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Published in: Malaria Journal 1/2020

Open Access 01-12-2020 | Malaria | Research

Variation in Anopheles distribution and predictors of malaria infection risk across regions of Madagascar

Authors: Nicholas J. Arisco, Benjamin L. Rice, Luciano M. Tantely, Romain Girod, Gauthier N. Emile, Hervet J. Randriamady, Marcia C. Castro, Christopher D. Golden

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Deforestation and land use change is widespread in Madagascar, altering local ecosystems and creating opportunities for disease vectors, such as the Anopheles mosquito, to proliferate and more easily reach vulnerable, rural populations. Knowledge of risk factors associated with malaria infections is growing globally, but these associations remain understudied across Madagascar’s diverse ecosystems experiencing rapid environmental change. This study aims to uncover socioeconomic, demographic, and ecological risk factors for malaria infection across regions through analysis of a large, cross-sectional dataset.

Methods

The objectives were to assess (1) the ecological correlates of malaria vector breeding through larval surveys, and (2) the socioeconomic, demographic, and ecological risk factors for malaria infection in four ecologically distinct regions of rural Madagascar. Risk factors were determined using multilevel models for the four regions included in the study.

Results

The presence of aquatic agriculture (both within and surrounding communities) is the strongest predictive factor of habitats containing Anopheles larvae across all regions. Ecological and socioeconomic risk factors for malaria infection vary dramatically across study regions and range in their complexity.

Conclusions

Risk factors for malaria transmission differ dramatically across regions of Madagascar. These results may help stratifying current malaria control efforts in Madagascar beyond the scope of existing interventions.
Appendix
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Literature
1.
go back to reference Myers SS, Gaffikin L, Golden CD, Ostfeld RS, Redford KH, Ricketts TH, et al. Human health impacts of ecosystem alteration. Proc Natl Acad Sci USA. 2013;110:18753–60.PubMedCrossRefPubMedCentral Myers SS, Gaffikin L, Golden CD, Ostfeld RS, Redford KH, Ricketts TH, et al. Human health impacts of ecosystem alteration. Proc Natl Acad Sci USA. 2013;110:18753–60.PubMedCrossRefPubMedCentral
2.
go back to reference Mutero CM, Kabutha C, Kimani V, Kabuage L, Gitau G, Ssennyonga J, et al. A transdisciplinary perspective on the links between malaria and agroecosystems in Kenya. Acta Trop. 2004;89:171–86.PubMedCrossRef Mutero CM, Kabutha C, Kimani V, Kabuage L, Gitau G, Ssennyonga J, et al. A transdisciplinary perspective on the links between malaria and agroecosystems in Kenya. Acta Trop. 2004;89:171–86.PubMedCrossRef
3.
go back to reference Gottdenker NL, Streicker DG, Faust CL, Carroll C. Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth. 2014;11:619–32.PubMedCrossRef Gottdenker NL, Streicker DG, Faust CL, Carroll C. Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth. 2014;11:619–32.PubMedCrossRef
4.
go back to reference Yasuoka J, Levins R. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg. 2007;76:450–60.PubMedCrossRef Yasuoka J, Levins R. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg. 2007;76:450–60.PubMedCrossRef
5.
go back to reference Grillet ME. Factors associated with distribution of Anopheles aquasalis and Anopheles oswaldoi (Diptera: Culicidae) in a malarious area, northeastern Venezuela. J Med Entomol. 2000;37:231–8.PubMedCrossRef Grillet ME. Factors associated with distribution of Anopheles aquasalis and Anopheles oswaldoi (Diptera: Culicidae) in a malarious area, northeastern Venezuela. J Med Entomol. 2000;37:231–8.PubMedCrossRef
6.
go back to reference Afrane YA, Githeko AK, Yan G. The ecology of Anopheles mosquitoes under climate change: case studies from the effects of environmental changes in east Africa highlands. Ann N Y Acad Sci. 2012;1249:204.PubMedPubMedCentralCrossRef Afrane YA, Githeko AK, Yan G. The ecology of Anopheles mosquitoes under climate change: case studies from the effects of environmental changes in east Africa highlands. Ann N Y Acad Sci. 2012;1249:204.PubMedPubMedCentralCrossRef
7.
