Ve te r i nar y P ar as i t o l og y 2 0 3 ( 2 01 4 ) 3 3 9 34 2

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Veterinary Parasitology
jo u r nal homep age: www.elsevier.com/locate/vetpar

Short communication

Dirofilaria immitis: An emerging parasite in dogs, red foxes

and golden jackals in Hungary
Z. Z. . L. T.
Tolnai a, Szll a , Sproch b, Szeredib,
Srter a,*
a L ab or at or y

o f P ar as i to l og y, F is h an d B ee D i sea s es , Veter i n ar y D i ag no s ti c Di r ec to ra te, Na ti on a l F oo d C h ai n S af et y Of fi c e, T bo rn o

k u tc a
2 , B u d ap es t H- 1 1 43 , H u ng ar y

b Lab or a tor y
o f M a m ma l i an , P ou l tr y a nd Wi l d li f e P at ho l og y, Vet er i na r y Di a gn os t ic D i rec t or at e, N at io n al Fo od C h a in Sa f ety O f fi c e,

T bo rn o k u tc a 2 , B u da p est H - 1 14 3 , Hu n ga r y

articleinfo abstract
Hungary was not considered to be a heartworm (Dirofilaria immitis) endemic country
until
Ar ti c l e h i st or y:
R ece i ve d 1 1 Fe br u a ry 20 1 4

2007, when the first autochthonous canine infection was described. Herein we report
addiR ece i ve d i n r ev i s ed fo r m 2 Ap r i l 20 1 4

tional autochthonous heartworm infections in two dogs (Canis familiaris), twenty red
foxes
A cce p te d 4 Ap r i l 2 0 1 4

(Vulpes vulpes) (n = 534; prevalence: 3.7%; 95% CI = 2.45.7%) and two golden
jackals (Canis
aureus) (n = 27; prevalence: 7.4%; 95% CI = 2.123.4%) coming from eight counties.
The identification of the parasite was based on morphology, morphometrics and amplification of
12S
K eyw or ds :

rDNA followed by sequencing in all cases. Our results indicate that Hungary became a
D.
H e ar t wo r m

immitis endemic country in the past decade. The prevalence and intensity of heartworm
D i r ofi l ar i a i m mi t is

infection in wild canids is similar to or lower than that observed in the Mediterranean
P r ev al e nce

countries of Europe (3.77.4% vs. 0.412.7% and 1.5 vs. 2.94.4 worms/animal).
These findD i s t ri b u t i on
Dog

ings are in line with the results of the recently developed climate based forecast model
to
R ed fo x

predict the establishment of D. immitis in Hungary.

G o l d en jac ka l

2014 Elsevier B.V. All rights

reserved.

1. Introduction heartworms and their antigenic products (Genchi et al.,

2007; Simn et al., 2012). Several species of mosquitoes
can
Heartworm disease is caused by the nematode Dirofi- serve as intermediate hosts worldwide (McCall et al., 2008).
laria immitis. Patent infections are possible in numerous Infected mosquitoes can transmit the parasite to humans,
wild and companion animal species. Wild animal reservoirs but the infection does not become patent. The infective larinclude wild canids and probably some other carnivore vae reach the lungs, become encapsulated and die causing
species in Europe (McCall et al., 2008; Simn et al., 2012). granulomatous reactions called coin lesions in humans.
In companion animals, heartworm disease is diagnosed The lesions are medically significant because radiographimainly in dogs and less commonly in cats and ferrets, due cally they appear similar to metastatic lung cancer (Genchi
to the differences of diagnostic techniques and the life- et al., 2007; Simn et al., 2012). Heartworm disease has
span of the parasites in these animals (Genchi et al., 2007). been reported worldwide in many countries with temHeartworm infection may lead to serious and potentially perate, semitropical or tropical climates (McCall et al.,
fatal cardiopulmonary disease caused primarily by adult 2008; Simn et al., 2012). In Europe, D. immitis infections
occur mainly in the southern countries including Spain,
Portugal, France, Italy, Greece and Turkey (Genchi et al.,
2009). These countries are considered to be the historically
* C o r re s p ond i ng
au t hor . T el . : + 36 1 4 6 0 63 2 2 ; fa x: + 3 6 1 2 52 5 1 77 .

endemic region of the continent. Recent reports from other

E- m ai l ad d res s : Sr et er T @neb i h. go v .hu (T . S r te r ).

htt p :/ /d x .d o i .o r g/ 1 0. 1 0 16 / j.v et p ar .2 0 1 4 .0 4 . 00 4
0 3 0 4 - 40 1 7 / 2 0 1 4 E l s ev i er B.V . Al l r i ght s r es e r ve d .

