{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T13:02:30Z","timestamp":1783688550103,"version":"3.55.0"},"reference-count":61,"publisher":"Veterinary World","license":[{"start":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T00:00:00Z","timestamp":1771804800000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vet. World"],"published-print":{"date-parts":[[2026,2,28]]},"abstract":"<jats:p>Background and Aim: The African Houbara bustard (Chlamydotis undulata), a species of high conservation concern, is maintained through intensive captive breeding programs where bacterial diseases may compromise productivity and reintroduction success. Escherichia coli is frequently implicated in reproductive failure, early mortality, and septicemic conditions; however, integrated phenotypic and genotypic characterization of antimicrobial resistance and virulence across life stages in this species remains scarce. This study aimed to determine the prevalence of E. coli across different life stages of captive African Houbara bustards, characterize multidrug-resistant (MDR), extensively drug-resistant (XDR), and extended-spectrum \u03b2-lactamase (ESBL) phenotypes, and profile avian pathogenic E. coli (APEC)\u2013associated virulence genes within a One Health framework. \n\nMaterials and Methods: A cross-sectional diagnostic investigation was conducted during the 2025 production season. A total of 110 samples were collected from early embryonic death (n = 50), chicks (n = 25), juveniles (n = 25), and adult females (n = 10). Isolation and identification of E. coli were performed using conventional bacteriology and the VITEK\u00ae2 system. Antimicrobial susceptibility testing was carried out using disk diffusion and VITEK\u00ae2 AST, with resistance patterns classified according to international MDR and XDR definitions. Phenotypic ESBL detection was undertaken, and a multiplex real-time polymerase chain reaction (PCR) assay targeting 15 APEC-associated virulence genes was applied to representative isolates. \n\nResults: E. coli was isolated from 62.7% (69\/110) of samples, with the highest prevalence observed in juveniles (84%) and chicks (80%). All isolates were resistant to ampicillin and fluoroquinolones, while complete susceptibility was observed to fosfomycin, aminoglycosides, and chloramphenicol. MDR was detected in 96.9% of tested isolates, and one XDR isolate resistant to 15 antibiotics was identified. ESBL-producing E. coli were detected in juveniles (14%) and early embryonic death samples (9%). Virulence profiling revealed a high gene burden, with most isolates harboring \u226510 virulence genes, particularly those associated with iron acquisition, protectins, and invasion. \n\nConclusion: Captive African Houbara bustards harbor highly virulent MDR and ESBL-producing E. coli across life stages, posing significant conservation, veterinary, and public health risks. Strengthened biosecurity, prudent antimicrobial stewardship, and integrated One Health surveillance are essential to improve breeding success and safeguard reintroduction programs. \n\nKeywords: African Houbara bustard, antimicrobial resistance, avian pathogenic Escherichia coli, captive breeding, extended-spectrum beta-lactamase, multidrug resistance, One Health, virulence genes.<\/jats:p>","DOI":"10.14202\/vetworld.2026.654-666","type":"journal-article","created":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T15:11:15Z","timestamp":1772032275000},"page":"654","update-policy":"https:\/\/doi.org\/10.14202\/vetworld.2022.policies","source":"Crossref","is-referenced-by-count":1,"title":["Phenotypic and genotypic characterization of multidrug-resistant avian pathogenic Escherichia coli across life stages of captive African Houbara bustards: Conservation and One Health implications"],"prefix":"10.14202","author":[{"given":"Sara M.","family":"Rashad","sequence":"first","affiliation":[{"name":"Labouratory manager, Bacteriology and Molecular biology units, International Foundation for Ecological Research (IFER), Errachidia, Morocco."