Prevalence and antimicrobial profile of Campylobacter isolates from free-range and conventional farming chicken meat during a 6-year survey

Food Control

Volume 56, October 01, 2015, Pages 161-168

  (Article)

Economou, V.^ab, 

Zisides, N.^a, 

Gousia, P.^a, 

Petsios, S.^a, 

Sakkas, H.^a, 

Soultos, N.^b, 

Papadopoulou, C.^a 

 

^a  Food-Water Microbiology Group, Department of Microbiology, Faculty of Medicine, School of Health Sciences, University of Ioannina, Ioannina, Greece
^b  Department of Hygiene and Technology of Foods of Animals Origin, Faculty of Veterinary Medicine, School of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece 

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Abstract

The present study aimed to investigate the prevalence of Campylobacter spp. in the meat of free-range and conventional farming broilers and to assess the respective antimicrobial susceptibility of the isolates. Three hundred and sixty nine fresh chicken meat samples were collected from different farms at slaughter (60 from free-range poultry farms and 309 from conventional farms) in North Western Greece. Susceptibility tests against 12 antimicrobials (amikacin, gentamicin, imipenem, cefamandole, cefotaxime, cefoxitin, imipenem, erythromycin, ampicillin, amoxicillin - clavulanic acid, ciprofloxacin, tetracycline) were performed. Campylobacter spp. was isolated from 91 (29.4%) of the free-range chicken meat and from 106 (28.7%) of the conventional farming chicken meat samples. The annual incidence of Campylobacter spp. among the free-range and conventional broilers was not statistically significant. However, a reducing trend was observed in the overall prevalence of Campylobacter spp. from 2005 to 2010. Variable resistance rates were observed towards the tested antimicrobials: erythromycin (76%), tetracyclines (71%), ampicillin (66%), ciprofloxacin (51%), cefamendole (41%) cefoxitin (27%), amikacin (15%), and cefotaxime (5%). No differences were observed in the antimicrobial susceptibility of isolates from free-range and conventional farming samples. © 2015 Elsevier Ltd.

Author keywords

Broilers; Campylobacter; Chicken; Conventional farming; Free-range; Susceptibility

ISSN: 09567135 CODEN: FOOCESource Type: Journal Original language: English

DOI: 10.1016/j.foodcont.2015.03.022Document Type: Article

Publisher: Elsevier Ltd

References (56)

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• 
  1

  Allen, V.M., Bull, S.A., Corry, J.E.L., Domingue, G., Jørgensen, F., Frost, J.A., Whyte, R., (...), Humphrey, T.J.

  Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation
  (2007) International Journal of Food Microbiology, 113 (1), pp. 54-61. Cited 75 times.
  doi: 10.1016/j.ijfoodmicro.2006.07.011
  
• 
  2

  Avrain, L., Humbert, F., L'Hospitalier, R., Sanders, P., Vernozy-Rozand, C., Kempf, I.

  Antimicrobial resistance in Campylobacter from broilers: Association with production type and antimicrobial use
  (2003) Veterinary Microbiology, 96 (3), pp. 267-276. Cited 77 times.
  doi: 10.1016/j.vetmic.2003.07.001
  
• 
  3

  Bahrndorff, S., Rangstrup-Christensen, L., Nordentoft, S., Hald, B.

  Foodborne disease prevention and broiler chickens with reduced Campylobacter infection
  (2013) Emerging Infectious Diseases, 19 (3), pp. 425-430. Cited 17 times.
  http://wwwnc.cdc.gov/eid/article/19/3/pdfs/11-1593.pdf
  doi: 10.3201/eid1903.111593
  
• 
  4

  Bostan, K., Aydin, A., Ang, M.K.

  Prevalence and antibiotic susceptibility of thermophilic Campylobacter species on beef, mutton, and chicken carcasses in Istanbul, Turkey.
  (2009) Microbial drug resistance (Larchmont, N.Y.), 15 (2), pp. 143-149. Cited 20 times.
  
• 
  5

  Castellini, C., Berri, C., Le Bihan-Duval, E., Martino, G.

