RESEARCH Open Access
P e alence o hea wo m in dogs and ca s
o Mad id, Spain
José Albe o Mon oya-Alonso
1
, Rod igo Mo chón
2
, Yaiza Falcón-Co dón
1
, So aya Falcón-Co dón
1
,
Fe nando Simón
2
and Elena Ca e ón
1*
Abs ac
Backg ound: Di o ila ia immi is causes hea wo m disease, a ch onic and po en ially a al ca diopulmona y disease
which mainly a ec s dogs and ca s. I is p esen in mos o Spain, due o a ou able clima ic ac o s. Mad id, loca ed
in he cen e o he Ibe ian Peninsula, is he mos highly popula ed ci y in he coun y. The e is a lack o cu en
da a on canine hea wo m and he e a e no published epidemiological da a ega ding eline hea wo m in his
egion, he e o e he aim o his s udy was o assess he p e alence and cu en dis ibu ion o canine and eline
di o ila iosis in hep o inceo Mad id.
Me hods: Se um samples om 1716 dogs and 531 ca s, om animals li ing in he me opoli an a ea o Mad id
and adjacen a eas, we e s udied. All he samples, ei he om ca s and dogs, we e es ed o ci cula ing D. immi is
an igens using a comme cial immunoch oma og aphic es ki . Fu he mo e, o es ablish he se op e alence o
hea wo m in ec ion in ca s, se ological echniques o an i-D. immi is and an i-Wolbachia an ibody de ec ion
we e used.
Resul s: P e alence o D. immi is in he canine popula ion o Mad id was 3%, showing an inc ease in compa ison
o p e ious da a. The p esence o hea wo m in he ci y cen e could be in luenced by he p esence o U ban
Hea Islands, while he posi i e dogs om me opoli an and adjacen a eas we e mainly loca ed unde he in luence
o i e s. Rega ding ca s, 0.2% we e posi i e o he an igens es and 7.3% we e se oposi i e o bo h an i-D. immi is and
Wolbachia su ace p o ein an ibodies, which demons a e he p esence o eline hea wo m in Mad id. Se oposi i e
ca s we e p esen in he same a eas whe e posi i e dogs we e ound. Indoo /ou doo ca s showed he highes
se op e alence whe eas he lowes co esponded o indoo ca s, demons a ing ha p ophylac ic ea men s
should be ca ied ou ega dless o li es yle. In ec ion was ound in 2.2% o dogs and 6.7% o he ca s < 1 yea -
old, which indica es ha ea ly p e en i e campaigns in puppies and ki ens should be implemen ed.
Conclusions: The esul s poin o he need o adequa e p ophylac ic measu es h ough he adminis a ion o
mac ocyclic lac ones in animals li ing in Mad id. Ve e ina ians should be awa e o he p esence o his disease
and include hea wo m in he di e en ial diagnosis when a pe p esen s wi h symp oms compa ible wi h D. immi is.
Keywo ds: Feline, Canine hea wo m, Di o ila ia immi is, Vec o -bo ne diseases, P e alence, Epidemiology, Spain
* Co espondence: [email p o ec ed]
1
In e nal Medicine, Facul y o Ve e ina y Medicine, Resea ch Ins i u e o
Biomedical and Heal h Sciences (IUIBS), Uni e si y o Las Palmas de G an
Cana ia, Las Palmas de G an Cana ia, Spain
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Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354
DOI 10.1186/s13071-017-2299-x
Backg ound
Hea wo m disease is caused by Di o ila ia immi is and
is a ch onic, p og essi e and po en ially a al disease o
he in ec ed animals. The main hos s a e dogs and ca s,
al hough in ec ion has been epo ed in o he ca ni o es,
including wild canines as well as domes ic and wild e-
lids. Fu he mo e, humans can be in ec ed since i is a
zoono ic disease [1]. The ansmission occu s h ough
he bi e o he species o culicid mosqui oes belonging
o he gene a Culex,Aedes and Anopheles, among
o he s. Thus, p e alences a e in luenced by he p esence
and abundance o ec o s, depending on clima ic ac o s
such as empe a u e and humidi y [1, 2].
