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. We acknowledge Cl
á
udia Sami a Va ela o labo a o y wo k suppo , K
á
ia Eu iza Jesus Pe ei a
Ba alha o s a is ical analysis suppo , and Jailson Jos
é
Ta a es Va ela, om he Na ional Ins i u e o Te i o ial
Managemen , o he map d awing.
Con lic s o In e es : The au ho s decla e no con lic s o in e es .
Re e ences
1. Wea e , S.C.; Reisen, W.K. P esen and u u e a bo i al h ea s. An i i . Res. 2010,85, 328–345. [C ossRe ]
2.
Sha ma, A.; Lal, S.K. Zika i us: T ansmission, de ec ion, con ol, and p e en ion. F on . Mic obiol.
2017
,
8, 110. [C ossRe ]
3.
Wilde -Smi h, A.; Guble , D.J.; Wea e , S.C.; Mona h, T.P.; Heymann, D.L.; Sco , T.W. Epidemic a bo i al
diseases: P io i ies o esea ch and public heal h. Lance In ec . Dis. 2017,17, e101–e106. [C ossRe ]
4.
B ady, O.J.; Ge hing, P.W.; Bha , S.; Messina, J.P.; B owns ein, J.S.; Hoen, A.G.; Moyes, C.L.; Fa low, A.W.;
Sco , W.T.; Hay, S.I. Re ining he global spa ial limi s o dengue i us ansmission by e idence-based
consensus. PLoS Negl. T op. Dis. 2012,6, e1760. [C ossRe ] [PubMed]
In . J. En i on. Res. Public Heal h 2020,17, 1291 9 o 11
5.
Le a, S.; Beyene, T.J.; De Cle cq, E.M.; Amenu, K.; K aeme , M.U.; Re ie, C.W. Global isk mapping o majo
diseases ansmi ed by Aedes aegyp i and Aedes albopic us.In . J. In ec . Dis.
2018
,67, 25–35. [C ossRe ]
[PubMed]
6.
Paix
ã
o, E.S.; Teixei a, M.G.; Rod igues, L.C. Zika, Chikungunya and dengue: The causes and h ea s o new
and e-eme ging a bo i al diseases. BMJ Glob. Heal h 2018,3(Suppl. 1), e000530.
7.
Glo ia-So ia, A.; Ayala, D.; Bheeca y, A.; Calde on-A guedas, O.; Chadee, D.D.; Chiappe o, M.; Coe zee, M.;
Elahee, K.B.; Fe nandez-Salas, I.; Kamal, H.A.; e al. Global gene ic di e si y o Aedes aegyp i. Mol. Ecol.
2016,25, 5377–5395. [C ossRe ] [PubMed]
8.
B aga, I.A.; Valle, D. Aedes aegyp i: Inse icidas, mecanismos de aç
ã
o e esis
ê
ncia. Epidemiol. Se . Sa
ú
de
2007
,
16, 279–293. [C ossRe ]
9.
Maciel-de-F ei as, R.; Ma ques, W.A.; Pe es, R.C.; Cunha, S.P.; Lou enço-de-Oli ei a, R. Va ia ion in Aedes
aegyp i (Dip e a: Culicidae) con aine p oduc i i y in a slum and a subu ban dis ic o Rio de Janei o du ing
d y and we seasons. Memó ias Ins . Oswaldo C uz 2007,102, 489–496. [C ossRe ]
10.
And ew, J.; Ba , A. Mo phology and mo phome y o Aedes aegyp i adul mosqui o. Annu. Re . Res. Biol.
2013,3, 52–69.
11.
Wo ld Heal h O ganiza ion. Dengue Fe e in Cape Ve de; upda e 1; WHO: Gene a, Swi ze land, 2009; A ailable
online: h p://www.who.in /cs /don/2009_11_18/en/index.h ml (accessed on 3 June 2019).
12.
Wo ld Heal h O ganiza ion. Zika Vi us In ec ion—Cape Ve de; WHO: Gene a, Swi ze land, 2015; A ailable
online: h p://www.who.in /cs /don/21-decembe -2015-zika-cape- e de/en/(accessed on 4 June 2019).
13.
Lou enço, J.; de Lou des Mon ei o, M.; Valdez, T.; Rod igues, J.M.; Pybus, O.; Fa ia, N.R. Zika i us ou b eak
in Cabo Ve de Islands, Wes A ica: Ea ly epidemiological indings. bioRxi 2017, 198952. [C ossRe ]
14. Lobban, R.A. Cape Ve de: C ioulo Colony o Independen Na ion; Rou ledge: Abingdon-on-Thames, UK, 2018.
15.
