• 1

    World Health Organization, 2000. Severe falciparum malaria. Trans R Soc Trop Med Hyg 94 :1–90.

  • 2

    Mishra SK, Newton CR, 2009. Diagnosis and management of the neurological complications of falciparum malaria. Nat Rev Neurol 5 :189–198.

    • Search Google Scholar
    • Export Citation
  • 3

    Boivin MJ, Bangirana P, Byarugaba J, Opoka RO, Idro R, Jurek AM, John CC, 2007. Cognitive impairment after cerebral malaria in children: a prospective study. Pediatrics 119 :e360–e366.

    • Search Google Scholar
    • Export Citation
  • 4

    Idro R, Carter JA, Fegan G, Neville BG, Newton CR, 2006. Risk factors for persisting neurological and cognitive impairments following cerebral malaria. Arch Dis Child 91 :142–148.

    • Search Google Scholar
    • Export Citation
  • 5

    John CC, Bangirana P, Byarugaba J, Opoka RO, Idro R, Jurek AM, Wu B, Boivin MJ, 2008. Cerebral malaria in children is associated with long-term cognitive impairment. Pediatrics 122 :e92–e99.

    • Search Google Scholar
    • Export Citation
  • 6

    Hunt NH, Golenser J, Chan-Ling T, Parekh S, Rae C, Potter S, Medana IM, Miu J, Ball HJ, 2006. Immunopathogenesis of cerebral malaria. Int J Parasitol 36 :569–582.

    • Search Google Scholar
    • Export Citation
  • 7

    Idro R, Jenkins NE, Newton CR, 2005. Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol 4 :827–840.

    • Search Google Scholar
    • Export Citation
  • 8

    van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE, 2006. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to micro-circulatory dysfunction. Trends Parasitol 22 :503–508.

    • Search Google Scholar
    • Export Citation
  • 9

    Beare NA, Harding SP, Taylor TE, Lewallen S, Molyneux ME, 2009. Perfusion abnormalities in children with cerebral malaria and malarial retinopathy. J Infect Dis 199 :263–271.

    • Search Google Scholar
    • Export Citation
  • 10

    Marchiafava E, Bignami A, 1894. On Summer-Autumnal Malaria Fevers. Malaria and the Parasites of Malaria Fevers, London: New Sydenham Society, 1–234.

  • 11

    Berendt AR, Tumer GD, Newbold CI, 1994. Cerebral malaria: the sequestration hypothesis. Parasitol Today 10 :412–414.

  • 12

    Newton CR, Hien TT, White N, 2000. Cerebral malaria. J Neurol Neurosurg Psychiatry 69 :433–441.

  • 13

    Moller HE, Kurlemann G, Putzler M, Wiedermann D, Hilbich T,V Fiedler B, 2005. Magnetic resonance spectroscopy in patients with MELAS. J Neurol Sci 229–230 :131–139.

    • Search Google Scholar
    • Export Citation
  • 14

    Petersen ET, Zimine I, Ho YC, Golay X, 2006. Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79 :688–701.

    • Search Google Scholar
    • Export Citation
  • 15

    Laureys S, Owen AM, Schiff ND, 2004. Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3 :537–546.

  • 16

    White NJ, Warrell DA, Looareesuwan S, Chanthavanich P, Phillips RE, Pongpaew P, 1985. Pathophysiological and prognostic significance of cerebrospinal-fluid lactate in cerebral malaria. Lancet 1 :776–778.

    • Search Google Scholar
    • Export Citation
  • 17

    Medana IM, Hien TT, Day NP, Phu NH, Mai NT, Chu’ong LV, Chau TT, Taylor A, Salahifar H, Stocker R, Smythe G, Turner GD, Farrar J, White NJ, Hunt NH, 2002. The clinical significance of cerebrospinal fluid levels of kynurenine pathway metabolites and lactate in severe malaria. J Infect Dis 185 :650–656.