Animal di o ila iosis has been ex ensi ely s udied in
Eu ope. The geog aphical loca ion o Spain, in sou he n
Eu ope, si ua es he Ibe ian Peninsula in he endemic a ea
o di o ila iosis on he con inen [3, 4]. In Spain, he in-
ec ion is p esen in mos o he e i o y, he highes
p e alences being ound in he sou hwes , Medi e anean
coas and i iga ed a eas o inland Spain and in he Cana y
Islands [5–7].
The p o ince o Mad id is in he cen e o he Ibe ian
Peninsula. The al i ude a ies om 550 o 700 m in
mos o he e i o y, excep in he no he nmos pa o
he p o ince, whe e he mean heigh mainly a ies om
1000 o 1700 m, eaching abo e 2000 m a some poin s.
Many i e basins c oss he e i o y om no h o
sou h, ca ying he wa e low o he Ri e Tajo, which
c osses he p o ince in he sou he n pa o he egion.
The p o ince p esen s cold win e s and mild summe s
in he no he n pa o he e i o y, while he es o he
e i o y is cha ac e ized by cold win e s and ho sum-
me s; hese a e he d ies seasons, while ains a e mo e
equen in au umn and sp ing.
The ci y o Mad id is he capi al o he p o ince, and
is also he capi al o Spain. I is he mos highly popu-
la ed ci y o he coun y, as only he cen e o Mad id
has a census o o e 3 million people, 275,000 dogs and
65,000 ca s [8, 9]. The ci y is included wi hin he me o-
poli an a ea, which su ounds he ci y ep esen ing he
mos highly popula ed me opoli an a ea o Spain, wi h
an es ima ed popula ion abo e 7 million and he i h
mos popula ed me opoli an a ea o Eu ope.
Published s udies epo ed canine di o ila iosis o 1.1
and 1.9%, in he p o ince o Mad id, be ween 1987 and
1990 [10, 11]. No s udies ollowed hese da a un il 2013,
when a s udy epo ed p e alences o 2.3% in a wide
a ea o cen al Spain which enclosed Mad id and Toledo
[12]. The e a e no epidemiological da a published e-
ga ding ca s.
The e is a lack o cu en epidemiological da a o ani-
mal hea wo m ocusing on he p o ince o Mad id.
The e o e, he aim o his s udy was o assess he p e a-
lence and cu en dis ibu ion o canine and eline
di o ila iosis in he me opoli an a ea o Mad id and ad-
jacen a eas.
Me hods
The p esen s udy included 1716 dogs and 531 ca s p e-
sen ed o e e ina y clinics be ween Ma ch 2015 and
Sep embe 2016. The samples we e collec ed a 20 e e -
ina y cen es loca ed in he s udied a ea om animals
li ing in he me opoli an a ea o Mad id and adjacen
a eas, including 98 municipali ies in 218 di e en pos al
codes (Fig. 1).
The inclusion c i e ia o animals we e: being o e
6 mon hs o age; no ha ing a elled ou side he a ea o
in e es o he s udy; ne e ha ing ecei ed ea men o
hea wo m disease; and no p e ious his o y o hea -
wo m in ec ion. A comple e eco d was kep o each
animal, including iden i ica ion (age, sex and b eed),
clinical his o y, and demog aphic da a.
O he dogs included, 46.7% we e emales and 53.3%
we e males. By b eed, he mos highly ep esen ed we e
mong el dogs (26.3%), ollowed by Yo kshi e Te ie s
(8.6%), Golden Re ie e s (6.9%), Cocke Spaniels (5.7%),
Boxe (5.3%), F ench Bulldog (4.8%), Ge man Shephe d
(4.1%) and 63 o he b eeds (38.3%). Rega ding he ca s
s udied, 51.4% we e emales and 48.4% we e males; by
b eed, he Eu opean sho hai was he mos highly ep-
esen ed (65.3%), ollowed by Pe sian ca s (14.7%), Siam-
ese ca s (12.2%) and o he 15 b eeds (7.8%). The ca s
we e u he classi ied as indoo (57.6%), ou doo
(12.6%) o indoo /ou doo (a leas 1–50% o he ime
spen ou doo s) (29.8%). The age anges o dogs and
ca s a e desc ibed in Table 1. The s udy included 845
dogs and 312 ca s li ing in he ci y o Mad id while 871
dogs and 219 ca s we e li ing in he es o he s udied
a ea (me opoli an and adjacen a ea).
