Campylobacter in Denmark: control, human risk and source attribution

In Denmark, the incidence of human campylobacteriosis cases, as well as the Campylobacter prevalence in broiler flocks, is strongly influenced by season with a summer peak in JulyeAugust. Therefore, it was considered that the prevalence of Campylobacter in broiler meat sold at retail in Denmark might also be influenced by season. A retrospective survey analysis was performed on 2001e2007 national surveillance data of the prevalence of thermotolerant Campylobacter in all conventional broiler flocks at slaughter, and in randomly sampled broiler meat at retail. There was a significant effect of season on the occurrence of Campylobacter in meat at retail; the largest effect was found for domestic chilled meat. Thus, the Campylobacter prevalence in Danish broiler flocks, which fluctuated with season, was found to be a strong predictor for the occurrence of Campylobacter in fresh, chilled, Danish broiler meat. However, besides flock prevalence, there was also a direct effect of season on the occurrence of Campylobacter in Danish broiler meat at retail. 2011 Elsevier Ltd. All rights reserved.

[1]  T. Cooper,et al.  Evidence of effectiveness. , 2022, Studies in history and philosophy of science.

[2]  H. Vigre,et al.  Seasonal influence on the prevalence of thermotolerant Campylobacter in retail broiler meat in Denmark. , 2011, Food microbiology.

[3]  Maarten Nauta,et al.  The Impact of Consumer Phase Models in Microbial Risk Analysis , 2011, Risk analysis : an official publication of the Society for Risk Analysis.

[4]  Nick Wilson,et al.  Marked campylobacteriosis decline after interventions aimed at poultry, New Zealand. , 2011, Emerging infectious diseases.

[5]  A H Geeraerd,et al.  Estimating distributions out of qualitative and (semi)quantitative microbiological contamination data for use in risk assessment. , 2010, International journal of food microbiology.

[6]  K. Song,et al.  Effect of UV-C irradiation on the inactivation of inoculated pathogens and quality of chicken breasts during storage , 2010 .

[7]  Daniel J. Wilson,et al.  Molecular and spatial epidemiology of human campylobacteriosis: source association and genotype-related risk factors , 2010, Epidemiology and Infection.

[8]  B. Christensen,et al.  Effect of organic acids and marination ingredients on the survival of Campylobacter jejuni on meat. , 2010, Journal of food protection.

[9]  E. Engvall,et al.  Trends in Campylobacter incidence in broilers and humans in six European countries, 1997-2007. , 2010, Preventive veterinary medicine.

[10]  Daniel J. Wilson,et al.  Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. , 2009, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[11]  B. Christensen,et al.  Chemical decontamination of Campylobacter jejuni on chicken skin and meat. , 2009, Journal of food protection.

[12]  I. Connerton,et al.  Survival at refrigeration and freezing temperatures of Campylobacter coli and Campylobacter jejuni on chicken skin applied as axenic and mixed inoculums. , 2009, International journal of food microbiology.

[13]  S. Ethelberg,et al.  Danish strategies to control Campylobacter in broilers and broiler meat: facts and effects , 2009, Epidemiology and Infection.

[14]  Tine Hald,et al.  Attributing the human disease burden of foodborne infections to specific sources. , 2009, Foodborne pathogens and disease.

[15]  S. Sheppard,et al.  Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. , 2009, The Journal of infectious diseases.

[16]  H. Rosenquist,et al.  Reduction of thermotolerant Campylobacter species on broiler carcasses following physical decontamination at slaughter. , 2009, Journal of food protection.

[17]  M. Nauta,et al.  A comparison of risk assessments on Campylobacter in broiler meat. , 2009, International journal of food microbiology.

[18]  P. Mullner.  Estimating the contribution of different sources to the burden of human campylobacteriosis and salmonellosis. , 2009 .

[19]  E. V. van Asselt,et al.  Campylobacter prevalence in the broiler supply chain in the Netherlands. , 2008, Poultry science.

[20]  Daniel J. Wilson,et al.  Tracing the Source of Campylobacteriosis , 2008, PLoS genetics.

[21]  H. Rosenquist,et al.  Interventions to control Campylobacter in the broiler production: Report of an International Expert Consultation Copenhagen, Denmark, 26–27 November 2007 , 2008 .

[22]  D. P. Smith,et al.  The effect of chilling in cold air or ice water on the microbiological quality of broiler carcasses and the population of Campylobacter. , 2008, Poultry science.

