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Low-Level Malaria Infections Detected by a Sensitive Polymerase Chain Reaction Assay and Use of This Technique in the Evaluation

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Low-Level Malaria Infections Detected by a Sensitive Polymerase Chain Reaction Assay and Use of This Technique in the Evaluation Am. J. Trop. Med. Hyg., 76(3), 2007, pp. 486–493 Copyright © 2007 by The American Society of Tropical Medicine and Hygiene LOW-LEVEL MALARIA INFECTIONS DETECTED BY A SENSITIVE POLYMERASE CHAIN REACTION ASSAY AND USE OF THIS TECHNIQUE IN THE EVALUATION OF MALARIA VACCINES IN AN ENDEMIC AREA EGERUAN B. IMOUKHUEDE,* LAURA ANDREWS, PAUL MILLIGAN, TAMARA BERTHOUD, KALIFA BOJANG, DAVIS NWAKANMA, JAMILA ISMAILI, CAROLINE BUCKEE, FANTA NJIE, SAIKOU KEITA, MAIMUNA SOWE, TRUDIE LANG, SARAH C. GILBERT, BRIAN M. GREENWOOD, AND ADRIAN V. S. HILL Medical Research Council Laboratories, Fajara, The Gambia; London School of Hygiene & Tropical Medicine, London, UK; Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK; Centre for Clinical Vaccinology & Tropical Medicine, University of Oxford, Oxford, UK Abstract. The feasibility of using a sensitive polymerase chain reaction (PCR) to evaluate malaria vaccines in small group sizes was tested in 102 adult Gambian volunteers who received either the malaria vaccine regimen FP9 ME- TRAP/MVA ME-TRAP or rabies vaccine. All volunteers received the antimalarial drugs primaquine and Lapdap plus artesunate to eliminate malaria parasites. Volunteers in a further group received an additional single treatment with sulfadoxine-pyrimethamine (SP) to prevent new infections. There was substantially lower T-cell immunogenicity than in previous trials with this vaccine regimen and no protection against infection in the malaria vaccine group. Using the primary endpoint of 20 parasites per mL, no difference was found in the prevalence of low-level infections in volunteers who received SP compared with those who did not, indicating that SP did not reduce the incidence of very low-density infection. However, SP markedly reduced the incidence of higher density infections. These findings support the feasi- bility and potential of this approach to screen pre-erythrocytic vaccines for efficacy against infection in small numbers of vaccinees in endemic areas. INTRODUCTION tween the results obtained with the experimental sporozoite challenge model and results obtained under conditions of Increased funding for malaria vaccine development, ad- natural challenge, field-efficacy trials will continue to play an vances in vaccine technology and the sequencing of the Plas- essential part in the early evaluation of candidate pre- modium falciparum genome have led to an increasing number erythrocytic vaccines. Because the power of a trial to detect of candidate malaria vaccines reaching the phase of clinical efficacy depends on the number of events observed, more evaluation. Although pre-erythrocytic vaccines can be tested sensitive methods of detection would allow smaller sample using sporozoite challenge with P. falciparum in non-immune sizes to be used. In semi-immune populations, most infections volunteers,1–3 it is uncertain how well this model will predict are cleared by blood-stage immunity prior to patency. Com- vaccine efficacy in populations exposed to natural infection parison of estimates of entomological inoculation rates with with genetically heterogeneous P. falciparum and provide evi- observed infection rates detected by peripheral blood micros- dence of efficacy in phase II studies in populations exposed to copy in villages near the town of Farafenni, The Gambia, in natural challenge that may be required before proceeding to 2002 suggested that the great majority of infectious bites did 7 a large phase III trial. RTS,S/AS02A, the most widely studied not lead to infections detectable by blood film. However, malaria vaccine, has consistently protected 30–45% of volun- many blood-stage infections may have been missed because teers challenged experimentally with sporozoites about 2 of the low sensitivity of microscopy, which has a lower limit of ∼ ␮ 9 weeks after final vaccination. Efficacy of this vaccine against detection of 10–50 parasites per L. Polymerase chain re- natural challenge with heterologous parasite strains in semi- action (PCR) assays that increase the sensitivity of detection immune adults in the field was 34% using a time-to-patent of blood-stage malaria infections by at least a hundred fold 4 compared with traditional microscopy have recently been de- infection analysis and 30% and 35% after 6 and 18 months, 1,3,10 respectively, against clinical malaria in Mozambican chil- veloped. 