Mathematical models of within-host and transmission dynamics to determine effects of malaria interventions in a variety of transmission settings

American Journal of Tropical Medicine and Hygiene

Volumn 88, Issue 5, 2013, Pages 817-827

  Eckhoff, Philip ^a  

^a Intellectual Ventures Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ARTICLE; MALARIA; MATHEMATICAL MODEL; NONHUMAN; OSCILLATION; PLASMODIUM FALCIPARUM; SEASONAL VARIATION; SIMULATION; VECTOR CONTROL;

ANIMALS; ANOPHELES; FEEDING BEHAVIOR; HUMANS; INSECT VECTORS; MALARIA VACCINES; MALARIA, FALCIPARUM; MODELS, BIOLOGICAL; MOSQUITO CONTROL; PLASMODIUM FALCIPARUM; POPULATION DYNAMICS; SEASONS;

ANOPHELES GAMBIAE; GAMBIAE SPECIES COMPLEX;

EID: 84876902157     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.12-0007     Document Type: Article

References (79)

1. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI, 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434: 214-217. (Pubitemid 40388051)
2. World Health Organization, 2011. World Malaria Report: 2011. Geneva: World Health Organization.
3. Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW, 2009. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6: e1000048.
4. Hay SI, Sinka ME, Okara RM, Kabaria CW, Mbithi PM, Tago CC, Benz D, Gething PW, Howes RE, Patil AP, Temperley WH, Bangs MJ, Chareonviriyaphap T, Elyazar IR, Harbach RE, Hemingway J, Manguin S, Mbogo CM, Rubio-Palis Y, Godfray HC, 2010. Developing global maps of the dominant Anopheles vectors of human malaria. PLoS Med 7: e1000209.
5. Gimnig JE, Kolczak MS, Hightower AW, Vulule JM, Schoute E, Kamau L, Phillips-Howard PA, Ter Kuile FO, Nahlen BL, Hawley WA, 2003. Effect of permethrin-treated bed nets on the spatial distribution of malaria vectors in western Kenya. Am J Trop Med Hyg 68: 115-120. (Pubitemid 38240690)
6. Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA, 2003. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg 68: 16-22. (Pubitemid 38240677)
7. Molineaux L, Gramiccia G, 1980. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization.
8. Romi R, Razaiarimanga MC, Raharimanga R, Rakotondraibe EM, Ranaivo LH, Pietra V, Raveloson A, Majori G, 2002. Impact of the malaria control campaign (1993-1998) in the highlands of Madagascar: parasitological and entomological data. Am J Trop Med Hyg 66: 2-6. (Pubitemid 34733145)
9. Killeen G, Fillinger U, Knols B, 2002. Advantages of larval control for African malaria vectors: low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage. Malar J 1: 8.
10. Fillinger U, Sonye G, Killeen GF, Knols BGJ, Becker N, 2004. The practical importance of permanent and semipermanent habitats for controlling aquatic stages of Anopheles gambiae sensu lato mosquitoes: operational observations from a rural town in western Kenya. Trop Med Int Health 9: 1274-1289. (Pubitemid 40037163)
11. Fillinger U, Kannady K, William G, Vanek M, Dongus S, Nyika D, Geissbuhler Y, Chaki P, Govella N, Mathenge E, Singer B, Mshinda H, Lindsay S, Tanner M, Mtasiwa D, de Castro M, Killeen G, 2008. A tool box for operational mosquito larval control: preliminary results and early lessons from the urban malaria control programme in Dar es Salaam, Tanzania. Malar J 7: 20.
12. Reddy M, Overgaard H, Abaga S, Reddy V, Caccone A, Kiszewski A, Slotman M, 2011. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J 10: 184.
13. Bugoro H, Iro'ofa C, Mackenzie D, Apairamo A, Hevalao W, Corcoran S, Bobogare A, Beebe N, Russell T, Chen C-C, Cooper R, 2011. Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J 10: 287.
14. Derua Y, Alifrangis M, Hosea K, Meyrowitsch D, Magesa S, Pedersen E, Simonsen P, 2012. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in northeastern Tanzania. Malar J 11: 188.
