i uses
Re iew
Can Ba s Se e as Rese oi s o A bo i uses?
Anna C. Fag e and Rebekah C. Kading *
Depa men o Mic obiology, Immunology, and Pa hology, Colo ado S a e Uni e si y, Fo Collins, CO 80523,
USA; [email p o ec ed]
*Co espondence: [email p o ec ed]; Tel.: +1-970-491-7833
Recei ed: 1 Feb ua y 2019; Accep ed: 1 Ma ch 2019; Published: 3 Ma ch 2019
Abs ac : Ba s a e known o ha bo and ansmi many eme ging and e-eme ging i uses, many o
which a e ex emely pa hogenic in humans bu do no cause o e pa hology in hei ba ese oi
hos s: henipa i uses (Nipah and Hend a), ilo i uses (Ebola and Ma bu g), and co ona i uses
(SARS-CoV and MERS-CoV). Di ec ansmission cycles a e o en implica ed in hese ou b eaks, wi h
i us shed in ba eces, u ine, and sali a. An addi ional mode o i us ansmission be ween ba s
and humans equi ing u he explo a ion is he sp ead o disease ia a h opod ec o s. Despi e he
sha ed ecological niches ha ba s ill wi h many hema ophagous a h opods (e.g., mosqui oes, icks,
bi ing midges, e c.) known o play a ole in he ansmission o medically impo an a bo i uses,
knowledge su ounding he po en ial o ba s o ac as ese oi s o a bo i uses is limi ed. To his
end, a comp ehensi e li e a u e e iew was unde aken examining he cu en unde s anding
and po en ial o ba s o ac as ese oi s o i uses ansmi ed by blood- eeding a h opods.
Se osu eillance and i al isola ion om ei he ee- anging o cap i e ba s a e desc ibed in
ela ion o ou a bo i al g oups (Bunya i ales,Fla i i idae,Reo i idae,Toga i idae). Fu he , ecological
associa ions be ween ba s and hema ophagous i al ec o s a e cha ac e ized (e.g., ba bloodmeals in
mosqui oes, inges ion o mosqui oes by ba s, e c). Las ly, knowledge gaps ela ed o hema ophagous
ec opa asi es (ba bugs and bed bugs (Cimicidae) and ba lies (Nyc e ibiidae and S eblidae)), in addi ion
o u u e di ec ions o cha ac e iza ion o ba - ec o - i us ela ionships a e desc ibed.
Keywo ds: a bo i uses; ba s; ese oi ; wildli e; zoonoses
1. In oduc ion
Ba s and he i uses hey ha bo ha e been o in e es o he scien i ic communi y due o he unique
associa ion wi h some high consequence human pa hogens in he absence o o e pa hology. Vi ologic
and se ologic epo s in he li e a u e demons a e he exposu e o ba s wo ldwide o a bo i uses
(a h opod-bo ne i uses) o medical and e e ina y impo ance [
1
]. Howe e , he epidemiological
signi icance o hese obse a ions is unclea as o whe he o no ba s a e con ibu ing o he ci cula ion
o a bo i uses.
His o ically, a zoono ic i us ese oi has been conside ed a e eb a e species which de elops a
pe sis en in ec ion in he absence o pa hology o loss o unc ion, while main aining he abili y o
shed he i us (e.g., u ine, eces, sali a) [
2
–
4
]. Haydon e al. ex ended his de ini ion o a ese oi
o include epidemiologically-connec ed popula ions o en i onmen s in which he pa hogen can be
pe manen ly main ained and om which in ec ion is ansmi ed o he de ined a ge popula ion.
The signi icance o he ela i e pa hogenici y o he in ec ious agen o he pu po ed ese oi hos
has been deba ed [
5
]. In he case o ba s as a ese oi species, igo ous ield and expe imen al
e idence now exis o solidi y he ole o he Egyp ian ouse e ba (Rouse us aegyp iacus) as he
ese oi o Ma bu g i us [
6
–
8
]. Conside ing a bo i uses, addi ional c i e ia mus be me in o de o
conside a pa icula e eb a e species a ese oi . Re iewed by Kuno e al., hese c i e ia include
Vi uses 2019,11, 215; doi:10.3390/ 11030215 www.mdpi.com/jou nal/ i uses
Vi uses 2019,11, 215 2 o 27
he pe iodic isola ion o he in ec ious agen om he e eb a e species in he absence o seasonal
ec o ac i i y, and he coincidence o ansmission wi h ec o ac i i y [
9
]. Fu he , he e eb a e
ese oi mus also de elop i emia su icien o allow he hema ophagous a h opod o acqui e
an in ec ious bloodmeal [
10
] in o de o ec o -bo ne ansmission o occu . Ba s ha e long been
suspec ed as ese oi s o a bo i uses [
11
], bu expe imen al da a ha would suppo a ole o ba s as
ese oi hos s o ce ain a bo i uses emain di icul o collec . He e we syn hesize wha in o ma ion
is cu en ly known ega ding he exposu e his o y and pe missi eness o ba s o a bo i us in ec ions,
and iden i y knowledge gaps ega ding hei designa ion as a bo i us ese oi s.
