EVIDENCE FOR TRANSMISSION OF PLASMODIUM VIVAX AMONG A DUFFY ANTIGEN NEGATIVE POPULATION IN WESTERN KENYA

JEFFREY R. RYAN Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by JEFFREY R. RYAN in
Current site
Google Scholar
PubMed
Close
,
JOSÉ A. STOUTE Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by JOSÉ A. STOUTE in
Current site
Google Scholar
PubMed
Close
,
JOSEPH AMON Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by JOSEPH AMON in
Current site
Google Scholar
PubMed
Close
,
RAYMOND F. DUNTON Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by RAYMOND F. DUNTON in
Current site
Google Scholar
PubMed
Close
,
RAMADHAN MTALIB Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by RAMADHAN MTALIB in
Current site
Google Scholar
PubMed
Close
,
JOSEPH KOROS Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by JOSEPH KOROS in
Current site
Google Scholar
PubMed
Close
,
BOAZ OWOUR Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by BOAZ OWOUR in
Current site
Google Scholar
PubMed
Close
,
SHIRLEY LUCKHART Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by SHIRLEY LUCKHART in
Current site
Google Scholar
PubMed
Close
,
ROBERT A. WIRTZ Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by ROBERT A. WIRTZ in
Current site
Google Scholar
PubMed
Close
,
JOHN W. BARNWELL Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by JOHN W. BARNWELL in
Current site
Google Scholar
PubMed
Close
, and
RONALD ROSENBERG Walter Reed Army Institute of Research, Washington, DC; US Army Medical Research Unit, Nairobi, Kenya; Uniformed Services University of Health Sciences, Bethesda, Maryland; Virginia Polytechnic Institute and State University, Blacksburg, Virginia; Centers for Disease Control and Prevention, Atlanta, Georgia

Search for other papers by RONALD ROSENBERG in
Current site
Google Scholar
PubMed
Close
Restricted access

We present evidence that a parasite with characteristics of Plasmodium vivax is being transmitted among Duffy blood group–negative inhabitants of Kenya. Thirty-two of 4,901 Anopheles gambiae and An. funestus (0.65%) collected in Nyanza Province were ELISA positive for the P. vivax circumsporozoite protein VK 247. All positives were found late in the rainy season, when An. funestus predominated, and disproportionately many were found at a single village. A P. vivax specific sequence of the SSU rRNA gene was amplified from three of six ELISA-positive mosquitoes. Erythrocytes from 31 children, including 9 microscopically diagnosed as infected with P. vivax, were negative by flow cytometry for the Fy3 or Fy6 epitopes, which indicate Duffy blood group expression. A DNA fragment specific for the C terminus of the gene for P. vivax merozoite surface protein 1 (MSP-1) was amplified from the blood of four of these children and subsequently sequenced from two.

Author Notes

  • 1

    Garnham PCC, 1966. Malaria Parasites and Other Haemosporidia. London: Blackwell, 118

    • PubMed
    • Export Citation
  • 2

    Westhoff CM, Reid ME, 2004. Review: The Kell, Duffy, and Kidd blood group systems. Immunohematology 20 :37–49.

  • 3

    Miller LH, Mason SJ, Clyde DF, McGinnis MH, 1976. The resistence factor to Plasmodium vivax in Blacks: Duffy blood group genotype FyFy. N Engl J Med 295 :302–304.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chaudhuri A, Polyakova J, Zbrzezna V, Williams K, Gulati S, Pogo AO, 1993. Cloning of glycoprotein D cDNA, which encodes the major subunit of the Duffy blood group system and the receptor for the Plasmodium vivax malaria parasite. Proc Natl Acad Sci USA 90 :10793–10797.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Mathews HM, Armstrong JC, 1981. Duffy blood types and vivax malaria in Ethiopia. Am J Trop Med Hyg 30 :299–303.

  • 7

    Sistonen P, Koistinen J, Aden Abdulle O, 1987. Distribution of blood groups in the East African Somali population. Hum Hered 37 :300–313.