[23]  Arie H. Havelaar,et al.  Risk-based standards for Campylobacter in the broiler meat chain , 2008 .

[24]  M. Nauta,et al.  Food Safety in the Domestic Environment: The Effect of Consumer Risk Information on Human Disease Risks , 2008, Risk analysis : an official publication of the Society for Risk Analysis.

[25]  V. Allen,et al.  Sources and spread of thermophilic Campylobacter spp. during partial depopulation of broiler chicken flocks. , 2008, Journal of Food Protection.

[26]  R. Lindqvist,et al.  Quantitative risk assessment of thermophilic Campylobacter spp. and cross-contamination during handling of raw broiler chickens evaluating strategies at the producer level to reduce human campylobacteriosis in Sweden. , 2008, International journal of food microbiology.

[27]  Evers Eg,et al.  Campylobacter source attribution by exposure assessment , 2008 .

[28]  P. Teixeira,et al.  Occurrence, identification, and characterization of Campylobacter species isolated from portuguese poultry samples collected from retail establishments. , 2008, Poultry science.

[29]  H. Skovgård,et al.  Use of Fly Screens to Reduce Campylobacter spp. Introduction in Broiler Houses , 2007, Emerging infectious diseases.

[30]  Hanne Rosenquist,et al.  A collaborative study on a Nordic standard protocol for detection and enumeration of thermotolerant Campylobacter in food (NMKL 119, 3. Ed., 2007). , 2007, International journal of food microbiology.

[31]  E. Engvall,et al.  Summary of the Swedish Campylobacter program in broilers, 2001 through 2005. , 2007, Journal of food protection.

[32]  M. Nauta,et al.  Modelling of Campylobacter survival in frozen chicken meat , 2007, Journal of applied microbiology.

[33]  Arie H Havelaar,et al.  A Risk Assessment Model for Campylobacter in Broiler Meat , 2007, Risk analysis : an official publication of the Society for Risk Analysis.

[34]  J. Wagenaar,et al.  Assessing Interventions to Reduce the Risk of Campylobacter Prevalence in Broilers , 2007, Risk analysis : an official publication of the Society for Risk Analysis.

[35]  D. P. Smith,et al.  Effect of dry air or immersion chilling on recovery of bacteria from broiler carcasses. , 2007, Journal of food protection.

[36]  R. Lowman,et al.  A farm-level study of risk factors associated with the colonization of broiler flocks with Campylobacter spp. in Iceland, 2001 – 2004 , 2007, Acta veterinaria Scandinavica.

[37]  A Kiermeier,et al.  Analysing microbiological data: Tobit or not Tobit? , 2007, International journal of food microbiology.

[38]  V. Atanassova,et al.  Prevalence of Campylobacter spp. in poultry and poultry products for sale on the Bulgarian retail market , 2007, Antonie van Leeuwenhoek.

[39]  Graham Purnell,et al.  Decontamination of poultry carcasses using steam or hot water in combination with rapid cooling, chilling or freezing of carcass surfaces. , 2007, International journal of food microbiology.

[40]  Arie H Havelaar,et al.  Effectiveness and Efficiency of Controlling Campylobacter on Broiler Chicken Meat , 2006, Risk analysis : an official publication of the Society for Risk Analysis.

[41]  C. Dervin,et al.  Estimation of Microbial Contamination of Food from Prevalence and Concentration Data: Application to Listeria monocytogenes in Fresh Vegetables , 2006, Applied and Environmental Microbiology.

[42]  A. Gücükoğlu,et al.  ACIDIFIED SODIUM CHLORITE, TRISODIUM PHOSPHATE AND POPULATIONS OF CAMPYLOBACTER JEJUNI ON CHICKEN BREAST SKIN , 2006 .

[43]  N. Stern,et al.  The influence of freezing and duration of storage on Campylobacter and indicator bacteria in broiler carcasses. , 2006, Food microbiology.

[44]  Gurbuz Gunes,et al.  Consumer awareness and acceptance of irradiated foods: Results of a survey conducted on Turkish consumers , 2006 .

[45]  B. Christensen,et al.  The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter. , 2006, International journal of food microbiology.

[46]  M. Doyle,et al.  Reduction of Campylobacter jejuni on chicken wings by chemical treatments. , 2006, Journal of food protection.

[47]  R. Smith,et al.  Three-year surveillance program examining the prevalence of Campylobacter and Salmonella in whole retail raw chicken. , 2006, Journal of food protection.

