Prevalence of Extended-Spectrum Beta-Lactamase-Producing Escherichia Coli in Broiler Farms: A Systematic Review and Meta-Analysis https://doi.org/10.12982/VIS.2025.033
Article Sidebar
Main Article Content
Abstract
Extended-spectrum beta-lactamases-producing Escherichia coli (ESBL E. coli) is a serious public health issue. ESBL E. coli in broiler production is known as potential risk for humans. This study aims to estimate the global pooled prevalence of ESBL E. coli in broiler farms. Literature searches were done via PubMed, Web of Science and Scopus. A random effect model was used to estimate the pooled prevalence. Heterogeneity was assessed by Cochrans’s Q test and I squared statistic (I2). Subgroup analysis and meta-regression was conducted to investigate the source of heterogeneity. Sensitivity and publication bias analyses were performed. Overall, 872 and 18 additional studies were retrieved from databases and bibliography searches. Thirty-seven studies met the inclusion criteria. Pooled prevalence of ESBL E. coli in broiler farms was 26.6% (95% CI = 18.2 to 37.3) and revealed high heterogeneity (Q = 1958.87 and I2 = 98.2%). The pooled prevalence of ESBL E. coli in broiler farms was almost identical between Asia; 33.0% (95% CI = 18.7 to 51.3) and Europe; 32.8% (95% CI = 15.0 to 57.4), while Africa showed the lowest at 12.4% (95% CI = 5.1 to 27.1). Prevalence of ESBL E. coli was found highest in fecal sources; 33.0% (95% CI = 21.5 to 46.8) followed by environmental sources; 28.3% (95% CI = 13.5 to 50.1) and other sources; 11.0% (95% CI = 5.0 to 22.8). Results from our study indicated moderate prevalence of ESBL E. coli in broiler farms globally and it has been fluctuating inconsistently in the last decade.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Abreu, R., Castro, B., Espigares, E., Rodriguez-Alvarez, C., Lecuona, M., Moreno, E., Espigares, M., Arias, A., 2014. Prevalence of CTX-M-type extended-spectrum beta-lactamases in Escherichia coli strains isolated in poultry farms. Foodborne. Pathog. Dis. 11(11), 868-873.
Apostolakos, I., Mughini-Gras, L., Fasolato, L., Piccirillo, A., 2019. Assessing the occurrence and transfer dynamics of ESBL/pAmpC-producing Escherichia coli across the broiler production pyramid. PLoS One. 14(5), e0217174.
Aworh, M.K., Kwaga, J., Okolocha, E., Harden, L., Hull, D., Hendriksen, R.S., Thakur, S., 2020. Extended-spectrum beta-lactamase-producing Escherichia coli among humans, chickens, and poultry environments in Abuja, Nigeria. One Health Outlook. 2, 11.
Baez, M., Espinosa, I., Collaud, A., Miranda, I., Montano, D.L.N., Feria, A.L., Hernandez-Fillor, R., 2021. Genetic features of extended-spectrum β-lactamase-producing Escherichia coli from poultry in Mayabeque Province, Cuba. Antibiotics. 10, 1-14.
Bhave, S., Kolhe, R., Mahadevaswamy, R., Bhong, C., Jadhav, S., Nalband, S., Gandhale, D., Muglikar, D., 2019. Phylogrouping and antimicrobial resistance analysis of extraintestinal pathogenic Escherichia coli isolated from poultry species. Turk. J. Vet. Anim. Sci. 43, 117-126.
Blaak, H., Van Hoek, A.H.A.M., Hamidjaja, R.A., Van Der Plaats, R.Q.J., Kerkhof-De Heer, L., De Roda Husman, A.M., Schets, F., 2015. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS One. 10(8), e0135402.
Boonyasiri, A., Tangkoskul, T., Seenama, C., Saiyarin, J., Tiengrim, S., Thamlikitkul, V., 2014. Prevalence of antibiotic-resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathog. Glob. Health. 108(5), 235-245.