go back to reference Singer BH, de Castro MC. Agricultural colonization and malaria on the Amazon frontier. Ann N Y Acad Sci. 2001;954:184–222.PubMedCrossRef Singer BH, de Castro MC. Agricultural colonization and malaria on the Amazon frontier. Ann N Y Acad Sci. 2001;954:184–222.PubMedCrossRef
8.
go back to reference Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg. 2006;74:772–8.PubMedCrossRef Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg. 2006;74:772–8.PubMedCrossRef
9.
go back to reference Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, et al. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006;74:3–11.CrossRefPubMed Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, et al. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006;74:3–11.CrossRefPubMed
10.
go back to reference Vittor AY, Pan W, Gilman RH, Tielsch J, Glass G, Shields T, et al. Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg. 2009;81:5–12.PubMedCrossRef Vittor AY, Pan W, Gilman RH, Tielsch J, Glass G, Shields T, et al. Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg. 2009;81:5–12.PubMedCrossRef
11.
go back to reference Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, et al. Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012;11:122.PubMedPubMedCentralCrossRef Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, et al. Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012;11:122.PubMedPubMedCentralCrossRef
12.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.PubMedPubMedCentralCrossRef Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.PubMedPubMedCentralCrossRef
13.
go back to reference Allnutt TF, Asner GP, Golden CD, Powell GV. Mapping recent deforestation and forest disturbance in northeastern Madagascar. Trop Cons Sci. 2013;6:1–15.CrossRef Allnutt TF, Asner GP, Golden CD, Powell GV. Mapping recent deforestation and forest disturbance in northeastern Madagascar. Trop Cons Sci. 2013;6:1–15.CrossRef
14.
go back to reference Vieilledent G, Grinand C, Rakotomalala FA, Ranaivosoa R, Rakotoarijaona J-R, Allnutt TF, et al. Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Bio Cons. 2018;222:189–97.CrossRef Vieilledent G, Grinand C, Rakotomalala FA, Ranaivosoa R, Rakotoarijaona J-R, Allnutt TF, et al. Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Bio Cons. 2018;222:189–97.CrossRef
15.
go back to reference Zinner D, Wygoda C, Razafimanantsoa L, Rasoloarison R, Andrianandrasana HT, Ganzhorn JU, et al. Analysis of deforestation patterns in the central Menabe, Madagascar, between 1973 and 2010. Reg Environ Change. 2014;14:157–66.CrossRef Zinner D, Wygoda C, Razafimanantsoa L, Rasoloarison R, Andrianandrasana HT, Ganzhorn JU, et al. Analysis of deforestation patterns in the central Menabe, Madagascar, between 1973 and 2010. Reg Environ Change. 2014;14:157–66.CrossRef
16.
go back to reference Vågen T-G. Remote sensing of complex land use change trajectories—a case study from the highlands of Madagascar. Agr Eco Env. 2006;115:219–28.CrossRef Vågen T-G. Remote sensing of complex land use change trajectories—a case study from the highlands of Madagascar. Agr Eco Env. 2006;115:219–28.CrossRef
18.
go back to reference Girond F, Randrianasolo L, Randriamampionona L, Rakotomanana F, Randrianarivelojosia M, Ratsitorahina M, et al. Analysing trends and forecasting malaria epidemics in Madagascar using a sentinel surveillance network: a web-based application. Malar J. 2017;16:72.PubMedPubMedCentralCrossRef Girond F, Randrianasolo L, Randriamampionona L, Rakotomanana F, Randrianarivelojosia M, Ratsitorahina M, et al. Analysing trends and forecasting malaria epidemics in Madagascar using a sentinel surveillance network: a web-based application. Malar J. 2017;16:72.PubMedPubMedCentralCrossRef
19.
go back to reference Howes RE, Mioramalala SA, Ramiranirina B, Franchard T, Rakotorahalahy AJ, Bisanzio D, et al. Contemporary epidemiological overview of malaria in Madagascar: operational utility of reported routine case data for malaria control planning. Malar J. 2016;15:502.PubMedPubMedCentralCrossRef Howes RE, Mioramalala SA, Ramiranirina B, Franchard T, Rakotorahalahy AJ, Bisanzio D, et al. Contemporary epidemiological overview of malaria in Madagascar: operational utility of reported routine case data for malaria control planning. Malar J. 2016;15:502.PubMedPubMedCentralCrossRef
20.
