Miller LH, Mason SJ, Clyde DF, McGinniss MH, 1976. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302–304.
Spencer HC, Miller LH, Collins WE, Knud-Hansen C, McGinnis MH, Shiroishi T, Lobos RA, Feldman RA, 1978. The Duffy blood group and resistance to Plasmodium vivax in Honduras. Am J Trop Med Hyg 27: 664–670.
Miller LH, McGinniss MH, Holland PV, Sigmon P, 1978. The Duffy blood group phenotype in American blacks infected with Plasmodium vivax in Vietnam. Am J Trop Med Hyg 27: 1069–1072.
Menard D et al.., 2010. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA 107: 5967–5971.
Lo E, Yewhalaw D, Zhong D, Zemene E, Degefa T, Tushune K, Ha M, Lee MC, James AA, Yan G, 2015. Molecular epidemiology of Plasmodium vivax and Plasmodium falciparum malaria among Duffy-positive and Duffy-negative populations in Ethiopia. Malar J 14: 84.
Abdelraheem MH, Albsheer MM, Mohamed HS, Amin M, Abdel Hamid MM, 2016. Transmission of Plasmodium vivax in Duffy-negative individuals in central Sudan. Trans R Soc Trop Med Hyg 110: 258–260.
Ryan JR et al.., 2006. Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in western Kenya. Am J Trop Med Hyg 75: 575–581.
Gunalan K, Lo E, Hostetler JB, Yewhalaw D, Mu J, Neafsey DE, Yan G, Miller LH, 2016. Role of Plasmodium vivax Duffy-binding protein 1 in invasion of Duffy-null Africans. Proc Natl Acad Sci USA 113: 6271–6276.
Pearson RD et al.., 2016. Genomic analysis of local variation and recent evolution in Plasmodium vivax. Nat Genet 48: 959–964.
Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, de Sousa B, do Rosario VE, Benito A, Berzosa P, Arez AP, 2011. Duffy negative antigen is no longer a barrier to Plasmodium vivax–molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis 5: e1192.
Poirier P et al.., 2016. The hide and seek of Plasmodium vivax in West Africa: report from a large-scale study in Beninese asymptomatic subjects. Malar J 15: 570.
Fru-Cho J, Bumah VV, Safeukui I, Nkuo-Akenji T, Titanji VP, Haldar K, 2014. Molecular typing reveals substantial Plasmodium vivax infection in asymptomatic adults in a rural area of Cameroon. Malar J 13: 170.
Ngassa Mbenda HG, Das A, 2014. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One 9: e103262.
Wurtz N et al.., 2011. Vivax malaria in Mauritania includes infection of a Duffy-negative individual. Malar J 10: 336.
Rogier E, Moss DM, Chard AN, Trinies V, Doumbia S, Freeman MC, Lammie PJ, 2017. Evaluation of immunoglobulin G responses to Plasmodium falciparum and Plasmodium vivax in Malian school children using multiplex bead assay. Am J Trop Med Hyg 96: 312–318.
Doumbo O, Koita O, Traore SF, Sangare O, Coulibaly A, Vincent R, Soula G, Quilici M, Toure YT, 1991. Les aspects parasitologiques de l’épidémiologie du paludisme dans le Sahara malien. Med Afr Noire 38: 103–109.
Koita OA et al.., 2012. Effect of seasonality and ecological factors on the prevalence of the four malaria parasite species in northern Mali. J Trop Med 2012: 367160.
Bernabeu M et al.., 2012. Plasmodium vivax malaria in Mali: a study from three different regions. Malar J 11 :405.
Coulibaly D et al.., 2013. Spatio-temporal analysis of malaria within a transmission season in Bandiagara, Mali. Malar J 12: 82.
Coulibaly D et al.., 2014. Stable malaria incidence despite scaling up control strategies in a malaria vaccine-testing site in Mali. Malar J 13: 374.
Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK, 2009. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol 47: 975–980.
Tournamille C, Colin Y, Cartron JP, Le Van Kim C, 1995. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10: 224–228.
Snounou G, White NJ, 2004. The co-existence of Plasmodium: sidelights from falciparum and vivax malaria in Thailand. Trends Parasitol 20: 333–339.
Shanks GD, White NJ, 2013. The activation of vivax malaria hypnozoites by infectious diseases. Lancet Infect Dis 13: 900–906.
Douglas NM, Nosten F, Ashley EA, Phaiphun L, van Vugt M, Singhasivanon P, White NJ, Price RN, 2011. Plasmodium vivax recurrence following falciparum and mixed species malaria: risk factors and effect of antimalarial kinetics. Clin Infect Dis 52: 612–620.
