malERA: An updated research agenda for characterising the reservoir and measuring transmission in malaria elimination and eradication

1. malERA Consultative Group on Integration Strategies. A research agenda for malaria eradication: cross-cutting issues for eradication. PLoS Med. 2011;8(1):e1000404. doi: 10.1371/journal.pmed.1000404 21283603

2. malERA Consultative Group on Monitoring ES. A research agenda for malaria eradication: monitoring, evaluation, and surveillance. PLoS Med. 2011;8(1):e1000400. doi: 10.1371/journal.pmed.1000400 21311581

3. World Health Organization. WHO malaria terminology Geneva: WHO; 2016. http://apps.who.int/iris/bitstream/10665/208815/1/WHO_HTM_GMP_2016.6_eng.pdf?ua=1.

4. Schapira A, Boutsika K. Malaria ecotypes and stratification. Adv Parasitol. 2012;78:97–167. doi: 10.1016/B978-0-12-394303-3.00001-3 22520442

5. Nájera J, Liese B, Hammer J. Malaria: new patterns and perspectives Washington, DC: The World Bank; 1992. http://documents.worldbank.org/curated/en/933151468740676854/pdf/multi-page.pdf.

6. World Health Organization. Malaria rapid diagnostic test performance Geneva: WHO; 2015. http://apps.who.int/iris/bitstream/10665/204118/1/9789241510035_eng.pdf?ua=1.

7. The malERA Refresh Consultative Panel on Combination Interventions and Modelling. malERA: An updated research agenda for combination interventions and modelling in malaria elimination and eradication. PLoS Med. 2017;14(11):e1002453. https://doi.org/10.1371/journal.pmed.1002453

8. Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, et al. "Asymptomatic" malaria: A chronic and debilitating infection that should be treated. PLoS Med. 2016;13(1):e1001942. doi: 10.1371/journal.pmed.1001942 26783752

9. Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12(12):833–40. doi: 10.1038/nrmicro3364 25329408

10. Wu L, van den Hoogen LL, Slater H, Walker PG, Ghani AC, Drakeley CJ, et al. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature. 2015;528(7580):S86–93. doi: 10.1038/nature16039 26633770

11. Cheng Q, Cunningham J, Gatton ML. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis. 2015;9(1):e3413. doi: 10.1371/journal.pntd.0003413 25569135

12. Moreira CM, Abo-Shehada M, Price RN, Drakeley CJ. A systematic review of sub-microscopic Plasmodium vivax infection. Malar J. 2015;14:360. doi: 10.1186/s12936-015-0884-z 26390924

13. Imwong M, Hanchana S, Malleret B, Renia L, Day NP, Dondorp A, et al. High-throughput ultrasensitive molecular techniques for quantifying low-density malaria parasitemias. J Clin Microbiol. 2014;52(9):3303–9. doi: 10.1128/JCM.01057-14 24989601

14. Robinson LJ, Wampfler R, Betuela I, Karl S, White MT, Li Wai Suen CS, et al. Strategies for understanding and reducing the Plasmodium vivax and Plasmodium ovale hypnozoite reservoir in Papua New Guinean children: a randomised placebo-controlled trial and mathematical model. PLoS Med. 2015;12(10):e1001891. doi: 10.1371/journal.pmed.1001891 26505753

15. Douglas NM, Simpson JA, Phyo AP, Siswantoro H, Hasugian AR, Kenangalem E, et al. Gametocyte dynamics and the role of drugs in reducing the transmission potential of Plasmodium vivax. J Infect Dis. 2013;208(5):801–12. doi: 10.1093/infdis/jit261 23766527

16. Anvikar AR, Shah N, Dhariwal AC, Sonal GS, Pradhan MM, Ghosh SK, et al. Epidemiology of Plasmodium vivax malaria in India. Am J Trop Med Hyg. 2016.