[48]  N. Stern,et al.  Enumeration and identity of Campylobacter spp. in Italian broilers. , 2006, Poultry science.

[49]  Anne Wingstrand,et al.  Fresh Chicken as Main Risk Factor for Campylobacteriosis, Denmark , 2006, Emerging infectious diseases.

[50]  Y. Hung,et al.  Efficacy of electrolyzed water in the prevention and removal of fecal material attachment and its microbicidal effectiveness during simulated industrial poultry processing. , 2005, Poultry science.

[51]  H. Kruse,et al.  Reduction in flock prevalence of Campylobacter spp. in broilers in Norway after implementation of an action plan. , 2005, Journal of food protection.

[52]  Sj James,et al.  Surface pasteurisation of chicken carcasses using hot water , 2005 .

[53]  R. Stephan,et al.  Dynamics of Campylobacter spp. Spread Investigated in 14 Broiler Flocks in Switzerland , 2005, Avian diseases.

[54]  E. Skjerve,et al.  Survival of Campylobacter on frozen broiler carcasses as a function of time. , 2005, Journal of food protection.

[55]  O. Oyarzabal.  Reduction of Campylobacter spp. by commercial antimicrobials applied during the processing of broiler chickens: a review from the United States perspective. , 2005, Journal of food protection.

[56]  J. Meng,et al.  Prevalence and Antimicrobial Resistance of Campylobacter spp. and Salmonella Serovars in Organic Chickens from Maryland Retail Stores , 2005, Applied and Environmental Microbiology.

[57]  Evers Eg,et al.  Risk assessment of Campylobacter in the Netherlands via broiler meat and other routes , 2005 .

[58]  K. Stärk,et al.  Campylobacter spp. in dogs and cats in Switzerland: risk factor analysis and molecular characterization with AFLP. , 2005, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[59]  J. Ketley,et al.  Prevalence of Campylobacter in the food and water supply: incidence, outbreaks, isolation and detection. , 2005 .

[60]  S. Bhaduri,et al.  Survival of Cold-Stressed Campylobacter jejuni on Ground Chicken and Chicken Skin during Frozen Storage , 2004, Applied and Environmental Microbiology.

[61]  Lasse Engbo Christiansen,et al.  Effects of Climate on Incidence of Campylobacter spp. in Humans and Prevalence in Broiler Flocks in Denmark , 2004, Applied and Environmental Microbiology.

[62]  J. Griffiths,et al.  The seasonality of human campylobacter infection and Campylobacter isolates from fresh, retail chicken in Wales , 2004, Epidemiology and Infection.

[63]  S. F. Bilgili,et al.  Effects of postchill application of acidified sodium chlorite to control Campylobacter spp. and Escherichia coli on commercial broiler carcasses. , 2004, Journal of food protection.

[64]  D. D. Bang,et al.  Flies and Campylobacter Infection of Broiler Flocks , 2004, Emerging infectious diseases.

[65]  M. Madsen,et al.  Longitudinal Study of the Excretion Patterns of Thermophilic Campylobacter spp. in Young Pet Dogs in Denmark , 2004, Journal of Clinical Microbiology.

[66]  Anne Wilcock,et al.  Consumer attitudes, knowledge and behaviour: a review of food safety issues , 2004 .

[67]  W. R. Windham,et al.  Effect of intestinal content contamination on broiler carcass Campylobacter counts. , 2004, Journal of food protection.

[68]  Tine Hald,et al.  A Bayesian Approach to Quantify the Contribution of Animal‐Food Sources to Human Salmonellosis , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[69]  P. Fratamico,et al.  Effect of temperature on viability of Campylobacter jejuni and Campylobacter coli on raw chicken or pork skin. , 2003, Journal of food protection.

[70]  Tine Hald,et al.  Salmonella Control Programs in Denmark , 2003, Emerging infectious diseases.

[71]  K. Mølbak,et al.  A case–control study of risk factors for sporadic campylobacter infections in Denmark , 2003, Epidemiology and Infection.

[72]  Hanne Rosenquist,et al.  Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. , 2003, International journal of food microbiology.

[73]  M. Lund,et al.  Evaluation of PCR for detection of Campylobacter in a national broiler surveillance programme in Denmark. , 2003, Journal of applied microbiology.

[74]  Y. Hung,et al.  Reduction of Campylobacter jejuni on poultry by low-temperature treatment. , 2003, Journal of food protection.

[75]  E. Gunnarsson,et al.  Campylobacter spp. in Icelandic poultry operations and human disease. , 2003, Epidemiology and infection.

