Detection and Characterization of Zoonotic Pathogens in Game Meat Hunted in Northwestern Italy
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sampling
2.2. Bacterial Isolation and Characterization
2.3. Hepatitis E Virus Detection
2.4. DNA Extraction and Whole Genome Sequencing (WGS)
2.5. Data Analysis of Whole Genome Sequencing (WGS)
3. Results
3.1. Bacterial Isolation and Characterization
3.2. Hepatitis E Virus Detection
3.3. Molecular Characterization of Y. enterocolitica and L. monocytogenes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hedman, H.D.; Varga, C.; Duquette, J.; Novakofski, J.; Mateus-Pinilla, N.E. Food Safety Considerations Related to the Consumption and Handling of Game Meat in North America. Vet. Sci. 2020, 7, 188. [Google Scholar] [CrossRef] [PubMed]
- Shivaprakash, K.N.; Sen, S.; Paul, S.; Kiesecker, J.M.; Bawa, K.S. Mammals, Wildlife Trade, and the next Global Pandemic. Curr. Biol. 2021, 31, 3671–3677.e3. [Google Scholar] [CrossRef] [PubMed]
- Avagnina, A.; Nucera, D.; Grassi, M.A.; Ferroglio, E.; Dalmasso, A.; Civera, T. The Microbiological Conditions of Carcasses from Large Game Animals in Italy. Meat Sci. 2012, 91, 266–271. [Google Scholar] [CrossRef] [PubMed]
- Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 Laying down Specific Hygiene Rules for Food of Animal Origin. Available online: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2004:139:0055:0205:en:PDF (accessed on 5 December 2023).
- Membré, J.-M.; Laroche, M.; Magras, C. Assessment of Levels of Bacterial Contamination of Large Wild Game Meat in Europe. Food Microbiol. 2011, 28, 1072–1079. [Google Scholar] [CrossRef] [PubMed]
- Eng, S.-K.; Pusparajah, P.; Ab Mutalib, N.-S.; Ser, H.-L.; Chan, K.-G.; Lee, L.-H. Salmonella: A Review on Pathogenesis, Epidemiology and Antibiotic Resistance. Front. Life Sci. 2015, 8, 284–293. [Google Scholar] [CrossRef]
- Bianchi, D.M.; Barzanti, P.; Adriano, D.; Martucci, F.; Pitti, M.; Ferraris, C.; Floris, I.; La Brasca, R.; Ligotti, C.; Morello, S.; et al. Food Safety Monitoring of Salmonella spp. in Northern Italy 2019–2021. Pathogens 2023, 12, 963. [Google Scholar] [CrossRef]
- European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union One Health 2021 Zoonoses Report. EFSA J. 2022, 20, e07666. [Google Scholar] [CrossRef]
- Bottone, E.J. Yersinia enterocolitica: The Charisma Continues. Clin. Microbiol. Rev. 1997, 10, 257–276. [Google Scholar] [CrossRef]
- Kathariou, S. Listeria monocytogenes Virulence and Pathogenicity, a Food Safety Perspective. J. Food Prot. 2002, 65, 1811–1829. [Google Scholar] [CrossRef]
- Espinosa, L.; Gray, A.; Duffy, G.; Fanning, S.; McMahon, B.J. A Scoping Review on the Prevalence of Shiga-Toxigenic Escherichia coli in Wild Animal Species. Zoonoses Public Health 2018, 65, 911–920. [Google Scholar] [CrossRef]
- Kaper, J.B.; Nataro, J.P.; Mobley, H.L.T. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2, 123–140. [Google Scholar] [CrossRef] [PubMed]
- Glassman, H.; Ferrato, C.; Chui, L. Epidemiology of Non-O157 Shiga Toxin-Producing Escherichia coli in the Province of Alberta, Canada, from 2018 to 2021. Microorganisms 2022, 10, 814. [Google Scholar] [CrossRef] [PubMed]
