[en] The presence of Campylobacter was assessed in different samples of poultry, pork and beef meat and carcasses from slaughterhouses, production plants and retail level. An introductory study from 1997 to 1999, had the purpose of establishing the optimum dilution to detect changes in prevalence and allowed a semi-quantitative estimation of poultry and pork contamination. Following this, between 2000 and 2003, 4254 samples were taken in order to study the trends. The poultry matrixes represented the greatest number and the most highly contaminated samples, with 30.9% (in 0.01 g) positive samples, 18.7% (in 1 g), 46.9% (in 25 g) and 19.6% (in 0.01 g) for broiler carcasses, broiler fillets, prepared chicken and layer carcasses, respectively. Broiler carcasses and fillets sampled at retail level were significantly less contaminated than samples from production plants. Pork, beef and veal samples were rarely contaminated and, where contamination existed, it was at a low prevalence (maximum 5.0%). The high and unvarying prevalence of Campylobacter in poultry necessitates the implementation of intervention measures at the primary production level, in addition to methods of minimizing cross-contamination at the processing level. A survey plan in line with the present study could be used in the future to monitor the effects of the planned measures and performance objectives and to follow the evolution of Campylobacter contamination at all stages of the food chain, in accordance with European legislation. (c) 2007 Elsevier B.V. All rights reserved.
Disciplines :
Food science Microbiology
Author, co-author :
Ghafir, Yasmine; Université de Liège - ULiège - ULG > Sciences des Denrées alimentaires > Microbiologie des Denrées alimentaires
China, Bernard; Université de Liège - ULiège - ULG > Sciences des Denrées alimentaires > Microbiologie des Denrées alimentaires
Dierick, Katelijne; Institut scientifique de la Santé publique - ISP > Microbiologie > Microbiologie des aliments
De Zutter, Lieven; Universiteit Gent - Ugent > Food Microbiology
Daube, Georges ; Université de Liège - ULiège > Sciences des denrées alimentaires > Microbiologie des denrées alimentaires
Language :
English
Title :
A seven-year survey of Campylobacter contamination in meat at different production stages in Belgium
Publication date :
2007
Journal title :
International Journal of Food Microbiology
ISSN :
0168-1605
eISSN :
1879-3460
Publisher :
Elsevier Science Bv, Amsterdam, Netherlands
Volume :
116
Issue :
1
Pages :
111-120
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
AFSCA - Agence Fédérale pour la Sécurité de la Chaîne Alimentaire [BE]
Allos B.M. Campylobacter jejuni infections: update on emerging issues and trends. Clinical Infectious Diseases 32 (2001) 1201-1206
Anonymous. Council Directive 95/65/EC of 14 December 1994 laying down the requirements for the production and placing on the market of minced meat and meat preparation. Official Journal of the European Union L368 (1994) 10-31
Anonymous, 2001. DANMAP 2000 - Resistance in zoonotic bacteria. In: Bager, F., Emborg, H.D. (Ed.), DANMAP 2000 - Consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. Danish Veterinary Laboratory, Danish Veterinary and Food Administration, Statens Serum Institute and Danish Medicines Agency, Copenhagen, pp. 21-28.
