Poultry hatcheries as potential reservoirs for antimicrobial-resistant Escherichia coli: A risk to public health and food safety

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Osman, Kamelia M ^a   Kappell, Anthony D ^b   Elhadidy, Mohamed ^c,d   Elmougy, Fatma ^e   El Ghany, Wafaa A Abd ^a   Orabi, Ahmed ^a   Mubarak, Aymen S ^f   Dawoud, Turki M ^f   Hemeg, Hassan A ^g   Moussa, Ihab M I ^f   Hessain, Ashgan M ^h   Yousef, Hend M Y ^a  

^a Cairo University   (Egypt)

^b Marquette University   (United States)

^c Mansoura University   (Egypt)

^d Zewail City of Science and Technology   (Egypt)

^e CAIRO UNIVERSITY   (Egypt)

^f KING SAUD UNIVERSITY   (Saudi Arabia)

^g TAIBAH UNIVERSITY   (Saudi Arabia)

^h KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BETA LACTAMASE; ESCHERICHIA COLI PROTEIN;

ANIMAL; ANIMAL HUSBANDRY; BETA-LACTAM RESISTANCE; BIOFILM; BIRD DISEASE; CHICKEN; DISEASE CARRIER; DRUG EFFECT; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; FOOD CONTAMINATION; FOOD CONTROL; FOOD SAFETY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; PHYSIOLOGY; PROCEDURES; SEROTYPING; VETERINARY MEDICINE;

ANIMAL HUSBANDRY; ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; BIOFILMS; CHICKENS; DISEASE RESERVOIRS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FOOD CONTAMINATION; FOOD MICROBIOLOGY; FOOD SAFETY; HUMANS; MICROBIAL SENSITIVITY TESTS; POULTRY DISEASES; SEROTYPING;

EID: 85045388489     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-23962-7     Document Type: Article

References (63)