2. Membe s o he O de Bunya i ales
The o de Bunya i ales is di ided in o eigh amilies, ou o which pose h ea s o public heal h
and e e ina y medicine– amilies Nai o i idae,Pe ibunya i idae,Phenui i idae, and Han a i idae [
12
].
While ba s ha e been demons a ed o hos han a i uses, hese i uses do no ely on an a h opod in
hei ansmission cycle and hus will no be discussed [
13
]. Vi uses in o de Bunya i ales ha ha e
been expe imen ally examined in ba s o desc ibed in ield s udies a e desc ied in Table 1.
2.1. Family Nai o i idae, Genus O honai o i us
Membe s o he genus O honai o i us o medical and e e ina y signi icance include C imean
Congo hemo hagic e e i us (CCHFV) and Nai obi sheep disease i us (NSDV) [
12
]. CCHFV is
ansmi ed by icks in gene a Rhipicephalus and Hyalomma [
14
]. While nei he li e i us no nucleic
acid o CCHFV has been de ec ed om ba s, se ologic e idence sugges s pas in ec ion o popula ions
o ba s ac oss a di e se geog aphic ange [15–17]. Fu he , ba s a e o en pa asi ized by bo h so and
ha d icks, which occupy a di e se ange o ecological niches in endemic coun ies [
18
–
20
]. A 2016
se op e alance s udy by Mülle and colleagues examining 16 A ican ba species (n= 1,135) ound
ha he p e alence o an ibodies agains CCHFV was much highe in ca e-dwelling ba s (3.6%–42.9%,
depending on species) han oliage-li ing ba s (0.6%–7.1%) [
15
]. They also sc eened 1,067 se um
samples by RT-PCR, bu all we e nega i e o CCHFV nucleic acid [
15
]. Expe imen al s udies o assess
he abili y o ba s o suppo eplica ion o CCHFV ha e no been published.
2.2. Family Pe ibunya i idae, Genus O hobunya i us
Membe s o he genus O hobunya i us include many i uses o impo ance o human and
e e ina y medicine, including Bunyamwe a i us, Cali o nia encephali is i us, James own Canyon
i us, Kaeng Khoi i us, and La C osse encephali is i us [
12
], bu limi ed e idence exis s ega ding
he exposu e o po en ial in ol emen o ba s in he ci cula ion o i uses in his amily.
Kaeng Khoi i us (KKV) has been isola ed om cimicid bugs (O de : Hemip e a, Family:
Cimicidae) (S ic icimex pa us and Cimex insue us) and om suckling w inkle-lipped ba s
(Tada ida plica a ) in ca es in Thailand, bu was no isola ed om so icks es ed in he same a ea
(O ni hodo us he msi) [
21
]. Addi ionally, KKV has been implica ed in he case o se e al mine wo ke s
who epo ed illness and we e disco e ed o ha e se ocon e ed [
22
], demons a ing spillo e o his
i us o humans in associa ion wi h he ca e en i onmen , and sugges ing ha cimicids may play
a ole in ec o ing i us be ween ba and human hos s. To da e, no expe imen al da a ha e been
gene a ed o add ess his hypo hesis.
Spence and colleagues a emp ed o expe imen ally in ec Jamaican ui ba s (A ibeus jamaicensis)
ia in amuscula injec ion wi h Nepuyo i us (G oup C se og oup), ye no in ec ious i us was
subsequen ly eco e ed om he ba s [
23
]. This is in e es ing conside ing wo s ains o Nepuyo i us
we e isola ed om Jamaican ui ba s (A ibeus jamaicensis) and g ea ui -ea ing ba s (A ibeus li e a us)
in Hondu as, and p o ec i e se a we e ound in Jamaican ui ba s in T inidad. [
24
,
25
]. Ba s o
unde e mined species we e in ol ed in a la ge se osu ey in B azil ha examined an ibodies in
wildli e agains he Gamboa se og oup o hobunya i uses, hough none we e ound o be posi i e [
26
].
Se en and wel e species o T inidadian ba s we e examined o an ibodies by HI agains Ca apa u
Vi uses 2019,11, 215 3 o 27
(G oup C se og oup) and Magua i (Bunyamwe a se og oup) i uses, espec i ely, and we e all ound
o be nega i e [25].
