Pathogenesis of malaria in tissues and blood

Mediterranean Journal of Hematology and Infectious Diseases

Volumn 4, Issue 1, 2012, Pages

  Autino, Beatrice ^a   Corbett, Yolanda ^b   Castelli, Francesco ^a   Taramelli, Donatella ^b  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT RESPIRATORY DISTRESS SYNDROME; ANEMIA; CELL ADHESION; CLINICAL FEATURE; COMPLEMENT ACTIVATION; DISEASE ASSOCIATION; DISEASE SEVERITY; HUMAN; INNATE IMMUNITY; KIDNEY FAILURE; LIVER FAILURE; MALARIA; NONHUMAN; PARASITE TRANSMISSION; PATHOGENESIS; PLACENTA MALARIA; REVIEW; THROMBOCYTOPENIA;

EID: 84875974853     PISSN: None     EISSN: 20353006     Source Type: Journal    
DOI: 10.4084/MJHID.2012.061     Document Type: Review

References (135)

1. World Health Organization (WHO) World Malaria Report 2011.
2. Marchiafava F, Bignami A. Sulle febbri malariche estivoautunnali. 1892. Rome: Loescher
3. Kyes S, Horrocks P, and Newbold C. Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 2001, 55: 673-707. http://dx.doi.org/10.1146/annurev.micro.55.1.673 PMid:11544371
4. Scherf A, Lopez-Rubio JJ, and Riviere L. Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 2008, 62: 445-470. http://dx.doi.org/10.1146/annurev.micro.61.080706.093134 PMid:18785843
5. Carvalho B O, Lopes SC, Nogueira PA, Orlandi PP, Bargieri DY, Blanco YC, Mamoni R, Leite JA, Rodrigues MM, Soares IS, Oliveira TR, Wunderlich G, Lacerda MV, del Portillo HA, Araújo MO, Russell B, Suwanarusk R, Snounou G, Rénia L, and Costa FT. On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis 2010, 202: 638-647. http://dx.doi.org/10.1086/654815 PMid:20617923
6. Grau GE, Craig AG. Cerebral malaria pathogenesis: revisiting parasite and host contributions. Future Microbiol. 2012, 7(2):291-302. http://dx.doi.org/10.2217/fmb.11.155 PMid:22324996
7. Dondorp AM, Pongponratn E, and White NJ. Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Trop 2004, 89: 309-317. http://dx.doi.org/10.1016/j.actatropica.2003.10.004 PMid:14744557
8. Chakravorty SJ, and Craig A. The role of ICAM-1 in Plasmodium falciparum cytoadherence. Eur J Cell Biol 2005, 84: 15-27. http://dx.doi.org/10.1016/j.ejcb.2004.09.002 PMid:15724813
9. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, and Nagachinta B. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 1994,145: 1057-1069 PMid:7526692 PMCid:1887431
10. Milner DA Jr. Rethinking cerebral malaria pathology. Curr Opin Infect Dis. 2010, 23:456-63. http://dx.doi.org/10.1097/QCO.0b013e32833c3dbe PMid:20613511
11. Fried M, Domingo GJ, Gowda CD, Mutabingwa TK, and Duffy PE. Plasmodium falciparum: chondroitin sulfate A is the major receptor for adhesion of parasitized erythrocytes in the placenta. Exp Parasitol 2006, 113: 36-42 http://dx.doi.org/10.1016/j.exppara.2005.12.003 PMid:16430888
12. Reeder JC, Cowman AF, Davern KM, Beeson JG, Thompson JK, Rogerson SJ, and Brown GV. The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1. Proc Natl Acad Sci USA. 1999, 96: 5198-5202. http://dx.doi.org/10.1073/pnas.96.9.5198
13. Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis, 2007, 7: 105-117. http://dx.doi.org/10.1016/S1473-3099(07)70022-1
14. von Itzstein, M, Plebanski M, Cooke BM, and Coppel RL. Hot, sweet and sticky: the glycobiology of Plasmodium falciparum. Trends Parasitol 2008, 24: 210-218. http://dx.doi.org/10.1016/j.pt.2008.02.007 PMid:18420458
15. Rowe JA, Claessens A, Corrigan RA, and Arman M. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 2009, 11: e16. http://dx.doi.org/10.1017/S1462399409001082 PMid:19467172 PMCid:2878476
16. Chen Q, Barragan A, Fernandez V, Sundström A, Schlichtherle M, Sahlén A, Carlson J, Datta S, and Wahlgren M. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 1998,187: 15-23. http://dx.doi.org/10.1084/jem.187.1.15 PMid:9419207 PMCid:2199182