go back to reference Ihantamalala FA, Rakotoarimanana FM, Ramiadantsoa T, Rakotondramanga JM, Pennober G, Rakotomanana F, et al. Spatial and temporal dynamics of malaria in Madagascar. Malar J. 2018;17:58.PubMedPubMedCentralCrossRef Ihantamalala FA, Rakotoarimanana FM, Ramiadantsoa T, Rakotondramanga JM, Pennober G, Rakotomanana F, et al. Spatial and temporal dynamics of malaria in Madagascar. Malar J. 2018;17:58.PubMedPubMedCentralCrossRef
21.
go back to reference Madagascar NMCP. National strategic plan for malaria control in Madagascar 2013–2017: consolidating the gains with a view to elimination of malaria from Madagascar, 2015–2017 revision. Antananarive, 2015. Madagascar NMCP. National strategic plan for malaria control in Madagascar 2013–2017: consolidating the gains with a view to elimination of malaria from Madagascar, 2015–2017 revision. Antananarive, 2015.
22.
go back to reference Kesteman T, Randrianarivelojosia M, Raharimanga V, Randrianasolo L, Piola P, Rogier C. Effectiveness of malaria control interventions in Madagascar: a nationwide case–control survey. Malar J. 2016;15:83.PubMedPubMedCentralCrossRef Kesteman T, Randrianarivelojosia M, Raharimanga V, Randrianasolo L, Piola P, Rogier C. Effectiveness of malaria control interventions in Madagascar: a nationwide case–control survey. Malar J. 2016;15:83.PubMedPubMedCentralCrossRef
23.
go back to reference Kesteman T, Rafalimanantsoa SA, Razafimandimby H, Rasamimanana HH, Raharimanga V, Ramarosandratana B, et al. Multiple causes of an unexpected malaria outbreak in a high-transmission area in Madagascar. Malar J. 2016;15:57.PubMedPubMedCentralCrossRef Kesteman T, Rafalimanantsoa SA, Razafimandimby H, Rasamimanana HH, Raharimanga V, Ramarosandratana B, et al. Multiple causes of an unexpected malaria outbreak in a high-transmission area in Madagascar. Malar J. 2016;15:57.PubMedPubMedCentralCrossRef
24.
go back to reference Golden CD, Fernald LC, Brashares JS, Rasolofoniaina BR, Kremen C. Benefits of wildlife consumption to child nutrition in a biodiversity hotspot. Proc Natl Acad Sci USA. 2011;108:19653–6.PubMedCrossRefPubMedCentral Golden CD, Fernald LC, Brashares JS, Rasolofoniaina BR, Kremen C. Benefits of wildlife consumption to child nutrition in a biodiversity hotspot. Proc Natl Acad Sci USA. 2011;108:19653–6.PubMedCrossRefPubMedCentral
25.
go back to reference Funari E, Testai E. Human health risk assessment related to cyanotoxins exposure. Crit Rev Tox. 2008;38:97–125.CrossRef Funari E, Testai E. Human health risk assessment related to cyanotoxins exposure. Crit Rev Tox. 2008;38:97–125.CrossRef
26.
go back to reference Bandyopadhyay S, Kanji S, Wang L. The impact of rainfall and temperature variation on diarrheal prevalence in Sub-Saharan Africa. Appl Geogr. 2012;33:63–72.CrossRef Bandyopadhyay S, Kanji S, Wang L. The impact of rainfall and temperature variation on diarrheal prevalence in Sub-Saharan Africa. Appl Geogr. 2012;33:63–72.CrossRef
27.
go back to reference Goodman S, Raherilalao M, Wohlhauser S. The terrestrial protected areas of Madagascar: their history, description, and biota. Antananarivo: Association Vahatra; 2018. Goodman S, Raherilalao M, Wohlhauser S. The terrestrial protected areas of Madagascar: their history, description, and biota. Antananarivo: Association Vahatra; 2018.