1. Wideman, R. F. Bacterial chondronecrosis with osteomyelitis and lameness in broilers: a review. Poult Sci 95, 325-44 (2016).
2. de Lange, G. Preventing cross-contamination in the hatchery Pas Reform The future of hatchery technologies at your finger tips. Pas Reform Hatchery Technologies, Bovendorpsstraat 117038 CH P.O. Box 27038 ZG Zeddam The Netherlands (Last accessed 17/9/2016).
3. FDA. The U.S. Food and Drug Administration Center for Food Safety and Applied Nutrition. Foodborne Illness-Causing Organisms in the U.S.: What You Need to Know (Page Last Updated: 01/07/2016).
4. AMR Control. Published in Official Association with the World. Alliance against Antibiotic Resistance (WAAAR), Global Health Dynamics 20 Quayside, Woodbridge, Suffolk IP12 1BH, UK, www.globalhealthdynamics.co.uk (2015).
5. Reich, F., Atanassova, V. & Klein, G. Extended-Spectrum ß-Lactamase-and AmpC-Producing Enterobacteria in Healthy Broiler Chickens, Germany. Emerg Infect Dis 19, 1253-9, https://doi.org/10.3201/eid1908.120879 (2013).
6. Paterson, D. L. & Bonomo, R. A. Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 18, 657-86, https://doi.org/10.1128/CMR.18.4.657-686.2005 (2005).
7. Souli, M., Galani, I. & Giamarellou, H. Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe. Euro Surveill 13(47), pii=19045, Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19045 (2008).
8. Boulianne, M. et al. Drug use and antimicrobial resistance among Escherichia coli and Enterococcus spp. isolates from chicken and turkey flocks slaughtered in Quebec, Canada. Can J Vet Res 80, 49-59 (2016).
9. Myint, M. S. Epidemiology of Salmonella contamination of poultry meat products: knowledge gaps in the farm to store products. Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy, USA (2004).
10. ECDPC. European Centre for Disease Prevention and Control. Antimicrobial resistance surveillance in Europe. Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm: The Centre (2011).
11. Burkhanova, K. H. K. Properties of E. coli strains isolated from diseased fowl. Vet Moscow 10, 66-68 (1980).
12. Al-khalaf, A. N. et al. Bacterial Contamination of Hatcheries. J Agric Vet Sci Qassim Univ 2, 67-76 (2009).
13. Nesse, L. L. et al. Potentially Pathogenic Escherichia coli Can Form a Biofilm under Conditions Relevant to the Food Production Chain. Appl Environ Microbiol 80, 2042-2049, https://doi.org/10.1128/AEM.03331-13 (2014).
14. Rodriguez-Siek, K. E., Giddings, C. W., Doetkott, C., Johnson, T. J., Fakhr, M. K. & Nolan, L. K. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 151, 2097-2110 (2005).
15. Vidotto, M. C. et al. Virulence factors of avian Escherichia coli. Avian Dis 34, 531-538 (1990).
16. Jaryal, S. C., Bareja, R. & Grover, P. S. Significance of haemolytic Escherichia coli among clinical isolates. Int J Rec Sci Res 7, 9093-9096 (2016).
17. Vaish, R., Pradeep, M. S. S., Setty, C. R. & Kandi, V. Evaluation of Virulence Factors and Antibiotic Sensitivity Pattern of Escherichia coli Isolated from Extraintestinal Infections. Cureus 8, e604, https://doi.org/10.7759/cureus.604 (2016).
18. Garcia, T. A., Ventura, C. L., Smith, M. A., Merrell, D. S. & O'Brien, A. D. Cytotoxic Necrotizing Factor 1 and Hemolysin from Uropathogenic Escherichia coli Elicit Different Host Responses in the Murine Bladder. Infect Immun 81, 99-109, https://doi.org/10.1128/IAI.00605-12 (2013).
19. Herlax, V., Henning, M., Bernasconi, A., Goni, F. & Bakas, L. The lytic mechanism of Escherichia coli α-hemolysin associated to outer membrane vesicles. Health 2, 484-492, https://doi.org/10.4236/health.2010.25072 (2010).
20. Drews, S. J. et al. Decreased prevalence of virulence factors among ciprofloxacin-resistant uropathogenic Escherichia coli isolates. J Clin Microbiol 43, 4218-4220, https://doi.org/10.1128/JCM.43.8.4218-4220.2005 (2005).
21. Shewmaker, F. et al. The functional curli amyloid is not based on in-register parallel beta-sheet structure. J Biol Chem 284, 25065-25076, https://doi.org/10.1074/jbc.M109.007054 (2009).
22. Styles, D. & Flammer, K. Preliminary Investigation⋯Congo Red Binding in Escherichia coli. AFA Watchbird 17, No 4 (1990).
23. Osman, K. M., Mustafa, A. M., Elhariri, M. & AbdElhamed, G. S. Identification of serotypes and virulence markers of Escherichia coli isolated from human stool and urine samples in Egypt. Indian J Med Microbiol 30, 308-313, https://doi.org/10.4103/0255-0857.99492 (2012).
24. Martinez-Medina, M. et al. Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol 9, 202, https://doi.org/10.1186/1471-2180-9-202 (2009).
25. Salo, J. et al. Biofilm formation by Escherichia coli isolated from patients with urinary tract infections. Clin Nephrol 71, 501-507, https://doi.org/10.5414/CNP71501 (2009).
26. Cremet, L. et al. Orthopaedic-implant infections by Escherichia coli: molecular and phenotypic analysis of the causative strains. J Infect 64, 169-175, https://doi.org/10.1016/j.jinf.2011.11.010 (2012).
27. Wang, R., Bono, J. L., Kalchayanand, N., Shackelford, S. & Harhay, D. M. Biofilm formation by Shiga toxin-producing Escherichia coli O157:H7 and non-O157 strains and their tolerance to sanitizers commonly used in the food processing environment. J Food Prot 75, 1418-1428, https://doi.org/10.4315/0362-028X.JFP-11-427 (2012).
28. Ryu, J. H. & Beuchat, L. R. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl Environ Microbiol 71, 247-254 (2005).
29. Simões, M., Simões, L. C. & Vieira, M. J. A review of current and emergent biofilm control strategies. LWT-Food Sci Technol 43, 573-583 (2010).
30. Wang, X., Demirci, A. & Puri, V. M. Biofilms in Dairy Products and Dairy Processing Equipment and Control Strategies, in Biofilms in the Food Environment. Second Edition (eds Pometto, A. L. & Demirci, A.) John Wiley & Sons, Ltd, Chichester, UK, https://doi.org/10.1002/9781118864036.ch8 (2015).