17. Vogt, AM, Barragan A, Chen Q, Kironde F, Spillmann D, and Wahlgren M. Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood 2003, 101: 2405-2411. http://dx.doi.org/10.1182/blood-2002-07-2016 PMid:12433689
18. Barragan, A, Kremsner PG, Wahlgren M, and Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 2000,68: 2971-2975 http://dx.doi.org/10.1128/IAI.68.5.2971-2975.2000 PMid:10768996 PMCid:97511
19. Rowe, J A, Handel IG, Thera MA, Deans AM, Lyke KE, Koné A, Diallo DA, Raza A, Kai O, Marsh K, Plowe CV, Doumbo OK, and Moulds JM. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci USA 2007, 104: 17471-17476. http://dx.doi.org/10.1073/pnas.0705390104 PMid:17959777 PMCid:2077280
20. Udomsanpetch, R, Thanikkul K, Pukrittayakamee S, and White NJ. Rosette formation by Plasmodium vivax. Trans R Soc Trop Med Hyg 1995, 89: 635-637. http://dx.doi.org/10.1016/0035-9203(95)90422-0
21. Angus, BJ, Thanikkul K, Silamut K, White NJ, and Udomsangpetch R. Short report: Rosette formation in Plasmodium ovale infection. Am J Trop Med Hyg 1996, 55: 560-561. PMid:8940990
22. Doumbo, OK, Thera MA, A. K. Koné AK, Raza A, Tempest LJ, Lyke KE, Plowe CV, and Rowe JA. High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am J Trop Med Hyg 2009, 81: 987-993. http://dx.doi.org/10.4269/ajtmh.2009.09-0406 PMid:19996426 PMCid:2877664
23. Le Scanf, C, Vigan-Womas I, Contamin H, Guillotte M, Bischoff E, and Mercereau-Puijalon O. Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey. Microbes Infect 2008, 10: 447-451. http://dx.doi.org/10.1016/j.micinf.2007.12.012 PMid:18400545
24. Uyoga, S, Skorokhod OA, Opiyo M, Orori EN, Williams TN, Arese P, and Schwarzer E. Transfer of 4-hydroxynonenal from parasitized to non-parasitized erythrocytes in rosettes. Proposed role in severe malaria anemia. Br J Haematol. 2012, [Epub ahead of print] http://dx.doi.org/10.1111/j.1365-2141.2011.09015.x PMid:22352722 PMCid:3412292
25. Stevenson, MM, and Riley EM. Innate immunity to malaria. Nat Rev Immunol 2004, 4: 169-180. http://dx.doi.org/10.1038/nri1311 PMid:15039754
26. Urban, BC, Ing R, and Stevenson MM. Early interactions between blood-stage plasmodium parasites and the immune system. Curr Top Microbiol Immunol 2005, 297: 25-70. http://dx.doi.org/10.1007/3-540-29967-X_2
27. Taramelli, D, Recalcati S, Basilico N, Olliaro P, and Cairo G. Macrophage preconditioning with synthetic malaria pigment reduces cytokine production via heme iron-dependent oxidative stress. Lab. Invest 2000, 80, 1-8. http://dx.doi.org/10.1038/labinvest.3780189 PMid:11140691
28. Kwiatkowski, D, Hill AV, Sambou I, Twumasi P, Castracane J, Manogue KR, Cerami A, Brewster DR, and Greenwood BM. TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 1990, 336: 1201-1204. http://dx.doi.org/10.1016/0140-6736(90)92827-5
29. Treeratanapiboon, L, Psathaki, K, Wegener, J, Looareesuwan, S, Galla, HJ, Udomsangpetch, R, In vitro study of malaria parasite induced disruption of blood-brain barrier. Biochem. Biophys. Res. Commun. 2005, 335, 810-818. http://dx.doi.org/10.1016/j.bbrc.2005.07.151 PMid:16105659
30. Janeway, CA, and Medzhitov, R. Innate immunity recognition. Ann Rev Immunol. 2002, 20:197-216 http://dx.doi.org/10.1146/annurev.immunol.20.083001.084359 PMid:11861602
31. Krishnegowda, G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, Akira S, Woods AS, and Gowda DC. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 2005,280: 8606-8616. http://dx.doi.org/10.1074/jbc.M413541200 PMid:15623512
32. Coban, C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, Horii T, and Akira S. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 2005, 201: 19-25. http://dx.doi.org/10.1084/jem.20041836 PMid:15630134 PMCid:2212757
33. Shio, MT, Tiemi Shio M, Eisenbarth SC, Savaria M, Vinet AF, Bellemare MJ, Harder KW, Sutterwala FS, Bohle DS, Descoteaux A, Flavell RA, and Olivier M. Malarial hemozoin activates the NLP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 2009, 5: e1000559. http://dx.doi.org/10.1371/journal.ppat.1000559 PMid:19696895 PMCid:2722371
