Cerebral malaria in children: Using the retina to study the brain

Brain

Volumn 137, Issue 8, 2014, Pages 2119-2142

  Maccormick, Ian J C ^a,b   Beare, Nicholas A V ^b,c   Taylor, Terrie E ^d,e,f   Barrera, Valentina ^b   White, Valerie A ^f   Hiscott, Paul ^b   Molyneux, Malcolm E ^a,g   Dhillon, Baljean ^h,i   Harding, Simon P ^b,c  

^a UNIVERSITY OF MALAWI   (Malawi)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

^d Blantyre Malaria Project   (Malawi)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f VANCOUVER GENERAL HOSPITAL   (Canada)

^g LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^h UNIVERSITY OF EDINBURGH   (United Kingdom)

ⁱ Edinburgh Eye Pavilion   (United Kingdom)

Author keywords

cerebral malaria; cerebral microvasculature; haemorheology; retinal microvasculature; surrogate marker

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1;

ARTERIOLE; BACTERIAL ENDOCARDITIS; BLEEDING; BLOOD RETINA BARRIER; BLOOD RHEOLOGY; BLOOD VESSEL OCCLUSION; BLOOD VISCOSITY; BRAIN; BRAIN BLOOD FLOW; BRAIN CIRCULUS ARTERIOSUS; BRAIN HERNIA; BRAIN MALARIA; BRAIN REGION; CAPILLARY DENSITY; CELL SWELLING; CEREBROVASCULAR DISEASE; CHILDHOOD DISEASE; COLOR VISION; COMPARATIVE STUDY; DIFFUSE AXONAL INJURY; DISEASE COURSE; DISEASE DURATION; ENDOTHELIAL DYSFUNCTION; ERYTHROCYTE DEFORMABILITY; GLASGOW COMA SCALE; HUMAN; LEUKEMIA; MALARIA FALCIPARUM; NEUROIMAGING; PRIORITY JOURNAL; RESPIRATORY ARREST; RETINA; RETINA BLOOD FLOW; RETINA BLOOD VESSEL; RETINA HEMORRHAGE; RETINA MACULA LUTEA; RETINOPATHY; REVIEW; SHEAR STRESS; TISSUE INJURY; VENOUS PRESSURE; WHITE MATTER;

CEREBRAL MALARIA; CEREBRAL MICROVASCULATURE; HAEMORHEOLOGY; RETINAL MICROVASCULATURE; SURROGATE MARKER;

BIOLOGICAL MARKERS; CHILD; HUMANS; MALARIA, CEREBRAL; PLASMODIUM FALCIPARUM; RETINAL VESSELS;

EID: 84905039792     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu001     Document Type: Review

References (194)

