Type: Article

References (87)

1. Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO, (2010) Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med 7: e1000221.
2. Desai M, Ter Kuile FO, Nosten F, McGready R, Asamoa K, et al. (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93-104.
3. Crocker IP, Tanner OM, Myers JE, Bulmer JN, Walraven G, et al. (2004) Syncytiotrophoblast degradation and the pathophysiology of the malaria-infected placenta. Placenta 25: 273-282.
4. Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW, (2007) Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis 7: 105-117.
5. Brabin BJ, Romagosa C, Abdelgalil S, Menendez C, Verhoeff FH, et al. (2004) The sick placenta-the role of malaria. Placenta 25: 359-378.
6. Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, et al. (2000) The impact of placental malaria on gestational age and birth weight. J Infect Dis 181: 1740-1745.
7. Scifres CM, Nelson DM, (2009) Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol 587: 3453-3458.
8. Mackintosh CL, Beeson JG, Marsh K, (2004) Clinical features and pathogenesis of severe malaria. Trends Parasitol 20: 597-603.
9. Imamura T, Sugiyama T, Cuevas LE, Makunde R, Nakamura S, (2002) Expression of tissue factor, the clotting initiator, on macrophages in Plasmodium falciparum-infected placentas. J Infect Dis 186: 436-440.
10. Poovassery J, Moore JM, (2006) Murine malaria infection induces fetal loss associated with accumulation of Plasmodium chabaudi AS-infected erythrocytes in the placenta. Infect Immun 74: 2839-2848.
11. Poovassery J, Moore JM, (2009) Association of malaria-induced murine pregnancy failure with robust peripheral and placental cytokine responses. Infect Immun 77: 4998-5006.
12. Poovassery JS, Sarr D, Smith G, Nagy T, Moore JM, (2009) Malaria-induced murine pregnancy failure: distinct roles for IFN-gamma and TNF. J Immunol 183: 5342-5349.
13. Perrault SD, Hajek J, Zhong K, Owino SO, Sichangi M, et al. (2009) Human immunodeficiency virus co-infection increases placental parasite density and transplacental malaria transmission in Western Kenya. Am J Trop Med Hyg 80: 119-125.
14. Othoro C, Moore JM, Wannemuehler K, Nahlen BL, Otieno J, et al. (2006) Evaluation of various methods of maternal placental blood collection for immunology studies. Clin Vaccine Immunol 13: 568-574.
15. Moore JM, Shi YP, Othoro C, Nahlen BL, Lal AA, et al. (2003) Comparative flow cytometric analysis of term placental intervillous and peripheral blood from immediate postpartum women in Western kenya. Placenta 24: 779-785.
16. Demas A, Oberstaller J, Debarry J, Lucchi NW, Srinivasamoorthy G, et al. (2011) Applied Genomics: Data Mining Reveals Species-Specific Malaria Diagnostic Targets More Sensitive than 18S rRNA. J Clin Microbiol 49: 2411-2418.
17. Gutierrez G, Sarto A, Berod L, Canellada A, Gentile T, et al. (2004) Regulation of interleukin-6 fetoplacental levels could be involved in the protective effect of low-molecular weight heparin treatment on murine spontaneous abortion. Am J Reprod Immunol 51: 160-165.
18. Bowen JA, Hunt JS, (1999) Expression of cell adhesion molecules in murine placentas and a placental cell line. Biol Reprod 60: 428-434.
19. Lucchi NW, Peterson DS, Moore JM, (2008) Immunologic activation of human syncytiotrophoblast by Plasmodium falciparum. Malar J 7: 42.
20. van Eijk AM, Ayisi JG, ter Kuile FO, Misore AO, Otieno JA, et al. (2003) HIV increases the risk of malaria in women of all gravidities in Kisumu, Kenya. Aids 17: 595-603.
21. Chaisavaneeyakorn S, Moore JM, Mirel L, Othoro C, Otieno J, et al. (2003) Levels of macrophage inflammatory protein 1 alpha (MIP-1 alpha) and MIP-1 beta in intervillous blood plasma samples from women with placental malaria and human immunodeficiency virus infection. Clin Diagn Lab Immunol 10: 631-636.
22. Moore JM, Chaisavaneeyakorn S, Perkins DJ, Othoro C, Otieno J, et al. (2004) Hemozoin differentially regulates proinflammatory cytokine production in human immunodeficiency virus-seropositive and-seronegative women with placental malaria. Infect Immun 72: 7022-7029.
