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Cystic echinococcosis and other helminth infections of wild boar in northeastern and northwestern regions of Tunisia

Published online by Cambridge University Press:  20 June 2019

Samia Lahmar Open the ORCID record for Samia Lahmar [Opens in a new window] ,
Paul R. Torgerson ,
Hana Mhemmed ,
Lamia Tizaoui ,
Néjib Mhadhbi ,
Abdelkader Bani ,
Hanan Driss ,
Nébiha Ghrissi ,
Manel Makhzoumi  and
Amel Ben Houidi
...Show all authors
Samia Lahmar*
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Paul R. Torgerson
Affiliation:
Section of Epidemiology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland
Hana Mhemmed
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Lamia Tizaoui
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Néjib Mhadhbi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Abdelkader Bani
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Hanan Driss
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Nébiha Ghrissi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Manel Makhzoumi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Amel Ben Houidi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Mokhtar Dhibi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Yousra Said
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, 2020 Sidi Thabet, Tunisia
Edoardo Pozio
Affiliation:
Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy
Belgees Boufana
Affiliation:
National Wildlife Management Centre, National Reference Laboratory for Trichinella and Echinococcus, Animal and Plant Health Agency, York, UK
*
Author for correspondence: Samia Lahmar, E-mail: [email protected]
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Abstract

This study identified helminth species of wild boar (Sus scrofa) originating from northeastern and northwestern regions of Tunisia using 297 lungs, 297 livers, 264 intestinal tracts, 120 samples of muscle tissue (tongue, masseter, diaphragm, inter-costal) and 232 faecal samples derived from a total of 591 animals. Host gender was registered for the lung and liver wild boar group, which included 163 males and 134 females. All animals, excluding those used to retrieve muscular samples, were classified into three age classes, <2 (n = 212), 2–3 (n = 208) and ⩾4 years old (n = 141). Helminth fauna of the examined wild boar included 14 parasite species: one trematode (adult, Brachylaemus suis), three cestodes (metacestodes of Echinococcus granulosus, Taenia hydatigena cysticercus, adult, Hymenolepis diminuta), nine nematodes (adults of Metastrongylus apri, Metastrongylus pudendotectus, Ascarops strongylina, Globocephalus urosubulatus, Physocephalus sexalatus, Gnathostoma hispidum, Gongylonema pulchrum and eggs of Strongyloides ransoni and Capillaria spp.) and one acanthocephalan (adult, Macracanthorhynchus hirudinaceus). Trichinella larvae were not recovered from any of the 30 wild boar examined. Results showed a 73.5% global prevalence of infection with visceral helminths, 67.3% of which were lung and hepatic infections and 80.3% of helminths were recovered from the gastrointestinal tract. The most prevalent parasite was M. hirudinaceus (61.7%) while the highest intensity of infection was observed for Metastrongylus spp. The most prevalent cestode was E. granulosus (18.9%). This is the first detailed study on helminth infections of wild boar from a North African country.

Keywords

EpidemiologyhelminthsnecropsySus scrofaTunisia
Type
Research Article
Information
Parasitology , Volume 146 , Issue 10 , September 2019 , pp. 1263 - 1274
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Copyright
Copyright © Cambridge University Press 2019 

