The pathogenesis of Plasmodium falciparum malaria in humans: Insights from splenic physiology

Blood

Volumn 117, Issue 2, 2011, Pages 381-392

  Buffet, Pierre A ^a,b,c   Safeukui, Innocent ^c,d   Deplaine, Guillaume ^a,c   Brousse, Valentine ^c,e   Prendki, Virginie ^a,f   Thellier, Marc ^a,b   Turner, Gareth D ^g   Mercereau Puijalon, Odile ^c,d  

^a SORBONNE UNIVERSITÉ   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f HÔPITAL JEAN VERDIER   (France)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; ARTESUNATE; MEFLOQUINE; QUININE; TETRACYCLINE;

ANEMIA; BRAIN MALARIA; CELL ADHESION; CLINICAL FEATURE; DISEASE COURSE; DISEASE EXACERBATION; ERYTHROCYTE; HUMAN; INNATE IMMUNITY; MALARIA FALCIPARUM; MICROCIRCULATION; NONHUMAN; PARASITE CLEARANCE; PARASITE LOAD; PARASITE TRANSMISSION; PARASITEMIA; PATHOGENESIS; PLASMODIUM; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SPLENECTOMY; SPLENOMEGALY;

EID: 78751531268     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-04-202911     Document Type: Review

References (100)

