ORIGINAL_ARTICLE Our aim was to evaluate the risk of human toxoplasmosis via meat consumption from wild boars by estimating the seroprevalence of Toxoplasma gondii in animals hunted in central Italy. Using a modified agglutination test, 213 sera from wild boars were examined for anti-Toxoplasma IgG antibodies. Diaphragm samples (n=65) from seropositive and seronegative animals were tested by nested-PCR to detect T. gondii DNA. Toxoplasma DNA from diaphragms was genotyped by PCR-RFLP using 12 genetic markers. Moreover, the aim of the study was also to identify helminth infections of wild boars in the selected area and to evaluate their hazard for humans. Examination of sera revealed a seroprevalence of 12.2%. Only one T. gondii strain could be genotyped from a seropositive animal and PCR-RFLP revealed that it belonged to type II. Analysis of 50 samples of faeces and 32 small intestines revealed that 78% and 15.6% of the samples harboured parasites, respectively, with the occurrence of parasites potentially dangerous for humans. These latter included Ascaris suum, Macracanthorhynchus hirudinaceus, Trichuris suis, and Metastrongylus spp. A significant association was found between coprological positivity and male sex. These results indicate that T. gondii infection may be present in wild boar tissues and consumption of undercooked or raw wild boar meat may expose humans to risk of toxoplasmosis in the study area. Furthermore, the study highlights that wild boars are hosts of helminths of veterinary and medical importance transmissible to pigs and humans. https://macvetrev.mk/Files/Article/2020/10. 2478/macvetrev-2018-0012/macvetrev-2018-0012.pdf 2018-03-15T09:00:00 83 93 10.2478/macvetrev-2018-0012 Toxoplasma gondii prevalence wild boars zoonotic helminthiases Italy Roberto Amerigo Papini roberto.amerigo.papini@unipi.it false 1 Department of Veterinary Sciences, Viale delle Piagge 2, 56124 Pisa, Italy LEAD_AUTHOR Sara Vannucci false 2 Department of Veterinary Sciences, Viale delle Piagge 2, 56124 Pisa, Italy AUTHOR Guido Rocchigiani false 3 Department of Veterinary Sciences, Viale delle Piagge 2, 56124 Pisa, Italy AUTHOR Simona Nardoni false 4 Department of Veterinary Sciences, Viale delle Piagge 2, 56124 Pisa, Italy AUTHOR Francesca Mancianti false 5 Department of Veterinary Sciences, Viale delle Piagge 2, 56124 Pisa, Italy AUTHOR Behavior and Biology of Wild Pigs. [Internet]. Available on line at http://wildpiginfo.msstate.edu/behavior-feral-pigs.html  (last access on September 20, 2017) 1 Santilli, F., Varuzza, P. (2013). Factors affecting wild boar (Sus scrofa) abundance in southern Tuscany. HYSTRIX 24 (2):169-173. 2 Massei, G., Kindberg, J., Licoppe, A., Gačić, D., Šprem, N., Kamler, J., et al. (2015). Wild boar populations up, numbers of hunters down?A review of trends and implications for Europe. Pest Manag Sci. 71 (4):492-500. PMid:25512181 3 10.1002/ps.3965 Amici, A., Serrani, F., Rossi, C. M., Primi, R. (2012). Increase in crop damage caused by wild boar (Sus scrofa L.):the “refuge effect“. Agron Sustain Dev. 32 (3):683-692. 4 10.1007/s13593-011-0057-6 Massei, G., Genov, P. V. (2004). The environmental impact of wild boar. Galemys 16 (1):135-145. 