Reducing Malaria Transmission in Africa: A Model-Based Evaluation of Intervention Strategies

English version České info

Background:
Over the past decade malaria intervention coverage has been scaled up across Africa. However, it remains unclear what overall reduction in transmission is achievable using currently available tools.

Methods and Findings:
We developed an individual-based simulation model for Plasmodium falciparum transmission in an African context incorporating the three major vector species (Anopheles gambiae s.s., An. arabiensis, and An. funestus) with parameters obtained by fitting to parasite prevalence data from 34 transmission settings across Africa. We incorporated the effect of the switch to artemisinin-combination therapy (ACT) and increasing coverage of long-lasting insecticide treated nets (LLINs) from the year 2000 onwards. We then explored the impact on transmission of continued roll-out of LLINs, additional rounds of indoor residual spraying (IRS), mass screening and treatment (MSAT), and a future RTS,S/AS01 vaccine in six representative settings with varying transmission intensity (as summarized by the annual entomological inoculation rate, EIR: 1 setting with low, 3 with moderate, and 2 with high EIRs), vector–species combinations, and patterns of seasonality. In all settings we considered a realistic target of 80% coverage of interventions. In the low-transmission setting (EIR∼3 ibppy [infectious bites per person per year]), LLINs have the potential to reduce malaria transmission to low levels (<1% parasite prevalence in all age-groups) provided usage levels are high and sustained. In two of the moderate-transmission settings (EIR∼43 and 81 ibppy), additional rounds of IRS with DDT coupled with MSAT could drive parasite prevalence below a 1% threshold. However, in the third (EIR = 46) with An. arabiensis prevailing, these interventions are insufficient to reach this threshold. In both high-transmission settings (EIR∼586 and 675 ibppy), either unrealistically high coverage levels (>90%) or novel tools and/or substantial social improvements will be required, although considerable reductions in prevalence can be achieved with existing tools and realistic coverage levels.

Conclusions:
Interventions using current tools can result in major reductions in P. falciparum malaria transmission and the associated disease burden in Africa. Reduction to the 1% parasite prevalence threshold is possible in low- to moderate-transmission settings when vectors are primarily endophilic (indoor-resting), provided a comprehensive and sustained intervention program is achieved through roll-out of interventions. In high-transmission settings and those in which vectors are mainly exophilic (outdoor-resting), additional new tools that target exophagic (outdoor-biting), exophilic, and partly zoophagic mosquitoes will be required.

: Please see later in the article for the Editors' Summary

Vyšlo v časopise: Reducing Malaria Transmission in Africa: A Model-Based Evaluation of Intervention Strategies. PLoS Med 7(8): e32767. doi:10.1371/journal.pmed.1000324
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1000324

Souhrn

Zdroje

1. BarnesKI

ChandaP

Ab BarnabasG

2009 Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar J 8 Suppl 1 S8

2. CeesaySJ

Casals-PascualC

ErskineJ

AnyaSE

DuahNO

2008 Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 372 1545 1554

3. O'MearaWP

BejonP

MwangiTW

OkiroEA

PeshuN

2008 Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372 1555 1562

4. SharpBL

KleinschmidtI

StreatE

MaharajR

BarnesKI

2007 Seven years of regional malaria control collaboration–Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg 76 42 47

5. World Health Organisation 2009 World Malaria Report 2009

6. YekutielP

1980 The Global Malaria Eradication Campaign.

KlingbergMA

Eradication of infectious diseases: a critical study Basel, Switzerland Karger 34 88

7. MolineauxL

GramicciaG

1980 The Garki Project Geneva World Health Organisation

8. MolineauxL

StoreyJ

CohenJE

ThomasA

1980 A longitudinal study of human malaria in the West African Savanna in the absence of control measures: relationships between different Plasmodium species, in particular P. falciparum and P. malariae. Am J Trop Med Hyg 29 725 737

9. DraperCC

SmithA

1960 Malaria in the Pare area of Tanganyika. Part II. Effects of three years' spraying of huts with dieldrin. Trans R Soc Trop Med Hyg 54 342 357

