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Evaluation of the Sticky MosquiTRAP

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PUBLIC HEALTH

Evaluation of the Sticky MosquiTRAP

TM

for Detecting

Aedes

(

Stegomyia

)

aegypti

(L.) (Diptera: Culicidae) during the Dry Season in Belo Horizonte,

Minas Gerais, Brazil

R

ENATA

A. G

AMA1

, E

RIC

M. S

ILVA1

, I

VONEIDE

M. S

ILVA1

, M

ARCELO

C. R

ESENDE2AND

Á

LVARO

E. E

IRAS1

1Lab. Ecologia Química de Insetos Vetores, Instituto de Ciências Biológicas, Univ. Federal de Minas Gerais. Av. Presidente Antônio Carlos, 6627 Pampulha, 31270-901, Belo Horizonte, MG

2Núcleo de Entomologia, Fund. Nacional de Saúde, Rua Rio de Janeiro 1200, Centro, 30160-000, Belo Horizonte, MG

Neotropical Entomology 36(2):294-302 (2007)

Avaliação da MosquiTRAP na Detecção de

Aedes

(

Stegomyia

)

aegypti

(L.) (Diptera: Culicidae) durante

Estação Seca em Belo Horizonte, MG

RESUMO - MosquiTRAP é uma armadilha desenvolvida para a captura de fêmeas grávidas de Aedes aegypti /HSHUPLWHDLGHQWL¿FDomRGRPRVTXLWRHPFDPSRGXUDQWHDYLVWRULDGDDUPDGLOKD2REMHWLYR desse estudo foi comparar essa armadilha com a pesquisa larvária e a ovitrampa para o monitoramento do A. aegyptiHPFDPSRGXUDQWHDHVWDomRVHFD2WUDEDOKRIRLUHDOL]DGRGHPDUoRDMXQKRHP TXDUWHLU}HVQREDLUUR,WDSRm%HOR+RUL]RQWH0*2PRQLWRUDPHQWRGDVDUPDGLOKDVIRLVHPDQDOHD pesquisa larvária foi realizada mensalmente. O Índice Predial (IP) e o Índice de Breteau (IB) apresentaram valores iguais durante todo o experimento (1,72 nos primeiros dois meses e zero nos dois últimos) e o ËQGLFHGH5HFLSLHQWH,5QRVGRLVSULPHLURVPHVHVIRLGHHUHVSHFWLYDPHQWHHQRVGRLV~OWLPRV IRL]HUR2ËQGLFHGH3RVLWLYLGDGHGH2YLWUDPSD,32YDULRXGHDHRËQGLFHGH3RVLWLYLGDGH GH0RVTXL75$3,30YDULRXGHD2ËQGLFHGH'HQVLGDGHGH2YRV,'2YDULRXGHD HQTXDQWRRËQGLFHGH'HQVLGDGHGH$GXOWRV,'$YDULRXGHDGXUDQWHWRGRRH[SHULPHQWR$ WHPSHUDWXUDHDSUHFLSLWDomRQmRLQÀXHQFLDUDPRVËQGLFHVGH3RVLWLYLGDGHHGH'HQVLGDGHPDVSDUHFHP WHULQÀXHQFLDGRRVtQGLFHVODUYiULRV$SHVDUGHD0RVTXL75$3WHUFROHWDGRXPQ~PHURSHTXHQRGHAedes, REVHUYRXVHTXHHODIRLPDLVVHQVtYHOSDUDGHWHFWDUDSUHVHQoDGHAedes do que a pesquisa larvária.

PALAVRAS-CHAVE: Monitoramento, dengue, mosquito

ABSTRACT - MosquiTRAPTMLVDVWLFN\WUDSVSHFL¿FDOO\GHVLJQHGWRFDSWXUHJUDYLGIHPDOHVRIAedes aegypti /DQGDOORZVWKHLGHQWL¿FDWLRQRIWKHPRVTXLWRLQWKH¿HOGGXULQJWKHLQVSHFWLRQRIWKHWUDS 7KLVVWXG\DLPVWRFRPSDUHWKLVVWLFN\WUDSWRODUYDODQGRYLWUDSVXUYH\VIRU¿HOGPRQLWRULQJRIA. aegypti during the dry season.7KHVWXG\ZDVFRQGXFWHGIURP0DUFKWR-XQHRILQEORFNVRIWKH district of Itapoã, Belo Horizonte, MG. The traps were monitored every week while the larval survey was FRQGXFWHGRQDPRQWKO\EDVLV7KHODUYDOLQGH[3UHPLVH,QGH[3,DQG%UHWHDX,QGH[%,KDGHTXDO YDOXHVWKURXJKRXWWKHH[SHULPHQWLQWKH¿UVWWZRPRQWKVDQG]HURLQWKHODVWWZR7KHFRQWDLQHU LQGH[&,GXULQJWKH¿UVWWZRPRQWKVZDVDQGUHVSHFWLYHO\DQG]HURLQWKHODVWWZR7KH 2YLWUDS3RVLWLYH,QGH[23,UDQJHGIURPWRDQGWKH0RVTXL75$33RVLWLYH,QGH[03, UDQJHGIURPWR7KH(JJ'HQVLW\,QGH[(',UDQJHGIURPWRZKLOHWKH$GXOW'HQVLW\ ,QGH[UDQJHGIURPWRWKURXJKRXWWKHH[SHULPHQW7HPSHUDWXUHDQGUDLQIDOOGLGQRWDIIHFWWKH3RVLWLYH DQG'HQVLW\,QGLFHVDOWKRXJKWKHVHHQYLURQPHQWDOYDULDEOHVVHHPHGWRKDYHDIIHFWHGWKHODUYDHLQGLFHV Although the MosquiTRAPFDXJKWDORZQXPEHURIAedes mosquitoes during the study, it was more sensitive than the larval survey to detect the presence of Aedes mosquitoes.