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References

Anderson, RC (1992) Nematode Parasites of Vertebrates: Their Development and Transmission, 1st Edn. Wallingford, UK: CAB International University Press, 358–359.Google Scholar
Beaver, PC, Jung, RC and Cupp, EW (1984) Clinical Parasitology, 9th Edn. Philadelphia, PA: Lea and Febiger, 291–292.Google Scholar
Bentounsi, B, Meradi, S, Ayachi, A and Cabaret, J (2009) Cestodes of untreated large stray dog populations in Algeria: a reservoir for herbivore and human parasitic diseases. Open Veterinary Sciences and Journal 3, 64–67.Google Scholar
Boufana, B, Lahmar, S, Rebaï, W, Ben Safta, Z, Jebabli, L, Ammar, A, Kachti, M, Aouadi, S and Craig, PS (2014) Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 706–714. https://doi.org/10.1093/trstmh/tru138.Google Scholar
Boufana, B, Said, Y, Dhibi, M, Craig, PS and Lahmar, S (2015) Echinococcus granulosus sensu stricto (s.s.) from the critically endangered antelope Addax nasomaculatus in Tunisia. Acta Tropica 152, 112–115. https://doi.org/10.1016/j.actatropica.2015.08.015.Google Scholar
Calvopina, M, Caballero, H, Morita, T and Korenag, M (2016) Case report: human pulmonary infection by the zoonotic Metastrongylus salmi nematode. The first reported case in the Americas Manuel. The American Society of Tropical Medicine and Hygiene 95, 871–873.Google Scholar
Chahed, MK, Bellali, H, Ben Alaya, N, Aoun, K and Zouari, B (2015) High risk areas for echinococcosis-hydatidosis in Tunisia. La Tunisie Médicale 93, 33–37.Google Scholar
Chaisiri, K, Aueawiboonsri, S, Kusolsuk, T, Dekumyoy, P, Sanguankiat, S, Homsuwan, N, Peunpipoom, G, Okamoto, M, Yanagida, T, Sako, Y and Ito, A (2017) Gastrointestinal helminths and Taenia spp. In parenteral tissues of free-roaming pigs (Sus scrofa indicus) from hill-tribe village at the western border of Thailand. Tropical Biomedicine 34, 464–470.Google Scholar
da Silva, D and Müller, G (2013) Parasites of the respiratory tract of Sus scrofa scrofa (wild boar) from commercial breeder in southern Brazil and its relationship with Ascaris suum. Parasitology Research 112, 1353–1356.Google Scholar
EFSA (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA Journal 15, 5077.Google Scholar
Eslami, A and Farsad-Hamdi, S (1992) Helminth parasites of wild boar, Sus scrofa, in Iran. Journal of Wildlife Diseases 28, 316–318.Google Scholar
Fassbender, CP and Mayer, P (1974) Uber die verteilung von Trichinella spiralis in der Mushulatur einiger nordafrikanischer Carnivoren. Deutsche Tierarztliche Wochenschrif 81, 284–287.Google Scholar
Foata, J, Culioli, JL and Marchand, B (2005) Helminth fauna of wild boar in Corsica. Acta Parasitologica 50, 168–170.Google Scholar
Fredriksson-Ahomaa, M (2018) Wild boar: a reservoir of foodborne zoonoses. Foodborne Pathogens and Disease 16, 153–165. doi: 10.1089/fpd.2018.2512.Google Scholar
Gamble, HR, Bessonov, AS, Cuperlovic, K, Gajadhar, AA, van Knapen, E, Noeckler, K, Schenone, H and Zhu, X (2000) International commission on trichinellosis: recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Veterinary Parasitology 93, 393–408.Google Scholar
García-González, AM, Pérez-Martín, JE, Gamito-Santos, JA, Calero-Bernal, R, Alcaide Alonso, M and Frontera Carrión, EM (2013) Epidemiologic study of lung parasites (Metastrongylus spp.) in wild boar (Sus scrofa) in southwestern Spain. Journal of Wildlife Diseases 49, 157–162. https://doi.org/10.7589/2011-07-217.Google Scholar
Gassó, D, Rossi, L, Mentaberre, G, Casas, E, Velarde, R, Nosal, P, Serrano, E, Segales, J, Fernandez-Llario, P and Feliu, C (2014) An identification key for the five most common species of Metastrongylus. Parasitology Research 113, 3495–3500. https://doi.10.1007/s00436-014-4001-y.Google Scholar
Gassó, D, Feliu, C, Ferrer, D, Mentaberre, G, Casas-Díaz, E, Velarde, R, Fernández-Aguilar, X, Colom-Cadena, A, Navarro-Gonzalez, N, López-Olvera, JR, Lavín, S, Fenández-Llario, P, Segalés, J and Serrano, E (2015) Uses and limitations of faecal egg count for assessing worm burden in wild boars. Veterinary Parasitology 209, 133–137. https://doi.org/10.1016/j.vetpar.2015.02.006.Google Scholar
Georgi, JR and McCulloch, CE (1989) Diagnostic morphometry: Identification of helminth eggs by discriminant analysis of morphometric data. Proceedings of The Helminthological Society of Washington 56, 44–57.Google Scholar
Humbert, JF and Henry, C (1989) Studies on the prevalence and the transmission of lung and stomach nematodes of the wild boar (Sus scrofa) in France. Journal of Wildlife Diseases 25, 335–341. https://doi.org/10.7589/0090-3558-25.3.335.Google Scholar