5 Rodríguez-Morales, B., Díaz-Varela, E. R., Marey-Pérez, M. F. (2013). Spatiotemporal analysis of vehicle collisions involving wild boar and roe deer in NW Spain. Accid Anal Prev. 60, 121-123. PMid:24056283 6 10.1016/j.aap.2013.07.032 Kose, O., Guler, F., Baz, A. B., Akalin, S., Turan, A. (2011). Management of a wild boar wound:a case report. Wilderness Environ Med. 22 (3):242-245. PMid:21962050 7 10.1016/j.wem.2011.06.005 Manipady, S., Menezes, R. G., Bastia, B. K. (2006). Death by attack from a wild boar. J Clin Forensic Med. 13 (2):89-91. PMid:16263321 8 10.1016/j.jcfm.2005.08.007 Meng, X. J., Lindsay, D. S., Sriranganathan, N. (2009). Wild boars as sources for infectious diseases in livestock and humans. Philos Trans R Soc Lond B Biol Sci. 364 (1530):2697-2707. PMid:196⇿9 PMCid:PMC2⇊94 9 10.1098/rstb.2009.0086 Tenter, A. M., Heckeroth, A.R., Weiss, L. M. (2000). Toxoplasma gondii:from animals to humans. Int J Parasitol. 30 (12-13):1217-1258. 10 10.1016/S0020-7519(00)00124-7 Rostami, A., Riahi, S. M., Fakhri, Y., Saber, V., Hanifehpour, H., Valizadeh, S., Gholizadeh, M., Pouya, R. H., Gamble, H. R. (2017). The global seroprevalence of Toxoplasma gondii among wild boars:A systematic review and meta-analysis. Vet Parasitol. 244, 12-20. PMid:28917302 11 10.1016/j.vetpar.2017.07.013 Ranucci, D., Veronesi, F., Moretti, A., Branciari, R., Miraglia, D., Manfredi, M. T., Piergili Fioretti, D. (2013). Seroprevalence of Toxoplasma gondii in wild boars (Sus scrofa) from central Italy. Parasite 20, 48. PMid:24280567 PMCid:PMC3841837 12 10.1051/parasite/2013048 Moretta I., Veronesi, F., Di Paola, R., Battistacci, L., Moretti, A. (2011). Indagine parassitologica in cinghiali (Sus scrofa) cacciati nella stagione venatoria 2009-2010 in Umbria (Italia centrale). Large Anim Rev. 17, 187-192. 13 Cahill, S., Llimona, F., Caba-eros, L., Calomardo, F. (2012). Characteristics of wild boar (Sus scrofa) habituation to urban areas in the Collserola Natural Park (Barcelona) and comparison with other locations. Anim Biodivers Conserv. 35 (2):221–233. 14 Mizgajska-Wiktor, H., Jarosz, W. (2010). Potential risk of zoonotic infections in recreational areas visited by Sus scrofa and Vulpes vulpes. Case study –Wolin Island, Poland. Wiad Parazytol. 56 (3):243–251. PMid:21174955 15 Bojar, H., Kłapeć, T. (2012). Contamination of soil with eggs of geohelminths in recreational areas in the Lublin region of Poland. Ann Agric Environ Med. 19 (2):267-270. PMid:22742799 16 Matschke, G. H. (1967). Aging European wild hogs by dentition. J Wildl Manage. 31 (1):109–113. 17 10.2307/3798365 Richomme, C., Aubert, D., Gilot-Fromont, E., Ajzenberg, D., Mercier, A., Ducrot, C., Ferté, H., Delorme, D., Villena, I. (2009). Genetic characterization of Toxoplasma gondii from wild boar (Sus scrofa) in France. Vet Parasitol. 164 (2-4):296-300. PMid:19592170 18 10.1016/j.vetpar.2009.06.014 Jones, C. D., Okhravi, N., Adamson, P., Tasker, S., Lightman, S. (2000). Comparison of PCR detection methods for B1, P30, and 18S rDNA genes of T. gondii in aqueous humor. Invest Ophthalmol Vis Sci. 41 (3):634-644. PMid:10711675 19 Su, C., Shwab, E. K., Zhou, P., Zhu, X. Q., Dubey, J. P. (2010). Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 137 (1):1-11. PMid:19765337 20 10.1017/S0031182009991065 Sloss, M. W., Kemp, R. L. (1978). Veterinary clinical parasitology. Fifth Edition. Iowa State University Press, Ames, Iowa. 21 Casarosa, L. (1986). Parassitologia degli animali domestici. Casa Editrice Ambrosiana, Milano. PMid:3802571 PMCid:PMC1542647 22 Schulp, C. J. E., Thuiller, W., Verburg, P. H. (2014). Wild food in Europe:A synthesis of knowledge and data of terrestrial wild food as an ecosystem service. Ecol Econon. 