Microbiological Risks in the Poultry Meat Production and Processing Chain: A Systematic Review of the Literature
Keywords:
bacteria, chicken meat, food safety, meat chain, poultryAbstract
Considering the continuous increase in global poultry meat consumption, along with a significant diversification of product ranges and increasingly sophisticated consumer demands, ensuring the microbial safety of carcasses and anatomically processed poultry cuts has become a fundamental priority in the food industry. This paper provides an integrated examination of bacterial contamination throughout the poultry meat processing chain - from poultry farms to the point of consumption - by identifying multiple sources of contamination. Consequently, the necessity of implementing advanced microbiological control strategies is highlighted, relying on rigorous standards and cutting-edge technologies that are essential for ensuring food safety, protecting public health, and optimizing economic efficiency by minimizing losses throughout the production chain.
References
Wu, D., Cui, D., Zhou, M., Ying, Y., Information perception in modern poultry farming: A review. Computers and Electronics in Agriculture, 2022, 199, https://doi.org/10.1016/j.compag.2022.107131
Alders R.G., Dumas S.E., Rukambile E., Magoke G., Maulaga W., Jong J., Costa R. - Family poultry: Multiple roles, systems, challenges, and options for sustainable contributions to household nutrition security through a planetary health lens. Maternal & Child Nutrition, 2018, 14(3) https://doi.org/10.1111/mcn.12668
Bolohan, I., Lazar, R., Madescu, B.M., Bolohan (Cociorva), R.M., Davidescu, M.D., Boisteanu, P.C., Stability of Poultry Meat During Refrigerated Storage, based on the Packaging Used. Scientific Papers: Animal Science and Biotechnologies, 2024, 57(1).
Barbut, S., Meat Industry 4.0: A Distant Future? Animal Frontiers, 2020, 10(4), 38–47. https://doi.org/10.1093/af/vfaa038
Yitbarek, M.B., Livestock and livestock product trends by 2050: Review. International Journal of Animal Research, 2019, 4, 3.
FAO, 2022 - Food Outlook – Biannual Report on Global Food Markets 10.4060/cb9427en Rome, Italy.
AVEC, 2021 - AVEC Annual Report 2021. Brussels, Belgium.
Meat Consumption (Indicator). Available online: https://www.oecd.org/en/data/indicators/meat-consumption.html (accessed on 11 February 2025)
Gonçalves-Tenório, A., Silva, B.N., Rodrigues, V., Cadavez, V., Gonzales-Barron, U., Prevalence of pathogens in poultry meat: a meta-analysis of European published surveys. Foods, 2018, 7(5), 69. https://doi.org/10.3390/foods7050069
Khalid, T., Hdaifeh, A., Federighi, M., Cummins, E., Boué, G., Guillou, S., Tesson, V., Review of Quantitative Microbial Risk Assessment in Poultry Meat: The Central Position of Consumer Behavior. Foods, 2020, 9(11), 1661; https://doi.org/10.3390/foods9111661
Rouger, A., Tresse, O., Zagorec, M., Bacterial Contaminants of Poultry Meat: Sources, Species, and Dynamics. Microorganisms, 2017, 5(3), 50; https://doi.org/10.3390/microorganisms5030050
De Quadros, T.A.; Bohnemberger, J.; Friebel, J.; Ebling, P.D., Principais Causas de Condenação Total de Frangos em Abatedouros de Santa Catarina. 6º AGROTEC-Simpósio de Agronomia e Tecnologia; Unidade Central de Educação Faem Faculdade: Itapiranga, Brasil, 2019.
Myintzaw, P., Jaiswal, A.K., Jaiswala, S., A Review on Campylobacteriosis Associated with Poultry Meat Consumption. Food Reviews International, 2023, 39 (4). https://doi.org/10.1080/87559129.2021.1942487
Wessels, K., Rip, D., Gouws, P., Salmonella in Chicken Meat: Consumption, Outbreaks, Characteristics, Current Control Methods and the Potential of Bacteriophage Use. Foods, 2021, 10(8), 1742; https://doi.org/10.3390/foods10081742 .