23. Freeman BD, Zehnbauer BA, Buchman TG, (2003) A meta-analysis of controlled trials of anticoagulant therapies in patients with sepsis. Shock 20: 5-9.
24. Levi M, de Jonge E, van der Poll T, (2001) Rationale for restoration of physiological anticoagulant pathways in patients with sepsis and disseminated intravascular coagulation. Crit Care Med 29: S90-94.
25. Matthay MA, (2001) Severe sepsis-a new treatment with both anticoagulant and antiinflammatory properties. N Engl J Med 344: 759-762.
26. Laskin CA, Spitzer KA, Clark CA, Crowther MR, Ginsberg JS, et al. (2009) Low molecular weight heparin and aspirin for recurrent pregnancy loss: results from the randomized, controlled HepASA Trial. J Rheumatol 36: 279-287.
27. Levi M, Lowenberg E, Meijers JC, (2010) Recombinant anticoagulant factors for adjunctive treatment of sepsis. Semin Thromb Hemost 36: 550-557.
28. Francischetti IM, Seydel KB, Monteiro RQ, (2008) Blood coagulation, inflammation, and malaria. Microcirculation 15: 81-107.
29. Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, et al. (2003) Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg 68: 115-119.
30. Levi M, van der Poll T, (2010) Inflammation and coagulation. Crit Care Med 38: S26-34.
31. Dusse LM, Rios DR, Pinheiro MB, Cooper AJ, Lwaleed BA, (2011) Pre-eclampsia: relationship between coagulation, fibrinolysis and inflammation. Clin Chim Acta 412: 17-21.
32. Camerer E, Kolsto AB, Prydz H, (1996) Cell biology of tissue factor, the principal initiator of blood coagulation. Thromb Res 81: 1-41.
33. van der Poll T, Levi M, Hack CE, ten Cate H, van Deventer SJ, et al. (1994) Elimination of interleukin 6 attenuates coagulation activation in experimental endotoxemia in chimpanzees. J Exp Med 179: 1253-1259.
34. Levi M, van der Poll T, ten Cate H, van Deventer SJ, (1997) The cytokine-mediated imbalance between coagulant and anticoagulant mechanisms in sepsis and endotoxaemia. Eur J Clin Invest 27: 3-9.
35. Fried M, Muga RO, Misore AO, Duffy PE, (1998) Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol 160: 2523-2530.
36. Teng YC, Lin QD, Lin JH, Ding CW, Zuo Y, (2009) Coagulation and fibrinolysis related cytokine imbalance in preeclampsia: the role of placental trophoblasts. J Perinat Med 37: 343-348.
37. Levi M, (2010) The coagulant response in sepsis and inflammation. Hamostaseologie 30: 10-12 14-16.
38. Isermann B, Hendrickson SB, Hutley K, Wing M, Weiler H, (2001) Tissue-restricted expression of thrombomodulin in the placenta rescues thrombomodulin-deficient mice from early lethality and reveals a secondary developmental block. Development 128: 827-838.
39. Mackman N, (2009) The many faces of tissue factor. J Thromb Haemost 7 (Suppl 1): 136-139.
40. Coughlin SR, (2000) Thrombin signalling and protease-activated receptors. Nature 407: 258-264.
41. Lucchi NW, Sarr D, Owino SO, Mwalimu SM, Peterson DS, et al. (2011) Natural hemozoin stimulates syncytiotrophoblast to secrete chemokines and recruit peripheral blood mononuclear cells. Placenta 32: 579-585.
42. Rojanasthien S, Surakamolleart V, Boonpucknavig S, Isarangkura P, (1992) Hematological and coagulation studies in malaria. J Med Assoc Thai 75 (Suppl 1): 190-194.
43. Rojanasthien S, Surakamollert V, Isarangkura P, Boonpucknavig S, (1993) A new method for factor VII deficient substrate preparation and coagulation studies in malaria. Southeast Asian J Trop Med Public Health 24 (Suppl 1): 225-228.
44. Prasad R, Das BK, Pengoria R, Mishra OP, Shukla J, et al. (2009) Coagulation Status and Platelet Functions in Children with Severe Falciparum Malaria and their Correlation of Outcome. J Trop Pediatr.