    • Search Google Scholar
    • Export Citation
  • 18

    Medana IM, Day NP, Hien TT, Mai NT, Bethell D, Phu NH, Farrar J, Esiri MM, White NJ, Turner GD, 2002. Axonal injury in cerebral malaria. Am J Pathol 160 :655–666.

    • Search Google Scholar
    • Export Citation
  • 19

    Medana IM, Idro R, Newton CR, 2007. Axonal and astrocyte injury markers in the cerebrospinal fluid of Kenyan children with severe malaria. J Neurol Sci 258 :93–98.

    • Search Google Scholar
    • Export Citation
  • 20

    Ross AJ, Sachdev PS, 2004. Magnetic resonance spectroscopy in cognitive research. Brain Res Brain Res Rev 44 :83–102.

  • 21

    Penet MF, Viola A, Confort-Gouny S, Le Fur Y, Duhamel G, Kober F, Ibarrola D, Izquierdo M, Coltel N, Gharib B, Grau GE, Cozzone PJ, 2005. Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J Neurosci 25 :7352–7358.

    • Search Google Scholar
    • Export Citation
  • 22

    Penet MF, Kober F, Confort-Gouny S, Le Fur Y, Dalmasso C, Coltel N, Liprandi A, Gulian JM, Grau GE, Cozzone PJ, Viola A, 2007. Magnetic resonance spectroscopy reveals an impaired brain metabolic profile in mice resistant to cerebral malaria infected with Plasmodium berghei ANKA. J Biol Chem 282 :14505–14514.

    • Search Google Scholar
    • Export Citation
  • 23

    von Zur Muhlen C, Sibson NR, Peter K, Campbell SJ, Wilainam P, Grau GE, Bode C, Choudhury RP, Anthony DC, 2008. A contrast agent recognizing activated platelets reveals murine cerebral malaria pathology undetectable by conventional MRI. J Clin Invest 118 :1198–1207.

    • Search Google Scholar
    • Export Citation
  • 24

    Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K, 2005. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53 :1432–1440.

    • Search Google Scholar
    • Export Citation
  • 25

    Sugiyama M, Ikeda E, Kawai S, Higuchi T, Zhang H, Khan N, Tomiyoshi K, Inoue T, Yamaguchi H, Katakura K, Endo K, Suzuki M, 2004. Cerebral metabolic reduction in severe malaria: fluorodeoxyglucose-positron emission tomography imaging in a primate model of severe human malaria with cerebral involvement. Am J Trop Med Hyg 71 :542–545.

    • Search Google Scholar
    • Export Citation
  • 26

    Khuong M, Balloul H, De Brucker T, Vachon F, Wolff M, Coulaud J, 1990. Un cas de syndrome cérébelleux au décours d’un neuropaludisme grave: lésions observées en IRM. Med Mal Infect 20 :157–159.

    • Search Google Scholar
    • Export Citation
  • 27

    Kampfl AW, Birbamer GG, Pfausler BE, Haring HP, Schmutzhard E, 1993. Isolated pontine lesion in algid cerebral malaria: clinical features, management, and magnetic resonance imaging findings. Am J Trop Med Hyg 48 :818–822.

    • Search Google Scholar
    • Export Citation
  • 28

    Saissy JM, Pats B, Renard JL, Dubayle P, Herve R, 1996. Isolated bulb lesion following mild Plasmodium falciparum malaria diagnosed by magnetic resonance imaging. Intensive Care Med 22 :610–611.

    • Search Google Scholar
    • Export Citation
  • 29

    Cordoliani YS, Sarrazin JL, Felten D, Caumes E, Leveque C, Fisch A, 1998. MR of cerebral malaria. AJNR Am J Neuroradiol 19 :871–874.

  • 30

    Sakai O, Barest GD, 2005. Diffusion-weighted imaging of cerebral malaria. J Neuroimaging 15 :278–280.

  • 31

    Gamanagatti S, Kandpal H, 2006. MR imaging of cerebral malaria in a child. Eur J Radiol 60 :46–47.