Anonymous. Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. Official Journal of the European Union L325 (2003) 31-40
Anonymous. Opinion of the Scientific Panel on Biological Hazards on the request from the Commission related to Campylobacter in animals and foodstuffs (Question N° EFSA-Q-2004-081). The EFSA Journal 177 (2005) 1-10
Anonymous. Trends and Sources of Zoonotic Agents in Animals, Feeding Stuffs, Food and Man in the European Union and Norway in 2003 (2005), Community Reference Laboratory on the Epidemiology of Zoonoses, Bfr, Berlin
Berndtson E., Danielsson-Tham M.L., and Engvall A. Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. International Journal of Food Microbiology 32 (1996) 35-47
Black R.E., Levine M.M., Clements M.L., Hughes T.P., and Blaser M.J. Experimental Campylobacter jejuni infection in humans. Journal of Infectious Diseases 157 (1988) 472-479
Boes J., Nesterling L., Nielsen E.M., Kranker S., Enøe C., Wachmann H.C., and Baggesen D.L. Prevalence and diversity of Campylobacter jejuni in pig herds on farms with and without cattle or poultry. Journal of Food Protection 68 (2005) 722-727
Borch E., Nesbakken T., and Christensen H. Hazard identification in swine slaughter with respect to foodborne bacteria. International Journal of Food Microbiology 30 (1996) 9-25
Butzler J.P. Campylobacter, from obscurity to celebrity. Clinical Microbiology and Infection 10 (2004) 868-876
CDC. Preliminary FoodNet data on the incident of infection with pathogens transmitted commonly through food - selected sites, United States, 2003. Morbidity and Mortality Weekly Report 53 (2004) 338-343
Cools I., Uyttendaele M., Caro C., D'Haese E., Nelis H.J., and Debevere J. Survival of Campylobacter jejuni strains of different origin in drinking water. Journal of Applied Microbiology 94 (2003) 886-892
Cools I., D'Haese E., Uyttendaele M., Storms E., Nelis H.J., and Debevere J. Solid phase cytometry as a tool to detect viable but non-culturable cells of Campylobacter jejuni. Journal of Microbiological Methods 63 (2005) 107-114
Cools I., Uyttendaele M., Cerpentier J., D'Haese E., Nelis H.J., and Debevere J. Persistence of Campylobacter jejuni on surfaces in a processing environment and on cutting boards. Letters in Applied Microbiology 40 (2005) 418-423
Cornelius A.J., Nicol C., and Hudson J.A. Campylobacter spp. in New Zealand raw sheep liver and human campylobacteriosis cases. International Journal of Food Microbiology 99 (2005) 99-105
Corry J.E., and Atabay H.I. Poultry as a source of Campylobacter and related organisms. Journal of Applied Microbiology (2001) 96S-114S
Ducoffre G. Surveillance des maladies infectieuses par un réseau de laboratories de microbiologie 2003 + tendances épidémiologiques 1983-2002 (2004), Scientific Institute of Public Health, Department of Epidemiology, Brussels
Duffy E.A., Belk K.E., Sofos J.N., Bellinger G.R., Pape A., and Smith G.C. Extent of microbial contamination in United States pork retail products. Journal of Food Protection 64 (2001) 172-178
Dufrenne J., Ritmeester W., Delfgou-van Asch E., van Leusden F., and de Jonge R. Quantification of the contamination of chicken and chicken products in the Netherlands with Salmonella and Campylobacter. Journal of Food Protection 64 (2001) 538-541
Ekdahl K., Normann B., and Andersson Y. Could flies explain the elusive epidemiology of campylobacteriosis?. BioMed Central Infectious Diseases 5 (2005) 1471-2334
Endtz H.P., Vliegenthartb J.S., Vandamme P., Weverink H.W., van den Braak N.P., Verbrugh H.A., and van Belkum A. Genotypic diversity of Campylobacter lari isolated from mussels and oysters in The Netherlands. International Journal of Food Microbiology 34 (1997) 79-88
Fernándes H., and Pisón V. Isolation of thermotolerant species of Campylobacter from commercial chicken livers. International Journal of Food Microbiology 29 (1996) 75-80
Fricker C.R., and Park R.W. A two-year study of the distribution of 'thermophilic' campylobacters in human, environmental and food samples from the Reading area with particular reference to toxin production and heat-stable serotype. Journal of Applied Bacteriology 66 (1989) 477-490
