1921
Volume 98, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

In pregnancy-associated malaria, infected erythrocytes accumulate in the placenta. It is unclear if in polyclonal infections this results in distinct peripheral and placental parasite populations. We used long amplicon deep sequencing of ID1-DBL2X from 15 matched peripheral and placental samples collected at delivery from a high transmission area to determine genetic homology. Despite substantial sequence variation and detecting 23 haplotypes, the matched pairs mostly contained the same genetic variants, with 11 pairs sharing 100% of their variants, whereas others showed some heterogeneity. Thus, at delivery, peripheral and placental parasites appear to intermix and placental genotypes can be inferred through peripheral sampling.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.17-0529
2017-10-30
2019-11-22
Loading full text...

Full text loading...

/deliver/fulltext/14761645/98/1/tpmd170529.html?itemId=/content/journals/10.4269/ajtmh.17-0529&mimeType=html&fmt=ahah

References

  1. Taylor SM, 2011. Quantification of the burden and consequences of pregnancy-associated malaria in the Democratic Republic of the Congo. J Infect Dis 204: 17621771. [Google Scholar]
  2. Miller LH, Baruch DI, Marsh K, Doumbo OK, , 2002. The pathogenic basis of malaria. Nature 415: 673679. [Google Scholar]
  3. Steketee RW, Nahlen BL, Parise ME, Menendez C, , 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 2835. [Google Scholar]
  4. van Geertruyden JP, Thomas F, Erhart A, D’Alessandro U, , 2004. The contribution of malaria in pregnancy to perinatal mortality. Am J Trop Med Hyg 71: 3540. [Google Scholar]
  5. Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD, , 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93104. [Google Scholar]
  6. Ayres Pereira M, 2016. Placental sequestration of Plasmodium falciparum malaria parasites is mediated by the interaction between VAR2CSA and chondroitin sulfate A on Syndecan-1. PLoS Pathog 12: e1005831. [Google Scholar]
  7. Salanti A, 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200: 11971203. [Google Scholar]
  8. Beeson JG, Amin N, Kanjala M, Rogerson SJ, , 2002. Selective accumulation of mature asexual stages of Plasmodium falciparum-infected erythrocytes in the placenta. Infect Immun 70: 54125415. [Google Scholar]
  9. Douki JB, Sterkers Y, Lepolard C, Traore B, Costa FT, Scherf A, Gysin J, , 2003. Adhesion of normal and Plasmodium falciparum ring-infected erythrocytes to endothelial cells and the placenta involves the rhoptry-derived ring surface protein-2. Blood 101: 50255032. [Google Scholar]
  10. Pouvelle B, Buffet PA, Lepolard C, Scherf A, Gysin J, , 2000. Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nat Med 6: 12641268. [Google Scholar]
  11. Scherf A, Pouvelle B, Buffet PA, Gysin J, , 2001. Molecular mechanisms of Plasmodium falciparum placental adhesion. Cell Microbiol 3: 125131. [Google Scholar]
  12. Bordbar B, 2014. Genetic diversity of VAR2CSA ID1-DBL2Xb in worldwide Plasmodium falciparum populations: impact on vaccine design for placental malaria. Infect Genet Evol 25: 8192. [Google Scholar]
  13. Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, Arnot DE, Hviid L, Theander TG, , 2003. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49: 179191. [Google Scholar]
  14. Brabin BJ, , 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 10051016. [Google Scholar]