3 40 Z . To l na i e t al . / Vete ri n a ry P ar a si t ol og y 2 03 (2 01 4 ) 3 39 34 2

European countries indicate an expansion of the dis- carried out with MedCalc 12.7 (MedCalc Software, Ostend,
tribution of the parasite (Genchi et al., 2005, 2009, Belgium) and EpiTools (Sergenat, 2014) programmes.
2011). In Eastern Europe, Bulgaria, Croatia, Romania and
Serbia are currently known to be endemic, and sporadic autochthonous cases were also reported from Czech 3. Results and discussion
Republic, Slovakia and Hungary (Genchi et al., 2007).
Herein we provide evidence that Hungary should also be During necropsy, four male and thirteen female adult
considered as a D. immitis endemic country. worms were detected in the right ventricle of the heart
of Dog 1, and a male adult worm was
found in the vena
2. Materials and methods cava of Dog 2 (Table 1). The worms collected from the
heart of Dog 1 and vena cava of Dog
2 and the microfilariae
The carcass of a 7-year-old male shepherd Mudi dog detected in the blood of Dog 1 were identified as D.
immi(Dog 1) and a 12-year-old female mongrel dog (Dog 2) was tis on the basis of the characteristic morphological
features
sent to the National Food Chain Safety Office of Budapest and morphometrics of the parasites (Genchi et al.,
2007).
with suspicion of poisoning in February 2013 and January The identification was also confirmed by 12S rDNAbased
2014. During necropsy, the heart and vena cava were slit PCR. The results of sequencing showed 100% agreement
open and visually inspected. Although the blood was par- with D. immitis (GenBank accession no. AJ544831).
Dog
tially clotted, blood samples could be collected from the 1 was born in a sheep farm near to Hajdbagos, county
heart of dogs and examined by the modified Knott test Hajd-Bihar (Fig. 1) and has never been outside of the
(Genchi et al., 2007). farm and the surrounding grazing area. Dog 2 was born
In order to reveal the spatial distribution of D. immitis in in jl orincfalva, county Heves and has never left
the vilthe warmest region of Hungary, heart and lungs of red foxes lage (Fig. 1). Therefore, both cases should be
considered
(Vulpes vulpes) killed by hunters and sent in individual plas- autochthonous. In 2007 and 2009, similar
autochthonous
tic bags at to the National Food Chain Safety Office heartworm infections were detected in a dog and a ferret
+4 C

were screened for heartworm infections from November in counties Jsz-Nagykun-Szolnok and Baranya (Jacs et
al.,
2013 to January 2014. Red fox carcasses, representing more 2009; Molnr et al., 2010).
than 1% of the total fox population (n = 534), were randomly Twenty foxes (3.7%; 95% CI = 2.45.7%) and two
jackselected out of all the foxes from the southern counties als (7.4%; 95% CI = 2.123.4%) coming from eight
counties
as described (Szll et al., 2008) (Fig. 1). All golden jackal (Baranya, Bks, Borsod-Abaj-Zempln, Csongrd,
Fejr,
(Canis aureus) carcasses (n = 27) sent to the laboratory from Heves, Jsz-Nagykun-Szolnok, Pest) in 2013 and
2014
November 2007 to January 2014 were included in the were infected with low number of D. immitis adults
present study (Fig. 1). Carcasses were individually labelled (m SE = 1.5 0.2; range: 15 worms/animal) (Fig. 1;

