Rethinking cerebral malaria pathology

Current Opinion in Infectious Diseases

Volumn 23, Issue 5, 2010, Pages 456-463

  Milner Jr , Danny A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Africa; cerebral malaria; intervention; models; mortality; pathology

Indexed keywords

CYTOKINE;

BRAIN MALARIA; COMATOSE PATIENT; HUMAN; MORTALITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARASITE TRANSMISSION; PATHOGENESIS; RETINITIS; REVIEW;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MALARIA, CEREBRAL; MICE; PLASMODIUM;

EID: 77956231000     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0b013e32833c3dbe     Document Type: Review

References (112)

1. WHO, Severe falciparum malaria. Trans Roy Soc Trop Med Hyg 2000; 94(Suppl 1):S1/1-90.
2. Rowe AK, Rowe SY, Snow RW, et al. The burden of malaria mortality among African children in the year 2000. Int J Epidemiol 2006:dyl027.
3. Van Den Berg H. Global status of DDT and its alternatives for use in vector control to prevent disease. Environ Health Perspect 2009; 117:1656-1663.
4. Sreehari U, Mittal PK, Razdan RK, et al. Impact of etofenprox (Vectron 20 WP) indoor residual spray on malaria transmission. Indian J Med Res 2009; 129:593-598.
5. Prasad H. Evaluation of malaria control programme in three selected districts of Assam, India. J Vector Borne Dis 2009; 46:280-287.
6. John CC, Riedesel MA, Magak NG, et al. Possible interruption of malaria transmission, highland Kenya, 2007-2008. Emerg Infect Dis 2009; 15:1917-1924.
7. Chen HH, Chen AL. Indoor residual spraying of DDT for malaria control. Am J Public Health 2009; 99:1350-1351. [author reply 1351].
8. Chanda P, Hamainza B, Mulenga S, et al. Early results of integrated malaria control and implications for the management of fever in under-five children at a peripheral health facility: a case study of Chongwe rural health centre in Zambia. Malar J 2009; 8:49.
9. Bukirwa H, Yau V, Kigozi R, et al. Assessing the impact of indoor residual spraying on malaria morbidity using a sentinel site surveillance system in Western Uganda. Am J Trop Med Hyg 2009; 81:611-614.
10. Smith DL, Hay SI, Noor AM, Snow RW. Predicting changing malaria risk after expanded insecticide-treated net coverage in Africa. Trends Parasitol 2009; 25:511-516.
11. Noor AM, Mutheu JJ, Tatem AJ, et al. Insecticide-treated net coverage in Africa: mapping progress in 2000-2007. Lancet 2009; 373:58-67.
12. Eisele TP, Keating J, Littrell M, et al. Assessment of insecticide-treated bednet use among children and pregnant women across 15 countries using standardized national surveys. Am J Trop Med Hyg 2009; 80:209-214.
13. Bejon P, Ogada E, Peshu N, Marsh K. Interactions between age and ITN use determine the risk of febrile malaria in children. PLoS One 2009; 4:e8321.
14. Aliyu AA, Alti-Mu'azu M. Insecticide-treated nets usage and malaria episodes among boarding students in Zaria, northern Nigeria. Ann Afr Med 2009; 8:85-89.
15. Zwang J, Olliaro P, Barennes H, et al. Efficacy of artesunate-amodiaquine for treating uncomplicated falciparum malaria in sub-Saharan Africa: a multi-centre analysis. Malar J 2009; 8:203.
16. Warsame M, Atta H, Klena JD, et al. Efficacy of monotherapies and artesu-nate-based combination therapies in children with uncomplicated malaria in Somalia. Acta Trop 2009; 109:146-151.
17. Thanh NX, Trung TN, Phong NC, et al. Open label randomized comparison of dihydroartemisinin-piperaquine and artesunate-amodiaquine for the treatment of uncomplicated Plasmodium falciparum malaria in central Vietnam. Trop Med Int Health 2009; 14:504-511.
18. Sinclair D, Zani B, Donegan S, Olliaro P, et al. Artemisinin-based combination therapy for treating uncomplicated malaria. Cochrane Database Syst Rev 2009:CD007483.
19. Price RN, Douglas NM. Artemisinin combination therapy for malaria: beyond good efficacy. Clin Infect Dis 2009; 49:1638-1640.
