Abundance and updated distribution of Aedes aegypti (Diptera: Culicidae) in Cabo Verde Archipelago : a neglected threat to public health

In e na ional Jou nal o En i onmen al Resea ch and Public Heal h A icle Abundance and Upda ed Dis ibu ion o Aedes aegyp i (Dip e a: Culicidae) in Cabo Ve de A chipelago: A Neglec ed Th ea o Public Heal h Sil ânia Da Veiga Leal 1,* , Isaias Bap is a Fe nandes Va ela 1, Ade i ow Augus o Lopes Gonçal es 1, Da idson Daniel Sousa Mon ei o 1, Celi ianne Ma isia Ramos de Sousa 1, Ma ia da Luz Lima Mendonça 1, Adilson JoséDe Pina 2, Ma ia João Al es 3,4 and Hugo Cos a Osó io 3,4 1 Labo a ó io de En omologia M é dica, Ins i u o Nacional de Sa ú de P ú blica, La go do Desas e da Assis ê ncia, Chãde A eia, P aia 719, Cabo Ve de; IsaiasB.V[email p o ec ed].c (I.B.F.V.); Ade i ow[email p o ec ed].c (A.A.L.G.); [email p o ec ed].c (D.D.S.M.); [email p o ec ed].c (C.M.R.d.S.); [email p o ec ed].c (M.d.L.L.M.) 2 P og ama de P é -Eliminaç ã o do Paludismo, CCS-SIDA, Minis é io da Sa ú de e da Segu ança Social, Va zea, P aia 855, Cabo Ve de; [email p o ec ed].c 3Ins i u o Nacional de Saúde Dou o Rica do Jo ge, Cen o de Es udos de Vec o es e Doenças In ecciosas, A enida da Libe dade 5, 2965-575 Águas de Mou a, Po ugal; [email p o ec ed] (M.J.A.); [email p o ec ed] (H.C.O.) 4Ins i u o de Saúde Ambien al, Faculdade de Medicina da Uni e sidade de Lisboa, A . P o . Egas Moniz, Ed. Egas Moniz, Piso 0, Ala C, 1649-028 Lisboa, Po ugal *Co espondence: [email p o ec ed].c Recei ed: 27 No embe 2019; Accep ed: 8 Decembe 2019; Published: 17 Feb ua y 2020   Abs ac : Backg ound: Mosqui o-bo ne i uses, such as Zika, dengue, yellow e e , and chikungunya, a e impo an causes o human diseases nea ly wo ldwide. The g ea es heal h isk o a bo i al disease ou b eaks is he p esence o he mos compe en and highly in asi e domes ic mosqui o, Aedes aegyp i. In Cabo Ve de, wo ecen a bo i us ou b eaks we e epo ed, a dengue ou b eak in 2009, ollowed by a Zika ou b eak in 2015. This s udy is he i s en omological su ey o Ae. aegyp i ha includes all islands o Cabo Ve de a chipelago, in which we aim o e alua e he ac ual isk o ec o -bo ne a bo i uses as a con inuous upda e o he geog aphical dis ibu ion o his species. Me hods: In o de o assess i s cu en dis ibu ion and abundance, we unde ook a mosqui o la al su ey in he nine inhabi ed islands o Cabo Ve de om No embe 2018 o May 2019. En omological la al su ey indices we e calcula ed, and he abundance analyzed. We collec ed and iden i ied 4045 Ae. aegyp i mosqui oes om 264 posi i e b eeding si es in 22 municipali ies and con i med he p esence o Ae. aegyp i in e e y inhabi ed island. Resul s : Wa e d ums we e ound o be he mos p e alen con aine s (n=3843; 62.9%), bu puddles (n=27; 0.4%) we e he mos p oduc i e habi a s ound. The o e all a e age o he House, Con aine , and B e eau la al indices we e 8.4%, 4.4%, and 10.9, espec i ely. Howe e , 15 ou o he 22 municipali ies showed ha he B e eau Index was abo e he epidemic isk h eshold. Conclusion: These esul s sugges ha i no ec o con ol measu es a e conside ed o be in place, he isk o new a bo i al ou b eaks in Cabo Ve de is high. The ec o con ol s a egy adop ed mus include measu es o public heal h di ec ed o domes ic wa e s o age and managemen . Keywo ds: Aedes aegyp i; a bo i uses; la al index; su eillance; con