2.3. Family Phenui i idae, Genus Phlebo i us
Vi uses in he genus Phlebo i us ( amily Phenui i idae) o impo ance o human and animal heal h
include Ri Valley e e i us (RVFV) and se e e e e wi h h ombocy openia synd ome i us
(SFTSV) [
12
]. Ba s o he species Miniop e us sch eibe sii (n= 1) and Ep esicus capensis (n= 2) we e
expe imen ally in ec ed wi h RVFV and he M. sch eibe sii ba ’s u ine and li e es ed posi i e o
an igen [
27
]. A ecen s udy by Balkema-Buschmann and colleagues expe imen ally in ec ed Egyp ian
ouse e ba s (Rouse us aegyp iacus) wi h accine s ain MP-12 and eco e ed in ec ious i us om
spleen and li e o some animals [
28
]. Oelo sen & Van de Rys (1999) examined 350 samples om
150 ield-caugh ba s in A ica, ye none we e posi i e o an igen by use o ELISA [
27
]. Kading e al
(2018) de ec ed neu alizing an ibodies agains RVFV in Egyp ian ouse e ba s and li le epaule ed
ui ba s (Epomopho us labia us) in Uganda, a coun y ha has ecen ly expe ienced human cases o
RVFV [
29
,
30
]. Whe he o no ba s se e as a ese oi o RVFV du ing in e epidemic pe iods emains
o be de e mined.
2.4. Unclassi ied Bunya i uses
Bangui i us (BGIV) is an unclassi ied bunya i us and was isola ed om an uniden i ied ba in
he Cen al A ican Republic (CAR) [
31
]. Mojuídos Campos i us (MDCV) is ano he ung ouped
bunya i us isola ed om an uniden i ied ba species [32,33].
Vi uses 2019,11, 215 4 o 27
Table 1. Table desc ibing species wi h published esul s desc ibing i us isola ion, molecula e idence, o se ocon e sion o species in amily Bunya i ales.
Family Vi us Vi us Isola ion/
Molecula E idence Se ologic E idence Re (s)
Nai o i idae, genus
O honai o i us
Ahun i us Myo is mys acinus, Pipis ellus pips ellus [34]
C imean-Congo Hemo hagic Fe e
Vi us (CCHF)
Rouse us aegyp iacus, Coleu a a a, Hipposide os c . ca e ,
Miniop e us in la us, Hipposide os gigas, Eidolon hel um,
Epomops anque i, Hypsigna hus mons osus, Mic op e opus
pusillus, Myonyc e is o qua a, Myo is dasycneme, Myo is
dauben onii, Myo is bly hii, Nyc alus noc ula
Uniden i ied species (F ance)
[15–17]
Gossas (GOSV) Tada ida sp. [35]
Issyk-Kul (IKV)
Nyc alus noc ula,Myo is bly hii,Vespe ilio
se o inus; A gasid icks collec ed om
Vespe ilio pips ellus, V. se o inus,
Nyac ulus noc ula, and Myo is bly hii
[35,36]
Kasoke o (KKOV) Rouse us aegyp iacus [35,37,38]
Ke e ah (KTRV)
Tick la ae (A gus pusillus) collec ed om
Sco ophilus emmincki [39]
Leopa ds Hill (LPHV) Hipposide os gigas [35,40]
Uzun Agach (UAV) Myo is bly hii [41]
Yogue (YOGV) Rouse us aegyp iacus [32,35,38]
Pe ibunya i idae,
genus
O hobunya i us
Bunyamwe a i us (BUNV)
Myo is luci ugus, Eidolon hel um, Rouse us
aegyp iacus, Mops condylu us Eidolon hel um, Rouse us aegyp iacus, Mops condylu us [42–46]
Bimi i i us (BIMV)
Anou a geo oyi, Ca ollia pe spicilla a, Phyllos omus has a us,
P e ono us pa nellii, Na alus umidi os us [25]
Cali o nia encephali is i us (CEV) Myo is keenii [47]
Ca ú i us (CATUV) Molossus obscu us
Anou a geo oyi, Ca ollia pe spicilla a, Phyllos omus has a us
[25]
Guama i us (GMAV) Uniden i ied ba Anou a geo oyi, Phyllos omus has a us, A ibeus li e a us [25,32]
Kaeng Khoi Vi us (KKV) Chae ephon plica a Taphazous heobaldi, Chae ephon plica a [21,22,48,49]
Manzanilla i us (MANV) Molossus a e [25]
Nepuyo i us (NEPV) A ibeus jamaicensis,A ibeus li e a us A ibeus jamaicensis, Phyllos omus has a us [24,25]
O iboca i us (ORIV) A ibeus li e a us [25]
Res an i us (RESV) A ibeus li e a us, A ibeus jamaicensis, Ca ollia pe spicilla a [25]
Vi uses 2019,11, 215 5 o 27
Table 1. Con .