1. Abu Sayeed A, Maude RJ, Hasan MU, Mohammed N, Hoque MG, Dondorp AM, et al. Malarial retinopathy in Bangladeshi adults. Am J Trop Med Hyg 2011; 84: 141-7.
2. Agrawal A, McKibbin MA. Purtscher's and Purtscher-like retinopathies: A review [Review]. Surv Ophthalmol 2006; 51: 129-36.
3. Akima M. A morphological study on the microcirculation of the central nervous system. Selective vulnerability to hypoxia. Neuropathology 1993; 13: 99-112.
4. Alm A, Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): A study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res 1973; 15: 15-29.
5. An H, Lin W. Cerebral venous and arterial blood volumes can be estimated separately in humans using magnetic resonance imaging. Magn Reson Med 2002 48 583-8.
6. Anand-Apte B, Hollyfield JG. Developmental Anatomy of the Retinal and Choroidal Vasculature. In: Dartt DA, editor. Encyclopedia of the eye. Oxford: Academic Press 2010.
7. Anderson B, Saltzman HA. Retinal oxygen utilization measured by hyperbaric blackout. Arch Ophthalmol 1964; 72: 792-5.
8. Andeweg J. The anatomy of collateral venous flow from the brain and its value in aetiological interpretation of intracranial pathology [Review]. Neuroradiology 1996; 38: 621-628.
9. Andeweg J. Consequences of the anatomy of deep venous outflow from the brain [Review]. Neuroradiology 1999; 41: 233-41.
10. Armah H, Dodoo AK, Wiredu EK, Stiles JK, Adjei AA, Gyasi RK, et al. High-level cerebellar expression of cytokines and adhesion molecules in fatal, paediatric, cerebral malaria. Ann Trop Med Parasitol 2005; 99: 629-47.
11. Baskurt OK, Meiselman HJ. Blood rheology and hemodynamics [Review]. Semin thromb hemost 2003; 29: 435-50.
12. Beare NA, Southern C, Chalira C, Taylor TE, Molyneux ME, Harding SP. Prognostic significance and course of retinopathy in children with severe malaria. Arch Ophthalmol 2004; 122: 1141-7.
13. Beare NA, Glover SJ, Lewallen S, Taylor TE, Harding SP, Molyneux ME. Prevalence of raised intracranial pressure in cerebral malaria detected by optic nerve sheath ultrasound. Am J Trop Med Hyg 2012; 87: 985-8.
14. Beare NA, Harding SP, Taylor TE, Lewallen S, Molyneux ME. Perfusion abnormalities in children with cerebral malaria and malarial retinopathy. J Infect Dis 2009; 199: 263-271.
15. Beare NA, Lewallen S, Taylor TE, Molyneux ME. Redefining cerebral malaria by including malaria retinopathy. Future Microbiol 2011; 6: 349-55.
16. Bek T, Jensen PK. Three-dimensional structure of human retinal vessels studied by vascular casting. Acta Ophthalmol (Copenh) 1993; 71: 506-13.
17. Bell MA, Ball MJ. Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 1985; 335: 139-43.
18. Van Den Bergh R, Van Der Eecken H. Anatomy and embryology of cerebral circulation. Prog Brain Res 1968; 30: 1-25.
19. Berntson GM. The characterization of topology: A comparison of four topological indices for rooted binary trees. J Theor Biol 1995; 177: 271-81.
20. Billig EMW, O'Meara WP, Riley EM, McKenzie FE. Developmental allometry and paediatric malaria. Malar J 2012; 11: 64.
21. Birbeck GL, Molyneux ME, Kaplan PW, Seydel KB, Chimalizeni YF, Kawaza K, et al. Blantyre Malaria Project Epilepsy Study (BMPES) of neurological outcomes in retinopathy-positive paediatric cerebral malaria survivors: A prospective cohort study. Lancet 2010; 9: 1173-81.
22. Birol G, Wang S, Budzynski E, Wangsa-Wirawan ND, Linsenmeier RA. Oxygen distribution and consumption in the macaque retina. Am J Physiol Heart Circ Physiol 2007; 293: H1696-704.
23. Bronzan RN, Taylor TE, Mwenechanya J, Tembo M, Kayira K, Bwanaisa L, et al. Bacteremia in Malawian children with severe malaria: Prevalence, etiology, HIV coinfection, and outcome. J Infect Dis 2007; 195: 895-904.
24. Brown H, Rogerson S, Taylor T, Tembo M, Mwenechanya J, Molyneux M, et al. Blood-brain barrier function in cerebral malaria in Malawian children. Am J Trop Med Hyg 2001; 64: 207-13.
25. Browning DJ. Patchy ischemic retinal whitening. Ophthalmology 2004; 111: 606-7.
26. Burton K, Nyong O, John W, Inkoom E, Pinder M, Bailey R. Retinopathy in Gambian children admitted to hospital with malaria. Trop Doct 2004; 34: 1-4.
27. Cassot F, Lauwers F, Fouard C, Prohaska S, Lauwers-Cances V. A novel three-dimensional computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex. Microcirculation 2006; 13: 1-18.
28. Cassot F, Lauwers F, Lorthois S, Puwanarajah P, Cances-Lauwers V, Duvernoy H. Branching patterns for arterioles and venules of the human cerebral cortex. Brain Res 2010; 1313: 62-78.
