BMC Infectious Diseases | |
Dynamics of malaria transmission and susceptibility to clinical malaria episodes following treatment of Plasmodium falciparum asymptomatic carriers: results of a cluster-randomized study of community-wide screening and treatment, and a parallel entomology study | |
Kamal Hamed2  Amitava Mukhopadhyay1  Sodiomon B Sirima3  Issa Nébié3  N Falé Sagnon3  Moussa W Guelbeogo3  Alfred B Tiono3  | |
[1] Novartis Healthcare Private Limited, Hyderabad, India;Novartis Pharmaceuticals Corporation, One Health Plaza, East Hanover, NJ 07936-1080, USA;Centre National de Recherche et de Formation sur le Paludisme (CNRFP), 01 BP 2208, Ouagadougou 01, Burkina Faso | |
关键词: Disease transmission; Parasite density; Entomological inoculation rate; Community screening; Asymptomatic carriers; Plasmodium falciparum; Malaria; | |
Others : 1145430 DOI : 10.1186/1471-2334-13-535 |
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received in 2013-04-25, accepted in 2013-11-11, 发布年份 2013 | |
【 摘 要 】
Background
In malaria-endemic countries, large proportions of individuals infected with Plasmodium falciparum are asymptomatic and constitute a reservoir of parasites for infection of newly hatched mosquitoes.
Methods
Two studies were run in parallel in Burkina Faso to evaluate the impact of systematic identification and treatment of asymptomatic carriers of P. falciparum, detected by rapid diagnostic test, on disease transmission and susceptibility to clinical malaria episodes. A clinical study assessed the incidence of symptomatic malaria episodes with a parasite density >5,000/μL after three screening and treatment campaigns ~1 month apart before the rainy season; and an entomological study determined the effect of these campaigns on malaria transmission as measured by entomological inoculation rate.
Results
The intervention arm had lower prevalence of asymptomatic carriers of asexual parasites and lower prevalence of gametocyte carriers during campaigns 2 and 3 as compared to the control arm. During the entire follow-up period, out of 13,767 at-risk subjects, 2,516 subjects (intervention arm 1,332; control arm 1,184) had symptomatic malaria. Kaplan-Meier analysis of the incidence of first symptomatic malaria episode with a parasite density >5,000/μL showed that, in the total population, the two treatment arms were similar until Week 11–12 after campaign 3, corresponding with the beginning of the malaria transmission season, after which the probability of being free of symptomatic malaria was lower in the intervention arm (logrank p < 0.0001). Similar trends were observed in infants and children <5 years and in individuals ≥5 years of age. In infants and children <5 years old who experienced symptomatic malaria episodes, the geometric mean P. falciparum density was lower in the intervention arm than the control arm. This trend was not seen in those individuals aged ≥5 years. Over the year, monthly variation in mosquito density and entomological inoculation rate was comparable in both arms, with September peaks in both indices.
Conclusion
Community screening and targeted treatment of asymptomatic carriers of P. falciparum had no effect on the dynamics of malaria transmission, but seemed to be associated with an increase in the treated community’s susceptibility to symptomatic malaria episodes after the screening campaigns had finished. These results highlight the importance of further exploratory studies to better understand the dynamics of disease transmission in the context of malaria elimination.
【 授权许可】
2013 Tiono et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD: Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379:413-431.
- [2]Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, Jima D, Gausi K, Komatsu R, Korenromp E, et al.: Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J 2009, 8:14. BioMed Central Full Text
- [3]Bhattarai A, Ali AS, Kachur SP, Martensson A, Abbas AK, Khatib R, Al-Mafazy AW, Ramsan M, Rotllant G, Gerstenmaier JF, et al.: Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med 2007, 4:e309.
- [4]Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, Sesay SS, Abubakar I, Dunyo S, Sey O, et al.: Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 2008, 372:1545-1554.
- [5]Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI, Durrheim DN, Ridl FC, Morris N, Seocharan I, Kunene S, et al.: Seven years of regional malaria control collaboration–Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg 2007, 76:42-47.
- [6]Khosa E, Kuonza LR, Kruger P, Maimela E: Towards the elimination of malaria in South Africa: a review of surveillance data in Mutale Municipality, Limpopo Province, 2005 to 2010. Malar J 2013, 12:7. BioMed Central Full Text
- [7]Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, et al.: A research agenda to underpin malaria eradication. PLoS Med 2011, 8:e1000406.
- [8]Greenwood BM: Control to elimination: implications for malaria research. Trends Parasitol 2008, 24:449-454.
- [9]Grueninger H, Hamed K: Transitioning from malaria control to elimination: the vital role of ACTs. Trends Parasitol 2012, 29:60-64.
- [10]The malERA Consultative Group on Drugs: A research agenda for malaria eradication: drugs. PLoS Med 2011, 8:e1000402.
- [11]von Seidlein L, Greenwood BM: Mass administrations of antimalarial drugs. Trends Parasitol 2003, 19:452-460.
- [12]Molineaux L, Gramiccia G: The Garki Project. Research on the epidemiology and control of malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization; 1980.
- [13]WHO: Guidelines for the Treatment of Malaria. 2nd edition. Geneva: World Health Organization; 2010.
- [14]Dunyo S, Milligan P, Edwards T, Sutherland C, Targett G, Pinder M: Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials 2006, 1:e20.