  • 32

    Looareesuwan S, Wilairatana P, Krishna S, Kendall B, Vannaphan S, Viravan C, White NJ, 1995. Magnetic resonance imaging of the brain in patients with cerebral malaria. Clin Infect Dis 21 :300–309.

    • Search Google Scholar
    • Export Citation
  • 33

    Das CJ, Sharma R, 2007. Central pontine myelinolysis in a case of cerebral malaria. Br J Radiol 80 :e293–e295.

  • 34

    Yadav P, Sharma R, Kumar S, Kumar U, 2008. Magnetic resonance features of cerebral malaria. Acta Radiol 49 :566–569.

  • 35

    Laothamatas J, Tosti CL, Golay X, Van Cauteren M, Lekprasert V, Tangpukdee N, Krudsood S, Leowattana W, Wilairatana P, Swaminathan SV, DeLaPaz RL, Brown TR, Looareesuwan S, Brittenham GM, 2006. Magnetic resonance imaging (MRI) evidence of white matter injury in patients with acute uncomplicated falciparum malaria. Am J Trop Med Hyg 75 :196 (abstract).

    • Search Google Scholar
    • Export Citation
  • 36

    Tosti CL, Laothamatas J, Golay X, Swaminathan SV, Van Cauteren M, Murdoch J, Lekprasert V, Tangpukdee N, Krudsood S, Leowattana W, Wilairatana P, DeLaPaz RL, Brown TR, Brittenham GM, 2007. Cerebrospinal fluid lactate in P. falciparum malaria: measurement by chemical shift imaging at 3 Tesla. Proc Intl Soc Mag Reson Med 15 :398.

    • Search Google Scholar
    • Export Citation
 
 

 

 

 

 

 

 

Cerebral Malaria: A New Way Forward with Magnetic Resonance Imaging (MRI)

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  • 1 Department of Clinical Tropical Medicine and Hospital for Tropical Diseases, Faculty of Tropical Medicine, and Department of Radiology, Ramathibodi Hospital, Faculty of Medicine, Mahidol University, Bangkok, Thailand; Departments of Radiology and Biomedical Engineering and of Pediatrics and Medicine, College of Physicians and Surgeons, Columbia University, New York, New York

Magnetic resonance studies offer a new way through the impasse that now seems to block further progress in disentangling the pathogenesis and improving the treatment of cerebral malaria, a catastrophic neurologic complication of infection with Plasmodium falciparum. The underlying mechanisms responsible for coma in cerebral malaria are still unknown and the relative contributions of the microvascular sequestration of infected erythrocytes, the inflammatory response to P. falciparum, disordered hemostasis, and other factors remain controversial. For more than a century, neuropathologic studies have provided the basis for concepts of causation of cerebral malaria. Magnetic resonance techniques now offer non-invasive means of determining essential anatomic, metabolic, biochemical, and functional features of the brain in patients with cerebral malaria during life that could transform our understanding of the pathogenesis of cerebral malaria and lead to the development of new neuroprotective treatments.

Magnetic resonance studies offer a new way through the impasse that now seems to block further progress in disentangling the pathogenesis and improving the treatment of cerebral malaria, a catastrophic neurologic complication of infection with Plasmodium falciparum. In many parts of the world, this complex syndrome of potentially reversible encephalopathy with coma is the most common clinical presentation and cause of death in patients with falciparum malaria. 1,2 In those who survive, persistent neurocognitive defects are now recognized, affecting up to one in four children in sub-Saharan Africa who recover from the acute episode.35 The underlying mechanisms responsible for coma in cerebral malaria are still unknown and the relative contributions of the microvascular sequestration of infected erythrocytes, the inflammatory response to P. falciparum, disordered hemostasis, and other factors remain controversial.69 Treatment continues to consist only of administration of antimalarials with emergency supportive care, including management of hypoxemia, hypoglycemia, hypovolemia, shock, anemia, metabolic acidosis, and seizures1; no specific or neuroprotective therapy is available.

