Prevalence and antimicrobial resistance profile in Salmonella spp. isolates from swine food chain


Submitted: 15 July 2021
Accepted: 10 January 2022
Published: 22 June 2022
Abstract Views: 904
PDF: 490
HTML: 15
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

  • Carlotta Lauteri Post-Graduate Specialization School in Food Inspection “G. Tiecco”, Faculty of Veterinary Medicine, University of Teramo, Italy.
  • Anna Rita Festino Post-Graduate Specialization School in Food Inspection “G. Tiecco”, Faculty of Veterinary Medicine, University of Teramo, Italy.
  • Mauro Conter Doctor in Veterinary Medicine, Parma, Italy.
  • Alberto Vergara Post-Graduate Specialization School in Food Inspection “G. Tiecco”, Faculty of Veterinary Medicine, University of Teramo, Italy.

The aim of this survey was to examine the prevalence and the antimicrobial resistance (AMR) of Salmonella spp. isolated from swine food chain. A total of 435 samples were collected: 360 from slaughterhouse (150 carcasses, 30 cecal samples, 180 environmental samples) and 75 from Italian traditional pork dry sausages. Thirty-six Salmonella were isolated and identified by Polymerase Chain Reaction (PCR): 13,3% (4/30) in fecal samples, 5,5% (10/180) in environmental samples, 7,3% (11/150) in carcasses, and 14,6% (11/75) in Italian traditional dry sausages. Salmonella serotypes were: S. Typhimurium (44,4%), S. Typhimurium monophasic variant (8,3%), S. Typhi (2,8%), S. Enteritidis (22,2%), S. Rissen (16,6%) and S. Derby (5,5%). Phenotypic and genotypic characterization of AMR Salmonella spp. isolates was executed through automatic system (VITEK 2, bioMèrieux) and PCR assays. Salmonella spp. showed phonotypical and genotypical resistance to at least one or more classes of antibiotic. All Salmonella spp. were resistant to aminoglycoside (amikacin and tobramycin) and gentamicin, 86,1% strains were resistant to tetracycline, 55,5% strains were resistant to ampicillin and piperacillin, 25% strains to trimethoprim, 5,5% strains to chloramphenicol, 2,8% strains to amoxicillin/ clavulanic acid, and nitrofurantoin. Among Salmonella isolates, the most detected AMR genes were catA for chloramphenicol (94,4%), nitrofuran nfsA (77.7%), nfsB (86,1%) and, for fluoroquinolone par C (100%) and gyrA (94,4%). This study reported epidemiological data regarding Salmonella spp. and AMR’s circulation in the swine food chain. This phenomenon (AMR) has critical repercussions on the final consumer health; therefore, it represents a crucial One-Health issue.


Aarestrup FM, 2005. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Bas Clin Phar Tox 96:271-81. DOI: https://doi.org/10.1111/j.1742-7843.2005.pto960401.x

Alcaine SD, Warnick LD, Wiedmann M, 2006. Antimicrobial Resistance in nontyphoidal Salmonella. J Food Prot 70:780-90. DOI: https://doi.org/10.4315/0362-028X-70.3.780

Astorga RJM, Salaberria AE, Garcìa AM, Jimenez SV, Martinez AC, Garcìa AA, Casas A, 2007. Surveillance and antimicrobial resistence of Salmonella strains isolated from slaughtered pigs in Spain. J Food Prot 70:1502-6. DOI: https://doi.org/10.4315/0362-028X-70.6.1502

Baptista FM, Dahl J, Nielsen LR, 2010. Factors influencing Salmonella carcass prevalence in Danish pig abattoirs. Prev Vet Med 95:231-8. DOI: https://doi.org/10.1016/j.prevetmed.2010.04.007

Bonardi S, 2017. Salmonella in the pork production chain and its impact on human health in the European Union. Epid Infec 145:1513-26. DOI: https://doi.org/10.1017/S095026881700036X

