https://doi.org/10.4081/ijfs.2022.10160
Microbial contamination, antimicrobial resistance and biofilm formation of bacteria isolated from a high-throughput pig abattoir
Submitted: 29 September 2021
Accepted: 26 January 2022
Published: 11 August 2022
Accepted: 26 January 2022
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Supplementary Table: 64
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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.
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The aim of this work was to assess the level of microbial contamination and resistance of bacteria isolated from a highthroughput heavy pig slaughterhouse (approx. 4600 pigs/day) towards antimicrobials considered as critical for human, veterinary or both chemotherapies. Samples, pre-operative and operative, were obtained in 4 different surveys. These comprised environmental sampling, i.e. air (ntotal = 192) and surfaces (ntotal = 32), in four different locations. Moreover, a total of 40 carcasses were sampled in two different moments of slaughtering following Reg. (CE) 2073/2005. Overall, 60 different colonies were randomly selected from VRBGA plates belonging to 20 species, 15 genera and 10 families being Enterobacteriaceae, Moraxellaceae and Pseudomonadaceae the most represented ones. Thirty-seven isolates presented resistance to at least one molecule and seventeen were classified as multi-drug resistant. Enterobacteriaceae, particularly E. coli, displayed high MIC values towards trimethoprim, ampicillin, tetracycline and sulphametoxazole with MICmax of 16, 32, 32 and 512 mg/L, respectively. Moreover, isolated Pseudomonas spp. showed high MIC values in critical antibiotics such as ampicillin and azithromycin with MICmax of 32 and 64 mg/L, respectively. Additionally, in vitro biofilm formation assays demonstrated that fifteen of these isolates can be classified as strong biofilm formers. Results demonstrated that a high diversity of bacteria containing antibiotic resistant and multiresistant species is present in the sampled abattoir. Considering these findings, it could be hypothesised that the processing environment could be a potential diffusion determinant of antibiotic resistant bacteria through the food chain and operators.
Abuoun M, Stubberfield EJ, Duggett NA, Kirchner M, Dormer L, Nunez-Garcia J, Randall LP, Lemma F, Crook DW, Teale C, Smith RP, Anjum MF, 2017. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J Antimicrob Chemother 72:2745-9.
DOI: https://doi.org/10.1093/jac/dkx286
Amador P, Fernandes R, Prudêncio C, Duarte I, 2019. Prevalence of antibiotic resistance genes in multidrug-resistant enterobacteriaceae on portuguese livestock manure. Antibiotics 8:23.
DOI: https://doi.org/10.3390/antibiotics8010023
Blagojevic B, Nesbakken T, Alvseike O, Vågsholm I, Antic D, Johler S, Houf K, Meemken D, Nastasijevic I, Vieira Pinto M, Antunovic B, Georgiev M, Alban L, 2021. Drivers, opportunities, and challenges of the European risk-based meat safety assurance system. Food Control 124:107870.
DOI: https://doi.org/10.1016/j.foodcont.2021.107870
Cosenza-Sutton GH, 2004. Enumeration of total airborne bacteria, yeast and mold contaminants and identification of Escherichia coli O157:H7, Listeria spp., Salmonella spp., and Staphylococcus spp. in a beef and pork slaughter facility. PhD Dissertation - University of Florida.
Di Ciccio P, Ossiprandi MC, Zanardi E, Ghidini S, Belluzzi G, Vergara A, Ianieri A, 2016. Microbiological contamination in three large-scale pig slaughterhouses in Northern Italy. Ital J Food Saf 5:6151
DOI: https://doi.org/10.4081/ijfs.2016.6151
EFSA, 2021. Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. EFSA J 19:6651.
DOI: https://doi.org/10.2903/j.efsa.2021.6651
European Commission, 2005. Reg (CE) 2073/2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union 338. https://doi.org/10.1109/MACE.2010.5536537
DOI: https://doi.org/10.1109/MACE.2010.5536537
Fernstrom A, Goldblatt M, 2013. Aerobiology and Its Role in the Transmission of Infectious Diseases. J Pathog 493960.
DOI: https://doi.org/10.1155/2013/493960
Flemming HC, 2011. The perfect slime. Colloids Surf. B. Biointerfaces 86:251–259.
DOI: https://doi.org/10.1016/j.colsurfb.2011.04.025
Haddrell AE, Thomas RJ, 2017. Aerobiology: Experimental considerations, observations, and future tools. Appl Environ Microbiol 83:809-26.
DOI: https://doi.org/10.1128/AEM.00809-17
Homeier-Bachmann T, Heiden SE, Lübcke PK, Bachmann L, Bohnert JA, Zimmermann D, Schaufler K , 2021. Antibiotic-resistant Enterobacteriaceae in wastewater of abattoirs. Antibiotics 10:568.
DOI: https://doi.org/10.3390/antibiotics10050568
Hrenovic J, Seruga Music M, Durn G, Dekic S, Hunjak B, Kisic I, 2019. Carbapenem-resistant acinetobacter baumannii recovered from swine manure. Microb Drug Resist 25:725-30.
DOI: https://doi.org/10.1089/mdr.2018.0087
I.Stat, 2021. Consistenze degli allevamenti (Consistency of farms) [WWW Document]. URL http://dati.istat.it/Index.aspx?DataSetCode=DCSP_CONSISTENZE# (accessed 7.2.21).