Menard D et al.., 2013. Whole genome sequencing of field isolates reveals a common duplication of the Duffy binding protein gene in Malagasy Plasmodium vivax strains. PLoS Negl Trop Dis 7: e2489.
Niang M et al.., 2015. A molecular survey of acute febrile illnesses reveals Plasmodium vivax infections in Kedougou, southeastern Senegal. Malar J 14: 281.
Motshoge T et al.., 2016. Molecular evidence of high rates of asymptomatic P. vivax infection and very low P. falciparum malaria in Botswana. BMC Infect Dis 16: 520.
Zimmerman PA et al.., 1999. Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci USA 96: 13973–13977.
Kochar DK, Das A, Kochar SK, Saxena V, Sirohi P, Garg S, Kochar A, Khatri MP, Gupta V, 2009. Severe Plasmodium vivax malaria: a report on serial cases from Bikaner in northwestern India. Am J Trop Med Hyg 80: 194–198.
Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti, Elyazar I, Bangs MJ, Maguire JD, Baird JK, 2007. Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Am J Trop Med Hyg 77: 984–991.
Genton B, D’Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I, 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127.
James SP, Nicol WD, Shute PG, 1936. Clinical and parasitological observations on induced malaria: (section of tropical diseases and parasitology). Proc R Soc Med 29: 879–894.
Dobson MJ, 1994. Malaria in England: a geographical and historical perspective. Parassitologia 36: 35–60.
Douglas NM et al.., 2014. Mortality attributable to Plasmodium vivax malaria: a clinical audit from Papua, Indonesia. BMC Med 12: 217.
Barber BE, William T, Grigg MJ, Parameswaran U, Piera KA, Price RN, Yeo TW, Anstey NM, 2015. Parasite biomass-related inflammation, endothelial activation, microvascular dysfunction and disease severity in vivax malaria. PLoS Pathog 11: e1004558.
Adekunle AI, Pinkevych M, McGready R, Luxemburger C, White LJ, Nosten F, Cromer D, Davenport MP, 2015. Modeling the dynamics of Plasmodium vivax infection and hypnozoite reactivation in vivo. PLoS Negl Trop Dis 9: e0003595.
Hester J, Chan ER, Menard D, Mercereau-Puijalon O, Barnwell J, Zimmerman PA, Serre D, 2013. De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes. PLoS Negl Trop Dis 7: e2569.
Ntumngia FB, Thomson-Luque R, Torres Lde M, Gunalan K, Carvalho LH, Adams JH, 2016. A novel erythrocyte binding protein of Plasmodium vivax suggests an alternate invasion pathway into Duffy-positive reticulocytes. MBio 7: e01261–e01216.
Gunalan K, Gao X, Yap SS, Huang X, Preiser PR, 2013. The role of the reticulocyte-binding-like protein homologues of Plasmodium in erythrocyte sensing and invasion. Cell Microbiol 15: 35–44.
Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH, 1996. The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med 184: 1531–1536.
Tran TM, Moreno A, Yazdani SS, Chitnis CE, Barnwell JW, Galinski MR, 2005. Detection of a Plasmodium vivax erythrocyte binding protein by flow cytometry. Cytometry A 63: 59–66.
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Plasmodium vivax was thought to infect only the erythrocytes of Duffy blood group positive people. In the last decade, P. vivax has appeared throughout Africa, both in areas where Duffy positive and negative people live side by side as in Madagascar and Ethiopia and in areas where people are primarily Duffy negative, such as in western Kenya. We performed quantitative polymerase chain reaction on blood samples dried onto filter paper to determine the prevalence of P. vivax and Plasmodium falciparum in a cohort of 300 children (newborn to 6 years of age) in Bandiagara, a Sahelian area of Mali, west Africa, where the people are Duffy negative. We report 1–3 occurrences of P. vivax in each of 25 Duffy-negative children at six time points over two rainy seasons and the beginning of the third season. The prevalence of P. vivax infection was 2.0–2.5% at every time point (June 2009 to June 2010). All children with P. vivax infections were asymptomatic and afebrile, and parasite densities were extremely low. Anemia, however, was the main burden of infection. Plasmodium vivax could become a burden to sub-Saharan Africa, and the evidence of P. vivax existence needs to be taken into consideration in designing malaria control and elimination strategies in Africa.
These authors contributed equally to this work.
Financial support: This work was supported by the cooperative agreement 5U01AI065683 from the National Institute of Allergy and Infectious Diseases; and the grant D43TW001589 from the Fogarty International Center, National Institutes of Health, Howard Hughes Medical Institute and the Intramural Research Program of the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health.
