Studying relationships between environment and malaria incidence in Camopi (French Guiana) through the objective selection of buffer-based landscape characterisations
Tóm tắt
Malaria remains a major health problem in French Guiana, with a mean of 3800 cases each year. A previous study in Camopi, an Amerindian village on the Oyapock River, highlighted the major contribution of environmental features to the incidence of malaria attacks. We propose a method for the objective selection of the best multivariate peridomestic landscape characterisation that maximises the chances of identifying relationships between environmental features and malaria incidence, statistically significant and meaningful from an epidemiological point of view. A land-cover map, the hydrological network and the geolocalised inhabited houses were used to characterise the peridomestic landscape in eleven discoid buffers with radii of 50, 100, 200, 300, 400, 500, 600, 700, 800, 900 and 1000 metres. Buffer-based landscape characterisations were first compared in terms of their capacity to discriminate between sites within the geographic space and of their effective multidimensionality in variable space. The Akaike information criterion (AIC) was then used to select the landscape model best explaining the incidences of P. vivax and P. falciparum malaria. Finally, we calculated Pearson correlation coefficients for the relationships between environmental variables and malaria incidence, by species, for the more relevant buffers. The optimal buffers for environmental characterisation had radii of 100 m around houses for P. vivax and 400 m around houses for P. falciparum. The incidence of P. falciparum malaria seemed to be more strongly linked to environmental features than that of P. vivax malaria, within these buffers. The incidence of P. falciparum malaria in children was strongly correlated with proportions of bare soil (r = -0.69), land under high vegetation (r = 0.68) and primary forest (r = 0.54), landscape division (r = 0.48) and the number of inhabited houses (r = -0.60). The incidence of P. vivax malaria was associated only with landscape division (r = 0.49). The proposed methodology provides a simple and general framework for objective characterisation of the landscape to account for field observations. The use of this method enabled us to identify different optimal observation horizons around houses, depending on the Plasmodium species considered, and to demonstrate significant correlations between environmental features and the incidence of malaria.
Tài liệu tham khảo
Carme B, Ardillon V, Girod R, Grenier C, Joubert M, Djossou F, Ravachol F: [Update on the epidemiology of malaria in French Guiana] (in French). Med Trop. 2009, 69: 19-25.
Hustache S, Nacher M, Djossou F, Carme B: Malaria risk factors in Amerindian children in French Guiana. Am J Trop Med Hyg. 2007, 76: 619-625.
Floch H: La lutte antipaludique en Guyane française. L'anophélisme. Riv Malariol. 1955, 24: 57-65.
Mouchet J, Nadire-Galliot M, Poman JP, Claustre J, Bellony S: Le paludisme en Guyane. Les caractéristiques des différents foyers et la lutte antipaludique. Bull Soc Pathol Exot. 1989, 82: 393-405.
Pajot F-X, Le Pont F, Molez J-F, Degallier N: Agressivité d'Anopheles (Nyssorhuynchus) darlingi Root, 1926 (Diptera, Culicidae) en Guyane française. Cah ORSTOM, sér Ent méd et Parasitol. 1977, 15: 15-22.
Girod R, Roux E, Berger F, Stefani A, Gaborit P, Carinci R, Issaly J, Carme B, Dusfour I: Unravelling the relationships between Anopheles darlingi (Diptera: Culicidae) densities, environmental factors and malaria incidence: understanding the variable patterns of malarial transmission in French Guiana (South America). Ann Trop Med Parasitol. 2011, 105: 107-122. 10.1179/136485911X12899838683322.
Charlwood JD, Alecrim WA: Capture-recapture studies with the South American malaria vector Anopheles darlingi, Root. Ann Trop Med Parasitol. 1989, 83: 569-576.
Basurko C, Hanf M, Han-Sze R, Rogier S, Héritier P, Grenier C, Joubert M, Nacher M, Carme B: Influence of climate and river level on the incidence of malaria in Cacao, French Guiana. Malar J. 2011, 10: 26-10.1186/1475-2875-10-26.
Beck LR, Lobitz BM, Wood BL: Remote sensing and human health: new sensors and new opportunities. Emerging Infect Dis. 2000, 6: 217-227. 10.3201/eid0603.000301.
Herbreteau V, Salem G, Souris M, Hugot J-P, Gonzalez J-P: Thirty years of use and improvement of remote sensing, applied to epidemiology: from early promises to lasting frustration. Health Place. 2007, 13: 400-403. 10.1016/j.healthplace.2006.03.003.