Rahman, M.M., Husna, A., Elshabrawy, H.A., Alam, J., Runa, N.Y., Badruzzaman, A.T.M., Banu, N.A., Al Mamun, M., Paul, B., Das, S., Rahman, M.M., Mahbub-E-Elahi, A.T.M., Khairalla, A.S., Ashour, H.M., Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Scientific Reports, 2020, 10, 21999. https://doi.org/10.1038/s41598-020-78367-2
Praveen, K., Debnath, C., Shekhar, S., Dalai, N., Ganguly, S., Incidence of Aeromonas spp. infection in fish and chicken meat and its related public health hazards: A review. Veterinary World, 2016, 9(1), 6-11. doi: 10.14202/vetworld.2016.6-11.
Chai, S., Cole, D., Nisler, A., Mahon, B., Poultry: The most common food in outbreaks with known pathogens, United States, 1998–2012. Epidemiology & Infection, 2017, 145 (2), 316–325. https://doi.org/10.1017/S0950268816002375
Ananchaipattana, C., Hosotani, Y., Kawasaki, S., Pongsawat, S., Md. Latiful, B., Isobe, S., Prevalence of foodborne pathogens in retailed foods in Thailand. Foodborne pathogens and disease, 2012, 9(9), 835–40. https://doi.org/10.1089/fpd.2012.1169
Thakur, S., Brake, J., Keelara, S., Zou, M., Susick, E., Farm and environmental distribution of Campylobacter and Salmonella in broiler flocks. Research in Veterinary Science, 2013, 94(1), 33-42, https://doi.org/10.1016/j.rvsc.2012.07.014
Kim, J., Diao, J., Shepherd, M.W., Jr. Singh, R., Heringa, S.D., Gong, C., Jiang, X., Validating thermal inactivation of Salmonella spp. in fresh and aged chicken litter. Appl. Environ. Microbiol., 2012, 78, 1302-1307. https://doi.org/10.1128/AEM.06671-11
Bolan, N.S., Szogi, A.A., Chuasavathi, T., Seshadri, B., Rothrock, M.J., Jr. Panneerselvam, P., Uses and management of poultry litter. World's Poultry Science Journal, 2010, 66, 673–698. https://doi.org/10.1017/S0043933910000656
Shepherd, M.W., Liang, P., Jiang, X., Doyle, M.P., Erickson, M.C., Microbiological analysis of composts produced on South Carolina poultry farms. Journal of Applied Microbiology, 2010, 108, 2067–2076. https://doi.org/10.1111/j.1365-2672.2009.04610.x
Berry, E.D., Woodbury, B.L., Nienaber, J.A., Eigenberg, R.A., Thurston, J.A., Wells, J.E., Incidence and persistence of zoonotic bacterial and protozoan pathogens in a beef cattle feedlot runoff control-vegetative treatment system. J. Environ. Qual., 2007, 36, 1873-1882. https://doi.org/10.2134/jeq2007.0100
Zimmer, M., Barnhart, H., Idris, U., Lee, M.D., Detection of Campylobacter jejuni Strains in the Water Lines of a Commercial Broiler House and Their Relationship to the Strains That Colonized the Chickens. Avian Dis, 2003, 47 (1), 101–107. DOI: 10.1637/0005-2086(2003)047[0101:DOCJSI]2.0.CO;2
Ellis-Iversen, J., Ridley, A., Morris, V., Sowa, A., Harris, J., Atterbury, R., Sparks, N., Allen, V., Persistent environmental reservoirs on farms as risk factors for Campylobacter in commercial poultry. Epidemiol. Infect., 2012, 140, 916–924. doi:10.1017/S095026881100118X