ol; Cabo Ve de In . J. En i on. Res. Public Heal h 2020,17, 1291; doi:10.3390/ije ph17041291 www.mdpi.com/jou nal/ije ph In . J. En i on. Res. Public Heal h 2020,17, 1291 2 o 11 1. In oduc ion Mosqui o-bo ne a bo i al diseases a e o global impo ance. Zika, dengue e e , and chikungunya a e cu en ly he mos challenging a bo i uses o in e na ional public heal h, despi e con ol p og am e o s and esea ch in new con ol me hodologies [ 1 – 3 ]. Fou billion people li e in geog aphic a eas sui able o dengue i us ansmission alone [ 4 – 6 ]. The p esence and abundance o ec o mosqui oes associa ed wi h hese diseases a e he key poin s o he heal h isks o a bo i al disease ou b eaks. Globally, Aedes aegyp i (Linnaeus, 1762) (=S egomyia aegyp i) is he p ima y ec o o all hese i uses, ollowed by o he Aedes species, namely Aedes albopic us (Skuse, 1895) (=S egomyia albopic a), which a e a compe en and epidemiologically signi ican species [ 1 ]. Ae. aegyp i is he in asi e mosqui o species ha ha e caused he mos human casual ies wo ldwide. They a e a highly an h opophilic, pe idomes ic, day bi ing species ha usually b eed in a i icial si es inside o a ound dwellings [7–10]. In Cabo Ve de, wo mosqui o-bo ne i us ou b eaks we e ecen ly epo ed o he i s ime: a dengue ou b eak in 2009, wi h mo e han 21,000 no i ied cases, including 174 cases o dengue hemo hagic e e and ou epo ed dea hs. This was ollowed by a Zika ou b eak in 2015, wi h mo e han 7500 no i ied cases and 18 associa ed cases o mic ocephaly [ 11 – 13 ]. This was he i s ime ha a Zika s ain associa ed wi h hese neu ological damages in in an s was de ec ed in A ica [ 12 ]. In Cabo Ve de, Ae. aegyp i is so a he only mosqui o ec o associa e o hese a bo i uses. The a chipelago o Cabo Ve de is loca ed on he wes coas o A ica, and is composed o 10 islands clus e ed in wo g oups: he Ba la en o g oup (comp ising he islands o San o An ã o, S ã o Vicen e, San a Luzia, S ã o Nicolau, Sal, and Boa is a) and he So a en o g oup (comp ising he islands o Maio, San iago, Fogo, and B a a). Howe e , each island has speci ic opog aphy and displays di e ences in mic oclima e and ege a ion. His o ically, he opog aphy and geog aphical loca ion o Cabo Ve de has p omo ed and allowed o he ac i e mo emen o popula ion and goods [ 14 ]. This inc eases he isk o pa hogen ci cula ion h ough in ec ed a ele s, which can cause he eme gence o e-eme gence o a bo i al diseases i compe en mosqui o ec o s a e p esen and ec o capaci y is high [ 15 ]. In 2015, Cabo Ve de had a passenge olume o mo e han 7000 a ele s om Zika-a ec ed coun ies, including di ec ligh s om B azil [ 13 ]. The modi ica ion o he en i onmen by an h opic ac ions, diso de ed u ban planning, popula ion g ow h, and eme gen ac o s ela ed o he globaliza ion p ocess and clima e change a ec he bionomics o mosqui o ec o s, inc easing hei ec o ial capaci y [16–18]. In he a chipelago o Cabo Ve de, 11 mosqui o species belonging o i e gene a we e epo ed: Aedes caspius (Pallas, 1771), Ae. aegyp i (Linnaeus, 1762), Anopheles p e o iensis (Theobald, 1903), Anopheles a abiensis (Pa on, 1905), Culex bi aenio hynchus (Giles, 1901), Culex quinque ascia us (Say, 1823), Culex pipiens (Linnaeus, 1758), Culex pe exiguus (Theobald, 1903), Culex i aenio hynchus (Giles, 1901), Lu zia ig ipes (de G andp e and de Cha moy, 1901),and Culise a longia