276
Views
37
CrossRef citations to date
0
Altmetric
Review

Suppression of vaccine responses by malaria: insignificant or overlooked?

&
Pages 409-429 | Published online: 09 Jan 2014

References

  • Snow RW, Korenromp EL, Gouws E. Pediatric mortality in Africa: Plasmodium falciparum malaria as a cause or risk? Am. J. Trop. Med. Hyg.71(2 Suppl.), 16–24 (2004).
  • Alonso PL, Lindsay SW, Armstrong Schellenberg JR et al. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, West Africa. 6. The impact of the interventions on mortality and morbidity from malaria. Trans. R. Soc. Trop. Med. Hyg.87(Suppl. 2), 37–44 (1993).
  • Kleinschmidt I, Schwabe C, Benavente L et al. Marked increase in child survival after four years of intensive malaria control. Am. J. Trop. Med. Hyg.80(6), 882–888 (2009).
  • Bronzan RN, Taylor TE, Mwenechanya J et al. Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J. Infect. Dis.195(6), 895–904 (2007).
  • Berkley JA, Bejon P, Mwangi T et al. HIV infection, malnutrition, and invasive bacterial infection among children with severe malaria. Clin. Infect. Dis.49(3), 336–343 (2009).
  • Bassat Q, Guinovart C, Sigauque B et al. Severe malaria and concomitant bacteraemia in children admitted to a rural Mozambican hospital. Trop. Med. Int. Health14(9), 1011–1019 (2009).
  • Kublin JG, Patnaik P, Jere CS et al. Effect of Plasmodium falciparum malaria on concentration of HIV-1-RNA in the blood of adults in rural Malawi: a prospective cohort study. Lancet365(9455), 233–240 (2005).
  • Moormann AM, Chelimo K, Sumba PO, Tisch DJ, Rochford R, Kazura JW. Exposure to holoendemic malaria results in suppression of Epstein–Barr virus-specific T cell immunosurveillance in Kenyan children. J. Infect. Dis.195(6), 799–808 (2007).
  • Piriou E, Kimmel R, Chelimo K et al. Serological evidence for long-term Epstein–Barr virus reactivation in children living in a holoendemic malaria region of Kenya. J. Med. Virol.81(6), 1088–1093 (2009).
  • Williamson WA, Greenwood BM. Impairment of the immune response to vaccination after acute malaria. Lancet1(8078), 1328–1329 (1978).
  • Greenwood BM, Bradley AK, Blakebrough IS, Whittle HC, Marshall TF, Gilles HM. The immune response to a meningococcal polysaccharide vaccine in an African village. Trans. R. Soc. Trop. Med. Hyg.74(3), 340–346 (1980).
  • Bradley-Moore AM, Greenwood BM, Bradley AK et al. Malaria chemoprophylaxis with chloroquine in young Nigerian children. II. Effect on the immune response to vaccination. Ann. Trop. Med. Parasitol.79(6), 563–573 (1985).
  • Greenwood AM, Greenwood BM, Bradley AK, Ball PAJ, Gilles HM. Enhancement of the immune response to meningococcal polysaccharide vaccine in a malaria endemic area by administration of chloroquine. Ann. Trop. Med. Parasitol.75(2), 261–263 (1981).
  • McGregor IA, Barr M. Antibody response to tetanus toxoid inoculation in malarious and non-malarious Gambian children. Trans. R. Soc. Trop. Med. Hyg.56(5), 364–367 (1962).
  • Greenwood BM, Bradley-Moore AM, Bryceson AD, Palit A. Immunosuppression in children with malaria. Lancet1(7743), 169–172 (1972).
  • Usen S, Milligan P, Ethevenaux C, Greenwood B, Mulholland K. Effect of fever on the serum antibody response of Gambian children to Haemophilus influenzae type b conjugate vaccine. Pediatr. Infect. Dis. J.19(5), 444–449 (2000).
  • Jones G, Steketee RW, Black RE, Bhutta ZA, Morris SS. How many child deaths can we prevent this year? Lancet362(9377), 65–71 (2003).
  • Mueller I, Galinski MR, Baird JK et al. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect. Dis.9(9), 555–566 (2009).
  • Viens P, Tarzaali A, Quevillon M. Inhibition of the immune response to pertussis vaccine during Plasmodium berghei yoelii infection in mice. Am. J. Trop. Med. Hyg.23(5), 846–849 (1974).