KEY WORDS: Monitoring, dengue, mosquito

$FFRUGLQJWRWKHGDWDUHFRUGHGE\WKH+HDOWK6XUYHLOODQFH 6HFUHWDULDW WKH QXPEHU RI UHSRUWHG GHQJXH FDVHV IURP -DQXDU\WR0D\LQFUHDVHGE\LQDVFRPSDUHG WRWKHVDPHSHULRGLQFDVHV7KHLQFUHDVHLQ WKHQXPEHURIGHQJXHFDVHVZDVORFDOL]HGWRWKHQRUWKDQG

northeastern states of Brazil, whereas cases decreased in VRXWKHUQVWDWHV0LQLVWpULRGD6D~GH

(2)

March - April 2007 Neotropical Entomology 36(2)

in 24 Brazilian States and the circulation of dengue 4 in QHLJKERULQJ FRXQWULHV 0LQLVWpULR GD 6D~GH 7KH presence of the mosquito vector Aedes(Stegomyia) aegypti /LQDOOVWDWHVRI%UD]LODQGWKHLQFUHDVHLQWKHQXPEHURI areas infested with Aedes(Stegomyia) albopictus (Skuse) (Diptera: Culicidae) creates cause for concern (Ministério GD6D~GHThe mosquito A. albopictus was not shown WREHUHVSRQVLEOHIRUGHQJXHHSLGHPLFVLQWKH$PHULFDVEXW LWZDVVKRZQWREHVXVFHSWLEOHWRLQIHFWLRQVXQGHUODERUDWRU\ FRQGLWLRQVDQGLWZDVIRXQGQDWXUDOO\LQIHFWHGLQWKH¿HOGLQ Campos Altos (MG, Brazil) and in Reynosa (Mexico) (Serufo et al,EixH]%HUQDOet al. 1997).

Currently, Brazil monitors A. aegypti populations using larval surveys and oviposition traps (ovitraps) (FUNASA $OWKRXJKRYLWUDSVZHUHSURYHGWREHPRUHVHQVLWLYH to detect A. aegypti SRSXODWLRQVLQWKH¿HOGZKHQFRPSDUHG with larval surveys (Braga et al.WKHODWWHUPHWKRGLV HPSOR\HGDVDVWDQGDUGE\WKH1DWLRQDO3URJUDPRI'HQJXH &RQWURO 13'& LQ %UD]LO 31&' 8QIRUWXQDOHW\ the larval survey does not detect the presence of A. aegypti during the dry season.

Methods for collecting adult mosquitoes such as human EDLWEDFNSDFNDVSLUDWRUVRUWUDSVKDYHQRWEHHQXVHGE\WKH +HDOWK0LQLVWU\RQDURXWLQHEDVLVGXHWRWKHULVNRIH[SRVXUH RI¿HOGWHFKQLFLDQVWRLQIHFWHGPRVTXLWRHVDQGDVKRUWDJHRI VSHFL¿FDQGHI¿FLHQWWUDSVIRUWKLVVSHFLHV0RQLWRULQJDGXOW SRSXODWLRQVKDVVHYHUDODGYDQWDJHVLQWKDWLWSURYLGHVDEHWWHU estimate of vector density and risk of transmission while SURYLGLQJ VSHFLPHQV IRU DQDO\VHV RI VSDWLDO GLVWULEXWLRQ SDULW\RYDULDQGHYHORSPHQWPLGJXWFRQWHQWVXVFHSWLELOLW\ to pathogens and resistance to insecticides (Barata et al )RFNV5LWFKLHet al.

The MosquiTRAPTM 9HUVLRQ (FRYHF /WGD LV D VWLFN\WUDSGHYHORSHGE\(LUDVSDWHQWSHQGLQJZKLFK ZDVGHYHORSHGEDVHGXSRQWKHEHKDYLRURIJUDYLGIHPDOH Aedes ZKHQWKH\H[SORUHEUHHGLQJVLWHV,WFRQVLVWVRID/ EODFNSODVWLFF\OLQGHU¿OOHGZLWKZDWHURYLSRVLWLRQDWWUDFWDQW DQGDQDGKHVLYHFDUG7KLVWUDSH[SORLWVERWKYLVXDOEODFN color) and olfactory stimuli (synthetic volatiles) attrative for gravid females. When the females enter the trap and land RQWKHZDOOVRIWKH0RVTXL75$3WKH\DGKHUHWRWKHEODFN VWLFN\FDUG,QODERUDWRU\DQG¿HOGWHVWVWKLVWUDSZDVVKRZQ WREHHIIHFWLYHDQGORZFRVWWKXVPDNLQJLWYLDEOHIRUXVHLQ ODUJHVFDOHRSHUDWLRQV7KH0RVTXL75$3DOVRHQDEOHVWKH LGHQWL¿FDWLRQRIWKHYHFWRUGXULQJ¿HOGLQVSHFWLRQVWKHUHE\ DYRLGLQJLQWHQVLYHODERURILGHQWLI\LQJLQVHFWVLQWKHODERUDWRU\ Similar sticky traps were used to entomological investigation of dengue transmission (Ritchie et alDQGIRUGLVSHUVDO studies of A. aegypti in Australia (Russel et al

The aim of this study was to compare the effectiveness, sensitivity and practicality of the MosquiTRAP, larval survey and the ovitrap to detect the presence of A. aegypti mosquito LQWKH¿HOGGXULQJWKHGU\VHDVRQ

Materials and Methods

Experimental area. The present study was conducted during ZHHNVIURP0DUFKWR-XQHLQWKHGLVWULFWRI,WDSRm which is located in the Pampulha region of the city of Belo

Horizonte, Minas Gerais, Brazil. This area was selected EHFDXVHRIWKHUHOLDEOHSUHVHQFHRIA. aegypti mosquitoes during previous larval surveys and ovitrap monitoring (Data VXSSOLHGE\WKH=RRQRVHV&RQWURO&HQWHURI%HOR+RUL]RQWH City Council). Most of the premises in this district consist RI EULFN KRXVHV ZLWK JDUGHQV EDFN\DUGV JRRG VDQLWDU\ FRQGLWLRQVZDWHUVXSSO\DQGJDUEDJHGLVSRVDOVHUYLFHWKUHH times a week. All the streets are paved with asphalt and the local “Lagoa do Nado” park is a pleasant green area for leisure and recreation for the local residents with a middle class socioeconomic level.