  Qualitative attributes and consumer perception of organic and free-range poultry meat
  (2008) World's Poultry Science Journal, 64 (4), pp. 500-512. Cited 42 times.
  doi: 10.1017/S0043933908000172
  
• 
  6

  (2013) Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. Cited 528 times.
  CLSI document M100-S23, USA
  

  •  
• 
  7

  Colles, F.M., Jones, T.A., McCarthy, N.D., Sheppard, S.K., Cody, A.J., Dingle, K.E., Dawkins, M.S., (...), Maiden, M.C.J.

  Campylobacter infection of broiler chickens in a free-range environment
  (2008) Environmental Microbiology, 10 (8), pp. 2042-2050. Cited 50 times.
  doi: 10.1111/j.1462-2920.2008.01623.x
  
• 
  8

  Commission Regulation (EC) No 2160/2003 of the European Parliament and of the Council of 17 November 2003 on the control of Salmonella and other specified food-borne zoonotic agents
  Official Journal of the European Union, L 325, pp. 1-15. Cited 62 times.
  

  •  
• 
  9

  Commission Regulation (EC) No 646/2007 of 12 June 2007 implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council as regards a Community target for the reduction of the prevalence of Salmonella Enteritidis and Salmonella Typhimurium in broilers and repealing Regulation (EC) No 1091/2005
  Official Journal of the European Union, L 151, pp. 21-25. Cited 4 times.
  

  •  
• 
  10

  Deckert, A., Valdivieso-Garcia, A., Reid-Smith, R., Tamblyn, S., Seliske, P., Irwin, R., Dewey, C., (...), McEwen, S.A.

  Prevalence and antimicrobial resistance in Campylobacter spp. Isolated from retail chicken in two health units in Ontario
  (2010) Journal of Food Protection, 73 (7), pp. 1317-1324. Cited 19 times.
  
• 
  11

  Desmonts, M.-H., Dufour-Gesbert, F., Avrain, L., Kempf, I.

  Antimacrobial resistance in Campylobacter strains isolated from French broilers before and after antimicrobial growth promoter bans
  (2004) Journal of Antimicrobial Chemotherapy, 54 (6), pp. 1025-1030. Cited 27 times.
  doi: 10.1093/jac/dkh473
  
• 
  12

  The community summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2008
  (2010) The EFSA Journal, 8 (1658).
  arxiv:2010.1658
  

  •  
• 
  13

  The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the european Union in 2006
  (2007) The EFSA Journal, 130.
  

  •  
• 
  14

  The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008
  (2010) The EFSA Journal, 8, p. 1496. Cited 249 times.
  

  •  
• 
  15

  The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009
  (2011) The EFSA Journal, 9, p. 2090. Cited 246 times.
  http://dx.doi.org.scopeesprx.elsevier.com/10.2903/j.efsa.2011.2090
  

  •  
• 
  16

  The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in the European Union in 2009
  (2011) The EFSA Journal, 9, p. 2154. Cited 24 times.
  http://dx.doi.org.scopeesprx.elsevier.com/10.2903/j.efsa.2011.2154
  

  •  
• 
  17

  The European Union summary report on trends and sources of zoonoses, Zoonotic Agents and Food-borne Outbreaks in the European Union in 2010
  (2012) The EFSA Journal, 10, p. 2597. Cited 310 times.
  http://dx.doi.org.scopeesprx.elsevier.com/10.2903/j.efsa.2012.2597
  

  •  
• 
  18

  The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010
  (2012) The EFSA Journal, 10, p. 2598. Cited 53 times.
  http://dx.doi.org.scopeesprx.elsevier.com/10.2903/j.efsa.2012.2598
  

  •  
• 
  19

  The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011
  (2013) The EFSA Journal, 11, p. 3129. Cited 267 times.
  http://dx.doi.org.scopeesprx.elsevier.com/10.2903/j.efsa.2014.3547
  

  •  
• 
  20

  Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain
  (2011) The EFSA Journal, 9 (4), p. 2105. Cited 99 times.
  

  •  
• 
  21

  Esteban, J.I., Oporto, B., Aduriz, G., Juste, R.A., Hurtado, A.

  A survey of food-borne pathogens in free-range poultry farms
  (2008) International Journal of Food Microbiology, 123 (1-2), pp. 177-182. Cited 39 times.
  doi: 10.1016/j.ijfoodmicro.2007.12.012
  
• 
  22

  (2014) Breakpoint tables for interpretation of MICs and zone diameters. Cited 183 times.
  Version 4.0, Accessed 14.05.14
  http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/Breakpoint_table_v_4.0.pdf
  

  •  
• 
  23

  Foley, S.
  Campylobacter jejuni
  (2012) Bad bug book: Foodborne pathogenic microorganisms and natural toxins handbook
  FDA, Washington DC, K.A. Lampel, S. Al-Khaldi, S.M. Cahill (Eds.)
  

