Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 20, Number 7—July 2014
Research

Independent Lineages of Highly Sulfadoxine-Resistant Plasmodium falciparum Haplotypes, Eastern Africa

Steve M. TaylorComments to Author , Alejandro L. Antonia1, Whitney E. Harrington, Morgan M. Goheen, Victor Mwapasa, Ebbie Chaluluka, Michal Fried, Edward Kabyemela, Mwayi Madanitsa, Carole Khairallah, Linda Kalilani-Phiri, Antoinette K. Tshefu, Stephen J. Rogerson, Feiko O. ter Kuile, Patrick E. Duffy, and Steven R. Meshnick
Author affiliations: Author affiliations: Duke University Medical Center, Durham, North Carolina, USA (S.M. Taylor); University of North Carolina, Chapel Hill, North Carolina, USA (S.M. Taylor, A.L. Antonia, M.M. Goheen, S.R. Meshnick); Seattle Children’s Hospital/University of Washington School of Medicine, Seattle, Washington, USA (W.E. Harrington); College of Medicine, Blantyre, Malawi (V. Mwapasa, E. Chaluluka, M. Madanitsa, L. Kalilani-Phiri); National Institutes of Health, Bethesda, Maryland, USA (M. Fried. P.E. Duffy); Seattle Biomedical Research Institute, Seattle (E. Kabyemela); Liverpool School of Tropical Medicine, Liverpool, UK (C. Khairallah, F.O. ter Kuile); University of Kinshasa, Kinshasha, Democratic Republic of the Congo (A.K. Tshefu); University of Melbourne, Melbourne, Victoria, Australia (S.J. Rogerson); University of Amsterdam, Amsterdam, the Netherlands (F.O. ter Kuile)

Main Article

Figure 2

Principal coordinates analyses of wild-type (SAKA) and mutant (SGEA and SGEG) Plasmodium falciparum dihydropteroate synthase (dhps) halotypes from eastern Africa based on analysis of variance (RST). Pairwise RST values were computed with SPAGeDi (26) for microsatellite profiles of 7 populations of parasites defined by dhps haplotype and location: SAKA parasites from Malawi (n = 24) and the Democratic Republic of the Congo (DRC) (n = 53) (blue dots); SGEA parasites from Malawi (n = 67) and DRC (n

Figure 2. Principal coordinates analyses of wild-type (SAKA) and mutant (SGEA and SGEG) Plasmodium falciparum dihydropteroate synthase (dhps) halotypes from eastern Africa based on analysis of variance (RST)Pairwise RST values were computed with SPAGeDi (26) for microsatellite profiles of 7 populations of parasites defined by dhps haplotype and location: SAKA parasites from Malawi (n = 24) and the Democratic Republic of the Congo (DRC) (n = 53) (blue dots); SGEA parasites from Malawi (n = 67) and DRC (n = 17) (green dots); and SGEG parasites from DRC (n = 5), Malawi (n = 10), and Tanzania (n = 17) (yellow dots)These pairwise values were inputted into principal coordinates analyses in GenAlEx (21), in which coordinates 1 and 2 cumulatively accounted for 96% of the varianceThe dhps haplotypes are defined by amino acids at codons 436, 437, 540, and 581Mutant amino acids are underlined and in bold.