29. Cheung N, Islam FMA, Saw Seang M, Shankar A, De Haseth K, Mitchell P, et al. Distribution and associations of retinal vascular caliber with ethnicity, gender, and birth parameters in young children. Invest Ophthalmol Vis Sci 2007; 48: 1018-24.
30. Cho YI, Cho DJ. Hemorheology and microvascular disorders [Review]. Korean Circ J 2011; 41: 287-95.
31. Chotivanich K, Sritabal J, Udomsangpetch R, Newton P, Stepniewska KA, Ruangveerayuth R, et al. Platelet-induced autoagglutination of Plasmodium falciparum-infected red blood cells and disease severity in Thailand. J Infect Dis 2004; 189: 1052-5.
32. Chugani HT. A critical period of brain development: Studies of cerebral glucose utilization with PET. Prev Med 1998; 27: 184-8.
33. Chugani HT, Phelps ME, Mazziotta JC. Positron emission tomography study of human brain functional development. Ann Neurol 1987; 22: 487-97.
34. Cogan DG, Kuwabara T. Comparison of retinal and cerebral vasculature in trypsin digest preparations. Br J Ophthalmol 1984; 68: 10-12.
35. Craig A, Scherf A. Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion [Review]. Mol Biochem Parasitol 2001; 115: 129-43.
36. Crane IJ, Liversidge J. Mechanisms of leukocyte migration across the blood-retina barrier [Review]. Semin Immunopathol 2008; 30: 165-77.
37. Dondorp AM, Angus BJ, Hardeman MR, Chotivanich KT, Silamut K, Ruangveerayuth R, et al. Prognostic significance of reduced red blood cell deformability in severe falciparum malaria. Am J Trop Med Hyg 1997; 57: 507-11.
38. Dondorp AM, Omodeo-Salè F, Chotivanich K, Taramelli D, White NJ. Oxidative stress and rheology in severe malaria [Review]. Redox Rep 2003; 8: 292-4.
39. Dondorp AM, Lee SJ, Faiz MA, Mishra S, Price R, Tjitra E, et al. The relationship between age and the manifestations of and mortality associated with severe malaria. Clin Infect Dis 2008; 47: 151-7.
40. Dorner GT, Polska E, Garhöfer G, Zawinka C, Frank B, Schmetterer L. Calculation of the diameter of the central retinal artery from noninvasive measurements in humans. Curr Eye Res 2002; 25: 341-5.
41. Dorovini-Zis K, Schmidt K, Huynh H, Fu W, Whitten Richard O, Milner D, et al. The neuropathology of fatal cerebral malaria in malawian children. Am J Pathol 2011; 178: 2146-58.
42. Doubal FN, Hokke PE, Wardlaw JM. Retinal microvascular abnormalities and stroke: A systematic review [Review]. J Neurol Neurosurg Psychiatry 2009; 80: 158-65.
43. Doubal FN, MacGillivray TJ, Patton N, Dhillon B, Dennis MS, Wardlaw JM. Fractal analysis of retinal vessels suggests that a distinct vasculopathy causes lacunar stroke. Neurology 2010; 74: 1102-7.
44. Duane TD, Osher RH, Green WR. White centered hemorrhages: Their significance. Ophthalmology 1980; 87: 66-9.
45. Duguid IG, Boyd AW, Mandel TE. Adhesion molecules are expressed in the human retina and choroid. Curr Eye Res 1992; 11 (Suppl): 153-9.
46. Duvernoy HM, Delon S, Vannson JL. Cortical blood vessels of the human brain. Brain Res Bull 1981; 7: 519-79.
47. Faraci FM. Protecting against vascular disease in brain [Review]. Am J Physiol Heart Circ Physiol 2011; 300: H1566-82.
48. Fedosov DA, Caswell B, Karniadakis GE. Wall shear stress-based model for adhesive dynamics of red blood cells in malaria. Biophys J 2011a; 100: 2084-93.
49. Fedosov DA, Caswell B, Suresh S, Karniadakis GE. Quantifying the biophysical characteristics of Plasmodium-falciparum-Parasitized red blood cells in microcirculation. Proc Natl Acad Sci USA 2011b; 108: 35-9.
50. Feke GT, Tagawa H, Deupree DM, Goger DG, Sebag J, Weiter JJ. Blood flow in the normal human retina. Invest Ophthalmol Vis Sci 1989; 30: 58-65.
51. Funatsu H, Yamashita H, Sakata K, Noma H, Mimura T, Suzuki M, et al. Vitreous levels of vascular endothelial growth factor and intercellular adhesion molecule 1 are related to diabetic macular edema. Ophthalmology 2005; 112: 806-16.
52. Ganesan P, He S, Xu H. Analysis of retinal circulation using an imagebased network model of retinal vasculature. Microvasc Res 2010; 80: 99-109.
53. Geeraerts T, Devys J-M, Berges O, Dureau P, Plaud B. Sevoflurane effects on retrobulbar arteries blood flow in children. Br J Anaesth 2005; 94: 636-41.
54. Griffiths MJ, Ndungu F, Baird KL, Muller DP, Marsh K, Newton CR. Oxidative stress and erythrocyte damage in Kenyan children with severe Plasmodium falciparum malaria. Br J Haematol 2001; 113: 486-91.
55. Guibert R, Fonta C, PlourabouéF. Cerebral blood flow modeling in primate cortex. J Cereb Blood Flow Metab 2010; 30: 1860-73.
56. Harding SP, Lewallen S, Beare NA, Smith A, Taylor TE, Molyneux ME. Classifying and grading retinal signs in severe malaria [Review]. Trop Doct 2006; 36 (Suppl 1): 1-13.
