Implementation and application of a multiplex assay to detect malaria-specific antibodies: a promising tool for assessing malaria transmission in Southeast Asian pre-elimination areas

Malaria Journal

Volumn 14, Issue 1, 2015, Pages

  Kerkhof, Karen ^a,b   Canier, Lydie ^c   Kim, Saorin ^c   Heng, Somony ^d   Sochantha, Tho ^d   Sovannaroth, Siv ^d   Vigan Womas, Inès ^e   Coosemans, Marc ^a,b   Sluydts, Vincent ^a,b   Ménard, Didier ^c   Durnez, Lies ^a  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^d National Centre for Parasitology Entomology and Malaria Control   (Cambodia)

^e INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

Author keywords

Cambodia; Malaria; Multiplex immunoassay; Serological markers

Indexed keywords

RECOMBINANT PROTEIN; SALIVA PROTEIN; PROTOZOON ANTIBODY;

ANALYTIC METHOD; ANOPHELES GAMBIAE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; BLOOD SAMPLING; CAMBODIA; CATALYSIS; DISEASE TRANSMISSION; HUMAN; IMMUNOASSAY; MALARIA; MALARIA CONTROL; MALARIA FALCIPARUM; MONOPLEX ASSAY; MULTIPLEX ASSAY; MULTIPLEX BEAD BASED IMMUNOASSAY; PLASMODIUM; PLASMODIUM VIVAX MALARIA; QUALITY CONTROL; SEROCONVERSION; SEROLOGY; SOUTHEAST ASIAN; ADOLESCENT; ADULT; AGED; BLOOD; CHILD; IMMUNOLOGY; INFANT; MALARIA, FALCIPARUM; MALARIA, VIVAX; MIDDLE AGED; PARASITOLOGY; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PRESCHOOL CHILD; PROCEDURES; REPRODUCIBILITY; TRANSMISSION; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, PROTOZOAN; CAMBODIA; CHILD; CHILD, PRESCHOOL; HUMANS; IMMUNOASSAY; INFANT; MALARIA, FALCIPARUM; MALARIA, VIVAX; MIDDLE AGED; PARASITOLOGY; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; REPRODUCIBILITY OF RESULTS; YOUNG ADULT;

EID: 85016924260     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-0868-z     Document Type: Article

References (56)

