Phylogrouping and genotyping of mcr-1 postives avian pathogenic Escherichia coli isolates in Algerian poultry farms
DOI:
https://doi.org/10.12834/VetIt.3929.40804.3Keywords:
APEC, genotyping, mcr-1, phylogrouping, virulanceAbstract
Colibacillosis is a highly prevalent bacterial disease in poultry, resulting in the widespread use of antibiotics for both curative and preventive purposes. Consequently, avian pathogenic Escherichia coli (APEC) continues to act as a reservoir for antibiotic resistance genes, including the mcr-1 gene, which codes for resistance to colistin, a crucial antibiotic in human medicine. The aim of this study was to evaluate the antibiotic resistance pattern of APEC and to investigate the genotyping, phylogrouping, and virulence of mcr-1-positive isolates. A total of 113 APEC were isolated, of which 92% were multidrug resistant (MDR). The mcr-1 gene was detected in 41 isolates originating from turkeys and broilers. Two isolates carried blaTEM, one of which also harboured blaCTX-M encoding beta-lactamases. The Clermont phylogrouping revealed that 76% of the isolates belonged to phylogroup B1. Concerning the detection of the virulence-associated genes, 88% of isolates carried at least 3 genes. The ERIC-PCR classified our isolates into 6 different clusters. Our study highlights the emergence of colistin resistance and MDR, which pose a real threat to poultry production and public health. Control of antibiotic use in the poultry sector is urgent and mandatory.References
Aberkane, C., Messaï, A., Messaï, C. R., & Boussaada, T. (2023). Antimicrobial resistance pattern of avian pathogenic Escherichia coli with detection of extended-spectrum β-lactamase-producing isolates in broilers in east Algeria. Veterinary World, 16 (3) 449‑454. https://doi.org/10.14202/vetworld.2023.449-454.
Ahmed, M. O., & Daw, M. A. (2023). Is Colistin Essential for the treatment and metaphylaxis of infections in Food-Producing Animals; One Health Debate. Public Health and Healthcare. https://doi.org/10.20944/preprints202311.0872.v1.
Akkari, H., Heleili, N., Ozgumus, O. B., Akarsu, N., & Kiliç, A. O. (2026). Intestinal carriage of mcr-1 and mcr-5 mediated colistin-resistant Escherichia coli in avian species : First report from broiler breeders and laying hens in Algeria. Microbial Pathogenesis, 210, 108180. https://doi.org/10.1016/j.micpath.2025.108180.
Alba, P., Leekitcharoenphon, P., Franco, A., Feltrin, F., Ianzano, A., Caprioli, A., Stravino, F., Hendriksen, R. S., Bortolaia, V., & Battisti, A. (2018). Molecular Epidemiology of mcr-Encoded Colistin Resistance in Enterobacteriaceae From Food-Producing Animals in Italy Revealed Through the EU Harmonized Antimicrobial Resistance Monitoring. Frontiers in Microbiology, 9, 1217. https://doi.org/10.3389/fmicb.2018.01217.
Al-Saiedi, R. L. R., & Al-Mayah, A. A. S. (2014). Pathogenicity testing of several APEC isolates obtained from naturally infected broiler birds reared in Basrah. International Journal of Poultry Science, 13(7), 374–378. https://doi.org/10.3923/ijps.2014.374.378.
Amer, M. M., Mekky, H. M., Fedawy, H. S., EL-Shemy, A., Bosila, M. A., & Elbayoumi, Kh. M. (2020). Molecular identification, genotyping of virulence-associated genes, and pathogenicity of cellulitis-derived Escherichia coli. Veterinary World, 13(12), 2703‑2712. https://doi.org/10.14202/vetworld.2020.2703-2712.
Anyanwu, M. U., Ikenna-Ezeh, N. H., Okafor, S. C., Ezemuoka, C. F., Nwobi, O. C., Ogunniran, T. M., Obodoechi, L. O., Okorie-Kanu, O. J., Mgbeahuruike, A. C., Okosi, I. R., & Jaja, I. F. (2024). Commercial Day-Old Chicks in Nigeria Are Potential Reservoirs of Colistin- and Tigecycline-Resistant Potentially Pathogenic Escherichia coli. Antibiotics, 13(11), 1067. https://doi.org/10.3390/antibiotics13111067.
Anyanwu, M. U., Jaja, I. F., & Nwobi, O. C. (2020). Occurrence and Characteristics of Mobile Colistin Resistance (mcr) Gene-Containing Isolates from the Environment : A Review. International Journal of Environmental Research and Public Health, 17(3), 1028. https://doi.org/10.3390/ijerph17031028.
Bachiri, T., Lalaoui, R., Bakour, S., Allouache, M., Belkebla, N., Rolain, J. M., & Touati, A. (2018). First report of the plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli ST405 isolated from wildlife in Bejaia, Algeria. Microbial Drug Resistance, 24(7), 890‑895. https://doi.org/10.1089/mdr.2017.0026.