105, 292-305. 23 10.1016/j.ecolecon.2014.06.018 Sales, J., Kotrba, R. (2013). Meat from wild boar (Sus scrofa L.):a review. Meat Sci 94(2):187–201. PMid:23501250 24 10.1016/j.meatsci.2013.01.012 West, B. C., Cooper, A. L., Armstrong, J. B. (2009). Managing wild pigs:A technical guide. Human-Wildlife Interactions Monograph 1, 1–55. 25 Choi, W. Y., Nam, H. W., Kwak, N. H., Huh, W., Kim, Y. R., Kang, M. W., Cho, S. Y., Dubey, J. P. (1997). Foodborne outbreaks of human toxoplasmosis. J Infect Dis. 175 (5):1280-1282. PMid:9129105 26 10.1086/593702 Vitale, M., Tumino, G., Partanna, S., La Chiusa, S., Mancuso, G., Giglia, M. L., Presti, V. D. (2014). Impact of traditional practices on food safety:a case of acute toxoplasmosis related to the consumption of contaminated raw pork sausage in Italy. J Food Prot. 77 (4):643-646. PMid:24680078 27 10.4315/0362-028X.JFP-13-285 Riemann, H. P., Brant, P. C., Behymer, D., E., Franti, C., E. (1975). Toxoplasma gondii and Coxiella burneti antibodies among Brazilian slaughterhouse employees. Am J Epidemiol. 102 (5):386-393. PMid:1200023 28 10.1093/oxfordjournals.aje.a112177 Ferroglio, E., Bosio, F., Trisciuoglio, A., Zanet, S. (2014). Toxoplasma gondii in sympatric wild herbivores and carnivores:epidemiology of infection in Western Alps. Parasit Vectors. 7, 196. PMid:24766665 PMCid:PMC4012061 29 10.1186/1756-3305-7-196 Calero-Bernal, R., Saugar, J. M., Fronters, E., Pérez-Martín, J. E., Habela, M. A., Serrano, F. J., Reina, D., Fuentes, I. (2015). Prevalence and genotype identification of Toxoplasma gondii in wild animals form southwestern Spain. J Wildl Dis. 51 (1):233-238. PMid:25375939 30 10.7589/2013-09-233 Vismarra, A., Barilli, E., Miceli, M., Mangia, C., Genchi, M., Brindani, F., Kramer, L., Bacci, C. (2017). Toxoplasma gondii in the Cornigliese sheep breed in Italy:Meat juice serology, in vitro isolation and genotyping. Vet Parasitol. 243, 125-129. PMid:28807281 31 10.1016/j.vetpar.2017.06.013 Chessa, G., Chisu, V., Porcu, R., Masala, G. (2014). Molecular characterization of Toxoplasma gondii type II in sheep abortion in Sardinia, Italy. Parasite 21, 6. PMid:24534616 PMCid:PMC3927306 32 10.1051/parasite/2014007 Puvanesuaran, V. R., Noordin, R., Balakrishnan, V. (2013). Genotyping of Toxoplasma gondii isolates from wild boars in Peninsular Malaysia. PLoS ONE 8 (4):e61730. PMid:23613920 PMCid:PMC3629149 33 10.1371/journal.pone.0061730 Sarkari, B., Yaghoobi, K., Mansouri, M., Asgari, Q., Abdolahi, S. (2017). Seroprevalence and genotyping of Toxoplasma gondii in wild boars (Sus scrofa) from Southwestern Iran. Jundishapur J Microbiol. 10 (1):e39516. 34 Popiolek, M., Knechi, D., Szczęsna-Staśkiewicz, J., Czerwińska-Rożalow, A. (2010). Helminths of the wild boar (Sus scrofa L.) in natural and breeding conditions. Bull Vet Inst Pulawy. 54, 161-166. 35 Shannon, L. K., Fischer, J. W., Monaghan, A. J., Beasley, J. C., Boughton, R., Campbell, T. A., et al. (2017). Quantifying drivers of wild pig movement across multiple spatial and temporal scales. Mov Ecol. 5, 14. PMid:2↶712 PMCid:PMC5471724 36 10.1186/s40462-017-0105-1 Foata, J., Culioli, J.-L., Marchand, B. (2005). Helminth fauna of wild boar in Corsica. Acta Parasitol. 50 (2):168-170. 