Blood samples we e collec ed om he cephalic o
jugula ein, placed in 3 ml se um ubes and cen i uged.
Se um was kep a -20 °C un il es s we e pe o med. All
he samples, ei he om ca s and dogs, we e es ed o
ci cula ing D. immi is an igens using a comme cial
immunoch oma og aphic es ki (U ano es Di o ila ia®,
U ano Ve SL, Ba celona, Spain) acco ding o he manu-
ac u e ’s ins uc ions.
Fu he mo e, o es ablish he se op e alence o hea -
wo m in ec ion in ca s, se ological echniques o an i-
D. immi is and an i-Wolbachia an ibody de ec ion we e
also used, as desc ibed by Mo chón e al. [13] wi h some
modi ica ions. In b ie , he pla es we e coa ed wi h
0.8 μgo D. immi is soma ic an igen and Wolbachia su -
ace p o ein (WSP). Se um samples we e p epa ed a 1/
100 o an i-D. immi is se um an ibodies and 1/40 o
an i-WSP an ibody de ec ion. An i- eline IgG an ibody,
ho se adish pe oxidase-labelled (Ki kegaa d and Pe y
Labo a o ies, Gai he sbu g, MD, USA), was applied a 1/
Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354 Page 2 o 6
Fig. 1 Dis ibu ion o canine and eline hea wo m in he p o ince o Mad id (Spain). The da k g ey a ea co esponds o he ci y o Mad id, while
he pale g ey a ea co esponds o he me opoli an and adjacen a ea included in he s udy. The main i e s a e illus a ed as hick black lines.
The posi i e animals a e ma ked as ollows: ed ci cles (hea wo m posi i e dogs); g een squa es (an ibodies-se oposi i e ca s); blue as e isk (an igens-
posi i e ca ). The municipali ies wi h highe p e alences and se op e alences a e indica ed as: 1, A anjuez; 2, Alcalá de Hena es; and 3, Majadahonda
Table 1 Dogs (n) and ca s (n) s udied by age anges, as well as p e alence o hea wo m (%) by each g oup o age
Age ange Dogs (n) Canine p e alence (%)
a
Ca s (n) Feline se op e alence (%)
b
< 1 yea 45 2.2 15 6.7
1–3 yea s 320 3.7 78 1.3
3–6 yea s 393 3.6 213 8.0
6–9 yea s 429 3.3 88 11.4
9–12 yea s 396 2.0 74 5.4
> 12 yea s 133 2.3 63 9.5
a
Based on de ec ion o ci cula ing D. immi is an igens
b
Based on se ological echniques o an i-D. immi is and an i-Wolbachia an ibody de ec ion (conside ed se oposi i e when an i-D. immi is and an i-Wolbachia
su ace p o eins an ibodies p esen ed join ly)
Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354 Page 3 o 6
4000 dilu ion. The op ical densi ies we e measu ed in an
Easy-Reade (Bio-Rad Labo a o ies, He cules, CA, USA)
a 492 nm. Cu -o poin s o ELISA D. immi is 0.8 and
ELISA WSP 0.6 we e ob ained as a i hme ic mean op-
ical densi y ± 3 s anda d de ia ions o se um o cli-
nically heal hy ca s. Ca s we e conside ed se oposi i e
when an i-D. immi is and an i-WSP an ibodies p esen ed
join ly [7, 14–16].
Da a we e analysed using SPSS Base 20.0 so wa e o
Windows (SPSS Inc./IBM, Chicago, IL, USA). Desc ip i e
analysis o he conside ed a iables was ca ied ou con-
side ing he p opo ions o he quali a i e a iables. χ
2
o
compa e p opo ions was pe o med. In all cases, he sig-
ni icance le el was es ablished a P<0.05.
Resul s
The p e alence o D. immi is in he canine popula ion o
he s udied a ea o Mad id was 3% (52/1716). The e
we e no signi ican di e ences in he p e alences be-
ween males (3.2%) and emales (2.9%) (χ
2
= 0.006, d =1,
P= 0.939). By b eed, mong el dogs showed highe bu
no signi ican ly di e en p e alences (4.2%) when com-
pa ed wi h pu e-b eed dogs (2.6%) (χ
2
= 2.902, d =1,
P= 0.088). By age anges, he highes p e alences we e
ound in dogs om 1 o 6 yea s, and signi ican di e ences
we e only obse ed be ween dogs be wee 9–12 yea -old
compa ed wi h dogs be ween 1 and 6 yea -old (χ
2
=2.753,
d =5,P=0.738)(Table1).
