Abstract
Aujeszky disease (AD) or pseudorabies is a viral disease of domestic and wild animals caused by the Suid alphaherpesvirus 1. In wild boar infection usually undergo latent phase but under certain conditions reactivation of the virus can result in a disease. Seroprevalence in wild boars ranges from 0.8 to 100%, and is among other influenced by region, type of management, age and sex of the studied animals. In this study we analyzed blood, lungs, olfactory bulbs and spleen from 222 free-living wild boars from different localities in Croatia and compared results obtained by ELISA with PCR, sex, age and locality. Total seroprevalence was 33.78%, ranging from 25.26% in males to 40.15% in females (p = 0.0346; χ2 = 4.47). According to the age categories prevalence was 10% in offspring, 27.53% in subadults, and 66.75% in adults. Seroprevalence in adult males (66.66%) and females (65.30%) was almost identical. In males, significantly lower seroprevalence was detected in offspring compared to subadults (χ2 = 4.07, p < 0.05) and adults (χ2 = 31.04; p < 0.05), and in subadults compared to adults (χ2 = 15.13; p < 0.0001). Among females, adults had a significantly higher prevalence compared to offspring (χ2 = 19.27; p < 0.0001) and subadults (χ2 = 8.62; p < 0.01). Analysis between counties revealed Sisačko-moslavačka county as a hot-spot for AD. None of the samples was positive for ADV antigens. The observed trend in prevalence points to the fact that the main transmission occurs during one part of the year (most probably the mating season). Also, triggers for virus reactivation might be more complex than previously thought, since none of our samples, collected during the mating and hunting season, was PCR positive. Finally, we can conclude that adult males represent the main transmission link between different wild boar groups.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AD:
-
Aujeszky disease
- ADV:
-
Aujeszky disease virus
- PRV:
-
pseudorabies virus
References
Alemañ N, Quiroga MI, López-Peña M, Vázquez S, Guerrero FH, Nieto JM (2001) Induction and inhibition of apoptosis by pseudorabies virus in the trigeminal ganglion during acute infection of swine. J Virol 75:469–479. doi: https://doi.org/10.1128/JVI.75.1.469-479.2001
Aujeszky A (1902) Uber eine neu Infektions Krankheit bei Haustieren. Zentralblatt für Bakteriologie und Parasitenkunde Abteil I. Orig 32:353–357
Banks M, Monsalve Torraca LS, Greenwood AG, Taylor DC (1999) Aujeszky’s disease in captive bears. Vet Rec 145:362–365. doi:https://doi.org/10.1136/vr.145.13.362
Boadella M, Vicente J, Ruiz-Fons F, De La Fuente J, Gortázar C (2012) Effects of culling Eurasian wild boar on the prevalence of Mycobacterium bovis and Aujeszky’s disease virus. Prev Vet Med 107:214–221. doi: https://doi.org/10.1016/j.prevetmed.2012.06.001
Briedermann L (2009) Schwarzwild – Neuausgabe bearbeitet von Burkhard Stöcker. Franckh-Kosmos Verlags-GmbH & Co. KG, Stuttgart, p 596
Cano-Manuel FJ, López-Olvera J, Fandos P, Soriguer RC, Pérez JM, Granados JE (2014) Long-term monitoring of ten selected pathogens in wild boar (Sus scrofa) in Sierra Nevada National Park, southern Spain. Vet Microbiol 174:148–154. doi: https://doi.org/10.1016/j.vetmic.2014.06.017
Card JP, Enquist LW (1995) Neurovirulence of pseudorabies virus. Crit Rev Neurobiol 9:137–162
Caruso C, Vitale N, Prato R, Radaelli MC, Zoppi S, Possidente R, Dondo A, Chiavacci L, Moreno Martin AM, Masoero L (2019) Pseudorabies virus in North-West Italian wild boar (Sus scrofa) populations: prevalence and risk factors to support a territorial risk-based surveillance. Vet Ital 54:337–341. doi: https://doi.org/10.12834/VetIt.1006.6613.2