Larval survey. 0RQWKO\ODUYDOVXUYH\VZHUHFDUULHGRXWE\

QLQH¿HOGDJHQWVDVUHFRPPHQGHGE\WKH1DWLRQDO3URJUDP of Dengue Control 31&'7HQSHUFHQWRIDOOWKH premises within the experimental area were sampled during WKH¿UVWZHHNRIHYHU\PRQWK0DUFKWR-XQH$OOFRQWDLQHUV ZKLFKPLJKWVHUYHDVEUHHGLQJVLWHVIRUA. aegypti larvae were LQVSHFWHGERWKLQVLGHDQGRXWVLGHSUHPLVHV/DUYDOVDPSOHV ZHUH VHQW WR WKH /DERUDWyULR GH &XOLFtGHRV ,QVWLWXWR GH &LrQFLDV%LROyJLFDVDWWKH8QLYHUVLGDGH)HGHUDOGH0LQDV *HUDLVIRUVSHFLHVLGHQWL¿FDWLRQ,QIRUPDWLRQIURPWKHODUYDO surveys was used to calculate the following indices: Premise ,QGH[3,QXPEHURISRVLWLYHKRXVHVWRWDORILQVSHFWHG KRXVHV[&RQWDLQHU,QGH[&,QXPEHURISRVLWLYH FRQWDLQHUVWRWDOQXPEHURIFRQWDLQHUVLQVSHFWHG[DQG %UHWHDX,QGH[%,QXPEHURISRVLWLYHFRQWDLQHUVWRWDO QXPEHURIKRXVHVLQVSHFWHG[

Trap placement. $Q DUHD HQFRPSDVVLQJ EORFNV ZDV

selected for the 17 weekly surveys. Two houses were VHOHFWHG ZLWKLQ HDFK EORFN DQG RQH KRXVH UHFHLYHG DQ ovitrap whereas the other house received MosquiTRAP so WKDWDWRWDORIKRXVHVZHUHEHLQJPRQLWRUHG(DFKWUDS was installed within a shaded area and protected from the UDLQ:LWKLQHDFKEORFNWKHWUDSVZHUHURWDWHGVRWKDWHDFK house had only one trap type for a maximum of one week, WRDYRLGELDVLQWKHUHVXOWVE\KDYLQJDKLJKO\SURGXFWLYH EUHHGLQJVLWHLQWKHSUHPLVH

Ovitrap.7KH RYLWUDS FRQVLVWV RI D PO EODFN SODVWLF

(3)

open inter

black sticky card

plastic cilinder

hole

infusion level

infusion

MosquiTRAP. 7KH 0RVTXL75$3 FRQVLVWV RI D PO

PDWWHEODFNFRQWDLQHUZLWKPORIVROXWLRQRIWKH FRZJUDVVLQIXVLRQ6DQWDQD$EODFNDGKHVLYHFDUG was placed inside the container wall to trap the mosquitoes (LUDV)LJ$JURZWKUHJXODWRUZDVDGGHGWRWKH 0RVTXL75$3WRSUHYHQWLWIURPEHFRPLQJDEUHHGLQJVLWH 7KH0RVTXL75$3ZHUHPRQLWRUHGRQDZHHNO\EDVLVDQGWKH LQVSHFWLRQLQFOXGHGWKHLGHQWL¿FDWLRQDQGTXDQWL¿FDWLRQRI adult mosquitoes captured on the sticky card and the presence of immature forms in the infusion. The adult mosquitoes were UHPRYHGIURPWKHWUDSE\PHDQVRIIRUFHSV DQGLGHQWL¿HG LQWKH¿HOGXVLQJDPDJQLI\LQJJODVV[7KHLQIXVLRQ

was changed every week and the card was replaced once a month. Informations from MosquiTRAP surveys was used to calculate the indices: MosquiTRAP Positive Index 03,1XPEHURISRVLWLYHWUDSVIRUAedesVSWRWDOQXPEHU RILQVSHFWHGWUDSV[DQG$GXOWV'HQVLW\,QGH[$', 7RWDOQXPEHURIDGXOWPRVTXLWRHVRIAedesVSFDSWXUHG WRWDOQXPEHURIWUDSVZHUHFDOFXODWHG

Meteorological data. Daily temperature and rainfall data ZHUHSURYLGHGE\,1)5$(52RI%HOR+RUL]RQWH¶V3DPSXOKD $LUSRUWDQGWKHGDWDZHUHXVHGWRDVVHVVKRZWKHVHYDULDEOHV DIIHFWWKHHQWRPRORJLFDOLQGLFHVREWDLQHGIURPWKHRYLWUDS the MosquiTRAP and the larval surveys.

Statistical analysis.&RUUHODWLRQEHWZHHQWKHLQGLFHVREWDLQHG

E\WKHRYLWUDSV(OPI and ODI) and the MosquiTRAPs (MPI DQG$', ZDV DVVHVVHG E\ XVLQJ 3HDUVRQ¶V FRUUHODWLRQ Linear regressions were carried out for temperature and UDLQIDOOYDULDEOHVZKLFKZHUHOLNHO\WRKDYHDIIHFWHGERWK WKHQXPEHURIHJJVDQGDGXOWVFROOHFWHGDQGWKHLQGLFHVRI the MosquiTRAP and ovitrap.

Results

Meteorological data. During the experimental period, the average weekly temperature ranged from 17.7ºC to ž&'XULQJWKHth to the 17th epidemiological week, WKHPLQLPXPWHPSHUDWXUHUDQJHGIURPž&WRž& ZKLOH WKH PD[LPXP UDQJHG IURP ž& WR ž&7KH temperature dropped over the 18th to the 26th week, and a PLQLPXPWHPSHUDWXUHRIž&DQGDPD[LPXPRIž& ZHUHREVHUYHG)LJ5DLQIDOORFFXUUHGEHWZHHQWKHth DQGth week and at the 18th week, and the mean weekly

Fig. 2. Variation of temperature (maximum and minimum) and precipitation during the 17 epidemiological weeks study at the GLVWULFWRI,WDSRm%HOR+RUL]RQWH0*

)LJ'LDJUDPRIWKHVWLFN\0RVTXL75$3YHUVLRQ

0 5 10 15 20 25 30 35

10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Weeks

Temperature (ºC)

0 2 4 6 8 10

Precipitation (mm

3)

(4)

March - April 2007 Neotropical Entomology 36(2) 297

UDLQIDOOYROXPHUDQJHGIURPPPWRPP (Fig. 2).

'XULQJWKHH[SHULPHQWDUDLQ\SHULRGZDVREVHUYHGIURP WKHth to the 18th epidemiological week, and a dry period from the 19th to 26th week.