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"5308","published-online":{"date-parts":[[2026,2,23]]},"reference":[{"key":"ref0","doi-asserted-by":"crossref","unstructured":"1.\tD\u00edaz S, Fargione J, Chapin FI, Tilman D. Biodiversity loss threatens human well-being. PLoS Biol. 2009;4:e277.","DOI":"10.1371\/journal.pbio.0040277"},{"key":"ref1","unstructured":"2.\tIUCN\/SSC. The IUCN Red List of Threatened Species: Chlamydotis undulata. International Union for Conservation of Nature; 2014."},{"key":"ref2","unstructured":"3.\tRalls K, Meadows L. Captive breeding programs and the conservation of endangered species. Conserv Biol. 2001;15:1080\u20131090."},{"key":"ref3","unstructured":"4.\tConde DA, Colchero F, Guill\u00e9n J. Integrating life history and demography in conservation programs. Biol Conserv. 2011;144:2562\u20132570."},{"key":"ref4","unstructured":"5.\tTaylor G, Lacy R, Feistner A. Captive breeding in conservation. Zoo Biol. 2017;36:127\u2013136."},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"6.\tCrispo E, Smith J, Thompson R. Genital infections in captive birds: salpingitis and peritonitis. Avian Pathol. 2025;54:12\u201325.","DOI":"10.1080\/03079457.2025.2499586"},{"key":"ref6","unstructured":"7.\tLandman W, Feberwee A, Mevius D. Avian colibacillosis: pathogenesis and control strategies. Avian Pathol. 2013;42:403\u2013410."},{"key":"ref7","unstructured":"8.\tNolan L, Barnes H, Vaillancourt J. Colibacillosis in poultry: new insights. Poult Sci. 2020;99:16\u201329."},{"key":"ref8","unstructured":"9.\tDobbin G, Paul N, Gibb ZZ. Zoonotic bacteria in wild birds. J Wildl Dis. 2005;41:725\u2013733."},{"key":"ref9","unstructured":"10.\tStievenart C, Mohammed H. Health status of Houbara bustards in captivity. Int J Avian Sci. 2004;146:203\u2013211."},{"key":"ref10","unstructured":"11.\tEffendi, Ramandinianto SC, Wibowo S, Fauziah I, Kusala MKJ, Fauzia KA, Furqoni AH, Raissa R. Omphalitis and yolk sac infection in poultry: etiology, pathology, and epidemiology. Vet World. 2024;17(12):1050\u20131060."},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"12.\tHermawan FA, Nadania Zega DIS, Triatjaya Y, Khairani S, Pratiwi U. Anatomical pathology features in day-old chicks with omphalitis. ARSHI Vet Lett. 2024;8(3):53\u201354.","DOI":"10.29244\/avl.8.3.53-54"},{"key":"ref12","unstructured":"13.\tShahjada F, Rahman M, Islam K. Pathogenic E. coli in poultry production. J Vet Sci. 2017;18:123\u2013130."},{"key":"ref13","unstructured":"14.\tOIE. World Organisation for Animal Health: antimicrobial resistance report. OIE Publishing; 2019."},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"15.\tNaghavi M, Vollset SE, Ikuta KS, Swetschinski LR, et al. Global burden of bacterial antimicrobial resistance 1990\u20132021: a systematic analysis with forecasts to 2050. Lancet. 2024;404(10459):1199\u20131226.","DOI":"10.1016\/S0140-6736(24)01867-1"},{"key":"ref15","unstructured":"16.\tWorld Health Organization. Global Antibiotic Resistance Surveillance Report 2025. Geneva: World Health Organization; 2025. ISBN: 9789240116337. Available from: https:\/\/www.who.int\/publications\/i\/item\/ 9789240116337."},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"17.\tPulingam T, Rahman A, Khan S. Inappropriate antibiotic use in veterinary medicine. Antibiotics. 