Cay AB, Letellier C (2009) Isolation of Aujeszky’s disease virus from two hunting dogs in Belgium after hunting wild boars. Vlaams Diergeneeskundig Tijdschrift 78:194–195
Closa-Sebastia F, Casas-Diaz E, Cuenca R, Lavin S, Mentaberre G, Marco I (2011) Antibodies to selected pathogens in wild boar (Sus scrofa) from Catalonia (NE Spain). Eur J Wildl Res 57:977–981. doi: https://doi.org/10.1007/s10344-010-0491-9
Davies EB, Beran GW (1981) Influence of environmental factors upon the survival of Aujeszky’s disease virus. Res Vet Sci 31:32–36. doi: https://doi.org/10.1016/S0034-5288(18)32516-5
Dekkers L, Elbers A (2000) Serosurveillance of notifiable veterinary diseases in wild boar in the Netherlands. Tijdschr Diergeneeskd 125:2–4
Denzin N, Conraths FJ, Mettenleiter TC, Freuling CM, Müller T (2020) Monitoring of Pseudorabies in Wild Boar of Germany—A. Spatiotemporal Anal Pathogens 9:276. doi:https://doi.org/10.3390/pathogens9040276
Eggermann J, Theuerkauf J, Pirga B, Milanowski A, Gula R (2013) Stress-hormone levels of wolves in relation to breeding season, pack size, human activity, and prey density. Ann Zool Fennici 50:170–175. doi: https://doi.org/10.5735/086.050.0304
Elbers A, Dekkers L, Van Der Giessen J (2000) Sero-surveillance of wild boar in the Netherlands, 1996–1999. OIE Rev Sci Tech 19:848–854. doi: https://doi.org/10.20506/rst.19.3.1254
Elbers A, Dekkers L, Spek G, Steinbusch L, Van Exsel A (2001) Sero-monitoring of notifiable diseases in wild boar in the Netherlands 1999–2001. Tijdschr Diergeneeskd 126:779–781
Fernández-Llario P, Møller AP (2019) Canine size, condition and health in wild boars. J Zool 309:35–42. doi: https://doi.org/10.1111/jzo.12686
Ferrara G, Longobardi C, D’Ambrosi F, Amoroso MG, D’Alessio N, Damiano S, Ciarcia R, Iovane V, Iovane G, Pagnini U, Montagnaro S (2021) Aujeszky’s Disease in South-Italian Wild Boars (Sus scrofa): A Serological Survey. Animals 11:3298. doi: https://doi.org/10.3390/ani11113298
Freuling CM, Müller TF, Mettenleiter TC (2017) Vaccines against pseudorabies virus (PrV). Vet Microbiol 206:3–9. doi: https://doi.org/10.1016/j.vetmic.2016.11.019
Gortázar C, Vicente J, Fierro Y, Leon L, Cubero MJ, Gonzalez M (2002) Natural Aujeszky’s disease in a Spanish wild boar population. Ann NY Acad Sci 969:210–212. doi: https://doi.org/10.1111/j.1749-6632.2002.tb04380.x
Grubešić M (2006) Uzgojna područja za jelena, divokozu i divlju svinju na području Republike Hrvatske (Breeding areas for red deer, chamois and wild boar on the territory of the Republic of Croatia). Ministry of Agriculture, Forestry and Water Management, Zagreb. (in Croatian)
Güldenpfennig J, Schmicke M, Hoedemaker M, Siebert U, Keuling O (2020) An approach to stress assessment during hunting: Cortisol levels of wild boar (Sus scrofa) during drive hunts. bioRxiv preprint. doi: https://doi.org/10.1101/2020.03.11.987628
Howarth JA (1969) A serologic study of pseudorabies in swine. JAVMA 154:1583–1589
Keros T, Jemeršić L, Brnić D, Prpić J, Dežđek D (2015) Pseudorabies in hunting dogs in Croatia with phylogenetic analysis of detected strains. Vet Rec Case Rep 1:e000181–e000181. doi: https://doi.org/10.1136/vetreccr-2015-000181
Kit S (1999) Pseudorabies virus (Herpesviridae). In: Granoff A, Webster RG (eds) Encyclopedia of Virology. Academic Press, New York, USA, pp 1421–1429
Leuenberger R, Boujon P, Thür B, Miserez R, Garin-Bastuji B, Rüfenacht J, Stärk KDC (2007) Prevalence of classical swine fever, Aujeszky’s disease and brucellosis in a population of wild boar in Switzerland. Vet Rec 160:362–368. doi: https://doi.org/10.1136/vr.160.11.362
Lindberg A (2018) Surveillance of infectious diseases in animals and humans in Sweden 2018. National Veterinary Institute (SVA), Uppsala, Sweden. SVA:s rapportserie 56 ISSN 1654–7098
