Fatal cerebral malaria: A venous efflux problem

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue NOV, 2014, Pages

  Frevert, Ute ^a   Nacer, Adéla ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

Brain edema; CD8+ T cell; Cytoadherence; Intracranial hypertension; Macrophage; Plasmodium; Postcapillary venule; Vascular leakage

Indexed keywords

ANIMAL; CAUSE OF DEATH; COMPLICATION; DISEASE MODEL; HUMAN; INTRACRANIAL HYPERTENSION; MALARIA; MORTALITY; MOUSE; PLASMODIUM FALCIPARUM;

ANIMALS; CAUSE OF DEATH; DISEASE MODELS, ANIMAL; HUMANS; INTRACRANIAL HYPERTENSION; MALARIA, CEREBRAL; MICE; PLASMODIUM FALCIPARUM;

EID: 84915811608     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2014.00155     Document Type: Article

References (86)

1. Andrade, B. B., Reis-Filho, A., Souza-Neto, S. M., Clarencio, J., Camargo, L. M., Barral, A., et al. (2010). Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar. J. 9:13. doi: 10.1186/1475-2875-9-13
2. Angulo, I., and Fresno, M. (2002). Cytokines in the pathogenesis of and protection against malaria. Clin. Diagn. Lab. Immunol. 9, 1145-1152. doi: 10.1128/CDLI.9.6.1145-1152.2002
3. Basilico, N., Speciale, L., Parapini, S., Ferrante, P., and Taramelli, D. (2002). Endothelin-1 production by a microvascular endothelial cell line treated with Plasmodium falciparum parasitized red blood cells. Clin. Sci. 103(Suppl. 48), 464S-466S. doi: 10.1042/CS103S464S
4. Beare, N. A., Glover, S. J., Lewallen, S., Taylor, T. E., Harding, S. P., and Molyneux, M. E. (2012). Prevalence of raised intracranial pressure in cerebral malaria detected by optic nerve sheath ultrasound. Am. J. Trop. Med. Hyg. 87, 985-988. doi: 10.4269/ajtmh.2012.11-0459
5. Beg, M. A., Khan, R., Baig, S. M., Gulzar, Z., Hussain, R., and Smego, R. A., et al. (2002). Cerebral involvement in benign tertian malaria. Am. J. Trop. Med. Hyg. 67, 230-232.
6. Brewster, D. R., Kwiatkowski, D., and White, N. J. (1990). Neurological sequelae of cerebral malaria in children. Lancet 336, 1039-1043. doi: 10.1016/0140-6736(90)92498-7
7. Buffet, P. A., Safeukui, I., Milon, G., Mercereau-Puijalon, O., and David, P. H. (2009). Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr. Opin. Hematol. 16, 157-164. doi: 10.1097/MOH.0b013e32832a1d4b
8. Cabrales, P., Zanini, G. M., Meays, D., Frangos, J. A., and Carvalho, L. J. (2011). Nitric oxide protection against murine cerebral malaria is associated with improved cerebral microcirculatory physiology. J. Infect. Dis. 203, 1454-1463. doi: 10.1093/infdis/jir058
9. Cabrales, P., Zanini, G. M., Meays, D., Frangos, J. A., and Carvalho, L. J. M. (2010). Murine cerebral malaria is associated with a vasospasm-like microcirculatory dysfunction, and survival upon rescue treatment is markedly increased by nimodipine. Am. J. Pathol. 176, 1306-1315. doi: 10.2353/ajpath.2010.090691
10. Cacheaux, L. P., Ivens, S., David, Y., Lakhter, A. J., Bar-Klein, G., Shapira, M., et al. (2009). Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J. Neurosci. 29, 8927-8935. doi: 10.1523/JNEUROSCI.0430-09.2009
11. Callera, G. E., Touyz, R. M., Teixeira, S. A., Muscara, M. N., Carvalho, M. H., Fortes, Z. B., et al. (2003). ETA receptor blockade decreases vascular superoxide generation in DOCA-salt hypertension. Hypertension 42, 811-817. doi: 10.1523/JNEUROSCI.0430-09.2009
