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Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary
G Model VETPAR-6825; No. of Pages 4
ARTICLE IN PRESS Veterinary Parasitology xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary Z. Széll a , G. Marucci b , E. Pozio b , T. Sréter a,∗ a Laboratory of Parasitology, Fish and Bee Diseases, Veterinary Diagnostic Directorate, National Food Chain Safety Office, Tábornok utca 2, H-1143 Budapest, Hungary b Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanitá, viale Regina Elena 299, 00161 Rome, Italy
a r t i c l e
i n f o
Article history: Received 1 March 2013 Received in revised form 15 April 2013 Accepted 21 April 2013 Keywords: Echinococcus multilocularis Trichinella spiralis Golden jackal Canis aureus Europe Hungary
a b s t r a c t Over the last decades the distribution area of the golden jackal (Canis aureus) has increased significantly in Europe, particularly in the Balkan Peninsula and in Central Europe. Vagrant individuals were described in many European countries. Herein, we report Echinococcus multilocularis (total worm count: 412) and Trichinella spiralis (101 larvae/g for muscles of the lower forelimb) infections in two golden jackals shot in Hungary. It is a new host record of E. multilocularis and T. spiralis in Europe and Hungary, respectively. As jackals migrate for long distances through natural ecological corridors (e.g., river valleys), they may play a significant role in the long distance spread of zoonotic parasites into non-endemic areas of Europe. Therefore, monitoring zoonotic parasites in this host species can be recommended in the European Union. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Over the first half of the 20th century, the European population of the golden jackal (Canis aureus) declined dramatically due to habitat fragmentation and intensive hunting pressure. The population density decreased in core areas (Balkan Peninsula) as well as at the edges of its distribution range, where the golden jackal disappeared completely during the last 50 years (Arnold et al., 2012). Thanks to conservation efforts, the density of the Balkan population (Bulgaria and Greece) of the golden jackal increased at the end of the last century. During this period, new populations were established in Turkey, Ukraine, Romania, Serbia, Croatia, Slovenia, Hungary and Austria (Arnold et al., 2012). Vagrant individuals were also recorded in Italy, Slovakia, Germany and Czech Republic (Arnold et al., 2012). Considering the lack of competitors,
∗ Corresponding author. Tel.: +36 1 460 6322; fax: +36 1 252 5177. E-mail address: [email protected] (T. Sréter).
its opportunistic behaviour and omnivorous diet, a further spread of the golden jackal can be postulated (Sillero-Zubiri et al., 2004; Szabó et al., 2009). According to the Directive 2003/99/EC (European Commission, 2003), each member state of the European Union should monitor zoonotic agents. Based on the high pathogenicity and economic significance of Echinococcus spp. and Trichinella spp. (Davidson et al., 2012; Cardona and Carmena, 2013; Pozio, 2013), the monitoring of these parasites is mandatory for all member states. Knowing the population increase of the golden jackal in Europe, the aim of this study was to collect information on the occurrence of Trichinella spp. and Echinococcus spp. in this host species in Hungary. 2. Materials and methods From 2007 to 2013, carcasses of 11 hunted golden jackals were sent to the Veterinary Diagnostic Directorate, Budapest in connection with the rabies immunization and control program. The animals were individually labelled
0304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.vetpar.2013.04.032
Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
G Model VETPAR-6825; No. of Pages 4
ARTICLE IN PRESS Z. Széll et al. / Veterinary Parasitology xxx (2013) xxx–xxx