  •  
• 
  24

  Franz, E., van der Fels-Klerx, H.J., Thissen, J., van Asselt, E.D.

  Farm and slaughterhouse characteristics affecting the occurrence of Salmonella and Campylobacter in the broiler supply chain
  (2012) Poultry Science, 91 (9), pp. 2376-2381. Cited 4 times.
  http://ps.fass.org/content/91/9/2376.full.pdf+html
  doi: 10.3382/ps.2009-00367
  
• 
  25

  Ge, B., Wang, F., Sjölund-Karlsson, M., McDermott, P.F.

  Antimicrobial resistance in Campylobacter: Susceptibility testing methods and resistance trends
  (2013) Journal of Microbiological Methods, 95 (1), pp. 57-67. Cited 28 times.
  doi: 10.1016/j.mimet.2013.06.021
  
• 
  26

  Ghafir, Y., China, B., Dierick, K., De Zutter, L., Daube, G.

  A seven-year survey of Campylobacter contamination in meat at different production stages in Belgium
  (2007) International Journal of Food Microbiology, 116 (1), pp. 111-120. Cited 56 times.
  doi: 10.1016/j.ijfoodmicro.2006.12.012
  
• 
  27

  Ghareeb, K., Awad, W.A., Mohnl, M., Schatzmayr, G., Böhm, J.

  Control strategies for Campylobacter infection in poultry production
  (2013) World's Poultry Science Journal, 69 (1), pp. 57-76. Cited 9 times.
  doi: 10.1017/S0043933913000068
  
• 
  28

  Gkogka, E., Reij, M.W., Havelaar, A.H., Zwietering, M.H., Gorris, L.G.M.

  Risk-based estimate of effect of foodborne diseases on public health, Greece
  (2011) Emerging Infectious Diseases, 17 (9), pp. 1581-1590. Cited 30 times.
  http://www.cdc.gov/eid/content/17/9/pdfs/101766.pdf
  doi: 10.3201/eid1709.101766
  
• 
  29

  Gousia, P., Economou, V., Sakkas, H., Leveidiotou, S., Papadopoulou, C.

  Antimicrobial resistance of major foodborne pathogens from major meat products
  (2011) Foodborne Pathogens and Disease, 8 (1), pp. 27-38. Cited 17 times.
  doi: 10.1089/fpd.2010.0577
  
• 
  30

  Control program of Salmonella carriage in broilers of the species Gallus gallus. Greek national printing office
  Ministry of Rural Development and Food (in Greek). Available online at.
  mailto:https://diavgeia.gov.gr/doc/%CE%92%CE%9F%CE%9D%CE%9D%CE%92-%CE%94%CE%97%CE%A9
  

  •  
• 
  31

  Habib, I., Berkvens, D., De Zutter, L., Dierick, K., Van Huffel, X., Speybroeck, N., Geeraerd, A.H., (...), Uyttendaele, M.

  Campylobacter contamination in broiler carcasses and correlation with slaughterhouses operational hygiene inspection
  (2012) Food Microbiology, 29 (1), pp. 105-112. Cited 17 times.
  doi: 10.1016/j.fm.2011.09.004
  
• 
  32

  Hansson, I., Plym Forshell, L., Gustafsson, P., Boqvist, S., Lindblad, J., Olsson Engvall, E., Andersson, Y., (...), Vågsholm, I.

  Summary of the Swedish Campylobacter program in broilers, 2001 through 2005
  (2007) Journal of Food Protection, 70 (9), pp. 2008-2014. Cited 19 times.
  