  • Chulay JD, Schneider I, Cosgriff TM et al. Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am. J. Trop. Med. Hyg.35(1), 66–68 (1986).
  • Blakebrough IS, Greenwood BM, Whittle HC, Bradley AK, Akintunde A. Sickle cell trait and the immune response to meningococcal vaccines. Trans. R. Soc. Trop. Med. Hyg.75(6), 905–906 (1981).
  • Faucher JF, Binder R, Missinou MA et al. Efficacy of atovaquone/proguanil for malaria prophylaxis in children and its effect on the immunogenicity of live oral typhoid and cholera vaccines. Clin. Infect. Dis.35(10), 1147–1154 (2002).
  • Monjour L, Bourdillon F, Schlumberger M et al. [Humoral and cellular immunity following antitetanus vaccination in malnourished and malaria-induced African children. 1. Study of the antitetanus antibody response]. Bull. World Health Organ.60(4), 589–596 (1982).
  • Brabin BJ, Nagel J, Hagenaars AM, Ruitenberg E, van Tilborgh AM. The influence of malaria and gestation on the immune response to one and two doses of adsorbed tetanus toxoid in pregnancy. Bull. World Health Organ.62(6), 919–930 (1984).
  • Monjour L, Bourdillon F, Froment A et al. [Measles vaccination in the Sudan-Sahel region of Africa. Absence of the immunodepressive effect of malaria]. Pathol. Biol. (Paris)33(4), 232–235 (1985).
  • Cenac A, Develoux M, Djibo A. Chloroquine treatment of malaria does not increase antibody response to measles vaccination. A controlled study of 580 rural children living in an endemic malaria area. Trans. R. Soc. Trop. Med. Hyg.82(3), 405 (1988).
  • Corrigall RJ. Asymptomatic malaria parasitaemia and the antibody response to tetanus toxoid vaccination. Trans. R. Soc. Trop. Med. Hyg.82(4), 540–541 (1988).
  • Simondon F, Preziosi MP, Pinchinat S et al. Randomised study of the possible adjuvant effect of BCG vaccine on the immunogenicity of diphtheria–tetanus–acellular pertussis vaccine in Senegalese infants. Eur. J. Clin. Microbiol. Infect. Dis.18(1), 23–29 (1999).
  • Spindel R, Baruzzi RG, Souza VA, Ferreira AW, Avila SL. Measles vaccine coverage and immune response in children of Caiabi and Metuktire Indian tribes living in malarial endemic area: Parque indigena do Xingu, Central Brazil. Trop. Doct.31(3), 142–144 (2001).
  • Schellenberg D, Menendez C, Kahigwa E et al. Intermittent treatment for malaria and anaemia control at time of routine vaccinations in Tanzanian infants: a randomised, placebo-controlled trial. Lancet357(9267), 1471–1477 (2001).
  • Massaga JJ, Kitua AY, Lemnge MM et al. Effect of intermittent treatment with amodiaquine on anaemia and malarial fevers in infants in Tanzania: a randomised placebo-controlled trial. Lancet361(9372), 1853–1860 (2003).
  • Rosen JB, Breman JG, Manclark CR et al. Malaria chemoprophylaxis and the serologic response to measles and diphtheria–tetanus–whole-cell pertussis vaccines. Malar. J.4, 53 (2005).
  • van Riet E, Retra K, Adegnika AA et al. Cellular and humoral responses to tetanus vaccination in Gabonese children. Vaccine26(29–30), 3690–3695 (2008).
  • Abdulla S, Oberholzer R, Juma O et al. Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. N. Engl. J. Med.359(24), 2533–2544 (2008).
  • Monjour L, Bourdillon F, Korinek AM et al. [Humoral immunity 5 years after anti-tetanus vaccination, in a group of malaria-infected and malnourished African children]. Pathol. Biol. (Paris)36(3), 235–239 (1988).
  • Prymula R, Siegrist CA, Chlibek R et al. Effect of prophylactic paracetamol administration at time of vaccination on febrile reactions and antibody responses in children: two open-label, randomised controlled trials. Lancet374(9698), 1339–1350 (2009).
  • Riley EM, Wagner GE, Akanmori BD, Koram KA. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol.23(2), 51–59 (2001).
