[en] Background and Aim: Eggs represent a vital dietary source globally; however, bacterial contamination poses a substantial public health risk. This systematic review and meta-analysis aimed to evaluate the global prevalence of bacterial contamination in table eggs and to characterize the antibiotic resistance profiles of these pathogens, emphasizing their implications for public health. Materials and Methods: A comprehensive bibliographic search of Web of Science, MEDLINE (PubMed), CAB Abstract, and Google Scholar databases was performed, identifying 136 studies published between 1979 and 2022. The systematic review utilized Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines and advanced bibliometric techniques for data collection. Microsoft Excel and R software (v5.0) were employed for data consolidation and statistical analysis. Heterogeneity among studies was assessed using Higgins' I² index, and a random-effects model was adopted for prevalence estimation and subgroup analyses. Results: Seventeen bacterial species were identified in eggs, primarily Salmonella spp., Escherichia coli, Staphylococcus aureus, Campylobacter spp., and Listeria monocytogenes. Overall, eggshell contamination rates exceeded those of egg contents. Salmonella spp. isolates exhibited complete resistance (100%) to nitrofurantoin, novobiocin, and polymyxin and substantial resistance (>50%) to commonly used antibiotics such as amoxicillin (74.5%), penicillin G (89.1%), and colistin (83.1%). E. coli isolates showed total resistance to penicillin G (100%) and high resistance to amoxicillin (72.2%) and ceftazidime (95.6%). Antibiotic resistance varied significantly across regions, notably higher in Asian and African isolates. Multidrug-resistant strains of E. coli and Campylobacter spp. were also identified. Conclusion: This study underscores the high global prevalence of pathogenic bacteria in poultry eggs and highlights concerning antibiotic resistance trends, particularly among Salmonella spp. and E. coli. The findings emphasize the urgent need for region-specific biosecurity protocols and antimicrobial stewardship strategies to reduce egg contamination and control antibiotic-resistant pathogens, ultimately safeguarding public health and food safety.
Research Center/Unit :
FARAH. Santé publique vétérinaire - ULiège
Disciplines :
Food science
Author, co-author :
Hinson, Cyrielle Elsy Akpédjè ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) ; Disease Research, Health
Tonouhewa, Are; Disease Research, Health
Azokpota, Paulin; Disease Research, Health
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires ; Disease Research, Health
Korsak Koulagenko, Nicolas ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) ; Disease Research, Health
Sessou, Philippe; Disease Research, Health ; Disease Research, Health
Language :
English
Title :
Global prevalence and antibiotic resistance profiles of bacterial pathogens in table eggs: A systematic review and meta-analysis
FAO. OMS Fardeau Que Représentent Les Maladies d’origines Alimentaire et Effets Positifs de l’investissement Dans La Sécurité Sanitaire Des Aliments. Available from: https://www.fao.org/3/CA2809FR/ca2809fr.pdf Retrieved on 1-04-2023.
Hanafi, M.E., Brahim, B., Sami, D., Said, D., Nadia, Z., Nourredine, B., Saadia, N. and Hakim, K. (2023) Prevalence of Salmonella spp. in food products of animal origin marketed in Rabat, Morocco [Prévalence de Salmonella Spp. dans les produits alimentaires d’origine animale commercialisés à Rabat, Maroc]. Int. J. Innov. Appl. Stud., 39: 711–718.
Lesnierowski, G. and Stangierski, J. (2018) What’s new in chicken egg research and technology for human health promotion? - A review. Trends Food Sci. Technol., 71: 46–51.
Nys, Y., Bain, M. and Immerseel, F.V. (2011) Egg chemistry, production and consumption. In: Improving the Safety and Quality of Eggs and Egg Products: Vol. 1. Elsevier, Netherlands.
Omhover-Fougy, L. and Hezard, B. (2023) Outbreaks and food microbiology [Toxi-infections alimentaires collectives et microbiologie de l’alimentation]. Rev. Francoph. Lab., 2023(550): 66–73.
Upadhyaya, I., Yin, H.B., Nair, M.S. and Venkitanarayanan, K. (2017) Natural approaches for improving postharvest safety of egg and egg products. In: Ricke, S.C., Gast, R.K., editors. Producing Safe Eggs. Ch. 19. Academic Press, San Diego, p391–420.
Naïtali, M., Guillier, L. and Dubois-Brissonnet, F. (2017) Risques Microbiologiques Alimentaires. Lavoisier, France, Paris.