45. Dennis LH, Eichelberger JW, Inman MM, Conrad ME, (1967) Depletion of coagulation factors in drug-resistant Plasmodium falciparum malaria. Blood 29: 713-721.
46. Vogetseder A, Ospelt C, Reindl M, Schober M, Schmutzhard E, (2004) Time course of coagulation parameters, cytokines and adhesion molecules in Plasmodium falciparum malaria. Trop Med Int Health 9: 767-773.
47. Clemens R, Pramoolsinsap C, Lorenz R, Pukrittayakamee S, Bock HL, et al. (1994) Activation of the coagulation cascade in severe falciparum malaria through the intrinsic pathway. Br J Haematol 87: 100-105.
48. Francischetti IM, (2008) Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol 24: 258-263.
49. Aziken ME, Akubuo KK, Gharoro EP, (2011) Efficacy of intermittent preventive treatment with sulfadoxine-pyrimethamine on placental parasitemia in pregnant women in midwestern Nigeria. Int J Gynaecol Obstet 112: 30-33.
50. Isermann B, Sood R, Pawlinski R, Zogg M, Kalloway S, et al. (2003) The thrombomodulin-protein C system is essential for the maintenance of pregnancy. Nat Med 9: 331-337.
51. Guo YH, Hernandez I, Isermann B, Kang TB, Medved L, et al. (2009) Caveolin-1-dependent apoptosis induced by fibrin degradation products. Blood 113: 4431-4439.
52. Petaja J, (2011) Inflammation and coagulation. An overview. Thromb Res 127 (Suppl 2): S34-37.
53. de Jonge E, Dekkers PE, Creasey AA, Hack CE, Paulson SK, et al. (2000) Tissue factor pathway inhibitor dose-dependently inhibits coagulation activation without influencing the fibrinolytic and cytokine response during human endotoxemia. Blood 95: 1124-1129.
54. Al-Ani B, Hewett PW, Cudmore MJ, Fujisawa T, Saifeddine M, et al. (2010) Activation of proteinase-activated receptor 2 stimulates soluble vascular endothelial growth factor receptor 1 release via epidermal growth factor receptor transactivation in endothelial cells. Hypertension 55: 689-697.
55. Estrada-Gutierrez G, Cappello RE, Mishra N, Romero R, Strauss JF 3rd, et al. (2011) Increased expression of matrix metalloproteinase-1 in systemic vessels of preeclamptic women: a critical mediator of vascular dysfunction. Am J Pathol 178: 451-460.
56. Landis SH, Lokomba V, Ananth CV, Atibu J, Ryder RW, et al. (2009) Impact of maternal malaria and under-nutrition on intrauterine growth restriction: a prospective ultrasound study in Democratic Republic of Congo. Epidemiol Infect 137: 294-304.
57. Luxemburger C, McGready R, Kham A, Morison L, Cho T, et al. (2001) Effects of malaria during pregnancy on infant mortality in an area of low malaria transmission. Am J Epidemiol 154: 459-465.
58. Munir M, Tjandra H, Rampengan TH, Mustadjab I, Wulur FH, (1980) Heparin in the treatment of cerebral malaria. Paediatr Indones 20: 47-50.
59. Rampengan TH, (1991) Cerebral malaria in children. Comparative study between heparin, dexamethasone and placebo. Paediatr Indones 31: 59-66.
60. Reid HA, Sucharit P, (1972) Ancrod, heparin, and-aminocaproic acid in simian Knowlesi malaria. Lancet 2: 1110-1112.
61. Howard WA, Collins WE, (1972) Heparin therapy in simian Plasmodium knowlesi malaria. Lancet 2: 738-739.
62. Dennis LH, Conrad ME, (1968) Anticoagulant and antimalarial action of heparin in simian malaria. Lancet 1: 769-771.
63. Stone WJ, Hanchett JE, Knepshield JH, (1972) Acute renal insufficiency due to falciparum malaria. Review of 42 cases. Arch Intern Med 129: 620-628.
64. Smitskamp H, Wolthuis FH, (1971) New concepts in treatment of malignant tertian malaria with cerebral involvement. Br Med J 1: 714-716.
65. Borochovitz D, Crosley AL, Metz J, (1970) Disseminated intravascular coagulation with fatal haemorrhage in cerebral malaria. Br Med J 2: 710.
66. Hall AP, (1976) The treatment of malaria. Br Med J 1: 323-328.
67. Reid HA, (1975) Letter: Adjuvant treatment of severe falciparum malaria, intravascular coagulation, and heparin. Lancet 1: 167-168.