15. Okell LC, Drakeley CJ, Bousema T, Whitty CJ, Ghani AC, 2008. Modelling the impact of artemisinin combination therapy and long-acting treatments on malaria transmission intensity. PLoS Med 5: e226.
16. von Seidlein L, Greenwood BM, 2003. Mass administrations of antimalarial drugs. Trends Parasitol 19: 452-460. (Pubitemid 38366142)
17. Khatib R, Skarbinski J, Njau J, Goodman C, Elling B, Kahigwa E, Roberts J, MacArthur J, Gutman J, Kabanywanyi A, Smith E, Somi M, Lyimo T, Mwita A, Genton B, Tanner M, Mills A, Mshinda H, Bloland P, Abdulla S, Kachur S, 2012. Routine delivery of artemisinin-based combination treatment at fixed health facilities reduces malaria prevalence in Tanzania: an observational study. Malar J 11: 140.
18. Huho B, Killeen G, Ferguson H, Tami A, Lengeler C, Charlwood JD, Kihonda A, Kihonda J, Kachur SP, Smith T, Abdulla S, 2012. Artemisinin-based combination therapy does not measurably reduce human infectiousness to vectors in a setting of intense malaria transmission. Malar J 11: 118.
19. Shekalaghe S, Drakeley C, van den Bosch S, ter Braak R, van den Bijllaardt W, Mwanziva C, Semvua S, Masokoto A, Mosha F, Teelen K, Hermsen R, Okell L, Gosling R, Sauerwein R, Bousema T, 2011. A cluster-randomized trial of mass drug administration with a gametocytocidal drug combination to interrupt malaria transmission in a low endemic area in Tanzania. Malar J 10: 247.
20. Penny MA, Maire N, Studer A, Schapira A, Smith TA, 2008. What should vaccine developers ask? Simulation of the effectiveness of malaria vaccines. PLoS ONE 3: e3193.
21. RTS SCTP, 2012. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med 367: 2284-2295.
22. De Castro MC, Yamagata Y, Mtasiwa D, Tanner M, Utzinger J, Keiser J, Singer BH, 2004. Integrated urban malaria control: a case study in Dar es Salaam, Tanzania. Am J Trop Med Hyg 71: 103-117. (Pubitemid 39121311)
23. McKenzie FE, Baird JK, Beier JC, Lal AA, Bossert WH, 2002. A biologic basis for integrated malaria control. Am J Trop Med Hyg 67: 571-577. (Pubitemid 36014912)
24. Killeen G, McKenzie F, Foy B, Schieffelin C, Billingsley P, Beier J, 2000. The potential impact of integrated malaria transmission control on entomologic inoculation rate in highly endemic areas. Am J Trop Med Hyg 62: 545-551. (Pubitemid 32210473)
25. Fillinger U, Ndenga B, Githeko A, Lindsay SW, 2009. Integrated malaria vector control with microbial larvicides and insecticide-treated nets in western Kenya: a controlled trial. Bull World Health Organ 87: 655-665.
26. Macdonald G, 1956. Theory of the eradication of malaria. Bull World Health Organ 15: 369-387.
27. Macdonald G, 1957. The Epidemiology and Control of Malaria. London: Oxford University Press.
28. Ross R, 1910. The Prevention of Malaria. London: J. Murray.
29. Garrett-Jones C, 1964. Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity. Nature 204: 1173-1175.
30. Depinay J-M, Mbogo C, Killeen G, Knols B, Beier J, Carlson J, Dushoff J, Billingsley P, Mwambi H, Githure J, Toure A, Ellis McKenzie F, 2004. A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission. Malar J 3: 29.
31. Bomblies A, Duchemin J-B, Eltahir E, 2009. A mechanistic approach for accurate simulation of village scale malaria transmission. Malar J 8: 223.
32. Okell L, Drakeley C, Ghani A, Bousema T, Sutherland C, 2008. Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar J 7: 125.
33. Maude R, Pontavornpinyo W, Saralamba S, Aguas R, Yeung S, Dondorp A, Day N, White N, White L, 2009. The last man standing is the most resistant: eliminating artemisinin-resistant malaria in Cambodia. Malar J 8: 31.
34. Boni MF, Smith DL, Laxminarayan R, 2008. Benefits of using multiple first-line therapies against malaria. Proc Natl Acad Sci USA 105: 14216-14221.