Aagaa d-Hansen, J.; Nombela, N.; Al a , J. Popula ion mo emen : A key ac o in he epidemiology o
neglec ed opical diseases. T op. Med. In . Heal h 2010,15, 1281–1288. [C ossRe ] [PubMed]
16.
Gi heko, A.K.; Lindsay, S.W.; Con alonie i, U.E.; Pa z, J.A. Clima e change and ec o -bo ne diseases:
A egional analysis. Bull. Wo ld Heal h O gan. 2000,78, 1136–1147. [PubMed]
17.
McMichael, A.J.; Wood u , R.E.; Hales, S. Clima e change and human heal h: P esen and u u e isks. Lance
2006,367, 859–869. [C ossRe ]
18.
Gould, E.; Pe e sson, J.; Higgs, S.; Cha el, R.; de Lamballe ie, X. Eme ging a bo i uses: Why oday?
One Heal h 2017,4, 1–13. [C ossRe ]
19.
Ribei o, H.; Ramos, H.D.C.; Capela, R.A.; Pi es, C.A. Os mosqui os de Capo Ve de (Dip e a: Culicidae).
Sis ema ica, dis ibuiç
ã
o, bioecologia e impo
â
ncia m
é
dica. Jun a In es ig. Cien . Ul ama Es ud. Ens.
Do . Lisboa 1980,135, 141.
20.
Cambou nac, F.J.C.; Oli ei a, M.C.; Co eia, A.; Cou inho, M.A.; Tou inho, J.; Soa es, B. Culex (Lu zia) ig ipes
(G andp é); mais uma espécie no a pa a Cabo Ve de. An. do Ins . de Hig. e Med. T op. 1984,10, 41–46.
21.
Al es, J.; Gomes, B.; Rod igues, R.; Sil a, J.; A ez, A.P.; Pin o, J.; Sousa, C.A. Mosqui o auna on he Cabo
Ve de Islands (Wes A ica): An upda e on species dis ibu ion and a new inding. J. Vec o Ecol.
2010
,
35, 307–312. [C ossRe ]
22.
Al es, J.; Pina, A.D.; Diallo, M.; Dia, I. Fi s epo o Culex (Culex) i aenio hynchus Giles, 1901 (Dip e a:
Culicidae) in he Cabo Ve de Islands. Zool. Cabo e diana 2014,5, 4–19.
23.
Salguei o, P.; Se ano, C.; Gomes, B.; Al es, J.; Sousa, C.A.; Abecasis, A.; Pin o, J. Phylogeog aphy and
in asion his o y o Aedes aegyp i, he Dengue and Zika mosqui o ec o in Cape Ve de islands (Wes A ica).
E ol. Appl. 2019,12, 1797–1811. [C ossRe ]
24.
Minis y o Heal h Cape Ve de; WHO; Uni e si y o Cali o nia. Elimina ing Mala ia: Case S udy 2. Mo ing
Towa ds Sus ainable Elimina ion in Cape Ve de; WHO: Gene a, Swi ze land, 2012. A ailable online: h p:
//www.who.in /mala ia/publica ions/a oz/9789241504386/en/(accessed on 1 No embe 2019).
25.
Dia, I.; Diagne, C.T.; Ba, Y.; Diallo, D.; Kona e, L.; Diallo, M. Insec icide suscep ibili y o Aedes aegyp i
popula ions om Senegal and Cabo Ve de A chipelago. Pa asi Vec o s 2012,5, 238. [C ossRe ] [PubMed]
26.
Rocha, H.D.R.; Pai a, M.H.S.; Sil a, N.M.; de A a
ú
jo, A.P.; da Mou a, A.J.F.; G
ó
mez, L.F.; Ay es, C.F.J.; de Melo
San os, M.A.V. Suscep ibili y p o ile o Aedes aegyp i om San iago Island, Cabo Ve de, o insec icides.
Ac a T op. 2015,152, 66–73. [C ossRe ] [PubMed]
27.
Conno , M.E.; Mon oe, W.M. S egomyia indices and hei alue in Yellow Fe e con ol. Am. J. T op. Med. Hyg.
1923,3, 9–19. [C ossRe ]