Badr, H., Samir, A., El-Tokhi, E. I., Shahein, M. A., Rady, F. M., Hakim, A. S., Fouad, E. A., El-Sady, E. F., & Ali, S. F. (2022). Phenotypic and Genotypic Screening of Colistin Resistance Associated with Emerging Pathogenic Escherichia coli Isolated from Poultry. Veterinary Sciences, 9(6), 282. https://doi.org/10.3390/vetsci9060282
Basak, S., Singh, P., & Rajurkar, M. (2016). Multidrug Resistant and Extensively Drug Resistant Bacteria : A Study. Journal of Pathogens, 2016, 1 5. https://doi.org/10.1155/2016/4065603.
Berrazeg, M., Hadjadj, L., Ayad, A., Drissi, M., & Rolain, J.-M. (2016). First detected human case in Algeria of mcr-1 plasmid-mediated colistin resistance in a 2011 Escherichia coli isolate. Antimicrobial agents and chemotherapy, 60(11), 6996 6997. https://doi.org/10.1128/aac.01117-16.
Biström, M., Vennerström, P., Lienemann, T., Kurittu, P., Heikinheimo, A., & Pohjanvirta, T. (2025). Genomic epidemiology of avian pathogenic Escherichia coli in two broiler colibacillosis outbreaks in Finland. Veterinary Microbiology, 308, 110617. https://doi.org/10.1016/j.vetmic.2025.110617.
Bougouizi, A., Chekroud, Z., Rahab, H., Boumegoura, A., & Touati, A. (2024). Prevalence and characterization of Carbapenem-Resistant Enterobacterales among inpatients and outpatients in Skikda, Algeria. The Journal of Infection in Developing Countries, 18(03), 383 390. https://doi.org/10.3855/jidc.18263.
Boukli-Hacene, F., Djouadi, L. N., Raddaoui, A., Hachem, Y., Boumerdassi, H., Achour, W., & Nateche, F. (2024). Sheep and goats as reservoirs of colistin-resistant E. coli : First detection of ETEC ST10 and E. coli ST6396 mcr-1 positive strains in North Africa. Journal of Applied Microbiology, 135(9), lxae227. https://doi.org/10.1093/jambio/lxae227.
Boulbair, I., Hu, J., Hammoudi, A., Zhang, B., Aissat, S., Wang, X., Foudil, M., & Wang, S. (2025). Molecular Characterization and Antibiotic Resistance of Avian Pathogenic Escherichia coli (APEC) Isolates from Broiler Chickens in Algeria. Animals, 15(22), 3324. https://doi.org/10.3390/ani15223324.
Casarez, E. A., Pillai, S. D., & Di Giovanni, G. D. (2007). Genotype diversity of Escherichia coli isolates in natural waters determined by PFGE and ERIC-PCR. Water Research, 41(16), 3643‑3648. https://doi.org/10.1016/j.watres.2007.03.020.
Chabou, S., Leulmi, H., & Rolain, J.-M. (2019). Emergence of mcr-1-mediated colistin resistance in Escherichia coli isolates from poultry in Algeria. Journal of Global Antimicrobial Resistance, 16, 115‑116. https://doi.org/10.1016/j.jgar.2018.12.012.
Chaalal, N., Touati, A., Bakour, S., Aissa, M. A., Sotto, A., Lavigne, J.-P., & Pantel, A. (2021). Spread of OXA-48 and NDM-1-Producing Klebsiella pneumoniae ST48 and ST101 in Chicken Meat in Western Algeria. Microbial Drug Resistance, 27(4), 492‑500. https://doi.org/10.1089/mdr.2019.0419Chelaghma, W., Loucif, L., Bendjama, E., Cherak, Z., Bendahou, M., & Rolain, J.-M. (2022). Occurrence of extended spectrum cephalosporin-, carbapenem-and colistin-resistant Gram-negative bacteria in fresh vegetables, an increasing human health concern in Algeria. Antibiotics, 11(8), 988. https://doi.org/10.3390/antibiotics11080988.
Chenouf, N. S., Messaï, C. R., Carvalho, I., Álvarez-Gómez, T., Silva, V., Zitouni, A., Hakem, A., Poeta, P., & Torres, C. (2025). Serogrouping and Molecular Characterization of ESBL-Producing Avian Pathogenic Escherichia coli from Broilers and Turkeys with Colibacillosis in Algeria. Antibiotics, 14(4), 356. https://doi.org/10.3390/antibiotics14040356.
Cherak, Z., Loucif, L., Bendjama, E., Moussi, A., Benbouza, A., Grainat, N., & Rolain, J.-M. (2022). Dissemination of carbapenemases and MCR-1 producing gram-negative bacteria in aquatic environments in Batna, Algeria. Antibiotics, 11(10), 1314. https://doi.org/10.3390/antibiotics11101314.
Clermont, O., Christenson, J. K., Denamur, E., & Gordon, D. M. (2012). The Clermont Escherichia coli phylotyping method revisited : Improvement of specificity and detection of new phylogroups. Environmental Microbiology Reports. 5(1), 58-65. https://doi.org/10.1111/1758-2229.12019.
CLSI (2012). Methods for dilution antimicrobialsusceptibility tests for bacteria that grow aerobically. Approved Standard, 9th Edn., CLSI document M07-A9.