El Ftouhy, F.Z., Nassik, S., Nacer, S., Kadiri, A., Charrat, N., Attrassi, K., Fagrach, A., Bahir, M.A., Derqaoui, S. and Hmyene, A. (2022) Bacteriological quality of table eggs in Moroccan formal and informal sector. Int. J. Food Sci., 2022: 6223404.
Yenil̇mez, F. and Bulancak, A. (2020) Microbiological quality of table eggs sold at different sales location. Çukurova J. Agric. Food Sci., 35: 115–124.
WHO Stop Overuse and Misuse of Antibiotics: Combat Resistance. Available from: https://www.who.int/westernpacific/news/item/10-11-2017-stop-overuse-and-misuse-of-antibiotics-combat-resistance Retrieved on 11-06-2024.
Atoyebi, O.E., Adetunji, V.O., Babalobi, O.O. and Atoyebi, T.J. (2019) Prevalence and antibiotics sensitivity of Escherichia coli O157:H7 in table eggs from poultry farms in Ibadan, Oyo State, Nigeria. Afr. J. Biomed. Res., 22: 275–279.
Sanders, P., Perrin-Guyomard, A. and Moulin, G. (2017) Evolution of antimicrobial usage in food-producing animals [Évolution de l’utilisation Des antibiotiques en production animale]. Cah. Nutr. Diet., 52: 301–311.
Çufaoğlu, G., Ambarcioğlu, P., Deriṅöz, A.N. and Ayaz, N.D. (2023) Prevalence, serotype diversity and antibiotic resistance of Salmonella among poultry meat and eggs in Turkiye: A meta-analysis. J. Agric. Sci, 29: 519–533.
WHO Antimicrobial Resistance. Available from: https://www.who.int/health-topics/antimicrobialresistance Retrieved on 1-04-2023.
Wu, R.A., Feng, J., Yue, M., Liu, D. and Ding, T. (2024) Overuse of food-grade disinfectants threatens a global spread of antimicrobial-resistant bacteria. Crit. Rev. Food Sci. Nutr., 64(19): 6870–6879.
Salam, M.A., Al-Amin, M.Y., Salam, M.T., Pawar, J.S., Akhter, N., Rabaan, A.A. and Alqumber, M.A.A. (2023) Antimicrobial resistance: A growing serious threat for global public health. Healthcare, 11: 19–46.
Kim, M., Weigand, M.R., Oh, S., Hatt, J.K., Krishnan, R., Tezel, U., Pavlostathis, S.G. and Konstantinidis, K.T. (2018) Widely used benzalkonium chloride disinfectants can promote antibiotic resistance. Appl. Environ. Microbiol., 84(17): e01201–e01218.
Short, F.L., Lee, V., Mamun, R., Malmberg, R., Li, L., Espinosa, M.I., Venkatesan, K. and Paulsen, I.T. (2021) Benzalkonium chloride antagonises aminoglycoside antibiotics and promotes evolution of resistance. EBioMedicine, 73: 103653.
Nordholt, N., Kanaris, O., Schmidt, S.B.I. and Schreiber, F. (2021) Persistence against benzalkonium chloride promotes rapid evolution of tolerance during periodic disinfection. Nat. Commun., 12: 6792.
Sultan, I., Rahman, S., Jan, A.T., Siddiqui, M.T., Mondal, A.H. and Haq, Q.M.R. (2018) Antibiotics, resistome and resistance mechanisms: A bacterial perspective. Front. Microbiol, 9: 2066.
Adeboye, O.A., Kwofie, M.K. and Bukari, N. (2020) Campylobacter, Salmonella and Escherichia coli food contamination risk in free-range poultry production system. Adv. Microbiol., 10(10): 525–542.
Hosseininezhad, B., Berizi, E., Nader, M., Mazloomi, S.M., Hosseinzadeh, S., Ebrahimi, L. and Zare, M. (2020) Prevalence of Salmonella contamination in consumed eggs in Iran: A systematic review and meta-analysis study on published studies from 1996 to 2018. Vet. World, 13(12): 2743–2751.
Authority (EFSA). and European Centre for Disease Prevention and Control (ECDC). (2023) The European union one health 2022 zoonoses report. EFSA J., 21: e8442.
