Breadth of anti-merozoite antibody responses is associated with the genetic diversity of asymptomatic plasmodium falciparum infections and protection against clinical malaria

Clinical Infectious Diseases

Volumn 57, Issue 10, 2013, Pages 1409-1416

  Rono, Josea ^a,b   Osier, Faith H A ^b   Olsson, Daniel ^a   Montgomery, Scott ^a,c   Mhoja, Leah ^d   Rooth, Ingegerd ^d   Marsh, Kevin ^b,e   Färnert, Anna ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^c ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^d Nyamisati Malaria Research Unit   (Tanzania)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Antibodies; Immunity; Malaria; Merozoite surface antigens; Multiclonal infections

Indexed keywords

MALARIA VACCINE; MEMBRANE ANTIGEN; MEROZOITE ANTIGEN; MEROZOITE SURFACE PROTEIN 2; UNCLASSIFIED DRUG;

ADOLESCENT; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CAPILLARY ELECTROPHORESIS; CHILD; COHORT ANALYSIS; CROSS-SECTIONAL STUDY; FOLLOW UP; GENETIC VARIABILITY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; TANZANIA;

ANTIBODIES; IMMUNITY; MALARIA; MEROZOITE SURFACE ANTIGENS; MULTICLONAL INFECTIONS;

ADOLESCENT; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ASYMPTOMATIC INFECTIONS; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; GENOTYPE; HUMANS; INFANT; MALARIA, FALCIPARUM; MEROZOITES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RISK; TANZANIA;

EID: 84887908446     PISSN: 10584838     EISSN: 15376591     Source Type: Journal    
DOI: 10.1093/cid/cit556     Document Type: Article

References (40)