Hazeleger, W.C., Bolder, N.M., Beumer, R.R., Jacobs-Reitsma, W.F., Darkling Beetles (Alphitobius diaperinus) and Their Larvae as Potential Vectors for the Transfer of Campylobacter jejuni and Salmonella enterica Serovar Paratyphi B Variant Java between Successive Broiler Flocks. Invertebrate Microbiology, 2008, 74 (22) https://doi.org/10.1128/AEM.00451-08
Velkers, F.C., Blokhuis, S.J., Veldhuis Kroeze, E.J.B., Burt, S.A., The role of rodents in avian influenza outbreaks in poultry farms: a review. Veterinary Quarterly, 2017, 37 (1), 182-194. https://doi.org/10.1080/01652176.2017.1325537
Sibanda, N., McKenna, A., Richmond, A., Ricke, S.C., Callaway, T., Stratakos, A.Ch., Gundogdu, O., Corcionivoschi, N., A Review of the Effect of Management Practices on Campylobacter Prevalence in Poultry Farms. Front. Microbiol., 2018, 9, https://doi.org/10.3389/fmicb.2018.02002
Wessels, K., Rip, D., Gouws, P., Salmonella in Chicken Meat: Consumption, Outbreaks, Characteristics, Current Control Methods and the Potential of Bacteriophage Use. Foods, 2021, 10(8), 1742; https://doi.org/10.3390/foods10081742
Dos Santos, V.M., Dallago, B.S.L., Racanicci, A.M.C., Santana, A.P., Bernal, F.E.M., Effects of season and distance during transport on broiler chicken meat. Poultry Science, 2017, 96(12), 4270-4279, https://doi.org/10.3382/ps/pex282
Machado dos Santos, V., Gabriel da Silva Oliveira, Salgado, C.B., Paula Gabriela da Silva Pires, Pedro Henrique Gomes de Sá Santos, Concepta McManus - Outcomes of Microbiological Challenges in Poultry Transport: A Mini Review of the Reasons for Effective Bacterial Control. Microbiol. Res., 2024, 15(2), 962-971; https://doi.org/10.3390/microbiolres15020063
Dianin K.C.S., Indicadores de Higiene e Pesquisa de Salmonella spp. em Linha de abate e Processamento de Frango de Corte. Master’s Thesis, Universidade Federal do Paraná, Palotina, Brasil, 2016.
Marin, C.; Lainez, M., Salmonella detection in feces during broiler rearing and after live transport to the slaughterhouse. Poultry Science, 2009, 88 (9), 1999–2005. https://doi.org/10.3382/ps.2009-00040
Huneau-Salaün, A., Scoizec, A., Thomas, R., Martenot, C., Schmitz, A., Pierre, I., Allée, C., Busson, R., Massin, P., Briand, F.X., Avian influenza outbreaks: Evaluating the efficacy of cleaning and disinfection of vehicles and transport crates. Poultry Science, 2022, 101(1), 101569 https://doi.org/10.1016/j.psj.2021.101569 .
Kraszczuk, V., Verificação do Processo de Higienização Pré-Operacional de um Abatedouro de Aves; Trabalho de Conclusão de Curso; Universidade Federal do Rio Grande do Sul: Porto Alegre, Brasil, 2010.
Shang, K., Wei, B., Jang, H.K., Kang, M., Phenotypic characteristics and genotypic correlation of antimicrobial resistant (AMR) Salmonella isolates from a poultry slaughterhouse and its downstream retail markets. Food Control, 2019, 100, 35–45. https://doi.org/10.1016/j.foodcont.2018.12.046
Perez‐Arnedo, I., Cantalejo, M.J., Martínez‐Laorden, A., Gonzalez‐Fandos, E., Effect of processing on the microbiological quality and safety of chicken carcasses at slaughterhouse. International Journal of Food Science & Technology, 2020, 56(4), 1855–1864, https://doi.org/10.1111/ijfs.14815 .
