Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: Comparison between 1993 and 2006

International Journal of Food Microbiology

Volumn 153, Issue 3, 2012, Pages 281-287

  Álvarez Fernández, Elena ^a   Alonso Calleja, Carlos ^a   García Fernández, Camino ^a   Capita, Rosa ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Antimicrobial resistance; Poultry; Prevalence; Salmonella enterica; Spain

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; CEFALOTIN; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; ENROFLOXACIN; ERYTHROMYCIN; FURAZOLIDONE; GENTAMICIN; NALIDIXIC ACID; NEOMYCIN; RIFAMPICIN; STREPTOMYCIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATION; NONHUMAN; POULTRY; SALMONELLA; SALMONELLA ENTERITIDIS; SALMONELLA INFANTIS; SALMONELLA NEWPORT; SALMONELLA POONA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SPAIN;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGE TYPING; CHICKENS; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; EUROPEAN UNION; FOOD CONTAMINATION; FOOD MICROBIOLOGY; HUMANS; MEAT; POULTRY DISEASES; PREVALENCE; PUBLIC HEALTH; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA FOOD POISONING; SALMONELLA INFECTIONS, ANIMAL; SEROTYPING; SPAIN;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR INFANTIS; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR NEWPORT; SALMONELLA ENTERITIDIS; SALMONELLA POONA; SALMONELLA TYPHIMURIUM;

EID: 84855980808     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.11.011     Document Type: Article

References (63)