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with an identification number reporting the information on the locality and date of collection. Carcasses were forwarded by the veterinary authorities in individual plastic bags at +4 ◦ C. The approximate delay between death and necropsy was 3 days. The intestinal tract was removed and stored at −20 ◦ C. For safety reasons, the intestinal tract was frozen at −80 ◦ C for 10 days before examination. After freezing, the gut was thawed at room temperature, the intestinal mucosa was collected and tested by sedimentation and counting technique according to a previously published protocol (Deplazes and Eckert, 1996). The intensity of infection was determined by counting worms by a stereomicroscope at 10-63× magnification. The morphology of worms was studied by a light microscope at 50–100× magnification. For molecular studies, worms were collected and stored in 70% (v/v) ethanol. The taxonomic status of the worms was confirmed by a polymerase chain reaction (PCR) assay of the mitochondrial 12S rRNA gene (Dinkel et al., 1998). To exclude the possibility of contamination with specific DNA, a negative control was included and underwent the entire procedure starting with the DNA extraction. DNA was extracted from five individual worms as previously described (Sréter et al., 2000). PCR reactions were performed by using a BioRad iCycler (BioRad Laboratories, Hercules, CA). The PCR conditions were those previously described (Dinkel et al., 1998). PCR products were separated by electrophoresis in 1.5% agarose gels and stained with ethidium bromide. Since muscles of the lower forelimb of the red fox (Vulpes vulpes) have been identified as predilection sites for Trichinella britovi and Trichinella spiralis larvae (Kapel et al., 2005), muscle samples were collected from the flexor and extensor muscles of the lower forelimb of golden jackals. More then 20 g of muscle tissue trimmed of fat and fascia, were collected from each animal. Muscle samples were digested according to the magnetic stirrer method for pooled sample digestion (European Community, 2005). However, as the reference method was not found to be suitable for a complete digestion of carnivore muscles, the digestion time was increased up to 90 min. Larvae were counted by a stereomicroscope at 15-63× magnification. Then, they were concentrated by centrifugation at 1000 × g for 3 min and stored in 90% ethanol. DNA was extracted from five individual larvae. Trichinella spp. larvae were identified at the species level by an accredited multiplex PCR as previously described (Pozio and La Rosa, 2003; www.iss.it/crlp). Data on the Trichinella isolate from the golden jackal (code ISS4545) is available at the International Trichinella Reference Centre database (www.iss/site/Trichinella/). 3. Results and discussion Out of 11 golden jackals examined, an adult female was found to be infected with 412 mature, mainly gravid worms of Echinococcus sp. The jackal was shot near to river Zala (46◦ 77 North, 17◦ 25 East) (Fig. 1A). Based on the most important morphometric parameters of the adult stage of Echinococcus (length of the worm: 1.3–2.5 mm; number of proglottids: 3–5; length of terminal proglottids:
Fig. 1. Panel A. Echinococcus multilocularis in red foxes (n = 90; filled circles) (Casulli et al., 2010) and in one golden jackal (n = 1, filled square) of Hungary (this study). Panel B. Trichinella spiralis in red foxes (n = 4, filled circles), wild boars, backyard pigs (n = 8, filled triangles) (Széll et al., 2008, 2012), and in one golden jackal (n = 1, filled square) of Hungary (this study).
0.5–1.1 mm; terminal proglottids in percentage of total worm length: 26–44; position of genital pore: anterior to middle; form of uterus: sack-like without lateral sacculations), the worms were identified as E. multilocularis (Jones and Pybus, 2001). Two amplicons of 373 bp and 250 bp were obtained by PCR, confirming the results of the morphological identification as E. multilocularis. This is the first record of E. multilocularis in the golden jackal of Europe (Eckert et al., 2001; Beiromvand et al., 2011). Until 2002, Hungary was thought to be an E. multilocularis free area. In the past decade, this parasite was described in the majority of the Hungarian counties (Fig. 1, panel A), and the spreading of the parasite from the north to the south of the country was confirmed by genetic studies using microsatellites (Sréter et al., 2003, 2004; Casulli et al., 2010). Although the sample size was low in this study, the apparent infection rate of E. multilocularis in the golden jackal is similar to that seen in red foxes earlier (9.1% vs. 10.7%) (Casulli et al., 2010). This is not surprising as the diet composition of the red fox and the golden jackal is similar. In habitats, where the common vole (Microtus arvalis) one of the most important intermediate host of E. multilocularis, is circulating, it is an important item of both fox and jackal diet (Lanszki et al., 2006). E. multilocularis infected vagrant individuals might play a significant role in long distance spread of this parasite from Hungary to non-endemic neighbouring countries (e.g., Croatia and Serbia).
Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
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Out of 11 golden jackals examined, an adult male was found to be infected with Trichinella sp. larvae. The jackal was shot near the river Dráva (45◦ 96 North, 17◦ 47 East) (Fig. 1B). Flexor and extensor muscles of the lower forelimb harboured 101 larvae/g. The multiplex PCR yielded a single band of 173 bp which is diagnostic for T. spiralis. Until 2006, Hungary was thought to be a T. spiralis-free country. In the past years, T. spiralis was detected in three backyard pigs, five wild boars (Sus scrofa) and four red foxes in the southern and eastern border region of Hungary (Fig. 1B) (Széll et al., 2008, 2012) where the golden jackal was shot. This Canidae is a new host record for T. spiralis in Hungary. The prevalence of T. spiralis in Croatia and Serbia bordering Hungary is high in the golden jackal (53.8%), and T. spiralis is the dominant Trichinella species in this host (Zivojinovic et al., 2013; www.iss/site/Trichinella). Jackals are opportunistic, venture into the domestic habitat at night and feed on garbage (Sillero-Zubiri et al., 2004). This feeding behaviour might explain the high prevalence of T. spiralis infection in jackals as T. spiralis is endemic in swine and wildlife of both Croatia and Serbia (Marinculic´ et al., 2001; Cuperlovic et al., 2005; Sofronic-Milosavljevic et al., 2013; Zivojinovic et al., 2013). The T. spiralis infected jackal might have reached Hungary through the ecological corridor of the river Dráva valley bordering Croatia or just by crossing the river Dráva from Croatia. In fact, most of T. spiralis infected animals detected in Hungary originated along the river Dráva valley (Fig. 1, panel B). As vagrant individuals migrate for long distances, T. spiralis infected jackals might introduce this parasite in new countries (e.g., Italy, Macedonia, Greece). Council Directive 92/43/EEC on the conservation of natural habitats with their fauna and flora encourages the management of features of the landscape, including ecological corridors (European Commission, 1992). These corridors are believed to preserve the biodiversity by promoting gene flow between isolated populations (McRae et al., 2012). However, it may promote the spread of zoonotic diseases. Jackals are well adapted to long distance running and are able to run for several hours maintaining speeds of 16 km per hour during hunting. They also trot for large distances (up to 50 km) in search of food (Sillero-Zubiri et al., 2004; Ujhelyi, 2005). Vagrant animals (mainly sub-adult males) may migrate for hundreds of kilometres (Ujhelyi, 2005; Duscher et al., 2013). As jackals can migrate for long distances through ecological corridors, they may play a significant role in the long distance spread of several zoonotic (e.g., Echinococcus granulosus, Dirofilaria immitis, Rhipicephalus sanguineus, Ehrlichia canis, Leishmania infantum) and animal (e.g., Hyalomma marginatum, Hepatozoon canis) parasites known to be endemic in the Balkanian countries. Therefore, monitoring zoonotic parasites in these animals can be recommended in the European Union according to the Directive 2003/99/EC (European Commission, 2003). Acknowledgements The work carried out at the Istituto Superiore di Sanità, Rome, Italy, was partially supported by the European Commission, Contract 2012.
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Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
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Sréter, T., Széll, Z., Egyed, Z., Varga, I., 2003. Echinococcus multilocularis: an emerging pathogen in Hungary and Central Eastern Europe? Emerg. Infect. Dis. 9, 384–386. Sréter, T., Széll, Z., Sréter-Lancz, Z., Varga, I., 2004. Echinococcus multilocularis in Northern Hungary. Emerg. Infect. Dis. 10, 1344–1346. ˝ Szabó, L., Heltai, M., Szucs, E., Lanszki, J., Lehoczki, R., 2009. Expansion range of golden jackal in Hungary between 1997 and 2006. Mammalia 73, 307–311. ˝ A., Pozio, E., Sréter, T., 2008. Széll, Z., Marucci, G., Bajmóczy, E., Cséplo, Spatial distribution of Trichinella britovi, T. pseudospiralis and T. spiralis in red foxes (Vulpes vulpes) in Hungary. Vet. Parasitol. 156, 210–215.
