Effect of malaria transmission reduction by insecticide-treated bed nets (ITNs) on the genetic diversity of Plasmodium falciparum merozoite surface protein (MSP-1) and circumsporozoite (CSP) in western Kenya

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Kariuki, Simon K ^a   Njunge, James ^b   Muia, Ann ^b   Muluvi, Geofrey ^b   Gatei, Wangeci ^c,d   Ter Kuile, Feiko ^e   Terlouw, Dianne J ^e   Hawley, William A ^d   Phillips Howard, Penelope A ^e   Nahlen, Bernard L ^f   Lindblade, Kim A ^d   Hamel, Mary J ^d   Slutsker, Laurence ^d   Shi, Ya Ping ^d  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b KENYATTA UNIVERSITY   (Kenya)

^c ATLANTA RESEARCH AND EDUCATION FOUNDATION   (United States)

^d CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^f President's Malaria Initiative   (United States)

Author keywords

Bed nets; CSP; Malaria; MSP 1; Parasite diversity; Transmission

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; EPITOPE; MEROZOITE SURFACE PROTEIN 1; NUCLEOTIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BED NET; CHILD; CONTROLLED STUDY; GENE FREQUENCY; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN CELL; KENYA; MALARIA; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD;

ANTIGENS, PROTOZOAN; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; DNA, PROTOZOAN; GENE FREQUENCY; GENETIC VARIATION; HUMANS; INFANT; INFANT, NEWBORN; INSECTICIDE-TREATED BEDNETS; KENYA; MALARIA, FALCIPARUM; MEROZOITE SURFACE PROTEIN 1; MOSQUITO CONTROL; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84883078233     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-295     Document Type: Article

References (56)