Cordeiro-Moura, J. R., Kraychete, G. B., de Araujo Longo, L. G., Corrêa, L. L., da Silva, N. M. V., Campana, E. H., Oliveira, C. J. B., & Picão, R. C. (2022). Description and comparative genomic analysis of a mcr-1-carrying Escherichia coli ST683/CC155 recovered from touristic coastal water in Northeastern Brazil. Infection, Genetics and Evolution, 97, 105196. https://doi.org/10.1016/j.meegid.2021.105196.
Dančová, N., Gregová, G., Szabóová, T., Regecová, I., Király, J., Hajdučková, V., & Hudecová, P. (2024). Quinolone and Tetracycline-Resistant Biofilm-Forming Escherichia coli Isolates from Slovak Broiler Chicken Farms and Chicken Meat. Applied Sciences, 14(20), 9514. https://doi.org/10.3390/app14209514.
Decré, D., Burghoffer, B., Gautier, V., Petit, J.-C., & Arlet, G. (2004). Outbreak of multi-resistant Klebsiella oxytoca involving strains with extended-spectrum β-lactamases and strains with extended-spectrum activity of the chromosomal β-lactamase. Journal of Antimicrobial Chemotherapy, 54(5), 881‑888. https://doi.org/10.1093/jac/dkh440.
Dhaouadi, S., Romdhani, A., Bouglita, W., Chedli, S., Chaari, S., Soufi, L., Cherif, A., Mnif, W., Abbassi, M. S., & Elandoulsi, R. B. (2023). High Biofilm-Forming Ability and Clonal Dissemination among Colistin-Resistant Escherichia coli Isolates Recovered from Cows with Mastitis, Diarrheic Calves, and Chickens with Colibacillosis in Tunisia. Life, 13(2), 299. https://doi.org/10.3390/life13020299.
Dhaouadi, S., Soufi, L., Hamza, A., Fedida, D., Zied, C., Awadhi, E., Mtibaa, M., Hassen, B., Cherif, A., Torres, C., Abbassi, M. S., & Landolsi, R. B. (2020). Co-occurrence of mcr-1 mediated colistin resistance and β-lactamase-encoding genes in multidrug-resistant Escherichia coli from broiler chickens with colibacillosis in Tunisia. Journal of Global Antimicrobial Resistance, 22, 538‑545. https://doi.org/10.1016/j.jgar.2020.03.017.
Dho-Moulin, M., & Fairbrother, J. M. (1999.). Avian pathogenic Escherichia coli (APEC). Veterinary research, 30(2-3), 299-316.
Dominguez, J. E., Redondo, L. M., Figueroa Espinosa, R. A., Cejas, D., Gutkind, G. O., Chacana, P. A., Di Conza, J. A., & Fernández Miyakawa, M. E. (2018). Simultaneous Carriage of mcr-1 and Other Antimicrobial Resistance Determinants in Escherichia coli From Poultry. Frontiers in Microbiology, 9, 1679. https://doi.org/10.3389/fmicb.2018.01679.
Drali, R., Berrazeg, M., Zidouni, L. L., Hamitouche, F., Abbas, A. A., Deriet, A., & Mouffok, F. (2018). Emergence of mcr-1 plasmid-mediated colistin-resistant Escherichia coli isolates from seawater. Science of the total environment, 642, 90 94. https://doi.org/10.1016/j.scitotenv.2018.05.387.
Dziri, O., Dziri, R., El Salabi, A. A., Alawami, A. A., Ksouri, R., & Chouchani, C. (2021). Polymyxin E–Resistant Gram-Negative Bacteria in Tunisia and Neighboring Countries : Are There Commonalities?. Infection and Drug Resistance, 14, 4821 4832. https://doi.org/10.2147/IDR.S327718.
EUCAST (2022). The European Committee onAntimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version12.0: 1-110.
Fancher, C. A., Thames, H. T., Colvin, M. G., Smith, M., Easterling, A., Nuthalapati, N., Zhang, L., Kiess, A., Dinh, T. T. N., & Theradiyil Sukumaran, A. (2021). Prevalence and Molecular Characteristics of Avian Pathogenic Escherichia coli in “No Antibiotics Ever” Broiler Farms. Microbiology Spectrum, 9(3), e00834-21. https://doi.org/10.1128/Spectrum.00834-21.
Fratamico, P. M., DebRoy, C., Liu, Y., Needleman, D. S., Baranzoni, G. M., & Feng, P. (2016). Advances in Molecular Serotyping and Subtyping of Escherichia coli. Frontiers in Microbiology, 7, 644. https://doi.org/10.3389/fmicb.2016.00644.
Ghanbarpour, R., Sami, M., Salehi, M., & Ouromiei, M. (2011). Phylogenetic background and virulence genes of Escherichia coli isolates from colisepticemic and healthy broiler chickens in Iran. Tropical Animal Health and Production, 43(1), 153‑157. https://doi.org/10.1007/s11250-010-9667-2.
Gharaibeh, M. H., Al Sheyab, S. Y., Malkawi, I. M., & Al Qudsi, F. R. (2024). Phenotypic and genotypic characterization of Escherichia coli isolated from the chicken liver in relation to slaughterhouse conditions. Heliyon, 10(6), e27759. https://doi.org/10.1016/j.heliyon.2024.e27759.