1. WHO. World malaria report 2013. Geneva: World Health Organization; 2013.
2. Bousema T, Stevenson J, Baidjoe A, Stresman G, Griffin JT, Kleinschmidt I, et al. The impact of hotspot-targeted interventions on malaria transmission: study protocol for a cluster-randomized controlled trial. Trials. 2013;14:36.
3. 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.
4. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SLR, Carneiro I, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA. 2005;102:5108-13.
5. 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.
6. Tangpukdee N, Duangdee C, Wilairatana P, Krudsood S. Malaria diagnosis: a brief review. Korean J Parasitol. 2009;47:93-102.
7. Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575-82.
8. Drakeley C, Cook J. Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. Adv Parasitol. 2009;69:299-352.
9. Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, et al. Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012;11:86.
10. Arnold BF, Priest JW, Hamlin KL, Moss DM, Colford JM, Lammie PJ. Serological measures of malaria transmission in Haiti: comparison of longitudinal and cross-sectional methods. PLoS One. 2014;9:e93684.
11. Von Fricken ME, Weppelmann TA, Lam B, Eaton WT, Schick L, Masse R, et al. Age-specific malaria seroprevalence rates: a cross-sectional analysis of malaria transmission in the Ouest and Sud-Est departments of Haiti. Malar J. 2014;13:361.
12. Noor AM, Mohamed MB, Mugyenyi CK, Osman MA, Guessod HH, Kabaria CW, et al. Establishing the extent of malaria transmission and challenges facing pre-elimination in the Republic of Djibouti. BMC Infect Dis. 2011;11:121.
13. Voller A. Fluorescent antibody methods and their use in malaria research. Bull World Health Organ. 1964;30:343-54.
14. She RC, Rawlins ML, Mohl R, Perkins SL, Hill HR, Litwin CM. Comparison of immunofluorescence antibody testing and two enzyme immunoassays in the serologic diagnosis of malaria. J Travel Med. 2007;14:105-11.
15. Fouda GG, Leke RFG, Long C, Druilhe P, Zhou A, Taylor DW, et al. Multiplex assay for simultaneous measurement of antibodies to multiple Plasmodium falciparum antigens. Clin Vaccine Immunol. 2006;13:1307-13.
16. Fernandez-Becerra C, Sanz S, Brucet M, Stanisic DI, Alves FP, Camargo EP, et al. Naturally-acquired humoral immune responses against the N- and C-termini of the Plasmodium vivax MSP1 protein in endemic regions of Brazil and Papua New Guinea using a multiplex assay. Malar J. 2010;9:29.
17. Ondigo BN, Park GS, Gose SO, Ho BM, Ochola LA, Ayodo GO, et al. Standardization and validation of a cytometric bead assay to assess antibodies to multiple Plasmodium falciparum recombinant antigens. Malar J. 2012;11:427.
18. Lammie PJ, Moss DM, Brook Goodhew E, Hamlin K, Krolewiecki A, West SK, et al. Development of a new platform for neglected tropical disease surveillance. Int J Parasitol. 2012;42:797-800.
19. Sluydts V, Heng S, Coosemans M, Van Roey K, Gryseels C, Canier L, et al. Spatial clustering and risk factors of malaria infections in Ratanakiri Province, Cambodia. Malar J. 2014;13:387.
20. Canier L, Khim N, Kim S, Sluydts V, Heng S, Dourng D, et al. An innovative tool for moving malaria PCR detection of parasite reservoir into the field. Malar J. 2013;12:405.
21. Luminex Corporation. xMAP Antibody Coupling Kit User Manual. http://www.luminexcorp.com/Products/ReagentsMicrospheres/xMAPAntibodyCouplingKit/. 2011.
22. Corporation Luminex. Description and operation of the luminex technology. Austin: Texas, USA; 2012. p. 20.
23. Luminex Corporation. Fundamental assay techniques protein training (CN-0164-01). http://www.cvent.com/events/luminex-learning-customer-education-event/eventsummary-2476c07b727540f6a1c1bdb34e400694.aspx. 2012.
24. Khaireh BA, Briolant S, Pascual A, Mokrane M, Machault V, Travaillé C, et al. Plasmodium vivax and Plasmodium falciparum infections in the Republic of Djibouti: evaluation of their prevalence and potential determinants. Malar J. 2012;11:395.
25. Sarr JB, Orlandi-Pradines E, Fortin S, Sow C, Cornelie S, Rogerie F, et al. Assessment of exposure to Plasmodium falciparum transmission in a low endemicity area by using multiplex fluorescent microsphere-based serological assays. Parasit Vectors. 2011;4:212.
26. Luminex Corporation. xMap technology. http://www.luminexcorp.com/TechnologiesScience/xMAPTechnology/#. 2012.
27. Van Gageldonk PGM, van Schaijk FG, van der Klis FR, Berbers GAM. Development and validation of a multiplex immunoassay for the simultaneous determination of serum antibodies to Bordetella pertussis, diphtheria and tetanus. J Immunol Methods. 2008;335:79-89.
28. R Core Team. R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria. 2014. http://www.R-project.org/.
29. Dudoit S, Van Der Laan MJ. Asymptotics of cross-validated risk estimation in estimator selection and performance assessment. Stat Methodol. 2005;2:131-54.
30. 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. PLoS One. 2009;4:e6083.