eola a (Macqua , 1838) [ 19 – 22 ]. En omological su eys in Cabo Ve de s a ed in he 1920s and Ae. aegyp i was epo ed o he i s ime by San ’Anna in 1931 on S ã o Vicen e island [ 19 ]. The da a om hese pionee su eillance ope a ions we e compiled wi h he las coun ywide mosqui o su ey [ 19 ]. In 2007, ano he en omological su ey was ca ied ou on he ou islands o he So a en o g oup: Maio, San iago, Fogo, and B a a. Ae. aegyp i was de ec ed on San iago, Fogo, and B a a [ 21 ]. In 2011, an en omological su ey was ca ied ou in San iago, whe e Ae. aegyp i was epo ed in he municipali ies o P aia and Ta a al [ 22 ]. Phylogeog aphic and popula ion gene ic s udies o Cabo Ve de’s Ae. aegyp i popula ion sugges ed an ancien Wes A ican o igin, mos likely om Senegal, and a popula ion belonging o he subspecies o mosus [ 23 ]. In eg a ed ec o con ol measu es, including s a egies o sou ce educ ion by b eeding si e elimina ion, biological con ol wi h ish, and chemical con ol wi h insec icides, ha e been used owa d con olling mala ia and dengue, Anopheles a abiensis, and Ae. aegyp i, espec i ely [ 24 ]. Rega ding insec icide suscep ibili y, knockdown esis ance (kd ) mu a ions, gene ic mu a ion con e ing esis ance o dichlo odiphenyl ichlo oe hane (DDT), and py e h oids insec icides we e no ound in 2007 and 2010 Ae. aegyp i samples. This is in line wi h insec icide suscep ibili y es s pe o med on Ae. aegyp i om San iago Island du ing he dengue ou b eak in 2009 [ 23 , 25 ]. Howe e , he si ua ion changed in 2012 and 2014, wi h he i s epo s o esis ance o hese insec icides [26]. In . J. En i on. Res. Public Heal h 2020,17, 1291 3 o 11 One o he ools used in Ae. aegyp i su eillance is he de e mina ion o S egomyia indices, namely he House Index (HI), Con aine Index (CI), and B e eau Index (BI). These indices measu e he abundance, spa ial dis ibu ion, and p o ide in o ma ion abou a eas o pe iods o mosqui o popula ion g ow h [27–31]. Mos o he s udies on Ae. aegyp i based on S egomyia indices suppo a signi ican associa ion be ween hese and he ansmission isk o a bo i uses [ 32 – 36 ]. In s udies ha did no obse e his associa ion, mosqui o and human mig a ion we e conside ed as possible ac o s ha a ec ed he lack o associa ion [ 37 – 39 ]. Hence, knowledge o hese indices allowed o he imely applica ion o con ol measu es and s a egies [40]. In his con ex , we aimed o e alua e he ac ual isk o ec o -bo ne a bo i uses in Cabo Ve de based on he S egomyia indices, as a con inuous upda e o he geog aphic dis ibu ion o Ae. aegyp i. To ou knowledge, his s udy ep esen s he i s en omological su ey o his species ha includes all islands o Cabo Ve de a chipelago. 2. Me hods 2.1. S udy A ea We collec ed mosqui o la ae in he 22 municipali ies o Cabo Ve de, a olcanic a chipelago wi h an a ea o 4033 km 2 loca ed abou 550 km o he coas o Senegal. The a chipelago consis s o 10 islands, nine o which a e inhabi ed wi h app oxima ely 537,660 inhabi an s (Figu e 1). I has an a id and semi-a id clima e, wa m and d y, wi h an a e age annual empe a u e o a ound 25 ◦ C, and low ain all. Two seasons can be iden i ied: he d y season, om Decembe o June, and he ainy season, om Augus o Oc obe [41,42]. In . J. En i on. Res. Public Heal h 2020, 17, 1291 3 o 11 om San iago Island du ing he dengue ou b eak in 2009 [23,25]. Howe e , he si ua ion changed in 2012 