Chapter 29 : Pathology and Pathogenesis of Malaria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Pathology and Pathogenesis of Malaria, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap29-1.gif /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap29-2.gif


This chapter focuses on the pathogenesis of malaria caused by and . It talks about two factors, parasite multiplication rate and cytoadherence of parasitized Red Blood Cells (RBCs), both of which enable parasites to achieve high densities and induce microvascular inflammation. The chapter considers several cytoadherence interactions between parasitized RBCs and host cells to better understand how parasites cause microvascular obstruction, inflammation, and dysfunction in vivo. Additional evidence for endothelial dysfunction in severe malaria has now been reported from a study of Indonesian adults. In this study, cell-free hemoglobin and arginase levels were elevated in patients with severe malaria, compared to those with moderately severe malaria or those who were healthy. The chapter presents the pathogenesis of vivax malaria, and discusses human genetic resistance to vivax malaria. It also describes working models of malaria pathogenesis which the authors believe provide useful frameworks for future studies. The authors propose that the levels of parasitemia and the strength of pathogen-host cell interactions are critically involved in the pathogenesis of malaria, and that host factors which interfere with parasite multiplication and sequestration are centrally important in ameliorating the severity of malaria. They suggest that RBC polymorphisms other than Duffy-negativity may reduce infection of RBCs or impair cytoadherence interactions between -infected RBCs and host cells. Like Duffy negativity, RBC polymorphisms that are found to protect against may teach the important aspects of the pathogenesis of this fascinating and sometimes deadly parasite.

Citation: Amaratunga C, Lopera-Mesa T, Tse J, Mita-Mendoza N, Fairhurst R. 2011. Pathology and Pathogenesis of Malaria, p 261-381. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch29

Key Concept Ranking

Acute Respiratory Distress Syndrome
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Life cycle of spp. Sporozoites injected into the dermis by female anopheline mosquitoes are carried through the blood and lymph to the liver, where they invade hepatocytes and form liver schizonts. After an incubation period of 7 to 14 days, each liver schizont releases tens of thousands of merozoites, which invade red blood cells (RBCs) and form ring-stage parasites. These forms are found freely circulating in the bloodstream until they mature to trophozoites, which sequester in microvessels while developing into schizonts. Merozoites released from schizonts establish rounds of asexual replication every 48 hours. Some ringstage parasites develop into sexualstage gametocytes, which circulate in the bloodstream and are taken up by female mosquitoes during a blood meal. After a cycle of sexual development in the mosquito, sporozoites enter the mosquito’s salivary gland and are injected into another host at the next blood meal. Image kindly reproduced with permission from Cell Press.

Citation: Amaratunga C, Lopera-Mesa T, Tse J, Mita-Mendoza N, Fairhurst R. 2011. Pathology and Pathogenesis of Malaria, p 261-381. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch29
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

A new model of falciparum malaria pathogenesis and protection. The sequestration of -infected red blood cells (RBCs) in microvessels is believed to activate microvascular endothelial cells (MVECs) and monocytes, which contribute to the microvessel inflammation associated with severe malaria. Hemoglobin (Hb) C and sickle HbS reduce the risk of severe malaria in sub-Saharan Africa. HbC and HbS are associated with abnormal display of erythrocyte membrane protein-1 (PfEMP-1), a family of antigenically variant cytoadherence ligands that serves as the parasite’s main virulence factor on the surface of parasitized RBCs. Reduced levels and abnormal distributions of PfEMP-1 are associated with impaired adherence of parasitized HbC and HbS RBCs to MVECs and monocytes (this is shown schematically at right as less intimate interactions between these parasitized RBCs, MVECs, and monocytes). By lowering the avidity of cytoadherence interactions, HbC and HbS may reduce the level of MVEC and monocyte activation in vivo and prevent the progression from uncomplicated to severe malaria. PfEMP-1-specific antibodies that reduce the avidity of these interactions may work in concert with Hb variants to dampen inflammation and ameliorate disease severity.

Citation: Amaratunga C, Lopera-Mesa T, Tse J, Mita-Mendoza N, Fairhurst R. 2011. Pathology and Pathogenesis of Malaria, p 261-381. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch29
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Agarwal, A.,, A. Guindo,, Y. Cissoko,, J. G. Taylor,, D. Coulibaly,, A. Kone,, K. Kayentao,, A. Djimde,, C. V. Plowe,, O. Doumbo,, T. E. Wellems, and, D. Diallo. 2000. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood 96:23582363.
2. Aidoo,, M.,, D. J. Terlouw,, M. S. Kolczak,, P. D. McElroy,, F. O. ter Kuile,, S. Kariuki,, B. L. Nahlen,, A. A. Lal, and, V. Udhayakumar. 2002. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 359:13111312.
3. Akech,, S. O.,, O. Hassall,, A. Pamba,, R. Idro,, T. N. Williams,, C. R. Newton, and, K. Maitland. 2008. Survival and haematological recovery of children with severe malaria transfused in accordance to WHO guidelines in Kilifi, Kenya. Malar. J. 7:256.
4. Allen,, S. J.,, A. O’Donnell,, N. D. Alexander,, M. P. Alpers,, T. E. Peto,, J. B. Clegg, and, D. J. Weatherall. 1997. alpha+-Thalassemia protects children against disease caused by other infections as well as malaria. Proc. Natl. Acad. Sci. USA 94:1473614741.
5. Allison, A. C. 1954. Protection afforded by sickle-cell trait against subtertian malareal infection. Br. Med. J. 1:290294.
6. Andrade,, B. B.,, A. Reis-Filho,, S. M. Souza-Neto,, J. Clarencio,, L. M. Camargo,, A. Barral, and, M. Barral-Netto. 2010. Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar. J. 9:13.