7HPSHUDWXUHDQGUDLQIDOOGLGQRWDIIHFWWKHQXPEHURIDGXOW FROOHFWHGE\WKH0RVTXL75$33!DQGUDLQIDOOGLGQRW DIIHFWHGWKHHJJFROHFWLRQE\WKHRYLWUDS7KHLQÀXHQFHRIWKH temperature and of the rainfall volume on the OPI was not VLJQL¿FDQW3!EXWWKHDPSOLWXGHRIWKHWHPSHUDWXUH

DIIHFWHGWKLVLQGH[\ [U2 7KHUHZDVQR

UHODWLRQEHWZHHQWKHGHQVLW\RIHJJVDQGRIDGXOWVDQGUDLQIDOO volume or temperature.

Larval survey. Larvae were only found during the rainy VHDVRQRIWKH¿UVWWZRPRQWKVRIWKHVXUYH\VZHHNth and thDQGERWKWKH+RXVHDQGWKH%UHWHDX,QGLFHVKDGLGHQWLFDO YDOXHV7DEOH

Ovitraps.During the four months of work, a total of 7,771

eggs of AedesVSZHUHFROOHFWHGLQWKHRYLWUDS7DEOH Eggs were collected throughout the experiment (17 weeks). 2XWRIWKLVWRWDOODUYDHKDWFKHGRIZKLFK 2,116 were A. aegypti DQGZHUHA. albopictus 7DEOH7KHPHGLDQRIAedeseggs collected was DQGWKHPHDQQXPEHURIHJJVSHUSDGGOHZDV 7KHUHZDVHYLGHQFHRIDSRVLWLYHDV\PPHWULFGLVWULEXWLRQDQG

high dispersion of the eggs (Fig. 4), and that the 2ndth, and 8thZHHNZHUHWKHPRVWUHSUHVHQWDWLYHRIWKHVHGLVWULEXWLRQV 5DLQIDOOGLGQRWDIIHFWWKHHJJFROOHFWLRQE\WKHRYLWUDS3 !7KH23,UDQJHGIURPWRZKLOHWKH03, UDQJHGIURP]HURWR7DEOH

MosquiTRAP.'XULQJWKHH[SHULHQWDWRWDORIDGXOWVZHUH

collected in MosquiTRAPs, of which 27 were A. aegypti and ZHUHA. albopictus. Most adults were captured during the thDQGWKHth week. The median of adults collected was 1, DQGWKHPHDQQXPEHURIAedes sp.SHUWUDSZDV7DEOH $GXOWPRVTXLWRHVZHUHFROOHFWHGRQO\LQZHHNVDQGWKH positive index of MosquiTRAP for A. aegypti ranged from zero

WRDQGIRUA. albopictusIURP]HURWR)LJ

7DEOHHouse (HI), Recipient (RI) and Breteau Indices from larval survey in Itapoã, Belo Horizonte, MG (March -XQH

Month (epidemiological week) HI RI BI March (10 th) 1.72 0.09 1.72

A

pril (15 th) 1.72 0.10 1.72

May (19 th) 0 0 0

June (24 th) 0 0 0

7DEOH3HUIRUPDQFHRIRYLWUDSLQFROOHFWLQJAedes eggs and MosquiTRAP catching adult mosquitoes in Itapoã district, %HOR+RUL]RQWH0*0DUFK-XQH

Ovitrap MosquiTRAP®

Weeks N. of

eggs Egg hatched(%) A. aegypti(%) A. albopictus (%) AedesTotalsp. A. aegypti(%) A. albopictus (%) 10 1042 345 (33.1) 345 (100.0) 0 (0.0) 6 5 (83.3) 1 (16.7) 11 351 181 (51.6) 97 (53.6) 84 (46.4) 1 1 (100.0) 0 (0.0) 12 350 139 (39.7) 125 (89.9) 14 (10.1) 3 3 (100.0) 0 (0.0) 13 517 218 (42.2) 193 (88.5) 25 (11.5) 8 6 (75.0) 2 (25.0) 14 678 344 (50.7) 323 (93.9) 21 (6.1) 1 1 (100.0) 0 (0.0) 15 562 132 (23.5) 132 (100.0) 0 (0.0) 3 1 (33.3) 2 (66.7)

16 533 91 (17.0) 87 (95.6) 4 (4.4) 0 0 (0.0) 0 (0.0)

17 1077 327 (30.4) 241 (73.7) 86 (26.3) 3 1 (33.3) 2 (66.7)

18 667 94 (14.1) 94 (100.0) 0 (0.0) 0 0 (0.0) 0 (0.0)

19 677 151 (22.3) 145 (96.0) 6 (4.0) 1 1 (100.0) 0 (0.0)

20 105 86 (81.9) 86 (100.0) 0 (0.0) 5 4 (80.0) 1 (20.0)

21 151 60 (39.7) 60 (100.0) 0 (0.0) 0 0 (0.0) 0 (0.0)

22 133 22 (16.5) 22 (100.0) 0 (0.0) 2 1 (50.0) 1 (50.0)

23 303 86 (28.4) 86 (100.0) 0 (0.0) 1 1 (100.0) 0 (0.0)

24 224 28 (12.5) 28 (100.0) 0 (0.0) 2 1 (50.0) 1 (50.0)

25 292 52 (17.8) 52 (100.0) 0 (0.0) 0 0 (0.0) 0 (0.0)

26 109 0 (0.0) 0 (0.0) 0 (0.0) 1 1 (100.0) 0 (0.0)

(5)

By comparing the variation in the positive indices of ERWK WUDSV GXULQJ WKH ¿HOG H[SHULPHQW D ZHDN SRVLWLYH FRUUHODWLRQEHWZHHQWKHWZRLQGLFHVZDVGHWHFWHG3HDUVRQ +RZHYHULIWKHSRVLWLYHLQGLFHVRIWKHRYLWUDSDQG WKH0RVTXL75$3DUHRQO\FRPSDUHGXSWRWKHHLJKWKZHHN of the study (17thHSLGHPLRORJLFDZHHNDVWURQJHUSRVLWLYH FRUUHODWLRQEHWZHHQWKHLQGLFHVFDQEHREVHUYHG3HDUVRQ = 0.53). It is apparent that from the 17th epidemiological ZHHNRQZDUGWKHUHZDVDGURSLQWKLVFRUUHODWLRQ3HDUVRQ WKXVVXJJHVWLQJDVWURQJHUZHWVHDVRQFRUUHODWLRQ as compared to a dry season correlation.

7KH HJJ GHQVLW\ LQGH[ (', UDQJHG IURP WR DQGWKHDGXOWVGHQVLW\LQGH[$',UDQJHGIURPWR

7DEOH7KHGHQVLW\LQGLFHVIRUWKHRYLWUDSDQGWKH 0RVTXL75$3GLGQRWVKRZVLPLODULWLHVLQWKHLUYDULDWLRQ pattern all over the trial (Pearson = -0.05).