12. Clark, I. A., and Rockett, K. A. (1994). The cytokine theory of human cerebral malaria. Parasitol. Today 10, 410-412. doi: 10.1016/0169-4758(94)90237-2
13. Cromer, D., Evans, K. J., Schofield, L., and Davenport, M. P. (2006). Preferential invasion of reticulocytes during late-stage Plasmodium berghei infection accounts for reduced circulating reticulocyte levels. Int. J. Parasitol. 36, 1389-1397. doi: 10.1016/j.ijpara.2006.07.009
14. Cui, W., Sun, C. M., and Liu, P. (2013). Alterations of blood-brain barrier and associated factors in acute liver failure. Gastroenterol. Res. Pract. 2013:841707. doi: 10.1155/2013/841707
15. Dai, M., Freeman, B., Bruno, F. P., Shikani, H. J., Tanowitz, H. B., Weiss, L. M., et al. (2012). The novel ETA receptor antagonist HJP-272 prevents cerebral microvascular hemorrhage in cerebral malaria and synergistically improves survival in combination with an artemisinin derivative. Life Sci. 91, 687-692. doi: 10.1016/j.lfs.2012.07.006
16. Day, N. P., Hien, T. T., Schollaardt, T., Loc, P. P., Chuong, L. V., Chau, T. T., et al. (1999). The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J. Infect. Dis. 180, 1288-1297. doi: 10.1086/315016
17. Dorovini-Zis, K., Schmidt, K., Huynh, H., Fu, W., Whitten, R. O., Milner, D., et al. (2011). The neuropathology of fatal cerebral malaria in malawian children. Am. J. Pathol. 178, 2146-2158. doi: 10.1016/j.ajpath.2011.01.016
18. Francischetti, I. M. (2008). Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol. 24, 258-263. doi: 10.1016/j.pt.2008.03.009
19. Freeman, B. D., Machado, F. S., Tanowitz, H. B., and Desruisseaux, M. S. (2014). Endothelin-1 and its role in the pathogenesis of infectious diseases. Life Sci. doi: 10.1016/j.lfs.2014.04.021. [Epub ahead of print].
20. Frerichs, F. T. (1858). Klinik der Leberkrankheiten. Braunschweig: Friedrich Vieweg und Sohn.
21. Goyal, J. P., and Makwana, A. M. (2014). Comparison of clinical profile between P. vivax and P. falciparum malaria in children: a tertiary care centre perspective from India. Malar. Res. Treat. 2014:132672. doi: 10.1155/2014/132672
22. Grau, G. E., and De Kossodo, S. (1994). Cerebral malaria: mediators, mechanical obstruction or more? Parasitol. Today 10, 408-409.
23. Haldar, K., Murphy, S. C., Milner, D. A., and Taylor, T. E. (2007). Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu. Rev. Pathol. 2, 217-249. doi: 10.1146/annurev.pathol.2.010506.091913
24. Harder, B., Hennerici, M. G., and Jonas, J. B. (2007). [Ophthalmodynamometry of central retinal vein collapse pressure in idiopathic intracranial hypertension]. Klin. Monbl. Augenheilkd. 224, 852-855. doi: 10.1055/s-2007-963634
25. Hawkes, M., Elphinstone, R. E., Conroy, A. L., and Kain, K. C. (2013). Contrasting pediatric and adult cerebral malaria: the role of the endothelial barrier. Virulence 4, 543-555. doi: 10.4161/viru.25949
26. Hawkes, M., Opoka, R. O., Namasopo, S., Miller, C., Conroy, A. L., Serghides, L., et al. (2011). Nitric oxide for the adjunctive treatment of severe malaria: hypothesis and rationale. Med. Hypotheses 77, 437-444. doi: 10.1016/j.mehy.2011.06.003
27. Hermsen, C., Van De Wiel, T., Mommers, E., Sauerwein, R., and Eling, W. (1997). Depletion of CD4+ or CD8+ T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology 114(Pt 1), 7-12. doi: 10.1017/S0031182096008293
