189
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Revealing microbial community composition and disinfection efficacy evaluation in wholesale pork markets through 16S rDNA sequencing

, , , , , , , , & show all
Article: 2351906 | Received 22 Nov 2023, Accepted 01 May 2024, Published online: 20 May 2024

References

  • Andritsos, N., Mataragas, M., Mavrou, E., Stamatiou, A., & Drosinos, E. (2012). The microbiological condition of minced pork prepared at retail stores in Athens, Greece. Meat Science, 91(4), 486–11. https://doi.org/10.1016/j.meatsci.2012.02.036
  • Aráoz, R., Anhalt, E., René, L., Badet-Denisot, M.-A., Courvalin, P., & Badet, B. (2000). Mechanism-based inactivation of VanX, a d-alanyl-d-alanine dipeptidase necessary for vancomycin resistance. Biochemistry, 39(51), 15971–15979. https://doi.org/10.1021/bi001408b
  • Bassey, A., Chen, Y., Zhu, Z., Odeyemi, O., Gao, T., Olusola, O., Ye, K., Li, C., & Zhou, G. H. (2021). Evaluation of spoilage indexes and bacterial community dynamics of modified atmosphere packaged super-chilled pork loins. Food Control, 130, 108383. https://doi.org/10.1016/j.foodcont.2021.108383
  • Bessems, E. (1998). The effect of practical conditions on the efficacy of disinfectants. International Biodeterioration & Biodegradation, 41(3), 177–183. https://doi.org/10.1016/S0964-8305(98)00022-5
  • Brooks, B. W., Devenish, J., Lutze-Wallace, C. L., Milnes, D., Robertson, R. H., & Berlie-Surujballi, G. (2004). Evaluation of a monoclonal antibody-based enzyme-linked immunosorbent assay for detection of Campylobacter fetus in bovine preputial washing and vaginal mucus samples. Veterinary Microbiology, 103(1), 77–84. https://doi.org/10.1016/j.vetmic.2004.07.008
  • Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583. https://doi.org/10.1038/nmeth.3869
  • Camara, P. G. (2018). Methods and challenges in the analysis of single-cell RNA-sequencing data. Current Opinion in Systems Biology, 7, 47–53. https://doi.org/10.1016/j.coisb.2017.12.007
  • Cauchie, E., Delhalle, L., Taminiau, B., Tahiri, A., Korsak, N., Burteau, S., Fall, P. A., Farnir, F., Baré, G., & Daube, G. (2020). Assessment of spoilage bacterial communities in food wrap and modified atmospheres-packed minced pork meat samples by 16S rDNA metagenetic analysis [Original Research]. Frontiers in Microbiology, 10, 10. https://doi.org/10.3389/fmicb.2019.03074
  • Charmpi, C., Van der Veken, D., Van Reckem, E., De Vuyst, L., & Leroy, F. (2020). Raw meat quality and salt levels affect the bacterial species diversity and community dynamics during the fermentation of pork mince. Food Microbiology, 89, 103434. https://doi.org/10.1016/j.fm.2020.103434
  • Cheung, P.-Y., Lo, K., Cheung, T., Yeung, W., Leung, P., & Kam, K. (2008). Streptococcus suis in retail markets: How prevalent is it in raw pork? International Journal of Food Microbiology, 127(3), 316–320. https://doi.org/10.1016/j.ijfoodmicro.2008.08.006
  • Cobo Díaz, J., Alvarez-Molina, A., Oniciuc, E., Walsh, C., Mencía-Ares, O., Puente-Gómez, P., Likotrafiti, E., Fernández-Gómez, P., Prieto, B., Crispie, F., Ruiz, L., Gonzalez-Raurich, M., López, M., Prieto, M., Cotter, P., & Alvarez-Ordóñez, A. (2021). Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity. Microbiome, 9(1), 204. https://doi.org/10.1186/s40168-021-01131-9
  • Correia Peres Costa, J., Bover-Cid, S., Bolívar, A., Cosano, G., & Pérez-Rodríguez, F. (2019). Modelling the interaction of the sakacin-producing Lactobacillus sakei CTC494 and listeria monocytogenes in filleted gilthead sea bream (Sparus aurata) under modified atmosphere packaging at isothermal and non-isothermal conditions. International Journal of Food Microbiology, 297, 72–84. https://doi.org/10.1016/j.ijfoodmicro.2019.03.002