7. Anstey,, N. M.,, T. Handojo,, M. C. Pain,, E. Kenangalem,, E. Tjitra,, R. N. Price, and, G. P. Maguire. 2007. Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and posttreatment alveolar-capillary inflammation. J. Infect. Dis. 195:589596.
8. Anstey, N. M.,, B. Russell,, T. W. Yeo, and, R. N. Price. 2009. The pathophysiology of vivax malaria. Trends Parasitol. 25:220227.
9. Armah,, H.,, A. K. Dodoo,, E. K. Wiredu,, J. K. Stiles,, A. A. Adjei,, R. K. Gyasi, and, Y. Tettey. 2005a. High-level cerebellar expression of cytokines and adhesion molecules in fatal, paediatric, cerebral malaria. Ann. Trop. Med. Parasitol. 99:629647.
10. Armah,, H.,, E. K. Wired,, A. K. Dodoo,, A. A. Adjei,, Y. Tettey, and R. Gyasi. 2005b. Cytokines and adhesion molecules expression in the brain in human cerebral malaria. Int. J. Environ. Res. Public Health 2:123131.
11. Atkinson, C. T., and, M. Aikawa. 1990. Ultrastructure of malaria-infected erythrocytes. Blood Cells 16:351368.
12. Awandare, G. A.,, B. Goka,, P. Boeuf,, J. K. Tetteh,, J. A. Kurtzhals,, C. Behr, and, B. D. Akanmori. 2006. Increased levels of inflammatory mediators in children with severe Plasmodium falciparum malaria with respiratory distress. J. Infect. Dis. 194:14381446.
13. Baird, J. K. 2007. Neglect of Plasmodium vivax malaria. Trends Parasitol. 23:533539.
14. Baird, J. K. 2009. Malaria zoonoses. Travel Med. Infect. Dis. 7:269277.
15. Barnwell,, J. W.,, P. Ingravallo,, M. R. Galinski,, Y. Matsumoto, and, M. Aikawa. 1990. Plasmodium vivax: malarial proteins associated with the membrane-bound caveola-vesicle complexes and cytoplasmic cleft structures of infected erythrocytes. Exp. Parasitol. 70:8599.
16. Baruch,, D. I.,, B. L. Pasloske,, H. B. Singh,, X. Bi,, X. C. Ma,, M. Feldman,, T. F. Taraschi, and, R. J. Howard. 1995. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:7787.
17. Biswas,, A. K.,, A. Hafiz,, B. Banerjee,, K. S. Kim,, K. Datta, and, C. E. Chitnis. 2007. Plasmodium falciparum uses gC1qR/HABP1/p32 as a receptor to bind to vascular endothelium and for platelet-mediated clumping. PLoS Pathog. 3:12711280.
18. Brabin,, B. J.,, C. Romagosa,, S. Abdelgalil,, C. Menendez,, F. H. Verhoeff,, R. McGready,, K. A. Fletcher,, S. Owens,, U. D’Alessandro,, F. Nosten,, P. R. Fischer, and, J. Ordi. 2004. The sick placenta-the role of malaria. Placenta 25:359378.
19. Buffet,, P. A.,, G. Milon,, V. Brousse,, J. M. Correas,, B. Dousset,, A. Couvelard,, R. Kianmanesh,, O. Farges,, A. Sauvanet,, F. Paye,, M. N. Ungeheuer,, C. Ottone,, H. Khun,, L. Fiette,, G. Guigon,, M. Huerre,, O. Mercereau-Puijalon, and, P. H. David. 2006. Ex vivo perfusion of human spleens maintains clearing and processing functions. Blood 107:37453752.
20. Calis,, J. C.,, K. S. Phiri,, E. B. Faragher,, B. J. Brabin,, I. Bates,, L. E. Cuevas,, R. J. de Haan,, A. I. Phiri,, P. Malange,, M. Khoka,, P. J. Hulshof,, L. van Lieshout,, M. G. Beld,, Y. Y. Teo,, K. A. Rockett,, A. Richardson,, D. P. Kwiatkowski,, M. E. Molyneux, and, M. B. van Hensbroek. 2008. Severe anemia in Malawian children. N. Engl. J. Med. 358:888899.
21. Cappadoro, M.,, G. Giribaldi,, E. O’Brien,, F. Turrini,, F. Mannu,, D. Ulliers,, G. Simula,, L. Luzzatto, and, P. Arese. 1998. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92:25272534.
22. Carlton,, J. M.,, J. H. Adams,, J. C. Silva,, S. L. Bidwell,, H. Lorenzi,, E. Caler,, J. Crabtree,, S. V. Angiuoli,, E. F. Merino,, P. Amedeo,, Q. Cheng,, R. M. Coulson,, B. S. Crabb,, H. A. Del Portillo,, K. Essien,, T. V. Feldblyum,, C. Fernandez-Becerra,, P. R. Gilson,, A. H. Gueye,, X. Guo,, S. Kang’a,, T. W. Kooij,, M. Korsinczky,, E. V. Meyer,, V. Nene,, I. Paulsen,, O. White,, S. A. Ralph,, Q. Ren,, T. J. Sargeant,, S. L. Salzberg,, C. J. Stoeckert,, S. A. Sullivan,, M. M. Yamamoto,, S. L. Hoffman,, J. R. Wortman,, M. J. Gardner,, M. R. Galinski,, J. W. Barnwell, and, C. M. Fraser-Liggett. 2008. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455:757763.
23. Cattani,, J. A.,, F. D. Gibson,, M. P. Alpers, and, G. G. Crane. 1987. Hereditary ovalocytosis and reduced susceptibility to malaria in Papua New Guinea. Trans. R. Soc. Trop. Med. Hyg. 81:705709.