Seliwiorstow, T., Baré, J., Berkvens, D., Damme, I.V., Uyttendaele, M., De Zutter, L., Identification of risk factors for Campylobacter contamination levels on broiler carcasses during the slaughter process. International Journal of Food Microbiology, 2016, 226, 26-32, doi.org/10.1016/j.ijfoodmicro.2016.03.010
Council Regulation. Council Regulation (EC) No. 1099/2009 of 24 September 2009 on the Protection of Animals at the Time of Killing. Available online: http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=uriserv:sa0002 (accessed on 02.02.2025)
Schroeder, M.W., Eifert, J.D., Ponder, M.A., Schmale, D.G., Association of Campylobacter spp. levels between chicken grow-out environmental samples and processed carcasses. Poultry Science, 2014, 93(3), 734-741. https://doi.org/10.3382/ps.2013-03646
Osiriphun, S., Tuitemwong, P., Koetsinchai, W., Tuitemwong, K., Erickson, L.E., Model of inactivation of Campylobacter jejuni in poultry scalding. Journal of Food Engineering, 2012, 110 (1), 38-43. https://doi.org/10.1016/j.jfoodeng.2011.12.011
Rasschaert, G., Houf, K., De Zutter, L., Impact of the slaughter line contamination on the presence of Salmonella on broiler carcasses Get access Arrow. Journal of Applied Microbiology, 2007, 103(2), 333-341, https://doi.org/10.1111/j.1365-2672.2006.03248.x
Fries, R., Reducing Salmonella transfer during industrial poultry meat production. World's Poultry Science Journal, 2007, 58(4), 527-540: https://doi.org/10.1079/WPS20020038
Rasschaert, G., Lieven De Zutter, Herman, L., Heyndrickx, M., Campylobacter contamination of broilers: the role of transport and slaughterhouse. International Journal of Food Microbiology, 2020, 322, https://doi.org/10.1016/j.ijfoodmicro.2020.108564
Arsenault, J., Letellier, A., Quessy, S., Boulianne, M., Prevalence and Risk Factors for Salmonella and Campylobacter spp. Carcass Contamination in Broiler Chickens Slaughtered in Quebec, Canada. Journal of Food Protection, 2007, 70(8), 1820-1828. https://doi.org/10.4315/0362-028X-70.8.1820
Peyrat, M.B., Soumet, C., Maris, P., Sanders, P., Recovery of Campylobacter jejuni from surfaces of poultry slaughterhouses after cleaning and disinfection procedures: Analysis of a potential source of carcass contamination. International Journal of Food Microbiology, 2008, 124(2), 188-194, https://doi.org/10.1016/j.ijfoodmicro.2008.03.030 .
Kudirkienė, E., Bunevičienė, J., Brøndsted, L., Ingmer, H., Olsen, J.E., Malakauskas, M., Evidence of broiler meat contamination with post-disinfection strains of Campylobacter jejuni from slaughterhouse. International Journal of Food Microbiology, 2011, 45 (1), https://doi.org/10.1016/j.ijfoodmicro.2010.06.024 .
Lusk, J.L., McCluskey, J., Understanding the Impacts of Food Consumer Choice and Food Policy Outcomes. Applied Economic Perspectives and Policy 2018, 40 (1), https://doi.org/10.1093/aepp/ppx054
Collineau, L., Chapman, B., Bao, X., Sivapathasundaram, B., Carson, CA, Fazil, A., Reid-Smith, RJ, Smith, B.A., A farm-to-fork quantitative risk assessment model for Salmonella Heidelberg resistant to third-generation cephalosporins in broiler chickens in Canada. International Journal of Food Microbiology, 2020, 330, 108559, https://doi.org/10.1016/j.ijfoodmicro.2020.108559
Signorini, M.L., Zbrun, M.V., Romero-Scharpen, A., Olivero, C., Bongiovanni, F., Soto, L.P., Frizzo, L.S., Rosmini, M.R., Quantitative risk assessment of human campylobacteriosis by consumption of salad cross-contaminated with thermophilic Campylobacter spp. from broiler meat in Argentina. Preventive Veterinary Medicine, 2013, 109 (1–2), 37-46, https://doi.org/10.1016/j.prevetmed.2012.09.011
Zhu, J., Bai, Y., Wang, Y., Song, X., Cui, S., Xu, H., Jiao, X., Li, F., A risk assessment of salmonellosis linked to chicken meals prepared in households of China.. Food Control, 2017, 79, 279-287. https://doi.org/10.1016/j.foodcont.2017.04.003
Brynestad, S., Braute, L., Luber, P., Bartelt, E., Quantitative microbiological risk assessment of campylobacteriosis cases in the German population due to consumption of chicken prepared in homes. International Journal of Risk Assessment and Management, 2008, 8 (3), 194-213, https://doi.org/10.1504/IJRAM.2008.018208