  • De Filippis, F., Storia, A., Villani, F., & Ercolini, D. (2018). Strain-level diversity analysis of Pseudomonas fragi after in situ pangenome reconstruction shows distinctive spoilage-associated metabolic traits clearly selected by different storage conditions. Applied and Environmental Microbiology, 85. https://doi.org/10.1128/AEM.02212-18
  • Del Blanco, A., Caro, I., Quinto, E. J., & Mateo, J. (2017). Quality changes in refrigerated stored minced pork wrapped with plastic cling film and the effect of glucose supplementation. Meat Science, 126, 55–62. https://doi.org/10.1016/j.meatsci.2016.12.007
  • Demaître, N., Van Damme, I., De Zutter, L., Geeraerd, A. H., Rasschaert, G., & De Reu, K. (2020). Occurrence, distribution and diversity of listeria monocytogenes contamination on beef and pig carcasses after slaughter. Meat Science, 169, 108177. https://doi.org/10.1016/j.meatsci.2020.108177
  • Emamjomeh, M., Mohd Hashim, A., Abdul-Mutalib, N., Khairil Mokhtar, N., Mustapha, N. A., Maeda, T., & Amin Nordin, S. (2023). Profiling bacterial communities and foodborne pathogens on food-associated surface following contact with raw beef, chicken and pork using 16S amplicon metagenomics. Food Control, 149, 109698. https://doi.org/10.1016/j.foodcont.2023.109698
  • Ercolini, D. (2013). High-throughput sequencing and metagenomics: Moving forward in the culture-independent analysis of food microbial ecology. Applied and Environmental Microbiology, 79(10), 3148–3155. https://doi.org/10.1128/AEM.00256-13
  • Ercolini, D., Casaburi, A., Nasi, A., Ferrocino, I., DiMonaco, R., Ferranti, P., Mauriello, G., & Villani, F. (2010). Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. International Journal of Food Microbiology, 142(1–2), 120–131. https://doi.org/10.1016/j.ijfoodmicro.2010.06.012
  • Illikoud, N., Rossero, A., Chauvet, R., Courcoux, P., Pilet, M.-F., Charrier, T., Jaffrès, E., & Zagorec, M. (2019). Genotypic and phenotypic characterization of the food spoilage bacterium brochothrix thermosphacta. Food Microbiology, 81, 22–31. https://doi.org/10.1016/j.fm.2018.01.015
  • Janse, R. J., Hoekstra, T., Jager, K. J., Zoccali, C., Tripepi, G., Dekker, F. W., & van Diepen, M. (2021). Conducting correlation analysis: Important limitations and pitfalls. Clinical Kidney Journal, 14(11), 2332–2337. https://doi.org/10.1093/ckj/sfab085
  • Johansson, M., Azzouz, M., Häggendal, B., Säljö, K., Malmi, H., Zavialov, A., & Teneberg, S. (2020). Glycosphingolipids recognized by Acinetobacter baumannii. Microorganisms [Internet], 8(4), 612. https://doi.org/10.3390/microorganisms8040612
  • Kadariya, J., Smith, T. C., & Thapaliya, D. (2014). Staphylococcus aureus and Staphylococcal Food-Borne disease: An ongoing challenge in public health. Biomed Research International, 2014, 827965. https://doi.org/10.1155/2014/827965
  • Kameník, J., Dušková, M., Šedo, O., Saláková, A., Pavlík, Z., Zdráhal, Z., & Karpíšková, R. (2015). Lactic acid bacteria in hot smoked dry sausage (non-fermented salami): Thermal resistance of Weissella viridescens strains isolated from hot smoked dry sausages. LWT - Food Science and Technology, 61(2), 492–495. https://doi.org/10.1016/j.lwt.2014.12.012
  • Kang, G., Seong, P.-N., Moon, S., Cho, S., Ham, H.-J., Park, K., Kang, S. M., & Park, B.-Y. (2014). Distribution channel and microbial characteristics of pig by-products in Korea. Korean Journal for Food Science of Animal Resources, 34(6), 792–798. https://doi.org/10.5851/kosfa.2014.34.6.792
  • Khatoon, Z., McTiernan, C. D., Suuronen, E. J., Mah, T.-F., & Alarcon, E. I. (2018). Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon, 4(12), e01067. https://doi.org/10.1016/j.heliyon.2018.e01067