57. Hassler O. Deep cerebral venous system in man. A microangiographic study on its areas of drainage and its anastomoses with the superficial cerebral veins. Neurology 1966; 16: 505-11.
58. Hayreh SS. In vivo choroidal circulation and its watershed zones [Review]. Eye (Lond) 1990; 4: 273-89.
59. Hayreh SS. Physiological anatomy of the retinal vasculature. In: Dartt DA, editor. Encyclopedia of the eye. Elsevier; 2010a. p. 431-8.
60. Hayreh SS. Physiological anatomy of the choroidal vasculature. In: Dartt DA, editor. Encyclopedia of the Eye. Elsevier; 2010b. p. 418-430.
61. Hero M, Harding SP, Riva CE, Winstanley PA, Peshu N, Marsh K. Photographic and angiographic characterization of the retina of Kenyan children with severe malaria. Arch Ophthalmol 1997; 115: 997-1003.
62. Van Der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE. A unified hypothesis for the genesis of cerebral malaria: Sequestration, inflammation and hemostasis leading to microcirculatory dysfunction [Review]. Trends Parasitol 2006; 22: 503-8.
63. Hirsch S, Reichold J, Schneider M, Székely G, Weber B. Topology and hemodynamics of the cortical cerebrovascular system [Review]. J Cereb Blood Flow Metab 2012; 32: 952-67.
64. Hochman S, Kim K. The impact of HIV coinfection on cerebral malaria pathogenesis [Review]. J Neuroparasitology 2012; 3: 1-29.
65. Hooshmand I, Rosenbaum AE, Stein RL. Radiographic anatomy of normal cerebral deep medullary veins: Criteria for distinguishing them from their abnormal counterparts. Neuroradiology 1974; 7: 75-84.
66. Huang YP, Wolf BS. Veins of the white matter of the cerebral hemispheres (the medullary veins). Am J Roentgenol Radium Ther Nucl Med 1964; 92: 739-55.
67. Hudetz AG, Fehér G, Kampine JP. Heterogeneous autoregulation of cerebrocortical capillary flow: Evidence for functional thoroughfare channels?. Microvasc Res 1996; 51: 131-6.
68. Hughes AD, Wong Tien Y, Witt N, Evans R, Thom SA, Klein BE, et al. Determinants of retinal microvascular architecture in normal subjects. Microcirculation 2009; 16: 159-66.
69. Ide K, Secher NH. Cerebral blood flow and metabolism during exercise [Review]. Prog Neurobiol 2000; 61: 397-414.
70. Idro R, Jenkins NE, Newton CRJ. Pathogenesis, clinical features, and neurological outcome of cerebral malaria [Review]. Lancet Neurol 2005; 4: 827-40.
71. International Conference on Harmonisation. ICH Topic E9 Statistical Principles for Clinical Trials 1998. URL http://www.ich.org/prod ucts/guidelines/efficacy/efficacy-single/article/statistical-principles- forclinical- Trials.html [29 May 2013 date last accessed]
72. Jespersen SN, Ostergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J Cereb Blood Flow Metab 2011; 32: 264-77.
73. Jonas JB, Schneider U, Naumann GO. Count and density of human retinal photoreceptors. Graefes Arch Clin Exp Ophthalmol 1992; 230: 505-10.
74. Kaul D. K, Roth EF, Nagel RL, Howard RJ, Handunnetti SM. Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 1991; 78: 812-9.
75. Kennedy C, Sokoloff L. An adaptation of the nitrous oxide method to the study of the cerebral circulation in children;normal values for cerebral blood flow and cerebral metabolic rate in childhood. J Clin Invest 1957; 36: 1130-7.
76. Kety SS. Blood flow and metabolism of the human brain in health and disease. Trans Stud Coll Physicians Phila 1950; 18: 103-8.
77. Kety SS. Human cerebral blood flow and oxygen consumption as related to aging. J Chronic Dis 1956; 3: 478-86.
78. Kety SS, Schmidt CF. The nitrous oxide method for the quantitative determination of cerebral blood flow in man: Theory, procedure and normal values. J Clin Invest 1948; 27: 476-83.
79. Kinnala A, Suhonen-Polvi H, Aärimaa T, Kero P, Korvenranta H, Ruotsalainen U, et al. Cerebral metabolic rate for glucose during the first six months of life: An FDG positron emission tomography study. Arch Dis Child Fetal Neonatal Ed 1996; 74: F153-7.
80. Kuppusamy K, Lin W, Cizek GR, Haacke EM. In vivo regional cerebral blood volume: Quantitative assessment with 3D T1-weighted pre- and postcontrast MR imaging. Radiology 1996; 201: 106-12.
81. Kur J, Newman E a, Chan-Ling T. Cellular and physiological mechanisms underlying blood Flow regulation in the Retina and Choroid in health and disease [Review]. Prog Retin Eye Res 2012; 31: 377-406.
82. Kuwabara T, Cogan DG. Studies of retinal vascular patterns. I. Normal architecture. Arch Ophthalmol 1960; 64: 904-11.
83. Lauwers F, Cassot F, Lauwers-Cances V, Puwanarajah P, Duvernoy H. Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles. Neuroimage 2008; 39: 936-48.
84. Lee KE, Klein BEK, Klein R, Knudtson MD. Familial aggregation of retinal vessel caliber in the beaver dam eye study. Invest Ophthalmol Vis Sci 2004; 45: 3929-33.