and 2014, wi h he i s epo s o esis ance o hese insec icides [26]. One o he ools used in Ae. aegyp i su eillance is he de e mina ion o S egomyia indices, namely he House Index (HI), Con aine Index (CI), and B e eau Index (BI). These indices measu e he abundance, spa ial dis ibu ion, and p o ide in o ma ion abou a eas o pe iods o mosqui o popula ion g ow h [27–31]. Mos o he s udies on Ae. aegyp i based on S egomyia indices suppo a signi ican associa ion be ween hese and he ansmission isk o a bo i uses [32–36]. In s udies ha did no obse e his associa ion, mosqui o and human mig a ion we e conside ed as possible ac o s ha a ec ed he lack o associa ion [37–39]. Hence, knowledge o hese indices allowed o he imely applica ion o con ol measu es and s a egies [40]. In his con ex , we aimed o e alua e he ac ual isk o ec o -bo ne a bo i uses in Cabo Ve de based on he S egomyia indices, as a con inuous upda e o he geog aphic dis ibu ion o Ae. aegyp i. To ou knowledge, his s udy ep esen s he i s en omological su ey o his species ha includes all islands o Cabo Ve de a chipelago. 2. Me hods 2.1. S udy A ea We collec ed mosqui o la ae in he 22 municipali ies o Cabo Ve de, a olcanic a chipelago wi h an a ea o 4033 km2 loca ed abou 550 km o he coas o Senegal. The a chipelago consis s o 10 islands, nine o which a e inhabi ed wi h app oxima ely 537,660 inhabi an s (Figu e 1). I has an a id and semi-a id clima e, wa m and d y, wi h an a e age annual empe a u e o a ound 25 °C, and low ain all. Two seasons can be iden i ied: he d y season, om Decembe o June, and he ainy season, om Augus o Oc obe [41,42]. Figu e 1. Geog aphic localiza ion o Cabo Ve de a chipelago (A), islands’ dis ibu ion in he a chipelago; (B), ega ding he Wes Coas o A ica). Figu e 1. Geog aphic localiza ion o Cabo Ve de a chipelago ( A ), islands’ dis ibu ion in he a chipelago; (B), ega ding he Wes Coas o A ica). In 2010, 141,762 accommoda ions, including 114,469 buildings, we e egis e ed in he coun y. O hose, 94,894 (82.9%) ha e one di ision/ oom, 10,646 (9.3%) ha e wo di isions/ ooms, and 6983 In . J. En i on. Res. Public Heal h 2020,17, 1291 4 o 11 (6.1%) a e buildings wi h h ee o mo e ooms. O he o al buildings, 74,404 (65%) a e inished, while he emaining a e unde cons uc ion. Rega ding he ype o habi a , 44,185 (38.6%) o he houses a e in u ban a eas and 30,449 (26.6%) in u al a eas [43]. Mo e han 95% o he popula ion use con en ional ma e ial o cons uc ion o hei houses, 3.9% use non-con en ional ma e ial, and 1.3% use a ha ched oo , b ass, d um pla es, o o he s o co e [44,45]. The mos common pa emen ypes (99.4%) a e cemen and mosaic, and only 0.6% a e clay o o he [ 46 ]. In e ms o wall cladding, 66.7% a e plas e ed and pain ed, while jus o e 16% do no ha e any ype o coa ing. Rega ding he ceilings, mos (79.3%) use ein o ced conc e e e aces [42]. One- hi d o Cape Ve deans do no ha e access o public wa e [ 45 ] and o hose who do ha e access, he dis ibu ion is i egula , leading o wa e s o age inside and ou side o he homes. In u al and semi- u al a eas, pig pens o henne ies a e ound a ound he houses, om which addi ional income is ob ained [47]. 