• 
  33

  Heuer, O.E., KPedersen, JSAndersen, MMadsen

  Prevalence and antimicrobial susceptibility of thermophilic campylobacter in organic and conventional broiler flocks
  (2001) Letters in Applied Microbiology, 33 (4), pp. 269-274. Cited 155 times.
  doi: 10.1046/j.1472-765X.2001.00994.x
  
• 
  34

  (2010) Hellenic ministry of rural development and food
  (in Greek)
  http://www.minagric.gr/images/stories/docs/agrotis/poulerika/ekthesi_apotelesmaton_salmonelosis2009_2010.pdf
  

  •  
• 
  35

  Hue, O., Allain, V., Laisney, M.-J., Le Bouquin, S., Lalande, F., Petetin, I., Rouxel, S., (...), Chemaly, M.

  Campylobacter contamination of broiler caeca and carcasses at the slaughterhouse and correlation with Salmonella contamination
  (2011) Food Microbiology, 28 (5), pp. 862-868. Cited 17 times.
  doi: 10.1016/j.fm.2010.11.003
  
• 
  36

  Karagiannis, I., Sideroglou, T., Gkolfinopoulou, K., Tsouri, A., Lampousaki, D., Velonakis, E.N., Scoulica, E.V., (...), Bonovas, S.

  A waterborne Campylobacter jejuni outbreak on a Greek island
  (2010) Epidemiology and Infection, 138 (12), pp. 1726-1734. Cited 24 times.
  doi: 10.1017/S0950268810002116
  
• 
  37

  (2013) Hellenic Center for disease control and prevention. laboratory capability of Campylobacter spp. isolation in Greek hospitals and number of positive cultures in 2013
  (in Greek)
  http://www.keelpno.gr/
  

  •  
• 
  38

  Lazou, T., Dovas, C., Houf, K., Soultos, N., Iossifidou, E.

  Diversity of Campylobacter in retail meat and liver of lambs and goat kids
  (2014) Foodborne Pathogens and Disease, 11 (4), pp. 320-328.
  www.liebertonline.com/fpd
  doi: 10.1089/fpd.2013.1678
  
• 
  39

  Lazou, T., Houf, K., Soultos, N., Dovas, C., Iossifidou, E.

  Campylobacter in small ruminants at slaughter: Prevalence, pulsotypes and antibiotic resistance
  (2014) International Journal of Food Microbiology, 173, pp. 54-61. Cited 3 times.
  doi: 10.1016/j.ijfoodmicro.2013.12.011
  
• 
  40

  Marinou, I., Bersimis, S., Ioannidis, A., Nicolaou, C., Mitroussia-Ziouva, A., Legakis, N.J., Chatzipanagiotou, S.

  Identification and antimicrobial resistance of Campylobacter species isolated from animal sources
  (2012) Frontiers in Microbiology, 3 (FEB). Cited 4 times.
  http://www.frontiersin.org/Journal/DownloadFile.ashx?pdf=1&FileId=1300&articleId=18220&Version=1&ContentTypeId=21&FileName=fmicb-03-00058.pdf
  doi: 10.3389/fmicb.2012.00058
  
• 
  41

  McCarthy, N., Giesecke, J.

  Incidence of Guillain-Barré syndrome following infection with Campylobacter jejuni
  (2001) American Journal of Epidemiology, 153 (6), pp. 610-614. Cited 93 times.
  doi: 10.1093/aje/153.6.610
  
• 
  42

  Mellou, K., Sourtzi, P., Tsakris, A., Saroglou, G., Velonakis, E.

  Risk factors for sporadic Campylobacter jejuni infections in children in a Greek region
  (2010) Epidemiology and Infection, 138 (12), pp. 1719-1725. Cited 3 times.
  doi: 10.1017/S0950268810001196
  
• 
  43

  Mellou, K., Velonakis, E.

  Clinical manifestations and epidemiology of Campylobacter spp infection
  (2011) Archives of Hellenic Medicine, 28 (6), pp. 746-753.
  http://www.mednet.gr/archives/2011-6/pdf/746.pdf
  
• 
  44

  Miraglia, D., Ranucci, D., Branciari, R., Cioffi, A., Mammoli, R., Cenci Goga, B.T., Avellini, P.

  Prevalence of Campylobacter jejuni and Campylobacter coli in chicken hybrids with different growth rates, reared according to conventional and "Free-Range" production methods
  (2007) Veterinary Research Communications, 31 (SUPPL. 1), pp. 381-384. Cited 5 times.
  doi: 10.1007/s11259-007-0042-3
  
• 
  45

  Moran, L., Scates, P.A.M., Madden, R.H.