Discussion

$ZLGHUDQJHRILQGLFHVREWDLQHGWKURXJKODUYDOVXUYH\V have been described as tools in the monitoring of A. aegypti populations (Focks 2003). Larval surveys consist of an active VHDUFK IRU SRVLWLYH EUHHGLQJ VLWHV RI WKH PRVTXLWR ERWK LQGRRUVDQGRXWGRRUVDQGRIFROOHFWLQJWKHLPPDWXUHIRUPV that are found (FUNASA 2001). The larval and/or pupae )LJ0RVTXL75$33RVLWLYH,QGH[03,IRUA. aegypti andA. albopictusGXULQJWKHHSLGHPLRORJLFDOZHHNVVWXG\DWWKH GLVWULFWRI,WDSRm%HOR+RUL]RQWH0*

0 5 10 15 20 25 30

10 12 14 16 18 20 22 24 26

We

ek

s

Positivity (%)

A. aegypti A. albopictus

)LJ9DULDWLRQRIGLVWULEXWLRQWKHHJJVLQRYLWUDSGXULQJZHHNVRIVWXG\LQGLVWULFW,WDSRm%HOR+RUL]RQWH0*0DUFK - June2003).

250

195

140

85

30

-25

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Eggs

(6)

March - April 2007 Neotropical Entomology 36(2) 299

1(', (JJV'HQVLW\,QGH[2ADI = adult density index

7DEOH 3RVLWLYHLQGH[HVIRURYLWUDSDQG0RVTXL75$3DQGWKHPHDQQXPEHURIHJJVRYLWUDSDQGDGXOWPRVTXLWR MosquiTRAP®GLVWULFW,WDSRm%HOR+RUL]RQWH0*0DUFK-XQH

Ovitrap MosquiTRAP® Density index Mean per trap Weeks

Number Positive Number Positive EDI1 ADI2 Eggs Adults

10 18 13 19 6 80.15 1.00 57.9 0.31

11 16 8 24 1 43.87 1.00 21.9 0.04

12 19 9 20 3 38.89 1.00 18.4 0.15

13 19 14 20 5 36.93 1.60 27.2 0.40

14 21 14 19 1 48.43 1.00 32.3 0.05

15 17 12 23 2 46.83 1.50 33.1 0.13

16 21 10 15 0 53.30 0.00 25.4 0.00

17 18 13 22 2 82.85 1.50 59.8 0.14

18 13 10 27 0 66.70 0.00 51.3 0.00

19 21 11 19 1 61.54 1.00 32.2 0.05

20 18 3 18 5 35.00 1.00 5.8 0.28

21 19 5 19 0 30.20 0.00 7.9 0.00

22 16 5 20 2 26.60 1.00 8.3 0.10

23 21 6 17 1 50.50 1.00 14.4 0.05

24 16 4 19 2 56.00 1.00 14.0 0.10

25 19 4 17 0 73.00 0.00 15.4 0.00

26 18 8 20 1 13.62 1.00 6.0 0.05

Total 310 149 338 32 52.15 1.16 25.07 0.11

)LJ3UHPLVH,QGH[3,DQG3RVLWLYHLQGH[IRURYLWUDS23,DQG0RVTXL75$303,GXULQJHSLGHPLRORJLFDOZHHNVRI VWXG\LQEDLUUR,WDSRm%HOR+RUL]RQWH0*0DUFK-XQH6KDGHGDUHDFRUUHVSRQGVWRWKHUDLQ\SHULRGRIWKHVWXG\ WKDWDUHFROOHFWHGDUHVHQWWRDODERUDWRU\IRULGHQWL¿FDWLRQ

DQGWKHEUHHGLQJFRQWDLQHUVDUHXVXDOO\FODVVL¿HGDVSRVLWLYH or negative for A. aegypti. Under normal circumstances the ODUYDOVXUYH\GDWDWDNHVXSWRZHHNVWREHFROOHFWHGDQG

organized which results in a delay to characterize the area as a risk area requiring control measures.

Among the existing indices, some are recommended E\ WKH:RUOG +HDOWK 2UJDQL]DWLRQ WR EH XVHG LQ YHFWRU

0 20 40 60 80 100

10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Weeks

Positivity index (%)

0 0.5 1 1.5 2

Premisses index

(7)

VXUYHLOODQFHDQGLGHQWL¿FDWLRQRIKRWVSRWV7KHVHLQFOXGH WKH+,WKH%,DQGWKH&,RIZKLFKWKH¿UVWWZRWKHPRVW commonly used. In Brazil, they are used for determining WKHSRWHQWLDODUHDVRIULVNIRUGHQJXHRXWEUHDNV)81$6$ 3,YDOXHVDERYHDQG%,DERYHLQGLFDWHULVN areas where dengue transmission is likely to occur (FUNASA 7KHXVHRIODUYDOVXUYH\VLQDVVHVVLQJWKHULVNRI GHQJXHRXWEUHDNVDQGWUDQVPLVVLRQKDVEHHQXQGHUDORWRI FULWLFLVPEHFDXVHWKHWUDQVPLVVLRQRIWKHGLVHDVHFDQVWLOO RFFXUZKHQVHHPLQJO\VDIHLQGLFHVZHUHREWDLQHG7XQ/LQ et al.)RFNV

In the present study, the four larval surveys conducted VKRZHGDSRVLWLYHUHODWLRQEHWZHHQ+,VDQG%,VZLWKWKH VDPHYDOXHVLQGLFDWLQJWKDWHDFKSRVLWLYHKRXVHKDGMXVWRQH SRVLWLYHEUHHGLQJVLWH7KLVORZQXPEHURISRVLWLYHFRQWDLQHUV ZDVUHÀHFWHGLQWKHORZ&RQWDLQHU,QGLFHVLQWKHWZRPRQWKV The CI is not suited to assess larval density when multiple containers are located in the vicinity of the premises, as REVHUYHGE\%DQJet al. (1981) in the southeast of Nigeria. These authors pointed out that even when the CI is low, the production of AedesFDQEHUHODWLYHO\KLJK