by the hunters with an identification number reporting the Table 1). All worms except one isolated from the
pulmonary
information on the nearest place to killing on the topo- artery were detected in the right ventricle of the heart.
graphic map and the date of collection. If the nearest place Microfilariae were not found in the uterus of the female
to hunting was a human settlement, the animal position worms or in the blood samples of the infected wild canids
within a municipality (illustrated with a symbol in Fig. 1) (Table 1). Species identification was based on morpholwas randomly chosen. The heart, pulmonary artery and ogy, morphometrics and amplification of 12S rDNA gene
lungs of the animals were slit open and examined visually followed by sequencing in all cases. The presence of
low
for the presence of parasites. In Dirofilaria positive cases, number of adult heartworms in foxes and jackals withvarious amount of non-clotted blood samples were col- out microfilaraemia might indicate that these species are
lected from the heart or the body cavities and examined by not good hosts for D. immitis (Marconcini et al., 1996).
modified Knott test (Genchi et al., 2007). Parasite species Therefore, the true impact of foxes and jackals on the
identification was based on morphology and morphomet- transmission dynamics of dirofilariosis should be
assessed
rics. (Simn et al., 2012).
Species identification was also confirmed by 12S rDNA- Our results indicate that the Hungarian lowland is a
D.
based PCR in all cases (Casiraghi et al., 2001). DNA was immitis endemic region. The prevalence and intensity of
extracted from worms and purified as described (Srter- heartworm infection in wild canids seems to be similar to
Lancz et al., 2007). The fragments of 12S rDNA were or lower than that observed in the Mediterranean countries
amplified (Casiraghi et al., 2001), and amplicons were of Europe (3.77.4% vs. 0.412.7% and 1.5 vs. 2.94.4
further characterised by sequence analysis (Srter-Lancz worms/animal) (Gortzar et al., 1994, 1998; Manas et al.,
et al., 2007). Sequencing data were visually inspected for 2005; Genchi et al., 2007; Magi et al., 2008). These
findings
reading errors and combined using Chromas (Technely- are in line with the results of the recently developed clisium, Tewantin) and MultAlin (Corpet, 1988) programmes. mate based forecast model to predict the occurrence of
the
Sequences were identified by comparison with GenBank parasite in Europe (Genchi et al., 2005, 2007). The yearly
entries using the BLAST software (National Center for average predicted heartworm generations are between 1
Biotechnology Information, 2014). and 5 in Hungary. Although it is lower than that predicted
The locality of origin of the dogs, foxes and jackals and in the majority of the territory of the Mediterranean
Basin
the number of D. immitis adults were marked on the map (110 generations), the climate of Hungary was thought
to
(vector point layer) by the Quantum GIS 1.8.0 software be suitable for the establishment of D. immitis in Hungary
(QGIS Team, 2012) (Fig. 1). Statistical calculations were (Genchi et al., 2005, 2007).

Z. T ol n a i et a l . / Veter i n ar y P ar as i to l ogy 20 3 ( 20 1 4) 33 9 3 4 2 3 41

F ig . 1. Map o f H u nga r y s ho wi ng u ni nfe cte d (o p en s y mb ol s ) and D i ro fil a ri a i mm i ti s i nfe cte d r e d f ox e s ( Vu l

pes vu l p es ) (fi l l ed ci r cl es ) , g o l d en jac ka l s ( C an i s
a u re us ) ( fil l ed tr i a ngl e s ) and d og s (C an i s f am i l ia r is ) ( fil l ed s q u ar es ) .
T a ble 1
N u mb e r o f he ar tw o rm s ( Di r ofi l a ri a i m m i ti s ) d et ec ted i n d o gs ( Ca n i s f a mi l i a ri s ), re d fo xe s (Vu l pe s vu l p es ) and g o ld e n
jack a l s ( C an i s a u re us ) i n H u ng ar y a nd

t he r es u l t s o f the Kno tt t es t .

H o s t s p e ci es N ear e s t hu man s et tl e men t N u mb er of he ar tw o r ms Res u l t o f th e Kno tt t es t

D o g H ajd b ag o s 1 3 g r av i d fe mal e s + 4 ma l es Po s i t i ve
jl o r i ncfa l va 1 m al e N eg at i ve

R ed fo x T s ze g 1 m al e N eg at i ve
Val k 1 m al e N eg at i ve

N ag yk r u 1 no n- g ra vi d fe mal e N eg at i ve
Ki s k u nl ach za 2 m al es N eg at i ve
Sze g hal o m 1 no n- g ra vi d fe mal e N eg at i ve

Ti s z an na 1 no n- g ra vi d fe mal e + 1 mal e N eg at i ve
Ki s zo mb o r 1 m al e N eg at i ve

T s ze g 1 m al e N eg at i ve
Mi nd s ze nt 3 no n- g ra vi d fe mal e s + 1 mal e N eg at i ve

H ar s ny 1 m al e N eg at i ve
Mag ya r b l y 1 no n- g ra vi d fe mal e N eg at i ve
Er d o te l ek 1 m al e N eg at i ve