34. Luty AJ, Kun JF, and Kremsner PG. Mannose-Binding Lectin Plasma Levels and Gene Polymorphisms in Plasmodium falciparum Malaria. J Infect. Dis 1998, 178: 1221-1224. http://dx.doi.org/10.1086/515690 PMid:9806066
35. Riley EM, Wahl S, Perkins DJ, Schofield L. Regulating immunity to malaria. Parasite Immunol. 2006,28:35-49. http://dx.doi.org/10.1111/j.1365-3024.2006.00775.x PMid:16438675
36. Langhorne, JF, Ndungu M, Sponaas AM, and Marsh K. Immunity to malaria: more questions than answers. Nat Immunol 2008,9: 725-732. http://dx.doi.org/10.1038/ni.f.205 PMid:18563083
37. Fried M, Nosten F, Brockman A, Brabin BJ, and Duffy PE. Maternal antibodies block malaria. Nature 1998,395: 851-852. http://dx.doi.org/10.1038/27570 PMid:9804416
38. Miller, LH, Baruch DI, K. Marsh K, and Doumbo OK. The pathogenic basis of malaria. Nature 2002, 415: 673-679. http://dx.doi.org/10.1038/415673a PMid:11832955
39. Nussenblatt V, Semba RD. Micronutrient malnutrition and the pathogenesis of malarial anemia. Acta Trop. 2002,82: 321-37 http://dx.doi.org/10.1016/S0001-706X(02)00049-9
40. Ghosh K, Ghosh K. Pathogenesis of anemia in malaria: a concise review. Parasitol Res. 2007, 101: 1463-9. http://dx.doi.org/10.1007/s00436-007-0742-1 PMid:17874326
41. Haldar K, Mohandas N. Malaria, erythrocytic infection and anemia. Hematology Am Soc Hematol Educ Program. 2009, 1: 87-93 http://dx.doi.org/10.1182/asheducation-2009.1.87 PMid:20008186 PMCid:2933134
42. Skorokhod OA, Caione L, Marrocco T, Migliardi G, Barrera V, Arese P, Piacibello W, Schwarzer E. Inhibition of erythropoiesis in malaria anemia: role of hemozoin and hemozoin-generated 4-hydroxynonenal. Blood. 2010,116:4328-37. http://dx.doi.org/10.1182/blood-2010-03-272781 PMid:20686121
43. Perkins DJ, Were T, Davenport GC, Kempaiah P, Hittner JB, Ong'echa JM. Severe malarial anemia: innate immunity and pathogenesis. Int J Biol Sci. 2011, 7: 1427-42. http://dx.doi.org/10.7150/ijbs.7.1427 PMid:22110393 PMCid:3221949
44. Pasvol G, Clough B, and Carlsson J. Malaria and red cell membrane. Blood 1992, 6: 183-92. http://dx.doi.org/10.1016/0268-960X(92)90014-H
45. Nweneka CV, Doherty CP, Cox S, Prentice A. Iron delocalization in the pathogenesis of malarial anaemia. Trans R Soc Trop Med Hyg. 2010, 104: 175-84. http://dx.doi.org/10.1016/j.trstmh.2009.08.007 PMid:19783267
46. Buffet PA, Safeukui I, Milon G, Marcereau-Puijalon O, David PH. Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr Opin Hematol. 2009, 16: 157-64. http://dx.doi.org/10.1097/MOH.0b013e32832a1d4b PMid:19384231
47. McDevitt MM, Xie J, Shanmugasundaram G, Griffith J, Liu A, McDonald C, Thuma P, Gordeuk VR, Metz CN, Mitchell R, Keefer J, David J, Leng L, Bucala R. A critical role for the host mediator macrophage migration inhibitory factor in the pathogenesis of malarial anaemia. J Exp Med. 2006, 203: 1185-96. http://dx.doi.org/10.1084/jem.20052398 PMid:16636133 PMCid:2121202
48. Pradhan P. Malarial anaemia and nitric oxide induced megaloblastic anaemia: a review on the causes of malarial anaemia. J Vector Borne Dis. 2009, 46: 100-8. PMid:19502689
49. Chang KH, Tam M, Stevenson MM. Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursor. Blood. 2004, 103: 3727-35. http://dx.doi.org/10.1182/blood-2003-08-2887 PMid:14739226
50. de Mast Q, Syafruddin D, Keijmel S, Riekerink TO, Deky O, Asih PB, Swinkels DW, van ser Ven AJ. Increased serum hepcidin and alterations in blood iron parameters associated with asymptomatic P. falciparum and P. vivax malaria. Haematologica. 2010, 95: 1068-74. http://dx.doi.org/10.3324/haematol.2009.019331 PMid:20133896 PMCid:2895029
51. Robson KJH, Weatherall DJ. Malarial anemia and STAT6. Haematologica. 2009, 94: 157-9. http://dx.doi.org/10.3324/haematol.2008.002311 PMid:19181787 PMCid:2635405