  Prevalence of campylobacter spp. in raw retail poultry on sale in northern ireland
  (2009) Journal of Food Protection, 72 (9), pp. 1830-1835. Cited 32 times.
  
• 
  46

  Näther, G., Alter, T., Martin, A., Ellerbroek, L.

  Analysis of risk factors for Campylobacter species infection in broiler flocks
  (2009) Poultry Science, 88 (6), pp. 1299-1305. Cited 25 times.
  http://ps.fass.org/cgi/reprint/88/6/1299
  doi: 10.3382/ps.2008-00389
  
• 
  47

  Newell, D.G., Fearnley, C.

  Sources of Campylobacter colonization in broiler chickens
  (2003) Applied and Environmental Microbiology, 69 (8), pp. 4343-4351. Cited 283 times.
  doi: 10.1128/AEM.69.8.4343-4351.2003
  
• 
  48

  Nobile, C.G.A., Costantino, R., Bianco, A., Pileggi, C., Pavia, M.

  Prevalence and pattern of antibiotic resistance of Campylobacter spp. in poultry meat in Southern Italy
  (2013) Food Control, 32 (2), pp. 715-718. Cited 13 times.
  doi: 10.1016/j.foodcont.2013.02.011
  
• 
  49

  Nyati, K.K., Nyati, R.
  Role of Campylobacter jejuni infection in the pathogenesis of Guillain-Barré syndrome: an update
  (2013) BioMed Research International
  http://dx.doi.org.scopeesprx.elsevier.com/10.1155/2013/852195
  

  •  
• 
  50

  Petridou, E., Zdragas, A.
  Investigation upon the presence of Campylobacter spp. in poultry meat and their antimicrobial resistance in Northern Greece
  (2009) 16th World veterinary poultry association Congress, Morocco, p. 419. Cited 2 times.
  

  •  
• 
  51

  Rasschaert, G., Houf, K., Van Hende, J., De Zutter, L.

  Investigation of the concurrent colonization with Campylobacter and Salmonella in poultry flocks and assessment of the sampling site for status determination at slaughter
  (2007) Veterinary Microbiology, 123 (1-3), pp. 104-109. Cited 19 times.
  doi: 10.1016/j.vetmic.2007.03.011
  
• 
  52

  Rivoal, K., Ragimbeau, C., Salvat, G., Colin, P., Ermel, G.

  Genomic diversity of Campylobacter coli and Campylobacter jejuni isolates recovered from free-range broiler farms and comparison with isolates of various origins
  (2005) Applied and Environmental Microbiology, 71 (10), pp. 6216-6227. Cited 61 times.
  doi: 10.1128/AEM.71.10.6216-6227.2005
  
• 
  53

  Rosenquist, H., Boysen, L., Krogh, A.L., Jensen, A.N., Nauta, M.

  Campylobacter contamination and the relative risk of illness from organic broiler meat in comparison with conventional broiler meat
  (2013) International Journal of Food Microbiology, 162 (3), pp. 226-230. Cited 12 times.
  doi: 10.1016/j.ijfoodmicro.2013.01.022
  
• 
  54

  Smulders, F.J.M., Gleisz, B., Sofka, D., Sacher, A., Omurtag, I., Paulsen, P., Hilbert, F.

  Microbial ecology on poultry carcasses along the production line
  (2011) Archiv fur Lebensmittelhygiene, 62 (5), pp. 170-174. Cited 6 times.
  doi: 10.2376/0003-925X-62-170
  
• 
  55

  Sopwith, W., Ashton, M., Frost, J.A., Tocque, K., O'Brien, S., Regan, M., Syed, Q.

  Enhanced surveillance of campylobacter infection in the North West of England 1997-1999
  (2003) Journal of Infection, 46 (1), pp. 35-45. Cited 41 times.
  doi: 10.1053/jinf.2002.1072
  
• 
  56

  Wright, S.L., Carver, D.K., Siletzky, R.M., Romine, S., Morrow, W.E.M., Kathariou, S.

  Longitudinal study of prevalence of Campylobacter jejuni and Campylobacter coli from Turkeys and swine grown in close proximity
  (2008) Journal of Food Protection, 71 (9), pp. 1791-1796. Cited 13 times.
  

  Papadopoulou, C.; Department of Microbiology, Faculty of Medicine, School of Health Sciences, University of Ioannina, Greece
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