17. Llanos-Cuentas A, Lacerda MV, Rueangweerayut R, Krudsood S, Gupta SK, Kochar SK, et al. Tafenoquine plus chloroquine for the treatment and relapse prevention of Plasmodium vivax malaria (DETECTIVE): a multicentre, double-blind, randomised, phase 2b dose-selection study. Lancet. 2014;383(9922):1049–58. doi: 10.1016/S0140-6736(13)62568-4 24360369

18. The malERA Refresh Consultative Panel on Tools for Malaria Elimination. malERA: An updated research agenda for diagnostics, drugs, vaccines, and vector control in malaria elimination and eradication. PLoS Med. 2017;14(11):e1002455. https://doi.org/10.1371/journal.pmed.1002455

19. Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11(6):623–39. doi: 10.1586/eri.13.45 23750733

20. Greenwood BM. Asymptomatic malaria infections—do they matter? Parasitol Today. 1987;3(7):206–14. 15462957

21. World Health Organization. Global technical strategy for malaria 2016–2030 Geneva: WHO; 2015. http://apps.who.int/iris/bitstream/10665/176712/1/9789241564991_eng.pdf.

22. Tiono AB, Ouedraogo A, Ogutu B, Diarra A, Coulibaly S, Gansane A, et al. 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. doi: 10.1186/1475-2875-12-79 23442748

23. The malERA Refresh Consultative Panel on Health Systems and Policy Research. malERA: An updated research agenda for health systems and policy research in malaria elimination and eradication. PLoS Med. 2017;14(11):e1002454. https://doi.org/10.1371/journal.pmed.1002454

24. Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30(4):183–90. doi: 10.1016/j.pt.2014.02.004 24642035

25. Churcher TS, Trape JF, Cohuet A. Human-to-mosquito transmission efficiency increases as malaria is controlled. Nat Commun. 2015;6:6054. doi: 10.1038/ncomms7054 25597498

26. Bousema T, Dinglasan RR, Morlais I, Gouagna LC, van Warmerdam T, Awono-Ambene PH, et al. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS ONE. 2012;7(8):e42821. doi: 10.1371/journal.pone.0042821 22936993

27. Churcher TS, Bousema T, Walker M, Drakeley C, Schneider P, Ouedraogo AL, et al. Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. Elife. 2013;2:e00626. doi: 10.7554/eLife.00626 23705071

28. Ouédraogo AL, Guelbéogo WM, Cohuet A, Morlais I, King JG, Gonçalves BP, et al. A protocol for membrane feeding assays to determine the infectiousness of P. falciparum naturally infected individuals to Anopheles gambiae. MWJ. 2013;4(16):1–4.

29. Ouedraogo AL, Goncalves BP, Gneme A, Wenger EA, Guelbeogo MW, Ouedraogo A, et al. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2016;213(1):90–9. doi: 10.1093/infdis/jiv370 26142435

30. Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22(9):424–30. doi: 10.1016/j.pt.2006.07.001 16846756

31. Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76(3):470–4. 17360869

32. Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, et al. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology. 1988;96 (Pt 2):251–63.

33. Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4(12):e8410. doi: 10.1371/journal.pone.0008410 20027314

34. Pethleart A, Prajakwong S, Suwonkerd W, Corthong B, Webber R, Curtis C. Infectious reservoir of Plasmodium infection in Mae Hong Son Province, north-west Thailand. Malar J. 2004;3:34. doi: 10.1186/1475-2875-3-34 15385050

35. Slater HC, Ross A, Ouedraogo AL, White LJ, Nguon C, Walker PG, et al. Assessing the impact of next-generation rapid diagnostic tests on Plasmodium falciparum malaria elimination strategies. Nature. 2015;528(7580):S94–101. doi: 10.1038/nature16040 26633771

36. Schneider P, Reece SE, van Schaijk BC, Bousema T, Lanke KH, Meaden CS, et al. Quantification of female and male Plasmodium falciparum gametocytes by reverse transcriptase quantitative PCR. Mol Biochem Parasitol. 2015;199(1–2):29–33. doi: 10.1016/j.molbiopara.2015.03.006 25827756

37. Zhou Z, Mitchell RM, Kariuki S, Odero C, Otieno P, Otieno K, et al. Assessment of submicroscopic infections and gametocyte carriage of Plasmodium falciparum during peak malaria transmission season in a community-based cross-sectional survey in western Kenya, 2012. Malar J. 2016;15(1):421. doi: 10.1186/s12936-016-1482-4 27543112

38. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24(2):377–410. doi: 10.1128/CMR.00051-10 21482730