24. Chakravorty, S. J., and, A. Craig. 2005. The role of ICAM-1 in Plasmodium falciparum cytoadherence. Eur. J. Cell Biol. 84:1527.
25. Chakravorty, S. J.,, K. R. Hughes, and, A. G. Craig. 2008. Host response to cytoadherence in Plasmodium falciparum. Biochem Soc. Trans. 36:221228.
26. Cholera,, R.,, N. J. Brittain,, M. R. Gillrie,, T. M. Lopera-Mesa,, S. A. Diakite,, T. Arie,, M. A. Krause,, A. Guindo,, A. Tubman,, H. Fujioka,, D. A. Diallo,, O. K. Doumbo,, M. Ho,, T. E. Wellems, and, R. M. Fairhurst. 2008. Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc. Natl. Acad. Sci. USA 105:991996.
27. Chotivanich, K.,, R. Udomsangpetch,, R. McGready,, S. Proux,, P. Newton,, S. Pukrittayakamee,, S. Looareesuwan, and, N. J. White. 2002. Central role of the spleen in malaria parasite clearance. J. Infect. Dis. 185:15381541.
28. Clark,, I. A.,, L. M. Alleva,, A. C. Budd, and, W. B. Cowden. 2008. Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Med. Infect. Dis. 6:6781.
29. Clark, I. A., and, W. B. Cowden. 2003. The pathophysiology of falciparum malaria. Pharmacol. Ther. 99:221260.
30. Cockburn,, I. A.,, M. J. Mackinnon,, A. O’Donnell,, S. J. Allen,, J. M. Moulds,, M. Baisor,, M. Bockarie,, J. C. Reeder, and, J. A. Rowe. 2004. A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc. Natl. Acad. Sci. USA 101:272277.
31. Cogswell, F. B. 1992. The hypnozoite and relapse in primate malaria. Clin. Microbiol. Rev. 5:2635.
32. Collins, W. E., and, G. M. Jeffery. 2007. Plasmodium malariae: parasite and disease. Clin. Microbiol. Rev. 20:579592.
33. Collins, W. E.,, G. M. Jeffery, and, J. M. Roberts. 2003. A retrospective examination of anemia during infection of humans with Plasmodium vivax. Am. J. Trop. Med. Hyg. 68:410412.
34. Cowman, A. F., and, B. S. Crabb. 2006. Invasion of red blood cells by malaria parasites. Cell 124:755766.
35. Cox-Singh,, J.,, T. M. Davis,, K. S. Lee,, S. S. Shamsul,, A. Matusop,, S. Ratnam,, H. A. Rahman,, D. J. Conway, and, B. Singh. 2008. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin. Infect. Dis. 46:165171.
36. Cserti, C. M., and, W. H. Dzik. 2007. The ABO blood group system and Plasmodium falciparum malaria. Blood 110:22502258.
37. Culleton,, R. L.,, T. Mita,, M. Ndounga,, H. Unger,, P. V. Cravo,, G. M. Paganotti,, N. Takahashi,, A. Kaneko,, H. Eto,, H. Tinto,, C. Karema,, U. D’Alessandro,, V. do Rosario,, T. Kobayakawa,, F. Ntoumi,, R. Carter, and, K. Tanabe. 2008. Failure to detect Plasmodium vivax in West and Central Africa by PCR species typing. Malar. J. 7:174.
38. Daneshvar,, C.,, T. M. Davis,, J. Cox-Singh,, M. Z. Rafa’ee,, S. K. Zakaria,, P. C. Divis, and, B. Singh. 2009. Clinical and laboratory features of human Plasmodium knowlesi infection. Clin. Infect. Dis. 49:852860.
39. Das, B. S. 2008. Renal failure in malaria. J. Vector Borne Dis. 45:8397.
40. David,, P. H.,, M. Hommel,, L. H. Miller,, I. J. Udeinya, and, L. D. Oligino. 1983. Parasite sequestration in Plasmodium falciparum malaria: spleen and antibody modulation of cytoadherence of infected erythrocytes. Proc. Natl. Acad. Sci. USA 80:50755079.
41. del Portillo,, H. A.,, C. Fernandez-Becerra,, S. Bowman,, K. Oliver,, M. Preuss,, C. P. Sanchez,, N. K. Schneider,, J. M. Villalobos,, M. A. Rajandream,, D. Harris,, L. H. Pereira da Silva,, B. Barrell, and, M. Lanzer. 2001. A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 410:839842.
42. Desai,, M.,, F. O. ter Kuile,, F. Nosten,, R. McGready,, K. Asamoa,, B. Brabin, and, R. D. Newman. 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect. Dis. 7:93104.
43. Dondorp, A. M. 2008. Clinical significance of sequestration in adults with severe malaria. Transfus. Clin. Biol. 15:5657.
44. Dondorp,, A. M.,, V. Desakorn,, W. Pongtavornpinyo,, D. Sahassananda,, K. Silamut,, K. Chotivanich,, P. N. Newton,, P. Pitisuttithum,, A. M. Smithyman,, N. J. White, and, N. P. Day. 2005. Estimation of the total parasite biomass in acute falciparum malaria from plasma PfHRP2. PLoS Med. 2:e204.
45. Dondorp,, A. M.,, C. Ince,, P. Charunwatthana,, J. Hanson,, A. van Kuijen,, M. A. Faiz,, M. R. Rahman,, M. Hasan,, E. Bin Yunus,, A. Ghose,, R. Ruangveerayut,, D. Limmathurotsakul,, K. Mathura,, N. J. White, and, N. P. Day. 2008. Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria. J. Infect. Dis. 197:7984.