Széll, Z., Marucci, G., Ludovisi, A., Gómez-Morales, M.A., Sréter, T., Pozio, E., 2012. Spatial distribution of Trichinella britovi, T. spiralis and T. pseudospiralis of domestic pigs and wild boars (Sus scrofa) in Hungary. Vet. Parasitol. 183, 393–396. Ujhelyi, P., 2005. Encylopedia of Wildlife. I. Animals of the Basin. Kossuth Kiadó, Budapest, pp. 1–550 Carpathian (in Hungarian). Zivojinovic, M., Sofronic-Milosavljevic, L.J., Cvetkovic, J., Pozio, E., Interisano, M., Plavsic, B., Radojicic, S., Kulisic, Z., 2013. Trichinella infections in different host species of an endemic district of Serbia. Vet. Parasitol., in press.
Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
ARTICLE IN PRESS Veterinary Parasitology xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary Z. Széll a , G. Marucci b , E. Pozio b , T. Sréter a,∗ a Laboratory of Parasitology, Fish and Bee Diseases, Veterinary Diagnostic Directorate, National Food Chain Safety Office, Tábornok utca 2, H-1143 Budapest, Hungary b Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanitá, viale Regina Elena 299, 00161 Rome, Italy
a r t i c l e
i n f o
Article history: Received 1 March 2013 Received in revised form 15 April 2013 Accepted 21 April 2013 Keywords: Echinococcus multilocularis Trichinella spiralis Golden jackal Canis aureus Europe Hungary
a b s t r a c t Over the last decades the distribution area of the golden jackal (Canis aureus) has increased significantly in Europe, particularly in the Balkan Peninsula and in Central Europe. Vagrant individuals were described in many European countries. Herein, we report Echinococcus multilocularis (total worm count: 412) and Trichinella spiralis (101 larvae/g for muscles of the lower forelimb) infections in two golden jackals shot in Hungary. It is a new host record of E. multilocularis and T. spiralis in Europe and Hungary, respectively. As jackals migrate for long distances through natural ecological corridors (e.g., river valleys), they may play a significant role in the long distance spread of zoonotic parasites into non-endemic areas of Europe. Therefore, monitoring zoonotic parasites in this host species can be recommended in the European Union. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Over the first half of the 20th century, the European population of the golden jackal (Canis aureus) declined dramatically due to habitat fragmentation and intensive hunting pressure. The population density decreased in core areas (Balkan Peninsula) as well as at the edges of its distribution range, where the golden jackal disappeared completely during the last 50 years (Arnold et al., 2012). Thanks to conservation efforts, the density of the Balkan population (Bulgaria and Greece) of the golden jackal increased at the end of the last century. During this period, new populations were established in Turkey, Ukraine, Romania, Serbia, Croatia, Slovenia, Hungary and Austria (Arnold et al., 2012). Vagrant individuals were also recorded in Italy, Slovakia, Germany and Czech Republic (Arnold et al., 2012). Considering the lack of competitors,
∗ Corresponding author. Tel.: +36 1 460 6322; fax: +36 1 252 5177. E-mail address: [email protected] (T. Sréter).