  15. Eisele TP, Larsen DA, Anglewicz PA, Keating J, Yukich J, Bennett A, Hutchinson P, Steketee RW, , 2012. Malaria prevention in pregnancy, birthweight, and neonatal mortality: a meta-analysis of 32 national cross-sectional datasets in Africa. Lancet Infect Dis 12: 942949. [Google Scholar]
  16. Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW, , 2007. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis 7: 105117. [Google Scholar]
  17. Clausen TM, 2012. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J Biol Chem 287: 2333223345. [Google Scholar]
  18. Bordbar B, Tuikue-Ndam N, Bigey P, Doritchamou J, Scherman D, Deloron P, , 2012. Identification of Id1-DBL2X of VAR2CSA as a key domain inducing highly inhibitory and cross-reactive antibodies. Vaccine 30: 13431348. [Google Scholar]
  19. EVI, 2017. European Vaccine Initiative - PRIMALVAC. Available at: http://www.euvaccine.eu/node/155/. Accessed June 15, 2017.
  20. EVI, 2017. European Vaccine Initiative - PlacMalVac. Available at: http://www.euvaccine.eu/node/156/. Accessed June 15, 2017.
  21. Patel JC, 2017. Increased risk of low birth weight in women with placental malaria associated with P. falciparum VAR2CSA clade. Sci Rep 7: 7768. [Google Scholar]
  22. Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK, , 2012. Genotype comparison of Plasmodium vivax and Plasmodium falciparum clones from pregnant and non-pregnant populations in North-west Colombia. Malar J 11: 392. [Google Scholar]
  23. Cohee LM, Kalilani-Phiri L, Mawindo P, Joshi S, Adams M, Kenefic L, Jacob CG, Taylor TE, Laufer MK, , 2016. Parasite dynamics in the peripheral blood and the placenta during pregnancy-associated malaria infection. Malar J 15: 483. [Google Scholar]
  24. Guitard J, Andersen P, Ermont C, Gnidehou S, Fievet N, Lund O, Deloron P, Ndam NT, , 2010. Plasmodium falciparum population dynamics in a cohort of pregnant women in Senegal. Malar J 9: 165. [Google Scholar]
  25. Jafari-Guemouri S, Ndam NT, Bertin G, Renart E, Sow S, Le Hesran JY, Deloron P, , 2005. Demonstration of a high level of parasite population homology by quantification of Plasmodium falciparum alleles in matched peripheral, placental, and umbilical cord blood samples. J Clin Microbiol 43: 29802983. [Google Scholar]
  26. Kamwendo DD, Dzinjalamala FK, Snounou G, Kanjala MC, Mhango CG, Molyneux ME, Rogerson SJ, , 2002. Plasmodium falciparum: PCR detection and genotyping of isolates from peripheral, placental, and cord blood of pregnant Malawian women and their infants. Trans R Soc Trop Med Hyg 96: 145149. [Google Scholar]
  27. Kassberger F, Birkenmaier A, Khattab A, Kremsner PG, Klinkert MQ, , 2002. PCR typing of Plasmodium falciparum in matched peripheral, placental and umbilical cord blood. Parasitol Res 88: 10731079. [Google Scholar]
  28. Mayengue PI, Rieth H, Khattab A, Issifou S, Kremsner PG, Klinkert MQ, Ntoumi F, , 2004. Submicroscopic Plasmodium falciparum infections and multiplicity of infection in matched peripheral, placental and umbilical cord blood samples from Gabonese women. Trop Med Int Health 9: 949958. [Google Scholar]
  29. Schleiermacher D, Le Hesran JY, Ndiaye JL, Perraut R, Gaye A, Mercereau-Puijalon O, , 2002. Hidden Plasmodium falciparum parasites in human infections: different genotype distribution in the peripheral circulation and in the placenta. Infect Genet Evol 2: 97105. [Google Scholar]
  30. Serra-Casas E, 2011. Persistence of Plasmodium falciparum parasites in infected pregnant Mozambican women after delivery. Infect Immun 79: 298304. [Google Scholar]
  31. Huynh BT, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, Guezo-Mevo B, Massougbodji A, Ndam NT, Deloron P, Cot M, , 2011. Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg 85: 214220. [Google Scholar]