Main Article

References
  1. Sridaran  S, McClintock  SK, Syphard  LM, Herman  KM, Barnwell  JW, Udhayakumar  V. Anti-folate drug resistance in Africa: meta-analysis of reported dihydrofolate reductase (dhfr) and dihydropteroate synthase (dhps) mutant genotype frequencies in African Plasmodium falciparum parasite populations. Malar J. 2010;9:247 . DOIPubMedGoogle Scholar
  2. Aponte  JJ, Schellenberg  D, Egan  A, Breckenridge  A, Carneiro  I, Critchley  J, Efficacy and safety of intermittent preventive treatment with sulfadoxine-pyrimethamine for malaria in African infants: a pooled analysis of six randomised, placebo-controlled trials. Lancet. 2009;374:153342 . DOIPubMedGoogle Scholar
  3. Dicko  A, Diallo  AI, Tembine  I, Dicko  Y, Dara  N, Sidibe  Y, Intermittent preventive treatment of malaria provides substantial protection against malaria in children already protected by an insecticide-treated bednet in Mali: a randomised, double-blind, placebo-controlled trial. PLoS Med. 2011;8:e1000407. DOIPubMedGoogle Scholar
  4. Konaté  AT, Yaro  JB, Ouedraogo  AZ, Diarra  A, Gansane  A, Soulama  I, Intermittent preventive treatment of malaria provides substantial protection against malaria in children already protected by an insecticide-treated bednet in Burkina Faso: a randomised, double-blind, placebo-controlled trial. PLoS Med. 2011;8:e1000408. DOIPubMedGoogle Scholar
  5. World Health Organization. WHO policy recommendation on intermittent preventive treatment during infancy with sulfadoxine-pyrimethamine (SP-IPTi) for Plasmodium falciparum malaria control in Africa 2010 [cited 2014 Apr 11]. http://www.who.int/malaria/news/WHO_policy_recommendation_IPTi_032010.pdf
  6. World Health Organization. WHO policy recommendation: seasonal malaria chemoprevention (SMC) for Plasmodium falciparum malaria control in highly seasonal transmission areas of the Sahel sub-region in Africa 2012 [cited 2014 Apr 11]. http://www.who.int/malaria/publications/atoz/who_smc_policy_recommendation/en/
  7. World Health Organization. WHO policy brief for the implementation of intermittent preventive treatment of malaria in pregnancy using sulfadoxine-pyrimethamine (IPTp-SP) 2013. [cited 2014 Apr 11]. http://www.who.int/malaria/publications/atoz/Policy_brief_IPTp-SP_implementation_11april2013.pdf
  8. Feng  G, Simpson  JA, Chaluluka  E, Molyneux  ME, Rogerson  SJ. Decreasing burden of malaria in pregnancy in Malawian women and its relationship to use of intermittent preventive therapy or bed nets. PLoS ONE. 2010;5:e12012. DOIPubMedGoogle Scholar
  9. Harrington  WE, Mutabingwa  TK, Kabyemela  E, Fried  M, Duffy  PE. Intermittent treatment to prevent pregnancy malaria does not confer benefit in an area of widespread drug resistance. Clin Infect Dis. 2011;53:22430. DOIPubMedGoogle Scholar
  10. Kublin  JG, Dzinjalamala  FK, Kamwendo  DD, Malkin  EM, Cortese  JF, Martino  LM, Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis. 2002;185:3808. DOIPubMedGoogle Scholar
  11. Gosling  RD, Gesase  S, Mosha  JF, Carneiro  I, Hashim  R, Lemnge  M, Protective efficacy and safety of three antimalarial regimens for intermittent preventive treatment for malaria in infants: a randomised, double-blind, placebo-controlled trial. Lancet. 2009;374:152132. DOIPubMedGoogle Scholar
  12. Harrington  WE, Mutabingwa  TK, Muehlenbachs  A, Sorensen  B, Bolla  MC, Fried  M, Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci U S A. 2009;106:902732. DOIPubMedGoogle Scholar
  13. Wootton  JC, Feng  X, Ferdig  MT, Cooper  RA, Mu  J, Baruch  DI, Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature. 2002;418:3203. DOIPubMedGoogle Scholar
  14. Roper  C, Pearce  R, Nair  S, Sharp  B, Nosten  F, Anderson  T. Intercontinental spread of pyrimethamine-resistant malaria. Science. 2004;305:1124. DOIPubMedGoogle Scholar
  15. Pearce  RJ, Pota  H, Evehe  MS. Bâ el-H, Mombo-Ngoma G, Malisa AL, et al. Multiple origins and regional dispersal of resistant dhps in African Plasmodium falciparum malaria. PLoS Med. 2009;6:e1000055.