For more than a century, neuropathologic studies have provided the basis for concepts of causation of cerebral malaria. 10 The studies examine only patients who die, typically after anti-malarial treatment, using tissue specimens obtained at various times after death. 11 Their findings provide information about the end result rather than the course of the disease. Although comparisons have been made between fatal and surviving cases using biochemical, immunologic and pathologic examinations of tissue obtained by biopsy or of cerebrospinal fluid, blood, urine, or other body fluids, the resulting data are generally indirect. In addition, their interpretation is subject to limitations arising both from the details of metabolism and clearance of the disease indicator studied and from the specific assays used. Genetic approaches and observations in experimental systems in vitro have made important contributions but their interpretation and application are also problematic. In some circumstances, animal “models” provide alternative means of examining the biologic origins of a disorder. Rodents and primates may be infected with natural species of malaria but the manifestations and progression of these animal malarias differ from those of P. falciparum. In particular, the histopathologic hallmark of human cerebral malaria—sequestration of infected erythrocytes within the cerebral microvasculature—is absent. 11,12

Magnetic resonance techniques offer a non-invasive means of determining essential anatomic, metabolic, biochemical, and functional features of the brain 13 in patients with cerebral malaria during life. Magnetic resonance imaging (MRI) can provide sensitive detection of structural lesions, edema, hemorrhage, and thrombosis. Time of flight magnetic resonance angiography (TOF-MRA) can detect macroscopic vascular stenosis and, together with diffusion-weighted (DWI) images, identify effects on distal cerebral perfusion, such as diffusion–perfusion mismatch. Measurement of cerebral blood flow using arterial spin labeling (ASL) techniques can provide information about regional tissue perfusion on a scale of millimeters. 14 Functional magnetic resonance studies (fMRI) are methodologically complex, in part because the coupling between neural activity and local cerebral blood flow almost certainly is different in patients with cerebral malaria and in healthy controls. Despite these difficulties, fMRI studies have the potential to provide information on the regional distribution of neural activity during coma and recovery that could help determine whether the severe neurologic dysfunction of cerebral malaria has its origin in specific regions of the brain or is the product of a global, diffuse process. 15 Proton magnetic resonance spectroscopy (1H MRS) can measure lactate, a key indicator of the severity of the pathologic processes responsible for cerebral malaria and an important independent predictor of poor outcome. 16,17 In addition, 1H MRS can determine N-acetylaspartate, an index of axonal integrity, providing a means of detecting diffuse axonal damage. 18,19 Moreover, 1H MRS can quantify total creatine (an indicator of intact energy metabolism), myoinositol (potentially, an astrocyte marker), glutamate (the principal excitatory neurotransmitter), glutamine (the amination product of glutamine in astrocytes), and choline compounds (involved in membrane turnover). 13, 31P magnetic resonance spectroscopy (31P MRS) permits assessment of brain bioenergetics by measurement of adenosine 5′-triphosphate, phosphocreatine, inorganic phosphate, and intracellular pH. 13,20 Magnetic resonance examinations of mice infected with Plasmodium berghei ANKA have documented the applicability of most of these techniques in vivo.2123 No magnetic resonance method has been developed to detect microvascular sequestration of infected erythrocytes but perfusion maps derived from ASL, fractional anisotropy maps from diffusion tensor imaging (DTI), and diffusional kurtosis imaging (DKI) 24 offer promising approaches. In the future, other imaging methods, such as positron emission tomography (PET), 25 may also become feasible in malaria-endemic areas.