- Ray, R.; Singh, P. Prevalence and Implications of Shiga Toxin-Producing E. coli in Farm and Wild Ruminants. Pathogens 2022, 11, 1332. [Google Scholar] [CrossRef] [PubMed]
- Yugo, D.; Meng, X.-J. Hepatitis E Virus: Foodborne, Waterborne and Zoonotic Transmission. Int. J. Environ. Res. Public Health 2013, 10, 4507–4533. [Google Scholar] [CrossRef] [PubMed]
- Sacristán, C.; Madslien, K.; Sacristán, I.; Klevar, S.; Das Neves, C.G. Seroprevalence of Hepatitis E Virus in Moose (Alces alces), Reindeer (Rangifer tarandus), Red Deer (Cervus elaphus), Roe Deer (Capreolus capreolus), and Muskoxen (Ovibos moschatus) from Norway. Viruses 2021, 13, 224. [Google Scholar] [CrossRef]
- Tei, S.; Kitajima, N.; Takahashi, K.; Mishiro, S. Zoonotic Transmission of Hepatitis E Virus from Deer to Human Beings. Lancet 2003, 362, 371–373. [Google Scholar] [CrossRef] [PubMed]
- Ferri, G.; Piccinini, A.; Olivastri, A.; Vergara, A. Hepatitis E Virus Detection in Hunted Wild Boar (Sus scrofa) Livers in Central Italy. Ital. J. Food Saf. 2022, 11, 9979. [Google Scholar] [CrossRef]
- Fonti, N.; Pacini, M.I.; Forzan, M.; Parisi, F.; Periccioli, M.; Mazzei, M.; Poli, A. Molecular and Pathological Detection of Hepatitis E Virus in Roe Deer (Capreolus capreolus) and Fallow Deer (Dama dama) in Central Italy. Vet. Sci. 2022, 9, 100. [Google Scholar] [CrossRef]
- Di Profio, F.; Sarchese, V.; Palombieri, A.; Fruci, P.; Lanave, G.; Robetto, S.; Martella, V.; Di Martino, B. Current Knowledge of Hepatitis E Virus (HEV) Epidemiology in Ruminants. Pathogens 2022, 11, 1124. [Google Scholar] [CrossRef]
- UNI CEI EN ISO/IEC 17025:2018; General Requirements for the Competence of Testing and Calibration Laboratories. UNI Ente Italiano Di Normazione: Roma, Italy, 2018.
- UNI EN ISO 11290-1:2017; Microbiologia Della Catena Alimentare—Metodo Orizzontale Per la Ricerca e la Conta di Listeria Monocytogenes e Listeria spp.—Parte 1: Metodo per la Ricerca. UNI Ente Italiano Di Normazione: Roma, Italy, 2017.
- D’agostino, M.; Wagner, M.; Vazquez-Boland, J.A.; Kuchta, T.; Karpiskova, R.; Hoorfar, J.; Novella, S.; Scortti, M.; Ellison, J.; Murray, A.; et al. A Validated PCR-Based Method To Detect Listeria monocytogenes Using Raw Milk as a Food Model—Towards an International Standard. J. Food Prot. 2004, 67, 1646–1655. [Google Scholar] [CrossRef]
- Doumith, M.; Buchrieser, C.; Glaser, P.; Jacquet, C.; Martin, P. Differentiation of the Major Listeria monocytogenes Serovars by Multiplex PCR. J. Clin. Microbiol. 2004, 42, 3819–3822. [Google Scholar] [CrossRef]
- Guidi, F.; Gattuso, A.; Orecchioni, F.; Marziali, A.; Gironacci, L.; Repetto, A.; Scuota, S.; Ottaviani, D.; Petruzzelli, A.; Fisichella, S.; et al. Molecular surveillance on Listeria monocytogenes isolates in Umbria and Marche (Italy) in 2017. Sanita’ Pubblica Vet. 2018. Available online: https://www.spvet.it/archivio/numero-108/682.html (accessed on 5 December 2023).
- UNI EN ISO 6579-1:2017; Microbiologia Della Catena Alimentare—Metodo Orizzontale Per la Ricerca, la Conta e la Sierotipizzazione di Salmonella—Parte 1: Metodo Orizzontale Per la Ricerca di Salmonella spp. UNI Ente Italiano Di Normazione: Roma, Italy, 2017.