52. Thawani N, Tam M, Stevenson MM. STAT6-mediated suppression of erythropoiesis in an experimental model of malarial anemia. Haematologica. 2008, 94: 195-204. http://dx.doi.org/10.3324/haematol.13422 PMid:19109218 PMCid:2635397
53. Haldar K, Murphy SC, Milner DA, Taylor TE. Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Ann Rev Pathol Mech Dis. 2007, 2: 217-49. http://dx.doi.org/10.1146/annurev.pathol.2.010506.091913 PMid:18039099
54. Maina RN, Walsh D, Gaddy C, Hongo G, Waitumbi J, Otieno L, Jones D, Ogutu BR. Impact of Plasmodium falciparum infection on haematological parameters in children living in Western Kenya. Malar J. 2010, 9: S4. http://dx.doi.org/10.1186/1475-2875-9-S3-S4 PMid:21144084 PMCid:3002140
55. Kochar DK, Das A, Kochar A, Middha S, Acharya J, Tanwar GS, Gupta A, Pakalapati D, Garg S, Saxena V, Subudhi AK, Boopathi PA, Sirohi P, Kochar SK. Thrombocytopenia in Plasmodium falciparum, Plasmodium vivax and mixed infection malaria: a study from Bikaner (Northwestern India). Platelets. 2010, 21: 623-7. http://dx.doi.org/10.3109/09537104.2010.505308 PMid:21050055
56. Leowattana W, Tangpukdee N, Thar SK, Nakasiri S, Srivilarit S, Kano S, Wilairatana P, Krudsood S. Changes in platelet count in uncomplicated and severe falciparum malaria. Southeast Asian J Trop Med Public Health. 2010, 41: 1035-41. PMid:21073022
57. Tan SO, McGready R, Zwang J, Pimanpanarak M, Sriprawat K, Thwai KL, Moo Y, Ashley EA, Edwards B, Singhasivanon P, White NJ, Nosten F. Thrombocytopaenia in pregnant women with malaria on the Thai-Burmese border. Malar J. 2008, 7:209. http://dx.doi.org/10.1186/1475-2875-7-209 PMid:18922167 PMCid:2579302
58. Lacerda MV, Mourão MP, Coelho HC, Santos JB. Thrombocytopenia in malaria: who cares. Mem Inst Oswaldo Cruz. 2011, 106: 52-63. http://dx.doi.org/10.1590/S0074-02762011000900007
59. de Mast Q, Groot E, Asih PB, Syafruddin D, Oosting M, Sebastian S, Ferwerda B, Netea MG, de Groot PG, van der Ven AJ, Fijnheer R. ADAMTS13 deficiency with elevated levels of ultra-large and active von Willebrand factor in P. falciparum and P. vivax malaria. Am J Trop Med Hyg. 2009, 80: 492-8. PMid:19270304
60. de Mast Q, de Groot PG, van Heerde WL, Roestenberg M, van Velzen JF, Verbruggen B, Roest M, McCall M, Nieman AE, Westendorp J, Syafruddin D, Fijnheer R, van Dongen-Lases EC, Sauerwein RW, van der Ven AJ. Thrombocytopenia in early malaria is associated with GP1b shedding in absence of systemic platelet activation and consumptive coagulopathy. Br J Haematol. 2010, 151: 495-503. http://dx.doi.org/10.1111/j.1365-2141.2010.08399.x PMid:20955404
61. Chaudhary SC, Sonkar SK, Kumar V, Gupta A. Falciparum malaria presenting as subdural haematoma. J Assoc Physicians India. 2011, 59: 325-6. PMid:21751613
62. Seshadri P, Dev AV, Viggeswarpu S, Sathyendra S, Peter JV. Acute pancreatitis and subdural haematoma in a patient with severe falciparum malaria: case report and review of literature. Malar J. 2008, 7:97 http://dx.doi.org/10.1186/1475-2875-7-97 PMid:18510778 PMCid:2426706
63. Misra DP, Das S, Pattnaik M, Singh SC, Jena RK. Relationship of hepatic and renal dysfunction with haemorrheological parameters in Plasmodium falciparum malaria. J Assoc Physicians India. 2011, 59: 552-6 PMid:22334967
64. WHO. Guidelines for the treatment of malaria. 2nd Ed., Geneva, World Health Organization. 2010
65. Sahu S, Mohanty NK, Rath J, Patnaik SB. Spectrum of malaria complications in an intensive care unit. Singapore Med J. 2010; 51: 226-9 PMid:20428736
66. Sharma A, Khanduri U. How benign is benign tertian malaria. J Vector Born Dis. 2009; 46: 141-4 PMid:19502694
67. Saleri N, Gulletta M, Matteelli A, Caligaris S, Tomasoni LR, Antonini B, Perandin F, Castelli F. Acute Respiratory Distress Syndrome in Plasmodium vivax malaria from Venezuela. Journal of Travel Medicine, 2006; 13: 112-113 http://dx.doi.org/10.1111/j.1708-8305.2006.00024.x PMid:16553597