Family Vi us Vi us Isola ion/
Molecula E idence Se ologic E idence Re (s)
Phenui i idae,
genus Phlebo i us
Malsoo i us Rouse us leschenaul ia [50]
Ri Valley e e i us (RVFV)
Miniop e us sch eibe sii, Ep esicus capensis,
Mic op e opus pusillus, Hipposide os abae,
Hipposide os ca e , Epomops anque i,
Glauconyc e is a gen a a
Rouse us aegyp iacus, Epomopho us labia us [1,27,29,51–53]
Toscana i us (TOSV) Pipis ellus kuhli [54,55]
Unclassi ied Bangui i us (BGIV) Uniden i ied ba [31]
Mojuídos Campos i us (MDCV) Uniden i ied ba [32,33]
Vi uses 2019,11, 215 6 o 27
3. Membe s o he Family Fla i i idae
The amily Fla i i idae includes many high-consequence eme ging a bo i uses, including Zika
i us (ZIKAV), yellow e e i us (YFV), and Dengue i us (DENV). Fla i i uses associa ed wi h
ba s ha do no appea o u ilize an a h opod ec o (“no-known ec o la i i uses”) ha e been
e iewed elsewhe e [
56
]. Vi uses in amily Fla i i idae ha ha e been expe imen ally examined in ba s
o desc ibed in ield s udies a e desc ied in Table 2.
3.1. Dengue Vi us
In e es ingly, despi e DENV isola ions om A ibeus spp. ba s in he wild, expe imen al in ec ions
o g ea ui -ea ing ba s (A. in e medius) wi h DENV-2 and Jamaican ui ba s wi h DENV se o ypes
1 and 4 esul ed in low le els o i emia, low a es o se ocon e sion, and lack o de ec ion o i al
RNA in he o gans ia RT-PCR, indica ing ha ba s may no ac as a sui able ese oi hos
[57–59]
.
Expe imen al in ec ion o he Indian lying ox (P e opus gigan eus) esul ed in no i emia o clinical
signs, bu in ace eb al inocula ion o li le b own ba s (Myo is luci ugus) esul ed in i i abili y,
pa alysis, and dea h [60,61].
DENV nucleic acid and an i-DENV an ibodies ha e been de ec ed in Mexican ba s on he Gul and
Paci ic coas , and nucleic acid has been de ec ed in he li e and/o se a o wild-caugh ba s in F ench
Guiana [
62
,
63
]. An i-DENV an ibodies ha e been de ec ed in mul iple ba species in Uganda [
29
].
Howe e , a su ey in Cen al and Sou he n Mexico analyzing 240 indi iduals ep esen ing 19 ba
species by RT-PCR esul ed in no de ec ion o i al nucleic acid [
64
]. A 2017 s udy by Vicen e-San os and
colleagues examined 12 ba species om Cos a Rica and ound a cumula i e se op e alence o 21.2%
(51/241) by PRNT and a p e alence o 8.8% (28/318) in o gans es ed by RT- PCR [
65
]. No in ec ious
i us was isola ed and i al loads we e conside ed oo low o he ba s o unc ion as ampli ying
hos s. Ra he , Vicen e-San os and colleagues su mised a spillo e e en om humans o ba s, wi h ba s
unc ioning as a dead-end hos [
65
]. The se um o Jamaican ui ba s (A ibeus jamaicensis) and G ea
ui -ea ing ba s (A. li e a us) om G enada (n= 50) we e also es ed o an ibodies agains DENV
1, 2, 3, and 4, and none we e se oposi i e [
66
]. While ield e idence suppo s he exposu e o ba s
o DENV in mul iple geog aphic a eas, expe imen al in ec ions conduc ed o da e a e consis en in
ha ba s a e no likely o suppo DENV eplica ion and ci cula ion o le els high enough o in ec
blood- eeding mosqui oes.
3.2. Japanese Encephali is Vi us
Mul iple s udies conduc ed expe imen al in ec ions o insec i o ous ba s wi h Japanese
encephali is i us (JBEV) and ound ha ba s we e suscep ible o in ec ion wi h his i us. Th ee species
o ba s (big b own ba s (Ep esicus uscus), li le b own ba s (Myo is luci igus) and Eas e n pipis elles
(Pipis ellus sub la us)) we e inocula ed wi h JBEV in he labo a o y and main ained in ec ion while held
unde simula ed hibe na ion condi ions. Ba s in ec ed p io o hibe na ion we e i emic upon a ousing
om hibe na ion, wi h ci cula ing i us de ec able as long as 112 days a e he ini ial in ec ion [
67
].
Big b own ba s also demons a ed ecu en i emia in he absence o clinical signs in a subsequen
s udy [
68
]. Impo an ly, esea che s demons a ed a mosqui o-ba -mosqui o ansmission cycle and
pos ula ed his may be an o e win e ing mechanism o JBEV since mosqui oes did success ully
ansmi JBEV o ba s a low empe a u es [
67
]. Eas e n pipis elles also became in ec ed wi h JBEV
a e consump ion o in ec ed mosqui oes, demons a ing ha ba s could be in ec ed o ally as well as
h ough a mosqui o bi e [
67
]. No demons able pa hologic e ec s no ed du ing in ec ion o h ee ba
species [big b own ba s (Ep esicus uscus), li le b own ba s (Myo is luci igus) and Mexican ee- ailed ba s
(Tada ida b asiliensie mexicana) wi h a ious s ains o JBEV o S . Louis encephali is i us (SLEV) [
69
].
