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01-09-2019 | Original Contribution

Limited Exchange of Salmonella Among Domestic Pigs and Wild Boars in Italy

Authors: Silvia Bonardi, Luca Bolzoni, Renato Giulio Zanoni, Marina Morganti, Margherita Corradi, Stefano Gilioli, Stefano Pongolini

Published in: EcoHealth | Issue 3/2019

Abstract

The study assessed Salmonella carriage in wild boars (Sus scrofa) and compared their isolates with those recovered from the domestic swine population of the same area of northern Italy (Emilia-Romagna), characterized by intensive pig farming and rather high density of wild boars. A total of 189 wild boars hunted during twelve months (2017–2018) were tested for Salmonella in mesenteric lymph nodes (MLN) and faecal samples. Antimicrobial resistance of recovered strains was tested against 14 antimicrobials. Salmonella was detected in 33/189 wild boars (17.5%), specifically from 30/189 MLN (15.9%) and 6/189 faecal samples (3.2%). Three animals were positive in both samples. Thirteen Salmonella serovars were identified, i.e. Typhimurium (the most common), Bovismorbificans, Coeln, Derby, Enteritidis, Gaminara, Hessarek, Houtenae IV, Kottbus, Napoli, Stanleyville, Thompson and Veneziana. Salmonella carriage was higher in warm than in cold months (P = 0.0013). Pregnancy status was never associated with Salmonella carriage, with significant difference in the recovery of the pathogen between non-pregnant and pregnant females (P = 0.003). Only one resistance pattern to streptomycin and tetracycline was found in 15 isolates (41.7%) belonging to Typhimurium (14/14; 100%) and Kottbus (1/3; 33.3%) serovars. Overlap with isolates from farmed pigs was limited at serotype level (Typhimurium, Derby, Enteritis, Bovismorbificans, Kottbus) and absent at PFGE level, and also antimicrobial resistance patterns were substantially different. This evidence indicates a substantial segregation of the two animal populations with regard to infectious contacts, possibly suggesting that biosecurity measures in place at industrial farm level limit the exchange of Salmonella.

Baudart J, Lemarchand K, Brisabois A, Lebaron P (2000) Diversity of Salmonella Strains Isolated from the Aquatic Environment as Determined by Serotyping and Amplification of the Ribosomal DNA Spacer Regions. Applied and Environmental Microbiology 66: 1544–1552.CrossRef

Bonardi S, Bassi L, Brindani F, D’Incau M, Barco L. Carra E, Pongolini S (2013) Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. International Journal of Food Microbiology 163: 248-257; https://doi.org/10.1016/j.ijfoodmicro.2013.02.012 CrossRefPubMed

Bonardi S, Bruini I, Alpigiani I, Vismarra A, Barilli E, Brindani F, Morganti M, Bellotti P, Bolzoni L, Pongolini S (2016) Influence of pigskin on Salmonella contamination of pig carcasses and cutting lines in an Italian slaughterhouse. Italian Journal of Food Safety 5: 65-68; https://doi.org/10.4081/ijfs.2016.5654 CrossRef

Botti V, Navillod FV, Domenis L, Orusa R, Pepe E, Robetto S, Guidetti C (2013) Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Veterinaria Italiana 49: 195-202. https://doi.org/10.12834/vetit.2013.492.201.208 CrossRefPubMed

Carnevali L, Pedrotti L, Riga F, Toso S (2009) Ungulates in Italy: Status, distribution, abundance, management and hunting of Ungulate populations in Italy. Biologia e Conservazione della Fauna 117:1-168

Chiari M, Zanoni M, Tagliabue S, Lavazza A, Alborali LG (2013) Salmonella serotypes in wild boars (Sus scrofa) hunted in northern Italy. Acta Veterinaria Scandinavica 55: 42. https://doi.org/10.1186/1751-0147-55-42 CrossRefPubMedPubMedCentral

Clinical and Laboratory Standards Institute (CLSI) (2018) Performance Standards for Antimicrobial Susceptibility Testing, 28^th ed. CLSI supplement M100. Wayne, PA

Cowled BD, Ward MP, Laffan SW, Galea F, Garner MG, MacDonald AJ, Marsh I, Muellner P, Negus K, Quasim S, Woolnough AP, Sarre SD (2012) Integrating survey and molecular approaches to better understand wildlife disease ecology. PLoS One 7: e46310. https://doi.org/10.1371/journal.pone.0046310 CrossRefPubMedPubMedCentral

Cummings KJ, Rodriguez-Rivera LD, Grigar MK, Rankin SC, Mesenbrink BT, Leland BR, Bodenchuk MJ (2016) Prevalence and characterization of Salmonella isolated from feral pigs throughout Texas. Zoonoses and Public Health 63: 436-441.CrossRef

European Food Safety Authority (EFSA) (2014) Evaluation of possible mitigation measures to prevent introduction and spread of African swine fever virus through wild boar. EFSA Journal 12(3):3616. https://doi.org/10.2903/j.efsa.2014.3616 CrossRef