Magnetic resonance examinations of patients infected with P. falciparum could transform our understanding of the pathogenesis of cerebral malaria. Until now, almost all MRI studies have involved unsystematic examinations of single or small series of patients who developed cerebral malaria after travel to an endemic area. 2631, The first (and still only) MRI study of a series of malaria patients living in an endemic area—more than a decade ago, using a 0.2 Tesla scanner—showed that cerebral edema is not consistently found in living patients with cerebral malaria and consequently cannot always be the cause of their coma. 32 The current generation of clinical magnetic resonance instrumentation now operates at 3.0 Tesla and the methods listed above have been refined or developed substantially in the years since this first study. Clinical MRI units are now available in or near some endemic areas and reports of single cases and small numbers of patients with cerebral malaria are beginning to appear. 33,34 Despite an array of technical and logistic challenges, these clinical MRI facilities can be adapted for investigational use. 35,36 We now need research teams and resources to overcome the challenges of using magnetic resonance techniques for the study of cerebral malaria. Over the past 30 years, billions of dollars have been invested in the development of magnetic resonance methods for studies of disorders affecting the developed world. Application of these methods to the study of malaria could provide enormous dividends in advancing our understanding of this scourge of the developing world and lead to the development of new neuroprotective treatments.

*

Address correspondence to Gary M. Brittenham, Columbia University College of Physicians and Surgeons, Children’s Hospital of New York, Room CHN 10-08, 3959 Broadway, New York, NY 10032. E-mail: gmb31@columbia.edu

Deceased.

Authors’ addresses: Jiraporn Laothamatas, Advanced Diagnostic Imaging and Image-guided Minimally Invasive Therapy Center, Sirikit Medical Building, Ramathibodi Hospital, Mahidol University, Rama VI Road, Ratchatewi, Bangkok 10400, Thailand, Tel: +66-2-246-0024, Fax: +66-2-354-7233, E-mail: laothamatas@gmail.com. Truman R. Brown, Columbia University College of Physicians and Surgeons, Hatch Magnetic Resonance Research Center, 710 West 168th Street, New York, NY 10032, Tel: 212-305-1864, Fax: 212-342-5773, E-mail: trb11@columbia.edu. Gary M. Brittenham, Columbia University College of Physicians and Surgeons, Children’s Hospital of New York, Room CHN 10-08, 3959 Broadway, New York, NY 10032, Tel: 212-305-7005, Fax: 212-305-8428, E-mail: gmb31@columbia.edu.

Disclosure: T. R. Brown wishes to disclose that he has served as a consultant to Philips Medical Systems, a manufacturer of MRI equipment. This statement is made in the interest of full disclosure and not because the author considers this to be a conflict of interest.

REFERENCES

  • 1

    World Health Organization, 2000. Severe falciparum malaria. Trans R Soc Trop Med Hyg 94 :1–90.

  • 2

    Mishra SK, Newton CR, 2009. Diagnosis and management of the neurological complications of falciparum malaria. Nat Rev Neurol 5 :189–198.

    • Search Google Scholar
    • Export Citation
  • 3

    Boivin MJ, Bangirana P, Byarugaba J, Opoka RO, Idro R, Jurek AM, John CC, 2007. Cognitive impairment after cerebral malaria in children: a prospective study. Pediatrics 119 :e360–e366.

    • Search Google Scholar
    • Export Citation
  • 4

    Idro R, Carter JA, Fegan G, Neville BG, Newton CR, 2006. Risk factors for persisting neurological and cognitive impairments following cerebral malaria. Arch Dis Child 91 :142–148.

    • Search Google Scholar
    • Export Citation
  • 5

    John CC, Bangirana P, Byarugaba J, Opoka RO, Idro R, Jurek AM, Wu B, Boivin MJ, 2008. Cerebral malaria in children is associated with long-term cognitive impairment. Pediatrics 122 :e92–e99.

    • Search Google Scholar
    • Export Citation
  • 6

    Hunt NH, Golenser J, Chan-Ling T, Parekh S, Rae C, Potter S, Medana IM, Miu J, Ball HJ, 2006. Immunopathogenesis of cerebral malaria. Int J Parasitol 36 :569–582.

    • Search Google Scholar
    • Export Citation
  • 7

    Idro R, Jenkins NE, Newton CR, 2005. Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol 4 :827–840.