Brower, C.H., Mandal, S., Hayer, S., Sran, M., Zehra, A., Patel, S.J., Kaur, R., Chatterjee, L., Mishra, S., Das, B.R., Singh, P., Singh, R., Gill, J.P.S., Laxminarayan, R., 2017. The Prevalence of Extended-Spectrum Beta-Lactamase-Producing multidrug-resistant Escherichia Coli in poultry chickens and variation according to farming practices in Punjab, India. Environ. Health. Perspect. 125(7), 077015.
Bui, T.K.N., Bui, T.M.H., Ueda, S., Le, D.T., Yamamoto, Y., Hirai, I., 2018. Potential transmission opportunity of CTX-M-producing Escherichia coli on a large-scale chicken farm in Vietnam. J. Glob. Antimicrob. Resist. 13, 1-6.
Bush, K., Bradford, P.A., 2016. β-Lactams and β-Lactamase Inhibitors: an overview. Cold. Spring. Harb. Perspect. Med. 6(8), a025247.
Cardozo, M.V., Liakopoulos, A., Brouwer, M., Kant, A., Pizauro, L.J.L., Borzi, M.M., Mevius, D., de Ávila, F.A., 2021. Occurrence and molecular characteristics of extended-spectrum beta-lactamase-producing Enterobacterales recovered from chicken, chicken meat, and human infections in Sao Paulo State, Brazil. Front. Microbiol. 12, 628738.
Carissa, D., Edward, N., Michael, A., Chika, E., Charles, E., 2013. Extended-spectrum beta-lactamase-producing Escherichia coli strains of poultry origin in Owerri, Nigeria. World. J. Med. Sci. 8(4), 349-354.
Castellanos, L.R., Donado-Godoy, P., León, M., Clavijo, V., Arevalo, A., Bernal, J.F., Timmerman, A.J., Mevius, D.J., Wagenaar, J.A., Hordijk, J., 2017. High heterogeneity of Escherichia coli sequence types harbouring ESBL/AmpC genes on IncI1 plasmids in the Colombian poultry chain. PLoS One. 12(1), e0170777.
Chong, Y., Ito, Y., Kamimura, T., 2011. Genetic evolution and clinical impact in extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect. Genet. Evol. 11(7), 1499-1504.
Chong, Y., Shimoda, S., Shimono, N., 2018. Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect. Genet. Evol. 61, 185-188.
Coyne, L., Arief, R., Benigno, C., Giang, V.N., Huong, L.Q., Jeamsripong, S., Kalpravidh, W., McGrane, J., Padungtod, P., Patrick, I., Schoonman, L., Setyawan, E., Harja Sukarno, A., Srisamran, J., Ngoc, P.T., Rushton, J., 2019. Characterizing antimicrobial use in the livestock sector in three South East Asian countries (Indonesia, Thailand, and Vietnam). Antibiotics (Basel). 8(1), 33.
De Koster, S., Ringenier, M., Lammens, C., Stegeman, A., Tobias, T., Velkers, F., Vernooij, H., Kluytmans-van den Bergh, M., Kluytmans, J., Dewulf. J., Goossens H., 2021. ESBL-producing, carbapenem- and ciprofloxacin-resistant Escherichia coli in Belgian and Dutch broiler and pig farms: a cross-sectional and cross-border study. Antibiotics. 10(8), 945.
De Kraker, M.E.A., Stewardson, A.J., Harbarth, S., 2016. Will 10 million people die a year due to antimicrobial resistance by 2050?. PLoS Med. 13(11), e1002184.
Dierikx, C.M., Van Der Goot, J.A., Smith, H.E., Kant, A., Mevius, D.J., 2013. Presence of ESBL/AmpC-producing Escherichia coli in the broiler production pyramid: a descriptive study. PLoS One. 8(11). e79005.
Ding, H., Gao, Y. M., Deng, Y., Lamberton, P.H., Lu, D.B., 2017. A systematic review and meta-analysis of the seroprevalence of Toxoplasma gondii in cats in mainland China. Parasit Vectors. 10(1), 27.
Doregiraee, F., Alebouyeh, M., Nayeri Fasaei, B., Charkhkar, S., Tajeddin, E., Zali, M.R., 2018. Changes in antimicrobial resistance patterns and dominance of extended spectrum β-lactamase genes among faecal Escherichia coli isolates from broilers and workers during two rearing periods. Ital. J. Anim. Sci. 17(3), 815-824.