28.
go back to reference Zohdy S, Derfus K, Headrick EG, Andrianjafy MT, Wright PC, Gillespie TR. Small-scale land-use variability affects Anopheles spp. distribution and concomitant Plasmodium infection in humans and mosquito vectors in southeastern Madagascar. Malar J. 2016;15:114.PubMedPubMedCentralCrossRef Zohdy S, Derfus K, Headrick EG, Andrianjafy MT, Wright PC, Gillespie TR. Small-scale land-use variability affects Anopheles spp. distribution and concomitant Plasmodium infection in humans and mosquito vectors in southeastern Madagascar. Malar J. 2016;15:114.PubMedPubMedCentralCrossRef
29.
go back to reference Kesteman T, Randrianarivelojosia M, Mattern C, Raboanary E, Pourette D, Girond F, et al. Nationwide evaluation of malaria infections, morbidity, mortality, and coverage of malaria control interventions in Madagascar. Malar J. 2014;13:465.PubMedPubMedCentralCrossRef Kesteman T, Randrianarivelojosia M, Mattern C, Raboanary E, Pourette D, Girond F, et al. Nationwide evaluation of malaria infections, morbidity, mortality, and coverage of malaria control interventions in Madagascar. Malar J. 2014;13:465.PubMedPubMedCentralCrossRef
30.
31.
go back to reference Mitchell SN, Kakani EG, South A, Howell PI, Waterhouse RM, Catteruccia F. Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science. 2015;347:985–8.PubMedPubMedCentralCrossRef Mitchell SN, Kakani EG, South A, Howell PI, Waterhouse RM, Catteruccia F. Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science. 2015;347:985–8.PubMedPubMedCentralCrossRef
32.
go back to reference Rubio-Palis Y. Variation of the vectorial capacity of some anophelines in western Venezuela. Am J Trop Med Hyg. 1994;50:420–4.PubMedCrossRef Rubio-Palis Y. Variation of the vectorial capacity of some anophelines in western Venezuela. Am J Trop Med Hyg. 1994;50:420–4.PubMedCrossRef
33.
go back to reference Omlin FX, Carlson JC, Ogbunugafor CB, Hassanali A. Anopheles gambiae exploits the treehole ecosystem in western Kenya: a new urban malaria risk? Am J Trop Med Hyg. 2007;77(6_Suppl):264–9.PubMedCrossRef Omlin FX, Carlson JC, Ogbunugafor CB, Hassanali A. Anopheles gambiae exploits the treehole ecosystem in western Kenya: a new urban malaria risk? Am J Trop Med Hyg. 2007;77(6_Suppl):264–9.PubMedCrossRef
34.
go back to reference Kang SY, Battle KE, Gibson HS, Ratsimbasoa A, Randrianarivelojosia M, Ramboarina S, et al. Spatio-temporal mapping of Madagascar’s Malaria Indicator Survey results to assess Plasmodium falciparum endemicity trends between 2011 and 2016. BMC Med. 2018;16:71.PubMedPubMedCentralCrossRef Kang SY, Battle KE, Gibson HS, Ratsimbasoa A, Randrianarivelojosia M, Ramboarina S, et al. Spatio-temporal mapping of Madagascar’s Malaria Indicator Survey results to assess Plasmodium falciparum endemicity trends between 2011 and 2016. BMC Med. 2018;16:71.PubMedPubMedCentralCrossRef
35.
go back to reference Golden CD, Rice BL, Randriamady HJ, Vonona AM, Randrianasolo JF, Tafangy AN, et al. Study protocol: a cross-sectional examination of socio-demographic and ecological determinants of nutrition and disease across Madagascar. Frontiers Publ Health. 2020;8(500). Golden CD, Rice BL, Randriamady HJ, Vonona AM, Randrianasolo JF, Tafangy AN, et al. Study protocol: a cross-sectional examination of socio-demographic and ecological determinants of nutrition and disease across Madagascar. Frontiers Publ Health. 2020;8(500).
36.
go back to reference Moat J, Smith PP. Atlas of the vegetation of Madagascar. Royal Botanic Gardens, Kew; 2007. Moat J, Smith PP. Atlas of the vegetation of Madagascar. Royal Botanic Gardens, Kew; 2007.