85. Lewallen S, Harding SP, Ajewole J, Schulenburg WE, Molyneux ME, Marsh K, 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: 619-22.
86. Lewallen SA, White VA, Whitten RO, Gardiner J, Hoar B, Lindley J, et al. Clinical-histopathological correlation of the abnormal retinal vessels in cerebral malaria. Arch Ophthalmol 2000; 118: 924-8.
87. Lewallen Susan, Bronzan RN, Beare NA, Harding SP, Molyneux ME, Taylor TE. Using malarial retinopathy to improve the classification of children with cerebral malaria. Trans R Soc Trop Med Hyg 2008; 102: 1089-94.
88. Li LJ, Cheung CY-L, Liu Y, Chia A, Selvaraj P, Lin X-Y, et al. Influence of blood pressure on retinal vascular caliber in young children. Ophthalmology 2011; 118: 1459-65.
89. Ling R, James B. White-centred retinal haemorrhages (Roth spots). Postgrad Med J 1998; 74: 581-2.
90. Lipowsky HH. Microvascular rheology and hemodynamics [Review]. Microcirculation 2005; 12: 5-15.
91. Lochhead J, Movaffaghy A, Falsini B, Harding S, Riva C, Molyneux M. The effects of hypoxia on the ERG in paediatric cerebral malaria. Eye 2010; 24: 259-64.
92. Lorthois S, Cassot F. Fractal analysis of vascular networks: Insights from morphogenesis. J Theor Biol 2010; 262: 614-33.
93. Lu M, Perez VL, Ma N, Miyamoto K, Peng HB, Liao JK, et al. VEGF increases retinal vascular ICAM-1 expression in vivo. Invest Ophthalmol Vis Sci 1999; 40: 1808-12.
94. Mackenzie S. Retinal haemorrhages and melanaemia as symptoms of ague. Medical Times and Gazette. London, 1877; 23 June: 663-5.
95. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 1985; 119: 385-401.
96. Madsen PL, Holm S, Herning M, Lassen NA. Average blood flow and oxygen uptake in the human brain during resting wakefulness: A critical appraisal of the Kety-Schmidt technique. J Cereb Blood Flow Metab 1993; 13: 646-55.
97. Maude RJ, Beare NAV, Abu Sayeed A, Chang CC, Charunwatthana P, Faiz MA, et al. The spectrum of retinopathy in adults with Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 2009; 103: 665-71.
98. Mckenna MC, Gruetter R, Sonnewald U, Waagepetersen HS, Schousboe A. Energy metabolism of the brain. In: Seigel GJ, Albers RW, Brady ST, Price DL, editors. Basic neurochemistry: Molecular, cellular and medical aspects. Amsterdam: Elsevier; 2006. p. 535.
99. McLeod D. Krogh cylinders in retinal development, panretinal hypoperfusion and diabetic retinopathy [Review]. Acta Ophthalmol 2010; 88: 817-35.
100. Medana IM, Day NPJ, Sachanonta N, Mai NT, Dondorp AM, Pongponratn E, et al. Coma in fatal adult human malaria is not caused by cerebral oedema. Malar J 2011; 10: 267.
101. Meder JF, Chiras J, Roland J, Guinet P, Bracard S, Bargy F. Venous territories of the brain [Review]. J Neuroradiol 1994; 21: 118-33.
102. Mendis KR, Balaratnasingam C, Yu P, Barry CJ, McAllister IL, Cringle Stephen J, et al. Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying retinal capillary detail. Invest Ophthalmol Vis Sci 2010; 51: 5864-9.
103. Miller LH, Ackerman HC, Su X-Z, Wellems TE. Malaria biology and disease pathogenesis: Insights for new treatments [Review]. Nat Med 2013; 19: 156-67.
104. Miyawaki E, Statland J. Cerebral blood vessels: Arteries. In: Aminoff MJ, Daroff RB, editors. Encyclopedia of the Neurological Sciences. New York: Academic Press; 2003a. p. 584-591.
105. Miyawaki E, Statland J. Cerebral blood vessels: Veins and venous sinuses. In: Aminoff MJ, Daroff RB, editors. Encyclopedia of the Neurological Sciences. New York: Academic Press; 2003b. p. 591-594.
106. Molyneux ME, Taylor TE, Wirima JJ, Borgstein A. Clinical features and prognostic indicators in paediatric cerebral malaria: A study of 131 comatose Malawian children. Q J Med 1989; 71: 441-59.
107. Montgomery J, Mphande FA, Berriman M, Pain A, Rogerson SJ, Taylor Terrie E, et al. Differential var gene expression in the organs of patients dying of falciparum malaria. Mol Microbiol 2007; 65: 959-67.
108. Moody DM, Bell MA, Challa VR. Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: An anatomic study. AJNR Am J Neuroradiol 1990; 11: 431-9.
109. Moxon CA, Grau GE, Craig AG. Malaria: Modification of the red blood cell and consequences in the human host [Review]. Br J Haematol 2011; 154: 670-9.
110. Moxon CA, Heyderman RS, Wassmer SC. Dysregulation of coagulation in cerebral malaria [Review]. Mol Biochem Parasitol 2009; 166: 99-108.
111. Moxon CA, Wassmer SC, Milner DA, Chisala N V, Taylor TE, Seydel KB, et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood 2013; 22: 842-51.
112. Mullins RF, Skeie JM, Malone EA, Kuehn MH. Macular and peripheral distribution of ICAM-1 in the human choriocapillaris and retina. Mol Vis 2006; 12: 224-35.