46. Dondorp,, A. M.,, M. Nyanoti,, P. A. Kager,, S. Mithwani,, J. Vreeken, and, K. Marsh. 2002. The role of reduced red cell deformability in the pathogenesis of severe falciparum malaria and its restoration by blood transfusion. Trans. R. Soc. Trop. Med. Hyg. 96:282286.
47. Doumbo,, O. K.,, M. A. Thera,, A. K. Kone,, A. Raza,, L. J. Tempest,, K. E. Lyke,, C. V. Plowe, and, J. A. Rowe. 2009. High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am. J. Trop. Med. Hyg. 81:987993.
48. Duffy, P. E. 2007. Plasmodium in the placenta: parasites, parity, protection, prevention and possibly preeclampsia. Parasitology 134:18771881.
49. Evans,, K. J.,, D. S. Hansen,, N. van Rooijen,, L. A. Buckingham, and, L. Schofield. 2006. Severe malarial anemia of low parasite burden in rodent models results from accelerated clearance of uninfected erythrocytes. Blood 107:11921199.
50. Faille, D.,, F. El-Assaad,, M. C. Alessi,, T. Fusai,, V. Combes, and, G. E. Grau. 2009. Platelet-endothelial cell interactions in cerebral malaria: the end of a cordial understanding. Thromb. Haemost. 102:10931102.
51. Fairhurst,, R. M.,, D. I. Baruch,, N. J. Brittain,, G. R. Ostera,, J. S. Wallach,, H. L. Hoang,, K. Hayton,, A. Guindo,, M. O. Makobongo,, O. M. Schwartz,, A. Tounkara,, O. K. Doumbo,, D. A. Diallo,, H. Fujioka,, M. Ho, and, T. E. Wellems. 2005. Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 435:11171121.
52. Fernandez-Becerra,, C.,, M. M. Yamamoto,, R. Z. Vencio,, M. Lacerda,, A. Rosanas-Urgell, and, H. A. del Portillo. 2009. Plasmodium vivax and the importance of the subtelomeric multigene vir superfamily. Trends Parasitol. 25:4451.
53. Field, J., and, P. Shute. 1956. Plasmodium vivax. The microscopic diagnosis of human malaria. erythrocytic parasites, vol. 2. A morphological study of the erythrocytic parasites. Institute for Medical Research, Kuala Lumpur, Malaysia.
54. Fowkes,, F. J.,, S. J. Allen,, A. Allen,, M. P. Alpers,, D. J. Weatherall, and, K. P. Day. 2008. Increased microerythrocyte count in homozygous alpha(+)-thalassaemia contributes to protection against severe malarial anaemia. PLoS Med. 5:e56.
55. Francischetti, I. M. 2008. Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol. 24:258263.
56. Francischetti,, I. M.,, K. B. Seydel,, and R. Q. Monteiro. 2008. Blood coagulation, inflammation, and malaria. Microcirculation 15:81107.
57. Francischetti,, I. M.,, K. B. Seydel,, R. Q. Monteiro,, R. O. Whitten,, C. R. Erexson,, A. L. Noronha,, G. R. Ostera,, S. B. Kamiza,, M. E. Molyneux,, J. M. Ward, and, T. E. Taylor. 2007. Plasmodium falciparum-infected erythrocytes induce tissue factor expression in endothelial cells and support the assembly of multimolecular coagulation complexes, J. Thromb. Haemost. 5:155165.
58. Fry,, A. E.,, M. J. Griffiths,, S. Auburn,, M. Diakite,, J. T. Forton,, A. Green,, A. Richardson,, J. Wilson,, M. Jallow,, F. Sisay-Joof,, M. Pinder,, N. Peshu,, T. N. Williams,, K. Marsh,, M. E. Molyneux,, T. E. Taylor,, K. A. Rockett, and, D. P. Kwiatkowski. 2008. Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum. Mol. Genet. 17:567576.
59. Galinski,, M. R.,, C. C. Medina,, P. Ingravallo, and, J. W. Barnwell. 1992. A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69:12131226.
60. Genton, B.,, V. D’Acremont,, L. Rare,, K. Baea,, J. C. Reeder,, M. P. Alpers, and, I. Muller. 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med. 5:e127.
61. Grimberg,, B. T.,, R. Udomsangpetch,, J. Xainli,, A. McHenry,, T. Panichakul,, J. Sattabongkot,, L. Cui,, M. Bockarie,, C. Chitnis,, J. Adams,, P. A. Zimmerman, and, C. L. King. 2007. Plasmodium vivax invasion of human erythrocytes inhibited by antibodies directed against the Duffy binding protein. PLoS Med. 4:e337.
62. Guindo,, A.,, R. M. Fairhurst,, O. K. Doumbo,, T. E. Wellems, and, D. A. Diallo. 2007. X-linked G6PD deficiency protects hemizygous males but not heterozygous females against severe malaria. PLoS Med. 4:e66.
63. Haldane, J. B. S. 1949. The rate in mutation in human genes. Hereditas 35:267273.
64. Handayani,, S.,, D. T. Chiu,, E. Tjitra,, J. S. Kuo,, D. Lampah,, E. Kenangalem,, L. Renia,, G. Snounou,, R. N. Price,, N. M. Anstey, and, B. Russell. 2009. High deformability of Plasmodium vivax-infected red blood cells under microfluidic conditions. J. Infect. Dis. 199:445450.
65. Hemmer,, C. J.,, F. G. Holst,, P. Kern,, C. B. Chiwakata,, M. Dietrich, and, E. C. Reisinger. 2006. Stronger host response per parasitized erythrocyte in Plasmodium vivax or ovale than in Plasmodium falciparum malaria. Trop. Med. Int. Health 11:817823.