37.
go back to reference Deen J, Walraven G, Von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Ped. 2002;48:78–83.CrossRef Deen J, Walraven G, Von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Ped. 2002;48:78–83.CrossRef
38.
go back to reference Ghinai I, Cook J, Hla TTW, Htet HMT, Hall T, Lubis IN, et al. Malaria epidemiology in central Myanmar: identification of a multi-species asymptomatic reservoir of infection. Malar J. 2017;16:16.PubMedPubMedCentralCrossRef Ghinai I, Cook J, Hla TTW, Htet HMT, Hall T, Lubis IN, et al. Malaria epidemiology in central Myanmar: identification of a multi-species asymptomatic reservoir of infection. Malar J. 2017;16:16.PubMedPubMedCentralCrossRef
39.
go back to reference Koram KA, Owusu-Agyei S, Fryauff DJ, Anto F, Atuguba F, Hodgson A, et al. Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana. Trop Med Int Health. 2003;8:793–802.PubMedCrossRef Koram KA, Owusu-Agyei S, Fryauff DJ, Anto F, Atuguba F, Hodgson A, et al. Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana. Trop Med Int Health. 2003;8:793–802.PubMedCrossRef
40.
go back to reference WHO. World Malaria Report 2018. Geneva: World Health Organization; 2018. WHO. World Malaria Report 2018. Geneva: World Health Organization; 2018.
41.
go back to reference Mariette N, Barnadas C, Bouchier C, Tichit M, Ménard D. Country-wide assessment of the genetic polymorphism in Plasmodium falciparum and Plasmodium vivax antigens detected with rapid diagnostic tests for malaria. Malar J. 2008;7:219.PubMedPubMedCentralCrossRef Mariette N, Barnadas C, Bouchier C, Tichit M, Ménard D. Country-wide assessment of the genetic polymorphism in Plasmodium falciparum and Plasmodium vivax antigens detected with rapid diagnostic tests for malaria. Malar J. 2008;7:219.PubMedPubMedCentralCrossRef
42.
go back to reference Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef
43.
go back to reference Willie N, Mehlotra RK, Howes RE, Rakotomanga TA, Ramboarina S, Ratsimbasoa AC, et al. Insights into the performance of SD Bioline Malaria Ag Pf/Pan rapid diagnostic test and Plasmodium falciparum histidine-rich protein 2 gene variation in Madagascar. Am J Trop Med Hyg. 2018;98:1683–91.PubMedPubMedCentralCrossRef Willie N, Mehlotra RK, Howes RE, Rakotomanga TA, Ramboarina S, Ratsimbasoa AC, et al. Insights into the performance of SD Bioline Malaria Ag Pf/Pan rapid diagnostic test and Plasmodium falciparum histidine-rich protein 2 gene variation in Madagascar. Am J Trop Med Hyg. 2018;98:1683–91.PubMedPubMedCentralCrossRef
44.
go back to reference Mehlotra RK, Howes RE, Cramer EY, Tedrow RE, Rakotomanga TA, Ramboarina S, et al. Plasmodium falciparum parasitemia and band sensitivity of the SD Bioline Malaria Ag Pf/Pan rapid diagnostic test in Madagascar. Am J Trop Med Hyg. 2019;100:1196–201.PubMedPubMedCentralCrossRef Mehlotra RK, Howes RE, Cramer EY, Tedrow RE, Rakotomanga TA, Ramboarina S, et al. Plasmodium falciparum parasitemia and band sensitivity of the SD Bioline Malaria Ag Pf/Pan rapid diagnostic test in Madagascar. Am J Trop Med Hyg. 2019;100:1196–201.PubMedPubMedCentralCrossRef
45.
go back to reference Tsy J-MLP, Duchemin J-B, Marrama L, Rabarison P, Le Goff G, Rajaonarivelo V, et al. Distribution of the species of the Anopheles gambiae complex and first evidence of Anopheles merus as a malaria vector in Madagascar. Malar J. 2003;2:33.CrossRef Tsy J-MLP, Duchemin J-B, Marrama L, Rabarison P, Le Goff G, Rajaonarivelo V, et al. Distribution of the species of the Anopheles gambiae complex and first evidence of Anopheles merus as a malaria vector in Madagascar. Malar J. 2003;2:33.CrossRef
46.
go back to reference Grjébine A. Faune de Madagascar: Insectes Dipteres Culicidae Anophelinae. XXII. ORSTOM; 1966. Grjébine A. Faune de Madagascar: Insectes Dipteres Culicidae Anophelinae. XXII. ORSTOM; 1966.