Lipowski A, Szszotka-Bochniarz A, Pejsak Z (2017) Prevalence of antibodies to Aujeszky’s disease virus in wild boar in Poland, between 2011 and 2014: a retrospective study. J Vet Res 61:397–404. doi: https://doi.org/10.1515/jvetres-2017-0052
Köppel C, Knopf L, Ryser MP, Miserez R, Thür B, Stärk KDC (2007) Serosurveillance for selected infectious disease agents in wild boars (Sus scrofa) and outdoor pigs in Switzerland. Eur J Wildl Res 53:212–220. doi: https://doi.org/10.1007/s10344-006-0080-0
Ma W, Lager KM, Richt JA, Stoffregen WC, Zhou F, Yoon KJ (2008) Development of real-time polymerase chain reaction assays for rapid detection and differentiation of wild-type pseudorabies and gene-deleted vaccine viruses. J Vet Diagn Invest 20:440–447. doi: https://doi.org/10.1177/104063870802000405
Meier RK, Ruiz-Fons F, Ryser-Degiorgis MP (2015) A picture of trends in Aujeszky’s disease virus exposure in wild boar in the Swiss and European contexts. BMC Vet Res 11:277. doi: https://doi.org/10.1186/s12917-015-0592-5
Mengeling WL, Lager KM, Volz DM, Brockmeier SL (1992) Effect of various vaccination procedures on shedding, latency and reactivation of attenuated and virulent pseudorabies virus in swine. Am J Vet Res 53:2164–2173
Merta D, Bobek B, Albrycht M, Furtek J (2015) The age structure and sex ratio in wild boar (Sus scrofa) populations as determined by observations of free-roaming populations and by harvests of collective hunts in southern Poland. Eur J Wildl Res 61:167–170. doi: https://doi.org/10.1007/s10344-014-0867-3
Mettenleiter TC, Ehlers B, Müller T, Yoon KJ, Teifke JP (2012) Herpesviruses. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds) Disease of Swine, 10th edn. Wiley-Blackwell, UK, pp 421–446
Montagnaro S, Sasso S, De Martino L, Longo M, Iovane V, Ghiurmino G, Pisanelli G, Nava D, Baldi L, Pagnini U (2011) Prevalence of antibodies to selected viral and bacterial pathogens in wild boar (Sus scrofa) in Campania region, Italy. J Wildl Dis 46:316–319. doi: https://doi.org/10.7589/0090-3558-46.1.316
Roić B, Jemeršić L, Terzić S, Keros T, Balatinac J, Florijančić T (2012) Prevalence of antibodies to selected viral pathogens in wild boars (Sus scrofa) in Croatia in 2005–2006 and 2009–2010. J Wildl Dis 48:131–137. doi:https://doi.org/10.7589/0090-3558-48.1.131
Ruiz-Fons F, Vicente J, Vidal D, Höfle U, Villanúa D, Gauss C, Segalés J, Almería S, Montoro V, Gortázar C (2006) Seroprevalence of six reproductive pathogens in European wild boar (Sus scrofa) from Spain: The effect on wild boar female reproductive performance. Theriogenol 65:731–743. doi: https://doi.org/10.1016/j.theriogenology.2005.07.001
Ruiz-Fons F, Vidal D, Höfle U, Vicente J, Gortázar C (2007) Aujeszky’s disease virus infection patterns in European wild boar. Vet Microbiol 120:241–250. doi: https://doi.org/10.1016/j.vetmic.2006.11.003
Ruiz-Fons F, Vidal D, Vicente J, Acevedo P, Fernández-de-Mera IG, Montoro V, Gortázar C (2008) Epidemiological risk factors of Aujeszky’s disease in wild boars (Sus scrofa) and domestic pigs in Spain. Eur J Wildl Res 54:549–555. doi: https://doi.org/10.1007/s10344-008-0179-6
Schulze C, Hlinak A, Wohlsein P, Kutzer P, Müller T (2010) Spontaneous Aujeszky’s disease (pseudorabies) in European wild boars (Sus scrofa) in the federal state of Brandenburg, Germany. Berl Munch Tierarztl Wochenschr 123:359–364
Sedlak K, Bartova E, Machova J (2008) Antibodies to selected viral disease agents in wild boars from the Czech Republic. J Wildl Dis 44:777–780. doi: https://doi.org/10.7589/0090-3558-44.3.777
Steinrigl A, Revilla-Fernández S, Kolodziejek J, Wodak E, Bagó Z, Nowotny N, Schmoll F, Köfer J (2012) Detection and molecular characterization of Suid herpesvirus type 1 in Austrian wild boar and hunting dogs. Vet Microbiol 157:276–284. doi: https://doi.org/10.1016/j.vetmic.2011.12.033