39. Lin JT, Ubalee R, Lon C, Balasubramanian S, Kuntawunginn W, Rahman R, et al. Microscopic Plasmodium falciparum gametocytemia and infectivity to mosquitoes in Cambodia. J Infect Dis. 2016;213(9):1491–4. doi: 10.1093/infdis/jiv599 26667316

40. Trape JF, Tall A, Sokhna C, Ly AB, Diagne N, Ndiath O, et al. The rise and fall of malaria in a West African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis. 2014;14(6):476–88. doi: 10.1016/S1473-3099(14)70712-1 24813159

41. Kangoye DT, Noor A, Midega J, Mwongeli J, Mkabili D, Mogeni P, et al. Malaria hotspots defined by clinical malaria, asymptomatic carriage, PCR and vector numbers in a low transmission area on the Kenyan Coast. Malar J. 2016;15:213. doi: 10.1186/s12936-016-1260-3 27075879

42. Mwakalinga VM, Sartorius BK, Mlacha YP, Msellemu DF, Limwagu AJ, Mageni ZD, et al. Spatially aggregated clusters and scattered smaller loci of elevated malaria vector density and human infection prevalence in urban Dar es Salaam, Tanzania. Malar J. 2016;15:135. doi: 10.1186/s12936-016-1186-9 26931372

43. Stresman GH, Baidjoe AY, Stevenson J, Grignard L, Odongo W, Owaga C, et al. Focal screening to identify the subpatent parasite reservoir in an area of low and heterogeneous transmission in the Kenya highlands. J Infect Dis. 2015;212(11):1768–77. doi: 10.1093/infdis/jiv302 26019285

44. Bisanzio D, Mutuku F, LaBeaud AD, Mungai PL, Muinde J, Busaidy H, et al. Use of prospective hospital surveillance data to define spatiotemporal heterogeneity of malaria risk in coastal Kenya. Malar J. 2015;14:482. doi: 10.1186/s12936-015-1006-7 26625721

45. Ndiath MM, Cisse B, Ndiaye JL, Gomis JF, Bathiery O, Dia AT, et al. Application of geographically-weighted regression analysis to assess risk factors for malaria hotspots in Keur Soce health and demographic surveillance site. Malar J. 2015;14:463. doi: 10.1186/s12936-015-0976-9 26581562

46. Zhou G, Afrane YA, Malla S, Githeko AK, Yan G. Active case surveillance, passive case surveillance and asymptomatic malaria parasite screening illustrate different age distribution, spatial clustering and seasonality in western Kenya. Malar J. 2015;14:41. doi: 10.1186/s12936-015-0551-4 25627802

47. Espie E, Diene Sarr F, Diop F, Faye J, Richard V, Tall A, et al. Spatio-temporal variations in malaria incidence in children less than 10 years old, health district of Sokone, Senegal, 2010–2013. PLoS ONE. 2015;10(9):e0137737. doi: 10.1371/journal.pone.0137737 26381623

48. Ndiath M, Faye B, Cisse B, Ndiaye JL, Gomis JF, Dia AT, et al. Identifying malaria hotspots in Keur Soce health and demographic surveillance site in context of low transmission. Malar J. 2014;13:453. doi: 10.1186/1475-2875-13-453 25418476

49. Bejon P, Williams TN, Nyundo C, Hay SI, Benz D, Gething PW, et al. A micro-epidemiological analysis of febrile malaria in Coastal Kenya showing hotspots within hotspots. Elife. 2014;3:e02130. doi: 10.7554/eLife.02130 24843017

50. Mosha JF, Sturrock HJ, Greenwood B, Sutherland CJ, Gadalla NB, Atwal S, et al. Hot spot or not: a comparison of spatial statistical methods to predict prospective malaria infections. Malar J. 2014;13:53. doi: 10.1186/1475-2875-13-53 24517452

51. Davis M, von Cavallar S, Wyres KL, Reumann M, Sepulveda MJ, Rogers P. Spatio-temporal information and knowledge representation of disease incidence and respective intervention strategies. Stud Health Technol Inform. 2014;205:1173–7. 25160374

52. Yamana TK, Bomblies A, Laminou IM, Duchemin JB, Eltahir EA. Linking environmental variability to village-scale malaria transmission using a simple immunity model. Parasit Vectors. 2013;6:226. doi: 10.1186/1756-3305-6-226 23919581