Authors’ addresses: Amadou Niangaly, Amed Ouattara, Drissa Coulibaly, Abdoulaye K. Kone, Mahamadou A. Thera, and Ogobara K. Doumbo, Malaria Research and Training Center, International Center for Excellence in Research, University of Sciences, Techniques and Technology of Bamako, Bamako, Mali, E-mails: niangaly@icermali.org, amouattara@som.umaryland.edu, coulibalyd@icermali.org, fankone@icermali.org, mthera@icermali.org, and okd@icermali.org. Karthigayan Gunalan, Juliana M. Sá, and Louis H. Miller, Laboratory of Malaria and Vector Research and National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, E-mails: karthigayan.gunalan@nih.gov, jsa@niaid.nih.gov, and lmiller@niaid.nih.gov. Amed Ouattara, Matthew Adams, Mark A. Travassos, Jennifer Ferrero, Matthew B. Laurens, and Christopher V. Plowe, Division of Malaria Research, Institute for Global Health, University of Maryland School of Medicine, Baltimore, MD, E-mails: amouattara@som.umaryland.edu, madams@som.umaryland.edu, mtravass@som.umaryland.edu, jferrero@thellf.org, mlaurens@som.umaryland.edu, and cplowe@som.umaryland.edu.
Miller LH, Mason SJ, Clyde DF, McGinniss MH, 1976. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302–304.
Spencer HC, Miller LH, Collins WE, Knud-Hansen C, McGinnis MH, Shiroishi T, Lobos RA, Feldman RA, 1978. The Duffy blood group and resistance to Plasmodium vivax in Honduras. Am J Trop Med Hyg 27: 664–670.
Miller LH, McGinniss MH, Holland PV, Sigmon P, 1978. The Duffy blood group phenotype in American blacks infected with Plasmodium vivax in Vietnam. Am J Trop Med Hyg 27: 1069–1072.
Menard D et al.., 2010. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA 107: 5967–5971.
Lo E, Yewhalaw D, Zhong D, Zemene E, Degefa T, Tushune K, Ha M, Lee MC, James AA, Yan G, 2015. Molecular epidemiology of Plasmodium vivax and Plasmodium falciparum malaria among Duffy-positive and Duffy-negative populations in Ethiopia. Malar J 14: 84.
Abdelraheem MH, Albsheer MM, Mohamed HS, Amin M, Abdel Hamid MM, 2016. Transmission of Plasmodium vivax in Duffy-negative individuals in central Sudan. Trans R Soc Trop Med Hyg 110: 258–260.
Ryan JR et al.., 2006. Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in western Kenya. Am J Trop Med Hyg 75: 575–581.
Gunalan K, Lo E, Hostetler JB, Yewhalaw D, Mu J, Neafsey DE, Yan G, Miller LH, 2016. Role of Plasmodium vivax Duffy-binding protein 1 in invasion of Duffy-null Africans. Proc Natl Acad Sci USA 113: 6271–6276.
Pearson RD et al.., 2016. Genomic analysis of local variation and recent evolution in Plasmodium vivax. Nat Genet 48: 959–964.
Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, de Sousa B, do Rosario VE, Benito A, Berzosa P, Arez AP, 2011. Duffy negative antigen is no longer a barrier to Plasmodium vivax–molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis 5: e1192.
Poirier P et al.., 2016. The hide and seek of Plasmodium vivax in West Africa: report from a large-scale study in Beninese asymptomatic subjects. Malar J 15: 570.
Fru-Cho J, Bumah VV, Safeukui I, Nkuo-Akenji T, Titanji VP, Haldar K, 2014. Molecular typing reveals substantial Plasmodium vivax infection in asymptomatic adults in a rural area of Cameroon. Malar J 13: 170.
Ngassa Mbenda HG, Das A, 2014. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One 9: e103262.
Wurtz N et al.., 2011. Vivax malaria in Mauritania includes infection of a Duffy-negative individual. Malar J 10: 336.
Rogier E, Moss DM, Chard AN, Trinies V, Doumbia S, Freeman MC, Lammie PJ, 2017. Evaluation of immunoglobulin G responses to Plasmodium falciparum and Plasmodium vivax in Malian school children using multiplex bead assay. Am J Trop Med Hyg 96: 312–318.
Doumbo O, Koita O, Traore SF, Sangare O, Coulibaly A, Vincent R, Soula G, Quilici M, Toure YT, 1991. Les aspects parasitologiques de l’épidémiologie du paludisme dans le Sahara malien. Med Afr Noire 38: 103–109.
