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References

  1. Ahmed AM, El-Atti NM. 2010. Existence of Listeria species in broiler carcasses with an attempt to control Listeria monocytogenes using trisodium phosphate. Afr. J. Food Sci. 4: 46-51.
  2. Ashraf MA, Sohaila F, Hassan A, Raafat H, Abdelazeem M, Khalid IE. 2010. Occurrence of Listeria species in meat, chicken products and human stools in Assiut city, Egypt with PCR use for rapid identification of Listeria monocytogenes. Veter. World 3: 353-359.
  3. Aury K, Bouquin SL, Toquin MT, Huneau-Salaun A, Le Notre Y, Allain V, et al. 2011. Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks. Prev. Vet. Med. 98: 271-278.
    Pubmed CrossRef
  4. Bauer A, Kirby W, Sherris JC, Turck M. 1996. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45: 493.
  5. Bertrand S, Huys G, Yde M, D’Haene K, Tardy F, Vrints M. 2005. Detection and characterization of tet(M) in tetracycline resistant Listeria strains from human and food processing origins in Belgium and France. J. Med. Microbiol. 54: 1151-1156.
    Pubmed CrossRef
  6. Castanon JI. 2007. History of the use of antibiotic as growth promoters in European poultry feeds. Poult. Sci. 86: 2466-2471.
    Pubmed CrossRef
  7. Chemaly M, Toquin MT, Le Nôtre Y, Fravalo P. 2008. Prevalence of Listeria monocytogenes in poultry production in France. J. Food Prot. 71: 1996-2000.
    Pubmed CrossRef
  8. Clinical and Laboratory Standards Institute (previously National Committee on Clinical Laboratory Standards). 2006. Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved Standard-Ninth Edition M2-A9. CLSI, Wayne, PA.
  9. Cocolin L, Stella S, Nappi R, Bozzetta E, Cantoni C, Comi G. 2005. Analysis of PCR-based methods for characterization of Listeria monocytogenes strains isolated from different sources. Int. J. Food Microbiol. 103: 167-178.
    Pubmed CrossRef
  10. Conter M, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri A. 2009. Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int. J. Food Microbiol. 128: 497-500.
    Pubmed CrossRef
  11. Cox NA, Bailey JS, Berrang ME. 1997. The presence of Listeria monocytogenes in the integrated poultry industry. J. Appl. Poult. Res. 6: 116-119.
    CrossRef
  12. Dijkstra RG. 1976. Listeria-encephalitis in cows through litter from a broiler-farm. Zentralbl. Bakteriol. Orig. B 161: 383-385.
    Pubmed
  13. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). 2015. The European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. 13: 3991.
    CrossRef
  14. Esteban JI, Oporto B, Aduriz G, Juste RA, Hurtado A. 2008. A survey of food-borne pathogens in free-range poultry farms. Int. J. Food Microbiol. 123: 177-182.
    Pubmed CrossRef
  15. Fallah AA, Saei-Dehkordi SS, Rahnama M, Tahmasby H, Mahzounieh M. 2012. Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control 28: 327-332.
    CrossRef
  16. Gomez D, Azon E, Marco N, Carraminana JJ, Rota C, Arino A, Yangüela J. 2014. Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol. 42: 61-65.
    Pubmed CrossRef
  17. Hof H, Nichterlein T, Kretschmar M. 1997. Management of listeriosis. Clin. Microbiol. Rev. 10: 345-357.
    Pubmed PMC
  18. Hosny FA. 2008. Poultry Sector Country Review. Food and Agriculture Organization of The United Nations (FAO). November 2006, Re-edited July 2008; pp. 1-47.
  19. ISO11290-1. 1996. Microbiology of food and animal feeding stuffs – horizontal method for the detection and enumeration of Listeria monocytogenes – Part 1: detection method. International Organization for Standardization, Geneva.
  20. Kanarat S, Jitnupong W, Sukhapesna J. 2011. Prevalence of Listeria monocytogenes in chicken production chain in Thailand. Thai J. Vet. Med. 41: 155-161.
  21. Li Q, Sherwood J, Logue C. 2007. Antimicrobial resistance of Listeria spp. recovered from processed bison. Lett. Appl. Microbiol. 44: 86-91.
    Pubmed CrossRef
  22. Liu D, Lawrence ML, Austin FW, Ainsworth AJ. 2007. A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. J. Microbiol. Methods 71: 133-140.
    Pubmed CrossRef
  23. Osaili TM, Alaboudi AR, Nesiar EA. 2011. Prevalence of Listeria spp. and antibiotic susceptibility of Listeria monocytogenes isolated from raw chicken and ready-to-eat chicken products in Jordan. Food Control 22: 586-590.
    CrossRef
  24. Petersen L, Madsen M. 2000. Listeria spp. in broiler flocks:recovery rates and species distribution investigated by conventional culture and the EiaFoss method. Int. J. Food Microbiol. 58: 113-116.
    CrossRef
  25. Skovgaard N, Morgen CA. 1988. Detection of Listeria spp. in faeces from animals, in feeds, and in raw foods of animal origin. Int. J. Food Microbiol. 6: 229-242.
    CrossRef
  26. Troxler R, von Graevenitz A, Funke G, Wiedemann B, Stock I. 2000. Natural antibiotic susceptibility of Listeria species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri strains. Clin. Microbiol. Infect. 6: 525-535.
    Pubmed CrossRef
  27. Vitas AI, Aguado V, Garcia-Jalon I. 2004. Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra (Spain). Int. J. Food Microbiol. 90: 349-356.
    CrossRef
  28. Zhang W, Wang X, Xia X, Yang B, Xi M, Meng J. 2013. Isolation and characterization of Listeria monocytogenes isolates from retail foods in Shaanxi Province, China. Foodborne Pathog. 10: 867-872.
    Pubmed CrossRef