28. Higgins, S. J., Kain, K. C., and Liles, W. C. (2011). Immunopathogenesis of falciparum malaria: implications for adjunctive therapy in the management of severe and cerebral malaria. Expert Rev. Anti Infect. Ther. 9, 803-819. doi: 10.1586/eri.11.96
29. Hunt, N. H., Golenser, J., Chan-Ling, T., Parekh, S., Rae, C., Potter, S., et al. (2006). Immunopathogenesis of cerebral malaria. Int. J. Parasitol. 36, 569-582. doi: 10.1016/j.ijpara.2006.02.016
30. Idro, R., Carter, J. A., Fegan, G., Neville, B. G., and Newton, C. R. (2006). Risk factors for persisting neurological and cognitive impairments following cerebral malaria. Arch. Dis. Child. 91, 142-148. doi: 10.1136/adc.2005.077784
31. Idro, R., Kakooza-Mwesige, A., Balyejjussa, S., Mirembe, G., Mugasha, C., Tugumisirize, J., et al. (2010a). Severe neurological sequelae and behaviour problems after cerebral malaria in Ugandan children. BMC Res. Notes 3:104. doi: 10.1186/1756-0500-3-104
32. Idro, R., Marsh, K., John, C. C., and Newton, C. R. (2010b). Cerebral malaria: mechanisms of brain injury and strategies for improved neurocognitive outcome. Pediatr. Res. 68, 267-274. doi: 10.1203/PDR.0b013e3181eee738
33. Jonas, J. B., Pfeil, K., Chatzikonstantinou, A., and Rensch, F. (2008). Ophthalmodynamometric measurement of central retinal vein pressure as surrogate of intracranial pressure in idiopathic intracranial hypertension. Graefes Arch. Clin. Exp. Ophthalmol. 246, 1059-1060. doi: 10.1007/s00417-008-0780-0
34. Kampondeni, S. D., Potchen, M. J., Beare, N. A., Seydel, K. B., Glover, S. J., Taylor, T. E., et al. (2013). MRI findings in a cohort of brain injured survivors of pediatric cerebral malaria. Am. J. Trop. Med. Hyg. 88, 542-546. doi: 10.4269/ajtmh.12-0538
35. Kennan, R. P., Machado, F. S., Lee, S. C., Desruisseaux, M. S., Wittner, M., Tsuji, M., et al. (2005). Reduced cerebral blood flow and N-acetyl aspartate in a murine model of cerebral malaria. Parasitol. Res. 96, 302-307. doi: 10.1007/s00436-005-1349-z
36. King-Vanvlack, C. E., Mewburn, J. D., Chapler, C. K., and Macdonald, P. H. (2003). Hemodynamic and proinflammatory actions of endothelin-1 in guinea pig small intestine submucosal microcirculation. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G940-G948. doi: 10.1152/ajpgi.00373.2001
37. Laveran, A. (1884). Traité Des Fièvres Palustres Avec La Description Des Microbes Du Paludisme. Paris: Octave Doin.
38. Le, A., Hoehn, M. E., Smith, M. E., Spentzas, T., Schlappy, D., and Pershad, J. (2009). Bedside sonographic measurement of optic nerve sheath diameter as a predictor of increased intracranial pressure in children. Ann. Emerg. Med. 53, 785-791. doi: 10.1016/j.annemergmed.2008.11.025
39. Liu, M., Amodu, A. S., Pitts, S., Patrickson, J., Hibbert, J. M., Battle, M., et al. (2012). Heme mediated STAT3 activation in severe malaria. PLoS ONE 7:e34280. doi: 10.1371/journal.pone.0034280
40. Macpherson, G. G., Warrell, M. J., White, N. J., Looareesuwan, S., and Warrell, D. A. (1985). Human cerebral malaria a quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am. J. Pathol. 119, 385-401.
41. Maegraith, B. (1974). Other pathological processes in malaria. Bull. Org. Mond. Santé Bull. Wld. Hlth Org 50, 187-193.