Beck LR, Rodriguez MH, Dister SW, Rodriguez AD, Rejmankova E, Ulloa A, Meza RA, Roberts DR, Paris JF, Spanner MA: Remote sensing as a landscape epidemiologic tool to identify villages at high risk for malaria transmission. Am J Trop Med Hyg. 1994, 51: 271-280.
Beck LR, Rodriguez MH, Dister SW, Rodriguez AD, Washino RK, Roberts DR, Spanner MA: Assessment of a remote sensing-based model for predicting malaria transmission risk in villages of Chiapas, Mexico. Am J Trop Med Hyg. 1997, 56: 99-106.
Achee NL, Grieco JP, Masuoka P, Andre RG, Roberts DR, Thomas J, Briceno I, King R, Rejmankova E: Use of remote sensing and geographic information systems to predict locations of Anopheles darlingi-positive breeding sites within the Sibun River in Belize, Central America. J Med Entomol. 2006, 43: 382-392. 10.1603/0022-2585(2006)043[0382:UORSAG]2.0.CO;2.
Pope KO, Rejmankova E, Savage HM, Arredondo-Jimenez JI, Rodriguez MH, Roberts DR: Remote sensing of tropical wetlands for malaria control in Chiapas, Mexico. Ecol Appl. 1994, 4: 81-90. 10.2307/1942117.
Rakotomanana F, Jeanne I, Duchemin JB, Pietra V, Raharimalala L, Tombo ML, Ariey F: Approche géographique dans la lutte contre le paludisme dans la région des Hautes Terres Centrales à Madagascar. Archives de l'Institut Pasteur de Madagascar. 2001, 67: 27-30.
Machault V, Vignolles C, Pagès F, Gadiaga L, Gaye A, Sokhna C, Trape J-F, Lacaux J-P, Rogier C: Spatial heterogeneity and temporal evolution of malaria transmission risk in Dakar, Senegal, according to remotely sensed environmental data. Malar J. 2010, 9: 252-10.1186/1475-2875-9-252.
Rodriguez AD, Rodriguez MH, Hernandez JE, Dister SW, Beck LR, Rejmankova E, Roberts DR: Landscape surrounding human settlements and Anopheles albimanus (Diptera: Culicidae) abundance in Southern Chiapas, Mexico. J Med Entomol. 1996, 33: 39-48.
Zhou G, Munga S, Minakawa N, Githeko AK, Yan G: Spatial relationship between adult malaria vector abundance and environmental factors in western Kenya highlands. Am J Trop Med Hyg. 2007, 77: 29-35.
Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Githeko AK, Yan G: Spatial distribution of anopheline larval habitats in Western Kenyan highlands: effects of land cover types and topography. Am J Trop Med Hyg. 2005, 73: 157-165.
Sainz-Elipe S, Latorre JM, Escosa R, Masià M, Fuentes MV, Mas-Coma S, Bargues MD: Malaria resurgence risk in southern Europe: climate assessment in an historically endemic area of rice fields at the Mediterranean shore of Spain. Malar J. 2010, 9: 221-10.1186/1475-2875-9-221.
Tran A, Ponçon N, Toty C, Linard C, Guis H, Ferré J-B, Lo Seen D, Roger F, de la Rocque S, Fontenille D, Baldet T: Using remote sensing to map larval and adult populations of Anopheles hyrcanus (Diptera: Culicidae) a potential malaria vector in Southern France. Int J Health Geogr. 2008, 7: 9-10.1186/1476-072X-7-9.
Munga S, Yakob L, Mushinzimana E, Zhou G, Ouna T, Minakawa N, Githeko A, Yan G: Land use and land cover changes and spatiotemporal dynamics of anopheline larval habitats during a four-year period in a highland community of Africa. Am J Trop Med Hyg. 2009, 81: 1079-1084. 10.4269/ajtmh.2009.09-0156.
Mushinzimana E, Munga S, Minakawa N, Li L, Feng C-C, Bian L, Kitron U, Schmidt C, Beck L, Zhou G, Githeko AK, Yan G: Landscape determinants and remote sensing of anopheline mosquito larval habitats in the western Kenya highlands. Malar J. 2006, 5: 13-10.1186/1475-2875-5-13.
Diuk-Wasser MA, Toure MB, Dolo G, Bagayoko M, Sogoba N, Sissoko I, Traore SF, Taylor CE: Effect of rice cultivation patterns on malaria vector abundance in rice-growing villages in Mali. Am J Trop Med Hyg. 2007, 76: 869-874.