  16. Vinayak  S, Alam  MT, Mixson-Hayden  T, McCollum  AM, Sem  R, Shah  NK, Origin and evolution of sulfadoxine resistant Plasmodium falciparum. PLoS Pathog. 2010;6:e1000830 . DOIPubMedGoogle Scholar
  17. Mita  T, Venkatesan  M, Ohashi  J, Culleton  R, Takahashi  N, Tsukahara  T, Limited geographical origin and global spread of sulfadoxine-resistant dhps alleles in Plasmodium falciparum populations. J Infect Dis. 2011;204:19808. DOIPubMedGoogle Scholar
  18. Taylor  SM, Antonia  AL, Chaluluka  E, Mwapasa  V, Feng  G, Molyneux  ME, Antenatal receipt of sulfadoxine-pyrimethamine does not exacerbate pregnancy-associated malaria despite the expansion of drug-resistant Plasmodium falciparum: clinical outcomes from the QuEERPAM study. Clin Infect Dis. 2012;55:4250 . DOIPubMedGoogle Scholar
  19. Taylor  SM, Messina  JP, Hand  CC, Juliano  JJ, Muwonga  J, Tshefu  AK, Molecular malaria epidemiology: mapping and burden estimates for the Democratic Republic of the Congo, 2007. PLoS ONE. 2011;6:e16420. DOIPubMedGoogle Scholar
  20. Taylor  SM, Antonia  AL, Parobek  CM, Juliano  JJ, Janko  M, Emch  M, Plasmodium falciparum sulfadoxine resistance is geographically and genetically clustered within the DR Congo. Sci Rep. 2013;3:1165.
  21. Peakall  R, Smouse  PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics. 2012;28:25379. DOIPubMedGoogle Scholar
  22. Excoffier  L, Smouse  PE, Quattro  JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992;131:47991 .PubMedGoogle Scholar
  23. Nei  M, Roychoudhury  AK. Sampling variances of heterozygosity and genetic distance. Genetics. 1974;76:37990 .PubMedGoogle Scholar
  24. Fluxus Engineering. Phylogenetic network software [cited 2012 Oct 19]. http://www.fluxus-engineering.com/sharenet.htm
  25. Bandelt  HJ, Forster  P, Rohl  A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:3748 . DOIPubMedGoogle Scholar
  26. Hardy  OJ, Vekemans  X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes. 2002;2:61820. DOIGoogle Scholar
  27. Felsenstein  J. PHYLIP - Phylogeny Inference Package (version 3.2). Cladistics. 1989;5:1646.
  28. Mobyle Portal. Institut Pasteur [cited 2013 Aug 27]. http://mobyle.pasteur.fr/cgi-bin/portal.py?#forms:neighbor
  29. Pritchard  JK, Stephens  M, Donnelly  P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:94559 .PubMedGoogle Scholar
  30. Hubisz  MJ, Falush  D, Stephens  M, Pritchard  JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour. 2009;9:1322–32.
  31. Evanno  G, Regnaut  S, Goudet  J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:261120. DOIPubMedGoogle Scholar
  32. Taylor  SM, Antonia  A, Feng  G, Mwapasa  V, Chaluluka  E, Molyneux  M, Adaptive evolution and fixation of drug-resistant Plasmodium falciparum genotypes in pregnancy-associated malaria: 9-year results from the QuEERPAM study. Infect Genet Evol. 2012;12:28290. DOIPubMedGoogle Scholar
  33. Minja  DT, Schmiegelow  C, Mmbando  B, Bostrom  S, Oesterholt  M, Magistrado  P, Plasmodium falciparum mutant haplotype infection during pregnancy associated with reduced birthweight, Tanzania. Emerg Infect Dis. 2013;19:144654. DOIPubMedGoogle Scholar
  34. Slatkin  M. A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995;139:45762 .PubMedGoogle Scholar
  35. Gutman  J, Mwandama  D, Wiegand  RE, Ali  D, Mathanga  DP, Skarbinski  J. Effectiveness of intermittent preventive treatment with sulfadoxine-pyrimethamine during pregnancy on maternal and birth outcomes in machinga district, Malawi. J Infect Dis. 2013;208:90716. DOIPubMedGoogle Scholar
  36. McCollum  AM, Poe  AC, Hamel  M, Huber  C, Zhou  Z, Shi  YP, Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis. 2006;194:18997. DOIPubMedGoogle Scholar
  37. Naidoo  I, Roper  C. Mapping ‘partially resistant’, ‘fully resistant’, and ‘super resistant’ malaria. Trends Parasitol. 2013;29:50515. DOIPubMedGoogle Scholar

Main Article

1Current affiliation: Duke University School of Medicine, Durham, North Carolina, USA.

Page created: June 17, 2014
Page updated: June 17, 2014
Page reviewed: June 17, 2014
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external