No pa hology no i emia was app ecia ed when pipis elles (Pipis ellus ab amus) we e in ec ed wi h
JBEV [
70
]. While expe imen al da a demons a ed ha some ba species can sus ain JBEV in ec ions
Vi uses 2019,11, 215 7 o 27
and suppo mosqui o-bo ne ansmission o his i us, he epidemiological signi icance o hese
obse a ions in he ield emains unclea .
JBEV has been isola ed om wild-caugh ba s in Taiwan (Miniop e us uliginosus and Hipposide os
a mige e asensis [
32
,
71
], China (Rouse us leschenaul ia and Mu ina au a a [
72
,
73
], Japan (Miniop e us
sch eibe si uliginosus and Rhinolophus co nu us co nu us [
74
]. An ibodies agains JBEV ha e been
de ec ed in wild-caugh ba s in Indonesia (unspeci ied species) [
75
], China (Rouse us leschenaul ia,
Cynop e us sphinx, Taphozous melanopogon, Miniop e us sch eibe sii, Pipis ellus ab amus, Rhinolophus
mac o is and Miniop e us uliginosus [
76
,
77
], Aus alia (P e opus scapula us and P e opus gouldi) [
78
],
Taiwan (unspeci ied species) [
79
], India (P e opus gigan eus, Hipposide os pomona, Hipposide os speo is,
Hipposide os bicolo , Hipposide os cine aceus, Megade ma ly a, Cynop e us sphynx, and Rhinolophus
ouxi) [
80
–
82
], and Japan (Miniop e us sch eibe si uliginosus, Rhinolophus e um equinum Nippon,
Vespe ilio supe ans, Myo is mac odac ylus, Rhinolophus co nu us co nu us, Pipis ellus ab amus, Myo is
mys acinus, Pleco us au i us sac imon is, and Mu ina leucogas e hilgendo i) [
83
]. Mul iple isola ions o
JBEV om loca ions whe e he i us is endemic, in addi ion o he ac ha gene ic cha ac e iza ion o
isola es has suppo ed hei simila i y o s ains iden i ied om human and mosqui o isola es, suppo
he ole o ba s in ongoing ci cula ion o JBEV [84].
3.3. S . Louis Encephali is Vi us
Ano he medically-impo an la i i us wi h bo h ield-ob ained in o ma ion and
in i o
expe imen al inocula ion is SLEV. A 1983 s udy by He bold and colleagues demons a ed ha 9% o
wild-caugh Ep esicus uscus and Myo is luci ugus (n= 390) in Ohio possessed neu alizing an ibodies
o SLEV [
85
]. O he se osu eillance e o s in No h Ame ica and G enada ocused on de ec ion o
SLEV in ee- anging ba popula ions ha e esul ed in la gely nega i e indings [
66
,
86
]. Following
expe imen al in ec ion, i emia and ansplacen al ansmission (albei in equen ) was app ecia ed
in Mexican ee- ailed ba s (Tada ida b asiliensis) [
69
,
87
]. The i emia in hese ba s eached 4 log uni s,
likely oo low a i e o acili a e ansmission o a blood- eeding mosqui o [
10
]. Upon inocula ion,
li le b own ba s (Myo is luci ugus) appea o be esis an o only sligh ly suscep ible o SLEV [
69
].
He bold and colleagues (1983) demons a ed ha inocula ion o Ep esicus uscus wi h SLEV esul s
in in ec ion and i us was main ained h oughou hibe na ion (70 days), wi h i emia de eloping
ou days ollowing a ousal (105 days pos -in ec ion) [
85
]. Low le els o i emia upon expe imen al
inocula ion in conjunc ion wi h low se op e alence da a indica e his i us likely does no u ilize ba s
as a ese oi hos in na u e.
3.4. Wes Nile Vi us
To da e, biosu eillance es ing o ba s in Cen al Ame ica o WNV ha e u ned up nega i e
esul s. G enadian A ibeus jamaicensis and A ibeus li e a us (n= 50) ba s we e nega i e o WNV
neu alizing an ibodies by PRNT [
66
], 14 T inidadian ba species (n= 384) we e nega i e by ELISA
o WNV an ibodies [
88
], and 16 Mexican ba species (n= 146) es ed o WNV RNA by RT-PCR we e
nega i e [
89
]. In No h Ame ica, esul s ha e been nega i e o indica i e o low le els o ci cula ion
in ba popula ions es ed. Tissues om 312 ield-collec ed ba s ep esen ing se en species in Illinois
es ed by RT-PCR we e all nega i e o WNV, and he same s udy epo ed one big b own ba (Ep esicus
uscus) wi h neu alizing an ibodies (n= 97) [
90
]. A ield su ey aking place in New Je sey and
New Yo k epo ed one big b own ba and one no he n long-ea ed ba (Myo is sep en ionalis) wi h
neu alizing an ibodies o WNV (n= 83) [
86
]. In ano he ield s udy, only wo o 149 ee- ailed ba s
(Tada ida b asiliensis) possessed neu alizing an ibodies agains WNV [
91
]. In Uganda, Kading e al.