Hernández-Avila JE, Rodríguez MH, Betanzos-Reyes AF, Danis-Lozano R, Méndez-Galván JF, Velázquez-Monroy OJ, Tapia-Conyer R: Determinant factors for malaria transmission on the coast of Oaxaca State, the main residual transmission focus in Mexico. Salud pública Méx. 2006, 48: 405-417.
Brooker S, Leslie T, Kolaczinski K, Mohsen E, Mehboob N, Saleheen S, Khudonazarov J, Freeman T, Clements A, Rowland M, Kolaczinski J: Spatial epidemiology of Plasmodium vivax, Afghanistan. Emerg Infect Dis. 2006, 12: 1600-1602. 10.3201/eid1210.060051.
Thomson MC, Connor SJ, D'Alessandro U, Rowlingson B, Diggle P, Cresswell M, Greenwood B: Predicting malaria infection in Gambian children from satellite data and bed net use surveys: the importance of spatial correlation in the interpretation of results. Am J Trop Med Hyg. 1999, 61: 2-8.
Raso G, Silué KD, Vounatsou P, Singer BH, Yapi A, Tanner M, Utzinger J, N'Goran EK: Spatial risk profiling of Plasmodium falciparum parasitaemia in a high endemicity area in Côte d'Ivoire. Malar J. 2009, 8: 252-10.1186/1475-2875-8-252.
Loha E, Lindtjørn B: Model variations in predicting incidence of Plasmodium falciparum malaria using 1998-2007 morbidity and meteorological data from south Ethiopia. Malar J. 2010, 9: 166-10.1186/1475-2875-9-166.
Kleinschmidt I, Bagayoko M, Clarke GP, Craig M, Le Sueur D: A spatial statistical approach to malaria mapping. Int J Epidemiol. 2000, 29: 355-361. 10.1093/ije/29.2.355.
Olson SH, Gangnon R, Elguero E, Durieux L, Guégan JF, Foley JA, Patz JA: Links between climate, malaria, and wetlands in the Amazon Basin. Emerging Infect Dis. 2009, 15: 659-662. 10.3201/eid1504.080822.
Hay SI, Snow RW, Rogers DJ: Predicting malaria seasons in Kenya using multitemporal meteorological satellite sensor data. Trans R Soc Trop Med Hyg. 1998, 92: 12-20. 10.1016/S0035-9203(98)90936-1.
Hay SI, Lennon JJ: Deriving meteorological variables across Africa for the study and control of vector-borne disease: a comparison of remote sensing and spatial interpolation of climate. Trop Med Int Health. 1999, 4: 58-71. 10.1046/j.1365-3156.1999.00355.x.
Adimi F, Soebiyanto RP, Safi N, Kiang R: Towards malaria risk prediction in Afghanistan using remote sensing. Malar J. 2010, 9: 125-10.1186/1475-2875-9-125.
Gaudart J, Touré O, Dessay N, Dicko AL, Ranque S, Forest L, Demongeot J, Doumbo OK: Modelling malaria incidence with environmental dependency in a locality of Sudanese savannah area, Mali. Malar J. 2009, 8: 61-10.1186/1475-2875-8-61.
Peterson AT: Ecological niche modelling and understanding the geography of disease transmission. Vet Ital. 2007, 43: 393-400.
Peterson AT: Ecologic niche modeling and spatial patterns of disease transmission. Emerging Infect Dis. 2006, 12: 1822-1826. 10.3201/eid1212.060373.
Romaña CA: Eco-épidémiologie. In Dictionnaire de la pensée médicale. 2004, Presses Universitaires de France. Paris: Lecourt, 378-382.
Lopes P, Lourenço P, Sousa C, Novo T, Rodrigues J, Almeida APG, Seixas J: Modelling patterns of mosquito density based on remote sensing images. 2005, In Estoril Congress Center
Dister SW, Fish D, Bros SM, Frank DH, Wood BL: Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. Am J Trop Med Hyg. 1997, 57: 687-692.
Frank DH, Fish D, Moy FH: Landscape features associated with lyme disease risk in a suburban residential environment. Landscape Ecol. 1998, 13: 27-36. 10.1023/A:1007965600166.
Cohen JM, Ernst KC, Lindblade KA, Vulule JM, John CC, Wilson ML: Local topographic wetness indices predict household malaria risk better than land-use and land-cover in the western Kenya highlands. Malar J. 2010, 9: 328-10.1186/1475-2875-9-328.
Tsayem-Demaze M, Manusset S: L'agriculture itinérante sur brûlis en Guyane française: la fin des durabilités écologique et socioculturelle?. Cah Outre Mer. 2008, 61: 31-48.