53. Valle D, Lima JM. Large-scale drivers of malaria and priority areas for prevention and control in the Brazilian Amazon region using a novel multi-pathogen geospatial model. Malar J. 2014;13:443. doi: 10.1186/1475-2875-13-443 25412882

54. Bousema T, Stresman G, Baidjoe AY, Bradley J, Knight P, Stone W, et al. The impact of hotspot-targeted interventions on malaria transmission in rachuonyo south district in the estern Kenyan highlands: A cluster-randomized controlled trial. PLoS Med. 2016;13(4):e1001993. doi: 10.1371/journal.pmed.1001993 27071072

55. Maude RJ, Pontavornpinyo W, Saralamba S, Aguas R, Yeung S, Dondorp AM, et al. The last man standing is the most resistant: eliminating artemisinin-resistant malaria in Cambodia. Malar J. 2009;8:31. doi: 10.1186/1475-2875-8-31 19228438

56. The malERA Refresh Consultative Panel on Insecticide and Drug Resistance. malERA: An updated research agenda for insecticide and drug resistance in malaria elimination and eradication. PLoS Med. 2017;14(11):e1002450. https://doi.org/10.1371/journal.pmed.1002450

57. Pinder M, Moorthy V, Mendis K, Brown G, on behalf of the WHO MALVAC committee. MALVAC 2010: Measures of efficacy of anti-malarial interventions against malaria transmission, 15–16 November 2010 in Geneva, Switzerland Geneva: WHO; 2010. http://www.who.int/immunization/research/meetings_workshops/MALVAC_2010_meeting_report.pdf.

58. 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 24480314

59. Briet OJ, Huho BJ, Gimnig JE, Bayoh N, Seyoum A, Sikaala CH, et al. Applications and limitations of Centers for Disease Control and Prevention miniature light traps for measuring biting densities of African malaria vector populations: a pooled-analysis of 13 comparisons with human landing catches. Malar J. 2015;14:247. doi: 10.1186/s12936-015-0761-9 26082036

60. Chaki PP, Mlacha Y, Msellemu D, Muhili A, Malishee AD, Mtema ZJ, et al. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J. 2012;11:172. doi: 10.1186/1475-2875-11-172 22624853

61. Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, et al. Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg. 2004;70(1):33–7. 14971695

62. Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J. 2014;13:111. doi: 10.1186/1475-2875-13-111 24656206

63. Wong J, Bayoh N, Olang G, Killeen GF, Hamel MJ, Vulule JM, et al. Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya. Malar J. 2013;12:143. doi: 10.1186/1475-2875-12-143 23631641

64. Sikaala CH, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, et al. Evaluation of alternative mosquito sampling methods for malaria vectors in Lowland South-East Zambia. Parasit Vectors. 2013;6:91. doi: 10.1186/1756-3305-6-91 23570257

65. Lima JB, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R. Is there an efficient trap or collection method for sampling Anopheles darlingi and other malaria vectors that can describe the essential parameters affecting transmission dynamics as effectively as human landing catches? A Review. Mem Inst Oswaldo Cruz. 2014;109(5):685–705. doi: 10.1590/0074-0276140134 25185008

66. Govella NJ, Maliti DF, Mlwale AT, Masallu JP, Mirzai N, Johnson PC, et al. An improved mosquito electrocuting trap that safely reproduces epidemiologically relevant metrics of mosquito human-feeding behaviours as determined by human landing catch. Malar J. 2016;15:465. doi: 10.1186/s12936-016-1513-1 27618941

67. Maliti DV, Govella NJ, Killeen GF, Mirzai N, Johnson PC, Kreppel K, et al. Development and evaluation of mosquito-electrocuting traps as alternatives to the human landing catch technique for sampling host-seeking malaria vectors. Malar J. 2015;14:502. doi: 10.1186/s12936-015-1025-4 26670881

68. Mweresa CK, Mukabana WR, Omusula P, Otieno B, Van Loon JJ, Takken W. Enhancing attraction of african malaria vectors to a synthetic odor blend. J Chem Ecol. 2016;42(6):508–16. doi: 10.1007/s10886-016-0711-1 27349651