113. Nagaoka T, Sato E, Takahashi A, Sogawa K, Yokota H, Yoshida A. Effect of aging on retinal circulation in normotensive healthy subjects. Exp Eye Res 2009; 89: 887-91.
114. Nagaoka T, Yoshida A. Noninvasive evaluation of wall shear stress on retinal microcirculation in humans. Invest Ophthalmol Vis Sci 2006; 47: 1113-9.
115. Nagatake T, Hoang VT, Tegoshi T, Rabbege J, Ann TK, Aikawa M. Pathology of falciparum malaria in Vietnam. Am J Trop Med Hyg 1992; 47: 259-64.
116. Nakamura Y, Okudera T, Hashimoto T. Vascular architecture in white matter of neonates: Its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol 1994; 53: 582-9.
117. Narsaria N, Mohanty C, Das BK, Mishra SP, Prasad R. Oxidative stress in children with severe malaria. J Trop Pediatr 2011; 58: 147-50.
118. Nelson MD, Gonzalez-Gomez I, Gilles FH. Dyke Award. The search for human telencephalic ventriculofugal arteries. AJNR Am J Neuroradiol 1991; 12: 215-22.
119. Newton CR, Kirkham FJ, Winstanley PA, Pasvol G, Peshu N, Warrell DA, et al. Intracranial pressure in African children with cerebral malaria. Lancet 1991; 337: 573-6.
120. Newton CR, Marsh K, Peshu N, Kirkham FJ. Perturbations of cerebral hemodynamics in Kenyans with cerebral malaria. Pediatr Neurol 1996; 15: 41-9.
121. Newton CR, Peshu N, Kendall B, Kirkham FJ, Sowunmi A, Waruiru C, et al. Brain swelling and ischaemia in Kenyans with cerebral malaria. Arch Dis Child 1994; 70: 281-7.
122. Newton CR, Taylor TE, Whitten RO. Pathophysiology of fatal falciparum malaria in African children [Review]. Am J Trop Med Hyg 1998; 58: 673-83.
123. Nguyen J, Nishimura N, Fetcho RN, Iadecola C, Schaffer CB. Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries. J Cereb Blood Flow Metab 2011; 1-12.
124. Nishimura N, Rosidi NL, Iadecola C, Schaffer CB. Limitations of collateral flow after occlusion of a single cortical penetrating arteriole. J Cereb Blood Flow Metab 2010; 30: 1914-27.
125. Nonaka H, Akima M, Hatori T, Nagayama T, Zhang Z, Ihara F. The microvasculature of the cerebral white matter: Arteries of the subcortical white matter. J Neuropathol Exp Neurol 2003a; 62: 154-61.
126. Nonaka H, Akima M, Hatori T, Nagayama T, Zhang Z, Ihara F. Microvasculature of the human cerebral white matter: Arteries of the deep white matter. Neuropathology 2003b; 23: 111-8.
127. Nonaka H, Akima M, Nagayama T, Hatori T. The fundamental architecture of the microvasculature of the basal ganglia and changes in senility. Neuropathology 1998; 18: 47-54.
128. Nowinski WL. Proposition of a new classification of the cerebral veins based on their termination [Review]. Surg Radiol Anat 2012; 34: 107-14.
129. Oka K, Rhoton AL, Barry M, Rodriguez R. Microsurgical anatomy of the superficial veins of the cerebrum. Neurosurgery 1985; 17: 711-48.
130. Ono M, Rhoton AL, Peace D, Rodriguez RJ. Microsurgical anatomy of the deep venous system of the brain. Neurosurgery 1984; 15: 621-57.
131. Oo MM, Aikawa M, Than T, Aye TM, Myint PT, Igarashi I, et al. Human cerebral malaria: A pathological study. J Neuropathol Exp Neurol 1987; 46: 223-31.
132. Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, Marsh K, et al. Plateletmediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci USA 2001; 98: 1805-10.
133. Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B. Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: A rationale based on homology between cerebral and retinal microvasculatures [Review]. J Anat 2005; 206: 319-48.
134. Patton N, Aslam TM, MacGillivray T, Deary IJ, Dhillon B, Eikelboom RH, et al. Retinal image analysis: Concepts, applications and potential [Review]. Prog Ret Eye Res 2006; 25: 99-127.
135. Penman A, Talbot JF, Chuang EL, Bird AC, Serjeant GR. Peripheral retinal vasculature in normal Jamaican children. Br J Ophthalmol 1994; 78: 615-7.
136. Pongponratn E, Riganti M, Punpoowong B, Aikawa M. Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: A pathological study. Am J Trop Med Hyg 1991; 44: 168-75.
137. Pongponratn E, Turner GDH, Day NPJ, Phu NH, Simpson JA, Stepniewska K, et al. An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am J Trop Med Hyg 2003; 69: 345-59.
138. Ponsford MJ, Medana IM, Prapansilp P, Hien TT, Lee SJ, Dondorp AM, et al. Sequestration and microvascular congestion are associated with coma in human cerebral malaria. J Infect Dis 2012; 205: 663-71.
139. Popel AS, Johnson PC. Microcirculation and hemorheology [Review]. Annu Rev Fluid Mech 2005; 37: 43-69.