In Brazil, the most common entomological surveillance indices for A. aegypti are the PI and the BI (FUNASA $FFRUGLQJWR7XQ/LQet al. (1996), they are the most representative indices, and are often correlated. In areas with low infestations, the PI and the BI are essentially the same, EXWDVWKHUDWHRILQIHVWDWLRQLQFUHDVHVWKHWZRLQGLFHVEHJLQ WRGLYHUJHGXHWRWKHODUJHQXPEHURIKRXVHVZLWKPXOWLSOH EUHHGLQJSODFHV6HUYLFH

,Q %HOR +RUL]RQWH¶V &LW\ &RXQFLO FRQGXFWHG WKUHH ODUYDO VXUYH\V ZLWK D VDPSOH RI GXULQJ -DQXDU\0DUFKDQG2FWREHULQWKHVDPHDUHDRIWKHSUHVHQW H[SHULPHQWDQGWKH3,VREWDLQHGZHUHDQG respectively. Although the sampled area was larger than the DUHDFRYHUHGE\WKHSUHVHQWH[SHULPHQWWKHUHLVDUHPDUNDEOH VLPLODULW\EHWZHHQWKHUHVXOWV7KHVDPHUHGXFHGWUHQGGXULQJ the dry months of May and June. Similarly, the present study revealed a reduced trend in the larval indices whenever the WHPSHUDWXUHDQGWKHUDLQIDOOGURSSHGEXWGXHWRWKHUHGXFHG QXPEHU RI VDPSOHV LW ZDV LPSRVVLEOH WR GR D VWDWLVWLFDO DQDO\VLVFRUUHODWLQJWKHVHYDULDEOHV

1RWRQO\GRWKHLQGLFHVREWDLQHGWKURXJKODUYDOVXUYH\V VKRZDORZFRUUHODWLRQZLWKWKHQXPEHURIDGXOWV6HUYLFH 7XQ/LQet al. 7XQ/LQet al. EXWWKH\DOVR PDNHLWGLI¿FXOWWRYHULI\WKRVHFRQWDLQHUVWKDWKDGA. aegypti mosquitoes, since different species of the Aedes mosquito FDQVKDUHWKHVDPHFRQWDLQHU)XUWKHUPRUHLIMXVWRQHODUYD LVXVHGLQWKHVDPSOLQJWKHUHVXOWFDQEHIDOVHQHJDWLYHIRU LWLVSUDFWLFDOO\LPSRVVLEOHWRGLVWLQJXLVKGLIIHUHQWVSHFLHVRI AedesLQWKH¿HOGZLWKRXWSURSHUHTXLSPHQWVXFKDVVWHUHR microscope. The wide variety of containers natural and KXPDQPDGHZKHUHWKLVYHFWRUFDQEHIRXQGDQGWKHSRVVLEOH ODFNRIVNLOORIVRPH¿HOGZRUNHUVDUHIDFWRUVWKDWLQWHUIHUH ZLWKWKHTXDOLW\RIWKHUHVXOWVREWDLQHGIURPODUYDOVXUYH\V $ VWXG\ LQ 6DQ 'RPLQJR 'RPLQLFDQ 5HSXEOLF WKDW utilized the capture of adult females (through active search) DQGWKHRYLWUDSGLGQRWVHHDQ\UHODWLRQEHWZHHQWKHGHQVLW\ RIDGXOWVDQGWKHWKUHHODUYDOLQGLFHVRUWKHQXPEHURIHJJV FROOHFWHG6HUYLFH7KH\FRQFOXGHGWKDWHQWRPRORJLFDO LQGLFHVEDVHGRQDGXOWGHQVLW\DUHPRUHVXLWDEOHIRUDVVHVVLQJ

WKHHI¿FDF\RIFRQWURODFWLRQVWKDQIRUPRQLWRULQJLPPDWXUH forms. Tun-Lin et al. (1996) expressed the need for low cost monitoring methods targeting adult A. aegypti, and suggested utilizing traps with a sticky lure to monitor adults of this vector.

At present, the oviposition trap is an important tool in PRQLWRULQJSURJUDPVSURYLGLQJUHOHYDQWLQIRUPDWLRQDERXW YHFWRUGLVWULEXWLRQ+RZHYHUFDOFXODWLQJWKHGHQVLW\RIWKH adult population of the vector is still a challenge. Monitoring E\PHDQVRIWKHRYLWUDSUHTXLUHVODERUDWRU\ODERUZKHUH those collected AedesHJJVKDYHWREHFRXQWHGDQGKDWFKHG EHIRUHWKHODUYDHFDQEHLGHQWL¿HG7KXVWKLVPHWKRGDIWHU the removal of the paddles from the ovitrap, it still needed DWOHDVWRQHZHHNWRKDYHWKHFRPSOHWHUHVXOWV)RFNV 'HVSLWHEHLQJIDVWHUDQGPRUHSUDFWLFDOIRUVXUYHLOODQFHWKDQ larval surveys, the ovitrap also takes from one to two weeks to analyze and characterize the hotspot areas.

In the present work, the egg hatching rate was low DQGZDVOLNHO\GXHWRGDPDJHWRWKHHJJVZKHQWKH SDGGOHVZHUHWUDQVSRUWHGIURPWKH¿HOGWRWKHODERUDWRU\,Q addition, the growth regulator added to the infusion may have impregnated the paddles and affected egg hatching.

$ JUHDWHU SURSRUWLRQ RI WKH LGHQWL¿HG ODUYDH ZHUHA. aegypti ZKHUHDV WKH RWKHUV ZHUHA. albopictus 7KHVHSURSRUWLRQVZHUHVOLJKWO\GLIIHUHQWIURPWKH DGXOWFDWFKLQJE\WKH0RVTXL75$3RIA. aegypti and RIA. albopictus). The AedesIHPDOHQHHGVMXVWRQH VXFFHVVIXOEORRGIHHGLQJWROD\XSWRHJJVDQGVLQFHWKH HJJVDUHQRWDOORYLSRVHGLQWKHVDPHFRQWDLQHUWKH\FDQEH found scattered in many ovitraps (Consoli & Oliveira 1994). ,WKDVDOVREHHQVSHFXODWHGIURPVWXGLHVRIRWKHUVSHFLHVRI Aedes(Kitronet al. 1989), a likely reduction in the laying of more eggs when the surface of the oviposition paddle is already full of eggs, which would require a search for new containers and the dispersion of the eggs. These may increase WKHQXPEHURISRVLWLYHEUHHGLQJSODFHVLQWKHHQYLURQPHQW In contrast, the MosquiTRAP captures females attempting WR OD\ HJJV LQ WKH WUDS WKHUHE\ HOLPLQDWLQJ WKH DELOLW\ WR OD\HJJVLQRWKHUWUDSVRULQFUHDVHWKHQXPEHURISRVLWLYH EUHHGLQJVLWHV