20. Ndiaye JL, Randrianarivelojosia M, Sagara I, et al. Randomized, multicentre assessment of the efficacy and safety of ASAQ: a fixed-dose artesunate-amodiaquine combination therapy in the treatment of uncomplicated Plas-modium falciparum malaria. Malar J 2009; 8:125.
21. Muller O, Sie A, Meissner P, et al. Artemisinin resistance on the Thai-Cambodian border. Lancet 2009; 374:1419.
22. Maude RJ, Pontavornpinyo W, Saralamba S, et al. The last man standing is the most resistant: eliminating artemisinin-resistant malaria in Cambodia. Malar J 2009; 8:31.
23. Kefyalew T, Animut A, Tamene T, et al. Efficacy of six-dose regimen of artemether-lumefantrine for the treatment of uncomplicated falciparum malaria, three years after its introduction into Ethiopia. Parasite 2009; 16:129-134.
24. Kayentao K, Maiga H, Newman RD, et al. Artemisinin-based combinations versus amodiaquine plus sulphadoxine-pyrimethamine for the treatment of uncomplicated malaria in Faladje, Mali. Malar J 2009; 8:5.
25. Hombhanje FW, Linge D, Saweri A, et al. Artemisinin-naphthoquine combination (ARCO) therapy for uncomplicated falciparum malaria in adults of Papua New Guinea: a preliminary report on safety and efficacy. Malar J 2009; 8:196.
26. Ehrhardt S, Meyer CG. Artemether-lumefantrine in the treatment of uncomplicated Plasmodium falciparum malaria. Ther Clin Risk Manag 2009; 5:805-815.
27. Dondorp AM, Nosten F, Yi P, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 2009; 361:455-467.
28. Bassat Q, Mulenga M, Tinto H, et al. Dihydroartemisinin-piperaquine and artemether-lumefantrine for treating uncomplicated malaria in African children: a randomised, noninferiority trial. PLoS One 2009; 4:e7871.
29. Asih PB, Dewi RM, Tuti S, et al. Efficacy of artemisinin-based combination therapyfor treatment of persons with uncomplicated Plasmodium falciparum malaria in West Sumba District, East Nusa Tenggara Province, Indonesia, and genotypic profiles of the parasite. Am J Trop Med Hyg 2009; 80:914-918.
30. Sacarlal J, Aide P, Aponte JJ, et al. Long-term safety and efficacy of the RTS,S/AS02A malaria vaccine in Mozambican children. J Infect Dis 2009; 200:329-336.
31. Polhemus ME, Remich SA, Ogutu BR, et al. Evaluation of RTS,S/AS02A and RTS,S/AS01Bin adultsin ahigh malaria transmission area. PLoS One 2009; 4:e6465.
32. Owusu-Agyei S, Ansong D, Asante K, et al. Randomized controlled trial of RTS,S/AS02D and RTS,S/AS01E malaria candidate vaccines given according to different schedules in Ghanaian children. PLoS One 2009; 4:e7302.
33. Lell B, Agnandji S, von Glasenapp I, et al. A randomized trial assessing the safety and immunogenicity of AS01 and AS02 adjuvanted RTS,S malaria vaccine candidates in children in Gabon. PLoS One 2009; 4:e7611.
34. Kester KE, Cummings JF, Ofori-Anyinam O, et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis 2009; 200:337-346.
35. Sacarlal J, Aponte JJ, Aide P, et al. Safety of the RTS,S/AS02A malaria vaccine in Mozambican children during a Phase IIb trial. Vaccine 2008; 26:174-184.
36. Kester KE, Cummings JF, Ockenhouse CF, et al. Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 2008; 26:2191-2202.
37. Bejon P, Lusingu J, Olotu A, et al. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 2008; 359:2521-2532.
38. Macete EV, Sacarlal J, Aponte JJ, et al. Evaluation of two formulations of adjuvanted RTS, S malaria vaccine in children aged 3 to 5 years living in a malaria-endemic region of Mozambique: a Phase I/IIb randomized double-blind bridging trial. Trials 2007; 8:11.
39. Macete E, Aponte JJ, Guinovart C, et al. Safety and immunogenicity of the RTS,S/AS02A candidate malaria vaccine in children aged 1-4 in Mozambique. Trop Med Int Health 2007; 12:37-46.
40. Stoute JA, Heppner DG Jr, Mason CJ, et al. Phase 1 safety and immuno-genicity trial of malaria vaccine RTS,S/AS02A in adults in a hyperendemic region of western Kenya. Am J Trop Med Hyg 2006; 75:166-170.