(2018) de ec ed neu alizing an ibodies o WNV in 2/8 A ican s aw-colo ed lying oxes (Eidolon
hel um), and 3/44 li le epaule ed ui ba s (Epomopho us labia us) [29].
Simpson and O’Sulli an (1968) demons a ed expe imen al inocula ion o A ican s aw-colo ed
lying oxes did no esul in i emia hough wo o h ee ba s de eloped neu alizing an ibody.
In he same s udy, wo o h ee Egyp ian ouse e ba s we e in ec ed bu only ace i emia was
Vi uses 2019,11, 215 8 o 27
de ec ed and se ocon e sion was no app ecia ed [
43
]. Expe imen al inocula ion o ee- ailed ba s
(Tada ida b asiliensis) did no esul in i emia, and in ec ion o big b own ba s esul ed in low i e s
(10–180 PFU/mL) [91], no capable o suppo ing ansmission o eeding mosqui oes [10].
3.5. Yellow Fe e Vi us
A emp s o expe imen ally in ec ampi e ba s (Desmodus o undus) and black mas i ba s
(Molossus u us) by mosqui o bi e (Aedes aegyp i) we e unsuccess ul [
11
]. Expe imen al inocula ion o
mul iple ba species (Eumops pe o is, Ca ollia pe spicilla a, Phyllos omus has a us and ba s in he genus
Mollosus) we e simila ly unsuccess ul [
92
]. S ill, Kading e al. de ec ed a signi ican neu alizing
an ibody i e agains YFV in one Egyp ian ouse e ba in Uganda in 2012, indica ing ba s a e exposed
o his i us in na u e [29]. Uganda has expe ienced ou b eaks o YFV in ecen yea s [93].
3.6. Zika Vi us
While mul iple A ican ba species (Eidolon hel um, Rouse us aegyp iacus, and Rouse us angolensis)
demons a ed i emia ollowing inocula ion wi h ZIKAV, Mops condylu us did no become i emic,
al hough did con ain low i us i e s in he kidney [
43
,
44
]. Expe imen ally-in ec ed li le b own ba s
we e suscep ible o he ZIKAV by he in ape i oneal, in ade mal, in ace eb al and in a ec al ou es
o exposu e, bu no suscep ible in anasally [
94
]. Howe e , i is unclea how ZIKAV could ci cula e
in ba popula ions. Kading e al. (2018) did no de ec neu alizing an ibodies o ZIKAV among
292 Ugandan ba s sc eened. Fla i i us in ec ions o ba s wi h an emphasis on he po en ial ole in Zika
i us ecology has been e iewed elsewhe e [95].
3.7. O he Membe s in Family Fla i i idae and Pan-Fla i i us Su eillance
Fla i i us se ology has been his o ically challenging due o he c oss- eac i i y o i al epi opes o
ci cula ing an ibodies [
96
]. The e o e, he esul s o se ologic su eillance s udies mus be in e p e ed
cau iously [
29
,
97
]. Fu he , mul iple me hods exis o an ibody de ec ion (e.g., HI, PRNT, ELISA), and
he biological signi icance o neu alizing s. non-neu alizing an ibodies mus be aken in o accoun .
In 2010, he se um o 140 Mexican ba s om h ee species (Glossophaga so icina, A ibeus jamaicensis,
and A ibeus li e a us) was assayed by PRNT using WNV, SLEV, and DENV 1–4, and 26 we e posi i e
o la i i us-speci ic an ibodies (19%). None o he i e s exceeded 80, and all samples we e also
nega i e when es ed o la i i us nucleic acid by RT-PCR [
97
]. In a 2015 se osu ey, eigh ba s (2.6%)
displayed non-speci ic hemagglu ina ion-inhibi ion (HI) esul s indica ing c oss- eac i i y o an ibodies
agains an unde e mined la i i us [
88
]. Kading and colleagues pe o med a se osu eillance s udy in
Ugandan ba s and iden i ied 13.6% (85/626) had non-speci ic la i i us an ibodies by plaque educ ion
neu aliza ion assay (Chae ephon pumilus,Hipposide os ube ,Mops condylu us,Nyc e is mac o us,Eidolon
hel um,Epomopho us mino , and Rouse us aegyp iacus) [
29
]. S ill, esul s gene ally suppo ed he
widesp ead exposu e o ba s in Uganda o la i i uses [29].