- [15]Mabunda S, Aponte JJ, Tiago A, Alonso P: A country-wide malaria survey in Mozambique. II. Malaria attributable proportion of fever and establishment of malaria case definition in children across different epidemiological settings. Malar J 2009, 8:74. BioMed Central Full Text
- [16]Vafa M, Troye-Blomberg M, Anchang J, Garcia A, Migot-Nabias F: Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar J 2008, 7:17. BioMed Central Full Text
- [17]Kern SE, Tiono AB, Makanga M, Gbadoe AD, Premji Z, Gaye O, Sagara I, Ubben D, Cousin M, Oladiran F, et al.: Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J 2011, 10:210. BioMed Central Full Text
- [18]Ogutu B, Tiono AB, Makanga M, Premji Z, Gbadoe AD, Ubben D, Marrast AC, Gaye O: Treatment of asymptomatic carriers with artemether-lumefantrine: an opportunity to reduce the burden of malaria? Malar J 2010, 9:30. BioMed Central Full Text
- [19]Crowell V, Briet OJ, Hardy D, Chitnis N, Maire N, Pasquale AD, Smith TA: Modelling the cost-effectiveness of mass screening and treatment for reducing Plasmodium falciparum malaria burden. Malar J 2013, 12:4. BioMed Central Full Text
- [20]Mapping Malaria Risk in Africa (MARA) Collaboration: Burkina Faso: Duration of the Malaria Transmission Season. http://www.mara.org.za webcite
- [21]Tiono AB, Ouedraogo A, Ogutu B, Diarra A, Coulibaly B, Gansane A, Sirima SB, O'Neil G, Mukhopadhyay A, Hamed K: A controlled, parallel, cluster-randomized trial of community-wide screening and treatment of asymptomatic carriers of Plasmodium falciparum in Burkina Faso. Malar J 2013, 12:79. BioMed Central Full Text
- [22]WHO: Manual on Practical Entomology in Malaria (Part 2). http://whqlibdoc.who.int/offset/WHO_OFFSET_13_(part2).pdf webcite
- [23]Burkot TR, Williams JL, Schneider I: Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Am J Trop Med Hyg 1984, 33:783-788.
- [24]Wirtz RA, Burkot TR, Graves PM, Andre RG: Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol 1987, 24:433-437.
- [25]Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, Koech DK: Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 1988, 25:9-16.
- [26]Fanello C, Santolamazza F, della TA: Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol 2002, 16:461-464.
- [27]Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D: Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 1998, 7:179-184.
- [28]Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH: Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 2000, 9:491-497.
- [29]Males S, Gaye O, Garcia A: Long-term asymptomatic carriage of Plasmodium falciparum protects from malaria attacks: a prospective study among Senegalese children. Clin Infect Dis 2008, 46:516-522.
- [30]Ouedraogo A, Tiono AB, Diarra A, Nebie IO, Konate AT, Sirima SB: The effects of a pre-season treatment with effective antimalarials on subsequent malaria morbidity in under five-year-old children living in high and seasonal malaria transmission area of Burkina Faso. Trop Med Int Health 2010, 15:1315-1321.
- [31]Konate AT, Yaro JB, Ouedraogo AZ, Diarra A, Gansane A, Soulama I, Kangoye DT, Kabore Y, Ouedraogo E, Ouedraogo A, et al.: Morbidity from malaria in children in the year after they had received intermittent preventive treatment of malaria: a randomised trial. PLoS One 2011, 6:e23391.
- [32]Farnert A, Rooth I, Svensson , 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.
- [33]Kinyanjui SM, Conway DJ, Lanar DE, Marsh K: IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar J 2007, 6:82. BioMed Central Full Text
- [34]Doolan DL, Dobano C, Baird JK: Acquired immunity to malaria. Clin Microbiol Rev 2009, 22:13-36.
- [35]Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, Nebie I, Roeffen W, Verhave JP, Luty AJF, et al.: Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PloS One 2009, 4:e8410.
- [36]Ouedraogo AL, Roeffen W, Luty AJ, de Vlas SJ, Nebie I, Ilboudo-Sanogo E, Cuzin-Ouattara N, Teleen K, Tiono AB, Sirima SB, et al.: Naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs48/45 and Pfs230 in an area of seasonal transmission. Infect Immun 2011, 79:4957-4964.
- [37]Ilboudo-Sanogo E, Tiono BA, Sagnon N, Cuzin ON, Nebie I, Sirima SB: Temporal dynamics of malaria transmission in two rural areas of Burkina Faso with two ecological differences. J Med Entomol 2010, 47:618-624.
- [38]Ilboudo-Sanogo E, Cuzin-Ouattara N, Diallo DA, Cousens SN, Esposito F, Habluetzel A, Sanon S, Ouedraogo AP: Insecticide-treated materials, mosquito adaptation and mass effect: entomological observations after five years of vector control in Burkina Faso. Trans R Soc Trop Med Hyg 2001, 95:353-360.
- [39]Curtis CF, Jana-Kara B, Maxwell CA: Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and pyrethroid resistance. J Vector Borne Dis 2003, 40:1-8.
- [40]Badolo A, Traore A, Jones CM, Sanou A, Flood L, Guelbeogo WM, Ranson H, Sagnon N: Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise? Malar J 2012, 11:232. BioMed Central Full Text
- [41]Eziefula AC, Gosling R, Hwang J, Hsiang MS, Bousema T, von Seidlein L, Drakeley C, Primaquine in Africa Discussion Group: Rationale for short course primaquine in Africa to interrupt malaria transmission. Malar J 2012, 11:360. BioMed Central Full Text
- [42]Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, Foy BD: Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J 2013, 12:153. BioMed Central Full Text