Article

Research article

J. Microbiol. Biotechnol. 2016; 26(9): 1551-1556

Published online September 28, 2016 https://doi.org/10.4014/jmb.1603.03075

Copyright © The Korean Society for Microbiology and Biotechnology.

Listeria Species in Broiler Poultry Farms: Potential Public Health Hazards

Hesham Dahshan 1*, Abdallah Mohamed Amin Merwad 2 and Taisir Saber Mohamed 3

1Department of Veterinary Public Health, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Sharkia Governorate, Egypt, 2Department of Zoonoses, Faculty of Veterinary Medicine, Zagazig University, Egypt, 3Department of Medical Microbiology and Immunology, Faculty of Medicine, Zagazig University, Egypt

Received: March 31, 2016; Accepted: June 10, 2016

Abstract

Broiler meat production worldwide has been plagued by lethal food-poisoning bacteria
diseases, including listeriosis. A fatality rate of 15.6% was recorded in human beings in the EU
in 2015. During 2013, a total of 200 poultry farm samples, including litter, chicken breast, farm
feed, and drinking water, were collected to generate baseline data for the characterization of
the genus Listeria in broiler poultry farms. Listeria spp. were detected in a total of 95 (47.5%)
poultry farm samples. The isolates of Listeria spp. included L. innocua (28.5%), L. ivanovii
(12.5%), L. welshimeri (4.5%), and L. monocytogenes and L. seeligeri (1% each). Listeria spp.
contamination rates were higher in farm feed (70%), followed by litter (52.5%), chicken breasts
(42.2%), and drinking water (10%). Almost all Listeria spp. isolates were resistant to more than
three classes of antibiotics (multidrug resistant). Besides this, we observed a significant
resistance level to penicillin and fluoroquinolone drugs. However, lower resistance levels
were recorded for broad-spectrum cephalosporins. The inlA, inlC, and inlJ virulence genes
were detected in almost all of the L. monocytogenes isolates. Thus, food safety management
approaches and interventions at all stages of the broiler rearing cycle were needed to control
cross-contamination and the zoonotic potential of listeriosis.

Keywords: Poultry farm, Listeria species, Antibiotic resistance, Virulence genes, Health hazards