In 2018, So omayo -Bonilla and colleagues epo ed ha li e and spleen samples om 12 Mexican
ba species es ed nega i e using pan- la i i us NS5 p ime s [
98
]. A ecen s udy in B azil sugges ed
a lack o a bo i al ci cula ion in ba popula ions, as 103 indi iduals om 9 species we e es ed o
molecula and se ologic e idence o alpha i us and la i i us in ec ion and all we e nega i e [
99
].
Resul s o expe imen al in ec ion o Egyp ian ouse e ba s wi h WNV and o Angolan ee- ailed ba s
(Mops condylu us) wi h N aya i us esul ed in e y low le els o i emia, while in ec ion o A ican
s aw-colo ed ui ba s wi h N aya i us esul ed in nei he pa hology no de ec able i emia [43].
Vi uses 2019,11, 215 9 o 27
Table 2.
Table desc ibing species wi h published esul s desc ibing i us isola ion, molecula e idence, o se ocon e sion o species in genus Fla i i us ( amily
Fla i i idae).
Vi us Vi us Isola ion/
Molecula E idence Se ologic E idence Re (s)
Banzi i us (BANV) Eidolon hel um, Epomopho us anu as, Miniop e us sch eibe sii, Tada ida pumila,
Mops condylu us [44]
Bussuqua a i us (BSQV) A ibeus jamaicensis [66]
Cen al Eu opean
encephali is i us Uniden i ied ba [1]
Dengue i us (DENV)
Desmodus o undus, A ibeus jamaicensis, Ca ollia
b e icauda, Myo is nig icans, Glossophaga so icina,
A ibeus li e a us, A ibeus plani os is, Ca ollia
pe spicilla a, Myo is luci ugus, A ibeus in e medius,
Molossus sinaloae, Molossus p e iosus, Rhogeessa
bickhami, Molossus u us, Eumops glaucinus
Myo is nig icans, P e ono us pa nellii, Na alus s amineus, A ibejus jamaicensis,
A ibeus spp., U ode ma spp., Molossus spp., Chae ephon pumilus, Mops
condylu us, Anou a geo oyi, A ibeus cine eus, A ibeus li e a us, Ca ollia
pe spicilla a, Molossus a e , Molossus molossus, Phyllos omus has a us, P e ono us
da yi, P e ono us pa nellii, S u ni a spp., P e opus gouldii, P e opus gigan eus,
Glossophaga so icina, A ibeus in e medius, Molossus sinaloae, Rhogeessa io,
Molossus p e iosus, Balan iop e yx plica a, Molossus u us, Rhogeessa bickhami,
Epomopho us labia us
[25,29,57,59–63,65,
78,97,100–102]
Ilheus i us (ILHV) Anou a geo oyi, Phyllos omus has a us, P e ono us da yi, A ibeus jamaicensis,
A ibeus li e a us, Desmodus o undus, Molossus a e [25]
Japanese encephali is i us
(JBEV)
Mu ina au a a,Rouse us leschenaul ia, Ep esicus
uscus, Myo is luci ugus, Pipis ellus sub la us,
Pipis ellus ab amus, Tada ida b asiliensis,
Hipposide os a mige e asensis, Miniop e us
uliginosus, Rhinolophus co nu us, Miniop e us
sch eibe sii, Rhinolophus co nu us, P e opus alec o,
Cynop e us sphinx
Rouse us leschenaul ia,Taphozous melanopogon,Miniop e us uliginosus, Myo is
mac odac ylus,Miniop e us sh eibe sii, Ep esicus uscus, P e opus alec o, P e opus
goldii, P e opus scapula us, Gene a Hipposide os and Miniop e us, P e opus
gigan eus, Mu ina leucogas e , Megade ma ly a, Cynop e us sphynx, Myo is
mys acinus, Pipis ellus ab amus, Pleco us au i us, Rhinolophus e um-equinum,
Vespe ilio supe ans, Hipposide os a mige , Hipposide os pomona, Hipposide os
speo is, Hipposide os bicolo , Hipposide os cine aceus, Rhinolophus co nu us,
Rhinolophus ouxi, Rouse us leschenaul ia, Miniop e us sch eibe sii, Pipis ellus
ab amus, Rhinolophus mac o us, unde e mined species
[32,67,69–83,87,
103–106]
Jug a i us (JUGV) Cynop e us b achyo is [32]
Kyasanu o es disease
i us (KFDV) Rhinolophus ouxi,Cynop e us sphinx
Rouse us leschenaul ii, Cynop e us sphinx, P e opus gigan eus, Rhinolophus ouxi
[107–109]
Mu ay Valley encephali is
i us (MVEV) Ep esicus pumilus, P e opus gouldi, P e opus scapula us, P e opus spp. [78,102,110,111]
N aya i us (NTAV) Eidolon hel um, Rouse us sp. [43,46]
Vi uses 2019,11, 215 16 o 27
depopula ion e o s in esponse o i al ou b eaks esul ed in inc eased i al spillo e , and a e no a
iable means o disease con ol and ha e e en esul ed in highe i us in ec ion a es in he ba species
when colonies epopula ed om neighbo ing oos s [
203
]. Fu he wo k should encompass di ec ed
ield su eillance complemen ed by bo h
in i o
and
in i o
app oaches, wi h ield su eillance
e o s ocused on op imiza ion o non-le hal and non-in asi e sampling [
204
–
207
]. When possible,
longi udinal sampling o iden i iable animals h ough use o ma king o agging allows o moni o ing
o se ocon e sion and i emia pe sis ence, p o iding a chance o be e cha ac e ize ansmission
pe iodici y and seasonal changes in i emia p o iles.