10. ShanksGD

HaySI

OmumboJA

SnowRW

2005 Malaria in Kenya's western highlands. Emerg Infect Dis 11 1425 1432

11. MouchetJ

1998 [Origin of malaria epidemics on the plateaus of Madagascar and the mountains of east and south Africa]. Bull Soc Pathol Exot 91 64 66

12. Garrett-JonesC

1964 Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity. Nature 204 1173 1175

13. BhattaraiA

AliAS

KachurSP

MartenssonA

AbbasAK

2007 Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med 4 e309 doi:10.1371/journal.pmed.0040309

14. KleinschmidtI

SchwabeC

BenaventeL

TorrezM

RidlFC

2009 Marked increase in child survival after four years of intensive malaria control. Am J Trop Med Hyg 80 882 888

15. GuerraCA

GikandiPW

TatemAJ

NoorAM

SmithDL

2008 The limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide. PLoS Med 5 e38 doi:10.1371/journal.pmed.0050038

16. HaySI

GuerraCA

GethingPW

PatilAP

TatemAJ

2009 A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6 e1000048 doi:10.1371/journal.pmed.1000048

17. HaySI

SinkaME

OkaraRM

KabariaCW

MbithiPM

2010 Developing global maps of the dominant Anopheles vectors of human malaria. PLoS Med 7 e1000209 doi:10.1371/journal.pmed.1000209

18. Roll Back Malaria Partnership 2008 The global malaria action plan Geneva WHO

19. Malaria Elimination 8 2009 Resolution of Malaria Elimination 8 Ministerial Meeting. Windhoek, Namibia

20. Zanzibar Malaria Control Program 2009 Malaria Elimination in Zanzibar - A Feasibility Assessment

21. BinkaFN

IndomeF

SmithT

1998 Impact of spatial distribution of permethrin-impregnated bed nets on child mortality in rural northern Ghana. Am J Trop Med Hyg 59 80 85

22. ClarkeSE

BoghC

BrownRC

PinderM

WalravenGE

2001 Do untreated bednets protect against malaria? Trans R Soc Trop Med Hyg 95 457 462

23. HawleyWA

ter KuileFO

SteketeeRS

NahlenBL

TerlouwDJ

2003 Implications of the western Kenya permethrin-treated bed net study for policy, program implementation, and future research. Am J Trop Med Hyg 68 168 173

24. KilleenGF

SmithTA

FergusonHM

MshindaH

AbdullaS

2007 Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med 4 e229 doi:10.1371/journal.pmed.0040229

25. LengelerC

2000 Insecticide-treated bednets and curtains for preventing malaria. Cochrane Database Syst Rev CD000363

26. OkellLC

DrakeleyCJ

BousemaT

WhittyCJ

GhaniAC

2008 Modelling the impact of artemisinin combination therapy and long-acting treatments on malaria transmission intensity. PLoS Med 5 e226 doi:10.1371/journal.pmed.0050226

27. OkellLC

DrakeleyCJ

GhaniAC

BousemaT

SutherlandCJ

2008 Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar J 7 125

28. SacarlalJ

AideP

AponteJJ

RenomM

LeachA

2009 Long-term safety and efficacy of the RTS,S/AS02A malaria vaccine in Mozambican children. J Infect Dis 200 329 336

29. GuinovartC

AponteJJ

SacarlalJ

AideP

LeachA

2009 Insights into long-lasting protection induced by RTS,S/AS02A malaria vaccine: further results from a phase IIb trial in Mozambican children. PLoS One 4 e5165 doi:10.1371/journal.pone.0005165

30. BarbosaA

NanicheD

AponteJJ

ManacaMN

MandomandoI

2009 Plasmodium falciparum-specific cellular immune responses after immunization with the RTS,S/AS02D candidate malaria vaccine in infants living in an area of high endemicity in Mozambique. Infect Immun 77 4502 4509