&RQGXFWLQJ ¿HOG VWXGLHV ZLWK D VWLFN\ RYLWUDS TXLWH similar to MosquiTRAP®, Ritchie et alREVHUYHGWKDW WKHSRVLWLYHLQGH[IRUWKHVWLFN\RYLWUDSZDVZKLOH WKHSRVLWLYHLQGH[RIWKHRYLWUDSZDVZLWKWKHIRUPHU EHLQJVOLJKWO\PRUHHIIHFWLYHLQGHWHFWLQJA. aegypti. In this VDPHVWXG\WKHDXWKRUVFRPSDUHGWKHHI¿FDF\RIWKLVVWLFN\ trap with the ovitrap and the larvitrap installed in an airport (vector entrance site) over a period of nine weeks. They REVHUYHGWKDWWKHVWLFN\RYLWUDSGHWHFWHGWKHYHFWRUPRUH frequently than the other two traps.

In Pedro Leopoldo city, Minas Gerais, Eiras (pers. &RPPREWDLQHGLQGLFHVUDQJLQJIURPWRZLWK WKH0RVTXL75$3DQGIURPWRZLWKWKHRYLWUDS ,Q WKLV VDPH VWXG\ D KLJK FRUUHODWLRQ 3HDUVRQ EHWZHHQWKHSRVLWLYHLQGLFHVRIWKHWZRWUDSVZDVREVHUYHG VXJJHVWLQJWKDWWKH0RVTXL75$3LVVXLWDEOHIRUGHWHFWLQJWKH vector in A. aegypti monitoring programs. However, the same SRVLWLYHFRUUHODWLRQRIWKH0RVTXL75$3REVHUYHGLQSUHYLRXV VWXGLHVZDVQRWREVHUYHGLQWKHSUHVHQWH[SHULPHQW

(8)

March - April 2007 Neotropical Entomology 36(2)

LQGH[ UDQJHG IURP ]HUR WR DQG DGXOWV ZHUH RQO\ FROOHFWHG GXULQJ ZHHNV 7KLV PD\ EH DWWULEXWHG WR PRVTXLWRHVEHLQJDEOHWRÀ\ZLWKLQWKH0RVTXL75$3DQG HVFDSHZLWKRXWODQGLQJDQGFRQVHTXHQWO\QRWEHLQJWUDSSHG Thus, this suggests that the MosquiTRAP needs further PRGL¿FDWLRQVLQRUGHUWRLQFUHDVHFDSWXUHRIDOOPRVTXLWRHV HQWHULQJWKHWUDS/RZQXPEHUVRIPRVTXLWRHVFDXJKWLQ VWLFN\WUDSVKDVDOVREHHQUHSRUWHGLQ$XVWUDOLD5LWFKLHet

al5XVVHOet al

The ovitrap detected the presence of the Aedes mosquitoes during the entire experimental period (17 weeks), whereas WKH0RVTXL75$3GHWHFWHGLWVSUHVHQFHIRURQO\ZHHNV 7KHODUYDOVXUYH\ZDVDEOHWRGHWHFWWKHSUHVHQFHRIAedes PRVTXLWRHVRQO\DWWKHthDQGth epidemiological weeks. Therefore, the MosquiTRAP was more sensitive to detect Aedes than the larval survey. Although the sensitivity of the ovitrap was higher than the MosquiTRAP in detecting the presence of the AedesVS0RVTXLWRWKHRYLWUDSZDVQRWDEOH to detect A. albopictus as the MosquiTRAP did during the ththth, 22nd and 24th epidemiological weeks.

1RVLJQL¿FDQWLQÀXHQFHRIWHPSHUDWXUHDQGUDLQIDOOZDV REVHUYHGLQWKHLQGLFHVFDOFXODWHGIRUWKHWZRWUDSVGXULQJ WKHH[SHULPHQWDOWKRXJKWKHHIIHFWVRIWKHVHYDULDEOHVRQ PRVTXLWRELRORJ\FDQQRWEHLJQRUHG7ZRPDUNHGSHULRGV ZHUHREVHUYHGGXULQJWKHH[SHULPHQW±DUDLQ\RQHIURP WKHth to the 18th epidemiological week, and a dry one, from the 19th to the 26th week. When each period is analyzed VHSDUDWHO\WKHLQÀXHQFHRIWKHUDLQIDOORQWKHQXPEHURIHJJV FROOHFWHGFDQEHREVHUYHG3)LJ'XULQJWKH UDLQ\SHULRGRIDOOWKHHJJVQ DQGRI the total adults (n =26) were collected. Thus, this suggests DVWURQJFRUUHODWLRQEHWZHHQWKHYROXPHRIUDLQIDOODQGWKH QXPEHURIDGXOWVFDXJKW

7KHFDSWXUHRIDGXOWVE\WKH0RVTXL75$3DQGRIHJJV E\WKHRYLWUDSZDVVXVWDLQHGHYHQGXULQJWKHGU\VHDVRQ (18th to the 26th epidemiological week). However, the larval VXUYH\ ZDV XQDEOH WR ORFDWH SRVLWLYH EUHHGLQJ VLWHV ZLWK ODUYDHGXULQJWKHGU\VHDVRQ,3 LQth and 24th weeks). $VWHPSHUDWXUHLQFUHDVHGWKHQXPEHURIFROOHFWHGHJJVDQG adults caught also increased, while the opposite was true in relation to the volume of rainfall. This reduction in the QXPEHURIHJJVDQGDGXOWVFDSWXUHGLVSUREDEO\GXHWRDQ LQFUHDVHLQWKHQXPEHURIEUHHGLQJSODFHVDQGDYDLODEOHLQ WKHDUHDFUHDWLQJDFRPSHWLWLRQEHWZHHQWKHQDWXUDOEUHHGLQJ places and the ovitraps and the MosquiTRAP.

