Antimicrobial resistance in E. coli isolates from conventionally and organically reared poultry: A comparison of agar disc diffusion and Sensi Test Gram-negative methods

Food Control

Volumn 30, Issue 1, 2013, Pages 227-234

  Álvarez Fernández, Elena ^a   Cancelo, Amaya ^a   Díaz Vega, Carmen ^a   Capita, Rosa ^a   Alonso Calleja, Carlos ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Antimicrobial resistance; Conventional poultry; Escherichia coli; Microbiological quality; Organic poultry

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PHASIANIDAE;

EID: 84866661594     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2012.06.005     Document Type: Article

References (39)

1. álvarez-Astorga M., Capita R., Alonso-Calleja C., Moreno B., García-Fernández C. Microbiological quality of retail chicken by-products in Spain. Meat Science 2002, 62:45-50.
2. Apajalahti J., Kettunen A., Graham H. Characteristics of the gastrointestinal microbial communities, with special reference to chicken. World's Poultry Science Journal 2004, 60:223-232.
3. Bülte M., Reuter G. Results of a collaborative study using the fluorogenic MUG (4-methylumbelliferyl-β-D-glucuronide) assay for detection of Escherichia coli in meat and meat products. Archiv Fur Lebensmittelhygiene 1989, 40:121-144.
4. Capita, R., & Alonso-Calleja, C. Antibiotic-resistant bacteria: a challenge for the food industry. Critical Reviews in Food Science and Nutrition. doi:10.1080/10408398.2010.519837.
5. Capita R., Alonso-Calleja C., García-Arias M.T., Moreno B., García-Fernández M.C. Methods to detect the occurrence of various indicator bacteria on the surface of retail poultry in Spain. Journal of Food Science 2002, 67(2):765-771.
6. Capita R., Alonso-Calleja C., Moreno B., García-Fernández M.C. Occurrence of Listeria species in retail poultry meat and evaluation of a cultural immunoassay for their detection. International Journal of Food Microbiology 2001, 65(1/2):75-82.
7. Capita R., Alonso-Calleja C., Prieto M. Prevalence of Salmonella enterica serovars and genovars from chicken carcasses from slaughterhouses in Spain. Journal of Applied Microbiology 2007, 103:1366-1375.
8. Cardinale E., Perrier Gros-Claude J.D., Tall F., Cissé M., Guèye E.F., Salvat G. Prevalence of Salmonella and Campylobacter in retail chicken carcasses in Senegal. Revue d'Elevage et de Medecine Veterinaire des Pays Tropicaux 2005, 56:13-16.
9. CLSI Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolated from animals. Approved standard M31-A3 2008, National Committee for Clinical Laboratory Standards, Pennsylvania.
10. Colmegna S., Invernizzi A., Mascher A.L., Corsale E., Ferrazzi V., Grilli G. Microbiological characteristics of poultry meats-results of inspections carried out in the province of Milano, Italy. Italian Journal of Animal Science 2009, 8:765-770.
11. Cui S., Ge B., Zheng J., Jianghong M. Prevalence and antimicrobial resistance of Campylobacter spp. and Salmonella serovars in organic chickens in Maryland retail stores. Applied and Environmental Microbiology 2005, 71:4108-4111.
12. El-Dengawy R.A., Nassar A.M. Investigation on the nutritive value and microbiological quality of wild carcasses. Food/Nahrung 2001, 45(1):50-54.
13. FAO Faostat: Food balance sheets 2011, Internet site, Accessed 20.12.11. http://faostat.fao.org/site/368/DesktopDefault.aspx%3fPageID%3d368#ancor.
14. Fliss I., Simard R.E., Ettriki A. Microbiological quality of different fresh meat species in tunisian slaughterhouses and markets. Journal of Food Protection 1991, 54:773-777.
15. Guevara-Franco J.A., Alonso-Calleja C., Capita R. Aminopeptidase activity by spoilage bacteria and its relationship to microbial load and sensory attributes of poultry legs during aerobic cold storage. Journal of Food Protection 2010, 73(2):322-326.
16. Izat A.L., Colberg M., Driggers C.D., Thomas R.A. Effects of sampling method and feed withdrawal period on recovery of microorganisms from poultry carcasses. Journal of Food Protection 1989, 52:480-483.
17. Jasson V., Sampers I., Botteldoorn N., López-Gálvez F., Baert L., Denayer S., et al. Characterization of Escherichia coli from raw poultry in Belgium and impact on the detection of Campylobacer jejuni using Bolton broth. International Journal of Food Microbiology 2009, 135:248-253.
18. Landis J.R., Koch G.G. The measurement of observer agreement for categorical data. Biometrics 1977, 33(1):159-174.
19. Lei T., Tian W., He L., Huang X.-H., Sun Y.-X., Deng Y.-T., et al. Antimicrobial resistance in Escherichia coli isolates from food animals, animal food products and companion animals in China. Veterinary Microbiology 2010, 146:85-89.