31. Landers, T. F., Cohen, B., Wittum, T. E. & Larson, E. L. A Review of Antibiotic Use in Food Animals: Perspective, Policy, and Potential. Public Health Rep 127, 4-22 (2012).
32. Collignon, P., Aarestrup, F. M., Irwin, R. & McEwen, S. Human Deaths and Third-Generation Cephalosporin use in Poultry, Europe. Emerg Infect Dis 19, 1339-1340, https://doi.org/10.3201/eid1908.120681 (2013).
33. WHO. 19th WHO Model List of EssentialMedicines (April 2015) (PDF). WHO. April 2015. Retrieved May 10, (2015).
34. Garonzik, S. M. et al. Population pharmacokinetics of colistin methanesulfonate and formed colistin in critically-ill patients from a multi-center study provide dosing suggestions for various categories of patients. Antimicrob Agents Chemother 55, 3284-3294 (2011).
35. Dierikx, C., van Essen-Zandbergen, A., Veldman, K., Smith, H. & Mevius, D. Increased detection of extended spectrum betalactamase producing Salmonella enterica and Escherichia coli isolates from poultry. Vet Microbiol 145, 273-278, https://doi.org/10.1016/j.vetmic.2010.03.019 (2010).
36. Ciccozzi, M. et al. Phylogenetic analysis of multidrug-resistant Escherichia coli clones isolated from humans and poultry. New Microbiol 36, 385-394 (2013).
37. Szmolka, A. & Nagy, B. Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol 4, 258, https://doi.org/10.3389/fmicb.2013.00258 (2013).
38. Mitchell, N. M., Johnson, J. R., Johnston, B., Curtiss, R. III & Mellata, M. Zoonotic Potential of Escherichia coli Isolates from Retail Chicken Meat Products and Eggs. Appl Environ Microbiol 81, 1177-87, https://doi.org/10.1128/AEM.03524-14 (2015).
39. Cantón, R. & Coque, T. M. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol 9, 466-475, https://doi.org/10.1016/j. mib.2006.08.011 (2006).
40. Coque, T. M., Baquero, F. & Canton, R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill 20, 13(47), pii: 19044 (2008).
41. Peter-Getzlaff, S. et al. Detection of AmpC beta-lactamase in Escherichia coli: comparison of three phenotypic confirmation assays and genetic analysis. J Clin Microbiol 49, 2924-2932, https://doi.org/10.1128/JCM.00091-11 (2011).
42. Animal and Plant Health Agency (formerly Animal Health and Veterinary), Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB (2013).
43. Feng, P., Weagant, S. D., Grant, M. A. & Burkhardt, W. Bacteriological Analytical Manual Chapter 4 Enumeration of Escherichia coli and the Coliform Bacteria, U.S. Food and Drug Administration 10903 New Hampshire Avenue Silver Spring, MD 20993 1-888-INFO-FDA (1-888-463-6332) (2015).
44. Marinho, C. M., Santos, T., Gonçalves, A., Poeta, P. & Igrejas, G. A Decade-Long Commitment to Antimicrobial Resistance Surveillance in Portugal. Front Microbiol 7, 1650, https://doi.org/10.3389/fmicb.2016.01650 (2016).
45. Niveditha, S., Pramodhini, S., Umadevi, S., Kumar, S. & Stephen, S. The Isolation and the Biofilm Formation of Uropathogens in the Patients with Catheter Associated Urinary Tract Infections (UTIs). J Clin Diagc Res: JCDR. 6, 1478-1482, https://doi.org/10.7860/JCDR/2012/4367.2537 (2012).
46. Christensen, G. D., Simpson, W. A., Bisno, A. L. & Beachey, E. H. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 37, 318-326 (1982).
47. Wakimoto, N. et al. Quantitative biofilm assay using a microtiter plate to screen for enteroaggregative Escherichia coli. Am J Trop Med Hyg 71, 687-690 (2004).
48. Maragkoudakis, P. A. et al. Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16, 189-199, https://doi.org/10.1016/j.idairyj.2005.02.009 (2009).
49. WHO. World Health Organization. Critically important antimicrobials for human medicine-5th rev. Geneva: World Health Organization; Licence: CC BY-NC-SA3.0 IGO (2017).
50. CLSI. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement CLSI document M100-S24. Wayne, PA: Clinical and Laboratory Standards Institute, (2014).
51. Heininger, A. et al. PCR and blood culture for detection of Escherichia coli bacteremia in rats. J Clin Microbiol 37, 2479-2482 (1999).
52. Pérez-Pérez, F. J. & Hanson, N. D. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40, 2153-2162, https://doi.org/10.1128/JCM.40.6.2153-2162.2002 (2002).
53. Colom, K. et al. Simple and reliable multiplex PCR assay for detection of blaTEM, blaSHV and blaOXA-1 genes in Enterobacteriaceae. FEMS Microbiol Lett 223, 147-151, https://doi.org/10.1016/S0378-1097(03)00306-9 (2003).
54. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://doi.org/http://www.R-project.org/(2017).
55. Wei, T., & Simko, V. The corrplot package. CRAN Repository. Retrieved from http://www.sthda.com/french/wiki/matrice-decorrelation-la-fonction-r-qui-fait-tout (2016).
56. Zhao, S., Guo, Y., Sheng, Q. & Shyr, Y. Heatmap3: an improved heatmap package with more powerful and convenient features. BMC Bioinformatics 15(Suppl 10), P16, https://doi.org/10.1186/1471-2105-15-S10-P16 (2014).
57. Murtagh, F. & Legendre, P. Ward's Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward's Criterion? Journal of Classification 31(3), 274-295, https://doi.org/10.1007/s00357-014-9161-z (2014).
58. Lê, S., Josse, J. & Husson, F. FactoMineR: An R Package for Multivariate Analysis. J. of Statistical Software 25(1), 1-18, https://doi.org/10.1016/j.envint.2008.06.007 (2008).
59. Kassambara, A. & Mundt, F. Factoextra: extract and visualize the results of multivariate data analyses. R Package Version, 1(3) (2016).
60. Hothorn, T., Bretz, F. & Westfall, P. "Simultaneous Inference in General Parametric Models". Biometrical Journal 50(3), 346-363, https://doi.org/10.1002/bimj.200810425 (2008).
61. Bretz, F., Hothorn, T. & Westfall, P. Multiple Comparisons Using R. Boca Raton, Florida, USA: Chapman \& Hall/CRC Press, ISBN: 978-1-58488-574-0 (2010).
62. Philippon, A., Arlet, G. & George, A. Jacoby Plasmid-determined AmpC-type β-lactamases. Antimicrobial agents and chemotherapy 46(1), 1-11 (2002).
63. Bradford, Patricia A. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clinical microbiology reviews 14(4), 933-951 (2001).