Carme B, Lecat J, Lefebvre P: Malaria in an outbreak zone in Oyapock (French Guiana): incidence of malaria attacks in the American Indian population of Camopi. (In French). Med Trop. 2005, 65: 149-154.
Ehrman FC, Ellis JM, Young MD: Plasmodium vivax Chesson strain. Science. 1945, 101: 377-
Hanf M, Stefani A, Basurko C, Nacher M, Carme B: Determination of the Plasmodium vivax relapse pattern in Camopi, French Guiana. Malar J. 2009, 8: 278-278. 10.1186/1475-2875-8-278.
Stefani A, Hanf M, Nacher M, Girod R, Carme B: Environmental, entomological, socioeconomic and behavioural risk factors for malaria attacks in Amerindian children of Camopi, French Guiana. Malar J. 2011, 10: 246-10.1186/1475-2875-10-246.
Jaeger JAG: Landscape division, splitting index, and effective mesh size: new measures of landscape fragmentation. Landscape Ecol. 2000, 15: 115-130. 10.1023/A:1008129329289.
Dray S, Legendre P, Peres-Neto PR: Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Modell. 2006, 196: 483-493. 10.1016/j.ecolmodel.2006.02.015.
Wagner HH: Spatial covariance in plant communities: integrating ordination, geostatistics, and variance testing. Ecology. 2003, 84: 1045-1057. 10.1890/0012-9658(2003)084[1045:SCIPCI]2.0.CO;2.
Roux E, Venâncio AF, Girres J, Romaña CA: Spatial patterns and eco-epidemiological systems - Part I: Multi-scale spatial modelling of the occurrence of Chagas disease insect vectors. Geospatial Health. 2011, 6: 41-51.
Moilanen A, Nieminen M: Simple connectivity measures in spatial ecology. Ecology. 2002, 83: 1131-1145. 10.1890/0012-9658(2002)083[1131:SCMISE]2.0.CO;2.
Ernst KC, Lindblade KA, Koech D, Sumba PO, Kuwuor DO, John CC, Wilson ML: Environmental, socio-demographic and behavioural determinants of malaria risk in the western Kenyan highlands: a case-control study. Trop Med Int Health. 2009, 14: 1258-1265. 10.1111/j.1365-3156.2009.02370.x.
Rozendaal JA: Biting and resting behavior of Anopheles darlingi in the Suriname rainforest. J Am Mosq Control Assoc. 1989, 5: 351-358.
Charlwood JD: Biological variation in Anopheles darlingi Root. Mem Inst Oswaldo Cruz. 1996, 91: 391-398.
Tadei WP, Thatcher BD, Santos JM, Scarpassa VM, Rodrigues IB, Rafael MS: Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg. 1998, 59: 325-335.
Tadei WP, Dutary Thatcher B: Malaria vectors in the Brazilian amazon: Anopheles of the subgenus Nyssorhynchus. Rev Inst Med Trop Sao Paulo. 2000, 42: 87-94. 10.1590/S0036-46652000000200005.
Olson SH, Gangnon R, Silveira GA, Patz JA: Deforestation and malaria in Mâncio Lima County, Brazil. Emerging Infect Dis. 2010, 16: 1108-1115.
Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA: 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.
Vittor AY, Pan W, Gilman RH, Tielsch J, Glass G, Shields T, Sánchez-Lozano W, Pinedo VV, Salas-Cobos E, Flores S, Patz JA: 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.
Patz JA, Graczyk TK, Geller N, Vittor AY: Effects of environmental change on emerging parasitic diseases. Int J Parasitol. 2000, 30: 1395-1405. 10.1016/S0020-7519(00)00141-7.
Raccurt CP: [Malaria, anopheles, the anti-malaria campaign in French Guyana: between dogmatism and judgment]. Med Trop. 1997, 57: 401-406.
Hiwat H, Issaly J, Gaborit P, Somai A, Samjhawan A, Sardjoe P, Soekhoe T, Girod R: Behavioral heterogeneity of Anopheles darlingi (Diptera: Culicidae) and malaria transmission dynamics along the Maroni River, Suriname, French Guiana. Trans R Soc Trop Med Hyg. 2010, 104: 207-213. 10.1016/j.trstmh.2009.07.007.
Fouque F, Gaborit P, Carinci R, Issaly J, Girod R: Annual variations in the number of malaria cases related to two different patterns of Anopheles darlingi transmission potential in the Maroni area of French Guiana. Malar J. 2010, 9: 80-10.1186/1475-2875-9-80.