Guabiraba, R., & Schouler, C. (2015). Avian colibacillosis : Still many black holes. FEMS Microbiology Letters, 362(15), fnv118. https://doi.org/10.1093/femsle/fnv118.
Hackman, H. K., Annison, L., Arhin, R. E., Aidoo, E. K., Wilberforce, E. A., Mensah, A. C., Appiah, L., Annison, S., & Ayim-Akonor, M. (2025). Awareness of antimicrobial resistance and antibiotic use among poultry farmers in Accra, Ghana : A cross-sectional survey. PLOS One, 20(12), e0337531. https://doi.org/10.1371/journal.pone.0337531.
Haenni, M., Poirel, L., Kieffer, N., Châtre, P., Saras, E., Métayer, V., Dumoulin, R., Nordmann, P., & Madec, J.-Y. (2016). Co-occurrence of extended spectrum β lactamase and MCR-1 encoding genes on plasmids. The Lancet Infectious Diseases, 16(3), 281‑282. https://doi.org/10.1016/S1473-3099(16)00007-4.
Halfaoui, Z., Rahab, H., Achek, R., & Menoueri, M. N. (2024). First report of detection of mcr-1 and virulence genes in avian pathogenic Escherichia coli in the center of Algeria. Iranian Journal of Veterinary Research, 25(1). https://doi.org/10.22099/ijvr.2024.47413.6840.
Halfaoui, Z., Menoueri, N. M., & Bendali, L. M. (2017). Serogrouping and antibiotic resistance of Escherichia coli isolated from broiler chicken with colibacillosis in center of Algeria. Veterinary World, 10(7), 830‑835. https://doi.org/10.14202/vetworld.2017.830-835.
Hamoudi, A., & Aggad, H. (2008). Antibioresistance of Escherichia coli Strains Isolated from Chicken Colibacillosis in Western Algeria. Turkish Journal of Veterinary & Animal Sciences, 32(2), 123-126.
Hulton, C. S., Higgins, C. F., & Sharp, P. M. (1991). ERIC sequences : A novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimurium and other enterobacteria. Molecular Microbiology, 5(4), 825‑834. https://doi.org/10.1111/j.1365-2958.1991.tb00755.x.
Igwaran, A., Iweriebor, B. C., & Okoh, A. I. (2018). Molecular characterization and antimicrobial resistance pattern of Escherichia coli recovered from wastewater treatment plants in Eastern Cape South Africa. International journal of environmental research and public health, 15(6), 1237. https://doi.org/10.3390/ijerph15061237.
Jalil, A., Masood, S., Ain, Q., Andleeb, S., Dudley, E. G., & Adnan, F. (2023). High resistance of fluoroquinolone and macrolide reported in avian pathogenic Escherichia coli isolates from the humid subtropical regions of Pakistan. Journal of Global Antimicrobial Resistance, 33, 5‑17. https://doi.org/10.1016/j.jgar.2023.01.009.
Jansen, W., Van Hout, J., Wiegel, J., Iatridou, D., Chantziaras, I., & De Briyne, N. (2022). Colistin Use in European Livestock : Veterinary Field Data on Trends and Perspectives for Further Reduction. Veterinary Sciences, 9(11), 650. https://doi.org/10.3390/vetsci9110650.
Jhandai, P., Mittal, D., Gupta, R., & Kumar, M. (2024). Phylogrouping of Escherichia coli strains from colibacillosis affected chicken. International Journal of Advanced Biochemistry Research, 8(3S), 182‑186. https://doi.org/10.33545/26174693.2024.v8.i3Sc.718.
Johnson, T. J., Miller, E. A., Flores-Figueroa, C., Munoz-Aguayo, J., Cardona, C., Fransen, K., Lighty, M., Gonder, E., Nezworski, J., Haag, A., Behl, M., Kromm, M., Wileman, B., Studniski, M., & Singer, R. S. (2022). Refining the definition of the avian pathogenic Escherichia coli (APEC) pathotype through inclusion of high-risk clonal groups. Poultry Science, 101(10), 102009. https://doi.org/10.1016/j.psj.2022.102009.
Johnson, T. J., Wannemuehler, Y., Doetkott, C., Johnson, S. J., Rosenberger, S. C., & Nolan, L. K. (2008). Identification of Minimal Predictors of Avian Pathogenic Escherichia coli Virulence for Use as a Rapid Diagnostic Tool. Journal of Clinical Microbiology, 46(12), 3987‑3996. https://doi.org/10.1128/JCM.00816-08.
Johnson, T. J., Siek, K. E., Johnson, S. J., & Nolan, L. K. (2006). DNA Sequence of a ColV Plasmid and Prevalence of Selected Plasmid-Encoded Virulence Genes among Avian Escherichia coli Strains. Journal of Bacteriology, 188(2), 745‑758. https://doi.org/10.1128/JB.188.2.745-758.2006.
Johnson, J. R., & Stell, A. L. (2000). Extended Virulence Genotypes of Escherichia coli Strains from Patients with Urosepsis in Relation to Phylogeny and Host Compromise. The Journal of Infectious Diseases, 181(1), 261‑272. https://doi.org/10.1086/315217.