Calayag AMB, Paclibare PAP, Santos PDM, Bautista CAC, Rivera WL, 2017. Molecular characterization and antimicrobial resistance of Salmonella enterica from swine slaughtered in two different types of Philippine abattoir. Food Microbiol 65:51-56. DOI: https://doi.org/10.1016/j.fm.2017.01.016

Crump AJ, Sjoulond-Karlsson M, Gordon MA, Parrye CM, 2015. Epidemiology clincial presentation, laboratory diagnosis, antimicrobial resistance and antimicrobial management of invasive Salmonella infection. Clin Microbiol Rev Oct 28:901-37. DOI: https://doi.org/10.1128/CMR.00002-15

de la Torre E, Zapata D, Tello M, Mejia W, Frias N, Garcia Pena FJ, Mateu EM, Torre E, 2003. Several Salmonella enterica subsp. enterica serotype 4,5,12:i:- phage types isolated from swine samples originate from serotype typhimurium DT U302. J Clin Microbiol 41:2395–400. DOI: https://doi.org/10.1128/JCM.41.6.2395-2400.2003

Deekshit VK, Kumar BK, Rai P, Srikumar S, Karunasagar I, 2012. Detection of class 1 integrons in Salmonella Weltevreden and silent antibiotic resistance genes in some seafood-associated nontyphoidal isolates of Salmonella in south-west coast of India. J App Microbiol 112:1113-22. DOI: https://doi.org/10.1111/j.1365-2672.2012.05290.x

Di Ciccio P, Ossiprandi MC, Zanardi E, Ghidini S, Belluzzi G, Vergara , Ianieri A, 2016. Microbiological contamination in three lare-scale pig slaughterhouses in Northern Italy. Ital J Food Saf 5:6151. DOI: https://doi.org/10.4081/ijfs.2016.6151

EFSA, 2014. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA Journal 12. DOI: https://doi.org/10.2903/j.efsa.2014.3547

EFSA, 2021. The European Union One Health 2019 Zoonoses Report. EFSA Journal 19:6406. DOI: https://doi.org/10.2903/j.efsa.2021.6406

EFSA, 2021. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA Journal 19:6490 DOI: https://doi.org/10.2903/j.efsa.2021.6490

European commission, 2003. Regulation (EC) No 1831/2003 of the European Parliament and of the council on additives for use in animal nutrition. In Official Journal, L268, pp. 29-39.

European commission, 2005. Regulation (EC) N.2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. In: Official Journal, L338, pp. 1-26.

European commission, 2014. Regulation (EU) n. 217/2014 of 7 March 2014 amending Regulation (EC9 n. 2073/2005 as regards Salmonella in pig carcasses. In Official Journal, L69, pp. 93-94.

European commission, 2015. Regulation (EU) n. 1474/2015 of 27 August 2015 concerning the use of recycled hot water to remove microbiological surface contamination from carcasses. In Official Journal, L225/7, pp. 83-85.

Fedorka-Cray PJ, Gray JT, Wray C. Salmonella infections in pigs. In: Wray C, Wray A, eds. Salmonella in Domestic Animals. Wallingford: CAB International, 2000, pp. 191–207. DOI: https://doi.org/10.1079/9780851992617.0191

Hauser E, Tietze E, Helmuth R, 2010. Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol 76:4601–10. DOI: https://doi.org/10.1128/AEM.02991-09

Hur J, Jawale C, Lee JH, et al, 2012. Antimicrobial resistance of Salmonella isolated from food animals: A review. Food Res Inter 45:819-30. DOI: https://doi.org/10.1016/j.foodres.2011.05.014

Hurd HS, Mc Kean JD, Griffith RW, Wesley IV, Rostagno MH, 2002. Salmonella enterica infections in market swine before and after transport and holding. Appl Envirom Microbiol 68:2376–81. DOI: https://doi.org/10.1128/AEM.68.5.2376-2381.2002

Kikuvi GM, Ombui JN, Mitema ES, 2010. Serotypes and antimicrobial residence profiles of Salmonella isolates from pigs at slaughter in Kenya. J Infect Dev Ctries 4:243-8. DOI: https://doi.org/10.3855/jidc.446

Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C, 2009.Antimicrobial Resistance in Escherichia coli Isolates from Swine and Wild Small Mammals in the Proximity of Swine Farms and in Natural Environments in Ontario, Can Appl Environ Microbiol, 559-566. DOI: https://doi.org/10.1128/AEM.01821-08

Lekagul A, Tangcharoensathien V, Yeung S, 2019. Patterns of antibiotic use in global pig production: a systemic review. Vet and Anim Scien 7;100058. DOI: https://doi.org/10.1016/j.vas.2019.100058

Lucarelli C, Dionisi AM, Torpdahl M, Villa L, Graziani C, Hopkins K, Threlfall J, Caprioli A, Luzzi I, 2010. Evidence for a second genomic island conferring multidrug resistance in a clonal group of strains of Salmonella enterica serovar Ty- phimurium and its monophasic variant circulating in Italy, Denmark, and the United Kingdom. J Clin Microbiol 48:2103–9. DOI: https://doi.org/10.1128/JCM.01371-09

Miller AJ, Twomey DF, Davies RH, Teale CJ, Williamson SM, Reichel R, Featherstone CA, Cook AJC, Snow LC, Armstrong JD, 2011. Salmonella serovars and antimicrobial resistance patterns on a sample of high seroprevalence pig farms in England and Wales (2003-2008). Zoon Publ Health 58:549–59. DOI: https://doi.org/10.1111/j.1863-2378.2011.01402.x

Molla B, Alemayehu D, Salah W, 2003. Spruces and distribution of Salmonella serotypes isolated from food animals, slaughterhouse personnel and retail meat products in Etiopia 1997-2002. Ethiop J Health Dev 17:63-70. DOI: https://doi.org/10.4314/ejhd.v17i1.9782

Mossong J, Marques P, Ragimbeau C, Huberty-Krau P, Losch S, Meyer G, Moris G, Strottner C, Rabsch W, Schneider F, 2006. Outbreaks of monophasic Salmonella enterica serovar 4,[5],12: i:- in Luxembourg. Euro Surveill 2007;12:E11–2. DOI: https://doi.org/10.2807/esm.12.06.00719-en

Mourao J, Novais C, Machado J, et al, 2015. Metal tolerance in emerging clinically relevant multidrug-resistant Salmonella enterica serotype 4,[5],12:i:- clones circulating in Europe. Int J Antimicrob Agents 45:610–6. DOI: https://doi.org/10.1016/j.ijantimicag.2015.01.013

Prasertsee T, Nattakarn K, Panuwat Y, Pannita S, Chokesajjawatee N, Patchanee P, 2016. Repertitive sequence-based PCR fingerprinting and the relationship of antimicrobial-resistence characteristics and corresponding genes among Salmonella strains from pig production. Asian Pac J Trop Dis 6:390-5. DOI: https://doi.org/10.1016/S2222-1808(15)61054-4

Shane AL, Mody RK, Crump JA, 2017. Infectious Diseases Society of America clinical practice guidelines for the diagnosis and management of infectious diarrhea. Clin Infect Dis 65:e45–80. DOI: https://doi.org/10.1093/cid/cix669

Valero A, Hernandez M, De Cesare A, Manfreda G, Garcia-Gimero RM, Gonzalez-Garcia P, Rodriguez-Lazaro D, 2014. Probabilistic approach for determining Salmonella spp. and L. monocytogenes concentration in pork meat from presence/absence microbiological data. Int J Food Microbiol 184:60-3. DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.02.025

Wang H, Ye K, Wei X, Cao J, Xu X, Zhou G, 2013. Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolated from resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control 33:378-84. DOI: https://doi.org/10.1016/j.foodcont.2013.03.030

1.
Lauteri C, Festino AR, Conter M, Vergara A. Prevalence and antimicrobial resistance profile in <em>Salmonella</em> spp. isolates from swine food chain. Ital J Food Safety [Internet]. 2022 Jun. 22 [cited 2024 May 12];11(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/9980

Downloads

Download data is not yet available.

Citations


Similar Articles

You may also start an advanced similarity search for this article.