5,6 Although PCR monitoring is being used increasingly in the dren. These results for RTS,S/ASO2A suggest that for this context of malaria vaccine volunteer challenge studies in de- vaccine, efficacy in the field against patent infection is similar veloped countries,11–14 few such studies have been conducted to that measured in the experimental challenge model. A in endemic areas. In endemic areas, many malaria infections randomized trial of DNA-MVA vaccination undertaken in in adults fail to reach a parasite density that is high enough to semi-immune adults in The Gambia in 2002 showed no sig- be detected by microscopy, and the sample size and hence the nificant efficacy against infection,7 although the same vacci- cost of efficacy trials is typically large, requiring hundreds of nation regimen resulted in significantly delayed time to par- volunteers per study arm.5,7 If low-density infections could be asitemia compared with unvaccinated controls in challenge detected reliably prior to blood-stage clearance, then the experiments with a heterologous strain in Oxford and fully sample size needed for the evaluation of pre-erythrocytic vac- protected one of eight non-immune volunteers.8 cines could be reduced. We have, therefore, undertaken a As long as uncertainty remains about the correlation be- randomized trial using repeated blood sampling with PCR monitoring to evaluate the feasibility of this method for vac- cine evaluation and to make a preliminary assessment of the * Address correspondence to Egeruan Babatunde Imoukhuede, Eu- safety, immunogenicity, and efficacy against malaria infection ropean Malaria Vaccine Initiative, 12 Bell House, Ewen Crescent, of the FP9 ME-TRAP/MVA ME-TRAP candidate malaria Tulse Hill, London, UK. E-mail: [email protected] vaccine, which has shown significant efficacy in volunteer 486 NEW PCR METHOD FOR MALARIA VACCINE FIELD TRIALS 487 challenge studies in the UK11,15 and promising immunogenic- rabies vaccine group received a single treatment with sulfa- ity in Gambian adults.16 doxine-pyrimethamine (SP) prior to the surveillance period to provide a “positive” control group in whom protection MATERIALS AND METHODS against malaria could be expected for a period of several weeks. P. falciparum remains sensitive to SP in the study area. Study area and study population. The study took place in Allowing for a steady rate of drop-out during follow-up nine villages east of Farafenni, The Gambia, from June to amounting to total of 20% of subjects by the end of the trial, October 2004, the time of year when the incidence of malaria the trial had at least 80% power (using 2-sided 5% signifi- in The Gambia is highest. The entomological inoculation rate cance level) to detect a difference in time to infection be- in the study area was ∼10–50 infectious bites per year. Vol- tween vaccine and control groups if the vaccine efficacy was unteers of age 15–45 years, identified using the demographic at least 60%, and at least 70% of the control group volunteers surveillance system (DSS), were invited to take part in the developed parasitemia during the trial. A randomization list study after prior consultations with local civil and religious was generated using a block size of 6; individuals were allo- leaders. Experienced field workers gave detailed explanations cated to treatment groups in a 1:1:1 ratio. Pre-prepared ran- of the nature of the trial in English and in their respective domization envelopes, numbered 1–120, contained slips with local languages, and written consent was obtained. In the case the treatment assignment. On the day on which the first dose of volunteers of age 15–17 years, written informed consent of vaccine was due, treatments were assigned according to was also obtained from a parent or guardian. Prior to screen- pre-prepared numbered envelopes. For logistic reasons, 30 ing, the age and identity of each volunteer were checked, and volunteers were enrolled in the malaria vaccine group, 37 in a trained member of the study team provided pre-HIV test the rabies vaccine plus SP group, and 35 in the rabies-alone counseling. Screening involved a thorough physical examina- group (Figure 1). All volunteers were scheduled to receive 3 tion as well as laboratory evaluation. The latter included mea- doses of either malaria or rabies vaccine given 4 weeks apart. surement of a full blood count (FBC), packed cell volume After vaccination, volunteers were observed for 1 hour to (PCV), plasma creatinine, and alanine amino transferase detect any immediate side effects and given a course of anti- (ALT) concentrations as well as HIV 1 and 2 screening by pyretic (paracetamol, 500 mg, 3 times a day) to take if re- ELISA (Capillus HIV1/HIV2 Kit, Trinity Biotech PLC, Ire- quired. Field workers made home visits on days 1 and 2 after land). A glucose-6-phosphate dehydrogenase (G6PD) defi- vaccination, and volunteers were seen by the study physician ciency test (visual colorimetric assay, Sigma Diagnostics, US) on days 7 and 28 after each vaccination to record any adverse was carried out because of the risk of hemolysis when pri- events on a standard diary card. All volunteers
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