2.2. En omological Collec ions and Sampling Me hodology F om No embe 2018 o May 2019, mosqui o la ae we e collec ed in all municipali ies o Cabo Ve de. We selec ed he sampling a ea wi h each municipal heal h delega ion eam, acco ding o he high incidence his o y o mosqui o-bo ne diseases, Ae. aegyp i densi ies, and he human popula ion. The houses we e selec ed andomly, bo h in u al and u ban a eas. In u ban a eas wi h wo pa allel ows o houses, he selec ion was made by choosing a i s house and hen skipping ou houses, coun ing a zigzag pa e n. All con aine s, o po en ial b eeding si es wi h wa e o la ae, we e inspec ed and eco ded (con aine ype, posi ion, ege a ion, and sun exposu e). The collec ed la ae we e anspo ed o he Na ional Ins i u e o Public Heal h (INSP) Medical En omology Labo a o y o mo phological iden i ica ion. 2.3. Mo phological Iden i ica ion La ae and ea ed adul mosqui oes we e mo phologically iden i ied as Ae. aegyp i unde a s e eomic oscope, acco ding o he iden i ica ion keys o Ribei o e al. [ 19 , 48 – 50 ]. The la ae we e moun ed on slides wi h 2% glyce ina ed Hoye ’s medium, and adul ea ed mosqui oes, and s o ed a −20 ◦C o u he molecula and gene ic analysis. 2.4. S a is ical Analysis We compiled he da a in o a Mic oso Excel da abase. Fo he da a analysis, he con inuous a iables we e exp essed in measu es o cen al endency and dispe sion, and he ca ego ical ones in simple equency. The chi-squa e es was used o de e mine he associa ion be ween he p esence o Ae. aegyp i and he ype o b eede /con aine ( ype, posi ion, and physical cha ac e is ics). We conside ed posi i e b eeding si es o Ae. aegyp i whe e he e was a leas one la a. The le el o signi icance o s a is ical analysis was 0.05. We used IBM SPSS S a is ics 20 (In e na ional Business Machines Co po a ion, New Yo k Ci y, NY, USA) o analyze he da a. La al indices we e calcula ed, namely, HI, CI, and BI. The maps we e d awn using A cGIS 10.6 (En i onmen al Sys ems Resea ch Ins i u e, Redlands, CA, USA). 3. Resul s A o al o 2612 houses we e su eyed in he 22 municipali ies o Cabo Ve de, and 6113 con aine s we e inspec ed. O hese, imma u e mosqui oes we e de ec ed in 7.5% (n=458) o all inspec ed con aine s, he majo i y (84.3%; n=386) loca ed ou doo s, and he o he s (15.7%; n=72) indoo s. No signi ican di e ences we e obse ed in he dis ibu ion o indoo /ou doo and posi i e/nega i e b eeding si es (p>0.05 in bo h cases) (Table 1). In . J. En i on. Res. Public Heal h 2020,17, 1291 5 o 11 Table 1. Numbe o houses, inspec ed con aine s, i s posi ion (indoo /ou doo ), and o al numbe o con aine s wi h mosqui oes’ la ae. Island Municipali ies All Species Ae. aegyp i To al o Inspec ed Houses To al o Inspec ed Con aine s Posi i e Houses Posi i e Con aine s Posi i e Houses Posi i e Con aine s Indoo Ou doo Indoo Ou doo San o An ão Paul 11 2 9 8 2 6 123 231 Po o No o 23 5 26 14 4 11 112 201 Ribei a G ande 18 2 18 8 1 7 125 251 São Vicen e São Vicen e 14 8 16 13 6 15 105 354 São Nicolau Ta a al 27 0 30 25 0 28 125 302 Ribei a B a a 56 2 68 14 1 19 103 240 Sal Sal 6 0 7 1 0 1 129 282 Boa is a Boa is a 13 0 18 4 0 5 107 246 Maio Maio 25 24 9 22 21 9 101 324 San iago Ta a al 21 6 21 16 0 21 120 274 São Miguel 19 4 22 10 4 8 149 276 San a Ca a ina 8 3 5 4 1 3 117 282 São Sal ado do Mundo 21 4 21 17 4 16 121 319 S ã o Lou enço dos Ó g ã os 11 2 15 3 0 5 130 406 San a C uz 3 1 3 2 1 1 142 359 São Domingos 20 1 19 8 1 7 134 281 P aia 11 2 12 7 1 7 140 386 Ribei a G ande 4 0 4 2 0 3 108 208 Fogo São Filipe 13 4 12 6 3 4 100 151 Mos ei os 4 