- UNI CEN ISO/TS 13136:2013; Microbiologia di Alimenti e Mangimi Per Animali—Metodo Basato Sulla Reazione di Polimerizzazione a Catena (PCR) in Tempo Reale Per la Ricerca dei Microrganismi Patogeni Degli Alimenti—Metodo Orizzontale per la Ricerca di Escherichia Coli Produttori di Shiga-Tossine (STEC), e Determinazione dei Sierogruppi O157, O111, O26, O103 e O145. UNI Ente Italiano Di Normazione: Roma, Italy, 2013.
- UNI EN ISO 10273:2017; Microbiologia Della Catena Alimentare—Metodo Orizzontale Per la Ricerca di Yersinia Enterecolitica Patogena. UNI Ente Italiano Di Normazione: Roma, Italy, 2017.
- UNI EN ISO 22174:2005; Microbiologia di Alimenti e Mangimi Per Animali—Reazione a Catena di Polimerizzazione (PCR) Per la Ricerca dei Microrganismi Patogeni Degli Alimenti—Requisiti Generali e Definizioni. UNI Ente Italiano Di Normazione: Roma, Italy, 2005.
- CCM 2016-HEV; Protocollo Per la Ricerca del Virus dell’Epatite E in Alimenti. Istituto Superiore di Sanità: Roma, Italy, 2017.
- Jothikumar, N.; Cromeans, T.L.; Robertson, B.H.; Meng, X.J.; Hill, V.R. A Broadly Reactive One-Step Real-Time RT-PCR Assay for Rapid and Sensitive Detection of Hepatitis E Virus. J. Virol. Methods 2006, 131, 65–71. [Google Scholar] [CrossRef] [PubMed]
- The Galaxy Community; Afgan, E.; Nekrutenko, A.; Grüning, B.A.; Blankenberg, D.; Goecks, J.; Schatz, M.C.; Ostrovsky, A.E.; Mahmoud, A.; Lonie, A.J.; et al. The Galaxy Platform for Accessible, Reproducible and Collaborative Biomedical Analyses: 2022 Update. Nucleic Acids Res. 2022, 50, W345–W351. [Google Scholar] [CrossRef]
- Tangaro, M.A.; Mandreoli, P.; Chiara, M.; Donvito, G.; Antonacci, M.; Parisi, A.; Bianco, A.; Romano, A.; Bianchi, D.M.; Cangelosi, D.; et al. Laniakea@ReCaS: Exploring the Potential of Customisable Galaxy on-Demand Instances as a Cloud-Based Service. BMC Bioinform. 2021, 22, 544. [Google Scholar] [CrossRef] [PubMed]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef]
- Wick, R.R.; Judd, L.M.; Gorrie, C.L.; Holt, K.E. Unicycler: Resolving Bacterial Genome Assemblies from Short and Long Sequencing Reads. PLoS Comput. Biol. 2017, 13, e1005595. [Google Scholar] [CrossRef] [PubMed]
- Larsen, M.V.; Cosentino, S.; Rasmussen, S.; Friis, C.; Hasman, H.; Marvig, R.L.; Jelsbak, L.; Sicheritz-Pontén, T.; Ussery, D.W.; Aarestrup, F.M.; et al. Multilocus Sequence Typing of Total-Genome-Sequenced Bacteria. J. Clin. Microbiol. 2012, 50, 1355–1361. [Google Scholar] [CrossRef] [PubMed]
- VFDB: Virulence Factors of Bacterial Pathogens. Available online: http://www.mgc.ac.cn/cgi-bin/VFs/v5/main.cgi (accessed on 5 July 2023).