68. Agarwal R, Nath A, Gupta D. Noninvasive ventilation in Plasmodium vivax related ALI/ARDS. Intern Med. 2007; 46: 2007-11 http://dx.doi.org/10.2169/internalmedicine.46.0401 PMid:18084125
69. Price L, Planche T, Rayner C, Krishna S. Acute respiratory distress syndrome in Plasmodium vivax malaria: case report and review of the literature. Trans R Soc Trop Med Hyg. 2007; 101: 655-9 http://dx.doi.org/10.1016/j.trstmh.2007.02.014 PMid:17433389
70. Haydoura S, Mazboudi O, Charafeddine K, Bouakl I, Baban TA, Taher AT, Kanj SS. Transfusion-related Plasmodium ovale malaria complicated by acute respiratory distress syndrome (ARDS) in a non endemic country. Parasitol Int. 2011; 60: 114-6 http://dx.doi.org/10.1016/j.parint.2010.10.005 PMid:20971212
71. Daneshvar C, Davis TM, Cox-Sing J, Rafa'ee MZ, Zakaria SK, Divis PC, Singh B. Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis. 2009; 49: 852-60 http://dx.doi.org/10.1086/605439 PMid:19635025 PMCid:2843824
72. William T, Menon J, Rajahram G, Chan L, Ma G, Donaldson S, Khoo S, Fredrick C, Jelip J, Anstey NM, Yeo TW. Severe Plasmodium knowlesi malaria in a terziary care hospital, Sabah, Malaysia. Emerg Infect Dis. 2011; 17: 1248-55 http://dx.doi.org/10.3201/eid1707.101017 PMid:21762579 PMCid:3381373
73. Sabbatani S, Fiorino S, Manfredi R. The emerging of the fifth malaria parasite (Plasmodium knowlesi). A public health concern. Braz Infect Dis. 2010; 14: 299-309 http://dx.doi.org/10.1590/S1413-86702010000300019 PMid:20835518
74. Mohan A, Sharma SK, Bollineni S. Acute lung injury and acute respiratory distress syndrome in malaria. J Vector Borne Dis. 2008; 45: 179-93 PMid:18807374
75. Gupta D, Ramanathan RP, Aggarwal AN, Jindal SK. Assessment of factors predicting outcome of acute respiratory distress syndrome in North India. Respirology. 2001; 6: 125-30 http://dx.doi.org/10.1046/j.1440-1843.2001.00324.x PMid:11422891
76. Anstey NM, Jacups SP, Cain T, Pearson T, Ziesing PJ, Fisher DA, Marks BJ, Maguire GP. Pulmonary manifestations of uncomplicated falciparum and vivax malaria: cough, small airways obstruction, impaired gas transfer, and increased pulmonary phagocytic activity. J Infect Dis. 2002; 185: 1326-34 http://dx.doi.org/10.1086/339885 PMid:12001051
77. Ephiphanio S, Campos MG, Pamplona A, Carapau D, Pena AC, Ataíde R, Monteiro CA, Félix N, Costa-Silva A, Marinho CR, Dias S, Mota MM. VEGF promotes malaria-associated acute lung injury in mice. PLoS Pathog. 2010; 6: e1000916 http://dx.doi.org/10.1371/journal.ppat.1000916 PMid:20502682 PMCid:2873913
78. Hee L, Dinudom A, Mitchell AJ, Grau GE, Cook DI, Hunt NH, Ball HJ. Reduced activity of the epithelial sodium channel in malaria-induced pulmonary oedema in mice. Int J Parasitol. 2011; 41: 81-8 http://dx.doi.org/10.1016/j.ijpara.2010.07.013 PMid:20816846
79. van den Steen PA, Geurts N, Deroost K, van Aelst I, Verhenne S, Heremans H, van Damme J, Opdenakker G. Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med. 2010; 181: 957-68 http://dx.doi.org/10.1164/rccm.200905-0786OC PMid:20093644
80. Seydel KB, Milner DA, Kamiza SB, Molyneux ME, Taylor TE. The distribution and intensity of parasite sequestration in comatose Malawian children. J Infect Dis. 2006; 194: 208-15 http://dx.doi.org/10.1086/505078 PMid:16779727 PMCid:1515074
81. Gillrie MR, Krishnegowda G, Lee K, Buret AG, Robbins SM, Looareesuwan S, Gowda DC, Ho M. Src-family kinase-dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood. 2007; 110: 3426-35 http://dx.doi.org/10.1182/blood-2007-04-084582 PMid:17693580 PMCid:2200906
82. Anand AC, Ramji C, Narula AS, Singh W. Malarial hepatitis: a heterogeneous syndrome. Natl Med J India. 1992; 5: 59-62 PMid:1304265
83. Mazumder R, Mishra RK, Mazumder H, Mukherjee P. Jaundice in falciparum malaria - some prospective observations. J Indian Med Assoc. 2002; 100: 312-4 PMid:12418632