  • Knight, R., Vrbanac, A., Taylor, B., Aksenov, A., Callewaert, C., Debelius, J., González, A., Kosciolek, T., McCall, L.-I., McDonald, D., Melnik, A., Morton, J., Navas, J., Quinn, R., Sanders, J., Swafford, A., Thompson, L., Tripathi, A. … Caporaso, J. G. (2018). Best practices for analysing microbiomes. Nature Reviews Microbiology, 16(7), 410–422. https://doi.org/10.1038/s41579-018-0029-9
  • Lagier, J.-C., Khelaifia, S., Tidjani Alou, M., Ndongo, S., Niokhor, D., Hugon, P., Caputo, A., Cadoret, F., Traore, S., Seck, E., Dubourg, G., Durand, G., Gaël, M., Guilhot, E., Togo, A., Bellali, S., Bachar, D., Cassir, N. … Levasseur, A. (2016). Culture of previously uncultured members of the human gut microbiota by culturomics. Nature Microbiology, 1(12). https://doi.org/10.1038/nmicrobiol.2016.203
  • Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., Beiko, R. G., & Huttenhower, C. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology, 31(9), 814–821. https://doi.org/10.1038/nbt.2676
  • Li, N., Zhang, Y., Wu, Q., Gu, Q., Chen, M., Zhang, Y., Sun, X., & Zhang, J. (2019). High-throughput sequencing analysis of bacterial community composition and quality characteristics in refrigerated pork during storage. Food Microbiology, 83, 86–94. https://doi.org/10.1016/j.fm.2019.04.013
  • Li, Y., Tan, X., Zhao, X., Xu, Z.-F., Dai, W., Duan, W., Huang, S., Zhang, E., Liu, J., Zhang, S., Yin, R., Shi, X., Lu, Z., & Pan, Y. (2020). Composition and function of oral microbiota between gingival squamous cell carcinoma and periodontitis. Oral Oncology, 107, 104710. https://doi.org/10.1016/j.oraloncology.2020.104710
  • Lim, S.-M., Lee, N.-K., & Paik, H.-D. (2019). Antibacterial and anticavity activity of probiotic lactobacillus plantarum 200661 isolated from fermented foods against streptococcus mutans. LWT, 118, 108840. https://doi.org/10.1016/j.lwt.2019.108840
  • Mahros, M., Abd-Elghany, S., & Sallam, K. (2021). Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern. International Journal of Food Microbiology, 346, 109165. https://doi.org/10.1016/j.ijfoodmicro.2021.109165
  • Møretrø, T., & Langsrud, S. (2017). Residential bacteria on surfaces in the food industry and their implications for food safety and quality: Residential bacteria in food industry …. Comprehensive Reviews in Food Science and Food Safety, 16(5), 1022–1041. https://doi.org/10.1111/1541-4337.12283
  • Naïtali, M., Dubois-Brissonnet, F., Cuvelier, G., & Bellon-Fontaine, M.-N. (2009). Effects of pH and oil-in-water emulsions on growth and physicochemical cell surface properties of listeria monocytogenes: Impact on tolerance to the bactericidal activity of disinfectants. International Journal of Food Microbiology, 130(2), 101–107. https://doi.org/10.1016/j.ijfoodmicro.2009.01.008
  • Nearing, J. T., Connors, J., Whitehouse, S., Van Limbergen, J., Macdonald, T., Kulkarni, K., & Langille, M. G. I. (2019). Infectious complications are associated with alterations in the gut microbiome in pediatric patients with acute lymphoblastic leukemia [Original Research]. Frontiers in Cellular and Infection Microbiology, 9, 9. https://doi.org/10.3389/fcimb.2019.00028
  • O’Brien, T. (2002). Emergence, spread, and environmental effect of antimicrobial resistance: How use of an antimicrobial anywhere can increase resistance to any antimicrobial anywhere else. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 34(Suppl 3), S78–84. https://doi.org/10.1086/340244