Kathayat, D., Lokesh, D., Ranjit, S., & Rajashekara, G. (2021). Avian Pathogenic Escherichia coli (APEC) : An Overview of Virulence and Pathogenesis Factors, Zoonotic Potential, and Control Strategies. Pathogens, 10(4), 467. https://doi.org/10.3390/pathogens10040467.
Kathayat, D., Helmy, Y. A., Deblais, L., & Rajashekara, G. (2018). Novel small molecules affecting cell membrane as potential therapeutics for avian pathogenic Escherichia coli. Scientific Reports, 8(1), 15329. https://doi.org/10.1038/s41598-018-33587-5.
Kiersten J., M., Zhang, L., Foxman, B., Bauer, R. J., & Marrs, C. F. (2003). Evaluation of Genotyping Large Numbers of Escherichia coli Isolates by Enterobacterial Repetitive Intergenic Consensus-PCR. Journal of Clinical Microbiology, 41(11), 5224‑5226. https://doi.org/10.1128/jcm.41.11.5224-5226.2003.
Kiiru, J., Kariuki, S., Goddeeris, B. M., & Butaye, P. (2012). Analysis of β-lactamase phenotypes and carriage of selected β-lactamase genes among Escherichia coli strains obtained from Kenyan patients during an 18-year period. BMC Microbiology, 12, 155. https://doi.org/10.1186/1471-2180-12-155.
Kimura, A. H., Koga, V. L., De Souza Gazal, L. E., De Brito, B. G., De Brito, K. C. T., Navarro-Ocaña, A., Nakazato, G., & Kobayashi, R. K. T. (2021). Characterization of multidrug-resistant avian pathogenic Escherichia coli : An outbreak in canaries. Brazilian Journal of Microbiology, 52(2), 1005‑1012. https://doi.org/10.1007/s42770-021-00443-0.
Kromann, S., Baig, S., Stegger, M., Olsen, R. H., Bojesen, A. M., Jensen, H. E., & Thøfner, I. (2022). Longitudinal study on background lesions in broiler breeder flocks and their progeny, and genomic characterisation of Escherichia coli. Veterinary Research, 53(1), 52. https://doi.org/10.1186/s13567-022-01064-7.
Kubelová, M., Koláčková, I., Gelbíčová, T., Florianová, M., Kalová, A., & Karpíšková, R. (2021). Virulence Properties of mcr-1-Positive Escherichia coli Isolated from Retail Poultry Meat. Microorganisms, 9(2), 308. https://doi.org/10.3390/microorganisms9020308.
Lima Barbieri, N., Nielsen, D. W., Wannemuehler, Y., Cavender, T., Hussein, A., Yan, S., Nolan, L. K., & Logue, C. M. (2017). Mcr-1 identified in Avian Pathogenic Escherichia coli (APEC). PLOS ONE, 12(3), e0172997. https://doi.org/10.1371/journal.pone.0172997.
Lounis, M., Zhao, G., Li, Y., Gao, Y., Wang, J., Oumouna, M., & Oumouna, K. (2020). Molecular profile of avian pathogenic Escherichia coli (APEC) from poultry associated with colibacillosis in Algeria. Journal of the Hellenic Veterinary Medical Society, 71(2), 2113. https://doi.org/10.12681/jhvms.23666.
Mageiros, L., Méric, G., Bayliss, S. C., Pensar, J., Pascoe, B., Mourkas, E., Calland, J. K., Yahara, K., Murray, S., Wilkinson, T. S., Williams, L. K., Hitchings, M. D., Porter, J., Kemmett, K., Feil, E. J., Jolley, K. A., Williams, N. J., Corander, J., & Sheppard, S. K. (2021). Genome evolution and the emergence of pathogenicity in avian Escherichia coli. Nature Communications, 12(1), 765. https://doi.org/10.1038/s41467-021-20988-w.
Mbanga, J., & Nyararai, Y. O. (2015). Virulence gene profiles of avian pathogenic Escherichia coli isolated from chickens with colibacillosis in Bulawayo, Zimbabwe. The Onderstepoort Journal of Veterinary Research, 82(1), e1‑e8. https://doi.org/10.4102/ojvr.v82i1.850.
Meguenni, N., Chanteloup, N., Tourtereau, A., Ahmed, C. A., Bounar-Kechih, S., & Schouler, C. (2019). Virulence and antibiotic resistance profile of avian Escherichia coli strains isolated from colibacillosis lesions in central of Algeria. Veterinary World, 12(11), 1840‑1848. https://doi.org/10.14202/vetworld.2019.1840-1848.
Meguenni, N., Le Devendec, L., Jouy, E., Le Corvec, M., Bounar-Kechih, S., Bakour, R., & Kempf, I. (2015). First Description of an Extended-Spectrum Cephalosporin- and Fluoroquinolone-Resistant Avian Pathogenic Escherichia coli Clone in Algeria. Avian Diseases, 59(1), 20‑23. https://doi.org/10.1637/10804-022414-Reg.1.
Mehat, J. W., Van Vliet, A. H. M., & La Ragione, R. M. (2021). The Avian Pathogenic Escherichia coli (APEC) pathotype is comprised of multiple distinct, independent genotypes. Avian Pathology, 50(5), 402‑416. https://doi.org/10.1080/03079457.2021.1915960.