84. Murthy GL, Sahay RK, Sreenivas DV, Sundaram C, Shantaram V. Hepatitis in falciparum malaria. Trop Gastroenterol. 1998; 19: 152-4 PMid:10228440
85. Sung YH, Park JM. A case of malarial hepatitis by Plasmodium vivax. Korean J Gastroenterol. 2010; 56: 329-33 http://dx.doi.org/10.4166/kjg.2010.56.5.329 PMid:21099242
86. Das SN, Mohapatra B, Mohanty R, Dash PC, Kar K, Dash PK. Malarial hepatitis as a component of multiorgan failure - a bad prognostic sign. J Indian Med Assoc. 2007; 105: 247-50 PMid:17915792
87. Ali H, Ahsan T, Mahmood T, Bakht SF, Faroog MU, Ahmed N. Parasite density and the spectrum of clinical illness in falciparum malaria. J Coll Physicians Surg Pak. 2008; 18: 362-8 PMid:18760048
88. Anand AC, Puri P. Jaundice in malaria. J Gastroenterol Hepatol. 2005; 20: 1322-32 http://dx.doi.org/10.1111/j.1440-1746.2005.03884.x PMid:16105116
89. Kochar DK, Singh P, Agarwal P, Kochar SK, Pokharna R, Sareen PK. Malarial hepatitis. J Assoc Physicians India 2003; 51: 1069-72 PMid:15260391
90. Bhalla A, Suri V, Singh V. Malarial hepatopathy. J Postgrad Med. 2006; 52: 315-20 PMid:17102560
91. Kochar DK, Agarwal P, Kochar SK, Jain R, Rawat N, Pokharna RK, Kachhawa S, Srivastava T. Hepatocyte dysfunction and hepatic encephalopathy in Plasmodium falciparum malaria. Q J Med. 2003; 96: 505-12 http://dx.doi.org/10.1093/qjmed/hcg091 PMid:12881593
92. Naicker S, Aboud O, Gharbi MB. Epidemiology of acute kidney injury in Africa. Semin Nephrol. 2008; 28: 348-53 http://dx.doi.org/10.1016/j.semnephrol.2008.04.003 PMid:18620957
93. Lombardi R, Yu L, Younes-Ibrahim M, Schor N, Burdmann EA. Epidemiology of acute kidney injury in Latin America. Semin Nephrol. 2008; 28: 320-9 http://dx.doi.org/10.1016/j.semnephrol.2008.04.001 PMid:18620955
94. Jha V, Chungh KS. Community-acquired acute kidney injury in Asia. Semin Nephrol. 2008; 28: 330-47 http://dx.doi.org/10.1016/j.semnephrol.2008.04.002 PMid:18620956
95. Assounga AG, Assambo-Kieku C, Mafoua A, Moyen G, Nzingoula S. Etiology and outcome of acute renal failure in children in Congo-Brazzaville. Saudi J Kidney Dis Transplant. 2000; 11: 40-3 PMid:18209297
96. Mishra SK, Mahanta KC, Mohanty S. Malaria associated acute renal failure - experience from Rourkela, eastern India. J Indian Med Assoc. 2008; 106: 640-2, 654 PMid:19552096
97. Rohani MA, Aliawshaei H, Aduolimi E. Acute renal failure in Yemeni patients. Saudi J Kidney Dis Transpl. 2011; 22: 829-33 PMid:21743244
98. Das BS. Renal failure in malaria. J Vector Borne Dis. 2008; 45: 83-97 PMid:18592837
99. Basu G, Chrispal A, Boorugu H, Gopinath KG, Chandy S, Prakash JAJ, Thomas K, Abraham AM, John GT. Acute kidney injury in tropical acute febrile illness in a tertiary care centre - RIFLE criteria validation. Nephrol Dial Transplant. 2011; 26: 524-31 http://dx.doi.org/10.1093/ndt/gfq477 PMid:20702532
100. Kanodia KV, Shah PR, Vanikar AV, Kasat P, Gumber M, Trivedi HL. Malaria induced acute renal failure: a single center experience. Saudi J Kidney Dis Transplant. 2010; 21: 1088-91 PMid:21060178
101. Ehrich JHH, Eke FU. Malaria-induced renal damage: facts and myths. Pediatr Nephol. 2007; 22: 626-37 http://dx.doi.org/10.1007/s00467-006-0332-y PMid:17205283
102. Kaur D, Wasir V, Gulati S, Bagga A. Unusual presentation of Plasmodium vivax malaria with severe thrombocytopenia and acute renal failure. J Trop Pediatr. 2007; 53: 210-2 http://dx.doi.org/10.1093/tropej/fml092 PMid:17264156
103. Neri S, Pulvirenti D, Patamia I, Zoccolo A, Castellino P. Acute renal failure in Plasmodium malariae infection. Neth J Med. 2008; 66: 166-8 PMid:18424865
104. Barsoun RS. Malaria nephropathies. Nephrol Dial Transplant. 1998; 13: 1588-97 http://dx.doi.org/10.1093/ndt/13.6.1588
105. Elsheikha HM, Sheashaa HA. Epidemiology, pathophysiology, management and outcome of renal dysfunction associated with plasmodia infection. Parasitol Res. 2007; 101: 1183-90 http://dx.doi.org/10.1007/s00436-007-0650-4 PMid:17628830
