Serological evidence of vector and parasite exposure in Southern Ghana: The dynamics of malaria transmission intensity

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Badu, Kingsley ^a   Gyan, Ben ^a   Appawu, Maxwell ^a   Mensah, Daniel ^a   Dodoo, Daniel ^a   Yan, Guiyun ^b   Drakeley, Chris ^c   Zhou, Guofa ^b   Owusu Dabo, Ellis ^d   Koram, Kwadwo Ansah ^a  

^a University of Ghana   (Ghana)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d KUMASI CENTRE FOR COLLABORATIVE RESEARCH IN TROPICAL MEDICINE   (Ghana)

Author keywords

Anopheles gambiae; Malaria exposure; Merozoite surface protein; Parasite prevalence; Salivary peptide; Seroconversion rate; Seroprevalence

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; GSG6-P1 PEPTIDE, HUMAN; MEROZOITE SURFACE PROTEIN 1; SALIVA PROTEIN;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANOPHELES GAMBIAE; ANTIGEN SPECIFICITY; ARTICLE; CHILD; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GHANA; HUMAN; IMMUNOGENICITY; MALARIA; MALARIA CONTROL; PARASITE CLEARANCE; PARASITE EXPOSURE; PARASITE PREVALENCE; RANDOMIZED CONTROLLED TRIAL; SEROCONVERSION; SEROEPIDEMIOLOGY; SEROPREVALENCE; VECTOR EXPOSURE; ANIMAL; BLOOD; IMMUNOLOGY; INSECT BITE; MALARIA, FALCIPARUM; METABOLISM; PRESCHOOL CHILD; TRANSMISSION; YOUNG ADULT;

ANOPHELES GAMBIAE;

ADOLESCENT; ADULT; ANIMALS; ANOPHELES GAMBIAE; CHILD; CHILD, PRESCHOOL; GHANA; HUMANS; IMMUNOGLOBULIN G; INSECT BITES AND STINGS; MALARIA; MALARIA, FALCIPARUM; MEROZOITE SURFACE PROTEIN 1; SALIVARY PROTEINS AND PEPTIDES; SEROEPIDEMIOLOGIC STUDIES; YOUNG ADULT;

EID: 85043225273     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-0861-y     Document Type: Article

References (53)