37 de-la Muela, N., Hernández-de-Luján, S., Ferre, I. (2001). Helminths of wild boar in Spain. J Wildl Dis. 37 (4):840-843. PMid:11763752 38 10.7589/0090-3558-37.4.840 Sato, H., Suzuki, K., Yokoyama, M. (2008). Visceral helminths of wild boars (Sus scrofa leucomystax) in Japan, with special reference to a new species of the genus Morgascaridia Inglis, 1958 (Nematoda:Schneidernematidae). J Helminthol. 82 (2):159-168. PMid:18328113 39 10.1017/S0022149X08936191 Magi, M., Bertani, M., Dell'Omodarme, M., Prati, M.C. (2005). Necropsy and coprology in wild boar (Sus scrofa) in Livorno Mountain Park (Tuscany, central Italy). Parassitologia 46 (3):311-313. 40 Gassó, D., Feliu, C., Ferrer, D., Mentaberre, G., Casas-Díaz, E., Velarde, R., et al. (2015). Uses and limitations of faecal egg count for assessing worm burden in wild boars. Vet Parasitol. 209 (1-2):133-137. PMid:25725547 41 10.1016/j.vetpar.2015.02.006 Kim, M.-K., Pyo, K.-H., Hwang, Y.-S., Park, K. H., Hwang, I. G., Chai, J.-Y., Shin, E.-H. (2012). Effect of temperature on embryonation of Ascaris suum eggs in an environmental chamber. Korean J Parasitol. 50 (3):239-242. PMid:22949753 PMCid:PMC3428571 42 10.3347/kjp.2012.50.3.239 Roepstorff, A., Grønvold, J., Larsen, M. N., Kraglund, H.-O., Fagerholm, H.-P. (2002). The earthworm Lumbricus terrestris as a possible paratenic or intermediate host of the pig parasite Ascaris suum. Comp Parasitol. 69 (2):206-210. 43 10.1654/1525-2647(2002)069[0206:TELTAA]2.0.|aCO;2 Nichols, E., Gómez, A. (2014). Dung beetles and fecal helminth transmission:patterns, mechanisms and questions. Parasitology 141 (5):614–623. PMid:24476794 44 10.1017/S0031182013002011 Nejsum, P., Parker, E. D. Jr., Frydenberg, J., Roepstorff, A., Boes, J., Haque, R., Astrup, I., Prag, J. (2005). Ascariasis is a zoonosis in Denmark. J Clin Microbiol. 43 (3):1142-1148. PMid:15750075 PMCid:PMC1081283 45 10.1128/JCM.43.3.1142-1148.2005 Arizono, N., Yoshimura, Y., Tohzaka, N., Yamada, M., Tegoshi, T., Onishi, K., Uchikawa, R. (2010). Ascariasis in Japan:is pig-derived Ascaris infecting humans?Jpn J Infect Dis. 63 (6):447-448. PMid:21099099 46 Bendall, R. P., Barlow, M., Betson, M., Stohard, J. R., Nejsum, P. (2011). Zoonotic ascariasis, United Kingdom. Emerg Infect Dis. 17 (10):1964-1966. PMid:22000387 PMCid:PMC3310658 47 10.3201/eid1710.101826 Zhou, C., Li, M., Yuan, K., Deng, S., Peng, W. (2012). Pig Ascaris:an important source of ascariasis in China. Infect Genet Evol. 12 (6):1172-1177. PMid:22561394 48 10.1016/j.meegid.2012.04.016 Betson, M., Nejsum, P., Bendall, R. P., Deb, R. M., Stohard, J. R. (2014). Molecular epidemiology of ascariasis:a global perspective on the transmission dynamics of Ascaris in people and pigs. J Infect Dis. 210 (6):932-941. PMid:24688073 PMCid:PMC4136802 49 10.1093/infdis/jiu193 Schneider, R., Auer, H. (2016). Incidence of Ascaris suum-specific antibodies in Austrian patients with suspected larva migrans visceralis (VLM) syndrome. Parasitol Res. 115 (3):1213–1219. PMid:26637313 50 10.1007/s00436-015-4857-5 Pinelli, E., Herremans, T., Harms, M. G., Hoek, D., Kortbeek, L. M. (2011). Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands:trends from 1998 to 2009. Eur J Clin Microbiol Infect Dis. 30 (7):873-879. PMid:21365288 51 10.1007/s10096-011-1170-9 Leles, D., Gardner, G. L., Reinhard, K., I-iguez, A., Araujo, A. (2012). Are Ascaris lumbricoides and Ascaris suum a single species?Parasit Vectors 5, 42. PMid:22348306 PMCid:PMC3293767 52 10.1186/1756-3305-5-42 Dutto, M., Petrosillo, N. (2013). Hybrid Ascaris suum/lumbricoides (Ascarididae) infestation in a pig farmer:a rare case of zoonotic ascariasis. Cent Eur J Public Health. 