Transactions of the Royal Society of Tropical Medicine and Hygiene
Volume 98, Issue 5 , Pages 302-310 , May 2004

Limited influence of haemoglobin variants on Plasmodium falciparum msp1 and msp2 alleles in symptomatic malaria

  • Frank P Mockenhaupt

      Affiliations

    • Institut fuer Tropenmedizin, Charité, Humboldt Universitaet, Spandauer Damm 130, 14050 Berlin, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49-30-30116-815; fax: +49-30-30116-888.
    • ,
  • Stephan Ehrhardt

      Affiliations

    • Institut fuer Tropenmedizin, Charité, Humboldt Universitaet, Spandauer Damm 130, 14050 Berlin, Germany
    • ,
  • Rowland Otchwemah

      Affiliations

    • School of Medicine and Health Sciences, University for Development Studies, PO Box TL 1650, Tamale, Ghana
    • ,
  • Teunis A Eggelte

      Affiliations

    • Division of Infectious Diseases, Tropical Medicine and AIDS, Academic Medical Centre, PO Box 22660, 1100 DD Amsterdam, The Netherlands
    • ,
  • Sylvester D Anemana

      Affiliations

    • Regional Health Administration, Takoradi, Ghana
    • ,
  • Klaus Stark

      Affiliations

    • Abteilung fuer Infektionsepidemiologie, Robert-Koch-Institut, Seestrasse 10, 13353 Berlin, Germany
    • ,
  • Ulrich Bienzle

      Affiliations

    • Institut fuer Tropenmedizin, Charité, Humboldt Universitaet, Spandauer Damm 130, 14050 Berlin, Germany
    • ,
  • Elisabeth Kohne

      Affiliations

    • Universitätskinderklinik, Prittwitzstrasse 43, 89075 Ulm, Germany

Received 20 May 2003 ,Revised 29 September 2003 ,Accepted 1 October 2003.