41. Haldar K, Mohandas N, Malaria, erythrocytic infection, and anemia. Hema-tology Am Soc Hematol Educ Program 2009;87-93.
42. Dondorp AM, Lee SJ, Faiz MA, et al. The relationship between age and the manifestations of and mortality associated with severe malaria. Clin Infect Dis 2008; 47:151-157.
43. White NJ, Turner GD, Medana IM, et al. The murine cerebral malaria phenomenon. Trends Parasitol 2010; 26:11-15.
44. Riley EM, Couper KN, Helmby H, et al. Neuropathogenesis of human and murine malaria. Trends Parasitol 2010. [Epub ahead of print]
45. Taylor T, Fu W, Carr R, et al. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 2004; 10:143-145.
46. Beare NA, Riva CE, Taylor TE, et al. Changes in optic nerve head blood flow in children with cerebral malaria and acute papilloedema. J Neurol Neurosurg Psychiatry 2006; 77:1288-1290.
47. Beare NAV, Southern C, Chalira C, et al. Prognostic significance and course of retinopathy in children with severe malaria. Arch Ophthalmol 2004; 122:1141-1147.
48. Beare NAV, Southern C, Kayira K, et al. Visual outcomes in children in Malawi following retinopathy of severe malaria. Br J Ophthalmol 2004; 88:321-324.
49. Beare NAV, Taylor TE, Harding SP, et al. Malarial retinopathy: a newly established diagnostic sign in severe malaria. Am J Trop Med Hyg 2006; 75:790-797.
50. Lewallen S, Harding SP, Ajewole J, et al. A review of the spectrum of clinical ocular fundus findings in P. falciparum malaria in African children with a proposed classification and grading system. Trans R Soc Trop Med Hyg 1999; 93:619-622.
51. Lewallen S, Taylor TE, Molyneux ME, et al. Ocular fundus findings in Malawian children with cerebral malaria. Ophthalmology 1993; 100:857-861.
52. Lewallen S, White VA, Whitten RO, et al. Clinical-histopathological correlation of the abnormal retinal vessels in cerebral malaria. Arch Ophthalmol 2000; 118:924-928.
53. Lewallen S, White VA, Whitten RO, et al. Clinical-histopathological correlation of the abnormal retinal vessels in cerebral malaria. Arch Ophthalmol 2000; 118:924-928.
54. White VA, Lewallen S, Beare NA, etal. Retinal pathology of pediatric cerebral malaria in Malawi. PLoS One 2009; 4:e4317.
55. Maude RJ, Dondorp AM, Abu Sayeed A, et al. The eye in cerebral malaria: what can it teach us? Trans R Soc Trop Med Hyg 2009; 103:661-664.
56. Maude RJ, Hassan MU, Beare NA. Severe retinal whitening in an adult with cerebral malaria. Am J Trop Med Hyg 2009; 80:881.
57. Mehta SA, Ansari AS, Jiandani P. Ophthalmoscopic findings in adult patients with severe falciparum malaria. Ocul Immunol Inflamm 2008; 16:239-241.
58. Looareesuwan S, Laothamatas J, Brown TR, Brittenham GM. Cerebral malaria: a new way forward with magnetic resonance imaging (MRI). Am J Trop Med Hyg 2009; 81:545-547.
59. Nickerson JP, Tong KA, Raghavan R. Imaging cerebral malaria with a susceptibility-weighted MR sequence. AJNR Am J Neuroradiol 2009; 30:e85-e86.
60. Yadav P, Sharma R, Kumar S, Kumar U. Magnetic resonance features of cerebral malaria. Acta Radiol 2008; 49:566-569.
61. Looareesuwan S, Wilairatana P, Krishna S, et al. Magnetic resonance imaging of the brain in patients with cerebral malaria. Clin Infect Dis 1995; 21:300-309.
62. Faille D, El-Assaad F, Alessi MC, etal. Platelet-endothelial cell interactions in cerebral malaria: the end of a cordial understanding. Thromb Haemost 2009; 102:1093-1102.
63. Faille D, Combes V, Mitchell AJ, etal. Platelet microparticles: a new player in malaria parasite cytoadherence to human brain endothelium. FASEB J 2009; 23:3449-3458.
64. Chakravorty SJ, Hughes KR, Craig AG. Host response to cytoadherence in Plasmodium falciparum. Biochem Soc Trans 2008; 36 (Pt 2):221-228.
65. Toure FS, Ouwe-Missi-Oukem-Boyer O, Bisvigou U, et al. Apoptosis: a potential triggering mechanism of neurological manifestation in Plasmodium falciparum malaria. Parasite Immunol 2008; 30:47-51.