its opportunistic behaviour and omnivorous diet, a further spread of the golden jackal can be postulated (Sillero-Zubiri et al., 2004; Szabó et al., 2009). According to the Directive 2003/99/EC (European Commission, 2003), each member state of the European Union should monitor zoonotic agents. Based on the high pathogenicity and economic significance of Echinococcus spp. and Trichinella spp. (Davidson et al., 2012; Cardona and Carmena, 2013; Pozio, 2013), the monitoring of these parasites is mandatory for all member states. Knowing the population increase of the golden jackal in Europe, the aim of this study was to collect information on the occurrence of Trichinella spp. and Echinococcus spp. in this host species in Hungary. 2. Materials and methods From 2007 to 2013, carcasses of 11 hunted golden jackals were sent to the Veterinary Diagnostic Directorate, Budapest in connection with the rabies immunization and control program. The animals were individually labelled
0304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.vetpar.2013.04.032
Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
G Model VETPAR-6825; No. of Pages 4
ARTICLE IN PRESS Z. Széll et al. / Veterinary Parasitology xxx (2013) xxx–xxx
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with an identification number reporting the information on the locality and date of collection. Carcasses were forwarded by the veterinary authorities in individual plastic bags at +4 ◦ C. The approximate delay between death and necropsy was 3 days. The intestinal tract was removed and stored at −20 ◦ C. For safety reasons, the intestinal tract was frozen at −80 ◦ C for 10 days before examination. After freezing, the gut was thawed at room temperature, the intestinal mucosa was collected and tested by sedimentation and counting technique according to a previously published protocol (Deplazes and Eckert, 1996). The intensity of infection was determined by counting worms by a stereomicroscope at 10-63× magnification. The morphology of worms was studied by a light microscope at 50–100× magnification. For molecular studies, worms were collected and stored in 70% (v/v) ethanol. The taxonomic status of the worms was confirmed by a polymerase chain reaction (PCR) assay of the mitochondrial 12S rRNA gene (Dinkel et al., 1998). To exclude the possibility of contamination with specific DNA, a negative control was included and underwent the entire procedure starting with the DNA extraction. DNA was extracted from five individual worms as previously described (Sréter et al., 2000). PCR reactions were performed by using a BioRad iCycler (BioRad Laboratories, Hercules, CA). The PCR conditions were those previously described (Dinkel et al., 1998). PCR products were separated by electrophoresis in 1.5% agarose gels and stained with ethidium bromide. Since muscles of the lower forelimb of the red fox (Vulpes vulpes) have been identified as predilection sites for Trichinella britovi and Trichinella spiralis larvae (Kapel et al., 2005), muscle samples were collected from the flexor and extensor muscles of the lower forelimb of golden jackals. More then 20 g of muscle tissue trimmed of fat and fascia, were collected from each animal. Muscle samples were digested according to the magnetic stirrer method for pooled sample digestion (European Community, 2005). However, as the reference method was not found to be suitable for a complete digestion of carnivore muscles, the digestion time was increased up to 90 min. Larvae were counted by a stereomicroscope at 15-63× magnification. Then, they were concentrated by centrifugation at 1000 × g for 3 min and stored in 90% ethanol. DNA was extracted from five individual larvae. Trichinella spp. larvae were identified at the species level by an accredited multiplex PCR as previously described (Pozio and La Rosa, 2003; www.iss.it/crlp). Data on the Trichinella isolate from the golden jackal (code ISS4545) is available at the International Trichinella Reference Centre database (www.iss/site/Trichinella/). 3. Results and discussion Out of 11 golden jackals examined, an adult female was found to be infected with 412 mature, mainly gravid worms of Echinococcus sp. The jackal was shot near to river Zala (46◦ 77 North, 17◦ 25 East) (Fig. 1A). Based on the most important morphometric parameters of the adult stage of Echinococcus (length of the worm: 1.3–2.5 mm; number of proglottids: 3–5; length of terminal proglottids:
Fig. 1. Panel A. Echinococcus multilocularis in red foxes (n = 90; filled circles) (Casulli et al., 2010) and in one golden jackal (n = 1, filled square) of Hungary (this study). Panel B. Trichinella spiralis in red foxes (n = 4, filled circles), wild boars, backyard pigs (n = 8, filled triangles) (Széll et al., 2008, 2012), and in one golden jackal (n = 1, filled square) of Hungary (this study).