0 4 3 0 3 105 138 San a Ca a ina 1 0 3 0 0 0 100 242 B a a B a a 35 2 44 29 2 35 116 360 To al 364 72 386 218 55 209 2612 6113 In . J. En i on. Res. Public Heal h 2020,17, 1291 6 o 11 O he 458 con aine s wi h imma u e mosqui oes, 57.6% (n=264) we e posi i e o Ae. aegyp i, o which 20.8% (n=55) we e ound inside dwellings, and 79.2% (n=209) we e ound ou side. A o al o 4045 Ae. aegyp i la ae and pupae we e collec ed om he 264 Aedes-posi i e con aine s ound in all 22 o he coun y’s municipali ies (Table 2). O he mosqui o species ound ac oss he su ey we e Aedes caspius,Anopheles p e o iensis,Anopheles a abiensis,Culex bi aenio hynchus,Culex pipiens s.l. (Culex quinque ascia us,Culex pipiens), Culex i aenio hynchus,Lu zia ig ipes, and Culise a longia eola a. Culex pipiens s.l. and An. p e o iensis we e ound sha ing he same b eeding si es wi h Ae. aegyp i. Wa e d ums (50–200 L) we e he mos common b eeding si es (62.9%; n=3843), ollowed by anks (1000–5000 L) (12.4%; n=756), cis e ns (5000–10,000 L) (6.3%; n=387), and o he ypes o con aine s ha comp ised 18.4% o o al b eeding si es. F om all inspec ed con aine s, 458 (7.5%) we e posi i e, and he p oduc i i y p opo ion analysis o each con aine showed puddles as he mos p oduc i e habi a (33%; n=9), ollowed by lowe po s (21%; n=47), o he (18%; n=53), and anks (12%; n=91). All o he ypes o con aine s showed ha p oduc i i y equaled less han 10% (Figu e 2). In . J. En i on. Res. Public Heal h 2020, 17, 1291 5 o 11 O he 458 con aine s wi h imma u e mosqui oes, 57.6% (n = 264) we e posi i e o Ae. aegyp i, o which 20.8% (n = 55) we e ound inside dwellings, and 79.2% (n = 209) we e ound ou side. A o al o 4045 Ae. aegyp i la ae and pupae we e collec ed om he 264 Aedes-posi i e con aine s ound in all 22 o he coun y’s municipali ies (Table 2). O he mosqui o species ound ac oss he su ey we e Aedes caspius, Anopheles p e o iensis, Anopheles a abiensis, Culex bi aenio hynchus, Culex pipiens s.l. (Culex quinque ascia us, Culex pipiens), Culex i aenio hynchus, Lu zia ig ipes, and Culise a longia eola a. Culex pipiens s.l. and An. p e o iensis we e ound sha ing he same b eeding si es wi h Ae. aegyp i. Wa e d ums (50–200 L) we e he mos common b eeding si es (62.9%; n = 3843), ollowed by anks (1000–5000 L) (12.4%; n = 756), cis e ns (5000–10,000 L) (6.3%; n = 387), and o he ypes o con aine s ha comp ised 18.4% o o al b eeding si es. F om all inspec ed con aine s, 458 (7.5%) we e posi i e, and he p oduc i i y p opo ion analysis o each con aine showed puddles as he mos p oduc i e habi a (33%; n = 9), ollowed by lowe po s (21%; n = 47), o he (18%; n = 53), and anks (12%; n = 91). All o he ypes o con aine s showed ha p oduc i i y equaled less han 10% (Figu e 2). Figu e 2. Numbe and p opo ion o posi i e and nega i e b eeding si es inspec ed du ing he s udy. Puddles Flowe po s O he s Tanks Ti es Wells Wa e oun ains Wa e d ums Ce amic po s Cis e ns Bucke s Nega i e 18 172 240 665 18 10 86 3627 112 373 334 Posi i e 9 47 53 91 2 1 7 216 6 14 12 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% Figu e 2. Numbe and p opo ion o posi i e and nega i e b eeding si es inspec ed du ing he s udy. The ou mos p oduc i e con aine s o Ae. aegyp i we e wa e d ums (61.4%), lowe po s (14.4%), anks (8.0%), and bucke s (3.8%) (Table 2). A posi i e associa ion be ween he con aine ype and