An igens es we e posi i e in 0.2% (1/531) o he ca s,
while 7.3% (39/531) o ca s we e se oposi i e o bo h
an i-D. immi is and WSP an ibodies. The e we e no s a-
is ically signi ican di e ences be ween emales (7.7%)
and males (7.0%) (χ
2
= 0.172, d =2,P= 0.918). By
b eed, he Eu opean sho hai p esen ed a se op e a-
lence o 7.5% while he mean se op e alence in he o he
b eeds was 7.1% (χ
2
= 0.036, d =1,P= 0.850). Indoo /
ou doo ca s showed he highes se op e alence (11.4%),
ollowed by ou doo ca s (10.4%) while he lowes co e-
sponded o indoo ca s (4.6%) (χ
2
= 8.201, d =2,
P= 0.017). By age anges, he highes se op e alence
was ound in ca s be ween 6 and 9 yea -old; no signi i-
can di e ences we e ound be ween all g oups o age
(χ
2
= 7.265, d =5,P= 0.202) (Table 1).
The p e alence o hea wo m in ec ion in he ci y o
Mad id in he canine popula ion was 3.3%. By sex, bo h
males and emales showed he same p e alence (3.3%).
The e we e posi i e dogs in 15 o he 21 dis ic s o he
ci y. The p e alence in he me opoli an and adjacen
a eas was 2.7% (2.4% in emales and 3% in males); he
dis ibu ion was no uni o m, he posi i e dogs being
mainly loca ed in he a ea o in luence o he majo i-
e s. By municipali ies, he highes p e alences we e ob-
se ed in A anjuez (10.0%), Majadahonda (6.4%) and
Alcalá de Hena es (5.9%), all o hem in luenced by i-
e s (Fig. 1).
When he ca s we e analysed, he se oposi i i y in he
ci y o Mad id was 6.1%. By sex, he se op e alence was
7.6% in emales and 4.3% in males. The e we e se oposi-
i e ca s p esen in 11 o he 21 dis ic s o he ci y.
The se op e alence was highe in he me opoli an
and adjacen a eas, his being 9.1% (7.7% in emales and
10.3% in males). Posi i e animals we e mainly ound in
a eas close o i e s. By municipali ies, he highes se o-
p e elances we e obse ed in Alcalá de Hena es (27.3%),
A anjuez (20.8%) and Majadahonda (11.1%), all o hem
unde he in luence o i e basins. The only ca posi i e
o he an igens es co esponded o a emale Eu opean
sho hai , li ing ou doo s in A anjuez (Fig. 1).
Discussion
The p esen s udy epo s he p esence o hea wo m in-
ec ion in he pe popula ion o Mad id and es ablishes
he cu en canine p e alence a 3%. P e ious epo ed
da a on hea wo m in ec ion in dogs om Mad id be-
ween 1987 and 1990 a ied om 1.1 o 1.9% [10, 11].
Mo e ecen da a epo ed a p e alence o 2.3% in 2013,
al hough he p e alence was de ined o a wide a ea o
cen al Spain which enclosed Mad id and Toledo wi h a
ela i ely low sample size [12]. Conside ing p e ious da a,
i can be conside ed ha he p e alence o canine hea -
wo m in Mad id has inc eased.
The e a e se e al clima ic condi ions ha could a ou
he ansmission o di o ila iosis in he s udied a ea. The
p o ince o Mad id is unde he in luence o se e al
i e basins, which p o ides a humid en i onmen ap-
p op ia e o he de elopmen o he mosqui oes. The
esul s om he s udy show how cu en ly posi i e dogs
ou side he ci y cen e a e mainly concen a ed in a eas
unde he in luence o he i e s Tajo, Ja ama, Hena es
and Guada ama. The p e alence de ec ed in A anjuez
is especially s iking; he a ea is a small u banized muni-
cipali y unde he in luence o he Ri e Tajo, whe e
dogs li e ou doo s mo e equen ly han in u ban a eas.