Frost J.A. Current epidemiological issues in human campylobacteriosis. Society for Applied Microbiology Symposium Series (2001) 85S-95S
Ghafir Y., China B., Korsak N., Dierick K., Collard J.-M., Godard C., De Zutter L., and Daube G. Belgian surveillance plans to assess changes in Salmonella prevalence in meat at different production stages. Journal of Food Protection 68 (2005) 2269-2277
Hald B., Skovgard H., Bang D.D., Pedersen K., Dybdahl J., Jespersen J.B., and Madsen M. Flies and Campylobacter infection of broiler flocks. Emerging Infectious Diseases 10 (2004) 1490-1492
Herman L., Heyndrickx M., Grijspeerdt K., Vandekerchove D., Rollier I., and De Zutter L. Routes for Campylobacter contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 131 (2003) 1169-1180
Hernandez F. A simple and inexpensive method to generate a microaerophilic atmosphere for the isolation of Campylobacter sp. Revista do Instituto de Medicina Tropical de São Paulo 38 (1996) 241-242
Heuer O.E., Pedersen K., Andersen J.S., and Madsen M. Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Letters in Applied Microbiology 33 (2001) 269-274
Hood A.M., Pearson A.D., and Shahamat M. The extent of surface contamination of retailed chicken with Campylobacter jejuni serogroups. Epidemiology and Infection 100 (1988) 17-25
Hu L., and Kopecko D.J. Campylobacter species. In: Miliotis M.D., and Bier J.W. (Eds). International Handbook of Foodborne Pathogens (2003), Marcel Dekker, New York 181-198
Humphrey T.J., Martin K.W., Slader J., and Durham K. Campylobacter spp. in the kitchen: spread and persistence. Journal of Applied Microbiology (2001) 115S-120S
Jorgensen F., Bailey R., Williams S., Henderson P., Wareing D.R., Bolton F.J., Frost J.A., Ward L., and Humphrey T.J. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. International Journal of Food Microbiology 76 (2002) 151-164
Keener K.M., Bashor M.P., Curtis P.A., Sheldon B.W., and Kathariou S. Comprehensive review of Campylobacter and poultry processing. Comprehensive Reviews in Food Science and Food Safety 3 (2004) 105-116
Kramer J.M., Frost J.A., Bolton F.J., and Wareing D.R. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. Journal of Food Protection 63 (2000) 1654-1659
Ledergerber U., Regula G., Stephan R., Danuser J., Bissig B., and Stark K.D. Risk factors for antibiotic resistance in Campylobacter spp. isolated from raw poultry meat in Switzerland. BMC Public Health 3 (2003) 39
Linton D., Lawson A.J., Owen R.J., and Stanley J. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. Journal of Clinical Microbiology 35 (1997) 2568-2572
Loewenherz-Lüning K., Heitmann M., and Hilderbrandt G. Survey about the occurrence of Campylobacter jejuni in foods of animal origin. Fleischwirtschaft 76 (1996) 958-961
Madden R.H., Moran L., and Scates P. Frequency of occurrence of Campylobacter spp. in red meats and poultry in Northern Ireland and their subsequent subtyping using polymerase chain reaction-restriction fragment length polymorphism and the random amplified polymorphic DNA method. Journal of Applied Microbiology 84 (1998) 703-708
Mayrhofer S., Paulsen P., Smulders F.J.M., and Hilbert F. Antimicrobial resistance profile of five major food-borne pathogens isolated from beef, pork and poultry. International Journal of Food Microbiology 97 (2004) 23-29
Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., and Tauxe R.V. Food-related illness and death in the United States. Emerging Infectious Diseases 5 (1999) 607-625
Meldrum R.J., Tucker I.D., Smith R.M., and Edwards C. Survey of Salmonella and Campylobacter contamination of whole, raw poultry on retail sale in Wales in 2003. Journal of Food Protection 68 (2005) 1447-1449
Miwa N., Takegahara Y., Terai K., Kato H., and Takeuchi T. Campylobacter jejuni contamination on broiler carcasses of C. jejuni-negative flocks during processing in a Japanese slaughterhouse. International Journal of Food Microbiology 84 (2003) 105-109
Mohammed K.A., Miles R.J., and Halablab M.A. Simple method to grow enteric Campylobacters in unsupplemented liquid medium without the need for microaerophilic kits. Journal of Microbiological Methods 61 (2005) 273-276