2022;11:678.","DOI":"10.3390\/antibiotics11111539"},{"key":"ref17","unstructured":"18.\tBartoloni A, Cutts F, Leoni S. Antibiotic resistance in remote areas. Trop Med Int Health. 2004;9:467\u2013471."},{"key":"ref18","unstructured":"19.\tGilliver R, Bennett M, Begon M. Antibiotic-resistant bacteria in wild animals. Environ Microbiol. 1999;1:361\u2013367."},{"key":"ref19","unstructured":"20.\tWoodford N, Kock R. Transmission of antibiotic-resistant bacteria. J Antimicrob Chemother. 1991;27:15\u201325."},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"21.\tWoodford N. Extended-spectrum beta-lactamases in Enterobacteriaceae. Clin Microbiol Infect. 2000;6:460\u2013466.","DOI":"10.1046\/j.1469-0691.2000.00107.x"},{"key":"ref21","unstructured":"22.\tPoirel L, Madec J, Lupo A. Resistance to cephalosporins via ESBLs in Enterobacteriaceae. Front Microbiol. 2018;9:2082."},{"key":"ref22","unstructured":"23.\tGiufr\u00e8 M, Accogli M, Cerquetti M. ESBL-producing E. coli in animals and humans. Antibiotics. 2021;10:125."},{"key":"ref23","unstructured":"24.\tCardozo M, Furlan J, Souza R. Extended-spectrum beta-lactamase producing E. coli: epidemiology and public health implications. J Glob Antimicrob Resist. 2022;28:62\u201370."},{"key":"ref24","unstructured":"25.\tPan Y, Zhao F, Li X. Interplay between virulence factors and antibiotic resistance in E. coli. Front Microbiol. 2020;11:1351."},{"key":"ref25","unstructured":"26.\tSora V, et al. Extraintestinal pathogenic E. coli: virulence gene profiles and antimicrobial resistance patterns. Microorganisms. 2021;9:1234."},{"key":"ref26","unstructured":"27.\tMaj\u00f3 Masferrer N, Dolz Pascual R. Atlas of Avian Necropsy: Macroscopic Diagnosis Sampling (Updated Edition). 2019."},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"28.\tEl Ftouhy FZ, Nassik S, Nacer S, Kadiri A, Charrat N, Attrassi K, Hmyene A. Bacteriological quality of table eggs in Moroccan formal and informal sector. Int J Food Sci. 2022;2022:6223404.","DOI":"10.1155\/2022\/6223404"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"29.\tNolan L, Barnes H, Vaillancourt J, Abdul-Aziz T, Logue CM. Colibacillosis. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE, eds. Diseases of Poultry. 14th ed. Ames, IA: Wiley-Blackwell; 2013. p. 751\u2013805.","DOI":"10.1002\/9781119421481.ch18"},{"key":"ref29","unstructured":"30.\tWHO Surveillance. Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization; 2003. Available from: https:\/\/iris.who.int\/handle\/10665\/42789."},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"31.\tMagiorakos AP, Srinivasan A, Carey RB. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268\u2013281.","DOI":"10.1111\/j.1469-0691.2011.03570.x"},{"key":"ref31","unstructured":"32.\tEwers C, Janssen T, Kiessling S, Philipp H, Wieler L. Avian pathogenic Escherichia coli (APEC). Vet Microbiol. 2007;123(1\u20133):91\u2013118."},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"33.\tDziva F, Stevens M. Colibacillosis in poultry: pathogenesis and strategies for control. Avian Pathol. 2008;37(2):133\u2013149.","DOI":"10.1080\/03079450802216652"},{"key":"ref33","unstructured":"34.\tLiang X, Wu J, Zhang Q. Multidrug-resistant E. coli in poultry farms. Front Vet Sci. 2023;10:101234."},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"35.\tAworh M, Kwaga J, Okeke I. Emergence of extensively drug-resistant E. coli in Nigerian poultry. Antimicrob Resist Infect Control. 2021;10:145.","DOI":"10.1186\/s13756-021-00930-x"},{"key":"ref35","unstructured":"36.\tBeatrice S, Marco P, Elisa R. Virulence genes and multidrug resistance in avian E. coli. Vet Microbiol. 2025;285:110615."},{"key":"ref36","unstructured":"37.