Howard, Z.R., O’Bryan, C.A., Crandall, P.G. and Ricke, S.C. (2012) Salmonella Enteritidis in eggshells: Current issues and prospects for control. Food Res. Int., 45: 755–764.
EFSA Salmonella Dashboard. Available from: https://www.efsa.europa.eu/en/microstrategy/salmonelladashboard Retrieved on 16-01-2024.
USDA. (2013) The Nationwide Microbiological Baseline Data Collection Program: Raw Liquid Eggs Survey. USDA, United States.
Parvin, M.S., Talukder, S., Ali, M.Y., Chowdhury, E.H., Rahman, M.T. and Islam, M.T. (2020) Antimicrobial resistance pattern of Escherichia coli isolated from frozen chicken meat in Bangladesh. Pathogens, 9(6): 420.
Hossain, M.S., Rahman, W., Ali, M.S., Sultana, T. and Hossain, K.M.M. (2021) Identification and antibiogram assay of Escherichia coli isolated from chicken eggs. J. Biosci., 29(1): 123–133.
Sharan, M., Dhaka, P., Bedi, J.S., Singh, R. and Mehta, N. (2023) Characterization of chicken eggs associated Escherichia coli and Staphylococcus aureus for biofilm production and antimicrobial resistance traits. Anim. Biotechnol., 34(8): 3533–3544.
WHO. E. coli Available from: https://www.who.int/news-room/fact-sheets/detail/e-coli Retrieved on 11-06-2024.
Zbrun, M.V., Rossler, E., Romero-Scharpen, A., Soto, L.P., Berisvil, A., Zimmermann, J.A., Fusari, M.L., Signorini, M.L. and Frizzo, L.S. (2020) Worldwide meta-analysis of the prevalence of Campylobacter in animal food products. Res. Vet. Sci., 132: 69–77.
Ansarifar, E., Riahi, S.M., Tasara, T., Sadighara, P. and Zeinali, T. (2023) Campylobacter prevalence from food, animals, human and environmental samples in Iran: A systematic review and meta-analysis. BMC Microbiol., 23: 126.
Liang, T., Liang, Z., Wu, S., Ding, Y., Wu, Q. and Gu, B. (2023) Global prevalence of Staphylococcus aureus in food products and its relationship with the occurrence and development of diabetes mellitus. Med. Adv., 1(1): 53–78.
Pondit,A.,Haque,Z.F.,Sabuj,A.A.M.,Khan,M.S.R.and Saha, S. (2018) Characterization of Staphylococcus aureus isolated from chicken and quail eggshell. J. Adv. Vet. Anim. Res., 5(4): 466–471.
Al-Jaff, B.M.A. (2004) The Risk of bacterial contamination in hen eggs of Sulaimani poultries. J. Zankoy Sulaimani A, 8(1): 63–71.
Korashy, E., Wahba, N. and Hassanein, R. (2008) Public health hazards of some bacterial pathogens associated with consumption of eggs and studying the best cooking methods for their destruction. Assiut. Vet. Med. J., 54(117): 1–19.
Chaemsanit, S., Akbar, A. and Anal, A.K. (2015) Isolation of total aerobic and pathogenic bacteria from table eggs and its contents. Food Appl. Biosci. J., 3(1): 1–9.
Favier, G.I., Escudero, M.E. and De Guzmán, A.M.S. (2005) Genotypic and phenotypic characteristics of Yersinia enterocolitica isolated from the surface of chicken eggshells obtained in Argentina. J. Food Prot., 68: 1812–1815.
Adesiyun, A.A., Nkuna, C., Mokgoatlheng-Mamogobo, M., Malepe, K. and Simanda, L. (2020) Food safety risk posed to consumers of table eggs from layer farms in Gauteng province, South Africa: Prevalence of Salmonella species and Escherichia coli, antimicrobial residues, and antimicrobial resistant bacteria. J. Food Saf., 40: 1–12.
Kariuki, J.W., Jacobs, J., Ngogang, M.P. and Howland, O. (2023) Antibiotic use by poultry farmers in Kiambu County, Kenya: Exploring practices and drivers of potential overuse. Antimicrob. Resist. Infect. Control, 12(1): 3.
Boamah, V.E., Agyare, C., Odoi, H. and Dalsgaard, A. (2016) Practices and factors influencing the use of antibiotics in selected poultry farms in Ghana. J. Antimicrob. Agents, 2: 120.