[76]  J. Collins,et al.  An assessment of steam pasteurization and hot water immersion treatments for the microbiological decontamination of broiler carcasses , 2003 .

[77]  I. Wilson.  Salmonella and campylobacter contamination of raw retail chickens from different producers: a six year survey , 2002, Epidemiology and Infection.

[78]  R. Brackett,et al.  Antimicrobial effect of electrolyzed water for inactivating Campylobacter jejuni during poultry washing. , 2002, International journal of food microbiology.

[79]  R. J. Buhr,et al.  Broiler carcass contamination with Campylobacter from feces during defeathering. , 2001, Journal of food protection.

[80]  G Gettinby,et al.  A quantitative risk assessment for the occurrence of campylobacter in chickens at the point of slaughter , 2001, Epidemiology and Infection.

[81]  K. Gradel,et al.  Pre-harvest surveillance of Campylobacter and Salmonella in Danish broiler flocks: a 2-year study. , 2001, International journal of food microbiology.

[82]  R. Davies,et al.  A trial of biosecurity as a means to control Campylobacter infection of broiler chickens. , 2001, Preventive veterinary medicine.

[83]  D. Newell,et al.  Sequential spread of Campylobacter infection in a multipen broiler house. , 2000, Avian diseases.

[84]  A H Havelaar,et al.  The Beta Poisson Dose‐Response Model Is Not a Single‐Hit Model , 2000, Risk analysis : an official publication of the Society for Risk Analysis.

[85]  J. Dickens,et al.  Presence and Level of Campylobacter spp. on Broiler Carcasses Throughout the Processing Plant , 2000 .

[86]  P. Gerner-Smidt,et al.  Prevalence of Campylobacter,Arcobacter, Helicobacter, andSutterella spp. in Human Fecal Samples as Estimated by a Reevaluation of Isolation Methods for Campylobacters , 2000, Journal of Clinical Microbiology.

[87]  M. Uyttendaele,et al.  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. , 1999, Journal of food protection.

[88]  H Straatman,et al.  Studying seasonality by using sine and cosine functions in regression analysis. , 1999, Journal of epidemiology and community health.

[89]  P. Coloe,et al.  Survival and growth of Campylobacter jejuni after artificial inoculation onto chicken skin as a function of temperature and packaging conditions. , 1998, Journal of food protection.

[90]  T. Abee,et al.  Physiological Activity of Campylobacter jejuni Far below the Minimal Growth Temperature , 1998, Applied and Environmental Microbiology.

[91]  P. Fields,et al.  Discrimination of Campylobacter jejuni isolates by fla gene sequencing , 1997, Journal of clinical microbiology.

[92]  E. Nielsen,et al.  Distribution of serotypes of Campylobacter jejuni and C. coli from Danish patients, poultry, cattle and swine. , 1997, FEMS immunology and medical microbiology.

[93]  W. Willis,et al.  Campylobacter jejuni seasonal recovery observations of retail market broilers. , 1997, Poultry science.

[94]  C. James,et al.  Salmonella, Campylobacter and Escherichia coli O157:H7 decontamination techniques for the future. , 1995, International journal of food microbiology.

[95]  M. Patterson.  Sensitivity of Campylobacter spp. to irradiation in poultry meat , 1995, Letters in applied microbiology.

[96]  N. Bolder,et al.  Cecal carriage of Campylobacter and Salmonella in Dutch broiler flocks at slaughter: a one-year study. , 1994, Poultry Science.

[97]  S. Ostroff,et al.  Epidemiological investigation of risk factors for Campylobacter colonization in Norwegian broiler flocks , 1993, Epidemiology and Infection.

[98]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[99]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[100]  J. Nicolet,et al.  Comparison of Campylobacter carriage rates in diarrheic and healthy pet animals. , 1992, Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series B.

[101]  G. Greer,et al.  Factors affecting the susceptibility of meatborne pathogens and spoilage bacteria to organic acids , 1992 .

[102]  J. H. Denton,et al.  Incidence and level of Campylobacter jejuni in broiler processing. , 1988, Poultry science.

[103]  J. Oosterom,et al.  Origin and Prevalence of Campylobaeter jejuni in Poultry Processing. , 1983, Journal of food protection.

[104]  D. Kilsby,et al.  The relevance of the distribution of micro-organisms within batches of food to the control of microbiological hazards from foods. , 1981, The Journal of applied bacteriology.