31. AbdullaS

OberholzerR

JumaO

KubhojaS

MacheraF

2008 Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. N Engl J Med 359 2533 2544

32. BejonP

LusinguJ

OlotuA

LeachA

LievensM

2008 Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 359 2521 2532

33. AlonsoPL

SacarlalJ

AponteJJ

LeachA

MaceteE

2005 Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet 366 2012 2018

34. AlonsoPL

SacarlalJ

AponteJJ

LeachA

MaceteE

2004 Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364 1411 1420

35. KilleenGF

SmithTA

2007 Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 101 867 880

36. Le MenachA

TakalaS

McKenzieFE

PerisseA

HarrisA

2007 An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malar J 6 10

37. O'MearaWP

SmithDL

McKenzieFE

2006 Potential impact of intermittent preventive treatment (IPT) on spread of drug-resistant malaria. PLoS Med 3 e141 doi:10.1371/journal.pmed.0030141

38. SmithDL

HaySI

NoorAM

SnowRW

2009 Predicting changing malaria risk after expanded insecticide-treated net coverage in Africa. Trends Parasitol 25 511 516

39. SmithT

KilleenGF

MaireN

RossA

MolineauxL

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

40. WhiteLJ

MaudeRJ

PongtavornpinyoW

SaralambaS

AguasR

2009 The role of simple mathematical models in malaria elimination strategy design. Malar J 8 212

41. BeierJC

KilleenGF

GithureJI

1999 Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg 61 109 113

42. SmithDL

DushoffJ

SnowRW

HaySI

2005 The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature 438 492 495

43. SmithDL

McKenzieFE

SnowRW

HaySI

2007 Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol 5 e42 doi:10.1371/journal.pbio.0050042

44. McKenzieFE

KilleenGF

BeierJC

BossertWH

2001 Seasonality, Parasite Diversity, and Local Extinctions in Plasmodium Falciparum Malaria. Ecology 82 2673 2681

45. SmithDL

HaySI

2009 Endemicity response timelines for Plasmodium falciparum elimination. Malar J 8 87

46. FilipeJA

RileyEM

DrakeleyCJ

SutherlandCJ

GhaniAC

2007 Determination of the processes driving the acquisition of immunity to malaria using a mathematical transmission model. PLoS Comput Biol 3 e255 doi:10.1371/journal.pcbi.0030255

47. GhaniAC

SutherlandCJ

RileyEM

DrakeleyCJ

GriffinJT

2009 Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One 4 e4383 doi:10.1371/journal.pone.0004383

48. OkellLC

GhaniAC

LyonsE

DrakeleyCJ

2009 Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis 200 1509 1517

49. TrapeJF

RogierC

1996 Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 236 240

50. HaySI

GuerraCA

TatemAJ

AtkinsonPM

SnowRW

2005 Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol 3 81 90

51. BonnetS

GouagnaLC

PaulRE

SafeukuiI

MeunierJY

2003 Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg 97 53 59

52. BoudinC

OlivierM

MolezJF

ChironJP

Ambroise-ThomasP

1993 High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg 48 700 706

53. GithekoAK

Brandling-BennettAD

BeierM

AtieliF

OwagaM

1992 The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg 86 355 358

54. Muirhead-ThomsonRC

1957 The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae); a random xenodiagnostic survey. Am J Trop Med Hyg 6 971 979

55. KilleenGF

RossA

SmithT

2006 Infectiousness of malaria-endemic human populations to vectors. Am J Trop Med Hyg 75 38 45

56. RossA

KilleenG

SmithT

2006 Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg 75 32 37

57. World Health Organisation 2006 Pesticides and their application Geneva World Health Organization

58. NoorAM

MoloneyG

BorleM

FeganGW

ShewchukT

2008 The use of mosquito nets and the prevalence of Plasmodium falciparum infection in rural South Central Somalia. PLoS One 3 e2081 doi:10.1371/journal.pone.0002081

59. KleinschmidtI

TorrezM

SchwabeC

BenaventeL

SeocharanI

2007 Factors influencing the effectiveness of malaria control in Bioko Island, equatorial Guinea. Am J Trop Med Hyg 76 1027 1032