    • Search Google Scholar
    • Export Citation
  • 8

    van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE, 2006. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to micro-circulatory dysfunction. Trends Parasitol 22 :503–508.

    • Search Google Scholar
    • Export Citation
  • 9

    Beare NA, Harding SP, Taylor TE, Lewallen S, Molyneux ME, 2009. Perfusion abnormalities in children with cerebral malaria and malarial retinopathy. J Infect Dis 199 :263–271.

    • Search Google Scholar
    • Export Citation
  • 10

    Marchiafava E, Bignami A, 1894. On Summer-Autumnal Malaria Fevers. Malaria and the Parasites of Malaria Fevers, London: New Sydenham Society, 1–234.

  • 11

    Berendt AR, Tumer GD, Newbold CI, 1994. Cerebral malaria: the sequestration hypothesis. Parasitol Today 10 :412–414.

  • 12

    Newton CR, Hien TT, White N, 2000. Cerebral malaria. J Neurol Neurosurg Psychiatry 69 :433–441.

  • 13

    Moller HE, Kurlemann G, Putzler M, Wiedermann D, Hilbich T,V Fiedler B, 2005. Magnetic resonance spectroscopy in patients with MELAS. J Neurol Sci 229–230 :131–139.

    • Search Google Scholar
    • Export Citation
  • 14

    Petersen ET, Zimine I, Ho YC, Golay X, 2006. Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79 :688–701.

    • Search Google Scholar
    • Export Citation
  • 15

    Laureys S, Owen AM, Schiff ND, 2004. Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3 :537–546.

  • 16

    White NJ, Warrell DA, Looareesuwan S, Chanthavanich P, Phillips RE, Pongpaew P, 1985. Pathophysiological and prognostic significance of cerebrospinal-fluid lactate in cerebral malaria. Lancet 1 :776–778.

    • Search Google Scholar
    • Export Citation
  • 17

    Medana IM, Hien TT, Day NP, Phu NH, Mai NT, Chu’ong LV, Chau TT, Taylor A, Salahifar H, Stocker R, Smythe G, Turner GD, Farrar J, White NJ, Hunt NH, 2002. The clinical significance of cerebrospinal fluid levels of kynurenine pathway metabolites and lactate in severe malaria. J Infect Dis 185 :650–656.

    • Search Google Scholar
    • Export Citation
  • 18

    Medana IM, Day NP, Hien TT, Mai NT, Bethell D, Phu NH, Farrar J, Esiri MM, White NJ, Turner GD, 2002. Axonal injury in cerebral malaria. Am J Pathol 160 :655–666.

    • Search Google Scholar
    • Export Citation
  • 19

    Medana IM, Idro R, Newton CR, 2007. Axonal and astrocyte injury markers in the cerebrospinal fluid of Kenyan children with severe malaria. J Neurol Sci 258 :93–98.

    • Search Google Scholar
    • Export Citation
  • 20

    Ross AJ, Sachdev PS, 2004. Magnetic resonance spectroscopy in cognitive research. Brain Res Brain Res Rev 44 :83–102.

  • 21

    Penet MF, Viola A, Confort-Gouny S, Le Fur Y, Duhamel G, Kober F, Ibarrola D, Izquierdo M, Coltel N, Gharib B, Grau GE, Cozzone PJ, 2005. Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J Neurosci 25 :7352–7358.

    • Search Google Scholar
    • Export Citation
  • 22

    Penet MF, Kober F, Confort-Gouny S, Le Fur Y, Dalmasso C, Coltel N, Liprandi A, Gulian JM, Grau GE, Cozzone PJ, Viola A, 2007. Magnetic resonance spectroscopy reveals an impaired brain metabolic profile in mice resistant to cerebral malaria infected with Plasmodium berghei ANKA. J Biol Chem 282 :14505–14514.

    • Search Google Scholar
    • Export Citation
  • 23

    von Zur Muhlen C, Sibson NR, Peter K, Campbell SJ, Wilainam P, Grau GE, Bode C, Choudhury RP, Anthony DC, 2008. A contrast agent recognizing activated platelets reveals murine cerebral malaria pathology undetectable by conventional MRI. J Clin Invest 118 :1198–1207.

