Original Scientific Article
Prevalence of Toxoplasma gondii and potentially zoonotic helminths in wild boars (Sus scrofa) hunted in central Italy
Roberto Amerigo Papini
*
,
Sara Vannucci
,
Guido Rocchigiani
,
Simona Nardoni
,
Francesca Mancianti
Abstract
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.
Keywords: Toxoplasma gondii, prevalence, wild boars, zoonotic helminthiases, Italy
References
2. Santilli, F., Varuzza, P. (2013). Factors affecting wild boar (Sus scrofa) abundance in southern Tuscany. HYSTRIX 24 (2):169-173.
3. 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. https://doi.org/10.1002/ps.3965 PMid:25512181
4. 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.
https://doi.org/10.1007/s13593-011-0057-6
5. Massei, G., Genov, P. V. (2004). The environmental impact of wild boar. Galemys 16 (1):135-145.
6. 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. https://doi.org/10.1016/j.aap.2013.07.032 PMid:24056283
7. 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.
https://doi.org/10.1016/j.wem.2011.06.005 PMid:21962050
9. 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. https://doi.org/10.1098/rstb.2009.0086 PMid:196⇿9 PMCid:PMC2⇊94
11. 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. https://doi.org/10.1016/j.vetpar.2017.07.013 PMid:28917302
12. 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. https://doi.org/10.1051/parasite/2013048 PMid:24280567 PMCid:PMC3841837
13. 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.
14. 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.
15. 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
16. 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
18. 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. https://doi.org/10.1016/j.vetpar.2009.06.014 PMid:19592170
19. 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
20. 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. https://doi.org/10.1017/S0031182009991065 PMid:19765337
21. Sloss, M. W., Kemp, R. L. (1978). Veterinary clinical parasitology. Fifth Edition. Iowa State University Press, Ames, Iowa.
22. Casarosa, L. (1986). Parassitologia degli animali domestici. Casa Editrice Ambrosiana, Milano. PMid:3802571 PMCid:PMC1542647
23. 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. https://doi.org/10.1016/j.ecolecon.2014.06.018
25. West, B. C., Cooper, A. L., Armstrong, J. B. (2009). Managing wild pigs:A technical guide. Human-Wildlife Interactions Monograph 1, 1–55.
26. 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. https://doi.org/10.1086/593702 PMid:9129105
27. 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. https://doi.org/10.4315/0362-028X.JFP-13-285 PMid:24680078
28. 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. https://doi.org/10.1093/oxfordjournals.aje.a112177 PMid:1200023
29. 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. https://doi.org/10.1186/1756-3305-7-196 PMid:24766665 PMCid:PMC4012061
30. 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. https://doi.org/10.7589/2013-09-233 PMid:25375939
31. 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. https://doi.org/10.1016/j.vetpar.2017.06.013 PMid:28807281
32. 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.
https://doi.org/10.1051/parasite/2014007 PMid:24534616 PMCid:PMC3927306
33. Puvanesuaran, V. R., Noordin, R., Balakrishnan, V. (2013). Genotyping of Toxoplasma gondii isolates from wild boars in Peninsular Malaysia. PLoS ONE 8 (4):e61730.
https://doi.org/10.1371/journal.pone.0061730 PMid:23613920 PMCid:PMC3629149
34. 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.
35. 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.
36. 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. https://doi.org/10.1186/s40462-017-0105-1 PMid:2↶712 PMCid:PMC5471724
37. Foata, J., Culioli, J.-L., Marchand, B. (2005). Helminth fauna of wild boar in Corsica. Acta Parasitol. 50 (2):168-170.
39. 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. https://doi.org/10.1017/S0022149X08936191 PMid:18328113
40. 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.
41. 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. https://doi.org/10.1016/j.vetpar.2015.02.006 PMid:25725547
42. 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. https://doi.org/10.3347/kjp.2012.50.3.239 PMid:22949753 PMCid:PMC3428571
45. 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. https://doi.org/10.1128/JCM.43.3.1142-1148.2005 PMid:15750075 PMCid:PMC1081283
46. 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
47. Bendall, R. P., Barlow, M., Betson, M., Stohard, J. R., Nejsum, P. (2011). Zoonotic ascariasis, United Kingdom. Emerg Infect Dis. 17 (10):1964-1966.
https://doi.org/10.3201/eid1710.101826 PMid:22000387 PMCid:PMC3310658
49. 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. https://doi.org/10.1093/infdis/jiu193 PMid:24688073 PMCid:PMC4136802
50. 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. https://doi.org/10.1007/s00436-015-4857-5 PMid:26637313
51. 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. https://doi.org/10.1007/s10096-011-1170-9 PMid:21365288
52. 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.
https://doi.org/10.1186/1756-3305-5-42 PMid:22348306 PMCid:PMC3293767
53. 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
55. 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.
https://doi.org/10.1016/j.vetpar.2006.06.024 PMid:16899340
56. 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. https://doi.org/10.2478/s11687-006-0017-x
58. 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. https://doi.org/10.4269/ajtmh.1965.14.774 PMid:5829134
59. 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
60. 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. https://doi.org/10.1080/00034983.1983.11811681 PMid:6882052
61. 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
62. 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. https://doi.org/10.1079/JOH2003168 PMid:12895286
63. 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. https://doi.org/10.1017/S0022149X12000193 PMid:22423595
64. 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. https://doi.org/10.1053/j.gastro.2005.01.005 PMid:15825065
65. 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. https://doi.org/10.1136/gut.2004.041749 PMid:15591509 PMCid:PMC1774382
66. 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. https://doi.org/10.1016/j.jaci.2009.08.006 PMid:19800680
67. 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. https://doi.org/10.4269/ajtmh.16-0247 PMid:27382078 PMCid:PMC5062791
Copyright
©2018 Papini R.A. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Acknowledgement
The authors would like to thank all the wild boar hunting teams for their important contribution and the University of Pisa for providing financial support to carry out this survey.
Conflict of Interest Statement
The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.
Citation Information
Macedonian Veterinary Review. Volume 41, Issue 1, Pages 83-93, p-ISSN 1409-7621, e-ISSN 1857-7415,DOI: 10. 2478/macvetrev-2018-0012, 2018