1. Feachem RGA, Phillips AA, Hwang J, Cotter C, Wielgosz B, Greenwood BM, et al. Shrinking the malaria map: progress and prospects. Lancet. 2010;376:1566-78. doi:10.1016/S0140-6736(10)61270-6.
2. James S, Takken W, Collins FH, Gottlieb M. Perspective piece: needs for monitoring mosquito transmission of malaria in a Pre-elimination world. Am J Trop Med Hyg. 2014;90:6-10. doi:10.4269/ajtmh.13-0175.
3. Alonso PL, Brown G, Arevalo-herrera M, Binka F, Chitnis C, Collins F, et al. A research agenda to underpin malaria eradication. PLoS Med. 2011;8:e1000406. doi:10.1371/journal.pmed.1000406.
4. Bousema T, Kreuels B, Gosling R. Adjusting for heterogeneity of malaria transmission in longitudinal studies. J Infect Dis. 2011;204:1-3. doi:10.1093/infdis/jir225.
5. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:1-7. doi:10.1371/journal.pmed.1001165.
6. Rotllant G, Bhattarai A, Stro J, Kahigwa E, Garcia M, Petzold M, et al. Influence of rapid malaria diagnostic tests on treatment and health outcome in fever patients, Zanzibar - a crossover validation study. PLoS Med. 2009;6:e1000070.
7. Clark TD, Greenhouse B, Njama-meya D, Nzarubara B, Maiteki-sebuguzi C, Maiteki-Sebuguzi N, et al. factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis. 2008;198:393-400. doi:10.1086/589778.
8. Hay SI, Rogers DJ, Toomer JF, Snow RW. Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg. 2000;94:113-27.
9. Kelly-hope LA, Mckenzie FE. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009;8:19. doi:10.1186/1475-2875-8-19.
10. Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010;9:62.
11. Beier JC, Killeen GF, Githure JI. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg. 2009;61:109-13.
12. Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg. 2007;77 Suppl 6:119-27.
13. Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, et al. Serologic markers for detecting malaria in areas of low endemicity. Emerg Infect Dis. 2010;16:392-9. doi:10.3201/eid1603.090732.
14. Badu K, Afrane YA, Larbi J, Stewart VN, Waitumbi J, Angov E, et al. Marked variation in MSP-119 antibody responses to malaria in western Kenyan highlands. BMC Infect Dis. 2012;12:50. doi:10.1186/1471-2334-12-50.
15. Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575-82. doi:10.1016/j.pt. 2007. 08. 023.
16. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, Mcdonald SLR, Malima R, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005;102:5108-13.
17. Cook J, Kleinschmidt I, Schwabe C, Nseng G, Bousema T, Corran PH, Riley EM, Drakeley CJ. Serological Markers Suggest Heterogeneity of Effectiveness of Malaria Control Interventions on Bioko Island, Equatorial Guinea. PLoS ONE 6(9): e25137. doi:10.1371/journal.pone.0025137.
18. Drakeley C, Cook J. Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. In: David Rollinson D, Hay SI, editors. Advances in Parasitology. Burlington: Academic Press; 2009. p. 299-352.
19. Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, et al. Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 2005;191:1589-98.
20. Badu K, Siangla J, Larbi J, Lawson BW, Afrane Y, Ong'echa J, et al. Variation in exposure to Anopheles gambiae salivary gland peptide (gSG6-P1) across different malaria transmission settings in the western Kenya highlands. Malar J. 2012;11:318.
21. Ribeiro JM, Makoul GT, Levine J, Robinson DR. Spielman A Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. J Exp Med. 1985;161:332-44.
22. Ribeiro JM. Blood-feeding arthropods: live syringes or invertebrate pharmacologists ? Infect Agents Dis. 1995;4(3):143-52.
23. Drame PM, Poinsignon A, Marie A, Noukpo H, Doucoure S, Cornelie S, et al. New Salivary Biomarkers of Human Exposure to Malaria Vector Bites, Anopheles mosquitoes - New insights into malaria vectors, Sylvie Manguin, Editor. ISBN: 978-953-51-1188-7, InTech, DOI:10.5772/55613. http://www.intechopen.com/books/anopheles-mosquitoes-new-insights-into-malaria-vectors/new-salivary-biomarkers-of-human-exposure-to-malaria-vector-bites
24. Dama E, Cornelie S, Bienvenu M, Camara M, Kambire R, Jamonneau C, et al. Bucheton AMB Identification of Glossina palpalis gambiensis specific salivary antigens: towards the development of a serologic biomarker of human exposure to tsetse flies in West Africa. Microb Infect. 2013;15:416-27.
25. Nascimento RJ, Santana JM, Lozzi SP, Araujo CN, Teixeira AR. Human IgG1 and IgG4: the main antibodies against Triatoma infestans (Hemiptera: Reduviidae) salivary gland proteins. Am J Trop Med Hyg. 2001;65:219-26.
26. Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, et al. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg. 2000;62:740-5.
27. Stone W, Bousema T, Jones S, Gesase S, Hashim R, Gosling R, et al. IgG responses to Anopheles gambiae salivary antigen gSG6 detect variation in exposure to malaria vectors and disease risk. PLoS One. 2012;7(6):e40170. doi:10.1371/journal.pone.0040170.
28. Remoue F, Cisse B, Ba F, Sokhna C, Herve JP, Boulanger D, et al. Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Trans R Soc Trop Med Hyg. 2006;100:363-70. doi:10.1016/j.trstmh.2005.06.032.
29. Lombardo F, Ronca R, Rizzo C, Fiorentino G, Bourgouin C. The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem &Mol Bio. 2009;39:457-66. doi:10.1016/j.ibmb.2009.04.006.