An inc ease in he p e alence om ha 6.8% epo ed in
1990 [10] o he cu en 10% was also obse ed. Fu he -
mo e, he ci y o Mad id is also unde he in luence o
he Ri e Manzana es, which c osses he ci y cen e
om wes o eas .
The high le els o u baniza ion o he ci y o Mad id
and he closes me opoli an a ea a e unde he in luence
o he phenomenon called U ban Hea Island (UHI). As
buildings and asphal e ain hea du ing he day which is
e-emi ed owa ds he a mosphe e, he empe a u e
inc eases se e al deg ees inside he ci y c ea ing mic ocli-
ma es [17, 18]. In he case o Mad id, mul iple s udies on
UHI ha e been ca ied ou du ing he las wo decades
[19, 20]. Fu he mo e, human ac i i y inc eases he
Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354 Page 4 o 6
densi y o mosqui oes and de elops a sui able en i on-
men o i s p oli e a ion due o an inc ease in he
p o ision o wa e sou ces and ege a ion which can be
ound in he p esence o pa ks and g een u ban a eas.
Since he mosqui oes can ep oduce in small con aine s
wi h wa e ( lowe po s, ponds, oun ains), all hese ac o s
a ou he clima ic condi ions o he de elopmen o
hea wo m la ae in mosqui o ec o s du ing he cold
mon hs o he yea . This phenomenon was also obse ed
in Ba celona, ano he la ge ci y in Spain [16, 21]. In he
p esen s udy, he p e alence obse ed in he ci y cen e
was 3.3%. A p e ious s udy epo ed a p e alence o 0.6%
in he u ban a ea o Mad id in 1990 [10], he e o e i can
be concluded ha he p e alence in he ci y cen e has
also inc eased. This could be due o he exace ba ion o
he phenomenon o he UHI, a g ea e p esence o g een
u ban a eas, a highe densi y o dogs in he ci y and a low
incidence chemop ophylaxis. Dogs li ing in u ban a eas
a e no sa e om hea wo m in ec ion and should ecei e
adequa e p ophylaxis wi h mac ocyclic lac ones, as con-
cluded in a simila s udy in Ba celona [21].
Geog aphical in o ma ion sys ems (GIS) can p edic
he dis ibu ion and epidemiological beha iou o di o-
ila iosis in di e en e i o ies [3, 21–23] based on cli-
ma ic, ecological and many o he da a ela ed o he
de eloping equi emen s o pa asi es and ec o s. A GIS
esea ch on he gene al p edic ion o he dis ibu ion o
di o ila iosis in Spain showed ha he a ea included in
his s udy is a high isk o D. immi is in ec ion [23];
among o he isk ac o s, due o he exis ence o i i-
ga ed c ops which inc eases he ansmission isk, p o-
iding excellen habi a s o mosqui o b eeding.
Rega ding ca s, he p esen esul s epo he i s epi-
demiological da a on eline D. immi is and demons a e
he p esence o eline hea wo m in Mad id. To da e, in
Spain epidemiological s udies in hea wo m in ec ion in
ca s ha e been p e iously epo ed only in he Cana y
Islands and in Ba celona [7, 14, 16]. The esul s showed
ha 0.2% o ca s we e posi i e o D. immi is an igens in
compa ison wi h 7.3% se oposi i i y o an ibodies. This
may be due o he ac ha he sensi i i y o an igen es-
ing is ela i ely low in ca s, and because hese only de-
ec adul and emale wo ms. The e o e, a nega i e
esul does no ule ou an in ec ion om male wo ms,
p e-adul wo ms o a single emale adul wo m, mos
o which a e common in ca s [24, 25]. On he o he
hand, an ibody es s de ec an ibodies p oduced by
he hos in esponse o in ec ion, which he e o e can
emain posi i e o a long ime a e he dea h o he
pa asi eanddono di e en ia eacu en o apas
in ec ion [24, 26]. Gi en he na u al esis ance o he
eline hos o hea wo m in ec ion, i is es ima ed ha
he eline di o ila iosis is 5–20% o ha o he canine
popula ion in he same a ea [27, 28], and eline
hea wo m epo ed in he p esen s udy is wi hin
hese anges.