- Atanassova, V.; Apelt, J.; Reich, F.; Klein, G. Microbiological Quality of Freshly Shot Game in Germany. Meat Sci. 2008, 78, 414–419. [Google Scholar] [CrossRef]
- Ranucci, D.; Roila, R.; Onofri, A.; Cambiotti, F.; Primavilla, S.; Miraglia, D.; Andoni, E.; Di Cerbo, A.; Branciari, R. Improving Hunted Wild Boar Carcass Hygiene: Roles of Different Factors Involved in the Harvest Phase. Foods 2021, 10, 1548. [Google Scholar] [CrossRef]
- Razzuoli, E.; Listorti, V.; Martini, I.; Migone, L.; Decastelli, L.; Mignone, W.; Berio, E.; Battistini, R.; Ercolini, C.; Serracca, L.; et al. Prevalence and Antimicrobial Resistances of Salmonella spp. Isolated from Wild Boars in Liguria Region, Italy. Pathogens 2021, 10, 568. [Google Scholar] [CrossRef]
- Zottola, T.; Montagnaro, S.; Magnapera, C.; Sasso, S.; De Martino, L.; Bragagnolo, A.; D’Amici, L.; Condoleo, R.; Pisanelli, G.; Iovane, G.; et al. Prevalence and Antimicrobial Susceptibility of Salmonella in European Wild Boar (Sus scrofa); Latium Region—Italy. Comp. Immunol. Microbiol. Infect. Dis. 2013, 36, 161–168. [Google Scholar] [CrossRef]
- Cilia, G.; Turchi, B.; Fratini, F.; Bilei, S.; Bossù, T.; De Marchis, M.L.; Cerri, D.; Pacini, M.I.; Bertelloni, F. Prevalence, Virulence and Antimicrobial Susceptibility of Salmonella spp., Yersinia enterocolitica and Listeria monocytogenes in European Wild Boar (Sus scrofa) Hunted in Tuscany (Central Italy). Pathogens 2021, 10, 93. [Google Scholar] [CrossRef]
- Altissimi, C.; Noé-Nordberg, C.; Ranucci, D.; Paulsen, P. Presence of Foodborne Bacteria in Wild Boar and Wild Boar Meat—A Literature Survey for the Period 2012–2022. Foods 2023, 12, 1689. [Google Scholar] [CrossRef] [PubMed]
- Navarro-Gonzalez, N.; Mentaberre, G.; Porrero, C.M.; Serrano, E.; Mateos, A.; López-Martín, J.M.; Lavín, S.; Domínguez, L. Effect of Cattle on Salmonella Carriage, Diversity and Antimicrobial Resistance in Free-Ranging Wild Boar (Sus scrofa) in Northeastern Spain. PLoS ONE 2012, 7, e51614. [Google Scholar] [CrossRef] [PubMed]
- Palacios-Gorba, C.; Moura, A.; Leclercq, A.; Gómez-Martín, Á.; Gomis, J.; Jiménez-Trigos, E.; Mocé, M.L.; Lecuit, M.; Quereda, J.J. Listeria spp. Isolated from Tonsils of Wild Deer and Boars: Genomic Characterization. Appl. Environ. Microbiol. 2021, 87, e02651-20. [Google Scholar] [CrossRef] [PubMed]
- Fredriksson-Ahomaa, M.; Sauvala, M.; Kurittu, P.; Heljanko, V.; Heikinheimo, A.; Paulsen, P. Characterisation of Listeria monocytogenes Isolates from Hunted Game and Game Meat from Finland. Foods 2022, 11, 3679. [Google Scholar] [CrossRef] [PubMed]
- Troxler, R.; Von Graevenitz, A.; Funke, G.; Wiedemann, B.; Stock, I. Natural Antibiotic Susceptibility of Listeria Species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri Strains. Clin. Microbiol. Infect. 2000, 6, 525–535. [Google Scholar] [CrossRef] [PubMed]