30. Poinsignon A, Cornelie S, Lanfrancotti A, Rossignol M, Boulanger D, Cisse B, et al. Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to anopheles bites. PLoS One. 2008;3:e2472. doi:10.1371/journal.pone.0002472.
31. Sagna AB, Sarr JB, Gaayeb L, Drame PM, Ndiath MO, Senghor S, et al. gSG6-P1 salivary biomarker discriminates micro-geographical heterogeneity of human exposure to Anopheles bites in low and seasonal malaria areas. Parasites & Vectors. 2013;6:68. doi:10.1186/1756-3305-6-68.
32. Drame PM, Poinsignon A, Besnard P, Cornelie S, Le MJ, Toto JL, et al. Human antibody responses to the Anopheles salivary gSG6-P1 peptide: a novel tool for evaluating the efficacy of ITNs in malaria vector control. PLoS One. 2010;5(12):e15596. doi:10.1371/journal.pone.0015596.
33. Adu B, Dodoo D, Adukpo S, Hedley PL, Arthur FKN, Gerd AT, et al. Fc gamma receptor IIIB (FccRIIIB) polymorphisms are associated with clinical malaria in Ghanaian children. PLoS One. 2012;7(9):e46197. doi:10.1371/journal.pone.0046197.
34. Afari EA, Appawu M, Dunyo S, Baffoe-Wilmot A, Nkrumah FK. Malaria infection, morbidity and transmission in two ecological zones Southern Ghana. Afr J Health Sci. 1995;2:312-5.
35. Akua I, Ansah E, Gyapong M, Adjei S, Barnish G, Evans D. Strategies to improve adherence to recommended chloroquine treatment regimes: a quasi-experiment in the context of integrated primary health care delivery in Ghana. Soc Sci Med. 2002;55:2215-26.
36. Tay SCK, Badu K, Mensah AA, Gbedema SY. The prevalence of malaria among HIV seropositive individuals and the impact of the co- infection on their hemoglobin levels. Ann Clin MicroB Antimicrob. 2015;14:10. doi:10.1186/s12941-015-0064-6.
37. Kusi KA, Bosomprah S, Dodoo D, Kyei-baafour E, Dickson EK, Mensah D, et al. Anti-sporozoite antibodies as alternative markers for malaria transmission intensity estimation. Malar J. 2014;9:317.
38. Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151-208. doi:10.1016/B978-0-12-800099-1.00003-X.
39. Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, et al. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010;9:169.
40. Drame PM, Diallo A, Poinsignon A, Boussari O, Dos S, Machault V. Evaluation of the effectiveness of malaria vector control measures in urban settings of Dakar by a specific anopheles salivary biomarker. PLoS One. 2013;8(6):e66354. doi:10.1371/journal.pone.0066354.
41. Rizzo C, Ronca R, Fiorentino G, Verra F, Mangano V, Poinsignon A, et al. Humoral response to the anopheles gambiae salivary protein gSG6: a serological indicator of exposure to afrotropical malaria vectors. PLoS One. 2011;6:e17980. doi:10.1371/journal.pone.0017980.
42. Orlandi-Pradines E, Almeras L, Denisde Senneville L, Barbe S, Remoué F, Villard C, et al. Antibody response against saliva antigens of Anopheles gambiae and Aedes aegypti in travellers in tropical Africa. Microbes Infect. 2007;9(12-13):1454-62.
43. Ambrosino E, Dumoulin C, Orlandi-Pradines E, Remoue F, Toure-Baldé A, Tall A, et al. A multiplex assay for the simultaneous detection of antibodies against 15 Plasmodium falciparum and Anopheles gambiae saliva antigens. Malar J. 2010;9:317. doi:10.1186/1475-2875-9-317.
44. Zhao X, Chen F, Feng Z, Li X, Zhou X. The temporal lagged association between meteorological factors and malaria in 30 counties in south-west China: a multilevel distributed lag non-linear analysis. Malar J. 2014;13:57. doi:10.1186/1475-2875-13-57.
45. Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, et al. Rapid assessment of malaria transmission using Age- specific sero-conversion rates. 2009. p. 4. doi:10.1371/journal.pone.0006083.
46. Drame PM, Poinsignon A, Besnard P, Le Mire J, Dos-santos MA, Sow CS, et al. Human antibody response to anopheles gambiae saliva: an immuno-epidemiological biomarker to evaluate the efficacy of insecticide-treated nets in malaria vector control. Am J Trop Med Hyg. 2010;83(1):115-21. doi:10.4269/ajtmh.2010.09-0684.
47. Sagna AB, Gaayeb L, Sarr JB, Senghor S, Poinsignon A, Boutouaba-Combe S, et al. Plasmodium falciparum infection during dry season: IgG responses to Anopheles gambiae salivary gSG6-P1 peptide as sensitive biomarker for malaria risk in Northern Senegal. Malar J. 2013;12:301. doi:10.1186/1475-2875-12-301.
48. Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum Spatial Analysis, Western Kenya Highlands. Emerg Infect Dis. 2005;11:1571-7.
49. Smith DL, Guerra CA, Snow RW, Hay SI. Standardizing estimates of the Plasmodium falciparum parasite rate. Malar J. 2007;6:131. doi:10.1186/1475-2875-6-131.
50. Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, Githure JI, et al. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J. 2006;5:107. doi:10.1186/1475-2875-5-107.
51. Hay SI, Smith DL, Snow RW, Gates M. Measuring malaria endemicity from intense to interrupted transmission. 378. 2008;8:369. doi:10.1016/S1473- 3099(08)70069-0.
52. Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, et al. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008;7:195. doi:10.1186/1475-2875-7-195.
53. Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G. Protein microarray analysis of antibody responses to Plasmodium falciparum in western Kenyan highland sites with differing transmission levels. PLoS One. 2013;8:e82246.