106. Nguansangiam S, Day NP, Hien TT, Mai NT, Chaisri U, Riganti M, Dondorp AM, Lee SJ, Phu NH, Turner GD, White NJ, Ferguson DJ, Pongponratn E. A quantitative ultrastructural study of renal pathology in fatal Plasmodium falciparum malaria. Trop Med Int Health. 2007; 12: 1037-50 http://dx.doi.org/10.1111/j.1365-3156.2007.01881.x
107. Sinniah R, Rui-Mei L, Kara AU. Up-regulation of cytokine in glomerulonephritis associated with murine malaria. Int. J. Path. 1999; 80: 87-95 http://dx.doi.org/10.1046/j.1365-2613.1999.00101.x PMCid:2517762
108. Mishra SK, Pati SS, Mahanta KC, Mohanty S. Rhabdomyolysis in falciparum malaria -a series of twelve cases (five children and seven adults). Trop Doct. 2010; 40: 87-8 http://dx.doi.org/10.1258/td.2009.090387 PMid:20305101
109. Siqueira AM, Alexandre MA, Mourao MP, Santos VS, Nagahashi-Marie SK, Alecrim MG, Lacerda MV. Case report: severe rhabdomyolysis caused by Plasmodium vivax malaria in the Brazilian Amazon. Am J Trop Med Hyg. 2010; 83: 271-3 http://dx.doi.org/10.4269/ajtmh.2010.10-0027 PMid:20682866 PMCid:2911169
110. Reynaud F, Mallet L, Lyon A, Rodolfo JM. Rhabdomyolysis and acute renal failure in Plasmodium falciparum malaria. Nephrol Dial Transplant. 2005; 20: 847-55 http://dx.doi.org/10.1093/ndt/gfh686 PMid:15772274
111. Khan FY. An imported case of P. falciparum malaria presenting as black water fever with acute renal failure. Travel Med Infect Dis. 2009; 7: 378-80 http://dx.doi.org/10.1016/j.tmaid.2009.11.002 PMid:19945017
112. Oumar AA, Poudiougou B, Sylla M, Sall A, Konate S, Togo B, Diakite M, Keita MM. Black water fever in children during cerebral malaria: 3 case-reports in Bamako. Arch Pediatr. 2007; 14: 993-5 http://dx.doi.org/10.1016/j.arcped.2007.04.005 PMid:17524629
113. Rogier C, Imbert P, Tall A, Sokhna C, Spiegel A, Trape JF. Epidemiological and clinic aspects of black water fever among African children suffering frequent malaria attacks. Trans R Soc Trop Med Hyg. 2003; 97: 193-7 http://dx.doi.org/10.1016/S0035-9203(03)90116-7
114. Bardaji A, Sigauque B, Sanz S, Maixenchs M, Ordi J, Aponte JJ, Mabunda S, Alonso PL, Menendez C. Impact of malaria at the end of pregnancy on infant mortality and morbidity. J Infect Dis. 2011; 203: 691-9 http://dx.doi.org/10.1093/infdis/jiq049 PMid:21199881 PMCid:3071276
115. Uneke CJ. Impact of Placental Plasmodium falciparum malaria on pregnancy and perinatal outcome in Sub-Saharan Africa. Part III: placental malaria, maternal health and public health. Yale J Biol Med. 2008; 81: 1-7 PMid:18604306 PMCid:2442721
116. Aribodor DN, Nwaorgu OC, Eneanya CI, Okoli I, Pukkila-Worley R, Etaga HO. Association of low birth weight and placental malarial infection in Nigeria. J Infect Dev Ctries. 2009; 3:620-3 http://dx.doi.org/10.3855/jidc.554
117. Adam I, Elhassan EM, Haggaz AE, Ali AA, Adam GK. A perspective of the epidemiology of malaria and anaemia and their impact on maternal and perinatal outcomes in Sudan. J Infect Dev Ctries. 2011; 5:083-7
118. Biswajit P, Bijeeyani M, Krishna K. Maternal deaths in a tertiary health care centre of Odisha: an in-depth study supplemented by verbal autopsy. Indian J Community Med. 2011; 36: 213-6 http://dx.doi.org/10.4103/0970-0218.86523 PMid:22090676 PMCid:3214447
119. Agan TU, Ekabua JE, Udoh AE, Ekanem EI, Efiok EE, Mgbekem MA. Prevalence of anemia in women with asymptomatic malaria parasitemia at first antenatal care visit at the University of Calabar Teaching Hospital, Calabar, Nigeria. Int J Womens Health. 2010; 2: 229-33 http://dx.doi.org/10.2147/IJWH.S11887 PMid:21072315 PMCid:2971745
120. Falade CO, Tongo OO, Ogunkunle OO, Orimadegun AE. Effects of malaria in pregnancy on newborn anthropometry. J Infect Dev Ctries. 2010; 4: 448-53 PMid:20818093