31. Ferbas J, Thomas J, Hodgson J, Gaur A, Casadevall N, Swanson SJ. Feasibility of a multiplex flow cytometric bead immunoassay for detection of anti-epoetin alfa antibodies. Clin Vaccine Immunol. 2007;14:1165-72.
32. Helb DA, Tetteh KKA, Felgner PL, Skinner J, Hubbard A, Arinaitwe E, et al. Novel serologic biomarkers provide accurate estimates of recent Plasmodium falciparum exposure for individuals and communities. Proc Natl Acad Sci USA. 2015;112:4438-47.
33. Cham GKK, Kurtis J, Lusingu J, Theander TG, Jensen ATR, Turner L. A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malar J. 2008;7:108.
34. Khim N, Siv S, Kim S, Mueller T, Fleischmann E, Singh B, et al. Plasmodium knowlesi Infection in Humans, Cambodia, 2007-2010. Emerg Infect Dis. 1900;2011:17.
35. Binnicker MJ, Jespersen DJ, Harring JA, Rollins LO, Beito EM. Evaluation of a multiplex flow immunoassay for detection of epstein-barr virus-specific antibodies. Clin Vaccine Immunol. 2008;15:1410-3.
36. Drummond JE, Shaw EE, Antonello JM, Green T, Page GJ, Motley CO, et al. Design and optimization of a multiplex anti-influenza peptide immunoassay. J Immunol Methods. 2008;334:11-20.
37. Whelan C, Shuralev E, O'Keeffe G, Hyland P, Kwok HF, Snoddy P, et al. Multiplex immunoassay for serological diagnosis of Mycobacterium bovis infection in cattle. Clin Vaccine Immunol. 2008;15:1834-8.
38. Michel A, Waterboer T, Kist M, Pawlita M. Helicobacter pylori multiplex serology. Helicobacter. 2009;14:525-35.
39. Elshal MF, McCoy JP. Multiplex bead array assays: performance evaluation and comparison of sensitivity to ELISA. Methods. 2006;38:317-23.
40. Ondigo BN, Hodges JS, Ireland KF, Magak NG, Lanar DE, Dutta S, et al. Estimation of recent and long-term malaria transmission in a population by antibody testing to multiple Plasmodium falciparum antigens. J Infect Dis. 2014;210:1123-32.
41. Scholzen A, Sauerwein RW. How malaria modulates memory: activation and dysregulation of B cells in Plasmodium infection. Trends Parasitol. 2013;29:252-62.
42. Taylor RR, Egan A, McGuinness D, Jepson A, Adair R, Drakely C, et al. Selective recognition of malaria antigens by human serum antibodies is not genetically determined but demonstrates some features of clonal imprinting. Int Immunol. 1996;8:905-15.
43. Muench H Jr. Catalytic Models in Epidemiology. 1st ed. Cambridge: Harvard University Press; 1959.
44. Hens N, Shkedy Z, Aerts M, Faes C, Van Damme P, Beutels P. Modeling infectious disease parameters based on serological and social contact data. New York, Heidelberg, Dordrecht, London: Springer; 2012.
45. Sutherland CJ. Surface antigens of Plasmodium falciparum gametocytes - a new class of transmission-blocking vaccine targets? Mol Biochem Parasitol. 2009;166:93-8.
46. Vigan-Womas I, Guillotte M, Juillerat A, Vallieres C, Lewit-Bentley A, Tall A, et al. Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS One. 2011;6:e16544.
47. Greenwood BM, Bojang K, Whitty CJM, Targett GAT. Malaria. Lancet. 2005;365:1487-98.
48. Fidock A, Gras-Masse H, Lepers J, Brahimi K, Benmohamed L, Mellouk S, et al. Liver stage antigen-1 is well conserved and contains potent B and T cell determinants. J Immunol. 1994;153:190-204.
49. Theisen M, Vuust J, Gottschau A, Jepsen S, Høgh B. Antigenicity and immunogenicity of recombinant glutamate-rich protein of Plasmodium falciparum expressed in Escherichia coli. Clin Diagn Lab Immunol. 1995;2:30-4.
50. Theisen M, Soe S, Jessing SG, Meng L, Oeuvray C, Druilhe P, Jepsen S. Identification of a major B-cell epitope of the Plasmodium falciparum glutamate-rich protein (GLURP), targeted by human antibodies mediating parasite killing. Vaccine. 2001;19:204-12.
51. Henry-Halldin CN, Sepe D, Susapu M, McNamara DT, Bockarie M, King CL, et al. High-throughput molecular diagnosis of circumsporozoite variants VK210 and VK247 detects complex Plasmodium vivax infections in malaria endemic populations in Papua New Guinea. Infect Genet Evol. 2011;11:391-8.
52. Cheng Y, Ito D, Sattabongkot J, Lim CS, Kong DH, Ha KS, et al. Serological responses to a soluble recombinant chimeric Plasmodium vivax circumsporozoite protein in VK210 and VK247 population. Malar J. 2013;12:323.
53. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, Crabb BS, et al. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol. 2000;38:706-18.
54. Yildiz Zeyrek F, Palacpac N, Yuksel F, Yagi M, Honjo K, Fujita Y, et al. Serologic markers in relation to parasite exposure history help to estimate transmission dynamics of Plasmodium vivax. PLoS One. 2011;6:e28126.
55. Menard D, Chan ER, Benedet C, Ratsimbasoa A, Kim S, Chim P, et al. Whole genome sequencing of field isolates reveals a common duplication of the Duffy binding protein gene in Malagasy Plasmodium vivax strains. PLoS Negl Trop Dis. 2013;7:e2489.
56. Poinsignon A, Cornelie S, Mestres-Simon M, Lanfrancotti A, Rossignol M, Boulanger D, et al. Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS One. 2008;3:e2472.