Malijan, G.M., Howteerakul, N., Ali, N., Siri, S., Kengganpanich, M., Nascimento, R., Booton, R.D., Turner, K.M.E., Cooper, B.S. and Meeyai, A.A (2022) Scoping review of antibiotic use practices and drivers of inappropriate antibiotic use in animal farms in WHO Southeast Asia Region. One Health, 15: 100412.
Owusu-Doubreh, B., Appaw, W.O. and Abe-Inge, V. (2023) Antibiotic residues in poultry eggs and its implications on public health: A review. Sci. Afr., 19: e01456.
Arsène, M.M.J., Davares, A.K.L., Viktorovna, P.I., Andreevna, S.L., Sarra, S., Khelifi, I. and Sergueïevna, D.M. (2022) The public health issue of antibiotic residues in food and feed: Causes, consequences, and potential solutions. Vet. World, 15: 662–671.
Mund, M.D., Khan, U.H., Tahir, U., Mustafa, B.E. and Fayyaz, A. (2017) Antimicrobial drug residues in poultry products and implications on public health: A review. Int. J. Food Prop., 20: 1433–1446.
Harsha, H. (2011) Prevalence and antibiotic resistance of Salmonella from the eggs of commercial samples. J. Microbiol. Infect. Dis, 1(3): 93–100.
Suresh, T., Hatha, A.A.M., Sreenivasan, D., Sangeetha, N. and Lashmanaperumalsamy, P. (2006) Prevalence and antimicrobial resistance of Salmonella Enteritidis and other Salmonella in the eggs and egg-storing trays from retails markets of Coimbatore, South India. Food Microbiol., 23(3): 294–299.
Ifeanyichukwu, I., Chika, E., Ogonna, A., Chidinma, I., Monique, A., Ikechukwu, M., Stanley, E., Emmanuel, N., Ngozi, A. and Agabus, N. (2016) Prevalence and antibiogram of Salmonella spp. isolated from poultry products in Ebonyi State, Nigeria. J. Adv. Vet. Anim. Res., 3(4): 353–359.
Okorie-Kanu, O.J., Ezenduka, E.V., Okorie-Kanu, C.O., Ugwu, L.C. and Nnamani, U.J. (2016) Occurrence and antimicrobial resistance of pathogenic Escherichia coli and Salmonella spp. in retail raw table eggs sold for human consumption in Enugu State, Nigeria. Vet. World, 9(11): 1312–1319.
Akhtar, F., Hussain, I., Khan, A. and Rahman, S.U. (2010) Prevalence and antibiogram studies of Salmonella Enteritidis isolated from human and poultry sources. Pak. Vet. J. 30(1): 25–28.
Singh, S., Yadav, A.S., Singh, S.M. and Bharti, P. (2010) Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res. Int., 43(8), 2027–2030.
Abubakar, U. and Salman, M. (2023) Antibiotic use among hospitalized patients in Africa: A systematic review of point prevalence studies. J. Rac. Ethn. Health Dispar., 11(3): 1308–1329.
Yushina, Y., Zaiko, E., Makhova, A., Bataeva, D. and Nasyrov, N. (2023) Antibiotic resistance in the pathogenic bacteria isolated from environmental samples of the food production facilities. BIO Web Conf., 67: e01014.
Cantón, R., Novais, A., Valverde, A., Machado, E., Peixe, L., Baquero, F. and Coque, T.M. (2008) Prevalence and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae in Europe. Clin. Microbiol. Infect., 14: 144–153.
Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C.M. and Zhang, Q. (2009) Antibiotic resistance in Campylobacter: Emergence, transmission and persistence. Future Microbiol., 4: 189–200.
Panyako, P.M., Lichoti, J.K. and Ommeh, S.C. (2022) Antimicrobial drug resistance in poultry pathogens: Challenges and opportunities. J. Agric. Sci. Technol., 21: 62–82.
Islam, M.S., Hossain, M.J., Sobur, M.A., Punom, S.A., Rahman, A.M.M.T. and Rahman, M.T. (2023) A systematic review on the occurrence of antimicrobial-resistant Escherichia coli in poultry and poultry environments in Bangladesh between 2010 and 2021. Biomed. Res. Int., 2023(1): 2425564.
Lima, É., Oliveira, M.B. and Freitas, A. (2023) Antibiotics in intensive egg production: Food safety tools to ensure regulatory compliance. Food Chem. Adv., 3: 100548.