21 (4) :224–226. PMid:24592729 53 Notes from the field:ascariasis associated with pig farming —Maine, 2010–2013. Available on line at http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6220a6.htm (last access on September 20, 2017). 54 Dalimi, A., Sattari, A., Motamedi, Gh. (2006). A study on intestinal helminths of dogs, foxes and jackals in the western part of Iran. Vet Parasitol. 142 (1-2):129-133. PMid:16899340 55 10.1016/j.vetpar.2006.06.024 Mowlavi, G. R., Massoud, J., Mobedi, I., Solaymani-Mohammadi. S., Gharagozlou, M. J., Mas-Coma, S. (2006). Very highly prevalent Macracanthorhynchus hirudinaceus infection of wild boar Sus scrofa in Khuzestan province, south-western Iran. Helminthologia 43 (2):86-91. 56 10.2478/s11687-006-0017-x Eslami, A., Farsad-Hamdi, S. (1992). Helminth parasites of wild boar, Sus scrofa, in Iran. J Wildl Dis. 28 (2):316-318. PMid:1602589 57 10.7589/0090-3558-28.2.316 Pradatsundarasar, A., Pechranond, K. (1965). Human infection with the acanthocephalan Macracanthorhynchus hirudinaceus in Bangkog:report of a case. Am J Trop Med Hyg. 14 (5):774-776. PMid:5829134 58 10.4269/ajtmh.1965.14.774 Radomyos, P., Chobchuanchom, A., Tungtrongchitr, A. (1989). Intestinal perforation due to Macracanthorhynchus hirudinaceus infection in Thailand. Trop Med Parasit. 40 (4):476-477. PMid:2623433 59 Leng, Y. J., Huang, W. D., Liang, P. N. (1983). Human infection with Macracanthorhynchus hirudinaceus Travassos, 1916 in Guangdong province, with notes on its prevalence in China. Ann Trop Med Parasitol. 77 (1):107-109. PMid:6882052 60 10.1080/00034983.1983.11811681 Beer, R. J. (1976). The relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of the pig. Res Vet Sci. 20 (1):47-54. PMid:1257627 61 Solaymani - Mohammadi, S., Mobedi, I., Rezaian, M., Massoud, J., Mohebali, M., Hooshyar, H., Ashrafi, K., Rokni, M. B. (2003). Helminth parasites of the wild boar, Sus scrofa, in Luristan province, western Iran and their public health significance. J Helminthol. 77 (3):263-267. PMid:12895286 62 10.1079/JOH2003168 Nejsum, P., Betson, M., Bendall, R. P., Thamsborg, S. M. (2012). Assessing the zoonotic potential of Ascaris suum and Trichuris suis:looking to the future from an analysis of the past. J Helminthol. 86 (2):148-155. PMid:22423595 63 10.1017/S0022149X12000193 Summers R.W., Elliott, D. E., Urban, J. F. Jr, Thompson, R. A., Weinstock, J. V. (2005). Trichuris suis therapy for active ulcerative colitis:a randomized controlled trial. Gastroenterology 128(4):825-832. PMid:15825065 64 10.1053/j.gastro.2005.01.005 Summers, R. W., Elliott, D. E., Urban, J. F. Jr, Thompson, R., Weinstock, J. V. (2005). Trichuris suis therapy in Crohn's disease. Gut 54 (1):87-90. PMid:15591509 PMCid:PMC1774382 65 10.1136/gut.2004.041749 Bager, P., Arnved, J., Renborg, S., Wohlfhart, J., Poulsen, L. K., Westergaard, T., et al. (2010). Trichuris suis ova therapy for allergic rhinitis:a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol. 125 (1):123-130. PMid:19800680 66 10.1016/j.jaci.2009.08.006 Calvopina, M., Caballero, H., Morita, T. Korenaga, M. (2016). Case report:human pulmonary Infection by the zoonotic Metastrongylus salmi nematode. The First reported case in the Americas. Am J Trop Med Hyg. 95 (4):871-873. PMid:27382078 PMCid:PMC5062791 67 10.4269/ajtmh.16-0247