he p esence o Ae. aegyp i was obse ed ( χ2 =133.816, p<0.001). The equency o o he b eeding si es was ela i ely low, 3% o cis e ns and o he con aine s, and lowe o d inking oun ains, puddles, po s, and i es (Table 2). Table 2. Posi i e con aine s o Aedes aegyp i. Con aine No. o Con aine s wi h Ae. aegyp i (%) No. o Ae. aegyp i (%) No. o Con aine s wi h O he Species (%) Ce amic po s 5 (1.9) 101 (2.5) 1 (0.5) Bucke s 10 (3.8) 102 (2.5) 2 (1.0) Cis e ns 8 (3.0) 107 (2.6) 6 (3.1) Wa e d ums 162 (61.4) 1904 (46.1) 53 (27.6) Flowe po s 38 (14.4) 1455 (36.0) 9 (4.7) Puddles 3 (1.1) 26 (0.6) 6(3.1) Tanks 21 (8.0) 249 (6.2) 70 (36.5) Ti es 2 (0.8) 11 (0.3) 0 (0.0) O he 8 (3.0) 47 (1.2) 45 (23.4) Wa e oun ains 7 (2.7) 43 (1.1) 0 (0.0) To al 264 4045 192 In . J. En i on. Res. Public Heal h 2020,17, 1291 7 o 11 En omological Indices The a e age HI, CI, and BI we e 8.4%, 4.4%, and 10.9, espec i ely. Fi een ou o he 22 s udied municipali ies p esen ed a BI abo e i e. The maximum alues we e in he municipali y o B a a (HI =25%; CI =9.7% and BI =30.2) and he minimum alues, below 1%, we e ound in Sal. In he municipali y o San a Ca a ina (Fogo island), despi e no Ae. aegyp i la ae being ound, adul s we e eco ded du ing he su ey (Table 3). Table 3. En omological indices in municipali ies. Island Municipali ies En omological Indices HI (%) CI (%) BI San o An ão Paul 6.5 3.5 6.5 Po o No o 12.5 7.5 13.4 Ribei a G ande 6.4 6.0 12.0 São Vicen e São Vicen e 12.4 5.9 20.0 São Nicolau Ta a al 20.0 9.27 22.4 Ribei a B a a 13.6 8.3 19.4 Sal Sal * 0.8 0.4 0.8 Boa is a Boa is a * 3.7 2.0 4.7 Maio Maio 21.8 9.3 29.7 San iago Ta a al 13.3 7.7 17.5 São Miguel 6.7 4.3 8.1 San a Ca a ina 3.4 1.4 3.4 São Sal ado do Mundo 14.1 6.3 16.5 S ã o Lou enço dos Ó g ã os * 2.3 1.2 3.8 San a C uz * 1.4 0.6 1.4 São Domingos 6.0 2.8 6.0 P aia 5.0 2.1 5.7 Ribei a G ande * 1.9 1.4 2.7 Fogo São Filipe 6.0 4.6 7.0 Mos ei os * 2.9 2.2 2.9 San a Ca a ina ** 0.0 0.0 0.0 B a a B a a 25.0 10.3 31.9 * Municipali ies wi h B e eau Index (BI) <5; ** No Ae. aegyp i la a ound; ** Ae. aegyp i adul mosqui oes we e eco ded du ing su ey. House Index (HI), Con aine Index (CI). 4. Discussion This s udy ep esen s he i s a chipelago-wide analysis o he Ae. aegyp i b eeding si es in Cabo Ve de, which a e exclusi ely domes ic con aine s. This domes ic mosqui o is one o he mos impo an a h opod ec o s o a bo i uses wo ldwide, namely dengue, Zika, chikungunya, and yellow e e [ 51 ]. Al hough he e has been an ongoing ocus on accine de elopmen o p e en ion o hese diseases, ec o con ol has been he key s a egy o con ol o p e en he ansmission o mosqui o-bo ne a bo i us in ec ions [ 52 ]. In p e ious s udies, Ae. aegyp i popula ions in ec ed wi h DENV-2 and DENV-4 we e ound in Cabo Ve de, wi h high ec o compe ence o ansmi DENV-2 and DENV-3, and o be in ec ed wi h and ansmi chikungunya and yellow e e [53–55]. In Cabo Ve de, ecen en omological da a on he mosqui o species dis ibu ion in he nine inhabi ed islands a e missing, and da a ega ding Ae. aegyp i a e sca ce. Al hough se e al ac o s in luence a b eeding si e’s a ailabili y and mosqui o dis ibu ion, in his s udy, Ae. aegyp i was mos ly ound in wa e d ums used in wa e s o age by he popula ion, which co obo a es p e ious esul s [56–60]. High ec o densi y and suscep ible human popula ion a e key ac o s o a bo i us disease