The esul s showed ha ca s li ing indoo /ou doo
and indoo p esen ed highe se op e alences, p esu-
mably because hey a e mo e exposed o mosqui o bi es.
Howe e , 4.6% o indoo ca s showed D. immi is an i-
bodies demons a ing ha an indoo li es yle does no
p o ec ca s om in ec ion [16, 29]. Ca s do no usually
ecei e chemop ophylaxis and he e o e he isk o in-
ec ion is highe in his species han in dogs. Se opo-
si i e ca s we e p esen in he same a eas whe e posi i e
dogs we e ound, in luenced by he same clima ic condi-
ions. The se op e alence is highe in ca s om me o-
poli an and adjacen a eas when compa ed wi h he ci y
cen e; p obably one o he easons may be because ca s
li ing in hose municipali ies spend ime ou doo s mo e
equen ly. The e o e, adequa e p ophylac ic ea men s
wi h mac ocyclic lac ones should be ca ied ou in his
species, ega dless o li es yle.
Al hough no s a is ically signi ican , mong el dogs
showed highe p e alences when compa ed wi h pu e-
b eed dogs, as epo ed in o he s udies [21]. Rega ding
ca s, no signi ican di e ences we e obse ed be ween
Eu opean sho hai and all he o he b eeds. By age, he
highes p e alence was ound in dogs om 1 o 3 yea s
ollowed by dogs om 3 o 6 yea s; o he s udies showed
he highes p e alences in olde dogs [14, 23]. In ca s, a
g ea a iabili y in he p e alences by age anges can be
obse ed when he esul s we e compa ed wi h o he
s udies [7, 14–16, 29]. I is no ewo hy o men ion ha
2.2% o dogs < 1 yea -old we e in ec ed and 6.7% o he
ca s we e se oposi i e, which indica es ha ea ly p e-
en i e campaigns in puppies and ki ens wi h mac o-
cyclic lac ones should be ca ied ou .
Conclusions
The esul s show he p esence o canine and eline
hea wo m in he p o ince o Mad id, in he cen e,
me opoli an and adjacen a eas and an inc ease in he
p e alence compa ed o p e ious s udies. These esul s
poin o he need o p ophylac ic measu es wi h he ad-
minis a ion o mac ocyclic lac ones o con ol he dis-
ease and o a oid zoono ic in ec ions. Ve e ina y
clinicians should be awa e o he p esence o his disease
and include hea wo m in he di e en ial diagnosis
when a pe p esen s wi h espi a o y signs o symp oms
compa ible wi h D. immi is.
Abb e ia ions
GIS: Geog aphical in o ma ion sys ems; UHI: U ban Hea Island;
WSP: Wolbachia su ace p o ein
Acknowledgmen s
The au ho s would like o hank all he e e ina y clinics which kindly
coope a ed in he p esen s udy; wi hou hem his s udy could no
ha e been ealized.
Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354 Page 5 o 6
Funding
This esea ch was suppo ed by Baye Hispania S. A.
A ailabili y o da a and ma e ials
All da a gene a ed o analysed du ing his s udy a e included in his
published a icle.
Au ho s’con ibu ions
JAMA and EC designed he s udy and w o e he manusc ip . RM, YFC, SFC
and FS o ganized he ieldwo k, pa icipa ed in he da a collec ions and
analysed he samples. All au ho s analysed he da a, ead and app o ed
he inal manusc ip .
E hics app o al and consen o pa icipa e
All he owne s ga e hei consen o pa icipa ion in his s udy. The s udy
was app o ed by he e hical commi ee o he Ve e ina y Medicine Se ice
o he Uni e si y o Las Palmas de G an Cana ia and was ca ied ou in
acco dance wi h he cu en Eu opean legisla ion on animal p o ec ion.
Consen o publica ion
No applicable.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Publishe ’sNo e
Sp inge Na u e emains neu al wi h ega d o ju isdic ional claims in published
maps and ins i u ional a ilia ions.
Au ho de ails
1
In e nal Medicine, Facul y o Ve e ina y Medicine, Resea ch Ins i u e o
Biomedical and Heal h Sciences (IUIBS), Uni e si y o Las Palmas de G an
Cana ia, Las Palmas de G an Cana ia, Spain.