  • Peruzy, M. F., Houf, K., Joossens, M., Yu, Z., Therese, Y., Proroga, R., & Murru, N. (2020). Evaluation of microbial contamination of different pork carcass areas through culture-dependent and independent methods in small-scale slaughterhouses. International Journal of Food Microbiology, 336. https://doi.org/10.1016/j.ijfoodmicro.2020.108902
  • Sato, Y., Ishihara, M., Nakamura, S., Fukuda, K., Kuwabara, M., Takayama, T., Hiruma, S., Murakami, K., Fujita, M., & Yokoe, H. (2019). Comparison of various disinfectants on bactericidal activity under organic matter contaminated environments. Biocontrol Science, 24(2), 103–108. https://doi.org/10.4265/bio.24.103
  • Stellato, G., La Storia, A., De Filippis, F., Borriello, G., Villani, F., Ercolini, D., & Elkins, C. A. (2016). Overlap of spoilage-associated microbiota between meat and the meat processing environment in small-scale and large-scale retail distributions. Applied and Environmental Microbiology, 82(13), 4045–4054. https://doi.org/10.1128/AEM.00793-16
  • Tassou, C., Argyri, A., Doulgeraki, A., Nychas, G.-J., Chorianopoulos, N., Grounta, A., Dourou, D., & Spyrelli, E. (2021). Microbiota of chicken breast and thigh fillets stored under different refrigeration temperatures by next generation sequencing. Foods, 10(4), 10. https://doi.org/10.3390/foods10040765
  • Tong, C., Hu, H., Chen, G., Li, Z., Aifeng, L., & Zhang, J. (2021). Chlorine disinfectants promote microbial resistance in pseudomonas sp. Environmental Research, 199, 111296. https://doi.org/10.1016/j.envres.2021.111296
  • Tong, C., Hu, H., Chen, G., Li, Z., Li, A., & Zhang, J. (2021). Disinfectant resistance in bacteria: Mechanisms, spread, and resolution strategies. Environmental Research, 195, 110897. https://doi.org/10.1016/j.envres.2021.110897
  • Tong, S., Ma, L., Ronholm, J., Hsiao, W., & Lu, X. (2021). Whole genome sequencing of campylobacter in agri-food surveillance. Current Opinion in Food Science, 39, 130–139. https://doi.org/10.1016/j.cofs.2020.12.020
  • Velez, F. J., Bosilevac, J. M., & Singh, P. (2021). Validation of high-resolution melting assays for the detection of virulent strains of Escherichia coli O26 and O111 in beef and pork enrichment broths. Food Control, 128, 108123. https://doi.org/10.1016/j.foodcont.2021.108123
  • Vojkovska, H., Karpiskova, R., Kajsiková, M., & Drahovska, H. (2015). Characterization of cronobacter spp. isolated from food of plant origin and environmental samples collected from farms and from supermarkets in the Czech Republic. International Journal of Food Microbiology, 217, 130–136. https://doi.org/10.1016/j.ijfoodmicro.2015.10.017
  • Wang, Z., Fang, Y., Zhi, S., Simpson David, J., Gill, A., McMullen Lynn, M., Neumann Norman, F., Gänzle Michael, G., & Björkroth, J. (2020). The locus of heat resistance confers resistance to chlorine and other oxidizing chemicals in Escherichia coli. Applied and Environmental Microbiology, 86(4), e02123–02119. https://doi.org/10.1128/AEM.02123-19
  • Wickramasinghe, N. N., Ravensdale, J., Coorey, R., Dykes, G. A., & Chandry, P. S. (2021). Transcriptional profiling of biofilms formed on chilled beef by psychrotrophic meat spoilage bacterium, Pseudomonas fragi 1793. Biofilm, 3, 100045. https://doi.org/10.1016/j.bioflm.2021.100045
  • Wilson, C. N., Pulford, C. V., Akoko, J., Perez Sepulveda, B., Predeus, A. V., Bevington, J., Duncan, P., Hall, N., Wigley, P., Feasey, N., Pinchbeck, G., Hinton, J. C. D., Gordon, M. A., Fevre, E. M., & Bourret, T. J. (2020). Salmonella identified in pigs in Kenya and Malawi reveals the potential for zoonotic transmission in emerging pork markets. PloS Neglected Tropical Diseases, 14(11), e0008796. https://doi.org/10.1371/journal.pntd.0008796