69. Pombi M, Jacobs F, Verhulst NO, Caputo B, della Torre A, Takken W. Field evaluation of a novel synthetic odour blend and of the synergistic role of carbon dioxide for sampling host-seeking Aedes albopictus adults in Rome, Italy. Parasit Vectors. 2014;7:580. doi: 10.1186/s13071-014-0580-9 25499569

70. Brady OJ, Godfray HC, Tatem AJ, Gething PW, Cohen JM, McKenzie FE, et al. Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination. Trans R Soc Trop Med Hyg. 2016;110(2):107–17. doi: 10.1093/trstmh/trv113 26822603

71. Dewald JR, Fuller DO, Muller GC, Beier JC. A novel method for mapping village-scale outdoor resting microhabitats of the primary African malaria vector, Anopheles gambiae. Malar J. 2016;15(1):489. doi: 10.1186/s12936-016-1534-9 27659918

72. Sikulu M, Dowell KM, Hugo LE, Wirtz RA, Michel K, Peiris KH, et al. Evaluating RNAlater(R) as a preservative for using near-infrared spectroscopy to predict Anopheles gambiae age and species. Malar J. 2011;10:186. doi: 10.1186/1475-2875-10-186 21740582

73. Mayagaya VS, Michel K, Benedict MQ, Killeen GF, Wirtz RA, Ferguson HM, et al. Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. Am J Trop Med Hyg. 2009;81(4):622–30. doi: 10.4269/ajtmh.2009.09-0192 19815877

74. Ntamatungiro AJ, Mayagaya VS, Rieben S, Moore SJ, Dowell FE, Maia MF. The influence of physiological status on age prediction of Anopheles arabiensis using near infra-red spectroscopy. Parasit Vectors. 2013;6(1):298. doi: 10.1186/1756-3305-6-298 24499515

75. Amoah LE, Abankwa J, Oppong A. Plasmodium falciparum histidine rich protein-2 diversity and the implications for PfHRP 2: based malaria rapid diagnostic tests in Ghana. Malar J. 2016;15:101. doi: 10.1186/s12936-016-1159-z 26891848

76. Murillo Solano C, Akinyi Okoth S, Abdallah JF, Pava Z, Dorado E, Incardona S, et al. Deletion of Plasmodium falciparum histidine-rich protein 2 (pfhrp2) and histidine-rich protein 3 (pfhrp3) genes in Colombian parasites. PLoS ONE. 2015;10(7):e0131576. doi: 10.1371/journal.pone.0131576 26151448

77. Tietje K, Hawkins K, Clerk C, Ebels K, McGray S, Crudder C, et al. The essential role of infection-detection technologies for malaria elimination and eradication. Trends Parasitol. 2014;30(5):259–66. doi: 10.1016/j.pt.2014.03.003 24726857

78. Cordray MS, Richards-Kortum RR. Emerging nucleic acid-based tests for point-of-care detection of malaria. Am J Trop Med Hyg. 2012;87(2):223–30. doi: 10.4269/ajtmh.2012.11-0685 22855751

79. Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med. 2015;12(3):e1001788. doi: 10.1371/journal.pmed.1001788 25734259

80. Kong TF, Ye W, Peng WK, Hou HW, Marcos, Preiser PR, et al. Enhancing malaria diagnosis through microfluidic cell enrichment and magnetic resonance relaxometry detection. Sci Rep. 2015;5:11425. doi: 10.1038/srep11425 26081638

81. Peng WK, Kong TF, Ng CS, Chen L, Huang Y, Bhagat AA, et al. Micromagnetic resonance relaxometry for rapid label-free malaria diagnosis. Nat Med. 2014;20(9):1069–73. doi: 10.1038/nm.3622 25173428

82. Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A. 2012;109(25):10030–5. doi: 10.1073/pnas.1200841109 22665809

83. Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, et al. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol. 2013;22(2):273–85. doi: 10.1111/mec.12099 23121253

84. Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang HH, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci U S A. 2015;112(22):7067–72. doi: 10.1073/pnas.1505691112 25941365

85. 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(7):1123–32. doi: 10.1093/infdis/jiu225 24737801

86. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, 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(14):5108–13. doi: 10.1073/pnas.0408725102 15792998

87. 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(6):e6083. doi: 10.1371/journal.pone.0006083 19562032