0.5–1.1 mm; terminal proglottids in percentage of total worm length: 26–44; position of genital pore: anterior to middle; form of uterus: sack-like without lateral sacculations), the worms were identified as E. multilocularis (Jones and Pybus, 2001). Two amplicons of 373 bp and 250 bp were obtained by PCR, confirming the results of the morphological identification as E. multilocularis. This is the first record of E. multilocularis in the golden jackal of Europe (Eckert et al., 2001; Beiromvand et al., 2011). Until 2002, Hungary was thought to be an E. multilocularis free area. In the past decade, this parasite was described in the majority of the Hungarian counties (Fig. 1, panel A), and the spreading of the parasite from the north to the south of the country was confirmed by genetic studies using microsatellites (Sréter et al., 2003, 2004; Casulli et al., 2010). Although the sample size was low in this study, the apparent infection rate of E. multilocularis in the golden jackal is similar to that seen in red foxes earlier (9.1% vs. 10.7%) (Casulli et al., 2010). This is not surprising as the diet composition of the red fox and the golden jackal is similar. In habitats, where the common vole (Microtus arvalis) one of the most important intermediate host of E. multilocularis, is circulating, it is an important item of both fox and jackal diet (Lanszki et al., 2006). E. multilocularis infected vagrant individuals might play a significant role in long distance spread of this parasite from Hungary to non-endemic neighbouring countries (e.g., Croatia and Serbia).
Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032
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Out of 11 golden jackals examined, an adult male was found to be infected with Trichinella sp. larvae. The jackal was shot near the river Dráva (45◦ 96 North, 17◦ 47 East) (Fig. 1B). Flexor and extensor muscles of the lower forelimb harboured 101 larvae/g. The multiplex PCR yielded a single band of 173 bp which is diagnostic for T. spiralis. Until 2006, Hungary was thought to be a T. spiralis-free country. In the past years, T. spiralis was detected in three backyard pigs, five wild boars (Sus scrofa) and four red foxes in the southern and eastern border region of Hungary (Fig. 1B) (Széll et al., 2008, 2012) where the golden jackal was shot. This Canidae is a new host record for T. spiralis in Hungary. The prevalence of T. spiralis in Croatia and Serbia bordering Hungary is high in the golden jackal (53.8%), and T. spiralis is the dominant Trichinella species in this host (Zivojinovic et al., 2013; www.iss/site/Trichinella). Jackals are opportunistic, venture into the domestic habitat at night and feed on garbage (Sillero-Zubiri et al., 2004). This feeding behaviour might explain the high prevalence of T. spiralis infection in jackals as T. spiralis is endemic in swine and wildlife of both Croatia and Serbia (Marinculic´ et al., 2001; Cuperlovic et al., 2005; Sofronic-Milosavljevic et al., 2013; Zivojinovic et al., 2013). The T. spiralis infected jackal might have reached Hungary through the ecological corridor of the river Dráva valley bordering Croatia or just by crossing the river Dráva from Croatia. In fact, most of T. spiralis infected animals detected in Hungary originated along the river Dráva valley (Fig. 1, panel B). As vagrant individuals migrate for long distances, T. spiralis infected jackals might introduce this parasite in new countries (e.g., Italy, Macedonia, Greece). Council Directive 92/43/EEC on the conservation of natural habitats with their fauna and flora encourages the management of features of the landscape, including ecological corridors (European Commission, 1992). These corridors are believed to preserve the biodiversity by promoting gene flow between isolated populations (McRae et al., 2012). However, it may promote the spread of zoonotic diseases. Jackals are well adapted to long distance running and are able to run for several hours maintaining speeds of 16 km per hour during hunting. They also trot for large distances (up to 50 km) in search of food (Sillero-Zubiri et al., 2004; Ujhelyi, 2005). Vagrant animals (mainly sub-adult males) may migrate for hundreds of kilometres (Ujhelyi, 2005; Duscher et al., 2013). As jackals can migrate for long distances through ecological corridors, they may play a significant role in the long distance spread of several zoonotic (e.g., Echinococcus granulosus, Dirofilaria immitis, Rhipicephalus sanguineus, Ehrlichia canis, Leishmania infantum) and animal (e.g., Hyalomma marginatum, Hepatozoon canis) parasites known to be endemic in the Balkanian countries. Therefore, monitoring zoonotic parasites in these animals can be recommended in the European Union according to the Directive 2003/99/EC (European Commission, 2003). Acknowledgements The work carried out at the Istituto Superiore di Sanità, Rome, Italy, was partially supported by the European Commission, Contract 2012.
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Please cite this article in press as: Széll, Z., et al., Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.04.032