European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC) (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal 16 (12):5500. https://doi.org/10.2903/j.efsa.2018.5500aaaaasssss CrossRef

Fenwick SG, Duignan PJ, Nicol CM, Leyland MJ, Hunter JE (2004). A comparison of Salmonella serotypes isolated from New Zealand sea lions and feral pigs on the Auckland Islands by pulsed-field gel electrophoresis. Journal of Wildlife Diseases 40: 566-570; https://doi.org/10.7589/0090-3558-40.3.566 CrossRefPubMed

Fisher IST, Jourdan-Da Silva N, Hächler H, Weill F-X, Schmid H, Danan C, Kérouanton A, Lane CR, Dionisi AM, Luzzi I (2009) Human infections due to Salmonella Napoli: a multicountry, emerging enigma recognized by the Enter-net international surveillance network. Foodborne Pathogens and Disease 6: 613–619 https://doi.org/10.1089/fpd.2008.0206 CrossRefPubMed

Funk J, Davies PR, Nichols MA. The effect of sample weight on detection of Salmonella enterica in swine feces. Journal of Veterinary Diagnostic Investigation 2000; 12: 412–418.CrossRef

Gethöffer F, Sodeikat G, Pohlmeyer K (2007). Reproductive parameters of wild boar (Sus scrofa) in three different parts of Germany. European Journal of Wildlife Research 53: 287-297.CrossRef

Gori M, Ebranati E, Scaltriti E, Huedo P, Ciceri G, Tanzi E, Pontello M, Zehender G, Pongolini S, Bolzoni L (2018) High-resolution diffusion pattern of human infections by Salmonella enterica serovar Napoli in Northern Italy explained through phylogeography. PLoS One 13: e0202573. https://doi.org/10.1371/journal.pone.0202573 CrossRefPubMedPubMedCentral

Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J (2007) Diseases shared between wildlife and livestock: a European perspective. European Journal of Wildlife Research 53: 241-256.CrossRef

Graziani C, Luzzi I, Owczarek S, Dionisi AM, Busani L (2015) Salmonella enterica Serovar Napoli Infection in Italy from 2000 to 2013: Spatial and spatio-temporal analysis of cases distribution and the effect of human and animal density on the risk of infection. PLoS ONE 10, e0142419. https://doi.org/10.1371/journal.pone.0142419 CrossRefPubMedPubMedCentral

Keuling O, Baub E, Duscher A, Ebert C, Fischer C, Monaco A, Podgorski T, Prevot C, Ronnenberg K, Sodeikat G, Stier N, Thurfjell H (2013) Mortality rates of wild boar Sus scrofa L. in central Europe. European Journal of Wildlife Research 59: 805-814.CrossRef

Krautwald-Junghanns ME, Stenkat J, Szabo I, Ortlieb F, Blindow I, Neul AK, Pees M, Schmidt V (2013) Characterization of Salmonella isolated from captive and free-living snakes in Germany. Berliner und Münchener Tierarztliche Wochenschrift 126: 209-215.PubMed

Haley BJ, Cole DJ, Lipp EK (2009) Distribution, diversity and seasonality of waterborne salmonellae in a rural watershed. Applied and Environmental Microbiology 75: 1248-1255; DOI: 10.1128/AEM.01648-08CrossRefPubMedPubMedCentral

Huedo P, Gori M, Zolin A, Amato E, Ciceri G, Bossi A, Pontello M (2017) Salmonella enterica rerotype Napoli is the first cause of invasive nontyphoidal salmonellosis in Lombardy, Italy (2010-2014), and belongs to Typhi subclade. Foodborne Pathogens and Disease 14: 148-151; https://doi.org/10.1089/fpd.2016.2206. Epub 2016 Dec 16CrossRefPubMed

Hurd HS, McKean JD, Griffith RD, Rostagno MH (2004) Estimation of the Salmonella enterica prevalence in finishing swine. Epidemiology and Infection 132:127-135.CrossRef

International Organization for Standardization (ISO) (2014) Microbiology of the Food Chain. Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella—Part III: Guidelines for Serotyping of Salmonella spp. ISO 6579-3:2014. Geneva

International Organization for Standardization (ISO) (2017) Microbiology of the Food Chain. Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella—Part I: Detection of Salmonella spp. ISO 6579-1:2017. Geneva

OIE (2015) OIE List of Antimicrobial Agents of Veterinary Importance. http://www.oie.int/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/Eng_OIE_List_antimicrobials_May2015.pdf. Accessed 12 May 2018

Paulsen P, Smulders FJM, Hilbert F (2012) Salmonella in meat from hunted game: A Central European perspective. Food Research International 45: 609–616; https://doi.org/10.1016/j.foodres.2011.06.055 CrossRef

Pittiglio C, Khomenko S, Beltran-Alcrudo D (2018) Wild boar mapping using population-density statistics: From polygons to high resolution raster maps. PLoS ONE 13(5): e0193295. https://doi.org/10.1371/journal.pone.0193295 CrossRefPubMedPubMedCentral