  • Tarzaali A, Viens P, Quevillon M. Inhibition of the immune response to whooping cough and tetanus vaccines by malaria infection, and the effect of pertussis adjuvant. Am. J. Trop. Med. Hyg.26(3), 520–524 (1977).
  • Lambert PH, Liu M, Siegrist CA. Can successful vaccines teach us how to induce efficient protective immune responses? Nat. Med.11(4 Suppl.), S54–S62 (2005).
  • Kieny MP, LaForce FM. The promise of conjugate vaccines for Africa. Vaccine25(Suppl. 1), A108–A110 (2007).
  • Gonzalez-Fernandez A, Faro J, Fernandez C. Immune responses to polysaccharides: lessons from humans and mice. Vaccine26(3), 292–300 (2008).
  • Cutts FT, Zaman SM, Enwere G et al. Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trial. Lancet365(9465), 1139–1146 (2005).
  • Whittle HC, Bradley-Moore A, Fleming A, Greenwood BM. Effects of measles on the immune response of Nigerian children. Arch. Dis. Child.48(10), 753–756 (1973).
  • Shaheen SO, Aaby P, Hall AJ et al. Cell mediated immunity after measles in Guinea-Bissau: historical cohort study. BMJ313(7063), 969–974 (1996).
  • Aaby P, Bukh J, Lisse IM, Smits AJ. Measles vaccination and reduction in child mortality: a community study from Guinea-Bissau. J. Infect.8(1), 13–21 (1984).
  • Aaby P, Bukh J, Lisse IM et al. Determinants of measles mortality in a rural area of Guinea-Bissau: crowding, age, and malnutrition. J. Trop. Pediatr.30(3), 164–168 (1984).
  • Hull HF, Williams PJ, Oldfield F. Measles mortality and vaccine efficacy in rural West Africa. Lancet1(8331), 972–975 (1983).
  • Cooper PJ, Espinel I, Paredes W, Guderian RH, Nutman TB. Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. J. Infect. Dis.178(4), 1133–1138 (1998).
  • Nookala S, Srinivasan S, Kaliraj P, Narayanan RB, Nutman TB. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect. Immun.72(5), 2598–2604 (2004).
  • Elliott AM, Kizza M, Quigley MA et al. The impact of helminths on the response to immunization and on the incidence of infection and disease in childhood in Uganda: design of a randomized, double-blind, placebo-controlled, factorial trial of deworming interventions delivered in pregnancy and early childhood [ISRCTN32849447]. Clin. Trials4(1), 42–57 (2007).
  • King GE, Markowitz LE, Heath J et al. Antibody response to measles–mumps–rubella vaccine of children with mild illness at the time of vaccination. JAMA275(9), 704–707 (1996).
  • Dennehy PH, Saracen CL, Peter G. Seroconversion rates to combined measles-mumps–rubella–varicella vaccine of children with upper respiratory tract infection. Pediatrics94(4 Pt 1), 514–516 (1994).
  • Ndikuyeze A, Munoz A, Stewart J et al. Immunogenicity and safety of measles vaccine in ill African children. Int. J. Epidemiol.17(2), 448–455 (1988).
  • Ballou WR. The development of the RTS,S malaria vaccine candidate: challenges and lessons. Parasite Immunol.31(9), 492–500 (2009).
  • Augustine AD, Hall BF, Leitner WW, Mo AX, Wali TM, Fauci AS. NIAID workshop on immunity to malaria: addressing immunological challenges. Nat. Immunol.10(7), 673–678 (2009).
  • Bygbjerg IC, Jepsen S, Theander TG. Lymphocyte response to purified Plasmodium falciparum antigens during and after malaria. Acta. Trop.43(1), 55–62 (1986).
  • Ho M, Webster HK, Looareesuwan S et al. Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J. Infect. Dis.153(4), 763–771 (1986).
  • Riley EM, Andersson G, Otoo LN, Jepsen S, Greenwood BM. Cellular immune responses to Plasmodium falciparum antigens in Gambian children during and after an acute attack of falciparum malaria. Clin. Exp. Immunol.73(1), 17–22 (1988).
  • Hviid L, Theander TG, Abdulhadi NH, Abu-Zeid YA, Bayoumi RA, Jensen JB. Transient depletion of T cells with high LFA-1 expression from peripheral circulation during acute Plasmodium falciparum malaria. Eur. J. Immunol.21(5), 1249–1253 (1991).