Mellata, M. (2013). Human and Avian Extraintestinal Pathogenic Escherichia coli : Infections, Zoonotic Risks, and Antibiotic Resistance Trends. Foodborne Pathogens and Disease, 10(11), 916‑932. https://doi.org/10.1089/fpd.2013.1533.
Milanov, D., Prunic, B., Velhner, M., Pajic, M., & Cabarkapa, I. (2015). RDAR morphotype : A resting stage of some Enteroba cteriaceae. Food and Feed Research, 42(1), 43‑50. https://doi.org/10.5937/FFR1501043.
Mišić, D., Kiskaroly, F., Szostak, M. P., Cabal, A., Ruppitsch, W., Bernreiter-Hofer, T., Milovanovic, V., Feßler, A. T., Allerberger, F., Spergser, J., Müller, E., Schwarz, S., Braun, S. D., Monecke, S., Ehricht, R., Korus, M., Benković, D., Korzeniowska, M., & Loncaric, I. (2021). The First Report of mcr-1-Carrying Escherichia coli Originating from Animals in Serbia. Antibiotics, 10(9), 1063. https://doi.org/10.3390/antibiotics10091063.
Mohamed, L., Ge, Z., Yuehua, L., Yubin, G., Rachid, K., Mustapha, O., Junwei, W., & Karine, O. (2018). Virulence traits of avian pathogenic (APEC) and fecal (AFEC) E. coli isolated from broiler chickens in Algeria. Tropical Animal Health and Production, 50(3), 547‑553. https://doi.org/10.1007/s11250-017-1467-5.
Monroy, I., Catalá-Gregori, P., & Sevilla-Navarro, S. (2025). Assessment of antibiotic resistance and virulence in Escherichia coli strains isolated from poultry in Spain. Poultry Science, 104(2), 104838. https://doi.org/10.1016/j.psj.2025.104838.
Nabti, L. Z., Sahli, F., Hadjadj, L., Ngaiganam, E. P., Lupande-Mwenebitu, D., Rolain, J.-M., & Diene, S. M. (2019). Autochthonous case of mobile colistin resistance gene mcr-1 from a uropathogenic Escherichia coli isolate in Sétif Hospital, Algeria. Journal of global antimicrobial resistance, 19, 356 357. https://doi.org/10.1016/j.jgar.2019.10.006.
Nawaz, S., Wang, Z., Zhang, Y., Jia, Y., Jiang, W., Chen, Z., Yin, H., Huang, C., & Han, X. (2024). Avian pathogenic Escherichia coli (APEC) : Current insights and future challenges. Poultry Science, 103(12), 104359. https://doi.org/10.1016/j.psj.2024.104359.
Ngbede, E. O., Poudel, A., Kalalah, A., Yang, Y., Adekanmbi, F., Adikwu, A. A., Adamu, A. M., Mamfe, L. M., Daniel, S. T., & Useh, N. M. (2020). Identification of mobile colistin resistance genes (mcr-1.1, mcr-5 and mcr-8.1) in Enterobacteriaceae and Alcaligenes faecalis of human and animal origin, Nigeria. International Journal of Antimicrobial Agents, 56(3), 106108. https://doi.org/10.1016/j.ijantimicag.2020.106108.
Osisiogu, E. U., Mahmoud, F. C., Waqas, F. B., Singh, B., Feglo, P. K., & Duedu, K. O. (2025). Environmental mediation of colistin resistance in the African context. A systematic scoping review. Journal of Global Antimicrobial Resistance, 41, 39 43. https://doi.org/10.1016/j.jgar.2024.12.002.
Osman, K., Mustafa, A., Elhariri, M., & AbdElhamed, G. (2012). Identification of serotypes and virulence markers of Escherichia coli isolated from human stool and urine samples in Egypt. Indian Journal of Medical Microbiology, 30(3), 308‑313. https://doi.org/10.4103/0255-0857.99492.
Ovi, F., Zhang, L., Nabors, H., Jia, L., & Adhikari, P. (2023). A compilation of virulence-associated genes that are frequently reported in avian pathogenic Escherichia coli (APEC) compared to other E. coli. Journal of Applied Microbiology, 134(3), lxad014. https://doi.org/10.1093/jambio/lxad014.
Peng, Z., Zhang, X., Li, X., Hu, Z., Li, Z., Jia, C., Dai, M., Tan, C., Chen, H., & Wang, X. (2021). Characteristics of colistin-resistant Escherichia coli from pig farms in Central China. Animal Diseases, 1(1), 9. https://doi.org/10.1186/s44149-021-00009-5.
Poirel, L., Madec, J.-Y., Lupo, A., Schink, A.-K., Kieffer, N., Nordmann, P., & Schwarz, S. (2018). Antimicrobial Resistance in Escherichia coli. Microbiology Spectrum, 6(4), 6.4.14. https://doi.org/10.1128/microbiolspec.ARBA-0026-2017.
Poirel, L., Jayol, A., & Nordmann, P. (2017). Polymyxins : Antibacterial Activity, Susceptibility Testing, and Resistance Mechanisms Encoded by Plasmids or Chromosomes. Clinical Microbiology Reviews, 30(2), 557‑596. https://doi.org/10.1128/CMR.00064-16.