PulseNet (2013) One-day (24-28 h) standardized laboratory protocol for molecular subtyping of Escherichia coli O157:H7, Salmonella serotypes, Shigella sonnei, and Shigella flexneri by Pulsed Field Gel Electrophoresis (PFGE). http://www.pulsenetinternational.org/assets/PulseNet/uploads/pfge/PNL05_Ec-Sal-ShigPFGEprotocol.pdf. Accessed 15 January 2018

Rossi M, Delogu M, Ostanello F, Caprioli A, Zanoni RG (2007) Antibiotic resistance patterns of faecal indicator organisms and occurrence of Salmonella spp. in wild boar (Sus scrofa scrofa) in Italy. In: Proceedings of the seventh International Symposium on the Epidemiology and Control of foodborne Pathogens in Pork—Safepork 2007, Verona, pp 493–495

Saez-Royuela C, Gomariz C, Telleria JL (1989) Age determination of European wild boar (Sus scrofa). Wildlife Society Bullettin 17: 326–329.

Sannö A, Aspán A, Hestvik G, Jacobson M (2014) Presence of Salmonella spp., Yersinia enterocolitica, Yersinia pseudotuberculosis and Escherichia coli O157:H7 in wild boars. Epidemiology and Infection 142: 2542-2547. https://doi.org/10.1017/s0950268814000119 CrossRefPubMed

Sannö A, Rosendal T, Aspán A, Backhans A, Jacobson M (2018) Distribution of enteropathogenic Yersinia spp and Salmonella spp in the Swedish wild boar population, and assessment of risk factors that may affect their prevalence. Acta Veterinaria Scandinavica 60: 40. 10.1186/s13028-018-0395-3.CrossRefPubMedPubMedCentral

Sasaki Y, Goshima T, Mori T, Murakami M, Haruna M, Ito K, Yamada Y (2013) Prevalence and antimicrobial susceptibility of foodborne bacteria in wild boars (Sus scrofa) and wild deer (Cervus nippon) in Japan. Foodborne Pathogens and Disease 10: 985-991; https://doi.org/10.1089/fpd.2013.1548 CrossRefPubMed

Singer N, Weissman Y, Yom-Tov Y, Marder U (1977) Isolation of Salmonella hessarek from starlings (Sturnus vulgaris). Avian Diseases 21:117-119.CrossRef

Thakur S, Sandfoss M, Kennedy-Stoskopf S, DePerno CS (2011) Detection of Clostridium difficile and Salmonella in feral swine population in North Carolina. Journal of Wildlife Diseases 47: 774-776; https://doi.org/10.7589/0090-3558-47.3.774 CrossRefPubMed

Thomas JL, Slawson RM, Taylor WD (2013) Salmonella serotype diversity and seasonality in urban and rural streams. Journal of Applied Microbiology 114: 907-922; https://doi.org/10.1111/jam.12079 CrossRefPubMed

Velarde R, Porrero MC, Serrano E, Marco I, García M, Téllez S, Domínguez L, Aymí R, Lavín S (2012). Septicemic salmonellosis caused by Salmonella Hessarek in wintering and migrating Song Thrushes (Turdus philomelos) in Spain. Journal of Wildlife Diseases 48:113-121.CrossRef

Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Springer, New York, USA.CrossRef

Vieira-Pinto M, Morais L, Caleja C, Themudo P, Torres C, Igrejas G, Poeta P, Martins C (2011) Salmonella sp. in game (Sus scrofa and Oryctolagus cuniculus). Foodborne Pathogens and Disease 8: 739-740; https://doi.org/10.1089/fpd.2010.0742 CrossRefPubMed

Wacheck S, Fredriksson-Ahomaa M, König M, Stolle A, Stephan R (2010) Wild boars as an important reservoir for foodborne pathogens. Foodborne Pathogens and Disease 7: 307-312; https://doi.org/10.1089/fpd.2009.0367 CrossRefPubMed

Ward MP, Cowled B., Galea F, Graeme Garner M, Laffan SW, Marsh I, Negus K, Sarre SD, Woolnough AP (2013) Salmonella infection in a remote, isolated wild pig population. Veterinary Microbiology 162: 921-929.CrossRef

Zottola T, Montagnaro S, Magnapera C, Sasso S, De Martino L, Bragagnolo A, D’Amici L, Condoleo R, Pisanelli G, Iovane G, Paganini U (2013) Prevalence and antimicrobial susceptibility of Salmonella in European wild boars (Sus scrofa); Latium Region-Italy. Comparative Immunology, Microbiology and Infectious Diseases 36: 161– 168; https://doi.org/10.1016/j.cimid.2012.11.004 CrossRefPubMed

Title: Limited Exchange of Salmonella Among Domestic Pigs and Wild Boars in Italy
Authors: Silvia Bonardi
Luca Bolzoni
Renato Giulio Zanoni
Marina Morganti
Margherita Corradi
Stefano Gilioli
Stefano Pongolini
Publication date: 01-09-2019
Publisher: Springer US
Published in: EcoHealth / Issue 3/2019
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI: https://doi.org/10.1007/s10393-019-01418-2

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