47.
go back to reference Lourenço PM, Sousa CA, Seixas J, Lopes P, Novo MT, Almeida APG. Anopheles atroparvus density modeling using MODIS NDVI in a former malarious area in Portugal. J Vector Ecol. 2011;36:279–91.PubMedCrossRef Lourenço PM, Sousa CA, Seixas J, Lopes P, Novo MT, Almeida APG. Anopheles atroparvus density modeling using MODIS NDVI in a former malarious area in Portugal. J Vector Ecol. 2011;36:279–91.PubMedCrossRef
48.
go back to reference Huang J, Walker E, Giroux P, Vulule J, Miller J. Ovipositional site selection by Anopheles gambiae: influences of substrate moisture and texture. Med Vet Entomol. 2005;19:442–50.PubMedCrossRef Huang J, Walker E, Giroux P, Vulule J, Miller J. Ovipositional site selection by Anopheles gambiae: influences of substrate moisture and texture. Med Vet Entomol. 2005;19:442–50.PubMedCrossRef
49.
go back to reference Koenraadt C, Githeko A, Takken W. The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop. 2004;90:141–53.PubMedCrossRef Koenraadt C, Githeko A, Takken W. The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop. 2004;90:141–53.PubMedCrossRef
50.
go back to reference Wood B, Washino R, Beck L, Hibbard K, Pitcairn M, Roberts D, et al. Distinguishing high and low anopheline-producing rice fields using remote sensing and GIS technologies. Prev Vet Med. 1991;11:277–88.CrossRef Wood B, Washino R, Beck L, Hibbard K, Pitcairn M, Roberts D, et al. Distinguishing high and low anopheline-producing rice fields using remote sensing and GIS technologies. Prev Vet Med. 1991;11:277–88.CrossRef
51.
go back to reference Team RC. R: A language and environment for statistical computing. 2013. Team RC. R: A language and environment for statistical computing. 2013.
52.
go back to reference Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Stat Softw. 2017;82:26637.CrossRef Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Stat Softw. 2017;82:26637.CrossRef
53.
go back to reference Verdonschot PF, Besse-Lototskaya AA. Flight distance of mosquitoes (Culicidae): a metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica. 2014;45:69–79.CrossRef Verdonschot PF, Besse-Lototskaya AA. Flight distance of mosquitoes (Culicidae): a metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica. 2014;45:69–79.CrossRef
54.
go back to reference Koumba AA, Koumba CRZ, Nguema RM, Djogbenou LS, Ondo PO, Ketoh GK, et al. Distribution spatiale et saisonnière des gîtes larvaires des moustiques dans les espaces agricoles de la zone de Mouila. Gabon. Int J Biol Chem Sci. 2018;12:1754–69.CrossRef Koumba AA, Koumba CRZ, Nguema RM, Djogbenou LS, Ondo PO, Ketoh GK, et al. Distribution spatiale et saisonnière des gîtes larvaires des moustiques dans les espaces agricoles de la zone de Mouila. Gabon. Int J Biol Chem Sci. 2018;12:1754–69.CrossRef
55.
go back to reference Fontenille D, Campbell GH. Is Anopheles mascarensis a new malaria vector in Madagascar? Am J Trop Med Hyg. 1992;46:28–30.PubMedCrossRef Fontenille D, Campbell GH. Is Anopheles mascarensis a new malaria vector in Madagascar? Am J Trop Med Hyg. 1992;46:28–30.PubMedCrossRef
56.
57.
go back to reference Marrama L, Rajaonarivelo E, Laventure S, Rabarison P. Anopheles funestus et la riziculture sur les plateaux de Madagascar. Cahiers d’études et de recherches francophones/Santé. 1995;5:415–9. Marrama L, Rajaonarivelo E, Laventure S, Rabarison P. Anopheles funestus et la riziculture sur les plateaux de Madagascar. Cahiers d’études et de recherches francophones/Santé. 1995;5:415–9.