1. Greenwood BM, Fidock DA, Kyle DE, et al. Malaria: progress, perils, and prospects for eradication. J Clin Invest. 2008;118(4):1266-1276. (Pubitemid 351500419)
2. Maier AG, Cooke BM, Cowman AF, Tilley L. Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol. 2009;7(5):341-354.
3. Layez C, Nogueira P, Combes V, et al. Plasmodium falciparum rhoptry protein RSP2 triggers destruction of the erythroid lineage. Blood. 2005;106(10):3632-3638.
4. Groom AC, Schmidt EE, MacDonald IC. Microcirculatory pathways and blood flow in spleen: new insights from washout kinetics, corrosion casts, and quantitative intravital videomicroscopy. Scanning Microsc. 1991;5(1):159-173; discussion, 173-174.
5. Buffet PA, Milon G, Brousse V, et al. Ex vivo perfusion of human spleens maintains clearing and processing functions. Blood. 2006;107(9):3745-3752.
6. Safeukui I, Correas JM, Brousse V, et al. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood. 2008;112(6):2520-2528.
7. Mohandas N, Gallagher PG. Red cell membrane: past, present, and future. Blood. 2008;112(10):3939-3948.
8. Looareesuwan S, Ho M, Wattanagoon Y, et al. Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med. 1987;317(11):675-679. (Pubitemid 17138193)
9. Turrini F, Ginsburg H, Bussolino F, Pescarmona GP, Serra MV, Arese P. Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: involvement of immune and nonimmune determinants and dependence on parasite developmental stage. Blood. 1992;80(3):801-808.
10. Lutz HU. Innate immune and non-immune mediators of erythrocyte clearance. Cell Mol Biol (Noisy-le-grand). 2004;50(2):107-116.
11. Steiniger B, Timphus EM, Barth PJ. The splenic marginal zone in humans and rodents: an enigmatic compartment and its inhabitants. Histochem Cell Biol. 2006;126(6):641-648. (Pubitemid 44899708)
12. Grau GE, Mackenzie CD, Carr RA, et al. Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis. 2003;187(3):461-466.
13. Marsh K, Forster D, Waruiru C, et al. Indicators of life-threatening malaria in African children. N Engl J Med. 1995;332(21):1399-1404.
14. Su X-Z, Heatwole VM, Wertheimer SP, et al. The large diverse family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell. 1995;82(1):89-100.
15. Smith JD, Chitnis CE, Craig AG, et al. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes [see comments]. Cell. 1995;82(1):101-110.
16. Baruch DI, Pasloske BL, Singh HB, et al. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes [see comments]. Cell. 1995;82(1):77-87.
17. Turner GD, Morrison H, Jones M, et al. 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. 1994;145(5):1057-1069.
18. Cranston HA, Boylan CW, Carroll GL, et al. Plasmodium falciparum maturation abolishes physiologic red cell deformability. Science. 1984;223(4634):400-403. (Pubitemid 14218329)
19. Suwanarusk R, Cooke BM, Dondorp AM, et al. The deformability of red blood cells parasitized by Plasmodium falciparum and P. vivax. J Infect Dis. 2004;189(2):190-194. (Pubitemid 38147241)
20. Simpson JA, Aarons L, Collins WE, Jeffery GM, White NJ. Population dynamics of untreated Plasmodium falciparum malaria within the adult human host during the expansion phase of the infection. Parasitology. 2002;124(Pt 3):247-263. (Pubitemid 34250739)
21. 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(3):385-401.
22. Maude RJ, Dondorp AM, Abu Sayeed A, Day NP, White NJ, Beare NA. The eye in cerebral malaria: what can it teach us? Trans R Soc Trop Med Hyg. 2009;103(7):661-664.
23. Dondorp AM, Desakorn V, Pongtavornpinyo W, et al. Estimation of the total parasite biomass in acute falciparum malaria from plasma PfHRP2. PLoS Med. 2005;2(8):e204.
24. Pongponratn E, Riganti M, Harinasuta T, Bunnag D. Electron microscopy of the human brain in cerebral malaria. Southeast Asian J Trop Med Pub Health. 1985;16(2):219-227.
25. 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(2):168-175.
26. White NJ, Chapman D, Watt G. The effects of multiplication and synchronicity on the vascular distribution of parasites in falciparum malaria. Trans R Soc Trop Med Hyg. 1992;86(6):590-597. (Pubitemid 23012896)
27. Bull PC, Marsh K. The role of antibodies to Plasmodium falciparum-infected erythrocyte surface antigens in naturally acquired immunity to malaria. Trends Microbiol. 2002;10(2):55-58. (Pubitemid 34119334)
28. Snow RW, Bastos de Azevedo I, Lowe BS, et al. Severe childhood malaria in two areas of markedly different falciparum transmission in east Africa. Acta Trop. 1994;57(4):289-300.
29. Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ. Malarial anemia: of mice and men. Blood. 2007; 110(1):18-28.
30. Price RN, Simpson JA, Nosten F, et al. Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg. 2001;65(5):614-622. (Pubitemid 33134602)
31. Nash GB, O'Brien E, Gordon-Smith EC, Dormandy JA. Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum. Blood. 1989;74(2):855-861. (Pubitemid 19208835)
32. Li J, Dao M, Lim CT, Suresh S. Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J. 2005;88(5):3707-3719. (Pubitemid 40586618)
33. Mills JP, Diez-Silva M, Quinn DJ, et al. Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Proc Natl Acad Sci U S A. 2007;104(22):9213-9217.
34. Buffet PA, Safeukui I, Milon G, Mercereau-Puijalon O, David PH. Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr Opin Hematol. 2009;16(3):157-164.