Szo l no k 1 no n- g ra vi d fe mal e N eg at i ve
Sze g ed - Sze ntm i hl y 1 no n- g ra vi d fe mal e N eg at i ve

Sza b ad k gy s 1 m al e N eg at i ve
Feg y ve r nek 1 no n- g ra vi d fe mal e N eg at i ve

S r nd 1 no n- g ra vi d fe mal e + 1 mal e N eg at i ve
Bk s cs a b a 1 no n- g ra vi d fe mal e N eg at i ve
Ber et ty jfal u 2 no n- g ra vi d fe mal e s + 3 mal e s N eg at i ve

Or o s hz a 1 no n- g ra vi d fe mal e N eg at i ve
G o l d en jac ka l H ev es a ra nyo s 1 m al e N eg at i ve
Sz k es fe hr v r 1 no n- g ra vi d fe mal e N eg at i ve

Europe has experienced the spreading of D. immitis,

2007; Simn et al., 2012; Otranto et
al., 2013a). The first
Dirofilaria repens and some other vector-borne helminths D. repens endemic region was detected in southern part of
from the Mediterranean countries towards the northern Hungary in 1998 (Szll et al., 1999), and D. repens is curand eastern ones in the past decades (Genchi et al., 2005, rently considered a widely distributed emerging parasite

3 42 Z . To l na i e t al . / Vete ri n a ry P ar a si t ol og y 2 03 (2 01 4 ) 3 39 34 2

in Hungary (Sznsi et al., 2008). Recently, another filarG or t za r, C ., C as t i l lo , J.A ., Lu ci en

tes , J., Bi anco , J.C . , Ar r i o l ab eng o a,
A., C al ve te , C ., 1 9 9 4. F act or s a ffe cti ng
D i ro fi l ar i a i m m i ti s p r ev al e nce
i n r ed

ial parasite occurring in the Mediterranean Basin (Otranto

fo xe s i n no r th- ea s te rn S p ai n. J.
Wi l d . Di s . 30 , 5 4 5 5 47 .

et al., 2013b), Onchocerca lupi has been reported from

G or t za r, C ., V i l l afu e r te , R., Lu ci e
ntr es , J., F er nnd e z- d e- Lu c o, D. , 1 9
9 8.

Hungary (Srter and Szll, 2008). Although the sample size

H ab i ta t re l at ed d i ff er ence s i n he
l mi nth p ar as i t es o f r ed fo xe s i n th
e
E br o va l l ey . Ve t. P a ra s i to l . 8 0 , 7 5 81 .

was smaller (n = 100) in our previous study (Srter et al.,

Jac s , O. , M nd o ki , M. , Ma jor o s ,
G . , P t s ch, M. , M or t ar i no , M. , G
enchi ,

2003), D. immitis was not detected in foxes of Hungary 11

C ., Fo k , ., 20 0 9 . F i rs t au t ocht
ho no u s D i ro fi l ar i a i m mi t is (L ei
dy,1856)

years ago. The present study has revealed that Hungary

i nfec ti o n i n a d o g i n H u ng ar y. He
l mi nt hol o g i a 4 6, 15 9 1 6 1.

became a D. immitis endemic country in the past decade.

McC a l l , J. W ., G e nchi , C . , Kr a mer , L .H . , G u er r er o , J. , Ve nco , L ., 2 0 0 8 . H e ar t-

wo r m d i s ea s e i n a ni mal s and hu
ma ns . Ad v . P ar as i t ol . 66 , 19 3 2
8 5.

Several factors including climate change (Genchi et al.,

Mag i , M. , C a ld e r i ni , P ., G ab r i el l i ,
S ., De l l O mo d ar me , M. , Mac chi o ni ,
M.,

2009, 2011; Simn et al., 2012; Otranto et al., 2013a), global

P ra ti , M .C . , C anc ri ni , G. , 2 0 0 8.
Vu lp es vu l pe s: a p os s i b l e w i l d
re s er v oi r
fo r zo o no ti c fil a ri a e. V ec to r Bo r ne Z oo no ti c D i s . 8 , 2 4 9 2 5 2 .

movement (Tatem et al., 2006) and nature conservation

Mana s , S. , Fer r er , D ., C as t el l , J., L
p e z- Mar t n, J. M. , 2 0 0 5 . Ca r d i op u l
-

efforts (Szll et al., 2013) might be in the background of

mo nar y hel mi nt h p ar as i t es o f r e d
fo xe s (Vu l p es vu l pe s) i n C at al o
ni a,

these changes. As the veterinary and public health signo rt h- eas t er n Sp a i n. Ve t. J. 1 69 ,