66. Hill,, A. V.,, C. E. Allsopp,, D. Kwiatkowski,, N. M. Anstey,, P. Twumasi,, P. A. Rowe,, S. Bennett,, D. Brewster,, A. J. McMichael, and, B. M. Greenwood. 1991. Common west African HLA antigens are associated with protection from severe malaria. Nature 352:595600.
67. Hviid, L., and, A. Salanti. 2007. VAR2CSA and protective immunity against pregnancy-associated Plasmodium falciparum malaria. Parasitology 134:18711876.
68. Imbert, P.,, C. Rapp, and, P. A. Buffet. 2009. Pathological rupture of the spleen in malaria: analysis of 55 cases (1958-2008). Travel Med. Infect. Dis. 7:147159.
69. Jakeman, G. N.,, A. Saul,, W. L. Hogarth, and, W. E. Collins. 1999. Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119:127133.
70. Karunaweera, N.,, D. Wanasekara,, V. Chandrasekharan,, K. Mendis, and, R. Carter. 2007. Plasmodium vivax: paroxysmassociated lipids mediate leukocyte aggregation. Malar, J. 6:62.
71. Karunaweera,, N. D.,, S. K. Wijesekera,, D. Wanasekera,, K. N. Mendis, and, R. Carter. 2003. The paroxysm of Plasmodium vivax malaria. Trends Parasitol. 19:188193.
72. Kasehagen,, L. J.,, I. Mueller,, B. Kiniboro,, M. J. Bockarie,, J. C. Reeder,, J. W. Kazura,, W. Kastens,, D. T. McNamara,, C. H. King,, C. C. Whalen, and, P. A. Zimmerman. 2007. Reduced Plasmodium vivax erythrocyte infection in PNG Duffy-negative heterozygotes. PLoS ONE 2:e336.
73. Kaul,, D. K.,, E. F. Roth, Jr.,, R. L. Nagel,, R. J. Howard, and, S. M. Handunnetti. 1991. Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78:812819.
74. Kirchgatter, K., and, A. Portillo Hdel. 2002. Association of severe noncerebral Plasmodium falciparum malaria in Brazil with expressed PfEMP1 DBL1 alpha sequences lacking cysteine residues. Mol. Med. 8:1623.
75. Kochar,, D. K.,, A. Das,, S. K. Kochar,, V. Saxena,, P. Sirohi,, S. Garg,, A. Kochar,, M. P. Khatri, and, V. Gupta. 2009. Severe Plasmodium vivax malaria: a report on serial cases from Bikaner in northwestern India. Am. J. Trop. Med. Hyg. 80:194198.
76. Kraemer,, S. M.,, S. A. Kyes,, G. Aggarwal,, A. L. Springer,, S. O. Nelson,, Z. Christodoulou,, L. M. Smith,, W. Wang,, E. Levin,, C. I. Newbold,, P. J. Myler, and, J. D. Smith. 2007. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8:45.
77. Kraemer, S. M., and, J. D. Smith. 2006. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr. Opin. Microbiol. 9:374380.
78. Kwiatkowski,, D.,, C. A. Bate,, I. G. Scragg,, P. Beattie,, I. Udalova, and, J. C. Knight. 1997. The malarial fever response—pathogenesis, polymorphism and prospects for intervention. Ann. Trop. Med. Parasitol. 91:533542.
79. Kyriacou,, H. M.,, G. N. Stone,, R. J. Challis,, A. Raza,, K. E. Lyke,, M. A. Thera,, A. K. Kone,, O. K. Doumbo,, C. V. Plowe, and, J. A. Rowe. 2006. Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Mol. Biochem. Parasitol. 150:211218.
80. Le Scanf, C.,, I. Vigan-Womas,, H. Contamin,, M. Guillotte,, E. Bischoff, and, O. Mercereau-Puijalon. 2008. Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey. Microbes Infect. 10:447451.
81. Looareesuwan,, S.,, T. M. Davis,, S. Pukrittayakamee,, W. Supanaranond,, V. Desakorn,, K. Silamut,, S. Krishna,, S. Boonamrung, and, N. J. White. 1991. Erythrocyte survival in severe falciparum malaria. Acta Trop. 48:263270.
82. Looareesuwan,, S.,, A. H. Merry,, R. E. Phillips,, R. Pleehachinda,, Y. Wattanagoon,, M. Ho,, P. Charoenlarp,, D. A. Warrell, and, D. J. Weatherall. 1987. Reduced erythrocyte survival following clearance of malarial parasitaemia in Thai patients. Br. J. Haematol. 67:473478.
83. Louicharoen, C.,, E. Patin,, R. Paul,, I. Nuchprayoon,, B. Witoonpanich,, C. Peerapittayamongkol,, I. Casademont,, T. Sura,, N. M. Laird,, P. Singhasivanon,, L. Quintana-Murci, and, A. Sakuntabhai. 2009. Positively selected G6PD-Mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science 326:15461549.
84. Luse, S. A., and, L. H. Miller. 1971. Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels. Am. J. Trop. Med Hyg. 20:655660.
85. Luzzatto, L.,, F. A. Usanga, and, S. Reddy. 1969. Glucose-6-phosphate dehydrogenase deficient red cells: resistance to infection by malarial parasites. Science 164:839842.
86. MacPherson,, G. G.,, M. J. Warrell,, N. J. White,, S. Looareesuwan, and, D. A. Warrell. 1985. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am. J. Pathol. 119:385401.
87. Maitland, K., and, K. Marsh. 2004. Pathophysiology of severe malaria in children. Acta Trop. 90:131140.
88. Matsumoto, Y.,, M. Aikawa, and, J. W. Barnwell. 1988. Immunoelectron microscopic localization of vivax malaria antigens to the clefts and caveola-vesicle complexes of infected erythrocytes. Am. J. Trop. Med. Hyg. 39:317322.