\tRafiq S, Khan A, Javed H. Antibiotic resistance and virulence profiling in poultry E. coli. Int J Vet Sci. 2024;15(3):112\u2013123."},{"key":"ref37","unstructured":"38.\tShobrak M, Hassan S, Sti\u00e9venart C, El-Deeb B, Gherbawy Y. Prevalence and antibiotic resistance profile of intestinal bacteria isolated from captive adult Houbara bustards (Chlamydotis macqueenii) exposed to natural weather conditions in Saudi Arabia. Glob Veterinaria. 2013;10(3):276\u2013284."},{"key":"ref38","unstructured":"39.\tHuff W, Rath N, Balog J. Environmental stressors and colibacillosis in poultry. Poult Sci. 2015;94(10):2319\u20132329."},{"key":"ref39","unstructured":"40.\tEl-Gazzar M, Kang S. Stress and immune function in captive birds. J Avian Med Surg. 2024;38(2):145\u2013156."},{"key":"ref40","unstructured":"41.\tGedeno J, Otiang E, Makau D. Risk factors for E. coli infections in juvenile poultry. Vet Rec. 2022;191(5):205\u2013212."},{"key":"ref41","doi-asserted-by":"crossref","unstructured":"42.\tJoseph J, Jennings M, Barbieri N, Zhang L, Adhikari P, Ramachandran R. Characterization of avian pathogenic Escherichia coli isolated from broiler breeders with colibacillosis in Mississippi. Poultry. 2023;2(1):24\u201339.","DOI":"10.3390\/poultry2010004"},{"key":"ref42","doi-asserted-by":"crossref","unstructured":"43.\tShterzer N, Rothschild N, Sbehat Y, Dayan J, Eytan D, Uni Z, et al. Vertical transmission of gut bacteria in commercial chickens is limited. Anim Microbiome. 2023;5:27.","DOI":"10.1186\/s42523-023-00272-6"},{"key":"ref43","doi-asserted-by":"crossref","unstructured":"44.\tRisalvato J, Sewid A, Eda S, Gerhold R, Wu J. Strategic detection of Escherichia coli in the poultry industry: food safety challenges, One Health approaches, and advances in biosensor technologies. Biosensors. 2025;15:419.","DOI":"10.3390\/bios15070419"},{"key":"ref44","doi-asserted-by":"crossref","unstructured":"45.\tTilli G, Rossi L, Bianchi A, Conti P. A systematic review on the role of biosecurity to prevent or control colibacillosis in broiler production. Poult Sci. 2024;103(7):103642.","DOI":"10.1016\/j.psj.2024.103955"},{"key":"ref45","doi-asserted-by":"crossref","unstructured":"46.\tLong JR, Moore SJ, Woodward MJ, et al. Longitudinal study on background lesions in broiler breeder flocks and their progeny, and genomic characterization of Escherichia coli. Vet Res. 2022;53:106.","DOI":"10.1186\/s13567-022-01064-7"},{"key":"ref46","doi-asserted-by":"crossref","unstructured":"47.\tRychlik I. Vertical transmission of gut bacteria in commercial chickens is limited. Anim Microbiome. 2023;5:35.","DOI":"10.1186\/s42523-023-00272-6"},{"key":"ref47","doi-asserted-by":"crossref","unstructured":"48.\tIbrahim G, Salah-Eldein A, Al-Zaban M, El-Oksh A, Ahmed E, Farid D, et al. Monitoring the genetic variation of some Escherichia coli strains in wild birds and cattle. Onderstepoort J Vet Res. 2023;90(1):a2085.","DOI":"10.4102\/ojvr.v90i1.2085"},{"key":"ref48","doi-asserted-by":"crossref","unstructured":"49.\tLiao M, Wu J, Li Y, Lu X, Tan H, Chen S, et al. Prevalence and persistence of ceftiofur-resistant Escherichia coli in a chicken layer breeding program. Animals. 2023;13(1):90.","DOI":"10.3390\/ani13010090"},{"key":"ref49","doi-asserted-by":"crossref","unstructured":"50.\tAhmed N, Gulhan T. Determination of antibiotic resistance patterns and genotypes of Escherichia coli isolated from wild birds. Microbiome. 2024;12(1):8.","DOI":"10.1186\/s40168-023-01729-1"},{"key":"ref50","doi-asserted-by":"crossref","unstructured":"51.\tOsman K, Kappell A, Elhadidy M, ElMougy F, Abd El-Ghany W, Orabi A, et al. Poultry hatcheries as potential reservoirs for antimicrobial-resistant Escherichia coli: a risk to public health and food safety. Sci Rep. 2018;8:5859.","DOI":"10.1038\/s41598-018-23962-7"},{"key":"ref51","doi-asserted-by":"crossref","unstructured":"52.