    • Search Google Scholar
    • Export Citation
  • 24

    Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K, 2005. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53 :1432–1440.

    • Search Google Scholar
    • Export Citation
  • 25

    Sugiyama M, Ikeda E, Kawai S, Higuchi T, Zhang H, Khan N, Tomiyoshi K, Inoue T, Yamaguchi H, Katakura K, Endo K, Suzuki M, 2004. Cerebral metabolic reduction in severe malaria: fluorodeoxyglucose-positron emission tomography imaging in a primate model of severe human malaria with cerebral involvement. Am J Trop Med Hyg 71 :542–545.

    • Search Google Scholar
    • Export Citation
  • 26

    Khuong M, Balloul H, De Brucker T, Vachon F, Wolff M, Coulaud J, 1990. Un cas de syndrome cérébelleux au décours d’un neuropaludisme grave: lésions observées en IRM. Med Mal Infect 20 :157–159.

    • Search Google Scholar
    • Export Citation
  • 27

    Kampfl AW, Birbamer GG, Pfausler BE, Haring HP, Schmutzhard E, 1993. Isolated pontine lesion in algid cerebral malaria: clinical features, management, and magnetic resonance imaging findings. Am J Trop Med Hyg 48 :818–822.

    • Search Google Scholar
    • Export Citation
  • 28

    Saissy JM, Pats B, Renard JL, Dubayle P, Herve R, 1996. Isolated bulb lesion following mild Plasmodium falciparum malaria diagnosed by magnetic resonance imaging. Intensive Care Med 22 :610–611.

    • Search Google Scholar
    • Export Citation
  • 29

    Cordoliani YS, Sarrazin JL, Felten D, Caumes E, Leveque C, Fisch A, 1998. MR of cerebral malaria. AJNR Am J Neuroradiol 19 :871–874.

  • 30

    Sakai O, Barest GD, 2005. Diffusion-weighted imaging of cerebral malaria. J Neuroimaging 15 :278–280.

  • 31

    Gamanagatti S, Kandpal H, 2006. MR imaging of cerebral malaria in a child. Eur J Radiol 60 :46–47.

  • 32

    Looareesuwan S, Wilairatana P, Krishna S, Kendall B, Vannaphan S, Viravan C, White NJ, 1995. Magnetic resonance imaging of the brain in patients with cerebral malaria. Clin Infect Dis 21 :300–309.

    • Search Google Scholar
    • Export Citation
  • 33

    Das CJ, Sharma R, 2007. Central pontine myelinolysis in a case of cerebral malaria. Br J Radiol 80 :e293–e295.

  • 34

    Yadav P, Sharma R, Kumar S, Kumar U, 2008. Magnetic resonance features of cerebral malaria. Acta Radiol 49 :566–569.

  • 35

    Laothamatas J, Tosti CL, Golay X, Van Cauteren M, Lekprasert V, Tangpukdee N, Krudsood S, Leowattana W, Wilairatana P, Swaminathan SV, DeLaPaz RL, Brown TR, Looareesuwan S, Brittenham GM, 2006. Magnetic resonance imaging (MRI) evidence of white matter injury in patients with acute uncomplicated falciparum malaria. Am J Trop Med Hyg 75 :196 (abstract).

    • Search Google Scholar
    • Export Citation
  • 36

    Tosti CL, Laothamatas J, Golay X, Swaminathan SV, Van Cauteren M, Murdoch J, Lekprasert V, Tangpukdee N, Krudsood S, Leowattana W, Wilairatana P, DeLaPaz RL, Brown TR, Brittenham GM, 2007. Cerebrospinal fluid lactate in P. falciparum malaria: measurement by chemical shift imaging at 3 Tesla. Proc Intl Soc Mag Reson Med 15 :398.

    • Search Google Scholar
    • Export Citation
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