1. WHO, World malaria report 2010 Geneva: World Health Organization http://wwwwhoint/malaria/world-malaria-report-2010/en/indexhtml
2. Insecticide-treated bed nets and curtains for preventing malaria. Lengeler C, Cochrane Database Syst Rev 2004 2 363
3. Impact of permethrin-treated bednets on malaria transmission by the Anopheles gambiae complex in The Gambia. Lindsay S, Snow RW, Broomfield GL, Janneh MS, Wirtz RA, Greenwood BM, Med Vet Entomol 1989 3 263 271 10.1111/j.1365-2915.1989.tb00226.x 2519671
4. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, Ter Kuile FO, Nahlen BL, Hightower AW, Hawley W, Am J Trop Med Hyg 2003 68 Suppl 4 16 22 12749481 (Pubitemid 38240677)
5. Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. Ter Kuile FO, Terlouw DJ, Kariuki SK, Phillips-Howard PA, Mirel LBHW, Friedman JF, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, Am J Trop Med Hyg 2003 68 Suppl 4 68 77 12749488 (Pubitemid 38240684)
6. The influence of the genetic complexity of Plasmodium falciparum infections on the epidemiology of malaria. Arnot DE, Trans R Soc Trop Med Hyg 2002 96 Suppl 1 131 136 12055826
7. Host-parasite interaction and morbidity in malaria endemic areas. Marsh K, Snow RW, Philos Trans R Soc Lond B Biol Sci 1997 352 1385 1394 10.1098/rstb.1997.0124 9355131 (Pubitemid 27434104)
8. Mortality in a seven-and-a-half-year follow-up of a trial of insecticide-treated mosquito nets in Ghana. Binka FN, Hodgson A, Adjuik M, Smith T, Trans R Soc Trop Med Hyg 2002 96 597 599 10.1016/S0035-9203(02)90321-4 12625130 (Pubitemid 36231476)
9. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, Ter Kuile FO, Hawley WA, Wannemuehler KA, Phillips-Howard PA, Rosen DH, Nahlen BL, Terlouw DJ, Adazu K, Vulule JM, Slutsker L, JAMA 2004 291 2571 2580 10.1001/jama.291.21.2571 15173148 (Pubitemid 38702775)
10. Sporozoite antibodies and malaria in children in a rural area of The Gambia. Snow RW, Shenton FC, Lindsay SW, Greenwood BM, Bennett S, Wheeler J, Del Giudice G, Verdini AS, Pessi A, Ann Trop Med Parasitol 1989 83 559 568 2694982 (Pubitemid 20055727)
11. The use of untreated bednets and malaria infection, morbidity and immunity. Genton B, Hii J, al-Yaman F, Paru R, Beck HP, Ginny M, Dagoro H, Lewis D, Alpers MP, Ann Trop Med Parasitol 1994 88 263 270 7944671 (Pubitemid 24231918)
12. Infant parasite rates and immunoglobulin M seroprevalence as a measure of exposure to Plasmodium falciparum during a randomized controlled trial of insecticide-treated bed nets on the Kenyan coast. Snow RW, Molyneux CS, Warn PA, Omumbo J, Nevill CG, Gupta S, Marsh K, Am J Trop Med Hyg 1996 55 144 149 8940968 (Pubitemid 26299197)
13. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. Askjaer N, Maxwell C, Chambo W, Staalsoe T, Nielsen M, Hviid L, Curtis C, Theander TG, Clin Diagn Lab Immunol 2001 8 1289 1291 11687480 (Pubitemid 33035771)
14. Effects of permethrin-treated bed nets on immunity to malaria in western Kenya II. Kariuki SK, Lal AA, Terlouw DJ, Ter Kuile FO, Ong'echa JM, Phillips-Howard PA, Orago AS, Kolczak MS, Hawley WA, Nahlen BL, Shi YP, Antibody responses in young children in an area of intense malaria transmission. Am J Trop Med Hyg 2003 68 Suppl 4 108 114
15. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP, Mol Biol Evol 2000 17 1467 1482 10.1093/oxfordjournals.molbev.a026247 11018154
16. Mating patterns in malaria parasite populations of Papua New Guinea. Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP, Science 1995 269 1709 1711 10.1126/science.7569897 7569897 (Pubitemid 26449518)
17. Random mating in a natural population of the malaria parasite Plasmodium falciparum. Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D, Parasitology 1994 109 413 421 10.1017/S0031182000080665 7800409 (Pubitemid 24327391)
18. Effects of transmission reduction by insecticide-treated bed nets (ITNs) on parasite genetics population structure: I. Gatei W, Kariuki S, Hawley W, Ter Kuile F, Terlouw D, Phillips-Howard P, Nahlen B, Gimnig J, Lindblade K, Walker E, Hamel M, Crawford S, Williamson J, Slutsker L, Shi YP, The genetic diversity of Plasmodium falciparum parasites by microsatellite markers in western Kenya. Malar J 2010 9 353
19. Merozoite surface antigen-I of Plasmodium. Cooper JA, Parasitol Today 1993 9 5 54
20. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA, J Exp Med 1990 172 379 382 10.1084/jem.172.1.379 1694225 (Pubitemid 20217284)
21. Predicted and observed alleles of Plasmodium falciparum merozoite surface protein-1 (MSP-1), a potential malaria vaccine antigen. Qari SH, Shi YP, Goldman IF, Nahlen BL, Tibayrenc M, Lal AA, Mol Biochem Parasitol 1998 92 241 252 10.1016/S0166-6851(98)00010-3 9657329 (Pubitemid 28248098)
22. High frequency of recombination-driven allelic diversity and temporal variation of Plasmodium falciparum msp1 in Tanzania. Tanabe K, Sakihama N, Rooth I, Björkman A, Färnert A, Am J Trop Med Hyg 2007 76 1037 1045 17556608 (Pubitemid 351837863)
23. Towards a blood-stage vaccine for malaria: are we following all the leads? Good MF, Nat Rev Immunol 2001 1 117 125 10.1038/35100540 11905819 (Pubitemid 33741965)
24. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M, Science 1980 207 71 73 10.1126/science.6985745 6985745 (Pubitemid 10142301)
25. DNA cloning of Plasmodium falciparum circumsporozoite gene: amino acid sequence of repetitive epitope. Enea V, Ellis J, Zavala F, Arnot DE, Asavanich A, Masuda A, Quakyi I, Nussenzweig RS, Science 1984 225 628 630 10.1126/science.6204384 6204384 (Pubitemid 14053765)
26. T cells, T sites, and malaria immunity-further optimism for vaccine development. Good MF, J Immunol 1988 140 1715 1716 3279122
27. SCTP: First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. The RTS, N Engl J Med 2011 365 1863 1875 22007715
28. SCTP: A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. The RTS, N Engl J Med 2012 367 2284 2295 23136909
29. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SK, Am J Trop Med Hyg 1994 50 529 536 7911282 (Pubitemid 24196338)
30. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, Ter Kuile FO, Alaii JA, Gimnig JE, Arudo J, Vulule JM, Odhacha A, Kachur SP, Schoute E, Rosen DH, Sexton JD, Oloo AJ, Hawley WA, Am J Trop Med Hyg 2003 68 Suppl 4 23 29 12749482 (Pubitemid 38240678)
31. Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL, Am J Trop Med Hyg 2003 68 Suppl 4 100 107 12749492 (Pubitemid 38240688)
32. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Tamura K, Dudley J, Nei M, Kumar S, Mol Biol Evol 2007 24 1596 1599 10.1093/molbev/msm092 17488738 (Pubitemid 47236692)
33. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R, Bioinformatics 2003 19 2496 2497 10.1093/bioinformatics/btg359 14668244 (Pubitemid 38016658)
34. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Librado PJR, Bioinformatics 2009 25 1451 1452 10.1093/bioinformatics/btp187 19346325
35. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Excoffier L, H.E L, Mol Ecol Resour 2010 10 564 567 10.1111/j.1755-0998.2010.02847.x 21565059
36. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. Takala SL, Coulibaly D, Thera MA, Dicko A, Smith DL, Guindo AB, Kone AK, Traore K, Ouattara A, Djimde AA, Sehdev PS, Lyke KE, Diallo DA, Doumbo OK, Plowe CV, PLoS Med 2007 4 93 10.1371/journal.pmed.0040093 17355170 (Pubitemid 46495320)
37. Genetic diversity of vaccine candidate antigens in Plasmodium falciparum isolates from the Amazon basin of Peru. Chenet SM, Branch OH, Escalante AA, Lucas CM, Bacon DJ, Malar J 2008 7 93 10.1186/1475-2875-7-93 18505558 (Pubitemid 351862287)
38. Limited allelic diversity of Plasmodium falciparum merozoite surface protein 1 gene from populations in the Solomon Islands. Sakihama N, Ohmae H, Bakote'e B, Kawabata M, Hirayama K, Tanabe K, Am J Trop Med Hyg 2006 74 31 40 16407343 (Pubitemid 46768627)
39. A polymerase chain reaction/ligase detection reaction fluorescent microsphere assay to determine Plasmodium falciparum MSP-119 haplotypes. Dent AE, Yohn CT, Zimmerman PA, Vulule J, Kazura JW, Moormann AM, Am J Trop Med Hyg 2007 77 250 255 17690395 (Pubitemid 351859272)
40. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Hughes AL, Mol Biol Evol 1992 9 381 393 1584009
41. Selection and genetic drift of polymorphisms within the merozoite surface protein-1 gene of Plasmodium falciparum. Tanabe K, Sakihama N, Nakamura Y, Kaneko O, Kimura M, Ferreira MU, Hirayama K, Gene 2000 241 325 331 10.1016/S0378-1119(99)00472-2 10675045 (Pubitemid 30009863)
42. Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite. Barry AE, Schultz L, Buckee CO, Reeder JC, Plasmodium falciparum. PLoS One 2009 4 8497 10.1371/journal.pone.0008497
43. Sequence diversity and linkage disequilibrium within the merozoite surface protein-1 (Msp-1) locus of Plasmodium falciparum: a longitudinal study in Brazil. Da Silveira LA, Ribeiro WL, Kirchgatter K, Wunderlich G, Matsuoka H, Tanabe K, Ferreira MU, J Eukaryot Microbiol 2001 48 433 439 10.1111/j.1550-7408. 2001.tb00176.x 11456319 (Pubitemid 32646455)
44. Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Ferreira MU, Ribeiro WL, Tonon AP, Kawamoto F, Rich SM, Gene 2003 304 65 75 12568716 (Pubitemid 36142063)
45. MSP-1 MVWG: Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. Ogutu BR, Apollo OJ, McKinney D, Okoth W, Siangla J, Dubovsky F, Tucker K, Waitumbi JN, Diggs C, Wittes J, Malkin E, Leach A, Soisson LA, Milman JB, Otieno L, Holland CA, Polhemus M, Remich SA, Ockenhouse CF, Cohen J, Ballou WR, Martin SK, Angov E, Stewart VA, Lyon JA, Heppner DG, Withers M, PLoS One 2009 4 4708 10.1371/journal.pone.0004708 19262754
46. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, Seydel K, McVean GA, Su XZ, Nat Genet 2007 39 126 130 10.1038/ng1924 17159981 (Pubitemid 46026512)
47. A study of genetic diversity in the gene encoding the circumsporozoite protein (CSP) of Plasmodium falciparum from different transmission areas-XVI. Escalante AA, Grebert HM, Isea R, Goldman IF, Basco L, Magris M, Biswas S, Kariuki S, Lal AA, Asembo Bay Cohort Project Mol Biochem Parasitol 2002 125 83 90 10.1016/S0166-6851(02)00216-5 (Pubitemid 35449248)
48. Diversity in the immunodominant determinants of the circumsporozoite protein of Plasmodium falciparum parasites from malaria-endemic regions of Papua New Guinea and Brazil. Shi YP, Alpers MP, Povoa MM, Lal AA, Am J Trop Med Hyg 1992 47 844 851 1281968 (Pubitemid 23019157)
49. RTS, S/AS02A malaria vaccine does not induce parasite CSP T cell epitope selection and reduces multiplicity of infection. Enosse S, Dobaño C, Quelhas D, Aponte JJ, Lievens M, Leach A, Sacarlal J, Greenwood B, Milman J, Dubovsky F, Cohen J, Thompson R, Ballou WR, Alonso PL, Conway DJ, Sutherland CJ, PLoS Clin Trials 2006 1 5 10.1371/journal.pctr.0010005 16871327
50. Impact of RTS, S/AS02(A) and RTS, S/AS01(B) on genotypes of P. falciparum in adults participating in a malaria vaccine clinical trial. Waitumbi JN, Anyona SB, Hunja CW, Kifude CM, Polhemus ME, Walsh DS, Ockenhouse CF, Heppner DG, Leach A, Lievens M, Ballou WR, Cohen JD, Sutherland CJ, PLoS One 2009 4 7849 10.1371/journal.pone.0007849 19924281
51. High-throughput sequence typing of T-cell epitope polymorphisms in Plasmodium falciparum circumsporozoite protein. Alloueche A, Silveira H, Conway DJ, Bojang K, Doherty T, Cohen J, Pinder M, Greenwood BM, Mol Biochem Parasitol 2000 106 273 282 10.1016/S0166-6851(99)00221-2 10699256 (Pubitemid 30123073)
52. Plasmodium falciparum: restricted polymorphism of T cell epitopes of the circumsporozoite protein in Brazil. Yoshida N, Di Santi SM, Dutra AP, Nussenzweig RS, Nussenzweig V, Enea V, Exp Parasitol 1990 71 386 392 10.1016/0014-4894(90)90064-J 1699781 (Pubitemid 20372355)
53. Geographically restricted heterogeneity of the Plasmodium falciparum circumsporozoite protein: relevance for vaccine development. Doolan DL, Saul AJ, Good MF, Infect Immun 1992 60 675 682 1730503
54. Genetic diversity of T-helper cell epitopic regions of circumsporozoite protein of Plasmodium falciparum isolates from India. Bhattacharya PR, Bhatia V, Pillai CR, Trans R Soc Trop Med Hyg 2006 100 395 400 10.1016/j.trstmh.2005.07. 012 16288791 (Pubitemid 43362140)
55. Sequence variation in the T-cell epitopes of the Plasmodium falciparum circumsporozoite protein among field isolates is temporally stable: a 5-year longitudinal study in southern Vietnam. Jalloh A, Van Thien H, Ferreira MU, Ohashi J, Matsuoka H, Kanbe T, Kikuchi A, Kawamoto F, J Clin Microbiol 2006 44 1229 1235 10.1128/JCM.44.4.1229-1235.2006 16597843
56. Factors affecting use of permethrin-treated bed nets during a randomized controlled trial in western Kenya. Alaii JA, Hawley WA, Kolczak MS, Ter Kuile FO, Gimnig JE, Vulule JM, Odhacha A, Oloo AJ, Nahlen BL, Phillips-Howard PA, Am J Trop Med Hyg 2003 68 Suppl 4 137 141 12749497 (Pubitemid 38240693)