1. Abdellah C., Fouzia R.F., Abdelkader C., Rachida S.B., Mouloud Z. Prevalence and anti-microbial susceptibility of Salmonella isolates from chicken carcasses and giblets in Meknès, Morocco. African Journal of Microbiology Research 2009, 3:215-219.
2. Anaraki S., Giraudon I., Cathcart S. Large outbreak of Salmonella Enteritidis in northeast London. Eurosurveillance 2005, 10. article 2. Available at:, Date last accessed: May 2, 2011. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2664.
3. Anonymous Council Directive 93/43/EEC of 14 June 1993 on the hygiene of foodstuffs. Official Journal of the European Union 1993, 175:1-11.
4. Antunes P., Reu C., Sousa J.C., Peixe L., Pestana N. Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. International Journal of Food Microbiology 2003, 82:97-103.
5. Arsenault J., Letellier A., Quessy S., Boulianne M. Prevalence and risk factors for Salmonella and Campylobacter spp. carcass contamination in broiler chickens slaughtered in Quebec. Journal of Food Protection 2007, 70:1820-1828.
6. Arslan S., Eyi A. Occurrence and antimicrobial resistance profiles of Salmonella species in retail meat products. Journal of Food Protection 2010, 73:1613-1617.
7. Barton M.D. Antibiotic use in animal feed and its impact on human health. Nutrition Research 2000, 13:279-299.
8. Berrang M.E., Bailey J.C., Altekruse S.F., Shaw W.K., Patel B.L., Mainersmann R.J., Fedorka-Cray P.J. Prevalence, serotype, and antimicrobial resistance of Salmonella on broiler carcasses postpick and postchill in 20 U.S. processing plants. Journal of Food Protection 2009, 72:1610-1615.
9. Capita, R., Alonso-Calleja, C., in press. Antibiotic-resistant bacteria: a challenge for the food industry. Critical Reviews in Food Science and Nutrition. doi:10.1080/10408398.2010.519837.
10. 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.
11. Cardinale E., Perrier Grosclaude J.D., Tall F., Cissé M., Guèye E.F., Salvat G. Prevalence of Salmonella and Campylobacter in retail chicken carcasses in Senegal. Revue d'Élevage et de Médecine Vétérinaire des Pays Tropicaux 2005, 56:13-16.
12. Carramiñana J.J., Rota C., Agustín I., Herrera A. High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Veterinary Microbiology 2004, 104:133-139.
13. CDC Preliminary FoodNet Data on the incidence of infection with pathogens transmitted commonly through food - 10 states, 2008 Available on:, Date last accessed: May 4, 2011. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5813a2.htm?s_cid=mm5813a2_e.
14. Cetinkaya F., Cibik R., Soyutemiz G.E., Ozakin C., Kayali R., Levent B. Shigella and Salmonella contamination in various foodstuffs in Turkey. Food Control 2008, 19:1059-1063.
15. Chung Y.-H., Know Y.-I., Kim S.-Y., Kim S.-H., Lee B.-K., Chang Y.-H. Antimicrobial susceptibilities and epidemiological analysis of Salmonella Enteritidis isolates in Korea by phage typing and pulsed-field gel electrophoresis. Journal of Food Protection 2004, 67:264-270.
16. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Test for Bacteria Isolated From Animals. Approved Standard M31-A2 2002, National Committee for Clinical Laboratory Standards, Pennsylvania.
17. Cook A., Reid-Smith R., Irwin R., McEwen S.A., Valdivieso-García A., Ribble C. Antimicrobial resistance in Campylobacter, Salmonella, and Escherichia coli isolated from retail turkey meat from Southern Ontario, Canadá. Journal of Food Protection 2009, 72:473-481.
18. Dallal M.M.S., Doyle M.P., Rezadehbashi M., Dabiri H., Sanaei M., Modarresi S., Bakhtiari R., Sharifiy K., Taremi M., Zali M.R., Sharifi-Yazdi M.K. Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp. isolated from retail chicken and beef, Tehran, Iran. Food Control 2010, 21:388-392.
19. Dias de Oliveira S., Siqueira Flores F., Ruschel dos Santos L., Brandelli A. Antimicrobial resistance in Salmonella enteritidis strains isolated from broiler carcasses, food, human and poultry-related samples. International Journal of Food Microbiology 2005, 97:297-305.
20. Dione M.M., Ieven M., Garin B., Marcotty T., Geerts S. Prevalence and antimicrobial resistance of Salmonella isolates from broiler farms, chicken carcasses, and street-vended restaurants in Casamance, Senegal. Journal of Food Protection 2009, 72:2423-2427.
21. Dogru A.K., Ayaz N.D., Gencay Y.E. Serotype identification and antimicrobial resistance profiles of Salmonella spp. isolated from chicken carcasses. Tropical Animal Health and Production 2010, 42:893-897.
22. Echeita A., Aladueña A., González-Sanz R., Díez R., De la Fuente M., Cerdán F., Arrollo M., Gutiérrez R. Análisis de las cepas de Salmonella spp. aisladas de muestras clínicas de origen humano en España. Años 2002 y 2003 (I). Boletín Epidemiológico Semanal 2005, 13:73-76.