8. Conclusions
To uly elucida e he ole o ba s as ese oi s o a bo i uses, ield su eillance s udies
documen ing na u al in ec ion and ansmission dynamics among ec o and e eb a e species
mus be supplemen ed wi h expe imen al in ec ions o cha ac e ize i emia p o iles and in ec iousness
o ec o s, i us-induced pa hology, and immune kine ics ollowing in ec ion. Wi h ba s, hese asks
a e no i ial, and ca y signi ican challenges in bo h he ield and he lab. These challenges a e
e idenced by he ew a bo i uses o which he e a e subs an ial ield and labo a o y da a in ol ing
he in ec ion o ba s. While many s udies ha e p esen ed se ologic da a indica i e o pas exposu e
o ee- anging ba s o a bo i uses o medical and e e ina y impo ance, hese s udies should be
ollowed up wi h labo a o y assessmen s o ese oi hos compe ence o shed ligh on he ue
epidemiological signi icance o he ield da a. Fu he , he de ec ion o i al nucleic acid in ee- anging
ba s does no necessa ily implica e he species as an a bo i al ese oi . Ra he , eco e y and isola ion
o li e i us a biologically ele an i e s, and demons a ing he pe sis ence o he pa hogen in na u e
among connec ed popula ions o a po en ial ese oi species is mo e de ini i e. Un o una ely, ew
es ablished ba colonies exis o use
in i o
i al pa hogenesis s udies, limi ing he achie abili y o
hese s udies.
To ul ill he e eb a e ese oi hos pa adigm,
in i o
in ec ions mus suppo indings in he
ield. The isola ion o Ma bu g i us om Egyp ian ouse e ba s in Uganda in addi ion o expe imen al
in ec ions demons a ing i emia and shedding in he absence o o e pa hology suppo he ole
o his ba species as he ese oi o Ma bu g i us [
6
,
7
,
208
]. Fo a bo i uses, he combina ion
o ield wo k and
in i o
pa hogenesis s udies a e lacking. S ill, se e al examples ha e eme ged
om his e iew ha poin o ba s as po en ially compe en ampli ying hos s o a bo i uses. Kaeng
Khoi i us was isola ed om bo h ba s and cimicid bugs in Thailand, and was also shown o be he
causa i e agen behind sick mine wo ke s [
21
]. Some ba species did de elop a i emia a a le el
ha would be in ec ious o mosqui oes when inocula ed expe imen ally wi h CHIKV, and ba s ha e
been ound exposed o CHIKV du ing ield in es iga ions [
66
,
143
]. Expe imen al e idence suppo ing
ansmission o RRV om P e opus poliocephalus o ecipien mosqui oes in addi ion o iden i ica ion o
RRV-se oposi i e ba s apped in Aus alia and Indonesia highligh s he need o u he in es iga ion
in o he ole o ba s in he ecology o his disease [
75
,
149
,
157
]. A mosqui o-ba -mosqui o ansmission
cycle was es ablished in he lab o JBEV [
67
]. Se ological e idence om he ield documen ing ba
exposu e o JBEV, he sus ained i emia in ba s du ing hibe na ion, and demons a ion o mosqui o
ansmission om and o ba s in he labo a o y collec i ely demons a e he capabili y o ba s o
unc ion as ese oi hos s o his i us. Ci cums an ial e idence om ield-sampled mosqui oes and
ba s suppo s he cycling o Babanki i us among ba s and mosqui oes in Uganda [
29
], bu expe imen al
da a a e s ill lacking. Fo RVFV, ba s e alua ed in he lab ha e suppo ed i us eplica ion, and mul iple
popula ions o ba s in he ield ha e been ound wi h neu alizing an ibodies o na u al in ec ion wi h
RVFV [
1
,
28
,
29
]. Addi ional s udies a e wa an ed on hese and o he i uses o which addi ional ield
o expe imen al da a a e needed o suppo he ole o ba s as a possible ese oi .
Au ho Con ibu ions:
A.C.F. and R.C.K. designed he s udy. A.C.F. and R.C.K. analyzed he da a. A.C.F. and
R.C.K. p epa ed he manusc ip .
Vi uses 2019,11, 215 17 o 27
Funding: This esea ch ecei ed no ex e nal unding.
Con lic s o In e es : The au ho s decla e no con lic o in e es .
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