35. Dondorp AM, Kager PA, Vreeken J, White NJ. Abnormal blood flow and red blood cell deformability in severe malaria [in process citation]. Parasitol Today. 2000;16(6):228-232. (Pubitemid 30332124)
36. Pouvelle B, Buffet PA, Lepolard C, Scherf A, Gysin J. Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nat Med. 2000;6(11):1264-1268.
37. Awah NW, Troye-Blomberg M, Berzins K, Gysin J. Mechanisms of malarial anaemia: potential involvement of the Plasmodium falciparum low molecular weight rhoptry-associated proteins. Acta Trop. 2009;112(3):295-302.
38. Israeli A, Shapiro M, Ephros MA. Plasmodium falciparum malaria in an asplenic man. Trans R Soc Trop Med Hyg. 1987;81(2):233-234.
39. Bachmann A, Esser C, Petter M, et al. Absence of erythrocyte sequestration and lack of multicopy gene family expression in Plasmodium falciparum from a splenectomized malaria patient. PLoS One. 2009;4(10):e7459.
40. Snow RW, Omumbo JA, Lowe B, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa [see comments]. Lancet. 1997;349(9066):1650-1654.
41. Giha HA, Elghazali G, A-Elgadir TM, A-Elbasit IE, Elbashir MI. Severe malaria in an unstable setting: clinical and laboratory correlates of cerebral malaria and severe malarial anemia and a paradigm for a simplified severity scoring. Eur J Clin Microbiol Infect Dis. 2009;28(6):661-665.
42. Urban BC, Ferguson DJ, Pain A, et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells [see comments]. Nature. 1999;400(6739):73-77.
43. Imbert P, Buffet P, Ficko C, Rapp C. Left upper quadrant abdominal pain in malaria: suspect pathological splenic rupture first. Trans R Soc Trop Med Hyg. 2010;104(10):628-629.
44. Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ. The pathology of human cerebral malaria. Am J Trop Med Hyg. 1990;43(2 Pt 2):30-37.
45. Prommano O, Chaisri U, Turner GD, et al. A quantitative ultrastructural study of the liver and the spleen in fatal falciparum malaria. Southeast Asian J Trop Med Pub Health. 2005;36(6):1359-1370.
46. Pongponratn E, Riganti M, Bunnag D, Harinasuta T. Spleen in falciparum malaria: ultrastructural study. Southeast Asian J Trop Med Pub Health. 1987;18(4):491-501.
47. Oo MM, Aikawa M, Than T, et al. Human cerebral malaria: a pathological study. J Neuropathol Exp Neurol. 1987;46(2):223-231.
48. Lee SH, Looareesuwan S, Wattanagoon Y, et al. Antibody-dependent red cell removal during P. falciparum malaria: the clearance of red cells sensitized with an IgG anti-D. Br J Haematol. 1989;73(3):396-402.
49. Looareesuwan S, Davis TM, Pukrittayakamee S, et al. Erythrocyte survival in severe falciparum malaria. Acta Trop. 1991;48(4):263-270.
50. Looareesuwan S, Merry AH, Phillips RE, et al. Reduced erythrocyte survival following clearance of malarial parasitaemia in Thai patients. Br J Haematol. 1987;67(4):473-478. (Pubitemid 18032047)
51. Munasinghe A, Ileperuma M, Premawansa G, Handunnetti S, Premawansa S. Spleen modulation of cytoadherence properties of Plasmodium falciparum. Scand J Infect Dis. 2009;41(6-7):538-539.
52. Petithory JC, Khelil A, Galeazzi G, Ardoin F. [Malaria in splenectomized patients. Three fatal cases]. Presse Med. 2005;34(7):519-521.
53. Demar M, Legrand E, Hommel D, Esterre P, Carme B. Plasmodium falciparum malaria in splenectomized patients: two case reports in French Guiana and a literature review. Am J Trop Med Hyg. 2004;71(3):290-293. (Pubitemid 39223504)
54. Pongponratn E, Viriyavejakul P, Wilairatana P, et al. Absence of knobs on parasitized red blood cells in a splenectomized patient in fatal falciparum malaria. Southeast Asian J Trop Med Pub Health. 2000;31(4):829-835.
55. Looareesuwan S, Suntharasamai P, Webster HK, Ho M. Malaria in splenectomized patients: report of four cases and review. Clin Infect Dis. 1993;16(3):361-366. (Pubitemid 23066942)
56. Grobusch MP, Borrmann S, Omva J, Issifou S, Kremsner PG. Severe malaria in a splenectomised Gabonese woman. Wien Klin Wochenschr. 2003;115(1-2):63-65. (Pubitemid 36285781)
57. Maharaj D, McDonald GA, Dobbie JW. Splenectomy and blackwater fever. Br J Haematol. 1982;51(4):663-664.
58. Chotivanich K, Udomsangpetch R, McGready R, et al. Central role of the spleen in malaria parasite clearance. J Infect Dis. 2002;185(10):1538-1541. (Pubitemid 34507982)
59. Le TA, Davis TM, Tran QB, Nguyen VP, Trinh KA. Delayed parasite clearance in a splenectomized patient with falciparum malaria who was treated with artemisinin derivatives. Clin Infect Dis. 1997;25(4):923-925.
60. Guerin B, Bouchaud O, Gachot B, Lebras J, Saimot AG. [Persistent parasitemia after treatment of Plasmodium falciparum flare-up in a nonimmune patient with splenectomy]. Ann Med Interne (Paris). 1996;147(2):129-130.
61. Ho M, Bannister LH, Looareesuwan S, Suntharasamai P. Cytoadherence and ultrastructure of Plasmodium falciparum-infected erythrocytes from a splenectomized patient. Infect Immun. 1992;60(6):2225-2228.
62. Bidegain F, Berry A, Alvarez M, et al. Acute Plasmodium falciparum malaria following splenectomy for suspected lymphoma in 2 patients. Clin Infect Dis. 2005;40(11):e97-e100.
63. Bach O, Baier M, Pullwitt A, et al. Falciparum malaria after splenectomy: a prospective controlled study of 33 previously splenectomized Malawian adults. Trans R Soc Trop Med Hyg. 2005;99(11):861-867.
64. Boone KE, Watters DA. The incidence of malaria after splenectomy in Papua New Guinea. BMJ. 1995;311(7015):1273.