The use of sticky ovitraps, such as the MosquiTRAP, has potential use for detecting Aedes sp. populations and perhaps for monitoring in hotspot areas to further develop QHZHQWRPRORJLFDOLQGLFHVIRUGHQJXHRXWEUHDNVLQXUEDQ areas. The functionality, practicality and low cost of the 0RVTXL75$3DUHIHDVLEOHWRXVHLQDODUJHVFDOHRIPRQLWRULQJ dengue vector programs. Although the MosquiTRAP caught DORZQXPEHURIAedes mosquitoes during the study, the results clearly showed that the MosquiTRAP was more sensitive to detect the presence of Aedes mosquitoes larval VXUYH\PHWKRGVZKLFKDUHFRUUHQWO\HPSOR\HGE\WKH13'& in Brazil. At the moment, a new updated version of the 0RVTXL75$3YHUVLRQLVXQGHUGHYHORSPHQWZKLFKXVHV V\QWKHWLFRYLSRVLWLRQDWWUDFWDQWLGHQWL¿HGIURPJUDVVLQIXVLRQ YRODWLOHV6DQWDQD

Acknowledgments

7R%HOR+RUL]RQWH¶V&LW\&RXQFLO3DPSXOKD6DQLWDU\ 'LVWULFWIRUWKHORJLVWLFVXSSRUWLQWKH¿HOGDFWLYLWLHV7R WKH¿HOGDJHQWVZKRFDUULHGRXWWKHODUYDOVXUYH\DQGWR 5RVHPDU\ 5RTXH ,VLV 0LUDQGD 0DtUD 1HYHV /L]DQGUD -XOLDQD DQG IURP WKH /DERUDWyULR GH &XOLFtGHRV DUH DOVR acknowledged for their help with the field. To CNPq, )81$6$(FRYHF/WGDIRUWKH¿QDQFLDOVXSSRUW

References

%DQJ<+'1%RZQ $22QZXELNR3UHYDOHQFHRI

larvae of potential yellow fever vectors in domestic water

FRQWDLQHUVLQVRXWKHDVW1LJpULD%XOO:+2

Barata, E.A.M.F., A.I.P. Costa, F. Chiaravalloti Neto, C.B. Glasser,

-06%DUDWD '1DWDO3RSXODomRGHAedes aegypti

(L) em área endêmica de dengue, Sudeste do Brasil. Rev. Saúde

3XEO

Braga, I.A., A.C. Gomes, M. Nelson, R.D. Mello, D.P. Bergamaschi

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surveys and ovitraps to monitor population of Aedes aegypti. 5HY6RF%UDV0HG7URS

Consoli, R.A.G.B. & R.L. Oliveira. 1994. Principais mosquitos de importância sanitária no Brasil. Ed. Fio Cruz, Rio de Janeiro, 228p.

(LUDV$($UPDGLOKDSDUDFDSWXUDGHLQVHWRV'HSyVLWR GHSDWHQWHQR%UDVLO3,

)RFNV'$$UHYLHZRIHQWRPRORJLFDOVDPSOLQJPHWKRGVDQG LQGLFDWRUVIRUGHQJXHYHFWRUV:+2*DLQVYLOOHS )XQGDomR1DFLRQDOGH6D~GH)81$6$'HQJXH,QVWUXomR

SDUDSHVVRDOGHFRPEDWHDRYHWRU0DQXDOGHQRUPDVWpFQLFDV HG$VFRP3UH)81$6$%UDVtOLDS

)XQGDomR1DFLRQDOGH6D~GH)81$6$3URJUDPDQDFLRQDO

de controle da dengue (PNCD). Ed. Min. da Saúde - FUNASA,

%UDVtOLDS

*RPHV$&0HGLGDVGRVQtYHLVGHLQIHVWDomRXUEDQDSDUD Aedes aegypti (Stegomyia) aegypti e Aedes (Stegomyia) albopictus HP SURJUDPDV GH YLJLOkQFLD HQWRPROyJLFD ,QI (SLGHPLRO

,EDxH]%HUQDO6%%ULVHxR-30XWHEL($UJRW*5RGUtJXH] &0DUWtQH]&DPSRV53D]53)XHQWH6DQ57DSLD&RQ\HU

& A. Flisserv. 1997. First record in America of Aedes albopictus QDWXUDOO\LQIHFWHGZLWKGHQJXHYLUXVGXULQJWKHRXWEUHDN DW5H\QRVD0p[LFR0HG9HW(QWRPRO .LWURQ8''::HEE 5-1RYDU2YLSRVLWLRQEHKDYLRU

of Aedes triseriatus (Diptera: Culicidae): Prevalence, intensity,

and aggregation of eggs in oviposition traps. J. Med. Entomol. 26: 462-67.

(9)

5LWFKLH$66/RQJ$+DUG&(:HEE 5&5XVVHOO $QDGXWLFLGDOVWLFN\RYLWUDSIRUVDPSOLQJFRQWDLQHUEUHHGLQJ

mosquitoes. J. Am. Mosq. Control. Assoc.

Ritchie, A.S., S. Long, A. Hard, G. Smith, A. Pyke & T.B. Knox.

(QWRPRORJLFDO LQYHVWLJDWLRQV LQ D IRFXV RI GHQJXH WUDQVPLVVLRQLQ&DLUQV4XHHQVODQG$XVWUDOLDE\XVLQJWKH

sticky ovitrap. J. Med. Entomol. 4: 1-4

5XVVHO5&&(:HEE&5:LOOLDQV $65LWFKLH0DUN

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Entomol. 19: 1-7.

6DQW¶$QD$/5RTXH5$ $((LUDV&KDUDFWHULVWLFVRI

grass infusions as oviposition attractants to Aedes (Stegomyia)

'LSWHUD&XOLFLGDH-0HG(QWRPRO

Serufo, J.C., H.M. Oca, V.A. Tavares, A.M. Souza, R.V. Rosa, M.C. Jamal, J.R. Lemos, M.A. Oliveira, R.M.R. Nogueira & H.G.

6FKDW]PD\U,VRODWLRQRIGHQJXHYtUXVW\SHIURPODUYDH

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7XQ/LQ:%+.D\ $%DUQHV7KHSUHPLVHFRQGLWLRQ

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7URS0HG+\J

Tun-Lin, W., B.H. Kay & A.S. Barnes. 1996. Forsyth. Critical examination of Aedes aegypti indices: correlations with DEXQGDQFH$P-7URS0HG+\J

Imagem

Fig. 2. Variation of temperature (maximum and minimum) and precipitation during the 17 epidemiological weeks study at the  GLVWULFWRI,WDSRm%HOR+RUL]RQWH0* )LJ'LDJUDPRIWKHVWLFN\0RVTXL75$3YHUVLRQ05101520253035 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Referências

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