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Research Article

Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people

Didier Ménard, Céline Barnadas, Christiane Bouchier, Cara Henry-Halldin, Laurie R. Gray, Arsène Ratsimbasoa, Vincent Thonier, Jean-François Carod, Olivier Domarle, Yves Colin, Olivier Bertrand, Julien Picot, Christopher L. King, Brian T. Grimberg, Odile Mercereau-Puijalon, and Peter A. Zimmerman
  1. aInstitut Pasteur de Madagascar, Unité de Recherche sur le Paludisme, Antananarivo 101, Madagascar;
  2. bInstitut Pasteur, Unité d’Immunologie Moléculaire des Parasites, Centre National de la Recherche Scientifique Unité de Recherche Associée 2581, Paris 75724 cedex 15, France;
  3. cCenter for Global Health and Diseases, Case Western Reserve University, School of Medicine, Cleveland, OH 44106-7286;
  4. dInstitut Pasteur, Plate-forme Génomique, Paris 75724 cedex 15, France;
  5. eMinistère de la Santé, du Planning Familial et de la Protection Sociale, Direction de la Lutte contre les Maladies Infectieuses, Antananarivo 101, Madagascar;
  6. fInstitut Pasteur de Madagascar, Centre de Biologie Clinique, Antananarivo 101, Madagascar;
  7. gInstitut National de Transfusion Sanguine, Unité Mixte de Recherche-S 665 Inserm/Université Paris Diderot, Paris 75739 cedex 15, France; and
  8. hVeterans Affairs Research Service, Cleveland, OH 44106

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PNAS first published March 15, 2010; https://doi.org/10.1073/pnas.0912496107
Didier Ménard
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  • For correspondence: dmenard@pasteur.fr omp@pasteur.fr paz@case.edu
Céline Barnadas
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Christiane Bouchier
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Cara Henry-Halldin
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Laurie R. Gray
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Arsène Ratsimbasoa
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Vincent Thonier
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Jean-François Carod
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Olivier Domarle
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Yves Colin
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Olivier Bertrand
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Julien Picot
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Christopher L. King
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Brian T. Grimberg
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Odile Mercereau-Puijalon
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  • For correspondence: dmenard@pasteur.fr omp@pasteur.fr paz@case.edu
Peter A. Zimmerman
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  • For correspondence: dmenard@pasteur.fr omp@pasteur.fr paz@case.edu
  1. Edited by Thomas E. Wellems, National Institutes of Health, Bethesda, MD, and approved February 22, 2010 (received for review October 29, 2009)

  2. ↵1D.M. and C. Barnadas contributed equally to this work.

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Abstract

Malaria therapy, experimental, and epidemiological studies have shown that erythrocyte Duffy blood group-negative people, largely of African ancestry, are resistant to erythrocyte Plasmodium vivax infection. These findings established a paradigm that the Duffy antigen is required for P. vivax erythrocyte invasion. P. vivax is endemic in Madagascar, where admixture of Duffy-negative and Duffy-positive populations of diverse ethnic backgrounds has occurred over 2 millennia. There, we investigated susceptibility to P. vivax blood-stage infection and disease in association with Duffy blood group polymorphism. Duffy blood group genotyping identified 72% Duffy-negative individuals (FY*BES/*BES) in community surveys conducted at eight sentinel sites. Flow cytometry and adsorption–elution results confirmed the absence of Duffy antigen expression on Duffy-negative erythrocytes. P. vivax PCR positivity was observed in 8.8% (42/476) of asymptomatic Duffy-negative people. Clinical vivax malaria was identified in Duffy-negative subjects with nine P. vivax monoinfections and eight mixed Plasmodium species infections that included P. vivax (4.9 and 4.4% of 183 participants, respectively). Microscopy examination of blood smears confirmed blood-stage development of P. vivax, including gametocytes. Genotyping of polymorphic surface and microsatellite markers suggested that multiple P. vivax strains were infecting Duffy-negative people. In Madagascar, P. vivax has broken through its dependence on the Duffy antigen for establishing human blood-stage infection and disease. Further studies are necessary to identify the parasite and host molecules that enable this Duffy-independent P. vivax invasion of human erythrocytes.

  • erythrocyte
  • evolution
  • DARC
  • Madagascar

Footnotes

  • 2To whom correspondence may be addressed. E-mail: dmenard{at}pasteur.fr, omp{at}pasteur.fr, or paz{at}case.edu.
  • Author contributions: D.M., C. Barnadas, A.R., C.L.K., O.M.-P., and P.A.Z. designed research; D.M., C. Barnadas, C. Bouchier, C.H.-H., L.R.G., A.R., V.T., J.-F.C., O.D., O.B., J.P., and B.T.G. performed research; C.H.-H., Y.C., C.L.K., and P.A.Z. contributed new reagents/analytic tools; D.M., C. Barnadas, C.H.-H., Y.C., O.B., C.L.K., O.M.-P., and P.A.Z. analyzed data; and D.M., C. Barnadas, Y.C., C.L.K., O.M.-P., and P.A.Z. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. GU130196 and GU130197).

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0912496107/DCSupplemental.

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Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people
Didier Ménard, Céline Barnadas, Christiane Bouchier, Cara Henry-Halldin, Laurie R. Gray, Arsène Ratsimbasoa, Vincent Thonier, Jean-François Carod, Olivier Domarle, Yves Colin, Olivier Bertrand, Julien Picot, Christopher L. King, Brian T. Grimberg, Odile Mercereau-Puijalon, Peter A. Zimmerman
Proceedings of the National Academy of Sciences Mar 2010, 200912496; DOI: 10.1073/pnas.0912496107

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Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people
Didier Ménard, Céline Barnadas, Christiane Bouchier, Cara Henry-Halldin, Laurie R. Gray, Arsène Ratsimbasoa, Vincent Thonier, Jean-François Carod, Olivier Domarle, Yves Colin, Olivier Bertrand, Julien Picot, Christopher L. King, Brian T. Grimberg, Odile Mercereau-Puijalon, Peter A. Zimmerman
Proceedings of the National Academy of Sciences Mar 2010, 200912496; DOI: 10.1073/pnas.0912496107
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