88. Franca CT, Hostetler JB, Sharma S, White MT, Lin E, Kiniboro B, et al. An antibody screen of a Plasmodium vivax antigen library identifies novel merozoite proteins associated with clinical protection. PLoS Negl Trop Dis. 2016;10(5):e0004639. doi: 10.1371/journal.pntd.0004639 27182597

89. 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. doi: 10.1186/1756-3305-4-212 22059951

90. Helb DA, Tetteh KK, 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 U S A. 2015;112(32):E4438–47. doi: 10.1073/pnas.1501705112 26216993

91. Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci U S A. 2010;107(15):6958–63. doi: 10.1073/pnas.1001323107 20351286

92. Goo YK, Seo EJ, Choi YK, Shin HI, Sattabongkot J, Ji SY, et al. First characterization of Plasmodium vivax liver stage antigen (PvLSA) using synthetic peptides. Parasit Vectors. 2014;7:64. doi: 10.1186/1756-3305-7-64 24520895

93. Armiyanti Y, Nuryady MM, Arifianto RP, Nurmariana E, Senjarini K, Fitri LE, et al. Detection of immunogenic proteins from Anopheles sundaicus salivary glands in the human serum. Rev Soc Bras Med Trop. 2015;48(4):410–6. doi: 10.1590/0037-8682-0185-2015 26312930

94. Londono-Renteria B, Drame PM, Weitzel T, Rosas R, Gripping C, Cardenas JC, et al. An. gambiae gSG6-P1 evaluation as a proxy for human-vector contact in the Americas: a pilot study. Parasit Vectors. 2015;8:533. doi: 10.1186/s13071-015-1160-3 26464073

95. Yao MX, Sun XD, Gao YH, Cheng ZB, Deng WW, Zhang JJ, et al. Multi-epitope chimeric antigen used as a serological marker to estimate Plasmodium falciparum transmission intensity in the border area of China-Myanmar. Infect Dis Poverty. 2016;5(1):98. doi: 10.1186/s40249-016-0194-x 27604628

96. Yman V, White MT, Rono J, Arca B, Osier FH, Troye-Blomberg M, et al. Antibody acquisition models: A new tool for serological surveillance of malaria transmission intensity. Sci Rep. 2016;6:19472. doi: 10.1038/srep19472 26846726

97. Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Jain A, Taghavian O, et al. Common asymptomatic and submicroscopic malaria infections in Western Thailand revealed in longitudinal molecular and serological studies: a challenge to malaria elimination. Malar J. 2016;15:333. doi: 10.1186/s12936-016-1393-4 27333893

98. Baidjoe AY, Stevenson J, Knight P, Stone W, Stresman G, Osoti V, et al. Factors associated with high heterogeneity of malaria at fine spatial scale in the Western Kenyan highlands. Malar J. 2016;15:307. doi: 10.1186/s12936-016-1362-y 27259286

99. Yeka A, Nankabirwa J, Mpimbaza A, Kigozi R, Arinaitwe E, Drakeley C, et al. Factors associated with malaria parasitemia, anemia and serological responses in a spectrum of epidemiological settings in Uganda. PLoS ONE. 2015;10(3):e0118901. doi: 10.1371/journal.pone.0118901 25768015

100. Cunha MG, Silva ES, Sepulveda N, Costa SP, Saboia TC, Guerreiro JF, et al. Serologically defined variations in malaria endemicity in Para state, Brazil. PLoS ONE. 2014;9(11):e113357. doi: 10.1371/journal.pone.0113357 25419900

101. Hsiang MS, Hwang J, Kunene S, Drakeley C, Kandula D, Novotny J, et al. Surveillance for malaria elimination in Swaziland: a national cross-sectional study using pooled PCR and serology. PLoS ONE. 2012;7(1):e29550. doi: 10.1371/journal.pone.0029550 22238621

102. Kobayashi T, Chishimba S, Shields T, Hamapumbu H, Mharakurwa S, Thuma PE, et al. Temporal and spatial patterns of serologic responses to Plasmodium falciparum antigens in a region of declining malaria transmission in southern Zambia. Malar J. 2012;11:438. doi: 10.1186/1475-2875-11-438 23276228