- Matle, I.; Mbatha, K.R.; Madoroba, E. A Review of Listeria monocytogenes from Meat and Meat Products: Epidemiology, Virulence Factors, Antimicrobial Resistance and Diagnosis. Onderstepoort J. Vet. Res. 2020, 87, 1–20. [Google Scholar] [CrossRef]
- Aubry, C.; Goulard, C.; Nahori, M.-A.; Cayet, N.; Decalf, J.; Sachse, M.; Boneca, I.G.; Cossart, P.; Dussurget, O. OatA, a Peptidoglycan O-Acetyltransferase Involved in Listeria monocytogenes Immune Escape, Is Critical for Virulence. J. Infect. Dis. 2011, 204, 731–740. [Google Scholar] [CrossRef]
- Begley, M.; Sleator, R.D.; Gahan, C.G.M.; Hill, C. Contribution of Three Bile-Associated Loci, Bsh, Pva, and btlB, to Gastrointestinal Persistence and Bile Tolerance of Listeria monocytogenes. Infect. Immun. 2005, 73, 894–904. [Google Scholar] [CrossRef] [PubMed]
- O’Riordan, M.; Marlena, A.M.; Daniel, A.P. Listeria Intracellular Growth and Virulence Require Host-Derived Lipoic Acid. Science 2003, 302, 462–464. [Google Scholar] [CrossRef] [PubMed]
- Modesto, P.; De Ciucis, C.G.; Vencia, W.; Pugliano, M.C.; Mignone, W.; Berio, E.; Masotti, C.; Ercolini, C.; Serracca, L.; Andreoli, T.; et al. Evidence of Antimicrobial Resistance and Presence of Pathogenicity Genes in Yersinia enterocolitica Isolate from Wild Boars. Pathogens 2021, 10, 398. [Google Scholar] [CrossRef] [PubMed]
- Carella, E.; Romano, A.; Domenis, L.; Robetto, S.; Spedicato, R.; Guidetti, C.; Pitti, M.; Orusa, R. Characterisation of Yersinia enterocolitica Strains Isolated from Wildlife in the Northwestern Italian Alps. J. Vet. Res. 2022, 66, 141–149. [Google Scholar] [CrossRef] [PubMed]
- Martins, B.T.F.; de Meirelles, J.L.; Omori, W.P.; de Oliveira, R.R.; Yamatogi, R.S.; Call, D.R.; Nero, L.A. Comparative Genomics and Antibiotic Resistance of Yersinia enterocolitica Obtained from a Pork Production Chain and Human Clinical Cases in Brazil. Food Res. Int. 2022, 152, 110917. [Google Scholar] [CrossRef] [PubMed]
- Peng, Z.; Zou, M.; Li, M.; Liu, D.; Guan, W.; Hao, Q.; Xu, J.; Zhang, S.; Jing, H.; Li, Y.; et al. Prevalence, Antimicrobial Resistance and Phylogenetic Characterization of Yersinia enterocolitica in Retail Poultry Meat and Swine Feces in Parts of China. Food Control 2018, 93, 121–128. [Google Scholar] [CrossRef]
- Seoane, A.; García Lobo, J.M. Identification of a Streptogramin A Acetyltransferase Gene in the Chromosome of Yersinia enterocolitica. Antimicrob Agents Chemother. 2000, 44, 905–909. [Google Scholar] [CrossRef] [PubMed]
- Bhagat, N.; Virdi, J.S. The Enigma of Yersinia enterocolitica Biovar 1A. Crit. Rev. Microbiol. 2011, 37, 25–39. [Google Scholar] [CrossRef]
- Sihvonen, L.M.; Hallanvuo, S.; Haukka, K.; Skurnik, M.; Siitonen, A. The ail Gene Is Present in Some Yersinia enterocolitica Biotype 1A Strains. Foodborne Pathog. Dis. 2011, 8, 455–457. [Google Scholar] [CrossRef]
- Platt-Samoraj, A. Toxigenic Properties of Yersinia enterocolitica Biotype 1A. Toxins 2022, 14, 118. [Google Scholar] [CrossRef]