1 1 8 1 20 .

nificance of these parasites are high, further studies are

Mar co nci ni , A. , M ag i , G . , Ma cchi o ni
, G. , S as s e tt i , M. , 19 9 6 . Fi l ar i o s i s
i n fo x es
i n I tal y . V et . Res . C omm u n. 2 0 , 3
16 3 1 9 .

needed on the distribution of vector-borne helminths of

Mo l nr , V ., P az r , P ., Ri g , D ., Mt
h, D. , F o k, ., Gl vi t s , R. , V ajd o vi c
h, P .,

dogs, cats and humans in other European countries includJacs , O ., Ba l o gh, L. , S s , E ., 2 0

1 0 . A u to cht hon ou s Di r ofi l ar i a i
mm i ti s

ing Hungary. As wild carnivores are excellent sentinels

i nfec ti o n i n a f er re t w i th ab e rr
ant l ar va l m i gr at i o n i n E u ro p e.
J. Sm al l
Ani m. Pr ac t. 5 1 , 3 9 3 39 6 .

for the spread of D. immitis, and the number of studies is

N at i ona l C e nte r fo r Bi o te chno l og y
Info r mat i o n, 20 1 4 . BLA ST , Acce s s ed
at :

limited in Europe (Simn et al., 2012), further investigahtt p :// ww w .nc bi . nl m. ni h.g o v/ bl
ast

tions can be encouraged in this field.

O tr ant o, D . , D a nta s- T o rr e s , F ., Br i
ant i , E. , Tr av e rs a , D . , Pe tr i c, D ., G
enchi ,
C ., C ap e l l i , G ., 2 0 1 3 a. V ec to r
-b o r ne hel mi nt hs of d o g s a nd hu
mans i n
E u ro p e. Pa r as i te s Vec to r s 6 , 1 6 .

Con ict of interest

O tr ant o, D . , Da nta s -T o r re s , F. , G i a
nnel l i , A. , La tr of a, M. S. , Pa p ad o p o u
l os ,
E ., C ar d o s o , L ., C o r te s , H. , 2 0
13 b . Z o ono t i c O nc h o c erc a l u p i
i nfe cti o n
i n d o gs , G r ee ce and P o r tu g al , 2
0 11 - 2 0 1 2 . E me rg . Infe ct. D i s . 1
9,

The authors declare that the research was conducted in

2 00 0 2 0 03 .

the absence of any commercial and financial relationships

Q GIS T e am, 2 0 1 2 . Q u ant u m G IS ,
Acc es s ed a t: htt p :/ /w ww . qg i s . or g

that could be construed as potential con ict of interest.

Si m n, F ., S i l es - Lu ca s , M. , Mo rc
hn, R ., G o nzl e z- Mi g u el , J. , Me l l
ad o , I.,
C ar r et n, E . , Mo nto y a- Al o ns o ,
J.A ., 2 0 1 2. H u m an a nd a ni mal d i
ro fil ar i as i s : t he em er ge nce o f a zo o
no ti c mo s ai c. C l in . Mi cr o bi o l .
Re v . 2 5,

Acknowledgements
5 07 5 4 4 .
Se r ge nat , E. S. G ., 2 0 1 4. Ep i T o ol s ep
i d e mi o l og i ca l ca l cu l at or . A u s Vet ,
Av ai l -

We thank Jnos Malinovszki and Zsolt Tth for their help

ab l e a t: ht tp :/ /e pi t o ol s . au s v
et .c om .a u
Sr ter , T ., S z l l , Z. , 2 0 0 8. O ncho ce r
cos i s : a ne wl y r e cog ni ze d d i s e as e i
n

in sample collection and Andrea Kollr for her technical

d o gs . V et . P ar as i t ol . 15 1 , 1 1 3 .

assistance.
Sr ter , T ., S z l l , Z. , Ma ru cc i , G. , P

oz i o, E . , Var g a, I. , 2 00 3 . E x tr ai nt es
t i nal
nema to d e i nfec ti o ns o f r ed f ox es
(Vu l pe s v u l pes ) i n H u nga r y. Ve t.
P ar as i to l . 1 4 8 , 3 6 5 3 7 0 .

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