Drugdova, Z., Kmet, V., 2013. Prevalence of beta-lactam and fluoroquinolone resistance, and virulence factors in Escherichia coli isolated from chickens in Slovakia. Biologia. 68(1), 11-17.
EFSA Panel on Biological Hazards (BIOHAZ), 2011. Scientific opinion on the public health risks of bacterial strains producing extended-spectrum β-lactamases and/or AmpC β-lactamases in food and food-producing animals. EFSA J. 9(8), 2322.
Egger, M., Smith, G.D., Schneider, M., Minder, C., 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ. 315(7109), 629-634.
Falgenhauer, L., Imirzalioglu, C., Oppong, K., Akenten, C.W., Hogan, B., Krumkamp, R., Poppert, S., Levermann, V., Schwengers, O., Sarpong, N., Owusu-Dabo, E., May, J., Eibach, D., 2019. Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Front. Microbiol. 10, 3358.
Food and Agriculture Organization of the United Nations, 2019. Monitoring and surveillance of antimicrobial resistance in bacteria from healthy food animals intended for consumption. In: Regional antimicrobial resistance monitoring and surveillance guidelines: Volume 1. Available online: https://openknowledge.fao.org/server/api/core/bitstreams/f31e70b6-b9e0-41b6-916a-1cb0c3654c4d/content.
Ferreira, J.C., Penha Filho, R.A.C., Andrade, L.N., Berchieri, A., Darini, A.L.C., 2014. Detection of chromosomal blaCTX-M-2 in diverse Escherichia coli isolates from healthy broiler chickens. Clin. Microbiol. Infect. 20(10), 623-626.
Gazal, L.E.D.S., Medeiros, L.P., Dibo, M., Nishio, E.K., Koga, V.L., Gonçalves, B.C., Grassotti, T.T., de Camargo, T.C.L., Pinheiro, J.J., Vespero, E.C., de Brito, K.C.T., de Brito, B.G., Nakazato, G., Kobayashi, R.K.T., 2021. Detection of ESBL/AmpC-producing and fosfomycin-resistant Escherichia coli from different sources in poultry production in Southern Brazil. Front. Microbiol. 11(11), 604544.
Gundran, R.S., Cardenio, P.A., Villanueva, M.A., Sison, F.B., Benigno, C.C., Kreausukon, K., Pichpol, D., Punyapornwithaya, V., 2019. Prevalence and distribution of blaCTX-M, blaSHV, and blaTEM genes in extended-spectrum β-lactamase-producing E. coli isolates from broiler farms in the Philippines. BMC Vet. Res. 15(1), 227.
Hassen, B., Abbassi, M.S., Ruiz-Ripa, L., Mama, O.M., Hassen, A., Torres, C., Hammami, S., 2020. High prevalence of mcr-1 encoding colistin resistance and first identification of blaCTX-M-55 in ESBL/CMY-2-producing Escherichia coli isolated from chicken faeces and retail meat in Tunisia. Int. J. Food. Microbiol. 318, 108478.
Higgins, J.P.T., Thompson, S.G., Deeks, J.J., ltman, D.G., 2003. Measuring inconsistency in meta-analyses. BMJ. 327(7414), 557-560.
Hinenoya, A., Tran, S.T.T., Nguyen, N.T., Nguyen, H.C., Nguyen, D.D.L., Hoang, P.H., Awasthi, S.P., Hassan, J., Sumimura, Y., Yamamoto, Y., Yamasaki, S., 2018. Isolation and molecular characterization of extended-spectrum beta-lactamase producing Escherichia coli from industrial food animals in Mekong Delta, Vietnam. JPN J. Vet. Res. 66(1), 1-12.
Ilyas, S., Rasool, M.H., Arshed, M.J., Qamar, M.U., Aslam, B., Almatroudi, A., Khurshid, M., 2021. The Escherichia coli sequence type 131 harboring extended-spectrum beta-lactamases and carbapenemases genes from poultry birds. Infect. Drug. Resist. 14, 805-813.