42. Marchiafava, E., and Bignami, A. (1894). "On summer-autumn malarial fevers," in Two Monographs on Malaria and the Parasites of Malarial Fevers (translated from the first Italian edition by J. H. Thompson) ed E. Marchiafava (London: The New Sydenham Society), 1-232.
43. Martins, C., Tanowitz, H., Weiss, L., and Desruisseaux, M. S. (2014). "Endothelin-1 treatment induces experimental cerebral malaria in Plasmodium berghei NK65 infected mice," in Malaria 2014: Advances in Pathophysiology, Biology and Drug Development, eds J. P. Daily, D. A. Fidock, and J. S. Henry (New York, NY: New York Academy of Sciences).
44. Martins, Y. C., and Daniel-Ribeiro, C. T. (2013). A new hypothesis on the manifestation of cerebral malaria: the secret is in the liver. Med. Hypotheses. 81, 777-783. doi: 10.1016/j.mehy.2013.08.005
45. McNally, J., O'Donovan, S. M., and Dalton, J. P. (1992). Plasmodium berghei and Plasmodium chabaudi chabaudi: development of simple in vitro erythrocyte invasion assays. Parasitology 105(Pt 3), 355-362.
46. Medana, I. M., and Turner, G. D. (2006). Human cerebral malaria and the blood-brain barrier. Int. J. Parasitol. 36, 555-568. doi: 10.1016/j.ijpara.2006.02.004
47. Milner, D. A. Jr., Valim, C., Carr, R. A., Chandak, P. B., Fosiko, N. G., Whitter, R., et al. (2013). A histological method for quantifying Plasmodium falciparum in the brain in fatal paediatric cerebral malaria. Malar. J. 12:191. doi: 10.1186/1475-2875-12-191
48. Moxon, C. A., Wassmer, S. C., Milner, D. A. Jr., Chisala, N. V., Taylor, T. E., Seydel, K. B., et al. (2013). Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood 122, 842-851. doi: 10.1182/blood-2013-03-490219
49. Murphy, S., Cserti-Gazdewich, C., Dhabangi, A., Musoke, C., Nabukeera-Barungi, N., Price, D., et al. (2011). Ultrasound findings in Plasmodium falciparum malaria: a pilot study. Pediatr. Crit. Care Med. 12, e58-e63. doi: 10.1097/PCC.0b013e3181e89992
50. Nacer, A., Movila, A., Baer, K., Mikolajczak, S. A., Kappe, S. H., and Frevert, U. (2012). Neuroimmunological blood brain barrier opening in experimental cerebral malaria. PLoS Pathog. 8:e1002982. doi: 10.1371/journal.ppat.1002982
51. Nacer, A., Movila, A., Sohet, F., Girgis, N. M., Gundra, U. M., Loke, P., et al. (in press). Experimental cerebral malaria pathogenesis - hemodynamics at the blood brain barrier. PLoS Pathog.