  • Riley E. Malaria vaccine trials: SPf66 and all that. Curr. Opin. Immunol.7(5), 612–616 (1995).
  • Nosten F, Luxemburger C, Kyle DE et al. Randomised double-blind placebo-controlled trial of SPf66 malaria vaccine in children in northwestern Thailand. Shoklo SPf66 Malaria Vaccine Trial Group. Lancet348(9029), 701–707 (1996).
  • Acosta CJ, Galindo CM, Schellenberg D et al. Evaluation of the SPf66 vaccine for malaria control when delivered through the EPI scheme in Tanzania. Trop. Med. Int. Health4(5), 368–376 (1999).
  • Urdaneta M, Prata A, Struchiner CJ, Tosta CE, Tauil P, Boulos M. Evaluation of SPf66 malaria vaccine efficacy in Brazil. Am. J. Trop. Med. Hyg.58(3), 378–385 (1998).
  • Alonso PL, Smith T, Schellenberg JR et al. Randomised trial of efficacy of SPf66 vaccine against Plasmodium falciparum malaria in children in southern Tanzania. Lancet344(8931), 1175–1181 (1994).
  • D’Alessandro U, Leach A, Drakeley CJ et al. Efficacy trial of malaria vaccine SPf66 in Gambian infants. Lancet346(8973), 462–467 (1995).
  • Alonso PL, Sacarlal J, Aponte JJ et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet364(9443), 1411–1420 (2004).
  • Aponte JJ, Aide P, Renom M et al. Safety of the RTS,S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled Phase I/IIb trial. Lancet370(9598), 1543–1551 (2007).
  • Bejon P, Lusingu J, Olotu A et al. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N. Engl. J. Med.359(24), 2521–2532 (2008).
  • Genton B, Betuela I, Felger I et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a Phase 1–2b trial in Papua New Guinea. J. Infect. Dis.185(6), 820–827 (2002).
  • Genton B, Al-Yaman F, Betuela I et al. Safety and immunogenicity of a three-component blood-stage malaria vaccine (MSP1, MSP2, RESA) against Plasmodium falciparum in Papua New Guinean children. Vaccine22(1), 30–41 (2003).
  • Bejon P, Mwacharo J, Kai O et al. The induction and persistence of T cell IFN-γ responses after vaccination or natural exposure is suppressed by Plasmodium falciparum. J. Immunol.179(6), 4193–4201 (2007).
  • Bejon P, Mwacharo J, Kai O et al. A Phase 2b randomised trial of the candidate malaria vaccines FP9 ME-TRAP and MVA ME-TRAP among children in Kenya. PLoS Clin. Trials1(6), e29 (2006).
  • Struik SS, Riley EM. Does malaria suffer from lack of memory? Immunol. Rev.201, 268–290 (2004).
  • Filipe JA, Riley EM, Drakeley CJ, Sutherland CJ, Ghani AC. Determination of the processes driving the acquisition of immunity to malaria using a mathematical transmission model. PLoS Comput. Biol.3(12), e255 (2007).
  • Drakeley CJ, Corran PH, Coleman PG et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc. Natl Acad. Sci. USA102(14), 5108–5113 (2005).
  • Singer LM, Mirel LB, ter Kuile FO et al. The effects of varying exposure to malaria transmission on development of antimalarial antibody responses in preschool children. XVI. Asembo Bay Cohort Project. J. Infect. Dis.187(11), 1756–1764 (2003).
  • Otoo LN, Riley EM, Menon A, Byass P, Greenwood BM. Cellular immune responses to Plasmodium falciparum antigens in children receiving long term anti-malarial chemoprophylaxis. Trans. R. Soc. Trop. Med. Hyg.83(6), 778–782 (1989).
  • Wang R, Arevalo-Herrera M, Gardner MJ et al. Immune responses to Plasmodium vivax pre-erythrocytic stage antigens in naturally exposed Duffy-negative humans: a potential model for identification of liver-stage antigens. Eur. J. Immunol.35(6), 1859–1868 (2005).
  • Ferreira MU, Zilversmit M, Wunderlic G. Origins and evolution of antigenic diversity in malaria parasites. Curr. Mol. Med.7(6), 588–602 (2007).