121. Tobón-Castaño A, Arismendi Solano M, Sánchez LG, Trujillo SB. Intrauterine growth retardation, low birth weight and prematurity in neonates of pregnant women with malaria in Colombia. Rev Soc Bras Med Trop. 2011; 44: 364-70 PMid:21625805
122. Carvalho BO, Matsuda JS, Luz SL, Martinez-Espinosa FE, Leite JA, Franzin F, Orlandi PP, Gregoracci GG, Lacerda MV, Nogueira PA, Costa FT. Gestational malaria associated to Plasmodium vivax and Plasmodium falciparum placental mixed-infection followed by foetal loss: a case report from an unstable transmission area in Brazil. Malar J. 2011; 10: 178 http://dx.doi.org/10.1186/1475-2875-10-178 PMid:21708032 PMCid:3141593
123. Nosten F, McGready R, Simpson JA, Thwai KL, Balkan S, Cho T, Hkirijaroen L, Looareesuwan S, White NJ. Effects of Plasmodium vivax malaria in pregnancy. Lancet. 1999; 354: 546-9 http://dx.doi.org/10.1016/S0140-6736(98)09247-2
124. Costa FT, Lopes SC, Ferrer M, Leite JA, Martin-Jaular L, Barnabeu M, Nogueira PA, Mourão MP, Fernandez-Becerra C, Lacerda MV, del Portillo H. On cytoadhesion of Plasmodium vivax: raison d'être. Mem Inst Oswaldo Cruz. 2011; 106: 79-84 PMid:21881760
125. Adegnika AA, Luty AJ, Grobusch MP, Ramharter M, Yazdanbakhsh M, Kremsner PG, Schwarz NG. AB0 blood group and the risk of placental malaria in sub-Saharan Africa. Malar J. 2011; 10: 101 http://dx.doi.org/10.1186/1475-2875-10-101 PMid:21513504 PMCid:3098819
126. Uneke CJ. Impact of Placental Plasmodium falciparum malaria on pregnancy and perinatal outcome in Sub-Saharan Africa. I: Introduction to placental malaria. Yale J Biol Med. 2007; 80: 39-50 PMid:18160989 PMCid:2140183
127. Sander AF, Salanti A, Lavstses T, Nielsen MA, Theander TG, Lehe RG, Lo YY, Bobbili N, Arnot DE, Taylor DW. Positive selection of Plasmodium falciparum parasites with multiple var2csa-type PfEMP1 genes during the course of infection in pregnant women. J Infect Dis. 2011; 203: 1679-85 http://dx.doi.org/10.1093/infdis/jir168 PMid:21592998 PMCid:3096795
128. Boeuf P, Hasang W, Hanssen E, Glazier JD, Rogerson SJ. Relevant assay to study the adhesion of Plasmodium falciparum-infected erythrocytes to the placental epithelium. PLoS One. 2011; 6: e21126 http://dx.doi.org/10.1371/journal.pone.0021126 PMid:21731654 PMCid:3123321
129. Rovira-Vallbona E, Dobaño C, Bardají A, Cisteró P, Romagosa C, Serra-Casass E, Quintó L, Bassat Q, Sigauque B, Alonso PL, Ordi J, Menéndez C, Mayor A. Transcription of var genes other than var2csa in Plasmodium falciparum parasites infecting Mozambican pregnant women. J Infect Dis. 2011; 204: 27-35 http://dx.doi.org/10.1093/infdis/jir217 PMid:21628655 PMCid:3307158
130. Conroy A, Serghides L, Finney C, Owino SO, Kumar S, Gowda DC, Liles WC, Moore J, Kain KC. C5a enhances dysregulated inflammatory and angiogenic responses to malaria in vitro: potential implications for placental malaria. PLoS One. 2009; 4: e4953 http://dx.doi.org/10.1371/journal.pone.0004953 PMid:19308263 PMCid:2655724
131. Conroy AL, McDonald CR, Silver KL, Liles WC, Kain KC. Complement activation: a critical mediator of adverse fetal outcomes in placental malaria. Trends Parasitol. 2011; 27: 294-9 http://dx.doi.org/10.1016/j.pt.2011.02.005 PMid:21493146
132. Muehlenbachs A, Fried M, Lachowitzer J, Mutabingwa TK, Duffy PE. Natural selection of FLT1 alleles and their association with malaria resistance in utero. PNAS. 2008; 105: 14488-91 http://dx.doi.org/10.1073/pnas.0803657105 PMid:18779584 PMCid:2567167
133. Haldar K, and Mohandas N. Erythrocyte remodeling by malaria parasites. Curr Opin Hematol 2007; 14: 203-209 http://dx.doi.org/10.1097/MOH.0b013e3280f31b2d PMid:17414208
134. Kraemer SM, and Smith JD. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 2006; 9: 374-380 http://dx.doi.org/10.1016/j.mib.2006.06.006 PMid:16814594
135. Kyes SA, Kraemer SM, Smith JD. Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family. Eukaryotic Cell 2007; 6:1511-1520 http://dx.doi.org/10.1128/EC.00173-07 PMid:17644655 PMCid:2043368