140. Potchen MJ, Kampondeni SD, Seydel KB, Birbeck GL, Hammond CA, Bradley WG, et al. Acute brain MRI findings in 120 Malawian children with cerebral malaria: New insights into an ancient disease. AJNR Am J Neuroradiol 2012; 33: 1740-6.
141. Pournaras CJ, Rungger-Brändle E, Riva Charles E, Hardarson SH, Stefansson E. Regulation of retinal blood flow in health and disease [Review]. Prog Retin Eye Res 2008; 27: 284-330.
142. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer [Review]. Pflugers Arch 2000; 440: 653-66.
143. Rasalkar DD, Paunipagar BK, Sanghvi D, Sonawane BD, Loniker P. Magnetic resonance imaging in cerebral malaria: A report of four cases. Br J Radiol 2011; 84: 380-5.
144. Reina-de La Torre F, Rodriguez-baeza A, Sahuquillo-Barris J. Morphological characteristics and distribution pattern of the arterial vessels in human cerebral cortex: A scanning electron microscope study. Anat Rec 1998; 251: 87-96.
145. Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA 2005; 293: 1461-70.
146. Roca-Feltrer A, Kwizombe CJ, Sanjoaquin MA, Sesay SS, Faragher B, Harrison J, et al. Lack of decline in childhood malaria, Malawi, 2001-2010. Emerg Infect Dis 2012; 18: 272-8.
147. Rochtchina E, Wang JJ, Taylor B, Wong TY, Mitchell P. Ethnic variability in retinal vessel caliber: A potential source of measurement error from ocular pigmentation?. The Sydney Childhood Eye Study. Invest Ophthalmol Vis Sci 2008; 49: 1362-6.
148. Rowe JA, Claessens A, Corrigan RA, Arman M. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: Molecular mechanisms and therapeutic implications. Expert Rev Mol Med 2009; 11: E16.
149. Sakai F, Nakazawa K, Tazaki Y, Ishii K, Hino H, Igarashi H, et al. Regional cerebral blood volume and hematocrit measured in normal human volunteers by single-photon emission computed tomography. J Cereb Blood Flow Metab 1985; 5: 207-13.
150. Sarda V, Nakashima K, Wolff B, Sahel JA, Paques M. Topography of patchy retinal whitening during acute perfused retinal vein occlusion by optical coherence tomography and adaptive optics fundus imaging. Eur J Ophthalmol 2011; 21: 653-6.
151. Sarpeshkar R. Ultra low power bioelectronics: Fundamentals, biomedical applications, and bio-inspired systems. Cambridge: Cambridge University press; 2010. p. 748.
152. Schaller B. Physiology of cerebral venous blood flow: From experimental data in animals to normal function in humans [Review]. Brain Res Brain Res Rev 2004; 46: 243-60.
153. Schmid-Schönbein GW. Biomechanics of microcirculatory blood perfusion [Review]. Annu Rev Biomed Eng 1999 1 73-102
154. Seifert T, Secher NH. Sympathetic influence on cerebral blood flow and metabolism during exercise in humans [Review]. Prog Neurobiol 2011; 95: 406-26.
155. Sein KK, Maeno Y, Thuc H V, Anh TK, Aikawa M. Differential sequestration of parasitized erythrocytes in the cerebrum and cerebellum in human cerebral malaria. Am J Trop Med Hyg 1993; 48: 504-11.
156. Semmer AE, McLoon LK, Lee MS. Orbital vascular anatomy. In: Dartt DA, editor. Encyclopedia of the Eye. Elsevier; 2010. p. 241-251.
157. Silamut K, Phu NH, Whitty C, Turner GD, Louwrier K, Mai NT, et al. A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am J Pathol 1999; 155: 395-410.
158. Smith JR, Choi D, Chipps TJ, Pan Y, Zamora DO, Davies MH, et al. Unique gene expression profiles of donor-matched human retinal and choroidal vascular endothelial cells. Invest Ophthalmol Vis Sci. 2007; 48: 2676-84.
159. Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 1997; 349: 1650-4.
160. Sokoloff L. Cerebral metabolism and blood flow. In: Aminoff MJ, Daroff RB, editors. Encyclopedia of the Neurological Sciences. New York: Academic Press; 2003. p. 609-617.
161. Sperber GO, Bill A. Blood flow and glucose consumption in the optic nerve, retina and brain: Effects of high intraocular pressure. Exp Eye Res 1985; 41: 639-53.
162. Spitz S. The pathology of acute falciparum malaria. Mil Surg 1946; 99: 555-72.
163. Spitznas M, Bornfeld N. The architecture of the most peripheral retinal vessels. Albrecht Von Graefes Arch Klin Exp Ophthalmol 1977; 203: 217-29.
164. StefÁnsson E, Wilson CA, Lightman SL, Kuwabara T, Palestine AG, Wagner HG. Quantitative measurements of retinal edema by specific gravity determinations. Invest Ophthalmol Vis Sci 1987; 28: 1281-9.
165. Stins MF, Pearce D, Di Cello F, Erdreich-Epstein A, Pardo CA, Sik Kim K. Induction of intercellular adhesion molecule-1 on human brain endothelial cells by HIV-1 gp120: Role of CD4 and chemokine coreceptors. Lab Invest 2003; 83: 1787-98.
166. Sun C, Ponsonby A, Wong Tien Y, Brown SA, Kearns LS, Cochrane J, et al. Effect of birth parameters on retinal vascular caliber: The Twins Eye Study in Tasmania. Hypertension 2009; 53: 487-93.