Moore J.E., Wilson T.S., Wareing D.R., Humphrey T.J., and Murphy P.G. Prevalence of thermophilic Campylobacter spp. in ready-to-eat foods and raw poultry in Northern Ireland. Journal of Food Protection 65 (2002) 1326-1328
Nesbakken T., Eckner K., Hoidal H.K., and Rotterud O.J. Occurrence of Yersinia enterocolitica and Campylobacter spp. in slaughter pigs and consequences for meat inspection, slaughtering, and dressing procedures. International Journal of Food Microbiology 80 (2003) 231-240
Oosterom J., De Wilde G.J.A., De Boer E., De Blaauw L.H., and Karman H. Survival of Campylobacter jejuni during poultry processing and pig slaughtering. Journal of Food Protection 46 (1983) 702-706
Oosterom J., den Uyl C.H., Banffer J.R., and Huisman J. Epidemiological investigations on Campylobacter jejuni in households with a primary infection. The Journal of Hygiene 93 (1983) 325-332
Oosterom J., Notermans S., Karman H., and Engels G.B. Origin and prevalence of Campylobacter jejuni in poultry processing. Journal of Food Protection 46 (1983) 339-344
Padungtod P., Hanson R., Wilson D.L., Bell J., Linz J.E., and Kaneene J.B. Identification of Campylobacter jejuni isolates from cloacal and carcass swabs of chickens in Thailand by a 5′ nuclease fluorogenic polymerase chain reaction assay. Journal of Food Protection 65 (2002) 1712-1716
Pearce R.A., Wallace F.M., Call J.E., Dudley R.L., Oser A., Yoder L., Sheridan J.J., and Luchansky J.B. Prevalence of Campylobacter within a swine slaughter and processing facility. Journal of Food Protection 66 (2003) 1550-1556
Pezzotti G., Serafin A., Luzzi I., Mioni R., Milan M., and Perin R. Occurrence and resistance to antibiotics of Campylobacter jejuni and Campylobacter coli in animals and meat in northeastern Italy. International Journal of Food Microbiology 82 (2003) 281-287
Reiter M.G.R., Bueno C.M.M., López C., and Jordano R. Occurrence of Campylobacter and Listeria monocytogenes in a poultry processing plant. Journal of Food Protection 68 (2005) 1903-1906
Rosenquist H., Nielsen N.L., Sommer H.M., Norrung B., and Christensen B.B. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology 83 (2003) 87-103
Stern N.J., Hiett K.L., Alfredsson G.A., Kristinsson K.G., Reiersen J., Hardardottir H., Briem H., Gunnarsson E., Georgsson F., Lowman R., Berndtson E., Lammerding A.M., Paoli G.M., and Musgrove M.T. Campylobacter spp. in Icelandic poultry operations and human disease. Epidemiology and Infection 130 (2003) 23-32
Tirado C., and Schmidt K. WHO surveillance programme for control of foodborne infections and intoxications: preliminary results and trends across greater Europe. World Health Organization. The Journal of Infection 43 (2001) 80-84
Uyttendaele M., De Troy P., and Debevere J. Incidence of Salmonella, Campylobacter jejuni, Campylobacter coli, and Listeria monocytogenes in poultry carcasses and different types of poultry products for sale on the Belgian retail market. Journal of Food Protection 62 (1999) 735-740
Vandamme P., Van Doorn L.J., al Rachid S.T., Quint W.G.V., van der Plas J., Chan V.L., and On S.L.W. Campylobacter hyoilei Alderton et al. 1995 and Campylobacter coli Veron and Chatelain 1973 are subjective synonyms. International Journal of Systematic Bacteriology 47 (1997) 1055-1060
Vellinga A., and Van Loock F. The dioxin crisis as experiment to determine poultry-related Campylobacter enteritis. Emerging Infectious Diseases 8 (2002) 19-22
Whyte P., McGill K., Cowley D., Madden R.H., Moran L., Scates P., Carroll C., O'Leary A., Fanning S., Collins J.D., McNamara E., Moore J.E., and Cormicanh M. Occurrence of Campylobacter in retail foods in Ireland. International Journal of Food Microbiology 95 (2004) 111-118
Wilson I.G. Antibiotic resistance of Campylobacter in raw retail chickens and imported chicken portions. Epidemiology and Infection 131 (2003) 1181-1186
Zanetti F., Varoli O., Stampi S., and de Luca G. Prevalence of thermophilic Campylobacter and Arcobacter butzleri in food of animal origin. International Journal of Food Microbiology 33 (1996) 315-321
