Implications for changes in Anopheles darlingi biting behaviour in three communities in the peri-Iquitos region of Amazonian Peru

Malaria Journal

Volumn 14, Issue 1, 2015, Pages

  Moreno, Marta ^a   Saavedra, Marlon P ^b   Bickersmith, Sara A ^c   Lainhart, William ^d   Tong, Carlos ^e   Alava, Freddy ^f   Vinetz, Joseph M ^a,e   Conn, Jan E ^c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b ASOCIACIÓN BENÉFICA PRISMA   (Peru)

^c WADSWORTH CENTER   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

^e INSTITUTO DE MEDICINA TROPICAL ALEXANDER VON HUMBOLDT   (Peru)

^f MINISTERIO DE SALUD   (Peru)

Author keywords

Amazonian Peru; Anopheles darlingi; Entomological inoculation rate; Human landing catch; Malaria

Indexed keywords

ANOPHELES; ANOPHELES DARLINGI; ANOPHELES DUNHAMI; ANOPHELES OSWALDOI; ARTICLE; BEHAVIOR CHANGE; CDC TRAP; CONTROLLED STUDY; DISEASE TRANSMISSION; ECOLOGICAL PROCEDURES; ENTOMOLOGICAL INOCULATION RATE; EPIDEMIC; GEOGRAPHIC DISTRIBUTION; HUMAN LANDING CATCH; INFECTION RATE; INOCULATION; INTERMETHOD COMPARISON; LONGITUDINAL STUDY; MALARIA; MOSQUITO BITE; NONHUMAN; PERU; SEASONAL VARIATION; SHANNON TRAP; ANIMAL; BITES AND STINGS; FEMALE; GENETICS; HUMAN; INSECT VECTOR; PHYSIOLOGY;

ANIMALS; ANOPHELES; BITES AND STINGS; FEMALE; HUMANS; INSECT VECTORS; LONGITUDINAL STUDIES; MALARIA; PERU;

EID: 84939205910     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-0804-2     Document Type: Article

References (54)