Järvis, T, Kapel, CH, Moks, E, Talvik, H and Mägi, E (2007) Helminths of wild boar in the isolated population close to the northern border of its habitat area. Veterinary Parasitology 150, 366–369.Google Scholar
Joly, DO and Messier, F (2004) The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves? Oecologia 140, 586–590.Google Scholar
Karem, A, Triplet, P and Lartiges, A (2009) Faune sauvage de Tunisie: écotourisme, chasse et développement communautaire. Ministère de l'Agriculture et des Ressources Hydrauliques, Direction Générale des Forêts, 128 p.Google Scholar
Khalil, LF, Jones, A and Bray, RA (1994) Keys to the Cestode Parasites of Vertebrates. Wallingford, UK: CAB International University Press, 751 pp.Google Scholar
Lahmar, S, Boufana, B, Lahmar, S, Inoubli, S, Guadraoui, M, Dhibi, M, Bradshaw, H and Craig, PS (2009 a) Echinococcus in the wild carnivores and stray dogs of northern Tunisia: the results of a pilot survey. Annals of Tropical Medicine and Parasitology 103, 323–331.Google Scholar
Lahmar, S, Rebaï, W, Boufana, B, Craig, PS, Ksantini, R, Daghfous, K, Chebbi, F, Ftériche, F, Bédioui, H, Jouini, M, Dhibi, M, Makni, A, Ayadi, MS, Ammous, A, Kacem, MJ and Ben Safta, Z (2009 b) Cystic echinococcosis in Tunisia: analysis of hydatid cysts that have been surgically removed from patients. Annals of Tropical Medicine & Parasitology 103, 593–604.Google Scholar
Lahmar, S, Trifi, M, Ben Naceur, S, Bouchhima, T, Lahouar, N, Lamouchi, I, Maâmouri, N, Selmi, R, Dhibi, M and Torgerson, PR (2013) Cystic echinococcosis in slaughtered domestic ruminants from Tunisia. Journal of Helminthology 87, 318–325.Google Scholar
Lahmar, S, Boufana, B, Jebabli, L, Craig, PS, Ayari, H, Basti, T, Dhibi, M and Torgerson, PR (2014) Modelling the transmission dynamics of cystic echinococcosis in donkeys of different ages from Tunisia. Veterinary Parasitology 205, 119–124. http://dx.doi.org/10.1016/j.vetpar.2014.06.007.Google Scholar
Lahmar, S, Arfa, I, Ben Othmen, S, Jguirim, W, Said, Y, Dhibi, A and Boufana, B (2017) Intestinal helminths of stray dogs from Tunisia with special reference to zoonotic infections. Parasitology Open 3, e18, 1–9. https://doi.org/10.1017/pao.2017.21.Google Scholar
Lamouchi, I (2009) Contribution à l’étude épidémiologique de l'hydatidose et de la cysticercose hépato-péritonéale chez les dromadaires et les caprins abattus dans la région de Tozeur (DVM Thesis). National School of Veterinary Medicine Sidi Thabet, Tunisia.Google Scholar
Levine, ND (1980) Nematode Parasites of Domestic Animals and Man, 2nd Edn. Minneapolis, Minnesota: Burgess Publishing Company, 477 pp.Google Scholar
Maâmouri, N (2005) Contribution à l'étude de l'hydatidose et de la cysticercose hépato- péritonéale chez les ruminants dans les abattoirs de Korba et Nabeul, Tunisie (DVM Thesis). National School of Veterinary Medicine Sidi Thabet, Tunisia.Google Scholar
Mansouri, M, Sakkari, B and Mowlavi, GR (2016) Helminth parasites of wild boars, Sus scrofa, in Bushehr Province, southwestern Iran. Iran Journal of Parasitology 11, 377–382.Google Scholar
Marrakchi, R, Ben Romdhane, K and Touati, S (1989) Découverte fortuite du premier cas de trichinose en Tunisie. Maghreb Médical, n°208, Août1989.Google Scholar
Mayer-Scholl, A, Pozio, E, Gayda, J, Thaben, N, Bahn, P and Nöckler, K (2017) Magnetic stirrer method for the detection of Trichinella larvae in muscle samples. Journal of Visualized Experiments 3, 121. https://doi.10.3791/55354.Google Scholar
Meng, XJ, Lindsay, DS and Sriranganathan, N (2009) Wild boars as sources for infectious diseases in livestock and humans. Philosophical Transactions of the Royal Society B 364, 2697–2707. https://doi.10.1098/rstb.2009.0086.Google Scholar
Miloshev, B (1956) Case of triple infection with Metastrongylus elongatus, thaeniarhynchus saginatus and Enterobius vermicularis [in Bulgarian]. Suvr Med. (Sofiia) 7, 94–97.Google Scholar
Nezri, M, Ruer, J, De Bruyne, A, Cohen-Valensi, R, Pozio, E and Dupouy-Camat, J (2006) Première observation d'un cas d'humain de trichinellose à Trichinella britovi en Algérie après consommation de viande de chacal (Canis aureus). Bulletin de la Société de Pathologie Exotique 99, 94–95.Google Scholar
Nöckler, K, Pozio, E, Voigt, WP and Heidrich, J (2000) Detection of Trichinella infection in food animals. Veterinary Parasitology 93, 335–350.Google Scholar