References

  1. Ahmed AM, El-Atti NM. 2010. Existence of Listeria species in broiler carcasses with an attempt to control Listeria monocytogenes using trisodium phosphate. Afr. J. Food Sci. 4: 46-51.
  2. Ashraf MA, Sohaila F, Hassan A, Raafat H, Abdelazeem M, Khalid IE. 2010. Occurrence of Listeria species in meat, chicken products and human stools in Assiut city, Egypt with PCR use for rapid identification of Listeria monocytogenes. Veter. World 3: 353-359.
  3. Aury K, Bouquin SL, Toquin MT, Huneau-Salaun A, Le Notre Y, Allain V, et al. 2011. Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks. Prev. Vet. Med. 98: 271-278.
    Pubmed CrossRef
  4. Bauer A, Kirby W, Sherris JC, Turck M. 1996. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45: 493.
  5. Bertrand S, Huys G, Yde M, D’Haene K, Tardy F, Vrints M. 2005. Detection and characterization of tet(M) in tetracycline resistant Listeria strains from human and food processing origins in Belgium and France. J. Med. Microbiol. 54: 1151-1156.
    Pubmed CrossRef
  6. Castanon JI. 2007. History of the use of antibiotic as growth promoters in European poultry feeds. Poult. Sci. 86: 2466-2471.
    Pubmed CrossRef
  7. Chemaly M, Toquin MT, Le Nôtre Y, Fravalo P. 2008. Prevalence of Listeria monocytogenes in poultry production in France. J. Food Prot. 71: 1996-2000.
    Pubmed CrossRef
  8. Clinical and Laboratory Standards Institute (previously National Committee on Clinical Laboratory Standards). 2006. Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved Standard-Ninth Edition M2-A9. CLSI, Wayne, PA.
  9. Cocolin L, Stella S, Nappi R, Bozzetta E, Cantoni C, Comi G. 2005. Analysis of PCR-based methods for characterization of Listeria monocytogenes strains isolated from different sources. Int. J. Food Microbiol. 103: 167-178.
    Pubmed CrossRef
  10. Conter M, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri A. 2009. Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int. J. Food Microbiol. 128: 497-500.
    Pubmed CrossRef
  11. Cox NA, Bailey JS, Berrang ME. 1997. The presence of Listeria monocytogenes in the integrated poultry industry. J. Appl. Poult. Res. 6: 116-119.
    CrossRef
  12. Dijkstra RG. 1976. Listeria-encephalitis in cows through litter from a broiler-farm. Zentralbl. Bakteriol. Orig. B 161: 383-385.
    Pubmed
  13. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). 2015. The European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. 13: 3991.
    CrossRef
  14. Esteban JI, Oporto B, Aduriz G, Juste RA, Hurtado A. 2008. A survey of food-borne pathogens in free-range poultry farms. Int. J. Food Microbiol. 123: 177-182.
    Pubmed CrossRef
  15. Fallah AA, Saei-Dehkordi SS, Rahnama M, Tahmasby H, Mahzounieh M. 2012. Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control 28: 327-332.
    CrossRef
  16. Gomez D, Azon E, Marco N, Carraminana JJ, Rota C, Arino A, Yangüela J. 2014. Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol. 42: 61-65.
    Pubmed CrossRef
  17. Hof H, Nichterlein T, Kretschmar M. 1997. Management of listeriosis. Clin. Microbiol. Rev. 10: 345-357.
    Pubmed KoreaMed
  18. Hosny FA. 2008. Poultry Sector Country Review. Food and Agriculture Organization of The United Nations (FAO). November 2006, Re-edited July 2008; pp. 1-47.
  19. ISO11290-1. 1996. Microbiology of food and animal feeding stuffs – horizontal method for the detection and enumeration of Listeria monocytogenes – Part 1: detection method. International Organization for Standardization, Geneva.
  20. Kanarat S, Jitnupong W, Sukhapesna J. 2011. Prevalence of Listeria monocytogenes in chicken production chain in Thailand. Thai J. Vet. Med. 41: 155-161.
  21. Li Q, Sherwood J, Logue C. 2007. Antimicrobial resistance of Listeria spp. recovered from processed bison. Lett. Appl. Microbiol. 44: 86-91.
    Pubmed CrossRef
  22. Liu D, Lawrence ML, Austin FW, Ainsworth AJ. 2007. A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. J. Microbiol. Methods 71: 133-140.
    Pubmed CrossRef
  23. Osaili TM, Alaboudi AR, Nesiar EA. 2011. Prevalence of Listeria spp. and antibiotic susceptibility of Listeria monocytogenes isolated from raw chicken and ready-to-eat chicken products in Jordan. Food Control 22: 586-590.
    CrossRef
  24. Petersen L, Madsen M. 2000. Listeria spp. in broiler flocks:recovery rates and species distribution investigated by conventional culture and the EiaFoss method. Int. J. Food Microbiol. 58: 113-116.
    CrossRef
  25. Skovgaard N, Morgen CA. 1988. Detection of Listeria spp. in faeces from animals, in feeds, and in raw foods of animal origin. Int. J. Food Microbiol. 6: 229-242.
    CrossRef
  26. Troxler R, von Graevenitz A, Funke G, Wiedemann B, Stock I. 2000. Natural antibiotic susceptibility of Listeria species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri strains. Clin. Microbiol. Infect. 6: 525-535.
    Pubmed CrossRef
  27. Vitas AI, Aguado V, Garcia-Jalon I. 2004. Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra (Spain). Int. J. Food Microbiol. 90: 349-356.
    CrossRef
  28. Zhang W, Wang X, Xia X, Yang B, Xi M, Meng J. 2013. Isolation and characterization of Listeria monocytogenes isolates from retail foods in Shaanxi Province, China. Foodborne Pathog. 10: 867-872.
    Pubmed CrossRef