23. Echeita A., Aladueña A., González-Sanz R., Díez R., De la Fuente M., Cerdán F., Arrollo M., Gutiérrez R. Análisis de las cepas de Salmonella spp. aisladas de muestras clínicas de origen humano en España. Años 2002 y 2003 (II). Boletín Epidemiológico Semanal 2005, 13:85-88.
24. EFSA The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2008. EFSA Journal 2010, 8:1658-1918. Available at:, Date last accessed: May 4, 2011. http://www.efsa.europa.eu/en/scdocs/doc/1658.pdf.
25. EFSA The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2009. EFSA Journal 2011, 9(3):2090-2477. Available at:, Date last accessed: May 4, 2011. http://www.efsa.europa.eu/en/efsajournal/doc/2090.pdf.
26. Ellerbroek L., Narapati D., Phu Tai N., Poosaran N., Pinthong R., Sirimalaisuwan A., Tshering P., Fries R., Zessin K.-H., Baumann M., Schroeter A. Antibiotic resistance in Salmonella isolates from imported chicken carcasses in Bhutan and from pig carcasses in Vietnam. Journal of Food Protection 2010, 73:376-379.
27. European Commission The Rapid Alert System for Food and Feed (RASFF). Annual Report 2009 2010, EU Directorate General for Health and Consumers, Luxemburg, Available at:, Date last accessed: May 4, 2011. http://ec.europa.eu/food/food/rapidalert/report2009_en.pdf.
28. Foley S.L., Lynne A.M., Nayak R. Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. Journal of Animal Science 2008, 86(E. Suppl.):E149-E162.
29. Galanis E., Lo Fo Wong D., Patrick M.E., Binsztein N., Cieslik A., Chalermachaikit T., Aidara-Kane A., Ellis A., Angulo F.J., Wegener H.C. Web-based surveillance and global Salmonella distribution, 2000-2002. Emerging Infectious Diseases 2006, 12:381-388.
30. Gillespie I.A., O'Brien S.J., Adak G.K., Ward L.R., Smith H.R. Foodborne general outbreaks of Salmonella Enteritidis phage type 4 infection, England and Wales, 1992-2002: where are the risks?. Epidemiology and Infection 2005, 133:795-801.
31. Hernández T., Sierra A., Rodríguez-Álvarez C., Torres A., Arevalo M.P., Calvo M., Arias A. Salmonella enterica serotypes isolated from imported frozen chicken meat in the Canary Islands. Journal of Food Protection 2005, 68:2702-2706.
32. Hue O., Le Bouquin S., Lalande F., Allain V., Rouxel S., Petetin I., Quesne S., Laisney M.-J., Gloaguen P.-Y., Picherot M., Salvat G., Bougeard S., Chemaly M. Prevalence of Salmonella spp. on broiler chicken carcasses and risk factors at the slaughterhouse in France in 2008. Food Control 2011, 22:1158-1164.
33. Hur J., Kim J.H., Park J.H., Lee Y.-J., Lee J.H. Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. The Veterinary Journal 2010, 189:306-311.
34. Johnsen P.J., Townsend J.P., Bohn T., Simonsen G.S., Sundsfjord A., Nielsen K.M. Retrospective evidence for a biological cost of vancomycin resistance determinants in the absence of glycopeptide selective pressures. Journal of Antimicrobial Chemotherapy 2011, 66:608-610.
35. Jones Y.E., Chappell S., McLaren I.M., Davies R.H., Wray C. Antimicrobial resistance in Salmonella isolated from animals and their environment in England and Wales from 1988 to 1999. Veterinary Record 2002, 150:649-654.
36. Lestari S.I., Han F., Wang F., Ge B. Prevalence and antimicrobial resistance of Salmonella serovars in conventional and organic chickens from Louisiana retail stores. Journal of Food Protection 2009, 72:1165-1172.
37. Logue C.M., Sherwood J.S., Olah P.A., Elijah L.M., Dockter M.R. The incidence of antmicrobial-resistant Salmonella spp. on freshly processed poultry from US Midwestern processing plants. Journal of Applied Microbiology 2003, 94:16-24.
38. Martínez E.V., Varela M.C., Cevallos C., Hernández-Pezzi G., Torres A., Ordóñez P. Brotes de enfermedades transmitidas por alimentos. España, 2004-2007 (excluye brotes hídricos). Boletín Epidemiológico Semanal 2008, 16:241-252.
39. Miranda J.M., Mondragón A.C., Martínez B., Guarddon M., Rodríguez J.A. Prevalence and antimicrobial resistance patterns of Salmonella from different raw foods in Mexico. Journal of Food Protection 2009, 72:966-971.
40. Nastasi A., Mammina C., Cannova L. Antimicrobial resistance in Salmonella enteritidis, southern Italy, 1990-1998. Emerging Infectious Diseases 2000, 6:401-403.
41. NCCLS Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved Standard M2-A7 2000, National Committee for Clinical Laboratory Standards, Pennsylvania.
42. Pan Z.M., Geng S.Z., Ahou Y.Q., Liu Z.Y., Fang Q., Liu B.B., Jiao X.A. Prevalence and antimicrobial resistance of Salmonella sp. isolated from domestic animals in eastern China. Journal of Animal and Veterinary Advances 2010, 9:2290-2294.