66. Bhattacharjee S, Van Ooij C, Balu B, et al. Maurer's clefts of Plasmodium falciparum are secretory organelles that concentrate virulence protein reporters for delivery to the host erythrocyte. Blood 2008; 111:241 8-2426.
67. Tripathi AK, Sha W, Shulaev V, et al. Plasmodium falciparum-infected erythrocytes induce NF-kappaB regulated inflammatory pathways in human cerebral endothelium. Blood 2009; 114:4243-4252.
68. Clark IA. Along a TNF-paved road from dead parasites in red cells to cerebral malaria, and beyond. Parasitology 2009; 136:1457-1468.
69. Wu X, Gowda NM, Kumar S, Gowda DC. Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol 2010; 184:4338-4348.
70. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 2007; 447:972-978.
71. Foster SL, Medzhitov R. Gene-specific control of the TLR-induced inflammatory response. Clin Immunol 2009; 130:7-15.
72. Francischetti IM, Seydel KB, Monteiro RQ. Blood coagulation, inflammation, and malaria. Microcirculation 2008; 15:81-107.
73. Francischetti IM. Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol 2008; 24:258-263.
74. Moxon CA, Heyderman RS, Wassmer SC. Dysregulation of coagulation in cerebral malaria. Mol Biochem Parasitol 2009; 166:99-108.
75. Finney OC, Riley EM, Walther M. Regulatory T cells in malaria: friend or foe? Trends Immunol 2010; 31:63-70.
76. Marinkovic M, Diez-Silva M, Pantic I, et al. Febrile temperature leads to significant stiffening of Plasmodium falciparum parasitized erythrocytes. Am J Physiol Cell Physiol 2009; 296:C59-C64.
77. Yeo TW, et al. Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proc Natl Acad Sci USA 2008; 105:17097-17102.
78. Kane MO, Etienne-Selloum N, Madeira SV, et al. Endothelium-derived contracting factors mediate the Ang II-induced endothelial dysfunction in the rat aorta: preventive effect of red wine polyphenols. Pflugers Arch 2010; 459:671-679.
79. Pamplona A, Hanscheid T, Epiphanio S, et al. Cerebral malaria and the hemolysis/methemoglobin/heme hypothesis: shedding new light on an old disease. Int J Biochem Cell Biol 2009; 41:711-716.
80. Epiphanio S, Mikolajczak SA, Goncalves LA, et al. Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection. Cell Host Microbe 2008; 3:331-338.
81. Pamplona A, Ferreira A, Balla J, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13:703-710.
82. Medana IM, Day NP, Hien TT, et al. Erythropoietin and its receptors in the brainstem of adults with fatal falciparum malaria. Malar J 2009; 8:261.
83. Phillips A, Bassett P, Zeki S, et al. Risk factors for severe disease in adults with falciparum malaria. Clin Infect Dis 2009; 48:871-878.
84. White VA, Lewallen S, Beare N, et al. Correlation of retinal haemorrhages with brain haemorrhages in children dying of cerebral malaria in Malawi. Trans R Soc Trop Med Hyg 2001; 95:618-621.
85. Weinberg JB, Lopansri BK, Mwaikambo E, Granger DL Arginine, nitric oxide, carbon monoxide, and endothelial function in severe malaria. Curr Opin Infect Dis 2008; 21:468-475.
86. Yeo TW, Lampah DA, Gitawati R, et al. Recovery of endothelial function in severe falciparum malaria: relationship with improvement in plasma L-arginine and blood lactate concentrations. J Infect Dis 2008; 198:602-608.
87. Yeo TW, Rooslamiati I, Gitawati R, et al. Pharmacokinetics of L-arginine in adults with moderately severe malaria. Antimicrob Agents Chemother 2008; 52:4381-4387.
88. Yeo TW, Lampah DA, Gitawati R, et al. Safety profile of L-arginine infusion in moderately severe falciparum malaria. PLoS One 2008; 3:e2347.
89. Dondorp AM. Clinical significance of sequestration in adults with severe malaria. Transfus Clin Biol 2008; 15 (1-2):56-57.
90. Dondorp AM, Ince C, Charunwatthana P, et al. Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria. J Infect Dis 2008; 197:79-84.
91. Dondorp A, Nosten F, Stepniewska K, et al. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet 2005; 366:717-725.