52. Newton, C. R., Crawley, J., Sowumni, A., Waruiru, C., Mwangi, I., English, M., et al. (1997). Intracranial hypertension in Africans with cerebral malaria. Arch. Dis. Child. 76, 219-226. doi: 10.1136/adc.76.3.219
53. Newton, C. R., Kirkham, F. J., Winstanley, P. A., Pasvol, G., Peshu, N., Warrell, D. A., et al. (1991). Intracranial pressure in African children with cerebral malaria. Lancet 337, 573-576. doi: 10.1016/0140-6736(91)91638-B
54. Noone, C., Parkinson, M., Dowling, D. J., Aldridge, A., Kirwan, P., Molloy, S. F., et al. (2013). Plasma cytokines, chemokines and cellular immune responses in pre-school Nigerian children infected with Plasmodium falciparum. Malar. J. 12:5. doi: 10.1186/1475-2875-12-5
55. Panichakul, T., Sattabongkot, J., Chotivanich, K., Sirichaisinthop, J., Cui, L., and Udomsangpetch, R. (2007). Production of erythropoietic cells in vitro for continuous culture of Plasmodium vivax. Int. J. Parasitol. 37, 1551-1557. doi: 10.1016/j.ijpara.2007.05.009
56. Penet, M.-F., Viola, A., Confort-Gouny, S., Le Fur, Y., Duhamel, G., Kober, F., et al. (2005). Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J. Neurosci. 25, 7352-7358. doi: 10.1523/JNEUROSCI.1002-05.2005
57. Postels, D. G., Chimalizeni, Y. F., Mallewa, M., Boivin, M. J., and Seydel, K. B. (2013). Pediatric cerebral malaria: a scourge of Africa. Future Neurol. 8, 67-85. doi: 10.2217/fnl.12.84
58. Randall, L. M., Kenangalem, E., Lampah, D. A., Tjitra, E., Mwaikambo, E. D., Handojo, T., et al. (2010). A study of the TNF/LTA/LTB locus and susceptibility to severe malaria in highland papuan children and adults. Malar. J. 9:302. doi: 10.1186/1475-2875-9-302
59. Russell, B., Suwanarusk, R., Borlon, C., Costa, F. T., Chu, C. S., Rijken, M. J., et al. (2011). A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood 118, e74-e81. doi: 10.1182/blood-2011-04-348748
60. Safeukui, I., Correas, J.-M., Brousse, V., Hirt, D., Deplaine, G., Mule, S., et al. (2008). Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood 112, 2520-2528. doi: 10.1182/blood-2008-03-146779
61. Saggu, R., Faille, D., Grau, G. E., Cozzone, P. J., and Viola, A. (2011). In the eye of experimental cerebral Malaria. Am. J. Pathol. 179, 1104-1109. doi: 10.1016/j.ajpath.2011.05.044
62. Sanni, L. A. (2001). The role of cerebral oedema in the pathogenesis of cerebral malaria. Redox Rep. 6, 137-142. doi: 10.1179/135100001101536238
63. Saqqur, M., Zygun, D., and Demchuk, A. (2007). Role of transcranial Doppler in neurocritical care. Crit. Care Med. 35, S216-S223. doi: 10.1097/01.CCM.0000260633.66384.FB
64. Sarkar, D., Ray, S., Saha, M., Chakraborty, A., and Talukdar, A. (2013). Clinico-laboratory profile of severe Plasmodium vivax malaria in a tertiary care centre in Kolkata. Trop. Parasitol. 3, 53-57. doi: 10.4103/2229-5070.113912
65. Schmutzhard, J., Kositz, C. H., Lackner, P., Dietmann, A., Fischer, M., Glueckert, R., et al. (2010). Murine malaria is associated with significant hearing impairment. Malar. J. 9:159. doi: 10.1186/1475-2875-9-159
66. Schmutzhard, J., Kositz, C. H., Lackner, P., Pritz, C., Glueckert, R., Fischer, M., et al. (2011). Murine cerebral malaria: histopathology and ICAM 1 immunohistochemistry of the inner ear. Trop. Med. Int. Health 16, 914-922. doi: 10.1111/j.1365-3156.2011.02801.x
67. Seydel, K., Kampondeni, S., Potchen, M., Birbeck, G., Molyneux, M., and Taylor, T. (2011). "Clinical correlates of magnetic resonance imaging in pediatric cerebral malaria," in ASTMH Annual Meeting (Philadelphia, PA: American Society of Tropical Medicine and Hygiene).
68. Sharma, R., Gohain, S., Chandra, J., Kumar, V., Chopra, A., Chatterjee, S., et al. (2012). Plasmodium vivax malaria admissions and risk of mortality in a tertiary-care children's hospital in North India. Paediatr. Int. Child Health 32, 152-157. doi: 10.1179/2046905512Y.0000000012
69. Shlosberg, D., Benifla, M., Kaufer, D., and Friedman, A. (2010). Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat. Rev. Neurol. 6, 393-403. doi: 10.1038/nrneurol.2010.74
70. Silamut, K., Phu, N. H., Whitty, C., Turner, G. D., Louwrier, K., Mai, N. T., et al. (1999). A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am. J. Pathol. 155, 395-410. doi: 10.1016/S0002-9440(10)65136-X
71. Smith, J. D., Rowe, J. A., Higgins, M. K., and Lavstsen, T. (2013). Malaria's deadly grip: cytoadhesion of Plasmodium falciparum-infected erythrocytes. Cell. Microbiol. 15, 1976-1983. doi: 10.1111/cmi.12183