  • Wu, J., Li, R., Zhang, M., Shan, K., Jia, X., Zhao, D., Nian, Y., & Li, C. (2021). Microbiota changes on the surface of pig carcasses during refrigerated transportation and marketing. Food Materials Research[Cdata[food materials research]], 1(1), 1–9. https://doi.org/10.48130/FMR-2021-0004
  • Xiao, X., Wang, W., Zhang, J., Liao, M., Rainwater, C., Yang, H., & Li, Y. (2021). A quantitative risk assessment model of salmonella contamination for the yellow-feathered broiler chicken supply chain in China. Food Control, 121, 107612. https://doi.org/10.1016/j.foodcont.2020.107612
  • Xu, L., Zhang, C. M., & Xu, P. (2017). Mechanisms of ultraviolet disinfection and chlorination of Escherichia coli: Culturability, membrane permeability, metabolism, and genetic damage. Journal of Environmental Sciences, 65. https://doi.org/10.1016/j.jes.2017.07.006
  • Xu, S., Lu, W., Liu, Y., Ming, Z., Liu, Y., Meng, R., & Wang, H. (2016). Structure and diversity of bacterial communities in two large sanitary landfills in China as revealed by high-throughput sequencing (MiSeq). Waste Management, 63, 41–48. https://doi.org/10.1016/j.wasman.2016.07.047
  • Xu, Y., Yang, G., Xu, J., Guan, X., Li, R., & Wang, S. (2022). Influence of the combination of cinnamon essential oil nanoemulsions and epsilon-polylysine on microbial community and quality of pork during refrigerated period and radio frequency cooking. International Journal of Food Microbiology, 381, 109911. https://doi.org/10.1016/j.ijfoodmicro.2022.109911
  • Yang, C., Che, Y., Qi, Y., Liang, P., & Song, C. (2016). High-throughput sequencing of viable microbial communities in raw pork subjected to a fast cooling process. Journal of Food Science, 82. https://doi.org/10.1111/1750-3841.13566
  • Yi, Z., Yan, J., Ding, Z., & Xie, J. (2022). The HD-GYP domain protein of shewanella putrefaciens YZ08 regulates biofilm formation and spoilage activities. Food Research International, 157, 111466. https://doi.org/10.1016/j.foodres.2022.111466
  • Zhang, L., Fu, Y., Xiong, Z., Ma, Y., Wei, Y., Qu, X., Zhang, H., Zhang, J., & Liao, M. (2018). Highly prevalent multidrug-resistant salmonella from chicken and pork meat at retail markets in Guangdong, China. Frontiers in Microbiology, 9, 9. https://doi.org/10.3389/fmicb.2018.02104
  • Zhang, Y., Hou, W., Yue, Q., Zhang, Y., Yi, Y., Min, T., & Wang, H. (2021). Effects of environmental humidity on microbial community and quality of chilled fresh pork. SSRN Electronic Journal. https://doi.org/10.2139/ssrn.3964470
  • Zhao, F., Wei, Z., Zhou, G., Kristiansen, K., & Wang, C. (2022). Effects of different storage temperatures on bacterial communities and functional potential in pork meat. Foods, 11(15), 2307. https://doi.org/10.3390/foods11152307
  • Zhao, F., Zhou, G., Ye, K., Wang, S., Xu, X., & Li, C. (2015). Microbial changes in vacuum-packed chilled pork during storage. Meat Science, 100, 145–149. https://doi.org/10.1016/j.meatsci.2014.10.004
  • Zhong, A., Chen, W., Duan, Y., Li, K., Tang, X., Tian, X., Wu, Z., Li, Z., Wang, Y., & Wang, C. (2021). The potential correlation between microbial communities and flavors in traditional fermented sour meat. LWT, 149, 111873. https://doi.org/10.1016/j.lwt.2021.111873
  • Zhou, J., Jin, Y., & Liang, Q. (2022). Effects of regulatory policy mixes on traceability adoption in wholesale markets: Food safety inspection and information disclosure. Food Policy, 107, 102218. https://doi.org/10.1016/j.foodpol.2022.102218
  • Zhu, Z., Shan, L., Zhang, X., Hu, F., Zhong, D., Yuan, Y., & Zhang, J. (2021). Effects of bacterial community composition and structure in drinking water distribution systems on biofilm formation and chlorine resistance. Chemosphere, 264, 128410. https://doi.org/10.1016/j.chemosphere.2020.128410