Acquired Immunity to Malaria Denise L
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DigitalCommons@University of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Public Health Resources Public Health Resources 2009 Acquired Immunity to Malaria Denise L. Doolan Queensland Institute of Medical Research, The Bancroft Centre, 300 Herston Road, Post Office Royal Brisbane Hospital, Brisbane, Queensland 4029, Australia Carlota Dobaño Barcelona Centre for International Health Research, Hospital Clínic/IDIBAPS, Universitat de Barcelona, Spain J. Kevin Baird Eijkman-Oxford Clinical Research Unit, Jalan Diponegoro No. 69, Jakarta, Indonesia, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/publichealthresources Doolan, Denise L.; Dobaño, Carlota; and Baird, J. Kevin, "Acquired Immunity to Malaria" (2009). Public Health Resources. 336. http://digitalcommons.unl.edu/publichealthresources/336 This Article is brought to you for free and open access by the Public Health Resources at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Public Health Resources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. CLINICAL MICROBIOLOGY REVIEWS, Jan. 2009, p. 13–36 Vol. 22, No. 1 0893-8512/09/$08.00ϩ0 doi:10.1128/CMR.00025-08 Copyright © 2009, American Society for Microbiology. All Rights Reserved. Acquired Immunity to Malaria Denise L. Doolan,1* Carlota Doban˜o,2 and J. Kevin Baird3,4 Queensland Institute of Medical Research, The Bancroft Centre, 300 Herston Road, Post Office Royal Brisbane Hospital, Brisbane, Queensland 4029, Australia1; Barcelona Centre for International Health Research, Hospital Clínic/IDIBAPS, Universitat de Barcelona, Spain2; Eijkman-Oxford Clinical Research Unit, Jalan Diponegoro No. 69, Jakarta, Indonesia3; and Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, Oxford University, Oxford, United Kingdom4 INTRODUCTION .........................................................................................................................................................13 LIFE CYCLE AND GEOGRAPHIC DISTRIBUTION ............................................................................................14 HISTORICAL OBSERVATIONS OF NAI ................................................................................................................15 HISTORICAL OBSERVATIONS OF ACTIVELY ACQUIRED OR INDUCED IMMUNITY...........................16 CHARACTERISTICS OF NAI....................................................................................................................................16 EFFICACY OF NAI......................................................................................................................................................18 EPIDEMIOLOGICAL ASPECTS OF NAI................................................................................................................18 Effect of Exposure.....................................................................................................................................................18 Effect of Age...............................................................................................................................................................20 Insights from Intervention Studies ........................................................................................................................22 ACQUISITION OF NAI...............................................................................................................................................23 Parasite Strains.........................................................................................................................................................23 Antigenic Variation...................................................................................................................................................24 Strain-Specific versus Cross-Reactive (Strain-Transcending) Immune Responses ........................................24 Strain-Specific versus Cross-Reactive (Strain-Transcending) Protection...........................................................25 EMPIRICAL OBSERVATIONS OF PREERYTHROCYTIC-STAGE IMMUNITY ............................................27 EMPIRICAL OBSERVATIONS OF ASEXUAL ERYTHROCYTIC-STAGE IMMUNITY.................................27 EMPIRICAL OBSERVATIONS OF TRANSMISSION-BLOCKING IMMUNITY.............................................28 STAGE SPECIFICITY OF NAI..................................................................................................................................28 FUTURE PERSPECTIVES..........................................................................................................................................29 ACKNOWLEDGMENTS .............................................................................................................................................30 REFERENCES ..............................................................................................................................................................30 INTRODUCTION 1897, Ronald Ross identified plasmodial oocysts in the guts of mosquitoes fed on parasitemic birds, thereby implicating mos- Each year malaria infects about one-half billion people, kill- quitoes as the vector of malaria (261). William George Mc- ing 1 million to 2 million and severely dampening economic Callum confirmed plasmodial exflagellation as a process of development (44, 123, 133, 289, 321a, 321b). The parasitic sexual reproduction in 1897 (200, 201), and Batistta Grassi et Plasmodium species causing malaria persist and even flourish despite the availability of tools for prevention, control, and al. confirmed anopheline mosquitoes as the vector of human treatment. Those tools consist of an array of drugs, diagnostics, malaria in 1900 (130). and insecticides and a detailed understanding of the breeding Human malaria has persisted through the development of site preferences of the many anopheline mosquito vectors. miracle drugs and insecticides, a global eradication effort, and Despite the tremendous strides in biotechnology during the 30 years of intensive efforts to develop a practical vaccine. Not past 5 decades and the application to malaria of the many only does malaria persist; it thrives. Today the global malaria breakthroughs in molecular biology, genetics, immunology, situation is “serious and becoming worse” according to the and vaccinology by talented researchers, useful vaccines of any WHO. The incidence and range of malaria, which were pushed type evade us. This review examines one factor that may con- to lows in about 1965 (the zenith of dichlorodiphenyltrichlo- tribute substantially to this failure: inadequate understanding roethane spraying campaigns), now increase sharply in areas of of naturally acquired immunity (NAI). endemicity and spread into areas where control or eradication The dawn of scientific understanding of malaria occurred on had been achieved. Worse still, this resurgence has been in 6 November 1880, when Alphonse Laveran observed a male progress for 40 years. Even as early as 1978 the historian gametocyte exflagellating in a blood smear from an Algerian Gordon Harrison wrote of the persistence of malaria in the patient with malaria. This event marked the identification of face of such vigorous efforts to attack it, “Failure so universal, plasmodia as the cause of malaria (181). Working in India in so apparently ineluctable, must be trying to tell us something. The lesson could be of course that we have proved incompe- tent warriors. It could also be that we have misconstrued the * Corresponding author. Mailing address: Queensland Institute of problem”(140). Three dominant factors account for the failure Medical Research, The Bancroft Centre, 300 Herston Road, Post to maintain control: (i) parasite resistance to safe and afford- Office Royal Brisbane Hospital, Brisbane, Queensland 4029, Australia. Phone: (61-7) 3362 0382. Fax: (61-7) 3362 0105. E-mail: Denise able antimalarials, (ii) the almost complete demise of vector [email protected]. control programs in developing tropical and subtropical coun- 13 14 DOOLAN ET AL. CLIN.MICROBIOL.REV. tries, and (iii) the failure to develop a practical vaccine that attacking holoendemic malaria, we also undertake this task to prevents malaria. Inadequate understanding of the mecha- emphasize that NAI may be a good model for vaccine devel- nisms of naturally acquired clinical immunity against plasmo- opment. Consider a vaccine that allows infants and young dia may be an important factor contributing to the failure to children the same immunity enjoyed by their older siblings and develop a practical vaccine. We explore this possibility by ex- parents: no disease with natural boosting, lifelong. Even if that amining the genesis and character of the current state of un- concept were to be rendered superfluous by a safe eradication derstanding of NAI. strategy, a more thorough understanding of NAI would almost In 1980, Bruce-Chwatt (50) wrote, “Malaria immunity may certainly arm vaccinologists with other concepts to explore and be defined as the state of resistance to the infection brought adapt to specific populations. The exploration of NAI is key to about by all those processes which are involved in destroying the rational development and deployment of vaccines and the plasmodia or by limiting their multiplication.