ou b eaks. Be ween hese wo, he i s one is he majo con ibu o and can be es ima ed by Aedes In . J. En i on. Res. Public Heal h 2020,17, 1291 8 o 11 indices, such as CI, HI, and BI [61]. These la al indices p o ide use ul in o ma ion o plan, e alua e, and moni o he e icacy o ec o con ol in e en ions. The BI is he mos used, conside ing he numbe o posi i e con aine s and sea ched houses. We no iced a ia ion in he indices among he municipali ies, wi h some municipali ies showing BI as high as 31.9 and o he s 0. This a ia ion is highly dependen on a con aine ’s a ailabili y, which can be a ec ed by nume ous ac o s, such as seasonali y ( ainy o d y season), local popula ion habi s, cus oms, and adi ions, and local mic oclima e. The i egula i ies in he wa e dis ibu ion o ce people o s o e wa e in con aine s; hus, his ac o plays an impo an ole in he ecology o la al mosqui o habi a s [ 59 ]. Posi i e con aine s ound ou side o dwellings we e associa ed wi h domes ic animals and ag icul u e (no s a is ically es ed), bu u he s udies should be done o app o e o disp o e his claim. In his s udy, he ieldwo k occu ed du ing he d y season and we obse ed ha Ae. aegyp i is ex emely adap ed o domes ic habi a s. I is also impo an o no e ha no co ela ion was ound be ween indoo and ou doo con aine s in his s udy. Thi een municipali ies p esen ed a BI abo e he epidemic isk h eshold [ 40 , 62 ]. Ou esul s sugges ha Ae. aegyp i is well es ablished in all a chipelago islands, and se e al municipali ies in Cabo Ve de a e a isk o a bo i al disease ou b eaks. 5. Conclusions Aedes aegyp i is a majo h ea o public heal h in Cabo Ve de, conside ing he alues o la al indices ound in his s udy associa ed wi h p e ious s udies showing Ae. aegyp i ec o compe ence o diseases egis e ed and no egis e ed in Cabo Ve de [ 54 , 63 ], as well as esis ance o insec icides in he a chipelago [ 25 , 26 ]. Ne e heless, mo e s udies a e c ucial o e alua e his species’ esis ance o mo e insec icides used in he public heal h con ex . We also ecommend implemen a ion o a coun ywide ec o con ol s a egy wi h en i onmen al managemen and modi ica ion, acco ding o gene al in e na ional guidelines [ 31 ]. A p og am o moni o ing Ae. aegyp i, ca ied ou by each municipali y’s heal h delega ion, wi h he suppo o he Minis y o Heal h, is also desi able. Au ho Con ibu ions: Design o he s udy, S.D.V.L. and I.B.F.V.; Collec ions and labo a o y wo k, D.D.S.M., C.M.R.d.S., A.A.L.G., and I.B.F.V.; Da a analyses, I.B.F.V., A.A.L.G., M.J.A., H.C.O., and S.D.V.L. O iginal D a P epa a ion, I.B.F.V., A.A.L.G., M.J.A., H.C.O., and S.D.V.L.; W i ing—Re iew and Edi ing, I.B.F.V., A.A.L.G., M.J.A., H.C.O., and S.D.V.L.; Re ision and Supe ision, A.J.D.P., M.d.L.L.M., and M.J.A. All au ho s ead and app o ed he inal manusc ip . Funding: This esea ch as also he APC we e unded by he Na ional Ins i u e o Public Heal h o Cabo Ve de g an numbe 65.06.01.04.29.01.-Re o ço Do Labo a ó io Nacional De Saúde Pública. Acknowledgmen s: We acknowledge he Na ional Ins i u e o Public Heal h o Cabo Ve de o suppo ing he s udy, and also o all he Heal h acili ies, heal h delega es, con ol ec o agen s, d i e s, and adminis a o s ha p o ided hei suppo du ing he en omological su ey. We a e also g a e ul o he Na ional P og am o ec o con ol. 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