58.
go back to reference PNLP Madagascar. Enquête sur les Indicateurs du Paludisme (EIPM). Antananarive, 2013. PNLP Madagascar. Enquête sur les Indicateurs du Paludisme (EIPM). Antananarive, 2013.
59.
go back to reference Randriamahefasoa T, Reason C. Interannual variability of rainfall characteristics over southwestern Madagascar. Theor Appl Climatol. 2017;128:421–37.CrossRef Randriamahefasoa T, Reason C. Interannual variability of rainfall characteristics over southwestern Madagascar. Theor Appl Climatol. 2017;128:421–37.CrossRef
60.
go back to reference Boonserm P, Ellar DJ, Li J. Crystallization and preliminary X-ray diffraction studies of a mosquito-larvicidal toxin from Bacillus thuringiensis subsp. israelensis. Acta Crystallogr D Biol Crystallogr. 2003;59:591–4.PubMedCrossRef Boonserm P, Ellar DJ, Li J. Crystallization and preliminary X-ray diffraction studies of a mosquito-larvicidal toxin from Bacillus thuringiensis subsp. israelensis. Acta Crystallogr D Biol Crystallogr. 2003;59:591–4.PubMedCrossRef
61.
go back to reference Rakotomanana F, Ratovonjato J, Randremanana RV, Randrianasolo L, Raherinjafy R, Rudant J-P, et al. Geographical and environmental approaches to urban malaria in Antananarivo (Madagascar). BMC Inf Dis. 2010;10:173.CrossRef Rakotomanana F, Ratovonjato J, Randremanana RV, Randrianasolo L, Raherinjafy R, Rudant J-P, et al. Geographical and environmental approaches to urban malaria in Antananarivo (Madagascar). BMC Inf Dis. 2010;10:173.CrossRef
62.
go back to reference Slutsker L, Taylor TE, Wirima JJ, Steketee RW. In-hospital morbidity and mortality due to malaria-associated severe anaemia in two areas of Malawi with different patterns of malaria infection. Trans R Soc Trop Med Hyg. 1994;88:548–51.PubMedCrossRef Slutsker L, Taylor TE, Wirima JJ, Steketee RW. In-hospital morbidity and mortality due to malaria-associated severe anaemia in two areas of Malawi with different patterns of malaria infection. Trans R Soc Trop Med Hyg. 1994;88:548–51.PubMedCrossRef
63.
go back to reference WHO. Report of the informal consultation on stratification for planning antimalaria action. Geneva: World Health Organizaton; 1985. WHO. Report of the informal consultation on stratification for planning antimalaria action. Geneva: World Health Organizaton; 1985.
64.
go back to reference Cox J, Sovannaroth S, Soley LD, Ngor P, Mellor S, Roca-Feltrer A. Novel approaches to risk stratification to support malaria elimination: an example from Cambodia. Malar J. 2014;13:371.PubMedPubMedCentralCrossRef Cox J, Sovannaroth S, Soley LD, Ngor P, Mellor S, Roca-Feltrer A. Novel approaches to risk stratification to support malaria elimination: an example from Cambodia. Malar J. 2014;13:371.PubMedPubMedCentralCrossRef
65.
go back to reference Pullan RL, Sturrock HJ, Magalhaes RJS, Clements AC, Brooker SJ. Spatial parasite ecology and epidemiology: a review of methods and applications. Parasitology. 2012;139:1870–87.PubMedCrossRef Pullan RL, Sturrock HJ, Magalhaes RJS, Clements AC, Brooker SJ. Spatial parasite ecology and epidemiology: a review of methods and applications. Parasitology. 2012;139:1870–87.PubMedCrossRef
Metadata
Title
Variation in Anopheles distribution and predictors of malaria infection risk across regions of Madagascar
Authors
Nicholas J. Arisco
Benjamin L. Rice
Luciano M. Tantely
Romain Girod
Gauthier N. Emile
Hervet J. Randriamady
Marcia C. Castro
Christopher D. Golden
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03423-1

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