References 

  1. Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Kone A, et al. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood. 2000;96:2358–2363
  2. Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002;359:1311–1312
  3. Allen SJ, O’Donnell A, Alexander ND, Alpers MP, Peto TE, Clegg JB, et al. alpha+-thalassemia protects children against disease caused by other infections as well as malaria. Proc. Natl. Acad. Sci. USA. 1997;94:14736–14741
  4. Allen SJ, Rowe P, Allsopp CE, Riley EM, Jakobsen PH, Hill AV, et al. A prospective study of the influence of alpha thalassaemia on morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in Gambian children. Trans. R. Soc. Trop. Med. Hyg. 1993;87:282–285
  5. Allison AC. Polymorphism and natural selection in human populations. Cold Spring Harb. Symp. Quant. Biol. 1964;29:137–149
  6. al-Yaman F, Genton B, Reeder JC, Anders RF, Smith T, Alpers MP. Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans. R. Soc. Trop. Med. Hyg. 1997;91:602–605
  7. Ariey F, Hommel D, Le Scanf C, Duchemin JB, Peneau C, Hulin A, et al. Association of severe malaria with a specific Plasmodium falciparum genotype in French Guiana. J. Infect. Dis. 2001;184:237–241
  8. Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, et al. Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J. Infect. Dis. 1997;175:921–926
  9. Binka FN, Morris SS, Ross DA, Arthur P, Aryeetey ME. Patterns of malaria morbidity and mortality in children in northern Ghana. Trans. R. Soc. Trop. Med. Hyg. 1994;88:381–385
  10. Branch OH, Takala S, Kariuki S, Nahlen BL, Kolczak M, Hawley W, et al. Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect. Immun. 2001;69:7783–7792
  11. Ehrhardt S, Mockenhaupt FP, Agana-Nsiire P, Mathieu A, Anemana SD, Stark K, et al. Efficacy of chloroquine in the treatment of uncomplicated, Plasmodium falciparum malaria in northern Ghana. Ann. Trop. Med. Parasitol. 2002;96:239–247
  12. Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE. Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood. 2003;101:3309–3315
  13. Färnert A, Rooth I, Svensson A, Snounou G, Bjorkman A. Complexity of Plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. J. Infect. Dis. 1999;179:989–995
  14. Flint J, Harding RM, Boyce AJ, Clegg JB. The population genetics of the haemoglobinopathies. Baillieres Clin. Haematol. 1998;11:1–51
  15. Goel VK, Li X, Chen H, Liu SC, Chishti AH, Oh SS. Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proc. Natl. Acad. Sci. USA. 2003;100:5164–5169
  16. Haldane JBS. The rate of mutation of human genes. Hereditas. 1949;35:267–272
  17. Huisman THJ. Separation of hemoglobins and hemoglobin chains by high performance liquid chromatography. J. Chromatogr. 1987;418:277–304
  18. Konate L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, et al. Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans. R. Soc. Trop. Med. Hyg. 1999;93(Suppl. 1):21–28
  19. Kun JFJ, Schmidt-Ott RJ, Lehman LG, Lell B, Luckner D, Greve B, et al. Merozoite surface antigen 1 and 2 genotypes and rosetting of Plasmodium falciparum in severe and mild malaria in Lambarene, Gabon. Trans. R. Soc. Trop. Med. Hyg. 1998;92:110–114
  20. Kwiatkowski D. Cytokines and anti-disease immunity to malaria. Res. Immunol. 1991;142:707–712
  21. Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, et al. The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin. Infect. Dis. 1999;28:794–799
  22. Liu YT, Old JM, Miles K, Fisher CA, Weatherall DJ, Clegg JB. Rapid detection of alpha-thalassaemia deletions and alpha-globin gene triplication by multiplex polymerase chain reactions. Br. J. Haematol. 2000;108:295–299
  23. Luzzi GA, Merry AH, Newbold CI, Marsh K, Pasvol G, Weatherall DJ. Surface antigen expression on Plasmodium falciparum-infected erythrocytes is modified in alpha- and beta-thalassemia. J. Exp. Med. 1991;173:785–791
  24. Magesa SM, Mdira KY, Babiker HA, Alifrangis M, Färnert A, Simonsen PE, et al. Diversity of Plasmodium falciparum clones infecting children living in a holoendemic area in north-eastern Tanzania. Acta Trop. 2002;84:83–92
  25. Mockenhaupt FP, Rong B, Günther M, Beck S, Till H, Kohne E, et al. Anaemia in pregnant Ghanaian women: importance of malaria, iron deficiency, and haemoglobinopathies. Trans. R. Soc. Trop. Med. Hyg. 2000;94:477–483
  26. Modiano D, Luoni G, Sirima BS, Simpore J, Verra F, Konate A, et al. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001;414:305–308
  27. Müller DA, Charlwood JD, Felger I, Ferreira C, do Rosario V, Smith T. Prospective risk of morbidity in relation to multiplicity of infection with Plasmodium falciparum in Sao Tome. Acta Trop. 2001;78:155–162
  28. Ntoumi F, Ekala MT, Makuwa M, Lekoulou F, Mercereau-Puijalon O, Deloron P. Sickle cell trait carriage: imbalanced distribution of IgG subclass antibodies reactive to Plasmodium falciparum family-specific MSP2 peptides in serum samples from Gabonese children. Immunol. Lett. 2002;84:9–16
  29. Ntoumi F, Rogier C, Dieye A, Trape JF, Millet P, Mercereau-Puijalon O. Imbalanced distribution of Plasmodium falciparum MSP-1 genotypes related to sickle-cell trait. Mol. Med. 1997;3:581–592
  30. Ntoumi F, Mercereau-Puijalon O, Ossari S, Luty A, Reltien J, Georges A, et al. Plasmodium falciparum: sickle-cell trait is associated with higher prevalence of multiple infections in Gabonese children with asymptomatic infections. Exp. Parasitol. 1997;87:39–46
  31. Ofosu-Okyere A, Mackinnon MJ, Sowa MP, Koram KA, Nkrumah F, Osei YD, et al. Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology. 2001;123:113–123
  32. Owusu-Agyei S, Smith T, Beck HP, Amenga-Etego L, Felger I. Molecular epidemiology of Plasmodium falciparum infections among asymptomatic inhabitants of a holoendemic malarious area in northern Ghana. Trop. Med. Int. Health. 2002;7:421–428
  33. Pattanapanyasat K, Yongvanitchit K, Tongtawe P, Tachavanich K, Wanachiwanawin W, Fucharoen S, et al. Impairment of Plasmodium falciparum growth in thalassemic red blood cells: further evidence by using biotin labeling and flow cytometry. Blood. 1999;93:3116–3119
  34. Robert F, Ntoumi F, Angel G, Candito D, Rogier C, Fandeur T, et al. Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar, Senegal. Trans. R. Soc. Trop. Med. Hyg. 1996;90:704–711
  35. Senok AC, Li K, Nelson EA, Arumanayagam M, Li CK. Flow cytometric assessment of oxidant stress in age-fractionated thalassaemic trait erythrocytes and its relationship to in vitro growth of Plasmodium falciparum. Parasitology. 1998;116:1–6
  36. Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans. R. Soc. Trop. Med. Hyg. 1999;93(Suppl. 1):59–64
  37. Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, et al. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans. R. Soc. Trop. Med. Hyg. 1999;93:369–374
  38. WHO, 1996. Assessment of therapeutic efficacy of antimalarial drugs for uncomplicated falciparum malaria in areas with intense transmission. World Health Organization, Geneva. WHO/MAL/96.1077.
  39. Wilkinson RJ, Pasvol G. Host resistance to malaria runs into swampy water. Trends Microbiol. 1997;5:213–215
  40. Williams TN, Weatherall DJ, Newbold CI. The membrane characteristics of Plasmodium falciparum-infected and -uninfected heterozygous alpha(0)thalassaemic erythrocytes. Br. J. Haematol. 2002;118:663–670
  41. Witte AM, Klever HJ, Brabin BJ, Eggelte TA, Van der Kaay HJ, Alpers MP. Field evaluation of the use of an ELISA to detect chloroquine and its metabolites in blood, urine and breast-milk. Trans. R. Soc. Trop. Med. Hyg. 1990;84:521–525

PII: S0035-9203(03)00089-0

doi: 10.1016/j.trstmh.2003.10.001

Transactions of the Royal Society of Tropical Medicine and Hygiene
Volume 98, Issue 5 , Pages 302-310 , May 2004

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