60. MahamaT

DesireeEJ

PierreC

FabriceC

2007 Effectiveness of permanet in Cote d'Ivoire rural areas and residual activity on a knockdown-resistant strain of Anopheles gambiae. J Med Entomol 44 498 502

61. GuW

MbogoCM

GithureJI

RegensJL

KilleenGF

2003 Low recovery rates stabilize malaria endemicity in areas of low transmission in coastal Kenya. Acta Trop 86 71 81

62. KilleenGF

KihondaJ

LyimoE

OketchFR

KotasME

2006 Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis 6 161

63. MarchantT

SchellenbergD

NathanR

Armstrong SchellenbergJ

MpondaH

2010 Assessment of a national voucher scheme to deliver insecticide-treated mosquito nets to pregnant women. Can Med Assoc J 82 152 156

64. WoolhouseME

DyeC

EtardJF

SmithT

CharlwoodJD

1997 Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci U S A 94 338 342

65. MaireN

AponteJJ

RossA

ThompsonR

AlonsoP

2006 Modeling a field trial of the RTS,S/AS02A malaria vaccine. Am J Trop Med Hyg 75 104 110

66. MaireN

TediosiF

RossA

SmithT

2006 Predictions of the epidemiologic impact of introducing a pre-erythrocytic vaccine into the expanded program on immunization in sub-Saharan Africa. Am J Trop Med Hyg 75 111 118

67. JohnCC

RiedeselMA

MagakNG

LindbladeKA

MengeDM

2009 Possible interruption of malaria transmission, highland Kenya, 2007–2008. Emerg Infect Dis 15 1917 1924

68. SaulA

2003 Zooprophylaxis or zoopotentiation: the outcome of introducing animals on vector transmission is highly dependent on the mosquito mortality while searching. Malar J 2 32

69. KilleenGF

SeyoumA

KnolsBG

2004 Rationalizing historical successes of malaria control in Africa in terms of mosquito resource availability management. Am J Trop Med Hyg 71 87 93

70. KulkarniMA

KwekaE

NyaleE

LyatuuE

MoshaFW

2006 Entomological evaluation of malaria vectors at different altitudes in Hai district, northeastern Tanzania. J Med Entomol 43 580 588

71. FornadelCM

NorrisDE

2008 Increased endophily by the malaria vector Anopheles arabiensis in southern Zambia and identification of digested blood meals. Am J Trop Med Hyg 79 876 880

72. RowlandM

DurraniN

KenwardM

MohammedN

UrahmanH

2001 Control of malaria in Pakistan by applying deltamethrin insecticide to cattle: a community-randomised trial. Lancet 357 1837 1841

73. OkumuFO

MadumlaEP

JohnAN

LwetoijeraDW

SumayeRD

2010 Attracting, trapping and killing disease-transmitting mosquitoes using odor-baited stations - The Ifakara Odor-Baited Stations. Parasit Vectors 3 12

74. KnolsBG

BukhariT

FarenhorstM

2010 Entomopathogenic fungi as the next-generation control agents against malaria mosquitoes. Future Microbiol 5 339 341

75. MullerGC

SchleinY

2008 Efficacy of toxic sugar baits against adult cistern-dwelling Anopheles claviger. Trans R Soc Trop Med Hyg 102 480 484

76. DevineGJ

PereaEZ

KilleenGF

StancilJD

ClarkSJ

2009 Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci U S A 106 11530 11534

77. FillingerU

NdengaB

GithekoA

LindsaySW

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

78. GovellaNJ

OkumuFO

KilleenGF

2010 Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg 82 415 419

79. GilliesMT

SmithA

1960 Effect of a residual house-spraying campaign on species balance in the Anopheles funestus group: the replacement of Anopheles gambie Giles with Anopheles rivulorum Leeson. Bull Entomol Res 55 1 16