72. Thapa, R., Patra, V., and Kundu, R. (2007). Plasmodium vivax cerebral malaria. Indian Pediatr. 44, 433-434.
73. Tripathi, A. K., Sha, W., Shulaev, V., Stins, M. F., and Sullivan, D. J. Jr. (2009). Plasmodium falciparum-infected erythrocytes induce NF-kappaB regulated inflammatory pathways in human cerebral endothelium. Blood 114, 4243-4252. doi: 10.1182/blood-2009-06-226415
74. Tsao, N., Hsu, H. P., Wu, C. M., Liu, C. C., and Lei, H. Y. (2001). Tumour necrosis factor-alpha causes an increase in blood-brain barrier permeability during sepsis. J. Med. Microbiol. 50, 812-821.
75. Turner, L., Lavstsen, T., Berger, S. S., Wang, C. W., Petersen, J. E., Avril, M., et al. (2013). Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498, 502-505. doi: 10.1038/nature12216
76. Van Der Heyde, H. C., Nolan, J., Combes, V., Gramaglia, I., and Grau, G. E. (2006). A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends Parasitol. 22, 503-508. doi: 10.1016/j.pt.2006.09.002
77. Van Hensbroek, M. B., Palmer, A., Jaffar, S., Schneider, G., and Kwiatkowski, D. (1997). Residual neurologic sequelae after childhood cerebral malaria. J. Pediatr. 131, 125-129. doi: 10.1016/S0022-3476(97)70135-5
78. Waller, D., Crawley, J., Nosten, F., Chapman, D., Krishna, S., Craddock, C., et al. (1991). Intracranial pressure in childhood cerebral malaria. Trans. R. Soc. Trop. Med. Hyg. 85, 362-364. doi: 10.1016/0035-9203(91)90291-6
79. White, N. J., and Ho, M. (1992). The pathophysiology of malaria. Adv. Parasitol. 31, 83-173. doi: 10.1016/S0065-308X(08)60021-4
80. White, N. J., Turner, G. D., Day, N. P., and Dondorp, A. M. (2013). Lethal malaria: Marchiafava and Bignami were right. J. Infect. Dis. 208, 192-198. doi: 10.1093/infdis/jit116
81. WHO. (2011). "World Malaria Report: 2011," in WHO Global Malaria Programme (Geneva: World Health Organization).
82. Willenborg, D. O., Staykova, M., Fordham, S., O'Brien, N., and Linares, D. (2007). The contribution of nitric oxide and interferon gamma to the regulation of the neuro-inflammation in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 191, 16-25. doi: 10.1016/j.jneuroim.2007.09.007
83. Xue, M., Minhas, N., Chow, S. O., Dervish, S., Sambrook, P. N., March, L., et al. (2010). Endogenous protein C is essential for the functional integrity of human endothelial cells. Cell. Mol. Life Sci. 67, 1537-1546. doi: 10.1007/s00018-010-0269-y
84. Yuh, E. L., and Dillon, W. P. (2010). Intracranial hypotension and intracranial hypertension. Neuroimaging Clin. N. Am. 20, 597-617. doi: 10.1016/j.nic.2010.07.012
85. Zhao, H., Aoshi, T., Kawai, S., Mori, Y., Konishi, A., Ozkan, M., et al. (2014). Olfactory plays a key role in spatiotemporal pathogenesis of cerebral malaria. Cell Host Microbe 15, 551-563. doi: 10.1016/j.chom.2014.04.008
86. Zhao, S. Z., and Mackenzie, I. J. (2011). Deafness: malaria as a forgotten cause. Ann. Trop. Paediatr. 31, 1-10. doi: 10.1179/146532811X12925735813724