89. May,, J.,, J. A. Evans,, C. Timmann,, C. Ehmen,, W. Busch,, T. Thye,, T. Agbenyega, and, R. D. Horstmann. 2007. Hemoglobin variants and disease manifestations in severe falciparum malaria. JAMA 297:22202226.
90. Medana, I. M., and, G. D. Turner. 2006. Human cerebral malaria and the blood-brain barrier. Int. J. Parasitol. 36:555568.
91. Ménard, D.,, C. Barnadas,, C. Bouchier,, C. Henry-Halldin,, L. R. Gray,, A. Ratsimbasoa,, V. Thonier,, J. F. Carod,, O. Domarle,, Y. Colin,, O. Bertrand,, J. Picot,, C. L. King,, B. T. Grimberg,, O. Mercereau-Puijalon, and, P. A. Zimmerman. 2010. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc. Natl. Acad. Sci. USA 107:59675971.
92. Mendis, K.,, B. J. Sina,, P. Marchesini, and, R. Carter. 2001. The neglected burden of Plasmodium vivax malaria. Am. J. Trop. Med. Hyg. 64:97106.
93. Miller,, L. H.,, S. J. Mason,, D. F. Clyde, and, M. H. McGinniss. 1976. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295: 302–304.
94. Mockenhaupt,, F. P.,, S. Ehrhardt,, J. P. Cramer,, R. N. Otchwemah,, S. D. Anemana,, K. Goltz,, F. Mylius,, E. Dietz,, T. A. Eggelte, and, U. Bienzle. 2004. Hemoglobin C and resistance to severe malaria in Ghanaian children. J. Infect. Dis. 190:10061009.
95. Modiano, D.,, G. Luoni,, B. S. Sirima,, J. Simpore,, F. Verra,, A. Konate,, E. Rastrelli,, A. Olivieri,, C. Calissano,, G. M. Paganotti,, L. D’Urbano,, I. Sanou,, A. Sawadogo,, G. Modiano, and, M. Coluzzi. 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 414:305308.
96. Mueller,, I.,, M. R. Galinski,, J. K. Baird,, J. M. Carlton,, D. K. Kochar,, P. L. Alonso, and, H. A. del Portillo. 2009. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect. Dis. 9:555566.
97. Mueller, I.,, P. A. Zimmerman, and, J. C. Reeder. 2007. Plasmodium malariae and Plasmodium ovale—the “bashful” malaria parasites. Trends Parasitol. 23:278283.
98. Nkhoma,, E. T.,, C. Poole,, V. Vannappagari,, S. A. Hall, and, E. Beutler. 2009. The global prevalence of glucose-6-phosphate dehydrogenase deficiency: a systematic review and meta-analysis. Blood Cells Mol. Dis. 42:267278.
99. Nunes, M. C., and, A. Scherf. 2007. Plasmodium falciparum during pregnancy: a puzzling parasite tissue adhesion tropism. Parasitology 134:18631869.
100. Odhiambo,, C. O.,, W. Otieno,, C. Adhiambo,, M. M. Odera, and, J. A. Stoute. 2008. Increased deposition of C3b on red cells with low CR1 and CD55 in a malaria-endemic region of western Kenya: implications for the development of severe anemia. BMC Med. 6:23.
101. Oo,, M. M.,, M. Aikawa,, T. Than,, T. M. Aye,, P. T. Myint,, I. Igarashi, and, W. C. Schoene. 1987. Human cerebral malaria: a pathological study. J. Neuropathol. Exp. Neurol. 46:223231.
102. Orengo,, J. M.,, A. Leliwa-Sytek,, J. E. Evans,, B. Evans,, D. van de Hoef,, M. Nyako,, K. Day, and, A. Rodriguez. 2009. Uric acid is a mediator of the Plasmodium falciparum- induced inflammatory response. PLoS ONE 4:e5194.
103. Persson,, K. E.,, F. J. McCallum,, L. Reiling,, N. A. Lister,, J. Stubbs,, A. F. Cowman,, K. Marsh, and, J. G. Beeson. 2008. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J. Clin. Invest. 118:342351.
104. Poespoprodjo,, J. R.,, W. Fobia,, E. Kenangalem,, D. A. Lampah,, A. Hasanuddin,, N. Warikar,, P. Sugiarto,, E. Tjitra,, N. M. Anstey, and, R. N. Price. 2009. Vivax malaria: a major cause of morbidity in early infancy. Clin. Infect. Dis. 48:17041712.
105. Pongponratn, E.,, M. Riganti,, B. Punpoowong, and, M. Aikawa. 1991. Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. Am. J. Trop. Med. Hyg. 44:168175.
106. Price, R. N.,, N. M. Douglas, and, N. M. Anstey. 2009. New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr. Opin. Infect. Dis. 22:430435.
107. Price, L.,, T. Planche,, C. Rayner, and, S. Krishna. 2007a. Acute respiratory distress syndrome in Plasmodium vivax malaria: case report and review of the literature. Trans. R. Soc. Trop. Med. Hyg. 101:655659.
108. Price,, R. N.,, J. A. Simpson,, F. Nosten,, C. Luxemburger,, L. Hkirjaroen,, F. ter Kuile,, T. Chongsuphajaisiddhi, and, N. J. White. 2001. Factors contributing to anemia after uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 65:614622.
109. Price,, R. N.,, E. Tjitra,, C. A. Guerra,, S. Yeung,, N. J. White, and, N. M. Anstey. 2007b. Vivax malaria: neglected and not benign. Am. J. Trop. Med. Hyg. 77:7987.
110. Prommano, O.,, U. Chaisri,, G. D. Turner,, P. Wilairatana,, D. J. Ferguson,, P. Viriyavejakul,, N. J. White, and, E. Pongponratn. 2005. A quantitative ultrastructural study of the liver and the spleen in fatal falciparum malaria. Southeast Asian J. Trop. Med. Public Health 36:13591370.