92. Dondorp AM, Silamut K, Charunwatthana P, et al. Levamisole inhibits sequestration of infected red blood cells in patients with falciparum malaria. J Infect Dis 2007; 196:460-466.
93. Staedke SG, Mwebaza N, Kamya MR, et al. Home management of malaria with artemether-lumefantrine compared with standard care in urban Ugandan children: a randomised controlled trial. Lancet 2009; 373:1623-1631.
94. Jensen TP, Bukirwa H, Njama-Meya D, et al. Use of the slide positivity rate to estimate changes in malaria incidence in a cohort of Ugandan children. Malar J 2009; 8:213.
95. Ssekabira U, Bukirwa H, Hopkins H, et al. Improved malaria case management after integrated team-based training of healthcare workers in Uganda. Am J Trop Med Hyg 2008; 79:826-833.
96. Njama-Meya D, Clark TD, Nzarubara B, et al. Treatment of malaria restricted to laboratory-confirmed cases: a prospective cohort study in Ugandan children. Malar J 2007; 6:7.
97. Kemble SK, Davis JC, Nalugwa T, et al. Prevention and treatment strategies used for the community management of childhood fever in Kampala, Uganda. Am J Trop Med Hyg 2006; 74:999-1007.
98. Nsobya SL, Parikh S, Kironde F, et al. Molecular evaluation of the natural history of asymptomatic parasitemia in Ugandan children. J Infect Dis 2004; 189:2220-2226.
99. Njama-Meya D, Kamya MR, Dorsey G. Asymptomatic parasitaemia as a risk factor for symptomatic malaria in a cohort of Ugandan children. Trop Med Int Health 2004; 9:862-868.
100. Friedman JF, Kurtis JD, Kabyemela ER, et al. The iron trap: iron, malaria and anemia at the mother-child interface. Microbes Infect 2009; 11:460-466.
101. Muehlenbachs A, Fried M, Lachowitzer J, et al. Natural selection of FLT1 alleles and their association with malaria resistance in utero. Proc Natl Acad Sci USA 2008; 105:14488-14491.
102. Kabyemela ER, Fried M, Kurtis JD, et al. Fetal responses during placental malaria modify the risk of low birth weight. Infect Immun 2008; 76:1527-1534.
103. Bansal D, Herbert F, Lim P, et al. IgG autoantibody to brain beta tubulin III associated with cytokine cluster-II discriminate cerebral malaria in central India. PLoS One 2009; 4:e8245.
104. Conroy AL, Lafferty EI, Lovegrove FE, et al. Whole blood angiopoietin-1 and-2 levels discriminate cerebral and severe (noncerebral) malaria from uncomplicated malaria. Malar J 2009; 8:295.
105. Dietmann A, Helbok R, Lackner P, et al. Endoglin in African children with Plasmodium falciparum malaria: a novel player in severe malaria pathogenesis? J Infect Dis 2009; 200:1842-1848.
106. Gyan B, Goka BQ, Adjei GO, et al. Cerebral malaria is associated with low levels of circulating endothelial progenitor cells in African children. Am J Trop Med Hyg 2009; 80:541-546.
107. HesselinkDA, Burgerhart JS, Bosmans-Timmerarends H, et al. Procalcitonin as a biomarker for severe Plasmodium falciparum disease: a critical appraisal of a semi-quantitative point-of-care test in a cohort of travellers with imported malaria. Malar J 2009; 8:206.
108. Kremsner PG, Valim C, Missinou MA, et al. Prognostic value of circulating pigmented cells in African children with malaria. J Infect Dis 2009; 199:142-150.
109. Lovegrove FE, Tangpukdee N, Opoka RO, et al. Serum angiopoietin-1 and-2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS One 2009; 4: e4912.
110. Matondo Maya DW, Mewono L, Nkoma AM, et al. Markers of vascular endothelial cell damage and P. falciparum malaria: association between levels of both sE-selectin and thrombomodulin, and cytokines, hemoglobin and clinical presentation. Eur Cytokine Netw 2008; 19:123-130.
111. Dietmann A, Helbok R, Lackner P, et al. Matrix metalloproteinases and their tissue inhibitors (TIMPs) in Plasmodium falciparum malaria: serum levels of TIMP-1 are associated with disease severity. J Infect Dis 2008; 197:161 4-1620.
112. Kusi KA, Gyan BA, Goka BQ, et al. Levels of soluble CD163 and severity of malaria in children in Ghana. Clin Vaccine Immunol 2008; 15:1456-1460.