  • Millington OR, Di Lorenzo C, Phillips RS, Garside P, Brewer JM. Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J. Biol.5(2), 5 (2006).
  • McBride JS, Micklem HS. Immunodepression of thymus-independent response to dextran in mouse malaria. Clin. Exp. Immunol.44(1), 74–81 (1981).
  • Greenwood BM, Playfair JH, Torrigiani G. Immunosuppression in murine malaria. I. General characteristics. Clin. Exp. Immunol.8(3), 467–478 (1971).
  • Wiedanz WP, Rank RG. Regional immunosuppression induced by Plasmodium berghei yoelii infection in mice. Infect. Immun.11(1), 211–212 (1975).
  • Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J. Exp. Med.197(2), 143–151 (2003).
  • Hafalla JC, Rai U, Bernal-Rubio D, Rodriguez A, Zavala F. Efficient development of plasmodium liver stage-specific memory CD8+ T cells during the course of blood-stage malarial infection. J. Infect. Dis.196(12), 1827–1835 (2007).
  • Mond JJ, Lees A, Snapper CM. T cell-independent antigens type 2. Annu. Rev. Immunol.13, 655–692 (1995).
  • Cobb BA, Kasper DL. Zwitterionic capsular polysaccharides: the new MHCII-dependent antigens. Cell. Microbiol.7(10), 1398–1403 (2005).
  • Weill JC, Weller S, Reynaud CA. Human marginal zone B cells. Annu. Rev. Immunol.27, 267–285 (2009).
  • Lopes-Carvalho T, Foote J, Kearney JF. Marginal zone B cells in lymphocyte activation and regulation. Curr. Opin. Immunol.17(3), 244–250 (2005).
  • Balazs M, Martin F, Zhou T, Kearney J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity17(3), 341–352 (2002).
  • Greenwood BM, Brown JC, De Jesus DG, Holborow EJ. Immunosuppression in murine malaria. II. The effect on reticulo-endothelial and germinal centre function. Clin. Exp. Immunol.9(3), 345–354 (1971).
  • Wykes MN, Good MF. What really happens to dendritic cells during malaria? Nat. Rev. Microbiol.6(11), 864–870 (2008).
  • Sponaas AM, Freitas do Rosario AP, Voisine C et al. Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood114(27), 5522–5531 (2009).
  • Schofield L, Uadia P. Lack of Ir gene control in the immune response to malaria. I. A thymus-independent antibody response to the repetitive surface protein of sporozoites. J. Immunol.144(7), 2781–2788 (1990).
  • Bate CA, Taverne J, Dave A, Playfair JH. Malaria exoantigens induce T-independent antibody that blocks their ability to induce TNF. Immunology70(3), 315–320 (1990).
  • Schofield L. On the function of repetitive domains in protein antigens of Plasmodium and other eukaryotic parasites. Parasitol. Today7(5), 99–105 (1991).
  • Greenwood BM, Brueton MJ. Complement activation in children with acute malaria. Clin. Exp. Immunol.18(2), 267–272 (1974).
  • Helegbe GK, Goka BQ, Kurtzhals JA et al. Complement activation in Ghanaian children with severe Plasmodium falciparum malaria. Malar. J.6, 165 (2007).
  • Nyakoe NK, Taylor RP, Makumi JN, Waitumbi JN. Complement consumption in children with Plasmodium falciparum malaria. Malar. J.8, 7 (2009).
  • Achtman AH, Khan M, MacLennan IC, Langhorne J. Plasmodium chabaudi chabaudi infection in mice induces strong B cell responses and striking but temporary changes in splenic cell distribution. J. Immunol.171(1), 317–324 (2003).
  • Urban BC, Hien TT, Day NP et al. Fatal Plasmodium falciparum malaria causes specific patterns of splenic architectural disorganization. Infect. Immun.73(4), 1986–1994 (2005).
  • Gosling RD, Carneiro I, Chandramohan D. Intermittent preventive treatment of malaria in infants: how does it work and where will it work? Trop. Med. Int. Health14(9), 1003–1010 (2009).
  • Philippe D, Jean-Marie OB, Marta GD, Thomas C. Global immunization: status, progress, challenges and future. BMC Int. Health Hum. Rights9(Suppl. 1), S2 (2009).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.