111. Rogerson, S. J., and, P. Boeuf. 2007. New approaches to pathogenesis of malaria in pregnancy. Parasitology 134:18831893.
112. Rogerson,, S. J.,, L. Hviid,, P. E. Duffy,, R. F. Leke, and, D. W. Taylor. 2007a. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect. Dis. 7:105117.
113. Rogerson, S. J.,, V. Mwapasa, and, S. R. Meshnick. 2007b. Malaria in pregnancy: linking immunity and pathogenesis to prevention. Am. J. Trop. Med. Hyg. 77:1422.
114. Rottmann, M.,, T. Lavstsen,, J. P. Mugasa,, M. Kaestli,, A. T. Jensen,, D. Muller,, T. Theander, and, H. P. Beck. 2006. Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children. Infect. Immun. 74:39043911.
115. Rowe,, A. K.,, S. Y. Rowe,, R. W. Snow,, E. L. Korenromp,, J. R. Schellenberg,, C. Stein,, B. L. Nahlen,, J. Bryce,, R. E. Black, and, R. W. Steketee. 2006. The burden of malaria mortality among African children in the year 2000. Int. J. Epidemiol. 35:691704.
116. Rowe, J. A.,, A. Claessens,, R. A. Corrigan, and, M. Arman. 2009a. Adhesion of Plasmodium falciparum- infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev. Mol. Med. 11:e16.
117. Rowe,, J. A.,, I. G. Handel,, M. A. Thera,, A. M. Deans,, K. E. Lyke,, A. Kone,, D. A. Diallo,, A. Raza,, O. Kai,, K. Marsh,, C. V. Plowe,, O. K. Doumbo, and, J. M. Moulds. 2007. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc. Natl. Acad. Sci. USA 104:1747117476.
118. Rowe,, J. A.,, J. M. Moulds,, C. I. Newbold, and, L. H. Miller. 1997. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388:292295.
119. Rowe, J. A.,, J. Obiero,, K. Marsh, and, A. Raza. 2002. Short report: positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am. J. Trop. Med. Hyg. 66:458460.
120. Rowe, J. A.,, D. H. Opi, and, T. N. Williams. 2009b. Blood groups and malaria: fresh insights into pathogenesis and identification of targets for intervention. Curr. Opin. Hematol. 16:480487.
121. Ru,, Y. X.,, B. Y. Mao,, F. K. Zhang,, T. X. Pang,, S. X. Zhao,, J. H. Liu, and, S. N. Wickramasinghe. 2009. Invasion of erythroblasts by Pasmodium vivax: a new mechanism contributing to malarial anemia. Ultrastruct. Pathol. 33:236242.
122. Ruwende, C.,, S. C. Khoo,, R. W. Snow,, S. N. Yates,, D. Kwiatkowski,, S. Gupta,, P. Warn,, C. E. Allsopp,, S. C. Gilbert,, N. Peschu,, C. I. Newbold,, B. M. Greenwood,, K. Marsh and, A. V. S. Hill. 1995. Natural selection of hemiand heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376:246249.
123. Safeukui,, I.,, J. M. Correas,, V. Brousse,, D. Hirt,, G. Deplaine,, S. Mule,, M. Lesurtel,, N. Goasguen,, A. Sauvanet,, A. Couvelard,, S. Kerneis,, H. Khun,, I. Vigan-Womas,, C. Ottone,, T. J. Molina,, J. M. Treluyer,, O. Mercereau-Puijalon,, G. Milon,, P. H. David, and, P. A. Buffet. 2008. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood 112:25202528.
124. Sanchez,, M. R.,, J. A. Ramirez,, J. Larriva-Sahd,, M. H. Rodriguez,, R. Mancilla, and, L. Ortiz-Ortiz. 1994. Antigenic characterization of Plasmodium vivax with monoclonal antibodies. Am. J. Trop. Med. Hyg. 51:6067.
125. Scherf, A.,, J. J. Lopez-Rubio, and, L. Riviere. 2008. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62:445470.
126. Simpson, J. A.,, K. Silamut,, K. Chotivanich,, S. Pukrittayakamee, and, N. J. White. 1999. Red cell selectivity in malaria: a study of multiple-infected erythrocytes. Trans. R. Soc. Trop. Med. Hyg. 93:165168.
127. Singh,, K.,, A. G. Gittis,, P. Nguyen,, D. C. Gowda,, L. H. Miller, and, D. N. Garboczi. 2008. Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A. Nat. Struct. Mol. Biol. 15:932938.
128. Smith,, J. D.,, C. E. Chitnis,, A. G. Craig,, D. J. Roberts,, D. E. Hudson-Taylor,, D. S. Peterson,, R. Pinches,, C. I. Newbold, and, L. H. Miller. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101110.
129. Snow,, R. W.,, C. A. Guerra,, A. M. Noor,, H. Y. Myint, and, S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214217.
130. Su,, X. Z.,, V. M. Heatwole,, S. P. Wertheimer,, F. Guinet,, J. A. Herrfeldt,, D. S. Peterson,, J. A. Ravetch, and, T. E. Wellems. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum- infected erythrocytes. Cell 82:89100.
131. Taylor,, T. E.,, W. J. Fu,, R. A. Carr,, R. O. Whitten,, J. S. Mueller,, N. G. Fosiko,, S. Lewallen,, N. G. Liomba, and, M. E. Molyneux. 2004. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat. Med. 10:143145.
132. Taylor, W. R., and, N. J. White. 2002. Malaria and the lung. Clin. Chest. Med. 23:457468.
133. Tjitra,, E.,, N. M. Anstey,, P. Sugiarto,, N. Warikar,, E. Kenangalem,, M. Karyana,, D. A. Lampah, and, R. N. Price. 2008. Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med. 5:e128.