  • 8

    Ryan JR, Dave K, Collins KM, Hochberg L, Sattabongkot J, Coleman RE, Dunton RF, Bangs MJ, Mbogo CM, Cooper RD, Schoeler GB, Rubio-Palis Y, Magris M, Romer LI, Padilla N, Quakyi IA, Bigoga J, Leke RG, Akinpelu O, Evans B, Walsey M, Patterson P, Wirtz RA, Chan AS, 2002. Extensive multiple test centre evaluation of the VecTest malaria antigen panel assay. Med Vet Entomol 16 :321–327.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Rosenberg R, Wirtz RA, Lanar DE, Sattabongkot J, Hall T, Waters AP, Prasittisuk C, 1989. Circumsporozoite protein heterogeneity in the human malaria Plasmodium vivax. Science 245 :973–976.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Luckhart S, Li K, Dunton R, Lewis E, Crampton A, Ryan J, Rosenberg R, 2003. Anopheles gambiae immune gene variants associated with natural Plasmodium infection. Mol Biochem Parasitol 128 :83–86.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Scott JA, Brogdon WG, Collins FH, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49 :520–529.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Wirtz RA, Zavala F, Charoenvit Y, 1987. Comparative testing of Plasmodium falciparum sporozoite monoclonal antibodies for ELISA development. Bull World Health Organ 65 :39–45.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Wirtz RA, Burkot TR, Andre RG, Rosenberg R, Collins WE, Roberts DR, 1985. Identification of Plasmodium vivax sporozoites in mosquitoes using an enzyme-linked immunosorbent assay. Am J Trop Med Hyg 34 :1048–1054.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Wirtz RA, Sattabongkot J, Hall T, Burkot TR, Rosenberg R, 1992. Development and evaluation of an ELISA for Plasmodium vivax-VK247 sporozoites. J Med Entomol 29 :854–857.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    De Arruda ME, Collins KM, Hochberg LP, Ryan PR, Wirtz RA, Ryan JR, 2004. Quantitative determination of sporozoites and circumsporozoite antigen in mosquitoes infected with Plasmodium falciparum or P. vivax. Ann Trop Med Parasitol 98 :121–127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Tyagi S, Kramer FR, 1996. Molecular beacons: Probes that fluoresce upon hybridization. Nat Biotechnol 14 :303–308.

  • 17

    Marras SA, Kramer FR, Tyagi S, 1999. Multiplex detection of single-nucleotide variations using molecular beacons. Genet Anal 14 :151–156.

  • 18

    Waitumbi JN, Donvito B, Kisserli A, Cohen JH, Stoute JA, 2004. Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J Infect Dis 190 :1183–1191.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Nichols ME, Rubinstein P, Barnwell JW, DeCordoba SR, Rosenfield RE, 1987. A new human Duffy blood group specifity defined by a murine monoclonal antibody. J Exp Med 166 :776–785.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Sandler SG, Mallory D, Wolfe JS, Byrne P, Lucas DM, 1997. Screening with monoclonal anti-Fy3 to provide blood for phenotype-matched transfusions for patients with sickle cell disease. Transfusion 37 :393–397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Galinski MR, Medina CC, Ingravallo P, Barnwell JW, 1992. A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69 :1213–1226.

  • 22

    Pasay MC, Cheng Q, Rzepczyk C, Saul A, 1995. Dimorphism of the C terminus of the Plasmodium vivax merozoite surface protein 1. Mol Biochem Parasitol 70 :217–219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Premawansa S, Snewin VA, Khouri E, Mendis KN, David PH, 1993. Plasmodium vivax: recombination between potential allelic types of the merozoite surface protein MSP1 in parasites isolated from patients. Exp Parasitol 76 :192–199.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Tsuboi T, Kappe SH, al-Yaman F, Prickett MD, Alpers M, Adams JH, 1994. Natural variation within the principal adhesion domain of the Plasmodium vivax duffy binding protein. Infect Immun 62 :5581–5586.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA, 1999. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg 60 :687–689.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Sanger F, Nicklen S, Coulson AR, 1977. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74 :5463–5467.