Puterflam, J., Souillard, R., Balaine, L., Galliot, P., Lucas, P., Bougeard, S., Kempf, I., Keita, A., Delannoy, S., Schouler, C., & Le Bouquin, S. (2022). Colisée—Controlling colibacillosis in chicken. Agronomic innovations, 85, pp.83-92. https://dx.doi.org/10.17180/ciag-2022-vol85-art07.
Rebelo, A. R., Bortolaia, V., Kjeldgaard, J. S., Pedersen, S. K., Leekitcharoenphon, P., Hansen, I. M., Guerra, B., Malorny, B., Borowiak, M., Hammerl, J. A., Battisti, A., Franco, A., Alba, P., Perrin-Guyomard, A., Granier, S. A., De Frutos Escobar, C., Malhotra-Kumar, S., Villa, L., Carattoli, A., & Hendriksen, R. S. (2018). Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance, 23(6). https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672.
Rezatofighi, S. E., Najafifar, A., Askari Badouei, M., Peighambari, S. M., & Soltani, M. (2021). An Integrated Perspective on Virulence-Associated Genes (VAGs), Antimicrobial Resistance (AMR), and Phylogenetic Clusters of Pathogenic and Non-pathogenic Avian Escherichia coli. Frontiers in Veterinary Science, 8, 758124. https://doi.org/10.3389/fvets.2021.758124.
Rodrigues, S. V., Laviniki, V., Borges, K. A., Furian, T. Q., Moraes, H. L. S., Nascimento, V. P., & Salle, C. T. P. (2019). Biofilm Formation by Avian Pathogenic Escherichia coli is Not Related to In Vivo Pathogenicity. Current Microbiology, 76(2), 194 199. https://doi.org/10.1007/s00284-018-1608-8.
Saeed, M. A., Asif, H., Ehtisham-ul-Haque, S., Khan, A. U., Rehman, A. U., Rehman, A., Rafique, M. K., Ahmed, I., Qamar, M. F., Tomaso, H., & El-Adawy, H. (2025). Detection and risk factor analysis of avian colibacillosis associated with colistin-resistant Escherichia coli and Klebsiella pneumoniae. Frontiers in Veterinary Science, 12, 1612542. https://doi.org/10.3389/fvets.2025.1612542.
Saha, O., Hoque, M. N., Islam, O. K., Rahaman, Md. M., Sultana, M., & Hossain, M. A. (2020). Multidrug-Resistant Avian Pathogenic Escherichia coli Strains and Association of Their Virulence Genes in Bangladesh. Microorganisms, 8(8), 1135. https://doi.org/10.3390/microorganisms8081135.
Saidani, M., Messadi, L., Mefteh, J., Chaouechi, A., Soudani, A., Selmi, R., Dâaloul-Jedidi, M., Chehida, F. B., Mamlouk, A., & Jemli, M. H. (2019). Various Inc-type plasmids and lineages of Escherichia coli and Klebsiella pneumoniae spreading blaCTX-M-15, blaCTX-M-1 and mcr-1 genes in camels in Tunisia. Journal of Global Antimicrobial Resistance, 19, 280‑283. https://doi.org/10.1016/j.jgar.2019.05.007.
Schouler, C., Schaeffer, B., Brée, A., Mora, A., Dahbi, G., Biet, F., Oswald, E., Mainil, J., Blanco, J., & Moulin-Schouleur, M. (2012). Diagnostic strategy for identifying avian pathogenic Escherichia coli based on four patterns of virulence genes. Journal of Clinical Microbiology, 50(5), 1673‑1678. https://doi.org/10.1128/JCM.05057-11.
Shankar, T. V. S., Sharma, A., & Grover, Y. P. (2010). Studies on different virulence factors of avian pathogenic Escherichia coli. Haryana Vet, 49, 45-47.
Sivaranjani, M., McCarthy, M. C., Sniatynski, M. K., Wu, L., Dillon, J.-A. R., Rubin, J. E., & White, A. P. (2022). Biofilm Formation and Antimicrobial Susceptibility of E. coli Associated With Colibacillosis Outbreaks in Broiler Chickens From Saskatchewan. Frontiers in Microbiology, 13, 841516. https://doi.org/10.3389/fmicb.2022.841516.
Skyberg, J. A., Siek, K. E., Doetkott, C., & Nolan, L. K. (2007). Biofilm formation by avian Escherichia coli in relation to media, source and phylogeny. Journal of Applied Microbiology, 102(2). https://doi.org/10.1111/j.1365-2672.2006.03076.
Smelikova, E., Tkadlec, J., & Krutova, M. (2022). How to : Screening for mcr-mediated resistance to colistin. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 28(1), 43-50. https://doi.org/10.1016/j.cmi.2021.09.009.
Srisrattakarn, A., Saiboonjan, B., Tippayawat, P., Angkititrakul, S., Chanawong, A., Pornchoo, C., Smithkittipol, C., & Lulitanond, A. (2025). CTX-M, SHV, TEM and VEB β-lactamases, and MCR-1 among multidrug-resistant Escherichia coli and Klebsiella isolates from environment near animal farms in Thailand. Journal of Infection and Public Health, 18(2), 102624. https://doi.org/10.1016/j.jiph.2024.102624.