80. LindbladeKA

GimnigJE

KamauL

HawleyWA

OdhiamboF

2006 Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol 43 428 432

81. BayohMN

MathiasDK

OdiereMR

MutukuFM

KamauL

2010 Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9 62

82. Roll Back Malaria Working Group 2009 Guidelines for Core Population Indicators. Available: http://www.rollbackmalaria.org/partnership/wg/wg_monitoring/docs/GuidelinesForCorePopulationFINAL9-20_Malaria.pdf. Accessed: 29 January 2010

83. NoorAM

MutheuJJ

TatemAJ

HaySI

SnowRW

2009 Insecticide-treated net coverage in Africa: mapping progress in 2000-07. Lancet 373 58 67

84. CarterR

MendisKN

RobertsD

2000 Spatial targeting of interventions against malaria. Bull World Health Organ 78 1401 1411

85. BousemaT

DrakeleyC

GesaseS

HashimR

MagesaS

2010 Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201 1764 1774

86. KilleenGF

TamiA

KihondaJ

OkumuFO

KotasME

2007 Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero Valley, southern Tanzania. BMC Infect Dis 7 121

87. KhatibRA

KilleenGF

AbdullaSM

KahigwaE

McElroyPD

2008 Markets, voucher subsidies and free nets combine to achieve high bed net coverage in rural Tanzania. Malar J 7 98

88. KulkarniMA

Vanden EngJ

DesrochersRE

CotteAH

GoodsonJL

2010 Contribution of integrated campaign distribution of long-lasting insecticidal nets to coverage of target groups and total populations in malaria-endemic areas in Madagascar. Am J Trop Med Hyg 82 420 425

89. HemingwayJ

RansonH

2000 Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45 371 391

90. DondorpAM

NostenF

YiP

DasD

PhyoAP

2009 Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361 455 467

91. GilksWR

RichardsonS

SpiegelhalterDJ

1996 Markov chain Monte Carlo in practice Chapman & Hall

92. BernardoJM

SmithAFM

1994 Bayesian theory Wiley

93. YeY

HoshenM

KyobutungiC

LouisVR

SauerbornR

2009 Local scale prediction of Plasmodium falciparum malaria transmission in an endemic region using temperature and rainfall. Glob Health Action 2

94. SiriJG

WilsonML

MurrayS

RosenDH

VululeJM

2010 Significance of travel to rural areas as a risk factor for malarial anemia in an urban setting. Am J Trop Med Hyg 82 391 397

95. TatemAJ

NoorAM

von HagenC

Di GregorioA

HaySI

2007 High resolution population maps for low income nations: combining land cover and census in East Africa. PLoS One 2 e1298

96. TatemAJ

RileyS

2007 Effect of poor census data on population maps. Science 318 43

97. CohuetA

SimardF

WondjiCS

Antonio-NkondjioC

Awono-AmbeneP

2004 High malaria transmission intensity due to Anopheles funestus (Diptera: Culicidae) in a village of savannah-forest transition area in Cameroon. J Med Entomol 41 901 905

98. KarchS

GarinB

AsidiN

ManzambiZ

SalaunJJ

1993 [Mosquito nets impregnated against malaria in Zaire]. Ann Soc Belg Med Trop 73 37 53

99. AppawuM

Owusu-AgyeiS

DadzieS

AsoalaV

AntoF

2004 Malaria transmission dynamics at a site in northern Ghana proposed for testing malaria vaccines. Trop Med Int Health 9 164 170

100. MendisC

JacobsenJL

Gamage-MendisA

BuleE

DgedgeM

2000 Anopheles arabiensis and An. funestus are equally important vectors of malaria in Matola coastal suburb of Maputo, southern Mozambique. Med Vet Entomol 14 171 180

101. ShiffCJ

MinjasJN

HallT

HuntRH

LyimoS

1995 Malaria infection potential of anopheline mosquitoes sampled by light trapping indoors in coastal Tanzanian villages. Med Vet Entomol 9 256 262

102. OkelloPE

Van BortelW

ByaruhangaAM

CorrewynA

RoelantsP

2006 Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg 75 219 225