Oliver, W and Leus, K (2008) Sus scrofa. The IUCN Red List of Threatened Species 2008: e.T41775A10559847. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T41775A10559847.en.Google Scholar
Oroian, TE, Oroian, RG, Paşca, I, Oroian, E and Covrig, I (2010) Methods of age estimation by dentition in Sus scrofa ferus sp. Bulletin UASVM Animal Science and Biotechnologies 67, 1843–5262.Google Scholar
Oudni-M'rad, M, M'rad, S, Ksia, A, Lamiri, R, Mekki, M, Nouri, A, Mezhoud, H and Babba, H (2016) First molecular evidence of the simultaneous human infection with two species of Echinococcus granulosus sensu lato: Echinococcus granulosus sensu stricto and Echinococcus canadensis. Parasitology Research 115, 1065–1069.Google Scholar
Paoletti, B, Della Salda, L, Di Cesare, A, Iorio, R, Vergara, A, Fava, C, Olivastri, A, Dessì, G, Scala, A and Varcasia, A (2018) Epidemiological survey on cystic echinococcosis in wild boar from Central Italy. Parasitology Research 118, 43–46. https://doi.org/10.1007/s00436-018-6112-3.Google Scholar
Popiolek, M, Knecht, D, Szczesna-Stas Kiewicz, J and Czerwinsska-Rozalow, A (2010) Helminths of the wild boar (Sus scrofa l.) in natural and breeding conditions. Bulletin of Veterinary Institute Pulawy 54, 161–166.Google Scholar
Pozio, E (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 3–21.Google Scholar
R Core, Team (2017) R : A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/Google Scholar
Roberts, MG, Lawson, JR and Gemmell, MA (1986) Population dynamics in echinococcosis and cysticercosis: mathematical model of the life-cycle of Echinococcus granulosus. Parasitology 92, 621–641.Google Scholar
Sánchez, E, Cáceres, O, Náquira, C, Miranda, E, Samudio, F and Fernandes, O (2012) Echinococcus granulosus genotypes circulating in alpacas (Lama pacos) and pigs (Sus scrofa) from an endemic region in Peru. The Memórias do Instituto Oswaldo Cruz 107, 275–278.Google Scholar
Scala, A, Pipia, AP, Dore, F, Sanna, G, Tamponi, C, Marrosu, R, Bandino, E, Carmona, C, Boufana, B and Varcasia, A (2015) Epidemiological updates and economic losses due to Taenia hydatigena in sheep from Sardinia, Italy. Parasitology Research 114, 3137–3143.Google Scholar
Schwartz, D (1993) Méthodes statistiques à l'usage des médecins et des biologists, 3rd Edn. Paris: Flammarion.Google Scholar
Selmi, R (2009) Contribution à l’étude épidémiologique de l'hydatidose chez les caprins et dromadaires abattus dans la région de Gabès (DVM Thesis). National School of Veterinary Medicine Sidi Thabet, Tunisia.Google Scholar
Senlik, B, Cirak, VY, Girisgin, O and Akyol, CV (2011) Helminth infections of wild boars (Sus scrofa) in the Bursa province of Turkey. Journal of Helminthology 85, 404–408. https://doi.org/10.1017/S0022149X1000074X.Google Scholar
Skrjabin, KI, Shikhobalova, NP, Shults, RS, Popova, TI, Boev, SN and Delyamure, SL (1952) Key to parasitic nematodes. III. Strongylata. Moscow: Academy of Sciences of the USSR. (English translation published by the Israel Program for Scientific Translations, 1961, 890pp.)Google Scholar
Smyth, JD and Barrett, NJ (1980) Procedures for testing the viability of human hydatid cysts following surgical removal, especially after chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 649–652.Google Scholar
Solaymani-Mohammadi, S, Mobedi, I, Rezaian, M, Massoud, J, Mohebali, M, Hooshyar, H, Ashrafi, K and Rokni, MB (2003) Helminth parasites of the wild boar, Sus scrofa, in Luristan province, western Iran and their public health significance. Journal of Helminthology 77, 263–267.Google Scholar
Souilem, O (1986) Contribution à l’étude des gongylonèmes chez les bovins du Cap-Bon (DVM Thesis). Sidi Thabet. Tunisia.Google Scholar
Syrjälä, P, Oksanen, A, Hälli, O, Peltoniemi, O and Heinonen, M (2010) Metastrongylus spp. infection in a farmed wild boar (Sus scrofa) in Finland. Acta Veterinaria Scandinavica 52(suppl. 1), S21. http://doi.org/10.1186/1751-0147-52-S1-S21.Google Scholar
Thienpont, D, Rochette, F and Vanparijs, OFJ (1986) Diagnosing helminthiasis by coprological examination. Beerse, Belgium: Janssen Research Fundation. 187 pp.Google Scholar
Torgerson, PR and Heath, DD (2003) Transmission dynamics and control options for Echinococcus granulosus. Parasitology 127(suppl), S143–S158.Google Scholar
Umhang, G, Richomme, C, Hormaz, V, Boucher, JM and Boué, F (2014) Pigs and wild boar in Corsica harbor Echinococcus canadensis G6/7 at levels of concern for public health and local economy. Acta Tropica 133, 64–68. https://doi.org/10.1016/j.actatropica.2014.02.005.Google Scholar