134. Treutiger,, C. J.,, I. Hedlund,, H. Helmby,, J. Carlson,, A. Jepson,, P. Twumasi,, D. Kwiatkowski,, B. M. Greenwood, and, M. Wahlgren. 1992. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am. J. Trop. Med. Hyg. 46:503510.
135. Turner,, G. D.,, V. C. Ly,, T. H. Nguyen,, T. H. Tran,, H. P. Nguyen,, D. Bethell,, S. Wyllie,, K. Louwrier,, S. B. Fox,, K. C. Gatter,, N. P. Day,, N. J. White, and, A. R. Berendt. 1998. Systemic endothelial activation occurs in both mild and severe malaria. Correlating dermal microvascular endothelial cell phenotype and soluble cell adhesion molecules with disease severity. Am. J. Pathol. 152:14771487.
136. Turner,, G. D.,, H. Morrison,, M. Jones,, T. M. Davis,, S. Looareesuwan,, I. D. Buley,, K. C. Gatter,, C. I. Newbold,, S. Pukritayakamee, and, B. Nagachinta. 1994. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am. J. Pathol. 145:10571069.
137. Udomsangpetch, R.,, O. Kaneko,, K. Chotivanich, and, J. Sattabongkot. 2008. Cultivation of Plasmodium vivax. Trends Parasitol. 24:8588.
138. Udomsanpetch, R.,, K. Thanikkul,, S. Pukrittayakamee, and, N. J. White. 1995. Rosette formation by Plasmodium vivax. Trans. R. Soc. Trop. Med. Hyg. 89:635637.
139. Valecha,, N.,, R. G. Pinto,, G. D. Turner,, A. Kumar,, S. Rodrigues,, N. G. Dubhashi,, E. Rodrigues,, S. S. Banaulikar,, R. Singh,, A. P. Dash, and, J. K. Baird. 2009. Histopathology of fatal respiratory distress caused by Plasmodium vivax malaria. Am. J. Trop. Med. Hyg. 81:758762.
140. Van den Eede,, P.,, H. N. Van,, C. Van Overmeir,, I. Vythilingam,, T. N. Duc,, X. Hung le,, H. N. Manh,, J. Anne,, U. D’Alessandro, and, A. Erhart. 2009. Human Plasmodium knowlesi infections in young children in central Vietnam. Malar. J. 8:249.
141. Verhoef,, H.,, C. E. West,, R. Kraaijenhagen,, S. M. Nzyuko,, R. King,, M. M. Mbandi,, S. van Laatum,, R. Hogervorst,, C. Schep, and, F. J. Kok. 2002. Malarial anemia leads to adequately increased erythropoiesis in asymptomatic Kenyan children. Blood 100:34893494.
142. White,, V. A.,, S. Lewallen,, N. A. Beare,, M. E. Molyneux, and, T. E. Taylor. 2009. Retinal pathology of pediatric cerebral malaria in Malawi. PLoS ONE 4:e4317.
143. World Health Organization. 2000. Severe falciparum malaria. World Health Organization, Communicable Diseases Cluster. Trans R Soc Trop Med Hyg 94 Suppl 1:S190.
144. World Health Organization. 2008. World Malaria Report. World Health Organization Press, Geneva, Switzerland.
145. Williams, T. N. 2006. Human red blood cell polymorphisms and malaria. Curr. Opin. Microbiol. 9:388394.
146. Williams,, T. N.,, T. W. Mwangi,, D. J. Roberts,, N. D. Alexander,, D. J. Weatherall,, S. Wambua,, M. Kortok,, R. W. Snow, and, K. Marsh. 2005a. An immune basis for malaria protection by the sickle cell trait. PLoS Med. 2:e128.
147. Williams,, T. N.,, T. W. Mwangi,, S. Wambua,, N. D. Alexander,, M. Kortok,, R. W. Snow, and, K. Marsh. 2005b. Sickle cell trait and the risk of malaria and other childhood diseases. J. Infect. Dis. 192:178186.
148. Williams,, T. N.,, S. Wambua,, S. Uyoga,, A. Macharia,, J. K. Mwacharo,, C. R. Newton, and, K. Maitland. 2005c. Both heterozygous and homozygous alpha+ thalassemias protect against severe and fatal Plasmodium falciparum malaria on the coast of Kenya. Blood 106:368371.
149. Yeo,, T. W.,, D. A. Lampah,, R. Gitawati,, E. Tjitra,, E. Kenangalem,, Y. R. McNeil,, C. J. Darcy,, D. L. Granger,, J. B. Weinberg,, B. K. Lopansri,, R. N. Price,, S. B. Duffull,, D. S. Celermajer, and, N. M. Anstey. 2007. Impaired nitric oxide bioavailability and L-arginine reversible endothelial dysfunction in adults with falciparum malaria. J. Exp. Med. 204:26932704.
150. Yeo,, T. W.,, D. A. Lampah,, E. Tjitra,, R. Gitawati,, E. Kenangalem,, K. Piera,, D. L. Granger,, B. K. Lopansri,, J. B. Weinberg,, R. N. Price,, S. B. Duffull,, D. S. Celermajer, and, N. M. Anstey. 2009. Relationship of cell-free hemoglobin to impaired endothelial nitric oxide bioavailability and perfusion in severe falciparum malaria. J. Infect. Dis. 200:15221529.


Generic image for table

Criteria for the diagnosis of severe malaria

Citation: Amaratunga C, Lopera-Mesa T, Tse J, Mita-Mendoza N, Fairhurst R. 2011. Pathology and Pathogenesis of Malaria, p 261-381. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch29

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error