65. Saint-Yves IFM. Splenectomy: follow-up of patients in the Solomon Islands. PNG Med. 1977;20:33-37.
66. Ayi K, Turrini F, Piga A, Arese P. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood. 2004;104(10):3364-3371.
67. Oeuvray C, Bouharoun-Tayoun H, Gras-Masse H, et al. Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood. 1994;84(5):1594-1602.
68. Bates I, Bedu-Addo G. Review of diagnostic criteria of hyper-reactive malarial splenomegaly. Lancet. 1997;349(9059):1178.
69. White NJ, Krishna S. Treatment of malaria: some considerations and limitations of the current methods of assessment. Trans R Soc Trop Med Hyg. 1989;83(6):767-777.
70. Newton PN, Chotivanich K, Chierakul W, et al. A comparison of the in vivo kinetics of Plasmodium falciparum ring-infected erythrocyte surface antigen-positive and -negative erythrocytes. Blood. 2001;98(2):450-457.
71. Anderson TJ, Nair S, Nkhoma S, et al. High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis. 2010;201(9):1326-1330.
72. Dondorp AM, Nosten F, Yi P, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361(5):455-467.
73. Greenwood B. Review: intermittent preventive treatment - a new approach to the prevention of malaria in children in areas with seasonal malaria transmission. Trop Med Int Health. 2006;11(7):983-991.
74. Wickramasinghe SN, Abdalla SH. Blood and bone marrow changes in malaria. Baillieres Best Pract Res Clin Haematol. 2000;13(2):277-299.
75. Seed TM, Kreier JP, eds. Erythrocyte Destruction Mechanisms in Malaria. New York, NY: Academic Press; 1980.
76. Lackritz EM, Campbell CC, Ruebush TK 2nd, et al. Effect of blood transfusion on survival among children in a Kenyan hospital. Lancet. 1992;340(8818):524-528.
77. Sowunmi A, Gbotosho GO, Happi CT, Fateye BA. Factors contributing to anaemia after uncomplicated Plasmodium falciparum malaria in children. Acta Trop. 2009;113(2):155-161.
78. Reyburn H, Mbatia R, Drakeley C, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA. 2005;293(12):1461-1470.
79. Baird JK. Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Ann Trop Med Parasitol. 1998;92(4):367-390. (Pubitemid 28312554)
80. Legros F, Bouchaud O, Ancelle T, et al. Risk factors for imported fatal Plasmodium falciparum malaria, France, 1996-2003. Emerg Infect Dis. 2007;13(6):883-888.
81. Dondorp AM, Lee SJ, Faiz MA, et al. The relationship between age and the manifestations of and mortality associated with severe malaria. Clin Infect Dis. 2008;47(2):151-157.
82. Bastien P. Epidemiologic peculiarities of severe attacks due to Plasmodium falciparum in a malaria epidemic context. Vanuatu, 1975-1985 [in French]. Médecine Tropicale. 1987;47(2):125-131.
83. Dondorp A, Nyanoti M, Kager PA, Mithwani S, Vreeken J, Marsh K. 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. 2002;96(3):282-286. (Pubitemid 34785066)
84. Zintl A, Gray JS, Skerrett HE, Mulcahy G. Possible mechanisms underlying age-related resistance to bovine babesiosis. Parasite Immunol. 2005;27(4):115-120. (Pubitemid 40806800)
85. Modiano D, Luoni G, Sirima BS, et al. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001;414(6861):305-308.
86. Weatherall DJ. Genetic variation and susceptibility to infection: the red cell and malaria. Br J Haematol. 2008;141(3):276-286.
87. Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg. 1989;83(3):293-303. (Pubitemid 19163208)
88. Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJ. The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. J Infect Dis. 2005;191(10):1631-1638. (Pubitemid 40656750)
89. Aidoo M, Terlouw DJ, Kolczak MS, et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002;359(9314):1311- 1312.
90. Kreuels B, Kreuzberg C, Kobbe R, et al. Differing effects of HbS and HbC traits on falciparum malaria, anemia and child growth. Blood. 2010;115(22):4551-4558.
91. Cholera R, Brittain NJ, Gillrie MR, et al. Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci U S A. 2008;105(3):991-996.
92. Luzzatto L, Nwachuku-Jarrett ES, Reddy S. Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet. 1970;1(7642):319-321.
93. Roth EF, Jr., Friedman M, Ueda Y, Tellez I, Trager W, Nagel RL. Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science. 1978;202(4368):650-652. (Pubitemid 9055627)
94. Makani J, Komba AN, Cox SE, et al. Malaria in patients with sickle cell anemia: burden, risk factors, and outcome at the outpatient clinic and during hospitalization. Blood. 2010;115(2):215-220.
95. Komba AN, Makani J, Sadarangani M, et al. Malaria as a cause of morbidity and mortality in children with homozygous sickle cell disease on the coast of Kenya. Clin Infect Dis. 2009;49(2):216-222.
96. Sadarangani M, Makani J, Komba AN, et al. An observational study of children with sickle cell disease in Kilifi, Kenya. Br J Haematol. 2009; 146(6):675-682.
97. Waitumbi JN, Donvito B, Kisserli A, Cohen JH, Stoute JA. Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J Infect Dis. 2004;190(6):1183-1191. (Pubitemid 39186807)
98. Stevenson MM, Riley EM. Innate immunity to malaria. Nat Rev Immunol. 2004;4(3):169-180.
99. Sutera SP, Gardner RA, Boylan CW, et al. Age-related changes in deformability of human erythrocytes. Blood. 1985;65(2):275-282.
100. Dondorp AM, Chotivanich KT, Fucharoen S, et al. Red cell deformability, splenic function, and anaemia in thalassaemia. Br J Haematol. 1999;105(2):505-508.