35. Ross A, Penny M, Maire N, Studer A, Carneiro I, Schellenberg D, Greenwood B, Tanner M, Smith T, 2008. Modelling the epidemiological impact of intermittent preventive treatment against malaria in infants. PLoS ONE 3: e2661.
36. Smith T, Killeen GF, Maire N, Ross A, Molineaux L, Tediosi F, Hutton G, Utzinger J, Dietz K, Tanner M, 2006. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg 75: 1-10.
37. Tediosi F, Hutton G, Maire N, Smith TA, Ross A, Tanner M, 2006. Predicting the cost-effectiveness of introducing a pre-erythrocytic malaria vaccine into the expanded program on immunization in Tanzania. Am J Trop Med Hyg 75: 131-143.
38. Struchiner CJ, Halloran ME, Spielman A, 1989. Modeling malaria vaccines. I: newuses for old ideas. Math Biosci 94: 87-113. (Pubitemid 19131651)
39. Smith T, Maire N, Ross A, Penny M, Chitnis N, Schapira A, Studer A, Genton B, Lengeler C, Tediosi F, De Savigny D, Tanner M, 2008. Towards a comprehensive simulation model of malaria epidemiology and control. Parasitology 135: 1507-1516.
40. Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basáñez M-G, Ghani AC, 2010. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med 7: e1000324.
41. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, Mendis K, Newman RD, Plowe CV, Rodríguez MH, Sinden R, Slutsker L, Tanner M, 2011. A research agenda to underpin malaria eradication. PLoS Med 8: e1000406.
42. The mal ERACGoM, 2011. A research agenda for malaria eradication: modeling. PLoS Med 8: e1000403.
43. Smith T, Ross A, Maire N, Chitnis N, Studer A, Hardy D, Brooks A, Penny M, Tanner M, 2012. Ensemble modeling of the likely public health impact of a pre-erythrocytic malaria vaccine. PLoS Med 9: e1001157.
44. Eckhoff P, 2011. A malaria transmission-directed model of mosquito life cycle and ecology. Malar J 10: 303.
45. Eckhoff P, 2012. P. falciparum infection durations and infectiousness are shaped by antigenic variation and innate and adaptive host immunity in a mathematical model. PLoS ONE 7: e44950.
46. Smith DL, McKenzie FE, 2004. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J 3: 13.
47. Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop 54: 55-72. (Pubitemid 23236067)
48. Eckhoff P, 2012. Malaria parasite diversity and transmission intensity affect development of parasitological immunity in a mathematical model. Malar J 11: 419.
49. Seyoum A, Sikaala C, Chanda J, Chinula D, Ntamatungiro A, Hawela M, Miller J, Russell T, Briet OJ, Killeen G, 2012. Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, south-east Zambia. Parasit Vectors 5: 101.
50. Kiware SS, Chitnis N, Devine GJ, Moore SJ, Majambere S, Killeen GF, 2012. Biologically meaningful coverage indicators for eliminating malaria transmission. Biol Lett 8: 874-877.
51. Recker M, Nee S, Bull PC, Kinyanjui S, Marsh K, Newbold C, Gupta S, 2004. Transient cross-reactive immune responses can orchestrate antigenic variation in malaria. Nature 429: 555-558. (Pubitemid 38737658)
52. Fowkes FJ, Richards JS, Simpson JA, Beeson JG, 2010. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med 7: e1000218.
53. Lengeler C, 2004. Insecticide-treated nets for malaria control: real gains. Bull World Health Organ 82: 84-84.
54. Pluess B, Tanser Frank C, Lengeler C, Sharp Brian L, 2010. Indoor Residual Spraying for Preventing Malaria. Cochrane Database of Systematic Reviews. New York: John Wiley & Sons, Ltd.
55. Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M, 2006. Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg 75: 11-18.
56. Collins WE, Jeffery GM, 1999. A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum: development of parasitologic and clinical immunity during primary infection. Am J Trop Med Hyg 61: 4-19.
57. Recker M, Buckee CO, Serazin A, Kyes S, Pinches R, Christodoulou Z, Springer AL, Gupta S, Newbold CI, 2011. Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathog 7: e1001306.
58. Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L, 2006. A model for natural immunity to asexual blood stages of Plasmodium falciparum malaria in endemic areas. Am J Trop Med Hyg 75: 19-31.
59. Garki, 2011. The Garki Portal. Available at: rhgarki.crc.nd.edu. Accessed February 7, 2013.
60. Govella NJ, Okumu FO, Killeen GF, 2010. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg 82: 415-419.
61. Russell T, Govella N, Azizi S, Drakeley C, Kachur SP, Killeen G, 2011. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10: 80.
62. Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, Olotu A, Osier FH, Hay SI, Färnert A, Marsh K, 2010. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med 7: e1000304.
63. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, Ghani A, Drakeley C, Gosling R, 2012. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165.
64. Charlwood JD, Vij R, Billingsley PF, 2000. Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am J Trop Med Hyg 62: 726-732. (Pubitemid 32281495)
65. Coluzzi M, Sabatini A, Petrarca V, Angela Di Deco M, 1977. Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature 266: 832-833. (Pubitemid 8074713)
66. Coluzzi M, Sabatini A, Petrarca V, Di Deco MA, 1979. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 73: 483-497. (Pubitemid 10245985)
67. Kulkarni MA, Desrochers RE, Kerr JT, 2010. High resolution niche models of malaria vectors in northern Tanzania: a new capacity to predict malaria risk? PLoS ONE 5: e9396.
68. Centre GPC, 2008. Full Data Reanalysis. Available at: http://gpcc.dwd.de. Accessed 2008.
69. Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, Bruce J, Mosha FW, Rowland MW, 2012. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS ONE 7: e31481.
70. Ferguson H, Maire N, Takken W, Lyimo I, Briet O, Lindsay S, Smith T, 2012. Selection of mosquito life-histories: a hidden weapon against malaria? Malar J 11: 106.
71. Guilbride DL, Patrick DL, Pawel PG, 2012. Malaria's deadly secret: a skin stage. Trends Parasitol 28: 142-150.
72. Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA, 2006. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol 22: 424-430. (Pubitemid 44176410)
73. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K, 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med 4: 358-360. (Pubitemid 28144099)
74. Langhorne J, Ndungu FM, Sponaas AM, Marsh K, 2008. Immunity to malaria: more questions than answers. Nat Immunol 9: 725-732. (Pubitemid 351859155)
75. Killeen GF, McKenzie FE, Foy BD, Bogh C, Beier JC, 2001. The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by African mosquito populations. Trans R Soc Trop Med Hyg 95: 469-476. (Pubitemid 34947396)
76. Graves PM, Burkot TR, Saul AJ, Hayes RJ, Carter R, 1990. Estimation of anopheline survival rate, vectorial capacity and mosquito infection probability from malaria vector infection rates in villages near Madang, Papua New Guinea. J Appl Ecol 27: 134-147.
77. Cohen JM, Smith DL, Vallely A, Taleo G, Malefoasi G, Sabot O, 2009. Holding the line. Feachem RG, Phillips AA, Targett GA, Group ME, eds. Shrinking the Malaria Map: A Prospectus on Malaria Elimination. San Francisco, CA: The Global Health Group: UCSF Global Health Sciences, 40-60.
78. Moonen B, Barrett S, Tulloch J, Jamison DT, 2009. Making the decision. Feachem RG, Phillips AA, Targett GA, Group ME, eds. Shrinking the Malaria Map: A Prospectus on Malaria Elimination. San Francisco, CA: The Global Health Group: UCSF Global Health Sciences, 1-18.
79. Smith DL, Smith TA, Hay SI, 2009. Measuring malaria for elimination. Feachem RG, Phillips AA, Targett GA, Group ME, eds. Shrinking the Malaria Map: A Prospectus on Malaria Elimination. San Francisco, CA: The Global Health Group: UCSF Global Health Sciences, 108-126.