1. Felger I, Irion A, Steiger S., Beck HP Genotypes of merozoite surface protein 2 of Plasmodium falciparum in Tanzania. Trans R Soc Trop Med Hyg 1999; 93(SUPPL. 1): 3-9.
2. Ntoumi F, Contamin H, Rogier C., Bonnefoy S, Trape JF, Mercereau-Puijalon O. Age-dependent carriage of multiple Plasmodium falciparum merozoite surface antigen-2 alleles in asymptomatic malaria infections. Am J Trop Med Hyg 1995; 52: 81-8.
3. Smith T, Felger I, Tanner M., Beck HP Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg 1999; 93(SUPPL. 1): 59-64.
4. Farnert A, Williams TN, Mwangi T.W., et al Transmission-dependent tolerance to multiclonal Plasmodium falciparum infection. J Infect Dis 2009; 200: 1166-75.
5. Smith T, Beck HP, Kitua A, et al Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg 1999; 93 (suppl 1): 15-20.
6. al-Yaman F., Genton B, Reeder J.C., Anders RF, Smith T, Alpers MP Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans R Soc Trop Med Hyg 1997; 91: 602-5.
7. Bereczky S, Liljander A, Rooth I., et al Multiclonal asymptomatic Plasmodium falciparum infections predict a reduced risk of malaria disease in a Tanzanian population. Microbes Infect 2007; 9: 103-10.
8. Farnert A, Rooth I, Svensson, Snounou G, Bjorkman A. Complexity of Plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. J Infect Dis 1999; 179: 989-95.
9. Cohen S, McGI, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature 1961; 192: 733-7.
10. al-Yaman F., Genton B, Anders R.F., et al Relationship between humoral response to Plasmodium falciparum merozoite surface antigen-2 and malaria morbidity in a highly endemic area of Papua New Guinea. Am J Trop Med Hyg 1994; 51: 593-602.
11. Osier FH, Fegan G, Polley S.D., et al Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun 2008; 76: 2240-8.
12. Osier FH, Polley SD, Mwangi T, Lowe B., Conway DJ, Marsh K. Naturally acquired antibodies to polymorphic and conserved epitopes of Plasmodium falciparum merozoite surface protein 3. Parasite Immunol 2007; 29: 387-94.
13. Polley SD, Conway DJ, Cavanagh D.R., et al High levels of serum antibodies to merozoite surface protein 2 of Plasmodium falciparum are associated with reduced risk of clinical malaria in coastal Kenya. Vaccine 2006; 24: 4233-46.
14. Polley SD, Mwangi T, Kocken C.H., et al Human antibodies to recombinant protein constructs of Plasmodium falciparum apical membrane antigen 1 (AMA1) and their associations with protection from malaria. Vaccine 2004; 23: 718-28.
15. Stanisic DI, Richards JS, McCallum F.J., et al Immunoglobulin G sub-class-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun 2009; 77: 1165-74.
16. Richards JS, Stanisic DI, Fowkes F.J., et al Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis 2010; 51: e50-60.
17. Liljander A, Wiklund L, Falk N., et al Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2). Malar J 2009; 8: 78.
18. Rooth I. Malaria morbidity and control in a Tanzanian village. Stockholm: Karolinska Institutet, 1992.
19. Rogier C, Commenges D, Trape JF Evidence for an age-dependent pyrogenic threshold of Plasmodium falciparum parasitemia in highly endemic populations. Am J Trop Med Hyg 1996; 54: 613-9.
20. Snounou G, Beck HP The use of PCR genotyping in the assessment of recrudescence or reinfection after antimalarial drug treatment. Parasitol Today 1998; 14: 462-7.
21. Ranford-Cartwright L.C., Balfe P, Carter R., Walliker D. Frequency of cross-fertilization in the human malaria parasite Plasmodium falciparum. Parasitology 1993; 107(Pt 1): 11-8.
22. Burghaus PA, Holder AA Expression of the 19-kilodalton carboxyterminal fragment of the Plasmodium falciparum merozoite surface protein-1 in Escherichia coli as a correctly folded protein. Mol Biochem Parasitol 1994; 64: 165-9.
23. Taylor RR, Smith DB, Robinson V.J., McBride JS, Riley EM Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the immunoglobulin G3 subclass. Infect Immun 1995; 63: 4382-8.
24. Polley SD, Tetteh KK, Lloyd J.M., et al Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis 2007; 195: 279-87.
25. Taylor TE, Molyneux ME, Wirima J.J., Borgstein A., Goldring JD, Hommel M. Intravenous immunoglobulin in the treatment of paediatric cerebral malaria. Clin Exp Immunol 1992; 90: 357-62.
26. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol 2004; 159: 702-6.
27. Murungi LM, Kamuyu G, Lowe B., et al A threshold concentration of anti-merozoite antibodies is required for protection from clinical episodes of malaria. Vaccine 2013; 31: 3936-42.
28. Lehnert-Batar A. pARtial: pARtial Package. R package version 0.1, 2006.
29. Benichou J. A review of adjusted estimators of attributable risk. Stat Methods Med Res 2001; 10: 195-216.
30. Branch OH, Takala S, Kariuki S., et al Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun 2001; 69: 7783-92.
31. Felger I, Smith T, Edoh D., et al Multiple Plasmodium falciparum infections in Tanzanian infants. Trans R Soc Trop Med Hyg 1999; 93(SUPPL. 1): 29-34.
32. Mayor A, Saute F, Aponte J.J., et al Plasmodium falciparum multiple infections in Mozambique, its relation to other malariological indices and to prospective risk of malaria morbidity. Trop Med Int Health 2003; 8: 3-11.
33. Mueller I, Schoepflin S, Smith T.A., et al Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A 2012; 109: 10030-5.
34. Kinyanjui SM, Conway DJ, Lanar D.E., Marsh K. IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar J 2007; 6: 82.
35. Sergent E, Parrot L. L'immunite, la premunition et la resistance innee. Archives de L'Institut Pasteur d'Algirie. 1935; 13: 279-319.
36. Greenhouse B, Ho B, Hubbard A., et al Antibodies to Plasmodium falciparum antigens predict a higher risk of malaria but protection from symptoms once parasitemic. J Infect Dis 2011; 204: 19-26.
37. Liljander A, Chandramohan D, Kweku M., et al Influences of intermittent preventive treatment and persistent multiclonal Plasmodium falciparum infections on clinical malaria risk. PLoS One 2010; 5: e13649.
38. Ekala MT, Jouin H, Lekoulou F., Mercereau-Puijalon O, Ntoumi F. Allelic family-specific humoral responses to merozoite surface protein 2 (MSP2) in Gabonese residents with Plasmodium falciparum infections. Clin Exp Immunol 2002; 129: 326-31.
39. Felger I, Steiger S, Hatz C., Smith T, Beck HP Antigenic cross-reactivity between different alleles of the Plasmodium falciparum merozoite surface protein 2. Parasite Immunol 2003; 25: 531-43.
40. Mackinnon MJ, Mwangi TW, Snow R.W., Marsh K., Williams TN Heritability of malaria in Africa. PLoS Med 2005; 2: e340.