Jericho KWF, Ho J, Kozub GC, 2000. Aerobiology of a high-line speed cattle abattoir. J Food Prot 63:1523–1528.
DOI: https://doi.org/10.4315/0362-028X-63.11.1523
Lerma LL, Benomar N, Casado Muñoz M del C, Gálvez A, Abriouel H, 2014. Antibiotic multiresistance analysis of mesophilic and psychrotrophic Pseudomonas spp. isolated from goat and lamb slaughterhouse surfaces throughout the meat production process. Appl Environ Microbiol 80:6792-806.
DOI: https://doi.org/10.1128/AEM.01998-14
Li L, Olsen RH, Ye L, Yan H, Nie Q, Meng H, Shi L, 2016. Antimicrobial Resistance and Resistance Genes in Aerobic Bacteria Isolated from Pork at Slaughter. J Food Prot 79:589-97.
DOI: https://doi.org/10.4315/0362-028X.JFP-15-455
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL, 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–81.
DOI: https://doi.org/10.1111/j.1469-0691.2011.03570.x
Masotti F, Cattaneo S, Stuknytė M, De Noni I, 2019. Airborne contamination in the food industry: An update on monitoring and disinfection techniques of air. Trends Food Sci Technol 90:147-56
DOI: https://doi.org/10.1016/j.tifs.2019.06.006
Møretrø T, Langsrud S, 2017. Residential Bacteria on Surfaces in the Food Industry and Their Implications for Food Safety and Quality. Compr Rev Food Sci Food Saf 16:1022–41.
DOI: https://doi.org/10.1111/1541-4337.12283
Neog N, Phukan U, Puzari M, Sharma M, Chetia P, 2021. Klebsiella oxytoca and Emerging Nosocomial Infections. Curr Microbiol 78:1115–23.
DOI: https://doi.org/10.1007/s00284-021-02402-2
Nordholt N, Kanaris O, Schmidt SBI, Schreiber F, 2021. Persistence against benzalkonium chloride promotes rapid evolution of tolerance during periodic disinfection. Nat Commun 12: 6792.
DOI: https://doi.org/10.1038/s41467-021-27019-8
Okraszewska-Lasica W, Bolton DJ, Sheridan JJ, McDowell DA, 2014. Airborne Salmonella and Listeria associated with Irish commercial beef, sheep and pig plants. Meat Sci 97:255-61.
DOI: https://doi.org/10.1016/j.meatsci.2014.01.025
Okraszewska-Lasica W, Bolton DJ, Sheridan JJ, McDowell DA, 2012. Comparison of aerial counts at different sites in beef and sheep abattoirs and the relationship between aerial and beef carcass contamination. Food Microbiol 32:325-31.
DOI: https://doi.org/10.1016/j.fm.2012.07.008
Pearce RA, Sheridan JJ, Bolton DJ, 2006. Distribution of airborne microorganisms in commercial pork slaughter processes. Int J Food Microbiol 107:186-91.
DOI: https://doi.org/10.1016/j.ijfoodmicro.2005.08.029
Pereira BMP, Wang X, Tagkopoulos I, 2021. Biocide-Induced Emergence of Antibiotic Resistance in Escherichia coli. Front Microbiol 12:640923.
DOI: https://doi.org/10.3389/fmicb.2021.640923
Prendergast DM, Daly DJ, Sheridan JJ, McDowell D.A., Blair, I.S., 2004. The effect of abattoir design on aerial contamination levels and the relationship between aerial and carcass contamination levels in two Irish beef abattoirs. Food Microbiol. 21:589–96.
DOI: https://doi.org/10.1016/j.fm.2003.11.002
Rodríguez-López P, Rodríguez-Herrera JJ, Cabo ML, 2020. Tracking bacteriome variation over time in Listeria monocytogenes-positive foci in food industry. Int J Food Microbiol 315:108439.
DOI: https://doi.org/10.1016/j.ijfoodmicro.2019.108439
Savin M, Bierbaum G, Hammerl JA, Heinemann C, Parcina M, Sib E, Voigt A, Kreyenschmidt J, 2020. Antibiotic-resistant bacteria and antimicrobial residues in wastewater and process water from German pig slaughterhouses and their receiving municipal wastewater treatment plants. Sci Total Environ 727:138788.
DOI: https://doi.org/10.1016/j.scitotenv.2020.138788
Schwaiger K, Huther S, Hölzel C, Kämpf P, Bauer J, 2012. Prevalence of antibiotic-resistant enterobacteriaceae isolated from chicken and pork meat purchased at the slaughterhouse and at retail in Bavaria, Germany. Int J Food Microbiol 154:206–11.
DOI: https://doi.org/10.1016/j.ijfoodmicro.2011.12.014
Stepanovic S, Vukovic D, Bonaventura GDI, Djukic S, Ruzicka F, 2007. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891–899.
DOI: https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
Supporting Agencies
Ministero della SaluteHow to Cite
1.
Ghidini S, De Luca S, Rodríguez-López P, Simon AC, Liuzzo G, Poli L, Ianieri A, Zanardi E. Microbial contamination, antimicrobial resistance and biofilm formation of bacteria isolated from a high-throughput pig abattoir. Ital J Food Safety [Internet]. 2022 Aug. 11 [cited 2024 Nov. 21];11(3). Available from: https://www.pagepressjournals.org/ijfs/article/view/10160
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