20. Luangtongkum T., Morishita T.Y., Ison A.J., Huang S., McDermott P.F., Zhang Q. Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp. in poultry. Applied and Environmental Microbiology 2006, 72(5):3600-3607.
21. Luber P., Bartelt E., Genschow E., Wagner J., Hahn H. Comparison of broth microdilution, E test, and agar dilution methods for antibiotic susceptibility testing of Campylobacter jejuni and Campylobacter coli. Journal of Clinical Microbiology 2003, 41(3):1062-1108.
22. Martins da Costa P., Oliveira M., Ramos B., Bernardo F. The impact of antimicrobial use in broiler chickens on growth performance and on the occurrence of antimicrobial-resistant Escherichia coli. Livestock Science 2011, 136:262-269.
23. Mead G.C., Hudson W.R., Hinton M.H. Microbiological survey of five poultry processing plants in the UK. British Poultry Science 1993, 34:497-503.
24. Miranda J.M., Guarddon M., Vázquez B.I., Gente C.A., Barros-velázquez J., Cepeda A., et al. Antimicrobial resistance in Enterobacteriaceae strains isolated from organic chicken, conventional chicken and conventional turkey meat: a comparative study. Food Control 2008, 19:412-416.
25. Nie C., Zepeda L. Lifestyle segmentation of US food shoppers to examine organic and local food consumption. Appetite 2011, 57(1):28-37.
26. Oteo J., Campos J., Baquero F., Spanish members of the European Antimicrobial Resistance Surveillance System (EARSS) Antibiotic resistance in 1962 invasive isolates of Escherichia coli in 27 Spanish hospitals participating in the European antimicrobial resistance surveillance system (2001). Journal of Antimicrobial Chemotherapy 2002, 50:945-952.
27. Oteo J., Lázaro E., de Abajo F.J., Baquero F., Campos J., Spanish members of EARSS Antimicrobial-resistant invasive Escherichia coli, Spain. Emerging Infectious Diseases 2005, 11(4):546-553.
28. Pascual-Anderson M.R. Aves y caza. Microbiología alimentaria: metodología analítica para alimentos y bebidas 1992, Díaz de Santos, Madrid, 163-170.
29. Sáenz Y., Zaragoza M., Briñas L., lantero M., Ruiz-Larrea F., Torres C. Antibiotic resistance in Escherichia coli isolates obtained from animals, foods and humans in Spain. International Journal of Antimicrobial Agents 2001, 18:353-358.
30. SCENIHR Assessment of the antibiotic resistance effects of biocides 2009, Scientific Committee On Emerging and Newly Identified Health Risks, 19 January 2009. Available at, Accessed 24.05.12. http://ec.europa.eu/health/ph_risk/committees/04_scenihr/docs/scenihr_o_021.pdf.
31. Schroeder C.M., White D.G., Ge B., Zhang Y., McDermott P.F., Ayers S., et al. Isolation of antimicrobial-resistant Escherichia coli from retail meats purchased in Greater Washington, DC, USA. International Journal of Food Microbiology 2003, 85:197-202.
32. Schroeder C.M., White D.G., Meng J. Retail meat and poultry as a reservoir of antimicrobial-resistant Escherichia coli. Food Microbiology 2004, 21:249-255.
33. Sjölund M., Bengtsson S., Bonnedahl J., Hernandez J., Olsen B., Kahlmeter G. Antimicrobial susceptibility in Escherichia coli of human and avian origin-a comparison of wild-type distributions. Clinical Microbiology and Infection 2009, 15:461-465.
34. Smith J.L., Drum D.J.V., Dai Y., Kim J.M., Sánchez S., Maurer J.J., et al. Impact of antimicrobial usage on antimicrobial resistance in commensal Escherichia coli strains colonizing broiler chickens. Applied and Environmental Microbiology 2007, 73(5):1404-1414.
35. Song L., Ning Y.-B., Zhang X.-Y., Sheng Q.-C., Zhang G.-C., Lin S.-M., et al. Comparative research on serogroups distribution and antimicrobial resistance of Escherichia coli isolates from poultry in different areas of China. Agricultural Sciences in China 2008, 7(3):381-386.
36. Soonthornchaikul N., Garelick H., Jones H., Jacobs J., Ball D., Choudhury M. Resistance to three antimicrobial agents of Campylobacter isolated for organically- and intensively-reared chickens purchased from retail outlets. International Journal of Antimicrobial Agents 2006, 27:125-130.
37. Soufi L., Sáenz Y., Vinué L., Abbasi M.S., Ruiz E., Zaragaza M., et al. Escherichia coli of poultry food origin as reservoir of sulphonamide resistance genes and integrons. International Journal of Food Microbiology 2011, 144:497-502.
38. Van T.T.H., Chin J., Chapman T., Tran L.T., Coloe P.J. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. International Journal of Food Microbiology 2008, 124:217-223.
39. Vorster S.M., Greebe R.P., Nortjé G.L. Incidence of Staphylococcus aureus and Escherichia coli in ground beef, broilers and processed meats in Pretoria, South Africa. Journal of Food Protection 1994, 57:305.