Jouini, A., Klibi, A., Elarbi, I., Chaabene, M.B., Hamrouni, S., Souiai, O., Hanachi, M., Ghram, A., Maaroufi, A., 2021. First detection of human ST131-CTX-M-15-O25-B2 clone and high-risk clonal lineages of ESBL/pAmpC-producing E. coli isolates from diarrheic poultry in Tunisia. Antibiotics, 10(6), 670.
Karanika, S., Karantanos, T., Arvanitis, M., Grigoras, C., Mylonakis, E., 2016. Fecal Colonization with Extended-spectrum Beta-lactamase–Producing enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis. Clin. Infect. Dis. 63(3), 310-318.
Kwoji, I.D., Musa, J.A., Daniel, N., Mohzo, D.L., Bitrus, A.A., Ojo, A.A., Ezema, K.U., 2019. Extended-spectrum beta-lactamase-producing Escherichia coli in chickens from small-scale (backyard) poultry farms in Maiduguri, Nigeria. Int. J. One. Health. 5, 26-30.
Laube, H., Friese, A., von Salviati, C., Guerra, B., Käsbohrer, A., Kreienbrock, L., Roesler, U., 2013. Longitudinal monitoring of extended-spectrum-beta-lactamase/AmpC-producing Escherichia coli at German broiler chicken fattening farms. Appl. Environ. Microbiol. 79(16), 4815-4820.
Li, S., Zhao, M.M., Liu, J.H., Zhou, Y.F., Miao, Z.M., 2016. Prevalence and antibiotic resistance profiles of extended-spectrum beta-lactamase-producing Escherichia coli isolated from healthy broilers in Shandong Province, China. J. Food. Prot. 79(7), 1169-1173.
Liebana, E., Carattoli, A., Coque, T.M., Hasman, H., Magiorakos, A.P., Mevius, D., Peixe, L., Poirel, L., Schuepbach-Regula, G., Torneke, K., Torren-Edo, J., Torres, C., Threlfall, J., 2013. Public health risks of enterobacterial isolates producing extended-spectrum β-lactamases or AmpC β-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin. Infect. Dis. 56(7), 1030-1037.
Mikhayel, M., Leclercq, S.O., Sarkis, D.K., Doublet, B., 2021. Occurrence of the colistin resistance gene mcr-1 and additional antibiotic resistance genes in ESBL/AmpC producing Escherichia coli from poultry in Lebanon: a nationwide survey. Microbiol. Spectr. 9(2), e0002521.
Moawad, A.A., Hotzel, H., Neubauer, H., Ehricht, R., Monecke, S., Tomaso, H., Hafez, H. M., Roesler, U., El-Adawy, H., 2018. Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: Emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli. Gut. Pathog. 10(1), 39.
Niero, G., Bortolaia, V., Vanni, M., Intorre, L., Guardabassi, L., Piccirillo, A., 2018. High diversity of genes and plasmids encoding resistance to third-generation cephalosporins and quinolones in clinical Escherichia coli from commercial poultry flocks in Italy. Vet. Microbiol. 216, 93-98.
World Organization for Animal Health, 2020. OIE Standards, Guidelines and Resolution on Antimicrobial Resistance and the use of antimicrobial agents. Available online: https://www.oie.int/en/document/book-amr-ang-fnl-lr/
Page, M.J., McKenzie, J.E., Bossuyt, P.M., Boutron, I., Hoffmann, T.C., Mulrow, C.D., Shamseer, L., Tetzlaff, J.M., Akl, E.A., Brennan, S.E., Chou, R., Glanville, J., Grimshaw, J.M., Hróbjartsson, A., Lalu, M.M., Li, T., Loder, E.W., Mayo-Wilson, E., McDonald, S., McGuinness, L.A., Stewart, L.A., Thomas, J., Tricco, A.C., Welch, V. A., Whiting, P., Moher, D., 2021. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021, 372.
Page, S.W., Gautier, P., 2012. Use of antimicrobial agents in livestock. Rev. Sci. Tech. 31(1), 145-188.