2
Labo a o y o Pa asi ology,
Facul y o Pha macy, Ins i u e o Biomedical Resea ch o Salamanca (IBSAL),
Uni e si y o Salamanca, Salamanca, Spain.
Recei ed: 18 Ap il 2017 Accep ed: 18 July 2017
Re e ences
1. Simón F, Siles-Lucas M, Mo chón R, González-Miguel J, Mellado I, Ca e ón E,
e al. Human and animal di o ila iasis: he eme gence o a zoono ic mosaic.
Clin Mic obiol Re . 2012;25(3):507–44.
2. Canc ini G, Magi M, Gab ielli S, A ispici M, Tola i F, Dell’Omoda me M, e al.
Na u al ec o s o di o ila iasis in u al and u ban a eas o he Tuscan egion,
cen al I aly. J Med En omol. 2006;43(3):574–79.
3. Genchi C, Rinaldi L, Mo a ino M, Genchi M, C ingoli G. Clima e and
Di o ila ia in ec ion in Eu ope. Ve Pa asi ol. 2009;163(4):286–92.
4. Genchi C, K ame LH, Ri asi F. Di o ila ial in ec ions in Eu ope. Vec o Bo ne
Zoono ic Dis. 2011;11(10):1307–17.
5. Mon oya JA, Mo ales M, Jus e M C, Co be a JA. Hea wo m (Di o ila ia
immi is) in ec ion in dogs: cu en upda e in Spain. In: Genchi C, Rinaldi L,
C ingoli G, edi o s. Di o ila ia immi is and D. epens in dog and ca and
human in ec ions. Naples: Rolando Edi o e; 2007. pp. 175–80.
6. Mo chón R, Ca e ón E, González-Miguel J, Mellado-He nández I. Hea wo m
disease (Di o ila ia immi is) and hei ec o s in Eu ope - new dis ibu ion
ends. F on Physiol. 2012;3:196.
7. Mon oya-Alonso JA, Ca e ón E, Mo chón R, Sil ei a-Vie a L, Falcón Y, Simón
F. The impac o he clima e on he epidemiology o Di o ila ia immi is in
he pe popula ion o he Cana y Islands. Ve Pa asi ol. 2016;216:66–71.
8. Census o domes ic animals o he ci y o Mad id, by dis ic . Ilus e Colegio
O icial de Ve e ina ios de Mad id and Ayun amien o de Mad id. 2016.
h p://da os.mad id.es/egob/ca alogo/207118-0-censo%20animales.xlsx
Accessed 17 Ma 2017.
9. [Municipal Regis e o Inhabi an s Ci y o Mad id]. Á ea de Gobie no de
Economía y Hacienda Subdi ección Gene al de Es adís ica. Ayun amien o
de Mad id. 2016. h p://www.mad id.es/UnidadesDescen alizadas/
UDCEs adis ica/Nue aweb/Demog a %C3%ADa%20y%20poblaci%C3%B3n/
Ci as%20de%20poblaci%C3%B3n/PMH/In o me/In o me_PMH%202016.pd
Accessed 17 Ma 2017.
10. Rojo-Vázquez FA, Valcá cel F, Gue e o J, Gómez M. P e alencia de la
di o ila iosis canina en cua o á eas geog á icas de España. Med Ve .
1990;7(5):297–305.
11. O ega-Mo a LM, Gomez-Bau is a M, Rojo-Vazquez F, Rodenas A, Gue e o J.
A su ey o he p e alence o canine ila iasis in Spain. P e en i e Ve Med.
1991;11(1):63–8.
12. Mi ó G, Mon oya A, Rou a X, Gál ez R, Sainz A. Se oposi i i y a es o
agen s o canine ec o -bo ne diseases in Spain: a mul icen e s udy. Pa asi
Vec o s. 2013;6:117.
13. Mo chón R, Fe ei a AC, Ma ín-Pacho JR, Mon oya-Alonso JA, Mo a ino M,
Genchi C, e al. Speci ic IgG an ibody esponse agains an igens o Di o ila ia
immi is and i s Wolbachia endosymbion bac e ium in ca s wi h na u al and
expe imen al in ec ions. Ve Pa asi ol. 2004;125(3–4):313–21.