- Pierson, D.E.; Falkow, S. Nonpathogenic Isolates of Yersinia enterocolitica Do Not Contain Functional Inv-Homologous Sequences. Infect. Immun. 1990, 58, 1059–1064. [Google Scholar] [CrossRef]
- Tomino, Y.; Andoh, M.; Horiuchi, Y.; Shin, J.; Ai, R.; Nakamura, T.; Toda, M.; Yonemitsu, K.; Takano, A.; Shimoda, H.; et al. Surveillance of Shiga Toxin-Producing Escherichia coli and Campylobacter spp. in Wild Japanese Deer (Cervus nippon) and Boar (Sus scrofa). J. Vet. Med. Sci. 2020, 82, 1287–1294. [Google Scholar] [CrossRef]
- Fitzgerald, S.F.; Mitchell, M.C.; Holmes, A.; Allison, L.; Chase-Topping, M.; Lupolova, N.; Wells, B.; Gally, D.L.; McNeilly, T.N. Prevalence of Shiga Toxin-Producing Escherichia coli O157 in Wild Scottish Deer with High Human Pathogenic Potential. Animals 2023, 13, 2795. [Google Scholar] [CrossRef]
- Lauzi, S.; Luzzago, C.; Chiani, P.; Michelacci, V.; Knijn, A.; Pedrotti, L.; Corlatti, L.; Buccheri Pederzoli, C.; Scavia, G.; Morabito, S.; et al. Free-ranging Red Deer (Cervus elaphus) as Carriers of Potentially Zoonotic Shiga Toxin-producing Escherichia coli. Transbound. Emerg. Dis. 2022, 69, 1902–1911. [Google Scholar] [CrossRef]
- Heredia, N.; García, S. Animals as Sources of Food-Borne Pathogens: A Review. Anim. Nutr. 2018, 4, 250–255. [Google Scholar] [CrossRef]
- Giuggioli, G.; Olivastri, A.; Pennisi, L.; Paludi, D.; Ianieri, A.; Vergara, A. The Hygiene-Sanitary Control in the Wild Game Meats. Ital. J. Food Saf. 2018, 6, 6875. [Google Scholar] [CrossRef] [PubMed]
Target | Primer Sequence (5′-3′) | Size | |
---|---|---|---|
prfa | Forward | GAT ACA GAA ACA TCG GTT GGC | 274 |
Reverse | GTG TAA CTT GAT GCC ATC AGG | ||
prs | Forward | GCT GAA GAG ATT GCG AAA GAA G | 370 |
Reverse | CAA AGA AAC CTT GGA TTT GCG G | ||
lmo0737 | Forward | AGG GCT TCA AGG ACT TAC CC | 691 |
Reverse | ACG ATT TCT GCT TGC CAT TC | ||
lmo1118 | Forward | AGG GGT CTT AAA TCC TGG AA | 906 |
Reverse | CGG CTT GTT CGG CAT ACT TA | ||
orf 2819 | Forward | AGC AAA ATG CCA AAA CTC GT | 471 |
Reverse | CAT CAC TAA AGC CTC CCA TTG | ||
orf 2110 | Forward | AGT GGA CAA TTG ATT GGT GAA | 597 |
Reverse | CAT CCA TCC CTT ACT TTG GAC |
Target | Oligo Sequence | |
---|---|---|
stx1 | Primer Forward | TTT GTY ACT GTSA CAG CWG AAG CYT TAC G |
Primer Reverse | CCC CAG TTC ARW GTR AGR TCM ACR TC | |
Probe | CTG GAT GAT CTC AGT GGG CGT TCT TAT GTA A | |
stx2 | Primer Forward | TTT GTY ACT GTSA CAG CWG AAG CYT TAC G |
Primer Reverse | CCC CAG TTC ARW GTR AGR TCM ACR TC | |
Probe | TCG TCA GGC ACT GTC TGA AAC TGC TCC | |
eae | Primer Forward | CAT TGA TCA GGA TTT TTC TGG TGA TA |
Primer Reverse | CTC ATG CGG AAA TAG CCG TTA | |
Probe | ATA GTC TCG CCA GTA TTC GCC ACC AAT ACC |
Salmonella spp. | Listeria monocytogenes | Yersinia enterocolitica | Shiga Toxin-Producing E. coli (STEC) | ||||||
---|---|---|---|---|---|---|---|---|---|
Matrix | Wildlife | No. of Samples Tested | No. Positive | No. of Samples Tested | Positive | No. of Samples Tested | Positive | No. of Samples Tested | Positive |