  32. Doritchamou J, Bertin G, Moussiliou A, Bigey P, Viwami F, Ezinmegnon S, Fievet N, Massougbodji A, Deloron P, Tuikue Ndam N, , 2012. First-trimester Plasmodium falciparum infections display a typical “placental” phenotype. J Infect Dis 206: 19111919. [Google Scholar]
  33. Magistrado PA, 2011. High efficacy of anti DBL4varepsilon-VAR2CSA antibodies in inhibition of CSA-binding Plasmodium falciparum-infected erythrocytes from pregnant women. Vaccine 29: 437443. [Google Scholar]
  34. Moore JM, Nahlen B, Ofulla AV, Caba J, Ayisi J, Oloo A, Misore A, Nahmias AJ, Lal AA, Udhayakumar V, , 1997. A simple perfusion technique for isolation of maternal intervillous blood mononuclear cells from human placentae. J Immunol Methods 209: 93104. [Google Scholar]
  35. Work TT, Jacobs JM, Spence JR, Volney WJ, , 2010. High levels of green-tree retention are required to preserve ground beetle biodiversity in boreal mixedwood forests. Ecol Appl 20: 741751. [Google Scholar]
  36. Oksanen J, 2016. Vegan: Community Ecology Package. R package version 2.4-1. Available at: https://cran.r-project.org/web/packages/vegan/index.html. Accessed November 15, 2016.
  37. Jombart T, Ahmed I, , 2011. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27: 30703071. [Google Scholar]
  38. Pfeifer B, Wittelsburger U, Ramos-Onsins SE, Lercher MJ, , 2014. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol 31: 19291936. [Google Scholar]
  39. Thompson JM, Irgens LM, Skjaerven R, Rasmussen S, , 2007. Placenta weight percentile curves for singleton deliveries. BJOG 114: 715720. [Google Scholar]
  40. Walker PG, Griffin JT, Cairns M, Rogerson SJ, van Eijk AM, ter Kuile F, Ghani AC, , 2013. A model of parity-dependent immunity to placental malaria. Nat Commun 4: 1609. [Google Scholar]
  41. Beeson JG, Brown GV, Molyneux ME, Mhango C, Dzinjalamala F, Rogerson SJ, , 1999. Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties. J Infect Dis 180: 464472. [Google Scholar]
  42. Fried M, Duffy PE, , 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 15021504. [Google Scholar]
  43. Ofori MF, Staalsoe T, Bam V, Lundquist M, David KP, Browne EN, Akanmori BD, Hviid L, , 2003. Expression of variant surface antigens by Plasmodium falciparum parasites in the peripheral blood of clinically immune pregnant women indicates ongoing placental infection. Infect Immun 71: 15841586. [Google Scholar]
  44. Doritchamou J, Sossou-tchatcha S, Cottrell G, Moussiliou A, Hounton Houngbeme C, Massougbodji A, Deloron P, Ndam NT, , 2014. Dynamics in the cytoadherence phenotypes of Plasmodium falciparum infected erythrocytes isolated during pregnancy. PLoS One 9: e98577. [Google Scholar]
  45. Kraemer SM, 2007. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45. [Google Scholar]
  46. Brolin KJ, Ribacke U, Nilsson S, Ankarklev J, Moll K, Wahlgren M, Chen Q, , 2009. Simultaneous transcription of duplicated var2csa gene copies in individual Plasmodium falciparum parasites. Genome Biol 10: R117. [Google Scholar]
  47. Sander AF, Salanti A, Lavstsen T, Nielsen MA, Magistrado P, Lusingu J, Ndam NT, Arnot DE, , 2009. Multiple var2csa-type PfEMP1 genes located at different chromosomal loci occur in many Plasmodium falciparum isolates. PLoS One 4: e6667. [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.17-0529
Loading
/content/journals/10.4269/ajtmh.17-0529
Loading

Data & Media loading...

Supplemental Table

  • Received : 03 Jul 2017
  • Accepted : 17 Aug 2017
  • Published online : 30 Oct 2017

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error