43. Parveen S., Taabodi M., Schwarz J.G., Oscar T.P., Harter-Dennis J., White D.G. Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. Journal of Food Protection 2007, 70:2466-2472.
44. Rabsch W., Hargis B.M., Tsolis R.M., Kingsley R.A., Hinz K.-H., Tschäpe H., Bäumler A.J. Competitive exclusion of Salmonella Enteritidis by Salmonella Gallinarum in poultry. Emerging Infectious Diseases 2000, 6:443-448.
45. Rodrigo S., Adesiyun A., Asgarali Z., Swanston W. Occurrence of selected foodborne pathogens on poultry and poultry giblets from small retail processing operations in Trinidad. Journal of Food Protection 2006, 68:1096-1105.
46. Sáenz Y., Zarazaga 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.
47. Sarwari A.R., Magder L.S., Levine P., McNamara A.M., Knower S., Armstrong G.L., Etzel R., Hollingsworth J., Morris J.G. Serotype distribution of Salmonella isolates from food animals after slaughter differs from that of isolates found in humans. Journal of Infectious Diseases 2001, 183:1295-1299.
48. Schroeter A., Hoog B., Helmuth R. Resistance of Salmonella isolates in Germany. Journal of Veterinary Medicine 2004, 51:389-392.
49. Shrestha A., Regmi P., Dutta R.K., Khanal D.R., Aryal S.R., Thakur R.P., Karki D., Singh U.M. First report on antimicrobial resistance of Salmonella isolated from poultry in Nepal. Veterinary Microbiology 2010, 144:522-524.
50. Sommer M.O.A., Dantas G. Antibiotics and the resistant microbiome. Current Opinion in Microbiology 2011, 14:556-563.
51. Su L.H., Chiu C.H., Chu C., Ou J.T. Antimicrobial resistance in nontyphoidal Salmonella serotypes: a global challenge. Clinical Infectious Diseases 2004, 39:546-551.
52. Suresh T., Hatha A.A.M., Harsha H.T., Lakshmanaperumalsamy P. Prevalence and distribution of Salmonella serotypes in marketed broiler chickens and processing environment in Coimbatore city of southern India. Food Research Internacional 2011, 44:823-825.
53. Usera M.A., Aladueña A., González R., De la Fuente M., García-Peña J., Frías N., Echeita M.A. Antibiotic resistance of Salmonella spp. from animal sources in Spain in 1996 and 2000. Journal of Food Protection 2002, 65:768-773.
54. Valdezate S., Arroyo M., González-Sanz R., Ramiro R., Herrera-León S., Usera M.A., De la Fuente M., Echeita A. Antimicrobial resistance and phage and molecular typing of Salmonella strains isolated from food human consumption in Spain. Journal of Food Protection 2007, 70:2741-2748.
55. van Duijkeren E., Wannet W.J.B., Houwers D.J., van Pelt W. Antimicrobial susceptibilities of Salmonella strains isolated from humans, cattle, pigs, and chickens in The Netherlands from 1984 to 2001. Journal of Clinical Microbiology 2003, 41:3574-3578.
56. van Nierop W., Duse A.G., Marais E., Aithma N., Thothobolo N., Kassel M., Stewart R., Potgieter A., Fernandes B., Galpin J.S., Bloomfield S.F. Contamination of chicken carcasses in Gauteng, South Africa, by Salmonella, Listeria monocytogenes and Campylobacter. International Journal of Food Microbiology 2005, 99:1-6.
57. Velasco L., Sobrino L., García M., Soler P., Martínez L. Infecciones por Salmonella no tifoidea de origin humano en España. Sistema de Información Microbiológica. Años 2000-2008. Boletín Epidemiológico Semanal 2009, 17:193-204.
58. Waldroup A.L. Contamination of raw poultry with pathogens. Worlds Poultry Science Journal 1996, 52:7-25. 84, 87, 90, 93.
59. Wilson I.G. Antimicrobial resistance of Salmonella in raw retail chickens, imported chicken portions, and human clinical specimens. Journal of Food Protection 2004, 67:1220-1225.
60. Yang S.J., Park K.Y., Kim S.H., No K.M., Besser T.E., Yoo H.S., Lee B.K., Park Y.H. Antimicrobial resistance in Salmonella enterica serovars Enteritidis and Typhimurium isolated from animals in Korea: comparison of phenotypic and genotypic resistance characterization. Veterinary Microbiology 2002, 86:295-301.
61. Yang B., Qu D., Zhang X., Shen J., Cui S., Shi Y., Xi M., Sheng M., Zhi S., Meng J. Prevalence and characterization of Salmonella serovars in retail metas of marketplace in Shaanxi, China. International Journal of Food Microbiology 2010, 141:63-72.
62. Yildirim Y., Gonulalan Z., Pamuk S., Ertas N. Incidence and antibiotic resistance of Salmonella spp. on raw chicken carcasses. Food Research International 2011, 44:725-728.
63. Zhao S., Fedorka-Cray P.J., Friedman S., McDermott P.F., Walker R.D., Qaiyumi S., Foley S.L., Hubert S.K., Ayers S., English L., Dargatz D.A., Salamone B., White D.G. Characterization of Salmonella Typhimurium of animal origin obtained from the national antimicrobial resistance monitoring system. Foodborne Pathogens and Disease 2005, 2:169-181.