Paivarinta, M., Pohjola, L., Fredriksson-Ahomaa, M., Heikinheimo, A., 2016. Low occurrence of extended-spectrum beta-lactamase-producing Escherichia coli in Finnish food-producing animals. Zoonoses. Public. Health. 63(8), 624-631.
Rodroo, J., Intanon, M., Kreausukon, K., Kongkaew, A., Bender, J., Awaiwanont, N., 2021. Occurrence of extended-spectrum beta-lactamase producing E. coli in broiler farm workers and the farm environment in Chiang Mai-Lamphun, Thailand. Vet. Integr. Sci. 19(1), 23-35.
Rojs, O.Z., Zdovc, I., Dovč, A., Žgajnar, J., Slavec, B., Krapež, U., Ambrožič, J.A., 2019. Presence and distribution of extended-spectrum and AmpC beta-lactamases-producing Escherichia coli on poultry farms in Slovenia. J. Appl. Poult. Res. 28(1), 200-209.
Roth, N., Käsbohrer, A., Mayrhofer, S., Zitz, U., Hofacre, C., Domig, K.J., 2019. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: a global overview. Poult. Sci. 98(4), 1791-1804.
Rousham, E.K., Asaduzzaman, M., Amin Uddin Mozmader, T.I.M., Amin, M.B., Rahman, M., Hossain, M.I., Islam, M.R., Mahmud, Z.H., Unicomb, L., Islam, M.A., 2021. Human colonization with extended-spectrum beta-lactamase-producing E. coli in relation to animal and environmental exposures in Bangladesh: an observational One Health study. Environ. Health. Perspect. 129(3), 37001.
Sayin, N., Turkyilmaz, S., 2020. Investigation of antimicrobial resistance status of aerobic bacteria causing arthritis in broilers. Refu. Vet. 75(3), 153-160.
Shafiq, M., Huang, J., Shah, J.M., Ali, I., Rahman, S.U., Wang, L., 2021. Characterization and resistant determinants linked to mobile elements of ESBL-producing and mcr-1-positive Escherichia coli recovered from the chicken origin. Microb. Pathog. 150, 104722.
Shoaib, M., Kamboh, A.A., Sajid, A., Mughal, G.A., Leghari, R.A., Malhi, K.K., Bughio, S., Ali, A., Alam, S., Khan, S., Ali, S., 2016. Prevalence of extended spectrum beta-lactamase producing Enterobacteriaceae in commercial broilers and backyard chickens. Adv. Anim. Vet. Sci. 4(4), 209-214.
Solà-Ginés, M., González-López, J.J., Cameron-Veas, K., Piedra-Carrasco, N., Cerdà-Cuéllar, M., Migura-Garcia, L., 2015. Houseflies (Musca domestica) as vectors for extended-spectrum β-lactamase-producing Escherichia coli on Spanish broiler farms. Appl. Environ. Microbiol. 81(11), 3604-3611.
Subramanya, S.H., Bairy, I., Nayak, N., Amberpet, R., Padukone, S., Metok, Y., Bhatta, D. R., Sathian, B., 2020. Detection and characterization of ESBL-producing Enterobacteriaceae from the gut of healthy chickens, Gallus gallus domesticus in rural Nepal: Dominance of CTX-M-15-non-ST131 Escherichia coli clones. PLoS One. 15(5), e0227725.
Ur Rahman, S., Ahmad, S., Khan, I., 2019. Incidence of ESBL-producing Escherichia coli in poultry farm environment and retail poultry meat. Pak. Vet. J. 39(1), 116-120.
Van Hoek, A.H.A.M., Dierikx, C., Bosch, T., Schouls, L., Van Duijkeren, E., Visser, M., 2020. Transmission of ESBL-producing Escherichia coli between broilers and humans on broiler farms. J. Antimicrob. Chemother. 75(3), 543-549.
Wibisono, F.J., Sumiarto, B., Untari, T., Effendi, M.H., Permatasari, D.A., Witaningrum, A. M., 2021. Cases of multidrug resistance (MDR) and extended spectrum beta-lactamase (ESBL) producing Escherichia coli from broiler chicken in Blitar, Indonesia. Biochem. Cell. Arch. 21, 1923-1929.