14. Mon oya-Alonso JA, Ca e ón E, Co be a JA, Jus e MC, Mellado I, Mo chón R,
e al. Cu en p e alence o Di o ila ia immi is in dogs, ca s and humans
om he island o G an Cana ia. Spain: Ve Pa asi ol; 2011;176(4):291–4.
15. Viei a L, Sil es e-Fe ei a AC, Fon es-Sousa AP, Bal ei a AC, Mo chón R,
Ca e ón E, e al. Se op e alence o hea wo m (Di o ila ia immi is)in
eline and canine hos s om cen al and no he n Po ugal. J Helmin hol.
2015;89(5):625–9.
16. Mon oya-Alonso JA, Ca e ón E, Ga cía-Guasch L, Expósi o J, A ma io B,
Mo chón R, e al. Fi s epidemiological epo o eline hea wo m in ec ion
in he Ba celona me opoli an a ea (Spain). Pa asi Vec o s. 2014;7:506.
17. Oke TR. The ene ge ic basis o he u ban hea island. Q J Roy Me eo Soc.
1982;108(455):1–24.
18. Gago EJ, Roldan J, Pacheco-To es R, O dóñez J. The ci y and u ban hea
islands: a e iew o s a egies o mi iga e ad e se e ec s. Renew Sus Ene g
Re . 2013;25:749–58.
19. Yagüe C, Zu i a E, Ma ínez A. S a is ical analysis o he Mad id u ban Hea
Island. A mos En i on. 1991;25B(3):327–32.
20. Sob ino JA, Sò ia G, Ol a-ca ió R, Jiménez-Muñoz JC, Romague a M,
Cuenca J, e al. DESIREX 2008: u ban Hea Island analysis in he Ci y o
Mad id. Re is a de Telede ección. 2009;31:80–92.
21. Mon oya-Alonso JA, Ca e ón E, Simón L, González-Miguel J, Ga cía-Guasch
L, Mo chón R, Simón F. P e alence o Di o ila ia immi is in dogs om
Ba celona: alida ion o a geospa ial p edic ion model. Ve Pa asi ol.
2015;212(3–4):456–9.
22. Mo a inoM,MusellaV,Cos aV,GenchiC,C ingoliG,RinaldiL.GIS
modeling o canine di o ila iosis isk assessmen in cen al I aly. Geospa
Heal h. 2008;2(2):253–61.
23. Simón L, A onin A, López-Díez LI, González-Miguel J, Mo chón R, Ca e ón E,
e al. Geo-en i onmen al model o he p edic ion o po en ial ansmission
isk o Di o ila ia in an a ea wi h d y clima e and ex ensi e i iga ed c ops.
The case o Spain. Ve Pa asi ol. 2014;200(3-4):257–64.
24. Lee AC, A kins CE. Unde s anding eline hea wo m in ec ion: disease,
diagnosis, and ea men . Top Companion Anim Med. 2010;25(4):224–30.
25. Be doulay P, Le y JK, Snyde PS, Pegelow MJ, Hooks JL, Ta a es LM, e al.
Compa ison o se ological es s o he de ec ion o na u al hea wo m
in ec ion in ca s. J Am Anim Hosp Assoc. 2004;40(5):376–84.
26. Venco L, Ma cheso i F, Manzocchi S. Feline hea wo m disease: A ’Rubik’s-
cube-like’diagnos ic and he apeu ic challenge. J Ve Ca diol. 2015;17(Suppl
1):S190–201.
27. Ryan GR, Newcomb KM. P e alence o eline hea wo m disease: a global
e iew. In: Sol MD, Knigh DH, edi o s. P oceedings o he hea wo m
symposium ‘95. Va a ia: Ame ican Hea wo m Socie y; 1995. p. 79-86.
28. Venco L, Genchi M, Genchi C, Ga i D, K ame L. Can hea wo m p e alence
in dogs be used as p o isional da a o assessing he p e alence o he
in ec ion in ca s? Ve Pa asi ol. 2011;176(4):300–3.
29. K ame L, Genchi C. Feline hea wo m in ec ion: se ological su ey o
asymp oma ic ca s li ing in no he n I aly. Ve Pa asi ol. 2002;104(1):43–50.
Mon oya-Alonso e al. Pa asi es & Vec o s (2017) 10:354 Page 6 o 6