Koita OA et al.., 2012. Effect of seasonality and ecological factors on the prevalence of the four malaria parasite species in northern Mali. J Trop Med 2012: 367160.
Bernabeu M et al.., 2012. Plasmodium vivax malaria in Mali: a study from three different regions. Malar J 11 :405.
Coulibaly D et al.., 2013. Spatio-temporal analysis of malaria within a transmission season in Bandiagara, Mali. Malar J 12: 82.
Coulibaly D et al.., 2014. Stable malaria incidence despite scaling up control strategies in a malaria vaccine-testing site in Mali. Malar J 13: 374.
Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK, 2009. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol 47: 975–980.
Tournamille C, Colin Y, Cartron JP, Le Van Kim C, 1995. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10: 224–228.
Snounou G, White NJ, 2004. The co-existence of Plasmodium: sidelights from falciparum and vivax malaria in Thailand. Trends Parasitol 20: 333–339.
Shanks GD, White NJ, 2013. The activation of vivax malaria hypnozoites by infectious diseases. Lancet Infect Dis 13: 900–906.
Douglas NM, Nosten F, Ashley EA, Phaiphun L, van Vugt M, Singhasivanon P, White NJ, Price RN, 2011. Plasmodium vivax recurrence following falciparum and mixed species malaria: risk factors and effect of antimalarial kinetics. Clin Infect Dis 52: 612–620.
Menard D et al.., 2013. Whole genome sequencing of field isolates reveals a common duplication of the Duffy binding protein gene in Malagasy Plasmodium vivax strains. PLoS Negl Trop Dis 7: e2489.
Niang M et al.., 2015. A molecular survey of acute febrile illnesses reveals Plasmodium vivax infections in Kedougou, southeastern Senegal. Malar J 14: 281.
Motshoge T et al.., 2016. Molecular evidence of high rates of asymptomatic P. vivax infection and very low P. falciparum malaria in Botswana. BMC Infect Dis 16: 520.
Zimmerman PA et al.., 1999. Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci USA 96: 13973–13977.
Kochar DK, Das A, Kochar SK, Saxena V, Sirohi P, Garg S, Kochar A, Khatri MP, Gupta V, 2009. Severe Plasmodium vivax malaria: a report on serial cases from Bikaner in northwestern India. Am J Trop Med Hyg 80: 194–198.
Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti, Elyazar I, Bangs MJ, Maguire JD, Baird JK, 2007. Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Am J Trop Med Hyg 77: 984–991.
Genton B, D’Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I, 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127.
James SP, Nicol WD, Shute PG, 1936. Clinical and parasitological observations on induced malaria: (section of tropical diseases and parasitology). Proc R Soc Med 29: 879–894.
Dobson MJ, 1994. Malaria in England: a geographical and historical perspective. Parassitologia 36: 35–60.
Douglas NM et al.., 2014. Mortality attributable to Plasmodium vivax malaria: a clinical audit from Papua, Indonesia. BMC Med 12: 217.
Barber BE, William T, Grigg MJ, Parameswaran U, Piera KA, Price RN, Yeo TW, Anstey NM, 2015. Parasite biomass-related inflammation, endothelial activation, microvascular dysfunction and disease severity in vivax malaria. PLoS Pathog 11: e1004558.
Adekunle AI, Pinkevych M, McGready R, Luxemburger C, White LJ, Nosten F, Cromer D, Davenport MP, 2015. Modeling the dynamics of Plasmodium vivax infection and hypnozoite reactivation in vivo. PLoS Negl Trop Dis 9: e0003595.
Hester J, Chan ER, Menard D, Mercereau-Puijalon O, Barnwell J, Zimmerman PA, Serre D, 2013. De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes. PLoS Negl Trop Dis 7: e2569.
Ntumngia FB, Thomson-Luque R, Torres Lde M, Gunalan K, Carvalho LH, Adams JH, 2016. A novel erythrocyte binding protein of Plasmodium vivax suggests an alternate invasion pathway into Duffy-positive reticulocytes. MBio 7: e01261–e01216.
Gunalan K, Gao X, Yap SS, Huang X, Preiser PR, 2013. The role of the reticulocyte-binding-like protein homologues of Plasmodium in erythrocyte sensing and invasion. Cell Microbiol 15: 35–44.
Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH, 1996. The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med 184: 1531–1536.
Tran TM, Moreno A, Yazdani SS, Chitnis CE, Barnwell JW, Galinski MR, 2005. Detection of a Plasmodium vivax erythrocyte binding protein by flow cytometry. Cytometry A 63: 59–66.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1238 | 1037 | 42 |
Full Text Views | 806 | 15 | 0 |
PDF Downloads | 321 | 11 | 0 |