Terveer, E. M., Nijhuis, R. H. T., Crobach, M. J. T., Knetsch, C. W., Veldkamp, K. E., Gooskens, J., Kuijper, E. J., & Claas, E. C. J. (2017). Prevalence of colistin resistance gene (mcr-1) containing Enterobacteriaceae in feces of patients attending a tertiary care hospital and detection of a mcr-1 containing, colistin susceptible E. coli. PloS One, 12(6), e0178598. https://doi.org/10.1371/journal.pone.0178598.
Thabet, A. M., Alzuheir, I. M., Al Laham, N. A., Helal, B. Y. A., Fayyad, A. F., Jalboush, N. H., & Gharaibeh, M. H. (2023). First report of mobile colistin resistance gene mcr-1 in avian pathogenic Escherichia coli isolated from turkeys in the Gaza Strip, Palestine. Veterinary World, 1260‑1265. https://doi.org/10.14202/vetworld.2023.1260-1265.
Thabet, S., Souissi, N., & Khazri, I. (2022). Assessment of antimicrobial resistance in avian pathogenic Escherichia coli Strains isolated over four years in Tunisian poultry. Afr. J. Bacteriol. Res, 14(1), 1-7. https://doi.org/10.5897/JBR2016.0212.
Touati, M., Hadjadj, L., Berrazeg, M., Baron, S. A., & Rolain, J. M. (2020). Emergence of Escherichia coli harbouring mcr-1 and mcr-3 genes in North West Algerian farmlands. Journal of global antimicrobial resistance, 21, 132‑137. https://doi.org/10.1016/j.jgar.2019.10.001.
Uddin, M. S., Masum, Md. H. U., Hosen, Md. R., Roy, S. C., Rahman, A. B. Z. N., Siddiquee, N. H., Siddiqua, A., Hossain, I., & Peas, T. (2025). Multidrug Resistance and Virulence Gene Profiles of E. coli in Broiler Chickens : A Study From Noakhali, Bangladesh. Veterinary Medicine International, 2025(1), 1157843. https://doi.org/10.1155/vmi/1157843.
Ugwu, I. C., Lee-Ching, L., Ugwu, C. C., Okoye, J. O. A., & Chah, K. F. (2020). In vitro assessment of pathogenicity and virulence encoding gene profiles of avian pathogenic Escherichia coli strains associated with colibacillosis in chickens. Iranian journal of veterinary research, 21(3), 180.
Valiakos, G., & Kapna, I. (2021). Colistin Resistant mcr Genes Prevalence in Livestock Animals (Swine, Bovine, Poultry) from a Multinational Perspective. A Systematic Review. Veterinary Sciences, 8(11), 265. https://doi.org/10.3390/vetsci8110265.
van der Westhuizen, W. A., & Bragg, R. R. (2012). Multiplex polymerase chain reaction for screening avian pathogenic Escherichia coli for virulence genes. Avian Pathology: Journal of the W.V.P.A, 41(1), 33‑40. https://doi.org/10.1080/03079457.2011.631982.
Vougat Ngom, R., Ferreira, H. C. D. C., Ayissi, G., Tanyienow, A., & Piccirillo, A. (2025). A systematic review and meta-analysis on the efficacy of antibiotic treatment in controlling colibacillosis in broiler production. PLOS One, 20(7), e0326535. https://doi.org/10.1371/journal.pone.0326535.
Wang, S., Liu, L., Du, L., Gao, S., Yu, X., Cheng, L., Chen, Y., Kou, Z., & Sun, W. (2025). Emergence of coexisting bla NDM and mcr-1 genes in Escherichia coli isolates from the guts of healthy individuals. Microbiology Spectrum, e02014-25. https://journals.asm.org/doi/pdf/10.1128/spectrum.02014-25.
Wu, C., Wang, Y., Shi, X., Wang, S., Ren, H., Shen, Z., Wang, Y., Lin, J., & Wang, S. (2018). Rapid rise of the ESBL and mcr-1 genes in Escherichia coli of chicken origin in China, 2008–2014. Emerging Microbes & Infections, 7(1), 1‑10. https://doi.org/10.1038/s41426-018-0033-1.
Zhu, Z., Cao, M., Wang, W., Zhu, Q., Wang, C., Zhang, Y., Shi, Y., Zhou, X., Cui, G., &Zhang, J. (2021). Virulence-Associated Genes and Genetic Diversity of Avian Pathogenic (APEC) and Fecal (AFEC) E. Coli Isolates From Chickens. Research Square Platform LLC. https://doi.org/10.21203/rs.3.rs-644399/v2.
Zhu Ge, X., Jiang, J., Pan, Z., Hu, L., Wang, S., Wang, H., Leung, F. C., Dai, J., & Fan, H. (2014). Comparative Genomic Analysis Shows That Avian Pathogenic Escherichia coli Isolate IMT5155 (O2:K1:H5; ST Complex 95, ST140) Shares Close Relationship with ST95 APEC O1:K1 and Human ExPEC O18:K1 Strains. PLoS ONE, 9(11), e112048. https://doi.org/10.1371/journal.pone.0112048.