  • 27

    Rosenberg R, Rungsiwongse J, 1991. The number of sporozoites produced by individual malaria oocysts. Am J Trop Med Hyg 45 :574–577.

  • 28

    Golenda CF, Burge R, Schneider I, 1992. Plasmodium falciparum and P. berghei: detection of sporozoites and the circumsporozoite proteins in the saliva of Anopheles stephensi mosquitoes. Parasitol Res 78 :563–569.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Miller LH, Aikawa M, Johnson JG, Shiroishi T, 1979. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J Exp Med 149 :172–184.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Zimmerman PA, Woolley I, Masinde GL, Miller SM, McNamara DT, Hazlett F, Mgone CS, Alpers MP, Genton B, Boatin BA, Kazura JW, 1999. Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci USA 96 :13973–13977.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Rubio JM, Benito A, Roche J, Berzosa PJ, Garcia ML, Mico M, Edu M, Alvar J, 1999. Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg 60 :183–187.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Gautret P, Legros F, Koulmann P, Rodier MH, Jacquemin JL, 2001. Imported Plasmodium vivax malaria in France: geographical origin and report of an atypical case acquired in Central or Western Africa. Acta Trop 78 :177–181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Heisch RB, Harper JO, 1949. An epidemic of malaria in the Kenya highlands transmitted by Anopheles funestus. J Trop Med 52 :187–190.

  • 35

    Tahar R, Ringwald P, Basco LK, 1998. Heterogeneity in the circumsporozoite protein gene of Plasmodium malariae isolates from sub-Saharan Africa. Mol Biochem Parasitol 92 :71–78.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Swardson-Olver CJ, Dawson TC, Burnett RC, Peiper SC, Maeda N, Avery AC, 2002. Plasmodium yoelii uses the murine Duffy antigen receptor for chemokines as a receptor for normocyte invasion and an alternative receptor for reticulocyte invasion. Blood 99 :2677–2684.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Xainli J, Adams JH, King CL, 2000. The erythrocyte binding motif of plasmodium vivax duffy binding protein is highly polymorphic and functionally conserved in isolates from Papua New Guinea. Mol Biochem Parasitol 111 :253–260.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Barnwell JW, Nichols ME, Rubinstein P, 1989. In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169 :1795–1802.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Wertheimer SP, Barnwell JW, 1989. Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor-like protein. Exp Parasitol 69 :340–350.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Taye A, Hadis M, Adugna N, Tilahun D, Wirtz RA, 2006. Biting behavior and Plasmodium infection rates of Anopheles arabiensis from Sille, Ethiopia. Acta Trop. 97 :50–54.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Rongnoparut P, Supsamran N, Sattabongkot J, Suwanabun N, Rosenberg R, 1995. Sequence diversity in the gene coding for the circumsporozoite proteins of Plasmodium vivax in Thailand. Mol Biochem Parasitol 74 :201–210.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Rodriguez MH, Gonzalez-Ceron L, Hernandez JE, Nettel JA, Villarreal C, Kain KC, Wirtz RA, 2000. Different prevalences of Plasmodium vivax phenotypes VK210 and VK247 associated with the distribution of Anopheles albimanus and Anopheles pseudopunctipennis in Mexico. Am J Trop Med Hyg 62 :122–127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Cavalli-Sforza LL, Menozzi P, Piazza A, 1994. The History and Geography of Human Genes. Princeton, NJ: Princeton University Press, 158–192.

    • PubMed
    • Export Citation
  • 44

    Mason SJ, Miller LH, Shiroishi T, Dvorak JA, McGinnis MH, 1977. Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes. Br J Haematol 36: 327–335.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Looareesuwan S, White NJ, Chittamas S, Bunnag D, Harinasuta T, 1987. High rate of Plasmodium vivax relapse following treatment of falciparum malaria in Thailand. Lancet 2 :1052–1055.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1235 1129 600
Full Text Views 551 6 0
PDF Downloads 208 8 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save