Liver | Chamois | 35 | 0 | 34 | 0 | 31 | 2 | 34 | 0 |
Roe deer | 22 | 0 | 22 | 0 | 18 | 0 | 18 | 0 | |
Wild boar | 27 | 0 | 28 | 2 | 27 | 5 | 24 | 0 | |
Deer | 26 | 0 | 26 | 0 | 25 | 1 | 24 | 0 | |
Total | 110 | 0 | 110 | 2 | 101 | 8 | 100 | 0 |
Salmonella spp. | HEV | ||||
---|---|---|---|---|---|
Matrix | Wildlife | No. of Samples Tested | No. Positive | No. of Samples Tested | Positive |
Muscle | Chamois | 42 | 0 | 26 | 0 |
Roe deer | 21 | 0 | 15 | 0 | |
Wild boar | 34 | 0 | 30 | 0 | |
Deer | 39 | 0 | 12 | 0 | |
Total | 136 | 0 | 83 | 0 |
Strain | Species Identification | CgMLST | MLST | Genotypic Antibiotic Resistance | Virulence Genes |
---|---|---|---|---|---|
1 | Y. enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ystB, myfA, ymoA, invA |
2 | Y enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ystB, myfA, ymoA, invA |
3 | Y. enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ail, ystB, myfA, ymoA, invA |
4 | Y. enterocolitica | 1695 | n.d. | Streptogramin, beta-lactam | ystB, myfA, ymoA, invA |
5 | Y. enterocolitica | 1695 | n.d. | Streptogramin, beta-lactam | ystB, myfA, ymoA, invA |
6 | Y. enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ail, ystB, myfA, ymoA, invA |
7 | Y. enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ail, ystB, myfA, ymoA, invA |
8 | Y. enterocolitica | 1674 | n.d. | Streptogramin, beta-lactam | ail, ystB, myfA, ymoA, invA |
9 | L. monocytogenes | n.d. | 21 | Fosfomycin | inlA, inlB, lpeA, lntA, pgdA, inlC, inlk, lplA1, svpA, uHpt, prfA, prsA2 |
10 | L. monocytogenes | n.d. | 451 | Fosfomycin | ActA, Ami, Lap, LapB, OatA, bsh, fbpA, inlA, inlB, inlC, inlF, inlJ, inlk, lntA, lpeA, lplA1, pgdA, svpA, uHpt, vip |
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Floris, I.; Vannuccini, A.; Ligotti, C.; Musolino, N.; Romano, A.; Viani, A.; Bianchi, D.M.; Robetto, S.; Decastelli, L. Detection and Characterization of Zoonotic Pathogens in Game Meat Hunted in Northwestern Italy. Animals 2024, 14, 562. https://doi.org/10.3390/ani14040562
Floris I, Vannuccini A, Ligotti C, Musolino N, Romano A, Viani A, Bianchi DM, Robetto S, Decastelli L. Detection and Characterization of Zoonotic Pathogens in Game Meat Hunted in Northwestern Italy. Animals. 2024; 14(4):562. https://doi.org/10.3390/ani14040562
Chicago/Turabian StyleFloris, Irene, Andrea Vannuccini, Carmela Ligotti, Noemi Musolino, Angelo Romano, Annalisa Viani, Daniela Manila Bianchi, Serena Robetto, and Lucia Decastelli. 2024. "Detection and Characterization of Zoonotic Pathogens in Game Meat Hunted in Northwestern Italy" Animals 14, no. 4: 562. https://doi.org/10.3390/ani14040562
APA StyleFloris, I., Vannuccini, A., Ligotti, C., Musolino, N., Romano, A., Viani, A., Bianchi, D. M., Robetto, S., & Decastelli, L. (2024). Detection and Characterization of Zoonotic Pathogens in Game Meat Hunted in Northwestern Italy. Animals, 14(4), 562. https://doi.org/10.3390/ani14040562