103. Rosas-Aguirre A, Speybroeck N, Llanos-Cuentas A, Rosanas-Urgell A, Carrasco-Escobar G, Rodriguez H, et al. Hotspots of malaria transmission in the Peruvian Amazon: Rapid assessment through a parasitological and serological survey. PLoS ONE. 2015;10(9):e0137458. doi: 10.1371/journal.pone.0137458 26356311

104. Sepulveda N, Paulino CD, Drakeley C. Sample size and power calculations for detecting changes in malaria transmission using antibody seroconversion rate. Malar J. 2015;14:529. doi: 10.1186/s12936-015-1050-3 26715538

105. Stevenson JC, Stresman GH, Baidjoe A, Okoth A, Oriango R, Owaga C, et al. Use of different transmission metrics to describe malaria epidemiology in the highlands of western Kenya. Malar J. 2015;14:418. doi: 10.1186/s12936-015-0944-4 26502920

106. van den Hoogen LL, Griffin JT, Cook J, Sepulveda N, Corran P, Conway DJ, et al. Serology describes a profile of declining malaria transmission in Farafenni, The Gambia. Malar J. 2015;14:416. doi: 10.1186/s12936-015-0939-1 26492873

107. Zakeri S, van den Hoogen LL, Mehrizi AA, Karimi F, Raeisi A, Drakeley C. Anti-malarial seroprevalence assessment during an elimination programme in Chabahar District, south-eastern Iran. Malar J. 2016;15(1):382. doi: 10.1186/s12936-016-1432-1 27448606

108. Weppelmann TA, von Fricken ME, Lam B, Telisma T, Existe A, Lemoine JF, et al. Sparse serological evidence of Plasmodium vivax transmission in the Ouest and Sud-Est departments of Haiti. Acta Trop. 2016;162:27–34. doi: 10.1016/j.actatropica.2016.05.011 27230796

109. 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. doi: 10.1186/1475-2875-11-86 22443375

110. Cameron A, Njeumi F, Chibeu D, Martin T. Risk-based disease surveillance: A manual for vetinarians on the deisgn and analysis of surveillance for demonstration of freedom from disease Rome: Food and Agriculture Organization of the United Nations; 2014. http://www.fao.org/3/a-i4205e.pdf.

111. Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207–11. doi: 10.1038/nature15535 26375008

112. Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000–10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383(9930):1739–47. doi: 10.1016/S0140-6736(13)62566-0 24559537

113. Tatem AJ. Mapping population and pathogen movements. Int Health. 2014;6(1):5–11. doi: 10.1093/inthealth/ihu006 24480992

114. MalariaGEN. 2016. Cited 05 Sept 2016. https://www.malariagen.net/data.

115. Worldpop. 2016. Cited 05 Sept 2016. http://www.worldpop.org.uk/.

116. Pindolia DK, Garcia AJ, Wesolowski A, Smith DL, Buckee CO, Noor AM, et al. Human movement data for malaria control and elimination strategic planning. Malar J. 2012;11:205. doi: 10.1186/1475-2875-11-205 22703541

117. Wesolowski A, Buckee CO, Pindolia DK, Eagle N, Smith DL, Garcia AJ, et al. The use of census migration data to approximate human movement patterns across temporal scales. PLoS ONE. 2013;8(1):e52971. doi: 10.1371/journal.pone.0052971 23326367

118. Marshall JM, Toure M, Ouedraogo AL, Ndhlovu M, Kiware SS, Rezai A, et al. Key traveller groups of relevance to spatial malaria transmission: a survey of movement patterns in four sub-Saharan African countries. Malar J. 2016;15:200. doi: 10.1186/s12936-016-1252-3 27068686

119. Blangiardo M, Cameletti M, Baio G, Rue H. Spatial and spatio-temporal models with R-INLA. Spat Spatiotemporal Epidemiol. 2013;4:33–49. doi: 10.1016/j.sste.2012.12.001 23481252

120. Ruktanonchai NW, DeLeenheer P, Tatem AJ, Alegana VA, Caughlin TT, Zu Erbach-Schoenberg E, et al. Identifying Malaria Transmission Foci for Elimination Using Human Mobility Data. PLoS Comput Biol. 2016;12(4):e1004846. doi: 10.1371/journal.pcbi.1004846 27043913