Tack J (2018) Wild Boar (Sus scrofa) populations in Europe: a scientific review of population trends and implications for management. European Landowners’ Organization, Brussels, p 56
Thrusfield M (2007) Veterinary Epidemiology, 3rd edn. Blackwell Science Ltd., Oxford, UK
TIBCO Software Inc (2020) Data Science Workbench, version 14. http://tibco.com
Vannier P (1986) Vaccination against Aujeszky’s disease by different routes using live attenuated and inactivated virus vaccines in pigs with or without passive immunity. Zentralbl Veterinarmed B 33:704–712. doi: https://doi.org/10.1111/j.1439-0450.1986.tb00089.x
Vengušt G, Valencak Z, Bidovec A (2006) A serological survey of selected pathogens in wild boar in Slovenia. J Vet Med B Infect Dis Vet Public Health 53:24–27. doi: https://doi.org/10.1111/j.1439-0450.2006.00899.x
Vicente J, León-Vizcaíno L, Gortázar C, Cubero MJ, González M, Martín- Atance P (2002) Antibodies to selected viral and bacterial pathogens in European wild boars from southcentral Spain. J Wildl Dis 38:649–652. doi: https://doi.org/10.7589/0090-3558-38.3.649
Vicente J, Ruiz-Fons F, Vidal D, Höfle U, Acevedo P, Villanúa D, Fernández-de-Mera IG, Martín MP, Gortázar C (2005) Serosurvey of Aujeszky’s disease virus infection in European wild boar in Spain. Vet Rec 156:408–412. doi: https://doi.org/10.1136/vr.156.13.408
Verin R, Varuzza P, Mazzei M, Poli A (2014) Serologic, molecular, and pathologic survey of pseudorabies virus infection in hunted wild boars (Sus scrofa) in Italy. J Wildl Dis 50:559–565. doi: https://doi.org/10.7589/2013-01-004
Zanin E, Capua M, Casaccia C, Zuin A, Moresco A (1997) Isolation and Characterization of Aujeszky’s Disease Virus in Captive Brown Bears from Italy. J Wildl Dis 33:632–634. doi: https://doi.org/10.7589/0090-3558-33.3.632
Župančić Ž, Biuk-Rudan N, Madić J, Grabarević Ž (1992) Aujeszky’s disease in hunting dogs in Croatia. Praxis Vet 40:175–178 (in Croatian)
Župančić Ž, Jukić B, Lojkić M, Čač Ž, Jemeršić L, Starešina V (2002) Prevalence of antibodies to classical swine fever, Aujeszky’s disease, porcine reproductive and respiratory syndrome and bovine viral diarrhoea viruses in wild boar in Croatia. J Vet Med B Infect Dis Vet Public Health 49:253–256. doi: https://doi.org/10.1046/j.1439-0450.2002.00562.x
Acknowledgements
Authors would like to thank Croatian Forests and hunting associations for their help during the sampling period.
Funding
This study received no external funding.
Author information
Authors and Affiliations
Contributions
DK made study design, wrote first draft of the manuscript; IS and MB performed field work; TK, JP and LJ performed laboratory work; KK, NT, LjB and DK analyzed data, all authors contributed to the final version of the manuscript and approved it.
Corresponding author
Ethics declarations
Declarations
Study was ethically approved by the Committee for Ethics in Veterinary Medicine, Veterinary Faculty University of Zagreb (Class: 640-01/20 − 17/02; No.: 251-61-44-20-11). All samples were obtained following regular game management operations, and no animals were killed for the purpose of this study.
Competing interests
The authors declare that they have no competing interests.
Consent to participate
All authors agreed with participation in this study.
Consent for publication
All authors agree with the publication of the manuscript.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Konjević, D., Sučec, I., Turk, N. et al. Epidemiology of Aujeszky disease in wild boars (Sus scrofa L.) in Croatia. Vet Res Commun 47, 631–639 (2023). https://doi.org/10.1007/s11259-022-10017-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-022-10017-6