68. Reyburn H, (2010) New WHO guidelines for the treatment of malaria. BMJ 340: c2637.
69. Greer IA, Nelson-Piercy C, (2005) Low-molecular-weight heparins for thromboprophylaxis and treatment of venous thromboembolism in pregnancy: a systematic review of safety and efficacy. Blood 106: 401-407.
70. Linhardt RJ, Gunay NS, (1999) Production and chemical processing of low molecular weight heparins. Semin Thromb Hemost 25 (Suppl 3): 5-16.
71. Merli GJ, Groce JB, (2010) Pharmacological and clinical differences between low-molecular-weight heparins: implications for prescribing practice and therapeutic interchange. P T 35: 95-105.
72. Carlson J, Ekre HP, Helmby H, Gysin J, Greenwood BM, et al. (1992) Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am J Trop Med Hyg 46: 595-602.
73. Rowe A, Berendt AR, Marsh K, Newbold CI, (1994) Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes. Exp Parasitol 79: 506-516.
74. Vogt AM, Pettersson F, Moll K, Jonsson C, Normark J, et al. (2006) Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathog 2: e100.
75. Kyriacou HM, Steen KE, Raza A, Arman M, Warimwe G, et al. (2007) In vitro inhibition of Plasmodium falciparum rosette formation by Curdlan sulfate. Antimicrob Agents Chemother 51: 1321-1326.
76. Leitgeb AM, Blomqvist K, Cho-Ngwa F, Samje M, Nde P, et al. (2011) Low anticoagulant heparin disrupts Plasmodium falciparum rosettes in fresh clinical isolates. Am J Trop Med Hyg 84: 390-396.
77. Havlik I, Looareesuwan S, Vannaphan S, Wilairatana P, Krudsood S, et al. (2005) Curdlan sulphate in human severe/cerebral Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 99: 333-340.
78. Mackinnon MJ, Walker PR, Rowe JA, (2002) Plasmodium chabaudi: rosetting in a rodent malaria model. Exp Parasitol 101: 121-128.
79. Badawy AM, Khiary M, Sherif LS, Hassan M, Ragab A, et al. (2008) Low-molecular weight heparin in patients with recurrent early miscarriages of unknown aetiology. J Obstet Gynaecol 28: 280-284.
80. Rowan JA, McLintock C, Taylor RS, North RA, (2003) Prophylactic and therapeutic enoxaparin during pregnancy: indications, outcomes and monitoring. Aust N Z J Obstet Gynaecol 43: 123-128.
81. Brenner B, (2005) Low-molecular-weight heparin in pregnancy: state of the art. Womens Health (Lond Engl) 1: 153-156.
82. Brenner B, Hoffman R, Blumenfeld Z, Weiner Z, Younis JS, (2000) Gestational outcome in thrombophilic women with recurrent pregnancy loss treated by enoxaparin. Thromb Haemost 83: 693-697.
83. Francischetti IM, Oliveira CJ, Ostera GR, Yager SB, Debierre-Grockiego F, et al. (2011) Defibrotide Interferes With Several Steps of the Coagulation-Inflammation Cycle and Exhibits Therapeutic Potential to Treat Severe Malaria. Arterioscler Thromb Vasc Biol.
84. Francischetti IM, Seydel KB, Monteiro RQ, Whitten RO, Erexson CR, et al. (2007) Plasmodium falciparum-infected erythrocytes induce tissue factor expression in endothelial cells and support the assembly of multimolecular coagulation complexes. J Thromb Haemost 5: 155-165.
85. Kornblum N, Ayyanar K, Benimetskaya L, Richardson P, Iacobelli M, et al. (2006) Defibrotide, a polydisperse mixture of single-stranded phosphodiester oligonucleotides with lifesaving activity in severe hepatic veno-occlusive disease: clinical outcomes and potential mechanisms of action. Oligonucleotides 16: 105-114.
86. Larocca A, Cavallo F, Magarotto V, Rossi D, Patriarca F, et al. (2008) Defibrotide: a review on clinical use and future development. Expert Opin Biol Ther 8: 1201-1212.
87. Richardson P, Linden E, Revta C, Ho V, (2009) Use of defibrotide in the treatment and prevention of veno-occlusive disease. Expert Rev Hematol 2: 365-376.