\tHosuru Subramanya S, Bairy I, Nayak N, Padukone S, Sathian B, Gokhale S. Low rate of gut colonization by extended spectrum \u03b2-lactamase producing Enterobacteriaceae in HIV infected persons as compared to healthy individuals in Nepal. PLoS ONE. 2019;14(2):e0212042.","DOI":"10.1371\/journal.pone.0212042"},{"key":"ref52","doi-asserted-by":"crossref","unstructured":"53.\tYang Y, Ashworth A, Willett C, Cook K, Upadhyay A, Owens P, et al. Review of antibiotic resistance, ecology, dissemination, and mitigation in U. S. broiler poultry systems. Front Microbiol. 2019;10:2.","DOI":"10.3389\/fmicb.2019.02639"},{"key":"ref53","doi-asserted-by":"crossref","unstructured":"54.\tRousham E, Unicomb L, Islam M. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and One Health approaches. Proc R Soc B Biol Sci. 2018;285(1876):2018033.","DOI":"10.1098\/rspb.2018.0332"},{"key":"ref54","doi-asserted-by":"crossref","unstructured":"55.\tFalgenhauer L, Imirzalioglu C, Oppong K, Akenten C, Hogan B, Krumkamp R, et al. Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Front Microbiol. 2019;9:3358.","DOI":"10.3389\/fmicb.2018.03358"},{"key":"ref55","unstructured":"56.\tBorzi M, Sordi M, Barbieri R. Synergistic action of virulence factors in avian E. coli. Vet Microbiol. 2018;220:1\u20139."},{"key":"ref56","doi-asserted-by":"crossref","unstructured":"57.\tAmer M, Mekky H, Amer A, Fedawy H. Antimicrobial resistance genes in pathogenic Escherichia coli isolated from diseased broiler chickens in Egypt and their relationship with the phenotypic resistance characteristics. Vet World. 2018;11(8).","DOI":"10.14202\/vetworld.2018.1082-1088"},{"key":"ref57","doi-asserted-by":"crossref","unstructured":"58.\tWang J, Tang P, Tan D, Wang L, Zhang S, Qiu Y, et al. The pathogenicity of chicken pathogenic Escherichia coli is associated with the numbers and combination patterns of virulence associated genes. Open J Vet Med. 2015;5(12).","DOI":"10.4236\/ojvm.2015.512033"},{"key":"ref58","doi-asserted-by":"crossref","unstructured":"59.\tSadek D, Rady M, Fedawy H, Rabie N. Molecular epidemiology and sequencing of avian pathogenic Escherichia coli (APEC) in Egypt. Adv Anim Vet Sci. 2020;8(5):499\u2013505.","DOI":"10.17582\/journal.aavs\/2020\/8.5.499.505"},{"key":"ref59","doi-asserted-by":"crossref","unstructured":"60.\tCollingwood C, Kemmett K, Williams N, Wigley P. Is the concept of avian pathogenic Escherichia coli as a single pathotype fundamentally flawed? Front Vet Sci. 2014;1:5.","DOI":"10.3389\/fvets.2014.00005"},{"key":"ref60","doi-asserted-by":"crossref","unstructured":"61.\tHeidemann Olsen R, Th\u00f8fner I, Pors S, Pires dos Santos T, Christensen J. Experimental induced avian Escherichia coli salpingitis: significant impact of strain and host factors on the clinical and pathological outcome. Vet Microbiol. 2016;188:59\u201366.","DOI":"10.1016\/j.vetmic.2016.04.011"}],"container-title":["Veterinary World"],"original-title":[],"link":[{"URL":"https:\/\/veterinaryworld.org\/Vol.19\/February-2026\/15.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T15:11:39Z","timestamp":1772032299000},"score":1,"resource":{"primary":{"URL":"https:\/\/veterinaryworld.org\/Vol.19\/February-2026\/15.php"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,23]]},"references-count":61,"URL":"https:\/\/doi.org\/10.14202\/vetworld.2026.654-666","relation":{},"ISSN":["0972-8988","2231-0916"],"issn-type":[{"value":"0972-8988","type":"print"},{"value":"2231-0916","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,23]]},"article-number":"15"}}