1. Kleinschmidt I, Sharp BL, Clarke GP, Curtis B, Fraser C (2001) Use of generalized linear mixed models in the spatial analysis of small-area malaria incidence rates in Kwazulu Natal, South Africa. Am J Epidemiol 153:1213-1221
2. Hirzel AH, Hausser J, Chessel D, Perrin N (2002) Ecological-niche factor analysis: how to compute habitat-suitability maps without absence data? Ecology 83:2027-2036
3. da Silva-Nunes M, Moreno M, Conn JE, Gamboa D, Abeles S, Vinetz JM et al (2012) Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop 12:281-291
4. Parker BS, Paredes Olortegui M, Penataro Yori P, Escobedo K et al (2013) Hyperendemic malaria transmission in areas of occupation-related travel in the Peruvian Amazon. Malar J 12:178
5. Chowell G, Munayco CV, Escalante AA, McKenzie FE (2009) The spatial and temporal patterns of falciparum and vivax malaria in Peru: 1994-2006. Malar J 8:142
6. MINSA (2014) Ministerio de Salud del Perú: Sala de Situación de Salud
7. Flores-Mendoza C, Fernandez R, Escobedo-Vargas KS, Vela-Perez Q, Schoeler GB (2004) Natural Plasmodium infections in Anopheles darlingi and Anopheles benarrochi (Diptera: Culicidae) from eastern Peru. J Med Entomol 41:489-494
8. Conn JE, Moreno M, Saavedra M, Bickersmith SA, Knoll E, Fernandez R et al (2013) Molecular taxonomy of Anopheles (Nyssorhynchus) benarrochi (Diptera: Culicidae) and malaria epidemiology in southern Amazonian Peru. Am J Trop Med Hyg 88:319-324
9. Reinbold-Wasson DD, Sardelis MR, Jones JW, Watts DM, Fernandez R, Carbajal F et al (2012) Determinants of Anopheles seasonal distribution patterns across a forest to periurban gradient near Iquitos. Peru. Am J Trop Med Hyg 86:459-463
10. Angella AF, Salgueiro P, Gil LH, Vicente JL, Pinto J, Ribolla PE (2014) Seasonal genetic partitioning in the neotropical malaria vector, Anopheles darlingi. Malar J 13:203
11. Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R (2006) Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J Med Entomol 43:947-956
12. Hiwat H, Bretas G (2011) Ecology of Anopheles darlingi Root with respect to vector importance: a review. Parasit Vectors 4:177
13. Gil LH, Alves FP, Zieler H, Salcedo JM, Durlacher RR, Cunha RP et al (2003) Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazonia. J Med Entomol 40:636-641
14. Moreno JE, Rubio-Palis Y, Paez E, Perez E, Sanchez V (2007) Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol 21:339-349
15. Rodriguez M, Perez L, Caicedo JC, Prieto G, Arroyo JA, Kaur H et al (2009) Composition and biting activity of Anopheles (Diptera: Culicidae) in the Amazon region of Colombia. J Med Entomol 46:307-315
16. Martins-Campos KM, Pinheiro WD, Vitor-Silva S, Siqueira AM, Melo GC, Rodrigues IC et al (2012) Integrated vector management targeting Anopheles darlingi populations decreases malaria incidence in an unstable transmission area, in the rural Brazilian Amazon. Malar J 11:351
17. Athrey G, Hodges TK, Reddy MR, Overgaard HJ, Matias A, Ridl FC et al (2012) The effective population size of malaria mosquitoes: large impact of vector control. PLoS Genet 8:e1003097
18. Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I et al (1987) Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65:39-45
19. Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE et al (1993) High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61:315-320
20. Hasan AU, Suguri S, Sattabongkot J, Fujimoto C, Amakawa M, Harada M et al (2009) Implementation of a novel PCR based method for detecting malaria parasites from naturally infected mosquitoes in Papua New Guinea. Malar J 8:182
21. Povoa MM, Machado RL, Segura MN, Vianna GM, Vasconcelos AS, Conn JE (2000) Infectivity of malaria vector mosquitoes: correlation of positivity between ELISA and PCR-ELISA tests. Trans R Soc Trop Med Hyg 94:106-107
22. Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR (1999) Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg 60:364-376
23. Santos LM, Gama RA, Eiras AE, Fonseca CG (2010) Genetic differences based on AFLP markers in the mosquito species Anopheles darlingi collected in versus near houses in the region of Porto Velho, RO, Brazil. Genet Mol Res 9:2254-2262
24. Mirabello L, Conn JE (2006) Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity (Edinb) 96:311-321
25. Pinedo-Cancino V, Sheen P, Tarazona-Santos E, Oswald WE, Jeri C, Vittor AY et al (2006) Limited diversity of Anopheles darlingi in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 75:238-245
26. Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Sanches Lozano W et al (2006) 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 74:3-11
27. Rosas-Aguirre A, Guzman-Guzman M, Moreno-Gutierrez D, Rodriguez-Ferrucci H, Vargas-Pacherrez D, Acuna-Gonzalez Y (2011) Long-lasting insecticide - treated bednet ownership, retention and usage 1 year after their distribution in Loreto, Peru. Rev Peru Med Exp Salud Publica 28:228-236 (in Spanish)
28. http://www.senamhi.gob.pe. Accessed 6 Nov 2014
29. Knols BG, de Jong R, Takken W (1995) Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg 89:604-606
30. Forattini OP (1962) Entomologia Medica, vol 1. Faculdade de Higiene e Sáude Publica, São Paulo
31. Faran ME, Linthicum KJ (1981) A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosquito System 13:1-81
32. Consoli RA, Lourenco-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Editora Fiocruz, Fundação Oswaldo Cruz
33. Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM (2007) Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg 77:67-72
34. Matson R, Rios CT, Chavez CB, Gilman RH, Florin D, Sifuentes VL et al (2008) Improved molecular technique for the differentiation of neotropical anopheline species. Am J Trop Med Hyg 78:492-498
35. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294-299
36. Foster PG, Bergo ES, Bourke BP, Oliveira TM, Nagaki SS, Sant'Ana DC et al (2013) Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). PLoS One 8:e54063
37. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
38. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755
39. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574
40. Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quinones ML et al (2010) Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz 105:899-903
41. Galardo AK, Arruda M, D'Almeida Couto AA, Wirtz R, Lounibos LP, Zimmerman RH (2007) Malaria vector incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg 76:461-469
42. Girod R, Gaborit P, Carinci R, Issaly J, Fouque F (2008) Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana. Mem Inst Oswaldo Cruz 103:702-710
43. Rubio-Palis Y, Bevilacqua M, Medina DA, Moreno JE, Cardenas L, Sanchez V et al (2013) Malaria entomological risk factors in relation to land cover in the Lower Caura River Basin, Venezuela. Mem Inst Oswaldo Cruz 108:220-228
44. Naranjo-Diaz N, Rosero DA, Rua-Uribe G, Luckhart S, Correa MM (2013) Abundance, behavior and entomological inoculation rates of anthropophilic anophelines from a primary Colombian malaria endemic area. Parasit Vectors 6:61
45. Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M et al (2014) Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J 13:125
46. Bugoro H, Iro'ofa C, Mackenzie DO, Apairamo A, Hevalao W, Corcoran S et al (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
47. Schoeler GB, Flores-Mendoza C, Fernandez R, Davila JR, Zyzak M (2003) Geographical distribution of Anopheles darlingi in the Amazon Basin region of Peru. J Am Mosq Control Assoc 19:286-296
48. Moutinho PR, Gil LH, Cruz RB, Ribolla PE (2011) Population dynamics, structure and behavior of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre, Brazil. Malar J 10:174
49. Hayes J, Calderon G, Falcon R, Zambrano V (1987) Newly incriminated anopheline vectors of human malaria parasites in Junin Department, Peru. J Am Mosq Control Assoc 3:418-422
50. Lima JB, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R (2014) 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 109:685-705
51. Hiwat H, De Rijk M, Andriessen R, Koenraadt CJ, Takken W (2011) Evaluation of methods for sampling the malaria vector Anopheles darlingi (Diptera, Culicidae) in Suriname and the relation with its biting behavior. J Med Entomol 48:1039-1046
52. Rubio-Palis Y, Moreno JE, Sanchez V, Estrada Y, Anaya W, Bevilacqua M et al (2012) Can mosquito magnet(R) substitute for human-landing catches to sample anopheline populations? Mem Inst Oswaldo Cruz 107:546-549
53. Gama RA, Silva IM, Geier M, Eiras AE (2013) Development of the BG-Malaria trap as an alternative to human-landing catches for the capture of Anopheles darlingi. Mem Inst Oswaldo Cruz 108:763-771
54. Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF (2013) Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J 12:49