167. Takahashi T, Shirane R, Sato S, Yoshimoto T. Developmental changes of cerebral blood flow and oxygen metabolism in children. AJNR Am J Neuroradiol 1999; 20: 917-22.
168. Tam J, Martin JA, Roorda A. Noninvasive visualization and analysis of parafoveal capillaries in humans. Invest Ophthalmol Vis Sci 2010; 51: 1691-8.
169. Tam J, Tiruveedhula P, Roorda A. Characterization of single-file flow through human retinal parafoveal capillaries using an adaptive optics scanning laser ophthalmoscope. Biomed Opt Express 2011; 2: 781-93.
170. Tapp RJ, Williams C, Witt N, Chaturvedi N, Evans R, Thom SA, et al. Impact of size at birth on the microvasculature: The Avon longitudinal study of parents and children. Pediatrics 2007; 120: E1225-8.
171. Taylor B, Rochtchina E, Wang JJ, Wong T Y, Heikal S, Saw SM, et al. Body mass index and its effects on retinal vessel diameter in 6-year-old children. Int J Obes (Lond) 2007; 31: 1527-33.
172. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JS, Fosiko NG, et al. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 2004; 10: 143-5.
173. Teksam M, Moharir M, Deveber G, Shroff M. Frequency and topographic distribution of brain lesions in pediatric cerebral venous thrombosis. AJNR Am J Neuroradiol 2008; 29: 1961-5.
174. Thanachartwet V, Desakorn V, Sahassananda D, Kyaw Win KK, Supaporn T. Acute renal failure in patients with severe falciparum malaria: Using the WHO 2006 and RIFLE criteria. Int J Nephrol 2013; 2013: 841518.
175. Turner G. Cerebral malaria [Review]. Brain Pathol 1997; 7: 569-82.
176. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JEV, Avril M, et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 2013; 498: 502-5.
177. Varela M, Groves AM, Arichi T, Hajnal JV. Mean cerebral blood flow measurements using phase contrast MRI in the first year of life. NMR Biomed 2012; 25: 1063-72.
178. Vovenko E. Distribution of oxygen tension on the surface of arterioles, capillaries and venules of brain cortex and in tissue in normoxia: An experimental study on rats. Pflügers Arch 1999; 437: 617-23.
179. Wang Q, Kocaoglu OP, Cense B, Bruestle J, Jonnal RS, Gao W, et al. Imaging retinal capillaries using ultrahigh-resolution optical coherence tomography and adaptive optics. Invest Ophthalmol Vis Sci 2011; 52: 6292-9.
180. White VA, Lewallen S, Beare N, Kayira K, Carr RA, Taylor TE. Correlation of retinal haemorrhages with brain haemorrhages in children dying of cerebral malaria in Malawi. Trans R Soc Trop Med Hyg 2001; 95: 618-21.
181. White VA, Lewallen S, Beare NAV, Molyneux ME, Taylor TE. Retinal pathology of pediatric cerebral malaria in Malawi. PloS One 2009; 4: E4317.
182. WHO. Severe falciparum malaria. Trans R Soc Trop Med Hyg 2000; 94: S1.
183. WHO. Guidelines for the treatment of malaria. 2nd ed. World Health Organization;2010. http://www.who.int/malaria/publications/atoz/ 9789241547925/en/index.html [29 May 2013 date last accessed]
184. WHO. World Malaria Report. 2012, http://www.who.int/malaria/publi cations/world-malaria-report-2012/report/en/ [29 May 2013 date last accessed]
185. Widjaja E, Griffiths PD. Intracranial MR venography in children: Normal anatomy and variations. AJNR Am J Neuroradiol 2004; 25: 1557-62.
186. Williamson TH, Harris A. Ocular blood flow measurement [Review]. Br J Ophthalmol 1994; 78: 939-45.
187. Wintermark M, Lepori D, Cotting J, Roulet E, Van Melle G, Meuli R, et al. Brain perfusion in children: Evolution with age assessed by quantitative perfusion computed tomography. Pediatrics 2004; 113: 1642-52.
188. Wolfram-Gabel R, Maillot C. Vascular networks of the nucleus lentiformis. Surg Radiol Anat 1994; 16: 373-77.
189. Wong-Riley M. Energy metabolism of the visual system. Eye Brain 2010; 2: 99-116.
190. Xu H, Manivannan A, Goatman KA, Jiang HR, Liversidge J, Sharp PF, et al. Reduction in shear stress, activation of the endothelium, and leukocyte priming are all required for leukocyte passage across the blood-retina barrier. J Leukoc Biol 2003; 75: 224-32.
191. Yadav P, Sharma R, Kumar S, Kumar U. Magnetic resonance features of cerebral malaria. Acta Radiol 2008; 49: 566-9.
192. Yu DY, Cringle S J. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease [Review]. Prog Retin Eye Res 2001; 20: 175-208.
193. Yu PK, Balaratnasingam C, Cringle Stephen J, McAllister IL, Provis J, Yu DY. Microstructure and network organization of the microvasculature in the human macula. Invest Ophthalmol Vis Sci 2010; 51: 6735-43.
194. Zehetner C, Bechrakis NE. White centered retinal hemorrhages in vitamin b(12) deficiency anemia. Case Rep Ophthalmol 2011; 2: 140-4.